ecology of the macrofauna in sandy intertidal habitats...
TRANSCRIPT
Ecology of the macrofauna in sandy
intertidal habitats
Ecología de la macrofauna en intermareales
arenosos
Iván Franco Rodil
Thesis submitted in fulfilment of the requirements for the
degree of Doctor in Biological Sciences
Memoria presentada para optar al grado de
Doctor en Biología
Universidad de Vigo
2008
Mariano Lastra Valdor, Profesor Titular del Departamento de
Ecología y Biología Animal de la Universidad de Vigo
CERTIFICA:
Que la presente memoria titulada “Ecología de la macrofauna de
intermareales arenosos”, presentada por D. Iván Franco Rodil para optar al
Grado de Doctor en Biología, ha sido realizada bajo mi dirección en el
Departamento de Ecología y Biología Animal de la Universidad de Vigo.
Y considerando que tiene la suficiente entidad para constituir un
trabajo de Tesis Doctoral, autorizo su presentación ante el Consejo de
Departamento y la Comisión de Doctorado.
Y para que así conste y surtan los efectos oportunos, expido y firmo la
presente certificación en Vigo a 15 de Noviembre de 2007
Fdo: Mariano Lastra Valdor.
i
Acknowledgments
During the last years I have met and benefited from the attention and
generosity of many people and institutions, some of them mentioned
individually at the end of each of the following chapters, who contributed to
my development as a scientist and as a person, sometimes in unexpected ways.
First of all, I want to thank Mariano because he introduced me to the
sandy beaches world and always kept a permanent place in store for me in the
lab. Thanks to all the Benthos Team, those who were part of and those who still
remain, somehow, in this abstract body, for everything. Mónica and Germán
deserve special mention because they woke me up at the very moment and
Celia because she showed me more than “two things”. Thanks all of you for
everything.
I am very grateful to Jenny, Mark, Dave and Pete because they made
me feel at home so far away on the other side of both oceans. Because you let
me learn.
To my family, the one which chose me and the one I chose, for your
patience, warm and, above all, your unselfishness friendship. Mum, thanks for
existing. Thanks grandma for loving your friend from Vigo so much. Thanks to
the Pacific.
The present thesis was financially supported by a Ph.D. grant of the
Xunta de Galicia (Maria Barbeito P.P. 0000 300s 140.08.). Additonal travel
grants were acquired from the Universidad de Vigo and Fundación Caixa
Galicia.
Nihil obstat quominus imprimatur
Quod scripsi, scripsi (John, 19,22)
ii
Agradecimientos
Durante los últimos años he contado con el apoyo y la generosidad de
mucha gente e instituciones, algunos de ellos se mencionan de forma individual
al final de cada Capítulo, que han contribuido a mi desarrollo como científico y
como persona, a veces de maneras inesperadas.
En primer lugar gracias a Mariano por haberme introducido en el
mundo de las playas y reservarme un hueco permanente en el laboratorio.
Gracias a todo el Equipo de Bentos, a los que estuvieron en algún momento y a
los que todavía forman parte, de alguna forma, de este ente abstracto, por todo.
Una mención especial merecen Mónica y Germán por espabilarme en el
momento adecuado y Celia, por enseñarme algo más que un “par de cosas”.
Gracias a todos por todo.
Gracias a Jenny, Mark, Dave y Pete por haberme hecho sentir como en
casa al otro lado de los océanos. Por dejarme aprender.
A mi familia, la que me escogió y se dejó escoger, por vuestra
paciencia, cariño y sobre todo por esa amistad desinteresada y sin límites.
Mamá gracias por existir. A mi abuela, por querer tanto a su amigo de Vigo.
Gracias al Pacífico.
El presente trabajo ha sido financiado por una beca predoctoral de la
Xunta de Galicia (Maria Barbeito). Becas de viaje adicionales para la
realización de estancias en centros extranjeros fueron obtenidas de la
Universidad de Vigo y de la Fundación Caixa Galicia.
Nihil obstat quominus imprimatur
Quod scripsi, scripsi (Juan, 19, 22)
iii
Preface
Sandy beaches geographically dominate many regions of the
worldwide coast and underpin a substantial part of coastal economies and
developments. Sandy beaches are teeming with life, microscopic and
macroscopic. The spectrum of life in the sediment includes clams, whelks,
worms, sand hoppers, crabs and a host of smaller animals as well as
protozoans, microscopic plants, and bacteria. In addition to these residents of
the intertidal, a variety of species move up over the beach from the surf zone on
the rising tide, and others descend onto the beach from the dunes on the falling
tide. All of these components interact in a trophic network to create the open
ecosystem of the sandy beach, which exchanges materials with sea and land
becoming an important environment linking two main ecosystems.
Beaches are in a constant state of flux, accreting and eroding in
response to waves, currents, winds, storms, and sea-level change. Intertidal
areas are under increasing pressure from urbanisation, with 50% of the world’s
population now living by the coast. The beach and nearshore coastal habitats
are substantially disturbed by and can be functionally degraded through
anthropogenic activities such as process of nourishment, recreational activities
or pollution. Coastal fisheries are an important socioeconomic productive
sector with ecological relevance in these shores. Furthermore, sandy beaches
attract most of the coastal tourism and are prime sites for human recreation,
sometimes with negative environmental consequences. The sand beach
represents a productive and unique habitat supporting dense concentrations of
benthic invertebrates that feed surf fishes, resident and migrating shorebirds,
and crabs. Algal wrack deposits represent the main food resource for upper
shore consumers. Grooming with heavy equipment, to remove drift
macrophytes, debris, and trash, is common on sandy beaches in populated
regions. Removal of wrack can seriously affect beach ecosystem trophic
dynamics because this deprives the ecosystem of valuable nutrient input,
impacting wrack-dependet species and affecting shorebirds that feed on the
iv
associated invertebrates. The ecological, economic, and social implications of
rising sea level associated with global warming are far-reaching and not yet
fully anticipated by scientists or adequately contemplated in social policy.
The main aim of this study was to improve our knowledge about the
sandy beach macrofauna in the North coast of Spain. This region had not seen
any major research on sandy beach ecology, despite the great importance of
beaches in both the local marine ecosystem and the local economy. This Ph.D.
thesis consists of a general summary of the work in sandy beaches (Chapter 1)
and five accompanying chapters (Chapters 2-6). The aim of the summary is to
present an integrated account of sandy-shore ecology. The chapters are listed in
the order followed to address this overall objective and all the studies were
conducted to elucidate different aspects of the ecology of the sandy shores.
This study also includes a final section where a general discussion is presented
and which attempts to draw general conclusions of the work conducted in this
particular system.
Keywords: sandy beaches, macrofauna, intertidal zonation, morphodynamic,
exposure rate, swash, biochemical composition of sedimentary organic matter,
biopolymeric fraction, invasive species, wrack macroalgae, north of Spain.
“Everything we hear is an opinion, not a fact. Everything we see is a
perspective, not the truth.”
“Such as are your habitual thoughts, such also will be the character of your
mind; for the soul is dyed by the thoughts”.
Marcus Aurelius
v
Prefacio
Las playas dominan geográficamente muchas regiones del mundo y
apuntalan una parte sustancial del desarrollo y de la economía costera. Las
playas rebosan de vida, microscópica y macroscópica. El espectro de vida
presente incluye almejas, bígaros, gusanos, pulgas de mar, cangrejos y
pequeños huéspedes como protozoos, plantas microscópicas y bacterias.
Además de los residentes del intermareal, una gran variedad de especies suben
por la playa desde la rompiente con la marea y otros desciende desde las dunas
con la bajamar. Todos estos componentes interactúan dentro de una red trófica
creando un ecosistema playero abierto donde se intercambia material con los
ecosistemas terrestre y marino convirtiéndose un ambiente importante nexo de
dos ecosistemas principales.
Las playas están en un estado de flujo constante, de acreación y erosión
en respuesta a las olas, corrientes, vientos, tormentas y al cambio del nivel del
mar. Las zonas intermareales se encuentran bajo una presión incesante debida a
la urbanización, con un 50% de la población mundial viviendo próxima a la
costa. Tanto la playa como los hábitats costeros están sustancialmente
modificados y degradados a través de las actividades antropogénicas como los
rellenos, actividades recreativas o la contaminación directa. La actividad de
marisqueo es un sector socioeconómico muy productivo con relevancia
ecológica para los intermareales. Además, al igual que en otras regiones, las
playas españolas atraen la mayor parte del turismo costero y son lugares
principales de ocio, algunas veces con consecuencias ambientales negativas.
Las playas representan un hábitat único y productivo que aporta grandes
concentraciones de invertebrados bentónicos a la dieta de peces, aves
migratorias y residentes y cangrejos. Los depósitos de algas varadas
representan la fuente de alimento principal para los consumidores de duna. Las
actividades de limpieza con equipo pesado, para remover las algas varadas,
restos y basura, es común en las playas de regiones pobladas. La eliminación de
estos acúmulos de algas puede afectar seriamente a la dinámica trófica porque
priva al ecosistema de playa de una aportación nutritiva valiosa, produciéndose
vi
un impacto en aquellas especies dependientes de los acúmulos de algas y
afectando a aquellas aves que se alimentan de los organismos asociados. Las
implicaciones ecológicas, económicas y sociales de un aumento del nivel del
mar asociado al calentamiento global están lejos de ser totalmente previstas por
los científicos o de estar adecuadamente contempladas en la política social.
El principal objetivo de este estudio fue mejorar nuestro conocimiento
sobre la macrofauna de playas en la costa Norte de España. Esta región no ha
sido objeto de investigaciones importantes en ecología de playas, a pesar de la
gran importancia que tienen tanto en el ecosistema marino como en la
economía local. Esta tesis, presenta un resumen general de la ecología de
playas (Capítulo 1) y cinco capítulos acompañantes (Capítulos 2-6). El objetivo
del resumen es presentar un informe integrado de la ecología de playas; para
ello los capítulos se ordenan siguiendo este objetivo global y todos los estudios
fueron llevados a cabo para elucidar diferentes aspectos de la ecología de
playas. Se incluye además una sección final con una discusión general que
pretende resumir las conclusiones más relevantes del trabajo.
Palabras clave: playas, macrofauna, zonación intermareal, morfodinámica,
gradiente de exposición, swash, composición bioquímica de la materia orgánica
sedimentaria, fracción biopolimérica, especies invasoras, algas de arribazón,
norte de España.
“Todo lo que oimos es una opinión, no un hecho. Todo lo que vemos es una
perspectiva, no la verdad”
“Cuales sean tus pensamientos habituales, tal será también el carácter de tu
alma, porque los pensamientos matizan el alma”
Marco Aurelio
Table of contents
Acknowledgments .......................................................................................... i
Agradecimientos ........................................................................................... ii
Preface .......................................................................................................... iii
Prefacio........................................................................................................... v
PART I. INTRODUCTION AND AIMS. ............................................. 13
Chapter 1. General introduction. ............................................................... 14
1.1.1. Soft intertidals: sandy beaches ...................................................... 15
1.1.1.1. What is a sandy beach? .............................................................. 15
1.1.1.2. The physical environment: tidal range and system stratification
.............................................................................................................................. 18
1.1.1.3. Beach morphodynamics ............................................................. 20
1.1.2. Benthic macrofauna communities ................................................ 24
1.1.2.1. What is macrofauna? ................................................................. 24
1.1.2.2. Sandy beach macrofauna ........................................................... 26
1.1.2.3. Macrofauna distribution patterns ............................................... 27
1.1.2.4. Macrofauna zonation in the sandy beach ................................... 30
1.1.2.5. Feeding habits and survival strategies of the macrofauna ......... 33
1.1.3. Food sources in sandy beaches ..................................................... 37
1.1.3.1. Food availability ........................................................................ 37
1.1.3.2. The role of the biochemical composition and hydrodynamic
conditions.............................................................................................................. 38
1.1.4. Aims and thesis linework. ............................................................. 39
1.1.5. List of references .......................................................................... 42
PARTE I. INTRODUCCIÓN Y OBJETIVOS. .................................... 47
Capítulo 1. Introducción general. .............................................................. 48
1.1.1. Intermareal arenoso: Playas. ......................................................... 49
1.1.1.1. ¿Qué es una playa? .................................................................... 49
1.1.1.2. El ambiente físico: rango mareal y estratificación del sistema .. 51
1.1.1.3. Morfodinamismo ....................................................................... 52
1.1.2. Comunidades de la macrofauna bentónica ................................... 55
1.1.2.1. ¿Qué es la macrofauna? ............................................................. 55
1.1.2.2. Macrofauna en las playas ........................................................... 56
Table of contents
1.1.2.3. Patrones de distribución de la macrofauna ................................ 57
1.1.2.4. Zonación de la macrofauna en la playa ...................................... 59
1.1.2.5. Hábitos alimenticios y estrategias de supervivencia de la
macrofauna de playas ........................................................................................... 62
1.1.3. Fuentes de alimento en las playas ................................................. 64
1.1.3.1. Disponibilidad del alimento ....................................................... 64
1.1.3.2. El papel de la composición bioquímica y de las condiciones
hidrodinámicas. ..................................................................................................... 65
1.1.4. Objetivos y líneas de investigación de la tesis. ............................. 67
PART II. THE ECOLOGY OF SANDY BEACHES ........................... 71
Chapter 2. Environmental factors affecting benthic macrofauna along a
gradient of intermediate sandy beaches in northern Spain ..................... 72
Abstract................................................................................................... 73
2.2.1.Introduction ................................................................................... 73
2.2.2. Material and methods ................................................................... 75
2.2.2.1. Study area .................................................................................. 75
2.2.2.2. Sampling design ........................................................................ 76
2.2.2.3. Statistical analysis ...................................................................... 77
2.2.3. Results .......................................................................................... 78
2.2.3.1. Physical environment ................................................................. 78
2.2.3.2. Composition and abundance of the macrofauna ........................ 79
2.2.3.3. Relationships between macrofauna and environmental variables
.............................................................................................................................. 81
2.2.4. Discussion ..................................................................................... 83
Acknowledgments .................................................................................. 86
2.2.5. References .................................................................................... 86
Chapter 3. Community structure and intertidal zonation of the
macroinfauna in intermediate sandy beaches in temperate latitudes:
North coast of Spain. ................................................................................... 89
Abstract................................................................................................... 90
2.3.1. Introduction .................................................................................. 91
2.3.2. Material and methods. .................................................................. 93
2.3.2.1. Study area .................................................................................. 93
2.3.2.2 Sampling design ......................................................................... 94
Table of contents
2.3.2.3. Statistical analysis ...................................................................... 95
2.3.3. Results .......................................................................................... 97
2.3.3.1. Physical environment ................................................................. 97
2.3.3.2. Composition and abundance of the Macrofauna ........................ 99
2.3.3.3. Intertidal zonation of the macroinfauna ................................... 100
2.3.3.4. Relationships between macroinfauna and environmental
variables. ............................................................................................................. 105
2.3.4. Discussion ................................................................................... 106
2.3.4.1. Macrofaunal characteristics ..................................................... 106
2.3.4.2. Zonation patterns of the macroinfauna .................................... 106
2.3.4.3. Relationships between macroinfauna and environmental
variables. ............................................................................................................. 112
Acknowledgments ................................................................................ 114
2.3.5. References .................................................................................. 115
PART III. THE IMPORTANCE OF EXPOSURE ON SANDY
BEACH MACROFAUNA: HYDRODINAMIC CONDITIONS AND
FOOD AVAILABILITY. ..................................................................... 120
Chapter 4. Macroinfauna community structure and biochemical
composition of sedimentary organic matter along a gradient of wave
exposure in sandy beaches (NW Spain). .................................................. 121
Abstract................................................................................................. 122
3.4.1. Introduction ................................................................................ 123
3.4.2. Material and methods ................................................................. 125
3.4.2.1. Study area ................................................................................ 125
3.4.2.2. Sampling design ...................................................................... 126
3.4.2.3. Biochemical analysis. .............................................................. 127
3.4.2.4. Data analysis. ........................................................................... 128
3.4.3. Results ........................................................................................ 129
3.4.3.1. Physical environment ............................................................... 129
3.4.3.2. Composition and abundance of the macroinfauna ................... 131
3.4.3.3. Intertidal distribution of the macroinfauna .............................. 132
3.4.3.4. Organic matter composition..................................................... 133
3.4.4. Discussion ................................................................................... 138
3.4.4.1. Macroinfauna characteristics in a gradient of exposure ........... 138
Table of contents
3.4.4.2. Biochemical composition of sedimentary organic matter ........ 142
Acknowledgements .............................................................................. 146
3.4.5. References .................................................................................. 147
PART IV. THE ROLE OF FOOD AVAILABILITY IN SANDY
BEACHES: SPATIAL AND TEMPORAL PATTERNS. .................. 151
Chapter 5. Seasonal variability in the vertical distribution of benthic
macrofauna and sedimentary organic matter in an estuarine beach (NW
Spain). ............................................................................................. 152
Abstract................................................................................................. 153
4.5.1. Introduction ................................................................................ 154
4.5.2. Material and methods. ................................................................ 156
4.5.2.1. Study area ................................................................................ 156
4.5.2.2. Sampling design ...................................................................... 157
4.5.2.3. Biochemical composition of the sedimentary organic matter .. 158
4.5.2.4. Data analysis ............................................................................ 158
4.5.3. Results. ....................................................................................... 160
4.5.3.1. Environmental characteristics. ................................................. 160
4.5.3.2. Macrobenthic community. ....................................................... 161
4.5.3.3. Organic matter composition and chlorophyll a content. .......... 167
4.5.3.4. Relationships between sedimentary organics and benthic fauna.
............................................................................................................................ 169
4.5.4. Discussion ................................................................................... 171
4.5.4.1. Benthic macrofauna community. ............................................. 171
4.5.4.2 Spatial and temporal changes in organic matter composition and
Chl a content. ...................................................................................................... 173
4.5.4.3. Relationships between environmental variables and benthic
macrofauna. ........................................................................................................ 177
Acknowledgements .............................................................................. 179
4.5.5. References. ................................................................................. 179
Chapter 6. Diferential effects of native and invasive algal wrack on
macrofaunal assemblages inhabiting exposed sandy beaches. .............. 182
Abstract................................................................................................. 183
4.6.1. Introduction ................................................................................ 183
4.6.2. Methods ...................................................................................... 186
Table of contents
4.6.2.1. Study area ................................................................................ 186
4.6.2.2. Experimental design ................................................................ 187
4.6.2.3. Laboratory analysis .................................................................. 188
4.6.2.4. Statistical analysis .................................................................... 189
4.6.3. Results ........................................................................................ 192
4.6.3.1. Microclimatic conditions of wrack patches: humidity and
temperature ......................................................................................................... 192
4.6.3.2. Analysis of the total organic matter and nutritional value ....... 192
4.6.3.3. Macrofauna abundance, number of species and diversity ....... 197
4.6.3.4. Analysis of variance of selected species: Patterns of colonisation
and succession .................................................................................................... 199
4.6.3.5. Analysis of assemblages in wrack patches .............................. 202
4.6.3.6. Influence of environmental variables on macrofauna
assemblages. ....................................................................................................... 203
4.6.4. Discussion ................................................................................... 205
4.6.4.1. Patterns of colonisation and succession ................................... 205
4.6.4.2. Abiotic factors affecting macrofaunal assemblages ................. 209
Acknowledgments ................................................................................ 213
4.6.5. References .................................................................................. 213
PART V. GENERAL DISCUSSION. ................................................. 217
5.7.1. The ecology of sandy beaches in the northern coast of the Iberian
Peninsula. ............................................................................................................ 218
5.7.1.1. Environmental factors affecting benthic macrofauna. ............. 219
5.7.1.2. Community structure and macrofauna zonation ...................... 220
5.7.1.3. Relationship between macroinfauna and environmental variables
............................................................................................................................ 221
5.7.2. The importance of exposure on sandy beach macrofauna:
hydrodynamic conditions and food availability. ................................................. 222
5.7.2.1. Macrofauna characteristics in a gradient of exposure .............. 223
5.7.2.2. Effect of the biochemical composition of sedimentary organic
matter on macrofauna ......................................................................................... 224
5.7.3. The role of food availability in the macrofauna community
structure of sandy beaches: spatial and temporal patterns. ................................. 225
5.7.3.1. Seasonal variability in the benthic macrofauna distribution and
food availability in a sheltered estuarine beach. ................................................. 226
Table of contents
5.7.3.2. Effect of invasive algal wrack in macrofauna assemblages in an
exposed sandy beach........................................................................................... 229
5.7.4. Open questions. .......................................................................... 232
5.7.5. List of references. ....................................................................... 235
PARTE V. DISCUSIÓN GENERAL. ................................................. 238
5.7.1. La ecología de playas de la costa norte de la Península Ibérica. . 239
5.7.1.1. Factores ambientales que afectan a la macrofauna bentónica. 240
5.7.1.2. Estructura de la comunidad y zonación de la macrofauna ....... 242
5.7.1.3. Relación entre la macrofauna y las variables ambientales ....... 243
5.7.2. La importancia de la exposición en la macrofauna de playas:
condiciones hidrodinámicas y disponibilidad de alimento. ................................ 245
5.7.2.1. Características de la macrofauna de playas en un gradiente de
exposición ........................................................................................................... 245
5.7.2.2. Efecto de la composición bioquímica de la materia orgánica en la
macrofauna ......................................................................................................... 247
5.7.3. El papel de la disponibilidad de alimento en la estructura de la
comunidad de playas: patrones espaciales y temporales. .................................... 248
5.7.3.1. Variabilidad estacional en la distribución de la macrofauna
bentónica y de la disponibilidad de alimento en una playa estuárica protegida. . 248
5.7.3.2. Efecto de las algas invasoras sobre la asociación macrofaunística
de una playa expuesta ......................................................................................... 252
5.7.4. Cuestiones abiertas. .................................................................... 256
PART VI. GENERAL CONCLUSIONS ............................................. 260
PART VII. APPENDIX ....................................................................... 264
PART I. INTRODUCTION AND AIMS.
“If the doors of perception were cleansed everything would appear to man as it
is, infinite. For man has chosen himself up, till he sees all things through
narrow chinks of his cavern”.
William Blake
Chapter 1. General introduction.
Chapter 1 Introduction
15
1.1.1. Soft intertidals: sandy beaches
1.1.1.1. What is a sandy beach?
Commonly known as sandy beaches, soft intertidals are very dynamic
environments, hostiles and cosmopolitans (McLachlan, 1996) which have been
defined to cover a wide range of environments in several forms, sometimes
with some lack of rigour.
“a wave-deposited accumulation of sand lying between modal wave
base (i.e. the maximum depth at which a wave can transport sediment towards
the shoreward) and upper swash limit” (Short, 1999).
As stated in this definition, three basic requirements arise to have a
sandy beach: sand, waves and tides. It is the sand that is transported by waves
and tides to the shoreline that forms the sandy beach. These three factors
together determine the morphodynamic, faunistic communities; as well as the
quantity and the quality of the organic matter (i.e. food availability) that we
find in the beaches. In this study, sandy beaches will be considered exposed
sandy shorelines possessing three dynamic zones: a zone of wave shoaling
seaward of the breaker point, a surf zone of breaking waves and a swash zone
of final wave dissipation on the subaerial beach. The nature and extent of each
of these zones will ultimately determine the beach morphodynamics (Figure
1.1).
Sand, and by extension sediment, can be classified according to its
origin and its grain size. The most common sediment component is silica,
generally in quartz form (terrestrial origin) although it is also frequent the
presence of carbonate (marine origin) sand. Sometimes sediment can be made
of shell hash, volcanic or coralline material and rocks pebble shaped, from
different origin. Sediment grain size is generally defined according to the scale
of Wenthworth (Buchanan, 1984) in phi units (φ = -log2 Ø) but in this study
and in most of the current papers about sandy beach ecology the metric scale
Chapter 1 Introduction
16
units are normally used. Everything between 63 µm and 2 mm (0<φ<4) is
defined as sand. Sediment grain size has been considered decisive in the
macroinfauna community structure in most of the outstanding sandy beach
ecology papers (e.g. Jaramillo and González, 1991; McLachlan and Dorvlo,
2005; Defeo and McLachlan, 2005) and it will be also considered in this study.
Figure 1.1. Features of a high energy sandy beach at mid tide (Modified from Short,
1999).
A wave is, in general, a wind-driven transport of energy through water. Waves
remain stable as long as the wave height (H) is less than 1/7 of the wave length
(L) (Figure 1.2.). Wave action penetrates the water column to a depth of
approximately half of the wave length. Close to the shore, water depth will
decrease to a point where the base of the wave will touch the sea floor. From
here on, the wave will not only transport energy but also sediment material.
This is the modal wave base from Short’s definition and therefore the lower
edge of the beach. The waves will start compacting, the wave length will
decrease and the H/L ratio increases. This is known as shoaling (Fig. 1.1.). The
Chapter 1 Introduction
17
velocity in the lower part of the wave will slow down because of the dragging
created by the sediment and the wave becomes depth-dependent; meanwhile
the upper part of the wave is moving with a different speed (Fig. 1.2.). The
wave will collapse when the H/L ratio surpasses the stability point of 1/7, this
is called breaking zone. The last phase of the wave action, after the point of
breaking, is where the water runs up and down the beach profile, called swash
zone where the wave energy is dissipated. The zone with surfing waves is the
surf zone (Fig. 1.1.).
Figure 1.2. Changes of a wave entering a beach (modified from Thurman and Burton,
2001) and schematic representation of a wave collapsing.
The point of breaking is a very turbulent area characterised by coarser
sediment, water loaded with sand and strong current (Figure 1.3.). The swash
zone reaches the intertidal as a water film, covering and spraying part of the
beach face depending on wave strength, tide range and also beach slope and
Waves reaching critical 1:7 ratio
ratio
Chapter 1 Introduction
18
Swash
Effluent line
Unsaturated sand
Surf zone
Breaker
includes the highest point reached by the highest wave and a water zone almost
stagnant. Traditionally the swash zone was divided in two parts: a saturated
part, always with water, and an unsaturated one reached periodically by the
highest waves with a successive drainage between wave and wave. The surfing
and saturated swash zones are also known as the sublittoral beach environment;
meanwhile the unsaturated zone belongs to the mesolittoral zone (Dahl, 1952).
Depending on the dynamic conditions of the tide and waves there will be a
wider or smaller submerge part in the beach, even during the spring tides.
Eventually, there is a spray zone that is never covered by water and belongs to
the upper part of the beach normally composed by some type of dune system.
This environment is also known as the supralittoral or subterrestrial zone,
constantly dried and where desiccation and temperature are the main stress
factors for the fauna.
Figure 1.3. Pine Knoll Shore (North Carolina). The different zones of the beach
including the effluent line
1.1.1.2. The physical environment: tidal range and system stratification
Tides are not required for beach formation; however increasing tide
range will, in combination with wave conditions, contribute substantially to
beach morphology. Tides cause main impact changing constantly the shoreline
face both horizontally and vertically depending on the tide range and beach
Chapter 1 Introduction
19
profile. In areas of high tide range, the tidal variation in nearshore water depth
can also modify breaker wave height by increasing wave shoaling at low tide.
The shoreline mobility also shifts the swash, surf and wave shoaling zones
(Short, 1999). The tidal regime were classified by Davies (1964) in three main
types (Figure 1.4.): microtidal (TR < 2 m), mesotidal (2 < TR < 4 m) and
macrotidal (TR > 4 m). The highest point reached by the waves during the
spring high tide is traditionally considered as the upper limit in sandy
intertidals, according to the sandy beach definition we are using (Figure 1.5.).
Due to the tidal variation, during low tide sandy beaches show a wide zone
where water drainage occurs. Particularly on exposed beaches, the great
vertical extent of the system and the drainage it experiences at low tide permit
the subdivision of the intertidal beach into layers or strata.
Figure 1.4. Traditional descriptive classifications based on qualitative observations and
tidal range.
Various schemes have been proposed to describe this (Salvat, 1964;
McLachlan, 1980) and one such scheme is shown in Figure 1.6. The layers
range from dry surface sand at the top of the shore to permanently saturated
sand lower down water table and linked to the swash. The permanently
saturated layers have little circulation and tend to become stagnated, while the
Chapter 1 Introduction
20
resurgence zone has gravitational water drainage through it during ebb tide; the
retention zone loses gravitational water but retains capillary moisture at low
tide. The retention lower limit is defined by the upper limit of capillary rise
above the water table during low tide. The zone of retention represents
optimum conditions for interstitial fauna, since there is a good balance between
water, oxygen and food input, physical stability and lack of stagnation
(McLachlan and Brown, 2006).
Figure 1.5. Tidal zonation scheme (modified from Short, 1999)
But sandy beaches are much more than the coastal shoreline. The
intertidal is a linkage environment between marine and terrestrial ecosystem.
We can make a general division in two ecological systems: the wind-driven
dune, with subterrestrial species exposed mainly to air and a wave and tide-
driven intertidal with water breather species. Further subdivision in the
intertidal will be deeply discussed in Chapter 3.
1.1.1.3. Beach morphodynamics
Sandy beach morphology is mainly due to the interactions between
sediment characteristics, wave exposure and marine currents, also called beach
morphodynamics. Since exposed sandy beaches are mostly considered as
physically controlled environments, the first beach classifications were focused
on the hydrodynamic processes underlying the depositional form (Short and
Chapter 1 Introduction
21
Wright, 1984) which span a continuum from reflective beaches, narrow and
steep, to dissipative systems, which are wide and flat. A series of intermediate
states are recognised between the above extremes.
Figure 1.6. Stratification of the interstitial system of an exposed sandy beach (after
Salvat, 1964 in McLachlan and Brown, 2006)
Within this general scheme, many variations are possible, creating a
wide range of beach types. Variations can be due to sediment type, sediment
grain size, wave action, exposure, tidal range and shore morphology. Many of
these factors are interdependent. Sediment grain size, for instance, depends on
the wave action, which in its turn depends on exposure and shore morphology.
Most beach type classifications are based on three parameters: sediment grain
size, wave action and tidal range. The most widely accepted classification using
these parameters (Figure 1.7.) was introduced by Masselink and Short (1993).
On the horizontal axis, Dean’s parameter (Ω = Hb / Ws * T), a function of
sedimentation velocity (Ws), breaker height (Hb) and breaker period (T),
divides the beaches into three types: reflectives (Ω < 1), intermediates (1 < Ω <
Chapter 1 Introduction
22
6) and dissipatives (Ω > 6). The relative tide range (RTR = MSR/Hb) on the
vertical axis is calculated from the mean spring tidal range and the breaker
height and increases with increasing tidal influence on the beach (see 1.1.1.2.).
Figure 1.7. Conceptual model covering beaches of all tide ranges, based on the
dimensionless fall velocity (Ω) and the relative tide range (RTR) (after Short, 1996).
When RTR < 3 and Ω < 2, the microtidal beach types dominate. When RTR is between
3 and 12, tide range increasingly modifies the wide intertidal beach. When RTR > 12,
the transition to tide dominated beaches is entered (modified from McLachlan and
Brown, 2006).
Reflective beaches are characterised by steep slopes and coarse
sediment. The waves break on the beach face itself, eliminating a surf zone.
The swash zone is narrow with high velocity. Dissipative beaches, in contrast,
have waves breaking far out at sea, and a wide surf zone, where much of the
wave is dissipated. This results in very flat beaches with fine to very fine sands.
An intermediate beach is anything in between, it is characterised by high
temporal variability and the most common beach type in the world (Fig. 1.7).
All the beach classification systems include some kind of wave
information (Davies, 1964; Masselink and Short 1993). Although wave regime
Chapter 1 Introduction
23
is probably the most important agent in sandy beach formation, it is difficult to
measure in the field. It can also be questioned to what extent the wave regime
at a given day is representative for the waves that formed the beach as it is on
that day. Both Dean’s parameter and RTR are predictive rather than descriptive
tools (Short, 1999). Therefore, several beach classification parameters, which
do not require wave measurements and which are descriptive, have been
developed. The Beach State Index (BSI), used to compare beaches subject to
differing tide ranges (McLachlan et al., 1993), involved multiplying Dean’s
parameter by a tidal factor, and this gave good correlations when a wide range
of beach types with different tide range is considered (see Chapters 2 and 3).
More recently, (see McLachlan and Dorvlo, 2005) the Beach Index and the
Beach Deposit Index (BI and BDI) were developed. These indexes are based on
a measure of beach face slope multiplied by a measure of sand particle size and
both are easy to measure in the field. The former includes tidal range, which is
useful on a large spatial scale when areas from different regions are compared
(see Chapter 4). The BDI is only suitable for studies on a smaller spatial scale,
with no or minor differences in tidal range between the studied sites.
Beaches are not only classified according to their morphodynamic, but
also according to exposure. A very comprehensive classification scheme was
proposed by McLachlan (1980) and although it is based on indirect variables,
with parameters difficult to measure in the field or with high temporal and
spatial variability, this classification is particularly important for ecological
studies since unifies relevant ecological concepts. Four categories, from very
sheltered to very exposed, are defined with a rating system based on wave,
biological and morphodynamic characteristics (Table 1.1.).
Sandy beaches are a very dynamic system where spatial and temporal
changes in physical and morphological characteristics are common. Sandy
beaches are physically controlled environments where communities are
structured by the independent responses of individual species to physical
factors, such as sediment texture and swash conditions (e.g. McArdle and
McLachlan, 1992; McLachlan, 1996; Defeo and McLachlan, 2005).
Chapter 1 Introduction
24
Sediment texture determines porosity (i.e., the volume for space
between the sand grains), permeability (i.e., the rate of drainage of water
through the sand) and penetrability (i.e. the force needed to penetrate the sand)
of the sand, and as such the filtration rate of the swash water and the water
content of the beach. This results in a higher permeability but lower porosity of
the sand. The water saturation level on beaches with coarse sand is much lower.
Therefore, the interstitial water table (i.e., level below which sediment
is completely water saturated) will surface lower on the beach. This surfacing
of the interstitial water table, or the transition between unsaturated and
saturated surface sand is called the effluent line (EL) and is easily seen as a
“glassy layer” (Fig. 1.3.).
Swash, the run-up and run-off of water on the beach face, is the
transferring agent of wave energy and water to the beach. The swash
characteristics are crucial in the formation of beaches. The swash period,
velocity and interval, in theory, are less favourable or “harsher” on reflective
beaches, with shorter swash periods and intervals and higher swash velocities,
especially at low tide. (McArdle and McLachlan, 1992; Short, 1999). Swash is
directly dependent on wave conditions and beach morphology and slope.
1.1.2. Benthic macrofauna communities
1.1.2.1. What is macrofauna?
Definitions of macrofauna or macrobenthos vary according to
different authors. Mees and Jones (1997) defined macrobenthos as all marine
fauna that is dependent of the sediment and retained on a sieve with 1 mm
mesh-size. Further subdivision includes three groups: endobenthos (i.e.,
animals living in the sediment), epibenthos (i.e., animals living on the
sediment) and hyperbenthos (i.e., animals living in the water column). These
categories do not display sharp boundaries and some species, for instance, live
partially hyperbenthic, partially endobenthic. In general, this kind of division is
based on the sampling device.
Chapter 1 Introduction
25
Parameter Rating Score
Wave action Practically absent 0
Variable, slight to moderate,
wave height seldom exceeds 0,5m. 1
Continuous, moderate,
wave height seldom exceeds 1 m. 2
Continuous, heavy,
wave height mostly exceeds 1m. 3
Continuous, extreme,
Wave height never less than 1.5 m. 4
Surf zone width Very wide, waves first break on bars 0
(only if wave action Moderate, waves usually break
score >1m) 50-100 m from shore 1
Narrow, large waves break on beach 2
% very fine sand >5% 0
(65-125m) 1-5% 1
<1% 2
Slope of the intertidal
Median particle diameter (m) >1/10 1/10-1/15 1/15-1/25 1/25-1/50 >1/50
>710 (>0.5) 5 6 7 7 7
500-710 (1-0.5). 4 5 6 7 7
350-450 (1.5-1). 3 4 5 6 7
250-350 (2-1.5). 2 3 4 5 6
180-250 (2.5-2). 1 2 3 4 5
180 (>2.5). 0 0 1 2 3
Depth of reduced layer (cm) 0-10 0
10-25 1
25-50 2
50-80 3
>80 4
Stable burrows Present 0
Absent 1
Maximum score 20
Minimum score 0
Score Beach type Description
1-5 Very sheltered Virtually no wave action, shallow reduced
layers, abundant macrofaunal burrows
6-10 Sheltered Little wave action, reduced layers present,
usually some macrofaunal burrows
11-15 Exposed Moderate to heavy wave action, reduced
layers deep if present, usually no burrows
16-20 Very exposed Heavy wave action, no reduced layers,
macrofauna only of tough motile fauna
Table 1.1. Rating scheme for assessing the degree of exposure of sandy beaches,
modified from McLachlan (1980)
Chapter 1 Introduction
26
Some other authors extend this size definition to all animals that are
retained on a 0.5 mm mesh-sized sieve (e.g. Brazeiro and Defeo, 1996; Defeo
and Martínez, 2003). In this study we use the macrofauna definition as
endobenthos, those animals that live buried in the sediment and are sampled by
means of a metal cylinder core (Ø= 25 and 15.5 cm) and a 1 mm mesh-sized
sieve (Figure 1.8.).
Figure 1.8. 1 mm sieving bag and metallic cylinder (25 cm Ø) for sampling procedure
During long time, ocean sandy beaches have been regarded as marine
deserts and the biological study has been traditionally lagged behind that of
rocky shores and other ecosystems with obvious exuberant life. The typical
sandy beach nature of constant change is the main macrofauna community
organizer (McLachlan, 1983). Although sandy beaches, at first sight, look
uniform and devoid of living organisms they are teeming with life, microscopic
and macroscopic.
1.1.2.2. Sandy beach macrofauna
Sandy beach macrofauna, as defined above, consists mainly of animals
belonging to three taxa: Crustacea, Annelida (mainly Polychaeta) and
Mollusca. Species composition and distribution of sandy beach macrofauna
change at different spatial scales. There are differences in macroscale (between
Chapter 1 Introduction
27
different coastal areas and latitudes) mesoscale (within one beach along shore
and cross-shore) and microscale (biological interactions locally). Whereas the
processes at the macro and mesoscale are physically driven on exposed sandy
beaches, biological interactions such as predation or competition start to play a
role on the microscale (Defeo and McLachlan, 2005; McLachlan and Brown,
2006). Due to these processes at different scales, there is a huge variety in
macrofaunal species richness, abundance and biomass in sandy beach
ecosystem1. Although there are several studies focused on meio and
microfauna, macrofauna forms are by far the better known. They are the main
component in the fauna community dwelling sandy beaches and they are also
easier to collect and identify. The main macrofauna characteristics are the high
mobility and burrowing adaptations to the sediment. It has been suggested that
crustaceans dominate the most exposed beaches and polychaetes the most
sheltered beaches with molluscs reaching maximum abundance in intermediate
situations (Dexter, 1983), although there are many exceptions in this theoretical
distribution (see Chapters 3 and 4).
1.1.2.3. Macrofauna distribution patterns
Within one geographical region the general pattern in sandy beach
macrofauna is a decrease in species richness, abundance and biomass when
moving along the morphodynamic gradient (Figure 1.9.); i.e., from the
dissipative to the reflective beach state. This pattern, which is found at any
place in the world, is now considered one paradigm in sandy beach ecology
(e.g. Defeo and McLachlan 2005; McLachlan and Brown, 2006). Beaches can
be described by a set of physical parameters; most of them could be potential
structuring factors for sandy beach macrofauna. In fact, sandy beaches are
considered physically controlled environments where the role of biological
1 Ecosystem in this text refers to a system made of individuals of many species, within
a delimited area, and involved in an interaction process, expressed by means of energy
exchange or a sequence of birth and death, and one of the results can be the evolution at
species level and the succession at system level. (Margalef, 1995).
Chapter 1 Introduction
28
factors in structuring beach communities2 is dubious (McLachlan and
Jaramillo, 1995). There is a general trend, for instance, of increasing species
richness with decreasing grain size and beach face slope, increasing tidal range
and intertidal width and/or decreasing harsh swash climate (e.g. Jaramillo and
McLachlan, 1993; Brazeiro, 1999; McLachlan and Dorvlo, 2005).
The main hypothesis proposed to explain the relationship between
macrofauna and beach morphodynamic is known as “Swash Exclusion
Hypothesis”. This hypothesis states that the decrease in species richness,
abundance and biomass is caused by increasing harshness of the swash climate
together with a steeper slope and coarser sand. In some situations, species can
be excluded from extreme systems (McLachlan et al., 1995). This theory
suggests that the burrowing ability could be a determinant factor in species
2 Community concept: Ecologists study the distributions, abundances and interactions
among organisms at a variety of spatial scales of organization. The problem arises
when the whole set of species found in the same place is considered. Communities are
supposedly the actual units of study for many ecologists and there seem to be two, very
different ways of viewing a community. One is that species exist in integrated
communities that have persistent features through time and are repeated in different
places. Thus, the ecological community of species is organized, structured and
integrated. The species are interdependently interactive and, often, it is presumed that
the interactions are, at least in part, responsible for maintaining the entity. The
alternative view describes community as the collection of organisms that are found in
the same place at the same time. They may or may not interact. They coexist because
they have similar physiological responses to physical components of the environment
and/or they have similar needs for resources of food and shelter. Alternatively, some of
them may be present because they need others as prey. The reality is probably
somewhere in between. To avoid some of the confusion associated with the term
community, the two ecological approaches will here be referred to using the term
“community” for tightly-knit, consistent sets of species and “assemblage” will be used
for the more loosely associate set of co-occurring species, where the whole set of
species is not a repeatable, identifiable set (Underwood, 2006).
Chapter 1 Introduction
29
distribution and community structure from different beach types (Dugan et al.,
2004). Those species with better burrowing capacity would be able to inhabit
successfully reflective beaches with steeper slopes and very active swash
climate.
In contrast, in flat slope beaches, organisms with a much wider range
of behavioural and morphological adaptations are expected. Furthermore, it is
important to have in mind the existence of semi-terrestrial species, less
influenced by the swash climate, which generally have autonomous active
movement on upper beach levels (Defeo and McLachlan, 2005).
Figure 1.9. General conceptual model relating biological descriptors and beach state
(after Defeo and McLachlan, 2005). At a finer scale and under more dissipative
conditions, biological factors become more important. (R: reflective; I: intermediate; D:
dissipative; UD: ultradissipative; TF: tidal flat)
At population level this was translated into the “Habitat Harshness Hypothesis”
(Defeo et al., 2001) which postulates that on reflective beaches the harsh
environment forces macrofauna to divert more energy towards maintenance,
leaving less for reproduction and causing higher mortality. Brazeiro (2001)
found that not only swash and sediment characteristics but also the accretion-
Chapter 1 Introduction
30
erosion dynamics on beaches could influence sandy beach macrofauna. All
these existing ideas were synthesised in the “Hypothesis of Macroscale
Physical Control” (McLachlan and Dorvlo, 2005) where two levels of factors
controlling the macroscale patterns are identified. The first level is controlled
by two main factors, tidal range and latitude which determine the maximum
number of species that can occur under ideal conditions in a particular region.
Furthermore, a second level is controlled by swash climate, sediment grain size
and beach stability which limit the actual species count through exclusion of
less well-adapted species under harsher, more reflective conditions.
1.1.2.4. Macrofauna zonation in the sandy beach
Faunal zonation is a well described feature of intertidal zones and has
been much studied in marine ecology. Zonation on sandy beaches is not nearly
as visible as on rocky shores. This is probably a consequence of the dynamic
environment of the beach and the shifting populations that occupy it. Like the
macroscale, macroinfauna communities and assemblages are primarily
physically structured (McLachlan, 1983). The macrofauna is spread alongshore
and cross-shore. In fact beach length is thought to play an important role with a
decrease in species richness with decreasing beach length (Brazeiro, 1999). In
general macrofaunal populations are most developed in the middle of a beach,
with a unimodal bell-shaped distribution towards both sides. Other factors that
can influence the along shore distribution of macrofaunal species include the
presence of rocky shores, human impact, estuarine input or the shape of the
beach (McLachlan and Brown, 2006). Cross-shore variability can be divided
into general macrofaunal patterns and zonation; i.e., the sum of the response of
each species to cross-shore gradients. The general cross-shore pattern is an
increase in species number towards the subtidal area (e.g. McLachlan and
Jaramillo, 1995; McLachlan and Brown, 2006).
Many studies have been published on the zonation of sandy beach
macrofauna (McLachlan and Jaramillo, 1995). Two general zonation schemes
have been traditionally used to determine distributions of organisms on sandy
beaches: Dahl (1952) defined three biological zones in terms of typical
Chapter 1 Introduction
31
crustacean fauna inhabiting each zone, and Salvat (1964) defined four physical
zone based on sand moisture content across shore (Figure 1.10. and Fig. 1.6.).
The correspondence between both schemes is fairly good and zonation schemes
proposed by other authors can generally be considered variations on these two
schemes. Perhaps the most elementary, but also widely applicable, zonation
scheme for sandy shores is that proposed by Brown (in McLachlan, 1983, cited
in Mclachlan and Brown, 2006). This suggests that only two zones can be
recognised on sandy shores (see Chapter 3): a zone of air-breathers (mainly
crustaceans and insects) at and above the drift line and a zone of water-
breathers below this. The general conclusion from the latter studies was that it
was difficult to fit the data neatly into any one of the schemes proposed
(McLachlan and Jaramillo, 1995; McLachlan and Brown, 2006).
Several studies in different regions have suggested that different beach types
and physical factors might cause differences in zonation (e.g. Trevallion et al.,
1970; Bally, 1983; Jaramillo et al., 1993; McLachlan y Jaramillo, 1995).
Quantitative analysis give partial support for three zones, but the number of
recognizable zones depends on beach type, reflective beaches having fewer
zones than dissipative beaches (McLachlan and Jaramillo, 1995; Defeo and
McLachlan, 2005). In dissipative and intermediate beaches, lower zones
present high macrofauna abundance and species richness and may frequently
be subdivided in three or even four different zones towards the most dissipative
cases. In the other hand, impoverished fauna was found downshore on
reflective beaches due to the harsh hydrodynamic conditions (Figure 1.11.). At
the extremes of beach morphodynamics, only the supralittoral zone may be
found on extreme reflective beaches and up to four zones are recognised on
wide dissipative beaches. In general, zones are clearest at the top of the shore
and become increasingly blurred moving downshore (McLachlan and
Jaramillo, 1995) where there is no clear agreement with Dahl’s scheme on
extreme reflective beaches (Fig. 1.9.).
Chapter 1 Introduction
32
Figure 1.10. Overview of the three most common zonation schemes for sandy beach
macrofauna (after McLachlan and Brown, 2006). ELWS: Extreme Low Water Spring
Tide; EHWS: Extreme High Water Spring Tide.
It should be noted that zonation on sandy beaches is an extremely
variable phenomenon, on both, the short and the long term (Brazeiro and
Defeo, 1996). Moreover, zones are not defined by sharp boundaries, making
the identification of zonation patterns difficult and often not statistically
supportable (Brazeiro, 1999). The causes and mechanisms for maintenance of
intertidal zones are complex and individual species exhibit great variability and
considerable overlaps with other species. Locomotory and migratory
adaptations of the fauna shuffle and recreate zones daily and with each tidal
cycle. These points indicate a dynamic and variable scenario but it is clear that
zonation occurs, although is not precise, and attempting to delineate it too
finely would be hazardous. At the population level, zonation patterns and
patchiness respond to an environment that is spatially and temporally structured
by sharp gradients. As faunal zones are dynamic, temporal studies are needed
Chapter 1 Introduction
33
for a full picture of zonation patterns, requiring intensive sampling to provide
unbiased estimates.
Biological factors are known to be of key importance in the
establishment and maintenance of zonation on rocky shores, with recruitment,
predation and competition all playing central roles (Underwood and Denley,
1984). On soft shores, however, factors controlling communities are different
(Peterson, 1991). Competition for space is unlikely to be important, because the
mobility of the macrofauna and vertical distribution through the sediment (see
Chapter 5). Because of this mobility, larval recruitment is less critical in
establishing or maintaining zones than in sessile species on rocky shores;
rather, it may play a role in the initial establishment of populations on a beach
(Brown, 1983). The only biological factors likely to be important in affecting
zonation on sandy beaches are predation and competition for food.
1.1.2.5. Feeding habits and survival strategies of the macrofauna
Ocean sandy beaches are a hostile, physically controlled environment
and conditions can vary considerably over very short time periods. Hence,
macrofauna inhabiting sandy beaches should be highly adapted to this dynamic
habitat. Food input to soft intertidals can be defined as erratic and unpredictable
in occurrence and it is strongly related to the external input from the water
column; either as particulate organic matter or as detritic dissolved organic
matter ready to be absorbed or filtrated. Food inputs to beaches may be divided
into the categories listed in Table 1.2. The resident primary producers on
beaches are epipsammic diatoms. On sheltered beaches and flats of fine sand
these may contribute to a measurable, but never high, primary productivity
(McLachlan and Brown, 2006). Several morphological and behavioural
solutions have evolved to cope with the dynamic and variable conditions on
sandy beaches.
Chapter 1 Introduction
34
Food type Source Remarks
Benthic microflora Beach sand On sheltered beaches
Surf diatoms, flagellates Surf water In well-developed surf zones
Stranded macrophytes The sea Near kelp beds, seagrass meadow,
estuaries, etc
Carrion The sea Especially near seabird and seal
colonies
Particulates The sea -
Dissolved organics The sea -
Insects The land Particularly during strong,
offshore winds
Organic detritus The land From dune vegetation
Table 1.2. Food sources for sandy beaches (modified from McLachlan and Brown,
2006).
Trophic groups among the intertidal macrofauna include predators,
scavengers, filter/suspension feeders and deposit feeders (the later only
important on relatively sheltered shores). Most of the food that is consumed in
sandy beaches is exogenous through swash (Romar and McLachlan, 1986) or
wrack input (Colombini and Chelazzi, 2003; Dugan et al., 2003), making
predation amongst macrofaunal species less important. The absence of attached
macrophytes on intertidal sands dictates a predominance of filter feeders and
scavengers among the resident invertebrate macrofauna. There are few highly
specialised feeders on sandy beaches, opportunism being the order of the day.
The number of carnivorous species in sandy beaches is very limited
and some of them feed on the interstitial meiofauna (McLachlan, 1990).
Scavengers, however, are very common on sandy beaches and they accept a
wide variety of food and will typically turn predator when the opportunity
arises because carrion represents a highly erratic food supply. These animals
have developed a number of feeding methods and have acquired several
morphological and behavioural adaptations to locate and consume carrion
efficiently. They can be found anywhere on a beach, from the sublittoral fringe
to the foredunes. In the turbulent environment of the sandy beach, suspended
food is always available, although it may be variable in nature and quantity.
Filter/suspension feeders usually dominate the community making direct
filtering of the swash or interstitial (McLachlan and Brown, 2006) and consist
largely of bivalves. Where conditions are optimal on exposed beaches (for
Chapter 1 Introduction
35
example, in dissipative situations where rich surf diatoms develop), suspension
feeders can maintain huge populations and biomass.
Figure 1.11. Diagrammatic representation of the zonation patterns of the intertidal
macroinfauna in sandy beaches of southern Chile (after Jaramillo et al. 1993).
1.Orchestia tuberculata (Amphipoda), 2.Excirolana hirsuticauda, 3.E. braziliensis,
4.E. monodi (Isopoda), 5.Phalerisidia maculata (Coleoptera), 6.Emerita analoga
(Anomura), 7.Bathypoireiapus magellanicus, 8.Huarp sp., 9.Phoxocephalopsis
mehuinensis (Amph.), 10.Nepthys impresa (Polychaeta), 11.Macrochiridothea setifer,
12.Chaetilia paucidens (Isop.), 13.Lepidopa chilensis (Anom), 14.Bellia picta
(Brachyura), 15.Mesodesma donacium (Bivalvia).
In most situations, and certainly on reflective and intermediate beaches,
motile feeders and scavenger/predators dominate the sandy beach macrofauna.
Where the fauna is impoverished, such as on steep beaches with coarse sand
(Fig. 1.11.), supralittoral macrofauna such as talitrids amphipods may be most
important as a consequence of the absence of truly intertidal forms. Deposit
Chapter 1 Introduction
36
feeders are usually a minor component, except on sheltered shores and in the
sublittoral. Sheltered intertidals are stable enough to allow the construction of
semipermanent burrows deposit feeders. Riccardi and Bourget’s (1999)
analysis of broad community patterns in marine sedimentary communities
showed that deposit feeders increase with more sheltered conditions, finer
sediments and flatter slopes with carnivores also preferring more sheltered
shores.
Macrofauna inhabiting exposed sandy beaches is basically dependent
on phytoplankton and marine macrophytes inputs because of the scant primary
production occurrence on this habitat itself (Inglis, 1989; McLachlan and
Brown, 2006). The sea is by far the more important source of food, supplying
particulates for the filter feeders and carrion and plant debris for the
scavengers. The size of beach populations is therefore probably closely related
to the richness of the inshore waters, particularly in terms of particulate
material (see Chapters 4, 5, and 6). The most important predatory pressure on
sandy beaches is exogenous as well: birds or insects from land and fish or large
crustaceans from the sea.
Other survival strategies refer to the locomotory and migration
adaptations, burrowing mechanisms and orientation. The extremely dynamic
nature of nutrition on sandy beaches in terms of availability and location
highlights the advantage of high mobility of macrofauna which is crucial for
optimising feeding time, reproduction and escape response. Generally, this
predator escape response consists of deep burrowing during low tide, although
some forms have swimming or crawling escape responses (McLachlan and
Brown, 2006). The locomotory and migratory adaptations itself originate from
the combination of three environmental challenges: the instability of the
substratum, the swash action and tide. There exist a number of burrowing
mechanisms depending on the species, whether it is a soft-bodied animal such
as polychaetes and molluscs or a crustacean with rigid exoskeleton. These
mechanisms, as well as reproduction are not the aim of this thesis and will not
be discussed further.
Chapter 1 Introduction
37
1.1.3. Food sources in sandy beaches
1.1.3.1. Food availability
It has been shown that food availability is a major structuring factor of
marine benthos affecting structure and metabolism of the marine benthic
community (e.g. Pearson and Rosenberg, 1987; Graf, 1989; Dugan et al.,
2003), and that species diversity in intertidal soft-sediments is strongly
correlated with food availability (Withlaton, 1981). Moreover, food resources
may be one of the most probable explanations for marine population patchiness
(Decho and Fleeger, 1988) and for benthic community distribution, temporal
variability and metabolism (Montagna, et al., 1983; Rudnick et al., 1985). Food
availability is tightly linked to the biochemical composition of organic matter
(Danovaro et al., 1993) and determining organic matter composition is crucial
in assessing food quality and quantity in benthic ecological studies (see
Chapters 4 and 5).
The biochemical composition of organic matter is the result of the
dynamic equilibrium between external inputs, autochthonous production and
heterotrophic utilisation (Fabiano and Danovaro, 1994). Organic matter in
marine sediments is composed of labile and refractory compounds (Fabiano
and Danovaro, 1994). Simple sugars, fatty acids and proteins that are rapidly
mineralised have been used to assess the labile portion of organic matter
(Fichez, 1991; Danovaro et al., 1993). These labile compounds have been used
to estimate the nutritional value of the sediment (Buchanan and Longbottom,
1970). The biochemical composition of sedimentary organic matter has been
broadly researched in many marine ecosystems, such as deep sea (Danovaro et
al., 1993), semi-enclosed marine systems (Pusccedu et al., 1999), subtidal
sandy sediments (Fabiano et al., 1995), seagrass bed (Danovaro et al., 1994)
and estuarine environments (Fabiano and Danovaro, 1994). However, in spite
of the importance of the biochemical composition of the sedimentary organic
matter (i.e. carbohydrates, lipids and proteins), there is a conspicuous lack of
information about concentrations and variability of these compounds in
intertidal sediments (Incera et al., 2003a).
Chapter 1 Introduction
38
1.1.3.2. The role of the biochemical composition and hydrodynamic
conditions
It is generally admitted that biological richness, abundance and
biomass differ significantly between sheltered and exposed intertidal
environments. Sheltered intertidals have a high abundance and diversity being
important nursery areas for a large number of vertebrate and invertebrate
species (Adam 1990). In the other hand, explained in previous section,
biological richness diminishes with increasing exposure of the intertidal (Fig.
1.9.). This is supposed to be a consequence of the different physical and
hydrodynamic features found between these two opposite intertidal habitats
(McLaclhlan, 1983) and it is suggested that the major hydrodynamic stress of
exposed localities limits their biological richness (McLachlan et al., 1996).
Other hypothesis rather than the Swash Exclusion Hypothesis can be proposed
to explain the relationship between macrofauna and beach characteristics
without being mutually exclusive. The larger availability of organic matter and
the higher retention of organic particles in flat as opposed to steep slope
beaches can explain the observed macrofaunal pattern, i.e., higher abundance
and diversity in sheltered shores compared to exposed beaches (Incera et al.,
2003a, b).
Beach profile and morphodynamics have relevant consequences on the
macrofaunal distribution patterns in the sediments, not only because of the
hydrodynamic activity but also because of the several nutritive contributions
throughout the intertidal profile. While, downshore in the exposed intertidal the
species richness diminishes, macrofauna finds a more stable environment upper
on the shore (Defeo and Gómez, 2005). This tidal level is less influenced by the
swash climate and insects and crustaceans inhabiting this zone are well adapted
to desiccation (McLachlan, 1990; Little, 2000). Invertebrate macrofauna
communities dwelling the supratidal depend largely upon allochthonous inputs
such as drift macrophytes and other stranded material (see Chapter 6)
associated with oceanographic processes (Colombini and Chelazzi, 2003,
Dugan et al., 2003). Sheltered beaches have more favourable environmental
Chapter 1 Introduction
39
conditions and higher sediment stability (see Chapters 4 and 5), which favour a
much wider range of behavioural and morphological adaptations.
Many exposed sandy beaches worldwide receive large amounts of drift
seaweed, known as wrack, from offshore algal beds and closer rocky intertidal
shores (Inglis, 1989; Rossi and Underwood, 2002; Dugan et al., 2003). The
importance of beach accumulations of wrack on the ecology of sandy beaches
has been well supplied in the literature (see Colombini and Chelazzi, 2003 and
references therein). Algal wrack deposits represent the main food resource for
upper shore detritus feeders like talitrid amphipods, oniscoid isopods and
tenebrionid and staphylinid beetles (Colombini and Chelazzi, 2003; Dugan et
al., 2003; Olabarria et al., 2007). Disturbance by wrack has been implicated as
a potentially important factor structuring local assemblages of invertebrates.
Furthermore, wrack also acts as a refuge supply for the supralittoral fauna,
mainly terrestrial and semiterrestrial arthropods, providing an opportunity to
study seaweed debris both as a food resource and shelter habitat (Inglis, 1989;
Colombini and Chelazzi, 2003). The origin and composition of sedimentary
organic matter have been proposed as one of the key factors, together with the
physical environment, for the control of the beach fauna (Incera et al., 2003b).
1.1.4. Aims and thesis linework.
Intertidal shoreline is a threaten ecosystem under increasing pressure
from urbanisation, with 50% of the world’s population now living by the coast
(GESAMP 1990). Because of the overwhelming rate of development on coastal
shorelines during the last decades and the vulnerability of this fragile
ecosystem in this region, there is growing public demand for sustainable
management intervention focused on the use, control and preservation of these
areas (Peterson et al., 2000, Peterson and Bishop, 2005). Furthermore, sandy
beach ecosystem is a highly productive interface between land and sea put at
severe risk of dramatic future modification from impacts of global warming
and consequent sea level rise (Brown and McLachlan, 2002; Peterson and
Bishop, 2005).
Chapter 1 Introduction
40
Together with the recreational interest, we have to take heed of the
outstanding anthropogenic activities in the northern coast of Spain. Galician
coast is well known due to the important production of marine species with
economical interest. For instance, clam and cockle collection by hand is a
common activity in this highly productive area. Coastal shellfish fisheries are
an important socioeconomic productive sector with ecological relevance in
Galician sandy shores. This, together with other economical activities, causes a
relevant effect in the structure and organization of benthic communities from
the intertidals.
Part II. The ecology of sandy beaches.
During this thesis, no quantitative studies had been published on the
macrofauna of sandy beaches from the North coast of Spain. Even more, few
general studies on mesotidal sandy beaches from temperate regions in Europe
have been accomplished. Hence, a baseline study about the ecology of sandy
beaches from this shoreline was required to start this study, and this was the
main task of the second part of this thesis.
Chapter 2 deals with the effect of several environmental factors on
benthic macrofauna inhabiting the most typical kind of exposed soft intertidal
worldwide, i.e., intermediate sandy beaches. The impact of morphodynamics
and abiotic factors on ten intermediate sandy beaches along the north coast of
the Iberian Peninsula was analysed following a gradient of exposure. Several
characteristics of sandy beach fauna were utilised; highlighting biotic factors
such as species richness, macrofauna abundance and biomass. This pioneer
study on sandy beach ecology was complemented with a broader analysis about
intertidal community structure and macrofauna zonation in Chapter 3. This
chapter of the thesis offers a more detailed study of the intertidal zonation,
focused on macrofauna community dynamics in intermediate sandy beaches.
The results obtained in this chapter were compared with several traditional
zonation schemes and it was suggested a possible macrofauna community
distribution and zonation based on the peculiar beach profile found in this
region. Different morphodynamic parameters and biotic factors were further
Chapter 1 Introduction
41
analysed and discussed. These two chapters have been published in Estuarine,
Coastal and Shelf Science.
Part III. The importance of exposure rate in the community structure:
hydrodynamic conditions and food available.
Chapter 4 goes deep in the characteristics of macrofauna community
structure, focusing on wave exposure and food availability in sandy beaches.
The effects of several physical parameters and food availability were analysed
and compared between sheltered and exposed sandy beaches. Both effects have
been considered main factors affecting community structure and benthic
metabolism. The results obtained in this study reaffirm the macrofauna
zonation patterns found previously in intermediate sandy beaches from the
North coast of Spain (Chapter 3). Furthermore, this study underline exposed
sandy beaches as physically controlled environments; while in sheltered
sedimentary environments biological interactions become more important. The
aims of this study were to investigate the influence of the physical
characteristics on the intertidal macroinfauna community along a gradient of
wave exposure and the importance of the food available in beaches with
different hydrodynamic conditions. The results and conclusions obtained in this
chapter were published in Hydrobiologia.
Part IV. The role of food availability in sandy beaches: spatial and
temporal patterns.
Due to the importance of external food inputs in the macrofauna
community structure of sandy beaches, this part of the thesis analysed
separately two types of beaches based on the exposure rate, i.e., sheltered and
exposed. Food availability is a potentially important determinant of consumer
abundance in natural communities, and the densities and growth rates of
consumers may be positively associated with food supply (in situ or
allochthonous) in soft intertidals. Macrofauna communities inhabiting sandy
beaches are supported almost entirely by allochthonous inputs of organic
material, mainly phytoplankton and marine macrophytes (macroalgae,
seagrasses). The role of food available in the exposed intertidal studied was
focused particularly on the wrack input, while in the sheltered intertidal the
Chapter 1 Introduction
42
effect of the biochemical composition of sedimentary organic matter in benthic
macrofauna community was stressed.
Chapter 5 describes the seasonal variability in the vertical distribution
of the benthic macrofauna and sedimentary parameters in a sheltered estuarine
beach. This chapter investigates the relationship between biochemical
composition of the sedimentary organic matter and macroinfauna from a
sheltered beach. This chapter was accepted for publication in Estuaries and
coasts.
In Chapter 6 we used experimental manipulation of algal wrack, i.e.,
artificial patches of macrophytes to test hypotheses about influences on
macrofaunal assemblages inhabiting the upper shore level and drift line of
different sites along an exposed sandy beach. We investigated the abundance of
colonising individuals and species and also succession processes (i.e., sequence
of colonisation and species replacement) and time variability. The novelty of
this study includes the effect of invasive wrack species on macrofaunal
assemblages on sandy beaches. This chapter was accepted for publication in
Journal of Experimental Marine Biology and Ecology.
Part V. General discussion.
In the general discussion, Chapter 7, all results of the previous chapters
were integrated and discussed. Some general concepts in sandy beach ecology
are confirmed, while others are put into question, and new ideas are proposed
based on collected results and observations.
1.1.5. List of references
Adam, P. 1990. Saltmarsh ecology. Cambridge: Cambridge University Press.
473pp.
Bally, R. 1983. Intertidal zonation on sandy beaches of the west coast of South
Africa. Cahiers de Biologie Marine 24: 85-103.
Brazeiro, A. 1999. Community patterns in sandy beaches of Chile: richness,
composition, distribution and abundance of species. Revista Chilena de
Historia Natural 72: 99-111.
Brazeiro, A. 2001. Relationship between species richness and morphodynamics
in sandy beaches: what are the underlying factors?. Marine Ecology
Progress Series 224: 35-44.
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Brazeiro, A. and Defeo, O. 1996. Macroinfauna zonation in microtidal sandy
beaches: is it possible to identify patterns in such variable
environments. Estuarine Coastal and Shelf Science 42: 523-536.
Brown, A.C. 1983. The ecophysiology of sandy beach animals, a partial
review. In Sandy beaches as ecosystems, A. McLachlan and T.
Erasmus (eds.), The Hague:Junk 575-605.
Brown, A.C. and McLachlan, A. 2002. Sandy shore ecosystems and the threats
facing them: some predictions for the year 2025. Environmental
Conservation 29: 62-77.
Buchanan, J. 1984. Sediment analysis. In: Holme and McIntyre (eds.). Methods
for the study of marine benthos. Oxford and Edinburg Blackwell
Scientific Publications: 41-65.
Buchanan, J.B. and Longbottom, M.R. 1970. The determination of organic
matter in marine muds: the effects of the presence of coal and the
routine determination of proteins. Journal of Experimental Marine
Biology and Ecology 5: 158-169.
Colombini, I. and Chelazzi, L. 2003. Influence of marine allochthonous input
on sandy beach communities. Oceanography and Marine Biology:
Annual review 41: 115-159.
Dahl, E. 1952. Some aspects of the ecology and zonation of the fauna on sandy
beaches. Oikos 4: 1-27.
Danovaro, R., Fabiano, M. and Della Croce, N. 1993. Labile organic matter
and microbial biomasses in deep-sea sediments (Eastern Mediterranean
Sea). Deep sea Research 40: 953-965.
Danovaro, R., Fabiano, M. and Boyer, M., 1994. Seasonal changes of benthic
bacteria in a seagrass bed (Posidonia oceanica) of the Ligurian Sea in
relation to origin, composition and fate of the sediment organic matter.
Marine Biology 119: 489-500.
Davies, J. 1964. A morphogenic approach to Word shorelines. A. Geomorphol.
8: 127-142.
Decho, A.W. and Fleeger, J.W. 1988. Microscale dispersion of meiobenthic
copepods in response to food-resource patchiness. Journal of
Experimental Marine Biology and Ecology 118: 229-243.
Defeo, O. and Martínez, G. 2003. The habitat harshness hypothesis revisited:
life history of the isopod Excirolana braziliensis in sandy beaches with
contrasting morphodynamics. Journal of Marine Biological
Association of United Kingdom 83: 331-340.
Defeo, O and McLachlan, A. 2005. Patterns, processes and regulatory
mechanisms in sandy beach macrofauna. A multiscale analysis. Marine
Ecology Progress Series 295: 1-20.
Defeo, O. and Gómez, J. 2005. Morphodynamics and habitat safety in sandy
beaches: life-history adaptations in a supralittoral amphipod. Marine
Ecology Progress Series 293. 143-153.
Defeo, O., Gómez, J. and Lercari, D. 2001. Testing the swash exclusion
hypothesis in sandy beach populations: the mole crab Emerita
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Dexter, D.M. 1983. Community structure of intertidal sandy beaches in New
South Wales, Australia. In McLachlan, A. and T. Erasmus (Eds.),
Sandy Beaches as Ecosystems. The Hague: Junk.
Dugan, J., Hubbard, D.M., McCrary, M.D. and Pierson, M.O. 2003. The
response of macrofauna communities and shorebirds to macrophyte
wrack subsidies on exposed sandy beaches of southern California.
Estuarine Coastal and Shelf Science 58S: 25-40.
Dugan, J., Jaramillo, E., Hubbard, D.M., Contreras, H. and Duarte, C. 2004.
Competitive interactions in macroinfaunal animals of exposed sandy
beaches. Oecologia 139: 630-640.
Fabiano, M. and Danovaro, R. 1994. Composition of organic matter in
sediments facing a river estuary (Tyrrhenian Sea): relationships with
bacteria and microphytobenthic biomass. Hydrobiologia 277: 71-84.
Fabiano, M., Danovaro, R. and Fraschetti, S. 1995. A 3-year time series of
elemental and biochemical composition of organic matter in subtidal
sandy sediments of the Ligurian Sea (north-western Mediterranean).
Continental Shelf Research 15: 1453-1469.
Fichez, R. 1991. Composition fate of organic matter in submarine cave
sediments; implications for the biogeochemical cycle of organic
carbon. Oceanologica Acta 14: 369-377.
GESAMP (Joint Group of Experts on the Scientific Aspects of Marine
Pollution) 1990. The state of the environment. Blackwell Scientific
Publications, Oxford.
Graf, G. 1989. Pelagic-benthic coupling in a deep-sea benthic community.
Nature 341: 437-439.
Incera, M., Cividanes, S.P., López, J. and Costas, R. 2003a. Role of
hydrodynamic conditions on quantity and biochemical composition of
sediment organic matter in sandy intertidal sediments (NW Atlantic
coast, Iberian Peninsula). Hydrobiologia 497: 39-51.
Incera, M, S.P. Cividanes, M. Lastra & J. López 2003b. Temporal and spatial
variability of sedimentary organic matter in sandy beaches on the
northwest coast of the Iberian Peninsula. Estuarine, Coastal and Shelf
Science 58: 55-61.
Inglis, G., 1989., The colonisation and degradation of stranded Macrocystis
pyrifera (L.) C. Ag. by the macrofauna of a New Zealand sandy beach.
Journal of Experimental Marine Biology and Ecology 125: 203- 217.
Jaramillo, E. and Gonzales, M. 1991. Community structure of the macrofauna
along a dissipative-reflective range of beach category in southern
Chile. Studies on Neotropical Fauna and Environment 26: 193-212.
Jaramillo, E. and McLachlan, A. 1993. Community and population responses
of the macroinfauna to physical factors over a range of exposed sandy
beaches in south-central Chile. Estuarine Coastal and Shelf Science 37:
615-624.
Jaramillo, E., McLachlan, A. and Coetzee, P., 1993. Intertidal zonation patterns
of macroinfauna over a range of exposed sandy beaches in south
central Chile. Marine Ecology Progress Series 101: 105-118.
Little, C., 2000. The Biology of Soft Shores Estuaries. Oxford University Press,
N. York. 252pp
Chapter 1 Introduction
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Margalef, R. 1996. Ecología. Ed. Omega. 951 pp.
Masselinck, G. and Short, A. 1993. The effect of tide range on beach
morphodynamics and morphology: a conceptual beach model. Journal
of Coastal Research 9 (3): 785-800.
Mees, J. and Jones, M. 1997. The hyperbenthos. Oceanography and Marine
Biology: Annual review 35: 221-255.
McArdle, S and McLachlan, A., 1992. Sand beach ecology: Swash features
relevant to the macrofauna. Journal of Coastal Research. 8: 398-407.
McLachlan, A. 1980. The definition of Sandy Beaches in Relation to Exposure:
Simple Rating System. South African Journal of Science. 76, 137-138.
McLachlan, A. 1983. Sandy beach ecology: a review. In: A. McLachlan and T.
Erasmus, (eds.). Sandy Beaches as Ecosystems. Junk. The Hague, The
Netherlands. 321-380 pp.
McLachlan, A. 1990. Dissipative beaches and macrofauna communities on
exposed intertidal sands. Journal of Coastal Research 1, 57-71.
McLachlan, A. 1996. Physical factors in benthic ecology: effects of changing
sand particle size on beach fauna. Marine Ecology Progress Series 131:
205-217.
McLachlan, A. and Jaramillo, E., 1995. Zonation on Sandy Beaches.
Oceanography and Marine Biology: an Annual Review 33: 305-335.
McLachlan, A. and A. Dorvlo 2005. Global patterns in sandy beach
macrobenthic communities. Journal of Coastal Research 21(4): 674-
687.
McLachlan, A., Brown, A.C., 2006. The ecology of sandy shores. Acad. Press,
Amsterdam.
McLachlan, A., Jaramillo, E., Donn, E. and Wessels, F., 1993. Sandy Beach
Macrofauna Communities and their Control by the Physical
Environment: A Geographical Comparison. Journal of Coastal
Research 15: 27-38.
McLachlan, A., Jaramillo, E., Defeo, O., Dugan, J., de Ruyck, A. and Cohetes,
P. 1995. Adaptations of bivalves to different beach types. Journal of
Experimental Marine Biology and Ecology 187: 147-160.
McLachlan, A., de Ruyck A. and Hacking, N. 1996. Community structure on
sandy beaches: patterns of richness and zonation in relation to tide
range and latitude. Revista Chilena de Historia Natural 69: 451-467.
Montagna, P.A., Coull, C.B., Herring, T.L. and Dudley, B.W. 1983. The
relationship between abundances of meiofauna and their suspected
microbial food (diatoms and bacteria). Estuarine, Coastal and Shelf
Science 17: 381-394.
Olabarria, C., Lastra, M. and Garrido, J. 2007. Succession of macrofauna on
macroalgal wrack of an exposed sandy beach: Effects of patch size and
site. Marine Environmental Research 63: 19-40.
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marine benthic communities. In Gee, J.H.R. & P. S. Giller (eds.).
Organization of Communities, Past and Present. Blackwell Scientific
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Peterson, C.H., Hickerson, D.H.M., and Johnson, G.G. 2000. Short-term
consequences of nourishment and bulldozing on the dominant large
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biomass in marine intertidal communities. Marine Ecology Progress
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nutrients as influences on intertidal macrobenthic assemblages:
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preliminary account of two sandy beaches in south west India. Marine
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45.
PARTE I. INTRODUCCIÓN Y OBJETIVOS.
(Según el acuerdo de 18/06/04 firmado por la Comisión de Doctorado de la
Universidad de Vigo acerca del idioma en que puede escribirse la Tesis doctoral).
Capítulo 1. Introducción general.
Capítulo 1 Introducción
49
1.1.1. Intermareal arenoso: Playas.
1.1.1.1. ¿Qué es una playa?
Comúnmente conocidas como playas, los intermareales arenosos son
ambientes muy dinámicos, hostiles y cosmopolitas (McLachlan, 1996) que han
sido definidos de múltiples maneras para un amplio rango de ambientes, a
veces incluso de forma poco rigurosa.
“una acumulación de arena depositada por el oleaje comprendida entre
la base modal de la ola (i.e. la máxima profundidad a la cual la ola puede
transportar sedimento hacia la orilla) y el límite superior de su zona de batida”
(Short, 1999).
De esta definición surgen los tres requisitos básicos que conforman una
playa: arena, oleaje y la marea. La arena que se ve transportada por el oleaje y
las mareas hacia la orilla conforma una playa. Estos tres factores, en su
conjunto van a determinar la morfodinámica, las comunidades faunísticas; así
como la cantidad y la calidad de la materia orgánica (i.e. disponibilidad de
alimento) que nos encontramos en las playas. En este estudio las playas serán
consideradas, por tanto, como áreas litorales arenosas expuestas al mar
incluyendo la zona de asomeramiento (“shoaling”), la zona de rompiente
(“surf”) y la zona de batida (“swash”) donde se disipa el oleaje (Figura 1.1).
La arena, y por extensión el sedimento, pueden ser clasificados de
acuerdo con su origen y el tamaño de grano. El componente más común de la
arena es el sílice, generalmente en forma de cuarzo (lo que indicaría un origen
terrestre) aunque también es frecuente la presencia de carbonatos (origen
marino). En algunas ocasiones la arena puede estar formada por cascajo de
conchas, materiales volcánicos, coralinos o rocas de diferente origen en forma
de guijarros. Aunque en sedimentología el tamaño de grano se define de
acuerdo con la escala de Wenthworht (Buchanan, 1984) en unidades phi (φ = -
log2 Ø), en este estudio y en la mayoría de los trabajos actuales sobre ecología
de playas se utiliza la escala métrica decimal. Así, cualquier tipo de sedimento
Capítulo 1 Introducción
50
entre 63 μm y 2 mm (0<φ<4) se definirá como arena. El tamaño de grano ha
sido considerado determinante en la estructura de la comunidad faunística en
todos los trabajos relevantes sobre ecología de playas (e.g. Jaramillo y
González, 1991; McLachlan y Dorvlo, 2005; Defeo y McLachlan, 2005) y será
también tratado en este estudio.
Una ola es, en general, el transporte de energía dirigida por el viento a
través del agua. La ola permanece estable mientras que la altura de la misma
(H) sea inferior a 1/7 de su longitud (L) (Figura 1.2.). La acción del oleaje
penetra en la columna de agua hasta una profundidad de aproximadamente la
mitad de la longitud de la ola. Cerca de la orilla, la profundidad del agua
disminuye hasta un punto donde la base de la ola toca el fondo marino. A partir
de aquí, la ola ya no transporta sólo energía sino también material
sedimentario. Esta es, según la definición de Short, la base modal de la ola y
por tanto el límite inferior de nuestra playa. Las olas a partir de este momento
empiezan a compactarse, la longitud de la ola disminuye y la proporción entre
la altura y la longitud de la ola aumenta. Esto corresponde con lo que se
denomina asomeramiento (Fig. 1.1.). La velocidad de la parte baja de la ola se
ralentiza progresivamente debido al arrastre creado por el sedimento y la ola se
hace dependiente de la profundidad; mientras que la parte superior de la ola se
mueve con una velocidad diferente (Fig. 1.2.). La rotura de la ola se produce
cuando la proporción H / L sobrepasa el punto de estabilidad de 1/7 en la zona
de rompiente del oleaje. En la última fase, tras la rotura de la ola, la lámina de
agua llega a la línea de costa y asciende por la pendiente de la playa y
posteriormente desciendo por efecto de la gravedad, mientras la energía de la
ola se disipa. Esta parte se conoce como la zona de batida o zona de swash
(Fig. 1.1.).
La zona de rompiente es un área de rotura turbulenta caracterizada por
una arena conchífera gruesa, agua cargada de arena en suspensión y fuerte
corriente (Figura 1.3.). La zona de batida alcanza la playa, salpicando y
cubriendo la pendiente en forma de una pequeña película de agua dependiendo
entre otras cosas de la fuerza de la ola y del rango mareal; así como de la
pendiente de la playa. Comprende el nivel máximo de subida de las olas y una
Capítulo 1 Introducción
51
zona de agua casi estancada. Tradicionalmente la zona de swash se ha dividido
en una parte saturada, siempre ocupada por el agua, y una insaturada, mojada
periódicamente por las grandes olas y caracterizada por un drenaje sucesivo
entre ola y ola. La zona de rompiente y la de batida saturada se conocen
también como ambiente sublitoral de la playa, mientras que la zona insaturada
correspondería con el mesolitoral (Dahl, 1952). Dependiendo de las
condiciones dinámicas de marea y oleaje habrá una zona de mayor o menor
tamaño permanentemente sumergida en la playa, incluso durante las mareas
más vivas. Finalmente nos encontramos con una zona de riego que nunca va a
estar cubierta por el oleaje pero que sufre la aspersión del mismo. Corresponde
a la parte más alta de la playa y normalmente está compuesta por algún tipo de
complejo dunar. Este ambiente se conoce también con el nombre de zona
supralitoral o subterrestre permanentemente seca y donde la desecación y la
temperatura son los factores de estrés principales para la fauna.
1.1.1.2. El ambiente físico: rango mareal y estratificación del sistema
Las mareas no son un elemento esencial para la formación de una
playa; sin embargo, un aumento de su rango mareal contribuirá
sustancialmente, junto con el oleaje, a la morfología de la playa. Las mareas
provocan impactos esenciales ya que cambian continuamente el perfil de la
orilla, tanto horizontalmente como verticalmente dependiendo del rango mareal
y del perfil del intermareal. En zonas de gran rango mareal, la variación de la
marea puede modificar la rotura de la ola aumentando la zona de
asomeramiento en bajamar. La movilidad de la orilla por sí misma también
cambia las zonas de batida, rompiente y asomeramiento (Short, 1999). Los
ambientes de marea fueron clasificados por Davies (1964) en tres tipos (Figura
1.4.): micromareales (TR < 2 m), mesomareales (2 < TR < 4 m) y
macromareales (TR > 4 m). El punto más alto alcanzado por el oleaje en
mareas vivas se toma tradicionalmente como el límite superior del intermareal
arenoso (“spring high tide”), de acuerdo con la definición de playa que estamos
utilizando (Figure 1.5.). Debido a la variación mareal, durante la bajamar las
playas muestran una zona amplia donde se produce drenaje de agua.
Capítulo 1 Introducción
52
Particularmente en el sistema de playas expuestas, la gran extensión vertical
que experimenta el sistema y el drenaje permite una subdivisión del intermareal
en capas o estratos.
Varios esquemas se han propuesto para explicar esto (Salvat, 1964;
McLachlan, 1980) y uno de los más utilizados se puede ver en la Figura 1.6.
Las capas se extienden desde una superficie de arena seca en la parte alta de la
playa hasta una zona permanentemente saturada bajo la capa freática y ligada al
swash. Las últimas capas tienen una menor circulación y tienden a estancarse,
mientras que en la zona de resurgencia el agua drena gravitacionalmente a
través del sedimento durante el flujo de la marea. En el límite superior de esta
zona aparece la capa freática. La zona de retención es el lugar óptimo para la
fauna intersticial ya que se ve alcanzada por el agua de todas las mareas
creándose un buen balance entre la disponibilidad de oxígeno, agua y alimento
así como cierta estabilidad física (McLachlan y Brown, 2006). También pierde
el agua gravitacional pero queda retenida el agua por capilaridad durante la
bajamar quedando el sedimento húmedo pero no saturado.
Pero una playa es mucho más que la zona litoral. El intermareal
arenoso es un ambiente que sirve de enlace entre el ecosistema marino y el
terrestre. De una forma general podemos incluir al menos dos sistemas
ecológicos: uno dunar, con fauna predominantemente terrestre y controlada
principalmente por el viento y una zona de oleaje con fauna marina controlada
por las olas y las mareas. Las posibles divisiones que nos podemos encontrar en
esta última zona se discutirán en profundidad en el Capítulo 3.
1.1.1.3. Morfodinamismo
La morfología de las playas se debe fundamentalmente a interacciones
entre los procesos de sedimentación, el oleaje y las corrientes marinas, en lo
que se dio por llamar morfodinámica de playas. Las primeras clasificaciones de
las playas fueron hechas atendiendo a los procesos hidrodinámicos que están
detrás de su forma deposicional (Short y Wright, 1984) obteniéndose dos tipos
de playas: disipativas y reflectivas. Esta primera impresión se vio ampliada con
Capítulo 1 Introducción
53
estudios posteriores, clasificando múltiples estados intermedios entre estos dos
extremos.
Dentro de este esquema general, nos encontramos con múltiples
variaciones generando un rango amplio de tipos de playas. Estas variaciones
serán debidas al tipo de sedimento, tamaño del grano, oleaje, morfología de la
orilla, rango mareal y exposición del intermareal. Muchos de estos factores son
a su vez interdependientes. El tamaño de grano, por ejemplo, depende de la
acción del oleaje, la cual a su vez depende del grado de exposición y del perfil
de la orilla. La mayor parte de las clasificaciones de las playas están basadas en
tres parámetros: el tamaño de grano del sedimento, el oleaje y el rango mareal.
La clasificación de playas más ampliamente aceptada (Figura 1.7.), usando
estos parámetros, fue introducida por Masselinck y Short (1993). En el eje
horizontal, el parámetro Dean (Ω = Hb / Ws * T) se encuentra en función de la
velocidad de sedimentación de las partículas (Ws), la altura media de la ola en
la rompiente (Hb) y el periodo de la ola (T) y divide las playas en tres tipos:
reflectivas (Ω < 1), intermedias (1 < Ω < 6) y disipativas (Ω > 6). El rango
mareal relativo (RTR = MSR/Hb) en el eje vertical se calcula a partir de la
media del rango mareal de mareas vivas y la altura media de la ola en la
rompiente y su importancia aumenta a medida que se incrementa la influencia
mareal en la playa (ver 1.1.1.2.).
Una playa reflectiva se caracteriza por pendientes pronunciadas y
sedimento grueso. Se asocia a un oleaje de baja energía donde la ola rompe
directamente encima del perfil de la playa, sin apenas zona de rompiente. La
zona de batida es estrecha y de gran velocidad. Por el contrario, la playa
disipativa tiene tendencia a un aplanamiento de la pendiente con arenas más
finas. Se amplia la zona de rompiente, lo que promueve la aparición de barras
de arena paralelas a la orilla, lo que provoca que las olas se rompan y formen
de nuevo varias veces. Las olas rompen lejos de la playa y la energía se disipa a
lo largo de la rompiente. Una playa intermedia será cualquier tipo de playa
que se encuentre entre estos dos tipos y su principal característica es la
variabilidad, además de ser el tipo de playa más frecuente (Fig. 1.7).
Capítulo 1 Introducción
54
Todos los intentos de clasificar las playas incluyen de alguna forma
información sobre el oleaje (Davies, 1964; Masselink y Short 1993). Aunque el
régimen del oleaje probablemente es el agente más importante en la formación
de playas, es difícil de medir en el campo y se puede cuestionar hasta qué punto
este régimen, en un momento dado, es representativo de las olas que han
conformado la playa. Además, tanto el parámetro Dean como el RTR han sido
criticados como medidas exclusivamente predictivas y no descriptivas (Short,
1999). Por lo tanto se han ido desarrollando parámetros de clasificación de las
playas que no requieran medidas del oleaje y/o que sean herramientas más
descriptivas. Un primer intento a partir de una serie de estudios comparativos
(McLachlan et al., 1993) creó el índice del estado de la playa (BSI, en sus
siglas en inglés), limitándose a combinar los efectos del parámetro Dean y del
RTR (ver Capítulos 2 y 3). Otros parámetros más recientes (ver McLachlan y
Dorvlo, 2005) son el índice de playa y el índice de depósito de playa (BI y
BDI). Ambos usan la pendiente del intermareal y la información del sedimento,
dos parámetros que pueden ser medidos fácilmente en la playa. El primer
índice también incluye el rango mareal, lo que facilita la comparación entre
playas a una escala espacial mayor (ver Capítulo 4). Mientras que el BDI se
presta más a estudios de una escala espacial menor, con ninguna o menor
diferencia en el rango mareal entre las playas estudiadas.
Además de por la morfodinámica, las playas se pueden clasificar
también en función de su grado de exposición. Aunque se basa en variables
indirectas, con parámetros difíciles de medir o con gran variabilidad espacio
temporal, unifica una serie de conceptos ecológicamente relevantes. Una
clasificación de fácil comprensión fue propuesta por McLachlan, (1980)
estableciendo cuatro categorías, desde muy expuesta a muy protegida, definidas
en base al oleaje y características biológicas y morfodinámicas (Tabla 1.1.).
Una playa es un sistema altamente dinámico en donde los cambios
espaciales y temporales de las características físicas y morfológicas son
habituales. Factores físicos como la textura del sedimento y las condiciones del
swash han sido reconocidos desde hace mucho tiempo como definitorios de la
Capítulo 1 Introducción
55
respuesta de la macrofauna bentónica de los intermareales arenosos (e.g.
McArdle y McLachlan, 1992; McLachlan, 1996; Defeo y McLachlan, 2005).
La textura del sedimento determinará, entre otras cosas, la porosidad
del sustrato (i.e. el volumen del espacio entre los granos de arena), la
permeabilidad (i.e. la tasa de percolación del agua a través de la arena) y la
penetrabilidad (i.e. la fuerza necesaria para penetrar en la arena); así como la
velocidad de filtración del agua en el sedimento y el contenido en agua de la
propia playa. En general, las arenas más gruesas filtran mucha más agua pero
retienen mucha menos. Esto da como resultado una mayor permeabilidad pero
menor porosidad de la arena y por tanto, el nivel de saturación en agua en
playas de grano más grueso es mucho menor. Por tanto, la superficie del nivel
freático (i.e. nivel por debajo del cual el sedimento está saturado en agua) se
encuentra más baja en este tipo de playa. Esta superficie del nivel freático, o la
transición entre superficie de arena saturada e insaturada, se denomina línea
efluente (EL) y se reconoce visualmente en las playas como un lámina de
espejo (Fig. 1.3.).
El swash es el agente que transfiere energía del oleaje y agua a la playa.
Como tal, las características del swash son cruciales en la formación de playas.
El periodo, la velocidad y el intervalo del swash son, en teoría, menos
favorables para la macrofauna en las duras condiciones de las playas
reflectivas, con cortos periodos e intervalos y mayor velocidad de swash
especialmente a nivel de la bajamar (McArdle y McLachlan, 1992; Short,
1999). El swash además es directamente dependiente de las condiciones del
oleaje así como de la morfología y pendiente de la playa.
1.1.2. Comunidades de la macrofauna bentónica
1.1.2.1. ¿Qué es la macrofauna?
Las definiciones de macrofauna o macrobentos varían de acuerdo con
los diferentes autores. Así por ejemplo, Mees y Jones (1997) definen el
macrobentos como toda fauna marina dependiente del sedimento y que se ve
Capítulo 1 Introducción
56
retenida por un tamiz de luz de malla de 1 mm. Una mayor subdivisión de este
término englobaría a otros tres grupos: el endobentos (i.e. animales que viven
en el sedimento), epibentos (i.e. animales que viven sobre el sedimento) e
hiperbentos (i.e. animales que viven en la columna de agua por encima del
fondo marino). Estas categorías no tienen límites bien definidos ya que algunas
especies, por ejemplo, son parcialmente endobentónicas e hiperbentónicas. En
general, las divisiones se basan en el material de muestreo empleado. Además
otros autores extienden el término de macrofauna a todos aquellos animales
retenidos en un tamiz de luz de malla de 0.5 mm (e.g. Brazeiro y Defeo, 1996;
Defeo y Martínez, 2003). En este estudio usaremos el término macrofauna para
aquellos animales que viven enterrados en el sedimento y han sido muestreados
por medio de un corer cilíndrico de extracción y una bolsa de malla de 1 mm
(Figura 1.8.).
Durante mucho tiempo las playas han sido consideradas desiertos
marinos y olvidadas como importante fuente de estudio a favor del visualmente
más exuberante litoral rocoso. La naturaleza de cambio constante típica de las
playas ha sido considerada como la fuerza estructurante principal de las
comunidades macrofaunísticas (McLachlan, 1983). Pero a pesar de su
apariencia uniforme y su, a primera vista, pobreza faunística, las playas pueden
estar habitadas por una gran diversidad faunística y de riqueza de especies.
1.1.2.2. Macrofauna en las playas
La macrofauna dominante de las playas, tal y como la hemos definido
anteriormente, consiste principalmente en animales pertenecientes a tres
taxones: Crustacea, Annelida (principalmente poliquetos) y Mollusca. La
composición y distribución de esta macrofauna está supeditada y adaptada a un
ambiente tan dinámico como es el del intermareal arenoso. Así; las diferencias
faunísticas que nos encontramos a macroescala (entre las distintas geografías y
latitudes costeras), mesoescala (zonación dentro de una misma playa debida al
hidrodinamismo de la misma) o incluso a nivel de microescala (interacciones
Capítulo 1 Introducción
57
tales como la depredación y competencia) han dado lugar a un ecosistema1 con
una gran riqueza específica, abundancia y biomasa (McLachlan y Brown,
2006). Aunque también se han realizado estudios que comprenden la
meiofauna y la microfauna, la macrofauna es uno de los componentes más
notables de la fauna presente en las playas y el más fácil de recolectar e
identificar. Las características más destacables son su gran movilidad y
habilidad para enterrarse rápidamente en el sedimento. Se ha sugerido que los
crustáceos dominan en general las playas más expuestas y los poliquetos las
más protegidas mientras que los moluscos serían los más abundantes en
situaciones intermedias (Dexter, 1983) aunque esta distribución teórica varía en
muchas ocasiones (ver capítulos 3 y 4).
1.1.2.3. Patrones de distribución de la macrofauna
Dentro de una misma región geográfica, el patrón general de la
macrofauna de playas muestra un descenso en la riqueza específica, la
abundancia y la biomasa a lo largo de un gradiente morfodinámico (Figura
1.9.), desde un estado disipativo más suave a uno reflectivo más duro. Este
patrón, que aparece en cualquier latitud del planeta, se ha convertido ya en un
paradigma en la ecología de playas (e.g. Defeo y McLachlan 2005; McLachlan
y Brown, 2006). Las playas pueden ser descritas mediante un conjunto de
parámetros físicos, la mayor parte de los cuales son factores estructurantes de la
composición faunística. De hecho se consideran ambientes controlados
físicamente, donde el papel de los factores biológicos a la hora de estructurar
las comunidades2 a veces es dudoso (McLachlan y Jaramillo, 1995).
1 Por ecosistema en este texto, se hace referencia a un sistema formado por individuos
de muchas especies, en el seno de un ambiente definido, e implicados en un proceso de
interacción, expresable bien como intercambio de materia y energía, bien como una
secuencia de nacimientos y muertes, y uno de cuyos resultados es la evolución a nivel
de las especies y la sucesión a nivel de sistema entero (Margalef, 1995).
2 En ecología se estudian las distribuciones, abundancias y las interacciones entre los
organismos en una variedad de escalas espaciales de organización. El problema surge a
la hora de considerar a todo el conjunto de especies que encontramos en el mismo
lugar. La comunidad es supuestamente la unidad real de estudio de muchos ecólogos y
tiene al menos dos puntos de vista diferentes a la hora de determinar este concepto. Un
punto de vista considera a las especies como integrantes de comunidades que tienen
Capítulo 1 Introducción
58
La riqueza específica, por ejemplo, aumenta a medida que disminuye el tamaño
de grano y la pendiente de la playa, a medida que aumenta el rango mareal y la
anchura del intermareal y/o a medida que disminuye la dureza del swash (e.g.
Jaramillo y McLachlan, 1993; Brazeiro, 1999; McLachlan y Dorvlo, 2005).
La principal hipótesis propuesta para explicar la relación entre la
macrofauna y la morfodinámica de las playas se conoce como la “Hipótesis de
Exclusión del Swash” (SEH en sus siglas en inglés). En esta hipótesis se
sugiere que las condiciones de dureza del swash, junto con un perfil de
pendiente pronunciada determinan un descenso progresivo en la diversidad y
abundancia de la macrofauna. Esto puede llevar, en situaciones extremas, a la
completa exclusión de especies intermareales en dicha zona (McLachlan et al.,
1995). Esta teoría sugiere que la capacidad de las especies para enterrarse
podría ser un factor determinante en la distribución de las especies y en la
estructura de la comunidad en playas con distinta pendiente (Dugan et al.,
2004). Las especies con mayor capacidad de enterramiento serían por tanto
capaces de habitar con éxito playas de pronunciada pendiente y swash muy
activo. Como contraste, en playas con una pendiente más suave podremos
encontrarnos con organismos con un rango más amplio de comportamientos y
adaptaciones morfológicas. Además hay que tener en cuenta la existencia de
especies semiterrestres que viven en la parte superior de los intermareales
una serie de características que han persistido en el tiempo (e.g. la composición de
especies) y que se repite en distintos lugares. Por tanto desde este punto de vista la
comunidad de especies está organizada, estructurada e integrada. Las especies son
interdependientes e interactivas y a veces se presume que las interacciones son, al
menos en parte, responsables en el mantenimiento de la entidad. El punto de vista
alternativo presupone que el término comunidad se usa para describir el conjunto de
organismos que se encuentran en el mismo lugar en el mismo momento. Pueden o no
ser interdependientes, pueden o no interactuar. Existe coexistencia debido a que tienen
las mismas respuestas fisiológicas al ambiente y/o las mismas necesidades alimenticias
o de protección o alternativamente porque algunas especies son necesarias como
presas. La realidad posiblemente, como en la mayor parte de las ocasiones, se
encuentre en algún punto en el medio de estas dos consideraciones. Para evitar
confusiones, las dos aproximaciones ecológicas van a ser referidas aquí usando el
término “comunidad” para el fuertemente relacionado y consistente conjunto de
especies y el término “asociación” para la relación más holgada de especies
concurrentes, donde el conjunto total de especies no es un grupo repetible o
identificable de forma coherente (Underwood, 2006).
Capítulo 1 Introducción
59
arenosos con independencia de los efectos del swash y que no van a mostrar
ninguna de estas tendencias (Defeo y McLachlan, 2005). En términos de
población faunística esto se ha traducido en la llamada “Hipótesis de la Dureza
del Hábitat” (HHH; Defeo et al., 2001) que predice que en playas reflectivas la
dureza del ambiente obliga a la macrofauna a emplear una gran parte de su
energía en sobrevivir, dejando menos cantidad disponible para la reproducción
y provocando además una mayor mortalidad. Brazeiro (2001) incluye además
del swash, las dinámicas de acreación-erosión de las playas como posible
influencia en la estructura de la macrofauna. Todas estas ideas han sido
sintetizadas en la “Hipótesis del Control Físico a Macroescala” (McLachlan y
Dorvlo, 2005) donde dos niveles de factores controlarán los patrones
principales de distribución faunística a nivel de macroescala. El primer nivel
posee dos factores principales; el rango mareal y la latitud, que determinarán el
número de especies que pueden ocurrir en condiciones ideales en una región
determinada. El segundo nivel mediado por el swash, el tamaño del sedimento
y la estabilidad de la playa que actuarán como factores excluyentes de aquellas
especies menos adaptadas a las condiciones duras del estado reflectivo.
1.1.2.4. Zonación de la macrofauna en la playa
La zonación faunística en intermareales es una característica bien
descrita y estudiada en ecología de playas. La zonación en playas no es, ni de
cerca, tan visible como en el litoral rocoso, probablemente como consecuencia
del ambiente tan dinámico de la playa y las poblaciones tan cambiantes que la
ocupan. Al igual que a nivel de macroescala, la variabilidad en los factores
físicos se considera la primera fuerza que controla las comunidades
macroinfaunales y sus asociaciones en las playas (McLachlan, 1983). La
macrofauna se distribuye a lo largo y ancho del intermareal. De hecho se han
encontrado fuertes relaciones entre la riqueza de especies y la longitud de la
playa (Brazeiro, 1999). En general las poblaciones macrofaunísticas están más
desarrolladas en la zona media de la playa presentando una distribución
unimodal en forma de campana hacia los lados. Otros factores, como la
presencia de zonas rocosas, el impacto antropogénico, aportes de estuarios o la
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60
forma de la propia playa van a afectar la distribución longitudinal de la
macrofauna en playas (McLachlan y Brown, 2006). En el caso de la
distribución horizontal a través del perfil de la playa, la macrofauna muestra
unos patrones generales o zonación; es decir, nos encontramos con la suma de
las respuestas de cada especie al gradiente intermareal. El patrón tradicional de
distribución horizontal muestra un aumento en el número de especies a medida
que nos dirigimos a la línea de agua (McLachlan y Jaramillo, 1995; McLachlan
y Brown, 2006).
Se han hecho varios intentos para establecer esquemas de zonación de
la macrofauna de playas (ver McLachlan y Jaramillo, 1995). Dos de ellos han
sido los más utilizados tradicionalmente: el esquema de Dahl (Dahl, 1952) que
divide la playa en tres zonas distintas basándose en la distribución de
crustáceos y las cuatro zonas físicamente delimitadas del esquema de Salvat
(Salvat, 1964) basado en el contenido en agua del sedimento a través del
intermareal (Figura 1.10. y Fig. 1.6.). La correspondencia entre ambos
esquemas es bastante buena y el resto de las zonaciones propuestas por
diversos autores generalmente pueden considerarse variaciones de estos dos
esquemas. Un esquema que quizás sea el más elemental, pero también el que se
puede aplicar más ampliamente, fue propuesto por Brown (en McLachlan,
1983 y citado en McLachlan y Brown, 2006) sugiriendo que sólo se podían
reconocer claramente dos zonas en los intermareales arenosos (ver capítulo 3).
Una zona habitada por animales de vida aérea (básicamente crustáceos) por
encima del punto más alto de sedimento depositado por las olas (drift line) y
otra habitada por verdaderas especies marinas en contacto directo con el agua.
La conclusión general, y una de las ideas más comúnmente citada, es que no
existe una zonación clara en las playas (McLachlan y Brown, 2006).
Varios estudios en diversas regiones del planeta sugieren que los
distintos tipos de playas y los diferentes factores físicos podrían causar
variaciones en la zonación de la macrofauna (e.g. Trevallion et al., 1970; Bally,
1983; Jaramillo et al., 1993; McLachlan y Jaramillo, 1995). Por un lado, las
playas disipativas e intermedias poseen una mayor riqueza en las zonas
inferiores del intermareal mostrando una división en tres e incluso cuatro zonas
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61
diferentes de distribución de especies. En el otro lado las playas reflectivas
muestran un empobrecimiento de la fauna intermareal sobre todo a causa del
mayor hidrodinamismo en la zona inferior de la playa. En este último caso se
dibuja una única zona de especies en el supralitoral o como mucho dos franjas
diferentes de especies cuando las condiciones no son tan duras (Figura 1.11.).
En general se puede considerar que las zonas son más fáciles de delimitar en
las partes altas de la orilla mientras que el esquema se desdibuja a medida que
nos dirigimos hacia la zona de batida (McLachlan y Jarmillo, 1995) donde la
aplicabilidad del esquema de Dahl desaparece en las zonas inferiores de las
playas reflectivas extremas (Fig. 1.9.). Una dificultad añadida para establecer
un esquema zonal se debe a la capacidad locomotora y a las adaptaciones
migratorias de la mayor parte de las criaturas que habitan el intermareal.
Podemos decir que la zonación en playas es un fenómeno
extremadamente variable tanto a corto como a largo plazo (Brazeiro y Defeo,
1996). Además, las zonas no están definidas por límites precisos, mostrando un
solapamiento zonal considerable entre las distintas especies lo que hace este
trabajo mucho más dificultoso y a menudo con poca validez estadística
(Brazeiro, 1999). Todo esto muestra un patrón espacial discreto de la
macrofauna de playas en forma de parches o manchas que se relacionan entre sí
y que muestran una cierta dinámica o cambio tanto en el espacio como en el
tiempo.
Los factores biológicos son una clave importante en el establecimiento
y mantenimiento de la zonación en el litoral rocoso, con reclutamiento,
depredación y competición jugando un papel central (Underwood y Denley,
1984). En intermareales arenosos, sin embargo, los factores que controlan la
comunidad son diferentes (Peterson, 1991). La competencia por el espacio, por
ejemplo es de improbable importancia debido a la movilidad de la fauna y a
cierta distribución vertical de la fauna en el sedimento (ver Capítulo 5). A
causa de esta movilidad, el reclutamiento de las larvas es menos crítico a la
hora de establecer las zonas que en un litoral rocoso aunque sí puede jugar un
papel inicial importante en el establecimiento de las poblaciones en la playa
(Brown, 1983). Los factores biológicos más importantes en la zonación de la
Capítulo 1 Introducción
62
macrofauna en playas se centran más en la depredación y la competencia por el
alimento.
1.1.2.5. Hábitos alimenticios y estrategias de supervivencia de la
macrofauna de playas
Las playas son ambientes hostiles muy controlados físicamente, donde
las condiciones pueden variar considerablemente en periodos cortos de tiempo.
Por tanto, la fauna que habita los intermareales arenosos debe estar muy
adaptada a este ambiente tan dinámico. El aporte alimenticio en los
intermareales se puede definir como errático e impredecible y está fuertemente
unido al variado aporte externo proveniente de la columna de agua; ya sea en
forma de restos orgánicos particulados o de materia orgánica disuelta lista para
ser absorbida o filtrada. Los principales aportes alimenticios disponibles,
aunque limitados, para la macrofauna bentónica se presentan en la Tabla 1.2.
Los intermareales más protegidos y la llanura intermareales pueden alcanzar
valores de producción primaria medibles aunque no muy elevados (McLachlan
y Brown, 2006). Diferentes características morfológicas y adaptativas han
surgido para hacer frente a las condiciones dinámicas y variables de las playas.
Los grupos tróficos presentes en los intermareales incluye carnívoros,
carroñeros, filtradores/suspensívoros y depositívoros (estos últimos son más
importantes en playas protegidas). La mayor parte del alimento que se consume
en una playa es de origen exógeno a través del swash (Romer y McLachlan,
1986) o de las algas varadas (Dugan et al., 2003) haciendo que la depredación
directa entre las especies sea menos importante. La ausencia de macrófitas
asociadas al sedimento intermareal promueve la predominancia de organismos
filtradores y carroñeros entre la macrofauna de invertebrados residente en el
intermareal.
El número de especies carnívoras en las playas está bastante limitado y
una parte importante de este grupo se alimenta de la meiofauna (McLachlan,
1990). Los carroñeros, sin embargo son muy comunes en las playas y pueden
actuar como carnívoros en tiempos de escasez, ya que esta fuente de alimento
tiende a ocurrir de forma variable. Se encuentran desde la franja dunar hasta la
Capítulo 1 Introducción
63
zona sublitoral. Estas especies son oportunistas y han adquirido varias
adaptaciones morfológicas y comportamentales para localizar y consumir
restos de forma eficiente. Otro tipo de hábito trófico muy abundante en las
playas es el de los organismos suspensívoros que filtran de forma general el
agua del swash o intersticial (McLachlan y Brown, 2006). En un ambiente tan
turbulento como una playa expuesta, la comida en suspensión está siempre
disponible aunque puede variar en cantidad y tipo. Los filtradores normalmente
dominan la comunidad del intermareal arenoso y consisten fundamentalmente
en moluscos bivalvos y algún crustáceo. En condiciones óptimas en playas
expuestas, por ejemplo en situación disipativa con gran cantidad de diatomeas
acumulándose en la zona de rompiente, los suspensívoros pueden mantener
grandes poblaciones y aportar gran biomasa al ecosistema.
En muchas situaciones, y sobre todo en playas reflectivas e
intermedias, los carroñeros/depredadores móviles dominan la macrofauna.
Donde la fauna es pobre, como en las playas de mucha pendiente y sedimento
grueso (Fig. 1.11.), la fauna del supralitoral tal como los talítridos anfípodos
son muy importantes como consecuencia de la ausencia de verdaderas formas
intermareales. Los depositívoros son más importantes en playas protegidas y en
la zona sublitoral. En estas zonas protegidas el sedimento es lo suficientemente
estable para permitir la construcción de galerías semipermanentes. Un análisis
amplio hecho por Riccardi y Bourget (1999) demuestra el aumento de
depositívoros con las condiciones protegidas, sedimento más fino y pendientes
más suaves con un consecuente aumento de los carnívoros.
La macrofauna que habita en las playas expuestas depende
exclusivamente de los aportes fitoplanctónicos exógenos y de algas macrófitas
de arribazón a causa de la escasez de producción primaria en ese hábitat (Inglis,
1989; McLachlan y Brown, 2006). La zona marina es la más importante fuente
de alimento, aportando partículas para los filtradores y restos orgánicos de
distintos orígenes (detritus de origen animal y plantas o algas) para los
carroñeros. Las características de las poblaciones que nos encontramos en un
intermareal están fuertemente relacionadas con la riqueza en el agua costera,
particularmente en términos del material particulado (ver Capítulos 4, 5 y 6).
Capítulo 1 Introducción
64
La mayor presión depredadora también es de origen externo; aves y/o insectos
desde la zona terrestre y peces o grandes crustáceos desde el mar.
Otras estrategias de supervivencia son la movilidad, la migración, el
enterramiento y la orientación. La naturaleza extremadamente dinámica del
ambiente de playa en términos de disponibilidad y localización de alimento
reflejan las ventajas que supone la existencia de una fauna de gran movilidad,
sobre todo para optimizar el tiempo de alimentación y reproducción, así como
para poder escapar de un depredador. Normalmente las técnicas de escape se
centran sobre todo en la capacidad de enterramiento durante la bajamar, aunque
algunas formas son capaces de nadar o reptar (McLachlan y Brown, 2006). La
actividad locomotora y migratoria se originan de la combinación de los tres
factores ambientales principales: la inestabilidad del sustrato, la acción del
oleaje y la marea. Existe un número variable de mecanismos de enterramiento
en el caso de la macrofauna dependiendo del grupo que estemos tratando, ya
sea un organismo de cuerpo blando como un poliqueto o un molusco o un
organismo con un rígido exoesqueleto como los crustáceos. Estos mecanismos,
al igual que la reproducción no son el objetivo de estudio de esta tesis así que
no se procederá a una discusión sobre el tema.
1.1.3. Fuentes de alimento en las playas
1.1.3.1. Disponibilidad del alimento
Se ha demostrado que la disponibilidad de alimento es uno de los
principales factores que afectan a la estructura y metabolismo de la comunidad
bentónica marina (e.g. Pearson y Rosenberg, 1987; Graf, 1989; Dugan et al.,
2003) y que las diversidad de especies en los intermareales de fondos blandos
está fuertemente relacionada con dicha disponibilidad (Withlaton, 1981).
Además, la fuente de alimento puede ser uno de las explicaciones para la
distribución y asociación de las distintas poblaciones (Decho y Fleeger, 1988) y
para la distribución de la comunidad bentónica, su variabilidad temporal y el
metabolismo (Montagna, et al., 1983; Rudnick et al., 1985). La disponibilidad
del alimento está fuertemente relacionada con la composición de la materia
Capítulo 1 Introducción
65
orgánica (Danovaro et al., 1993) por lo que determinar la composición de dicha
materia es crucial a la hora de valorar la calidad y cantidad de alimento en los
estudios de ecología bentónica (ver Capítulos 4 y 5).
La composición bioquímica de la materia orgánica no es más que el
resultado de un equilibrio dinámico entre los aportes exógenos, la producción
autóctona y el uso heterotrófico (Fabiano y Danovaro, 1994). La materia
orgánica en los sedimentos marinos está compuesta de una fracción lábil y otra
más refractaria (Fabiano y Danovaro, 1994). Los azúcares simples, ácidos
grasos y proteínas son rápidamente mineralizados y por tanto han sido usados
para valorar la porción lábil de la materia orgánica (Fichez, 1991; Danovaro et
al., 1993). Estos componentes más lábiles han sido usados tradicionalmente
para estimar el valor nutricional del sedimento (Buchanan y Longbottom,
1970). La composición bioquímica de la materia orgánica sedimentaria ha sido
ampliamente investigada en diversos ecosistemas marinos, como los fondos
marinos (Danovaro et al., 1993), sistemas semicerrados (Pusccedu et al., 1999),
fondos submareales (Fabiano et al., 1995), praderas de fanerógamas (Danovaro
et al., 1994) y sistemas estuáricos (Fabiano y Danovaro, 1994). Sin embargo, y
a pesar de la importancia de la composición bioquímica de la materia orgánica
sedimentaria (i.e. carbohidratos, lípidos y proteínas) hay muy poca información
sobre las concentraciones y variabilidad de estos compuestos en intermareales
arenosos (Incera et al., 2003a).
1.1.3.2. El papel de la composición bioquímica y de las condiciones
hidrodinámicas.
Se considera, de una forma general, que tanto los valores de la
abundancia como los de la biomasa de la macrofauna bentónica difieren
significativamente entre un intermareal expuesto y otro protegido. Así, los
intermareales más protegidas tienen una fauna muy abundante y diversa siendo
importantes como zona de cría de diversas especies de peces e invertebrados
(Adam 1990). Por el contrario, y como ya se explicó anteriormente, a medida
que aumenta el grado de exposición en un intermareal, la riqueza biológica
disminuye (Fig. 1.9.). Esto ha sido sugerido como una consecuencia de las
Capítulo 1 Introducción
66
distintas características físicas e hidrodinámicas de estos dos ambientes tan
opuestos (McLaclhlan, 1983) e implica que el mayor estrés hidrodinámico de
las localidades expuestas es el factor limitante de la riqueza biológica
(McLachlan et al., 1996). Junto a la ya comentada “Hipótesis de Exclusión del
Swash”, surgen otras hipótesis que pueden explicar la relación entre la
macrofauna y las características de las playas sin ser necesariamente
excluyentes entre sí. La gran cantidad de materia orgánica en los intermareales
protegidos puede llegar a inducir una repuesta significativa en la macrofauna
bentónica que podría explicar, de forma parcial, la abundancia y diversidad
faunística de estos ambientes comparados con los intermareales expuestos
(Incera et al., 2003a, b).
La morfodinámica y el perfil de la playa condicionarán de alguna
manera la distribución y los patrones faunísticos de la misma; no sólo por la
actividad hidrodinámica, sino también por los distintos aportes nutritivos
presentes a lo largo del perfil del intermareal. Mientras que la parte inferior de
las playas más expuestas sufre una disminución de la riqueza específica, la
macrofauna encuentra un ambiente mucho más estable en la zona supralitoral
de las mismas (Defeo y Gómez, 2005). Esta zona alejada del swash está
habitada generalmente por insectos o crustáceos bien adaptados a la desecación
(McLachlan, 1990; Little, 2000) y considerados organismos dependientes de
aportes orgánicos alóctonos tan específicos como las algas de arribazón (ver
Capítulo 6) asociadas a distintos procesos oceanográficos (Colombini y
Chelazzi, 2003, Dugan et al., 2003). Las playas más protegidas tienen unas
condiciones ambientales más favorables y una mayor estabilidad sedimentaria
(ver Capítulos 4 y 5) lo cual favorece un rango mucho más amplio de
comportamientos y de adaptaciones morfológicas y tróficas.
Muchas playas expuestas de todas las latitudes reciben grandes
cantidades de algas provenientes del submareal e intermareales rocosos
próximos (Inglis, 1989; Rossi y Underwood, 2002; Dugan et al., 2003). La
importancia de estas acumulaciones, sobre todo en playas expuestas, ha sido
documentado en la literatura previamente (ver Colombini y Chelazzi, 2003).
Estos depósitos representan la fuente principal de alimentación para
Capítulo 1 Introducción
67
organismos detritívoros como anfípodos talítridos, isópodos y coleópteros
(Colombini y Chelazzi, 2003; Dugan et al., 2003; Olabarria et al., 2007). Estas
acumulaciones de algas también actúan como refugio para la fauna del
supralitoral, principalmente artrópodos terrestres y semiterrestres, aportando
una oportunidad para estudiar este material tanto como una fuente de alimento
como de protección. (Inglis, 1989; Colombini y Chelazzi, 2003). El origen y la
composición bioquímica de la materia orgánica han sido propuestos como
factores claves, junto con el medio ambiente físico, para el control de la
comunidad bentónica de playas (Incera et al., 2003b).
1.1.4. Objetivos y líneas de investigación de la tesis.
Los intermareales son ecosistemas que están bajo una incesante presión
antropogénica debida fundamentalmente a la urbanización del litoral, con
aproximadamente un 50% de la población mundial viviendo junto a la costa
(GESAMP, 1990). A causa de la arrolladora tasa de desarrollo que se ha
producido en los últimos años en la línea costera y de la vulnerabilidad de este
frágil ecosistema, la demanda para una intervención sostenible en el litoral
centrada en su uso, control y preservación es acuciante. Además, el ecosistema
de playas es un punto de unión altamente productivo situado entre la tierra y el
mar en severo riesgo de una futura modificación dramática como consecuencia
del aumento del nivel del mar, en ciertas regiones, debido al calentamiento
global (Brown y McLachlan, 2002; Peterson y Bishop, 2005).
Al interés recreativo y lúdico típico de las zonas costeras hay que
añadir la relevante importancia industrial y pesquera del litoral en el norte de
España. La costa gallega es bien conocida como lugar de producción de
especies marinas de gran interés económico. La recolección manual de almejas
y berberechos del intermareal es una actividad muy común en esta área tan
productiva. Esta y otras actividades económicas tienen un efecto relevante en la
estructura y organización de las comunidades bentónicas de los intermareales.
Parte II. La ecología de las playas arenosas.
Al comienzo de este estudio, ningún trabajo cuantitativo sobre la
macrofauna de playas en España había sido publicado; además, se puede decir
Capítulo 1 Introducción
68
que muy pocos estudios se habían llevado a cabo sobre la ecología de playas en
regiones de latitudes templadas, sobre todo en Europa. Por tanto, un estudio
inicial sobre la ecología de la macrofauna de intermareales de la costa norte de
la Península Ibérica es requisito esencial para iniciar este trabajo y en esta tarea
se ha centrado esta primera parte de la tesis.
El Capítulo 2 se centra en el efecto que tienen varios factores
ambientales sobre la macrofauna bentónica que reside en el tipo de playa
expuesta más característica del litoral a escala mundial. Se sometió a estudio el
efecto de diversas variables abióticas en un gradiente de diez playas
intermedias a lo largo de la costa norte de la Península Ibérica. Varias
características bióticas fueron utilizadas, destacando la riqueza de especies, la
abundancia y la biomasa de la macrofauna. Este estudio pionero de la ecología
de la macrofauna de playas del norte de España se completa con un análisis
más amplio y profundo sobre la estructura de la comunidad y la zonación
intermareal de la macroinfauna de la misma región. El Capítulo de 3 de esta
tesis es un complemento del capítulo anterior, centrado en la dinámica de las
comunidades macrofaunísticas de playas de tipo intermedio. Los resultados se
comparan con los distintos esquemas tradicionales de zonación que han sido
propuestos para la macroinfauna de playas y se sugiere una distribución
característica de la macrofauna basada en el peculiar perfil de las playas de esta
región. Distintos parámetros morfodinámicos y variables biológicas fueron
analizadas y discutidas. Los resultados de estos dos capítulos fueron publicados
en la revista Estuarine, Coastal and Shelf Science.
Parte III. La importancia del grado de exposición en la estructura de la
comunidad: condiciones hidrodinámicas y disponibilidad de alimento.
El capítulo 4 de esta sección ahonda en las características de la
estructura de la comunidad de macrofauna de las playas pero poniendo énfasis
en el efecto del gradiente de exposición al oleaje y en la disponibilidad de
alimento. Los efectos de los parámetros físicos y la disponibilidad de alimento
son analizados comparativamente entre playas protegidas y expuestas. Se
consideran ambos efectos como factores principales que pueden afectar a la
estructura y metabolismo de la comunidad bentónica marina. Además de
Capítulo 1 Introducción
69
comprobar y reafirmar los patrones de zonación y cómo afecta la exposición a
la distribución faunística, se pone de relieve el paradigma del control físico en
las playas expuestas. También se analiza el posible patrón que regula
principalmente el aumento de los parámetros bióticos en los intermareales
protegidos, donde las interacciones biológicas se convierten en un factor
importante en la estructura macrofaunística. Los resultados y conclusiones
obtenidas en este capítulo han sido publicados en la revista Hydrobiologia.
Parte IV. El papel de la disponibilidad de alimento en las playas:
patrones espaciales y temporales.
Dada la importancia de los aportes alimenticios externos en la
estructura de la comunidad macrofaunística, en esta parte del estudio se
analizan dos tipos de playas definidos por su grado de exposición, protegida y
expuesta, y como afecta la disponibilidad del alimento en cada una de las dos
situaciones. En ambos casos, los aportes alimenticios son externos, pero
mientras que en el intermareal expuesto se estudia el aporte exógeno más
característico, las algas macrófitas de arribazón, en el intermareal protegido se
pone más énfasis en la composición bioquímica del sedimento y su influencia
en la estructura de la comunidad. En el capítulo 5 se realiza un estudio sobre la
variabilidad estacional y la distribución vertical de la materia orgánica
sedimentaria de una playa estuárica protegida y su relación con la macrofauna.
Este capítulo ha sido aceptado para su publicación en la revista científica
Estuaries and coasts.
En el capítulo 6 el estudio se centra en la influencia de los aportes de
macroalgas sobre las comunidades macrofaunísticas y en sus distintos tipos de
asociación. No sólo se presenta la abundancia de las especies colonizadoras,
sino también los procesos de sucesión (i.e. secuencia de colonización y
reemplazamiento de especies) y su variación en el tiempo. Un factor novedoso
de este estudio consiste en valorar el efecto de un alga invasiva sobre la
macrofauna de una playa como aporte exógeno y compararlo con el efecto de
un alga nativa. Este capítulo ha sido aceptado para su publicación en la revista
Journal of Experimental Marine Biology and Ecology.
Capítulo 1 Introducción
70
Parte V. Discusión general.
En la discusión general del capítulo 7, todos los resultados de los
capítulos anteriores se han integrado y discutido. Algunos conceptos generales
sobre la ecología de las playas son confirmados mientras que otros se ponen en
cuestión y nuevas ideas y posibles nuevos objetivos de investigación se han
propuesto basados en los resultados y observaciones obtenidos.
PART II. THE ECOLOGY OF SANDY BEACHES
“And the more we learn of the nature of things, the more evident is it that what
we call rest is only unperceived activity; that seeming peace is silent but
strenuous battle. In every part, at every moment, the state of the cosmos is the
expression of a transitory adjustment of contending forces; a scene of strife, in
which all the combatants fall in turn. What is true of each part is true of the
whole.”
-Thomas Henry Huxley,
Evolution and Ethics
Content:
Rodil, I.F. and Lastra, M. 2004 Environmental factors affecting benthic
macrofauna along a gradient of intermediate sandy beaches in northern
Spain. Estuarine Coastal and Shelf Science 61: 37-44.
Rodil, I.F., Lastra, M. and Sánchez-Mata, A.G. 2006 Community
structure and intertidal zonation of the macroinfauna in intermediate
sandy beaches in temperate latitudes: North coast of Spain. Estuarine
Coastal and Shelf Science 67: 267-279.
Chapter 2. Environmental factors affecting benthic
macrofauna along a gradient of intermediate sandy
beaches in northern Spain
Rodil, I.F., and Lastra, M.
Published in Estuarine, Coastal and Shelf Science (2004). 61:37-44.
Chapter 2 Environmental factors
73
Abstract
Ten sandy beaches along the north coast of Spain were studied during
September 1999 to analyse the number of species, abundance and biomass of
macroinfauna along a gradient of intermediate beach types and exposure range.
Faunal samples were collected with metallic cylinders (25 cm diameter,15 cm
depth) at 10 equally spaced shore levels along six replicated transects separated
randomly and extending from above the drift line to the low tide swash zone.
Exposure rate, Dean’s parameter (Ω), beach state index (BSI) and relative tidal
range (RTR) were estimated at each beach. Length and width of the beach,
intertidal slope, sorting and median grain size and also swash amplitude and
wave characteristics were measured. Number of species was between 10 and
29. Macrofaunal abundances ranged between 4962 and 71228 ind. m-1 and
between 31 and 329 ind. m-2, while biomass (ash free dry weight) per square
meter of beach ranged between 0.027 and 0.278 g m-2 and between 3 and 61 g.
m -1. Results show some significant trends: number of species is the biotic
variable more affected by physic and morphodynamic factors, increasing
linearly with relative tidal range and decreasing with increasing average grain
size; the same trend was observed from exposed to very exposed beaches; the
biomass decreased exponentially with increasing average grain size. These
trends agree with previous studies in different coasts in the world where coarse
sands limit the benthic macrofauna. The morphodynamic parameters such as
Dean’s parameter and Beach State Index did not show a predictive value. The
results suggest that different characteristics of benthic macrofauna communities
in intermediate beaches can be affected in different ways by the physical
processes involved in beach morphodynamics.
Keywords: sandy beaches; benthic macrofauna; morphodynamic state;
exposure rate; swash; northern Spain.
2.2.1. Introduction
Beaches are present in all coasts, latitudes and climates worldwide,
having a wide spectrum of sizes, morphologies, exposure range and
oceanographic conditions, together with a high diversity in biotic
Chapter 2 Environmental factors
74
characteristics. The most dynamic of soft bottom habitats (McLachlan, et al.,
1996), exposed sandy beaches occur on the open coasts of tropical and
temperate regions (Davies, 1972). Exposed sandy beaches can be described in
terms of the interaction between wave exposure, tide ranges and sediment
characteristics, also called beach morphodynamics. This ecosystem harbours a
diverse and abundant macroinfauna, with Crustacea, Polychaeta and Bivalvia
being the most typical taxa (Brown and McLachlan, 1990). Since exposed
sandy beaches are mostly considered as physically controlled environments,
interactions between the main parameters have been frequently analysed.
Several studies on micro and mesotidal coasts have shown trends in intertidal
macroinfauna, with community structure related to beach morphodynamic and
wave environment (McLachlan et al., 1981; Defeo et al., 1992; McLachlan, et
al. 1993; McLachlan et al., 1996).
McLachlan et al. (1993) found that beach type, defined by the
dimensionless Dean’s parameter (Ω = Hb/ (Ws x T), where Hb is breaker
height in cm, Ws the sand fall velocity in cm.s-1 (Gibbs et al., 1971) and T the
wave period in seconds, is a good predictor of species richness, abundance and
biomass for microtidal beaches across different geographic regions, thus
classifying beach types into reflective, intermediate and dissipative. The scale
for the morphodynamic state would be as follow: Ω > 6 dissipative beach, Ω <
1 reflective beach and 1< Ω < 6 in the intermediate case. When tidal range
varies among different coastal areas, tidal effects must be taken into account
since elevated tidal energy (i.e. tidal range greater than 2-3 m) increases the
dissipative nature of beaches (Masselink and Short, 1993). To account for this,
McLachlan et al. (1993) created the beach state index (BSI = log [(Hb x M/Ws
x T x E) + 1]), where M is the maximum tide range and E is the theoretical
equilibrium tide for which the earth covered in water (E=0.8 m). Based upon a
comparative study of about 70 beaches, McLachlan et al., 1993; suggested the
following scale for BSI: <0.5 reflective beaches, 0.5-1 low to medium energy
intermediate beaches, 1.0.-1.5 high energy intermediate-dissipative beaches,
1.5-2.0 fully dissipative beaches, and > 2.0 ultradissipative macrotidal beaches.
Chapter 2 Environmental factors
75
Studies on beach fauna in relation to morphodynamic state indicate that
Dean’s and BSI are generally well correlated with community variables such as
number of species, abundance per linear meter and biomass (Jaramillo and
McLachlan, 1993; McLachlan et al. 1993; Hacking, 1998; McLachlan et al.
1998; Nell, pers. comm..). The biotic characteristics of exposed sandy beaches
have been related to many abiotic factors and physical variability has been
emphasised as the primary force controlling macroinfaunal communities
(McLachlan, 1983 a review). Beach morphology seems to have relevant
consequences on the intertidal macrofauna zonation, and McLachlan (1990)
and McLachlan et al. (1981) found significant correlations between
macroinfaunal community parameters and grain size, beach face slope and
beach type. Thus, species richness, as well as total abundance and biomass of
the macroinfauna tend to increase from narrow beaches having coarse sands
and steep slopes (i.e. reflective beaches, sensu Short and Wright, 1983), to
wider beaches having finer sands and flatter slopes (i.e. dissipative beaches,
sensu Short and Wright, 1983). Hence, macroinfaunal changes are related to
changes in physical characteristics occurring along a gradient of beach
morphodynamic types (Brazeiro 2001).
Following previous works, the aim of this study was to analyse the
macroinfauna community of exposed sandy beaches along the northern coast of
Spain. Variation in number of species, biomass and abundance of the intertidal
macrofauna was analysed along a coastal area where mostly intermediate sandy
beaches occur, with different morphologies and exposure conditions. The
significance of physical and morphodynamic parameters facing biotic factors
has been tested when only intermediate type of beach was present.
2.2.2. Material and methods
2.2.2.1. Study area
Ten sandy beaches on the northern coast of Spain, Oyambre, Liencres,
Langre, Berria, Laredo, Salvaje, Bakio, Laga, Zarautz and Hendaya (Fig.1),
were sampled during low spring tides of September 1999. Beaches were
Chapter 2 Environmental factors
76
located along circa 300 km of coast along the southern coast of the Bay of
Biscay, including the regions of Cantabria and Vasque Country. Tides in this
shore are semidiurnal and mesotidal, with maximum ranges close to 4 m.
Figure 1. Location of the ten sandy beaches studied at northern part of Spain.
2.2.2.2. Sampling design
Macrofauna sampling was carried out at six replicated transects
randomly-separated at the central area of each beach during low tide. At each
transect, 10 equally spaced shore levels extending from above the drift line
(level 10) to the low swash zone (level 1) were sampled. Previous studies of
macroinfauna in exposed beaches (Bally, 1983) showed that the highest
abundances are usually found in the first 15-20 cm depth, so, samples were
collected with metallic cylinders of 25 cm of diameter penetrating 15 cm depth
into the substrate. An area of 0.3 m2 was sampled at each level, the sediment
sieved through 1 mm mesh and the residue was preserved in 4% formalin. The
result was 3 m2 of total sampling surface in each beach; that means enough
surface in order to get a high percentage (90%) of the total number of species
and total abundance in temperate beaches, following Jaramillo et al., (1995).
FRANCEGULF OFBISCAY
Santander
Bilbao San Sebastián
Oya
mbre
Lie
ncre
s
Langre
Berr
iaLare
do
Hen
daya
Zara
utz
Laga
Bakio
43ºN
44ºN
4ºW 3ºW 2ºW
25 km
Chapter 2 Environmental factors
77
The individuals were later sorted from the sediments, identified and counted in
the laboratory.
Shell-free biomass was determined by drying at 100ºC for 24 hours
and 500ºC for 6 hours, obtaining ash free dry weigh values (A.F.W.D.).
Abundance and biomass values per running meter (i.e. estimates of total
macroinfauna in an intertidal across shore transect 1 m wide) were obtained by
linear interpolation between sampling levels, after obtaining mean values of
biomass and abundances per m2.
Three samples of sediment for grain size analyses were collected at
each level by inserting a 3 cm diameter metal corer to a depth of 15 cm. Grain
size of sand was analysed using a Coulter LS 200 laser diffraction particle size
analyser and the coarser fraction (> 2 mm) by dry sieving (Folk, 1980). Wave
height was estimated by measuring the height of breaking waves with
graduated poles against the horizon. Beach slope at each site was determined
by Emery’s profiling technique (Emery, 1961). From the average wave height
(Hb), wave period (T) and sand fall velocity of particles (values estimated
using the mean grain-size from the swash zone and conversion tables given by
Gibbs et al., 1971) dimensionless Dean’s parameter (Gourlay, pers.comm.;
Short and Wright, 1983) was calculated. The wave period was the time interval
between breakers and swash environment was estimated measuring maximum
swash amplitude, calculated as the distance between highest and lowest turning
point of the upswash and backswash respectively during five minutes period.
Beach State Index, from McLachlan et al. (1993), was also calculated in order
to analyse differences due to different tidal range in the ten studied beaches.
The 20-point rating system proposed by McLachlan (1980) was used to
estimate the wave exposure rate at each beach.
2.2.2.3. Statistical analysis
Regression analyses to test for relationships between biotic and abiotic
variables were carried out with SPSS program. The value of α (0.05) was
modified with the sequential Bonferroni correction when the same dependent
Chapter 2 Environmental factors
78
0
2
4
6
8
0
2
4
6
8
0 100 200 300
02468
m a
bo
ve lo
w t
ide level
02468
02468
02468
02468
02468
02468
0 100 200 300
02468
Oyambre Salvaje
Liencres
Langre Laga
Bakio
Berria
Laredo Hendaya
Zarautz
variable was analysed against various independent variables, according to
Holm (1979).
2.2.3. Results
2.2.3.1. Physical environment
The beach face morphology is shown in Fig. 2. The slopes varied
between 1/22 (Bakio) and 1/48 (Oyambre and Laredo). The physical
characteristics of substrate are shown in Table 1. Sands from these beaches
ranged from coarse (564 µm in Bakio) to medium sands (260 µm Berria) and
sediments were very poorly sorted, varying between 1.5 φ and 1.8 φ, indicating
a moderate grain selection in all the beaches sampled. Mean wave periods
during sampling dates varied from 12 s (Oyambre) to 17 s (Hendaya), with
wave heights from 0.31 m (Laredo) to 2.09 m (Zarautz). Maximum swash
amplitude ranged from 11 to 49 m (Table 1).
Figure 2. Beach face slopes at the ten sites sampled.
Chapter 2 Environmental factors
79
The values of dimensionless Dean’s parameter (table 1) tend to include
most of these beaches in the intermediate morphodynamic state, except the
beaches of Laredo and Hendaya which were close to a reflective state (sensu
Short and Wright, 1983). BSI values (Table 1) classified some of the beaches in
low to medium energy intermediate types (Langre, Laredo, Salvaje, Bakio,
Laga and Hendaya) and others in high energy intermediate/dissipative beaches
(Oyambre, Liencres, Berria and Zarautz). The 20-point rating system proposed
by McLachlan (1980) defined the beach of Hendaya as sheltered (maximum
score = 10), the beaches of Langre (15) and Laredo (12) as exposed, whereas
the rest of the beaches were defined as very exposed (> 15).
2.2.3.2. Composition and abundance of the macrofauna
Characteristics of the macrofauna community are shown in Table 2.
The number of species was highest at the beach of Laredo (29) and the lowest
at Salvaje and Bakio (10). Density values as high as 329 ind.m-2 were found at
Salvaje while 31 ind.m-2 were found at Liencres. Biomass values ranged
between 0.03 and 0.278 g.m-2. Abundances per running meter ranged between
4962 (Liencres) and 71228 ind.m-1 (Salvaje) and biomass per running meter
ranged between 3 (Bakio) and 61 g. m-1 (Laredo).
Chapter 2 Environmental factors
80
Ta
ble
1.
Ph
ysi
cal
char
acte
rist
ics
of
10
bea
ches
of
no
rther
n S
pai
n.
a Len
gth
of
bea
ch.
b W
idth
of
bea
ch
c Mea
n ±
SD
of
the
mea
sure
d v
alues
at e
ach s
am
ple
d t
ran
sect.
d M
ean ±
SD
of
the
mea
sure
d v
alues
duri
ng l
ow
tid
e (n
> 3
0)
e Sen
su M
cLac
hla
n’s
(1
98
0)
rati
ng s
yst
em (
i.e.
[w
ave
acti
on,
surf
zo
ne
wid
th,
% v
ery f
ine
sand
, m
edia
n p
arti
cle
dia
met
er a
nd
slo
pe,
dep
th o
f re
duce
d l
ayer
s, s
tab
le b
urr
ow
s.]
Ω:
D
ea
n’
s
pa
ra
me
te
r.
M.
G.
S.
M
ea
n
gr
ai
n
si
ze
.
Wave
s
Beach
L (
m)a
W (
m)b
Inte
rtid
al slo
pe
M.G
.S.
(µm
)cS
ort
ing
cP
eriod (
s)d
Hb (
m)
ΩR
TR
Sw
as
h
(m
)B
SI
Exp
osure
rating
e
Oya
mbre
1800
200
1/4
7.9
344±79
1.7
±0.1
12
1.2
51.9
23.1
625
1.0
216[3
,1,2
,6,3
,1]
Lie
ncre
s2800
180
1/3
4.3
527±41
1.6
±0.1
15
2.0
92.4
01.8
918
1.1
119[4
,1,2
,7,4
,1]
Lang
re800
194
1/4
4.6
400±57
1.6
±0.1
12
0.9
11.3
64.3
421
0.8
915[2
,0,2
,6,4
,1]
Berr
ia2000
260
1/5
5.9
260±21
1.6
±0.1
14
1.1
72.2
43.4
622
1.0
916[2
,1,2
,6,4
,1]
Lare
do
4250
243
1/4
8.2
270±17
1.7
±0.1
15.7
0.3
10.4
913.2
13
0.5
412[1
,1,2
,5,2
,1]
Salv
aje
752
200
1/3
2.
438±46
1.6
±0.0
14.5
2.8
01.1
81.4
139
0.8
317[4
,1,2
,7,3
,1]
Bakio
540
115
1/2
2.1
9564±40
1.5
±0.1
16.4
1.4
01.1
62.8
16
0.8
317[3
,1,2
,6,4
,1]
Lag
a574
178
1/4
2.4
1542±61
1.7
±0.1
12.1
0.8
31.0
94.8
16
0.8
16[2
,0,2
,7,4
,1]
Zara
utz
2500
180
1/3
8.2
457±28
1.6
±0.1
13.3
3.2
11.9
21.2
49
1.0
219[4
,1,2
,7,4
,1]
Hendaya
3000
145
1/4
7.4
315±39
1.8
±0.0
17
0.3
80.5
110.4
19
0.5
410[1
,0,1
,5,2
,1]
Chapter 2 Environmental factors
81
2.2.3.3. Relationships between macrofauna and environmental variables
The biplots of biotic variables (i.e. number of species, abundance and
biomass) versus abiotic factors (BSI, RTR, slope, average grain size and
exposure) are shown in fig. 3. No significant correlation at α = 0.05 was found
among macrofaunal characteristics with slope or BSI. Beach State Index has
been used as a modification of the Dean’s parameter to compare beaches from
different geographic areas with different tide ranges (McLachlan et al., 1993).
A very significant linear correlation between Dean morphodynamic parameter
and Beach State Index was obtained, since no different tidal range was found in
the studied beaches (BSI =0.43+0.3 Dean; r2 = 0.97, p <0.0001, powerα = 0.05
=1.0). Since Dean’s parameter should really only be used for microtidal
beaches and BSI combines this with a measure of tide range, we think BSI may
be more appropriate here. Consequently, Dean’s parameter has not been
included in the analysis.
Table 2. Characteristics of the macrofauna at the northern studied beaches. a Means of the values at each sampled transect.
The correlations between number of species and average grain size and
exposure rating were not significant when they were modified with the
sequential Bonferroni correction. Thus, the findings should be interpreted
cautiously. The number of species was linearly correlated with RTR (number
of species = 9.32 + 1.19 x RTR; r2 = 0.75, p<0.01, powerα = 0.05 = 0.94).
Macrofaunal number of species was also linearly correlated with average grain
size (number of species = 28.01 – 0.032 x grain size; r2 = 0.424, p<0.05,
Biomass
Beach Number of species Abundance (ind.m-1
) Density (ind.m-2
)a
(gm-1
) g(m-2
)
Oyambre 14 22954 106±37 23 0.121
Liencres 13 4962 31±17.2 25 0.128
Langre 16 11563 60±9.7 9 0.044
Berria 16 17110 70±55.5 49 0.199
Laredo 29 35245 143±13.2 61 0.278
Salvaje 10 71228 329±98.7 15 0.072
Bakio 10 9157 76±14.2 3 0.03
Laga 14 7549 45±9.6 5 0.027
Zarautz 11 28904 155±32.3 11 0.058
Hendaya 16 17902 105±25 26 0.178
Chapter 2 Environmental factors
82
powerα = 0.05 = 0.54) and with exposure rating (number of species =34.8 – 1.27 x
exposure rating; r2 = 0.426, p<0.05, powerα = 0.05 = 0.54). Biomass, either in m-2
or as m-1, was exponentially and linearly correlated with average grain size,
respectively (biomass [g.m-2] = 0.041 + 3.25 exp (-0.011 grain size); r2 = 0.77,
p<0.01, powerα = 0.05 = 0.95), (log biomass [g.m-1] = 78.5 – 0.13 x grain size; r2
= 0.64, p<0.01, powerα = 0.05 = 0.83).
RTR
2 4 6 8 10 12
r2 =0.75
M.G.S
300 400 500
r2 = 0.64
BSI
0,5 1,0 1,5 2,0
Nu
mb
er
of
sp
ec
ies
5
10
15
20
25
Exposure rate
10 12 14 16 18
De
ns
ity
(in
d.
m-2
)
100
200
300
Ab
un
da
nc
e
(in
d.
m-1
)
20000
40000
60000
Bio
ma
ss
(g.
m-2
)
0,05
0,10
0,15
0,20
0,25
Oyambre
Liencres
Langre
Berria
Laredo
Salvaje
Bakio
Laga
Zarautz
Hendaya
Slopes
0,01 0,02 0,03 0,04
r2 =0.77
r2 =0.42r2 =0.42
Lo
g b
iom
as
s
(g.
m-1
)
0,01
0,1
1
10
Beaches
Figure 3. Biplots of average values of biomass, abundance, density and number of
species vs. BSI (sensu Short and Wright, 1983), RTR, intertidal slope, median swash
grain size and exposure rating (sensu McLachlan, 1980a). Lines indicate significant
regressions at α= 0.05.
Chapter 2 Environmental factors
83
2.2.4. Discussion
Community analysis shows that macroinfauna values of density (31 to
329 ind.m-2) and biomass (0.03 to 0.27 g.m-2) of the 10 intermediate sandy
beaches in northern Spain were included within the range of density and
biomass values obtained in exposed sandy beaches worldwide (e.g. McLachlan
et al., 1981a; Defeo et al., 1992; Jaramillo et al., 1993; McLachlan et al., 1996,
Hacking, 1997). Results of number of species, ranging from 10 to 29, were
similar to values obtained in beaches from other temperate latitudes such as
Belgium (Degraer et al. 1999) and California (Dugan, et al. 2003), but differ
from results for beaches in Chile and Uruguay, where values obtained were
lower (Defeo et al., 1992; McLachlan et al. 1993; Jaramillo et al., 1993).
Moreover, a wider range of differences in species richness can be observed by
comparison with intermediate beaches from lower latitudes. Thus, the present
values are higher than those found in South African beaches (McLachlan et al.,
1981a), lower than values obtained in Oman (McLachlan et al., 1998) and
similar to species richness found in beaches sampled in Australia (McLachlan,
1996; Hacking, 1998). It is thought that this high variability comes from poorly
known factors such as biogeographic, latitudinal and oceanographic conditions
and particular local events, rather than just beach morphodynamic differences.
The general patterns found on sandy beach macroinfauna show a
negative correlation between species richness and exposure rating and grain
size (McLachlan and Jaramillo, 1995; McLachlan, 1996) as the present results
confirm. The greater the grain size and the higher the exposure rate, the higher
flushed and oxygenated interstitial spaces will be (McLachlan, 1989), resulting
in fewer macroinfauna by effects of waves and currents in exposed sandy
beaches. Conversely, reduction in beach exposure and average grain size can be
more favourable for macroinfauna (McLachlan and Jaramillo, 1995;
McLachlan et al., 1996).
The results plotted in Figure 3, show that number of species is the
biotic parameter most affected by the abiotic factors, increasing linearly with
RTR and diminishing from exposed to very exposed beaches and also
Chapter 2 Environmental factors
84
diminishing with increasing average grain size, although we have worked with
only a limitated range of particles, from 260 to 564µm. On the other hand,
biomass, either in g.m-2 or as log (g.m-1) decreases exponentially with
increasing average grain size. These trends agree with the predictions of
McLachlan et al., 1981b and Brown and McLachlan 1990, stating a negative
relationship between grain size and biomass. McLachlan et al. 1993 found all
these trends in beaches of United States, Australia and South Africa, and
Jaramillo, et al., 1993 found the same trends in beaches of Chile. Furthermore,
Hacking (1997) and Nell (pers. comm.) found the same trends in beaches of
Australia and South Africa respectively.
There are not enough differences in face slope, among the ten beaches
studied, to determine macrofauna trends since significant correlations have not
been found with any community variable. This low predictive value can be
partially related to the similarity of intermediate beach profiles in our ten
sampled beaches (Coefficient of Variation, C.V. = 31%) as compared with
variability of number of species (C.V. =35%), abundance m-2 (C.V. =73%),
abundance m-1 (C.V. =82%), biomass m-2 (C.V. =70%) and biomass m-1 (C.V.
=80%). This result differs from previous studies where steep slopes limit beach
macroinfauna (McLachlan et al., 1981a and McLachlan, 1990).
No significant trend was found between morphodynamic state of the
beaches (Dean’s parameter and BSI) and macrofauna. This has been shown
previously in present beaches for meiofauna (Rodriguez et al., 2003), and it is
opposite to the general patterns of sandy beach macroinfauna found in previous
studies (McLachlan, et al., 1981a; McLachlan, 1983 a review; Brown and
McLachlan, 1990; Jaramillo et al., 1993; McLachlan et al. 1993; McLachlan et
al., 1996; McLachlan et al. 1998 and Hacking, 1998). Since the parameters
(Dean and BSI), that include variables such as period and wave height did not
show significant correlations with our community characteristics, the
importance of these morphodynamic parameters seems to decrease. Dean’s
parameter values from Laredo and Hendaya show them as reflective beaches
instead of real intermediate-dissipative beaches, as it is stated by their beach
face slopes (1/48 and 1/47, respectively) and grain size (270±17 and 315±39
Chapter 2 Environmental factors
85
µm, respectively). The low values of Dean’s and BSI parameters are mostly
because of the low height break of the waves observed during the sampling
period. Moreover, the values obtained from wave height and period on these
beaches have a wide range of variation at different periods of time throughout
the year (Lastra, pers. com.). Therefore, it can be suggested that beach
morphodynamics described by Dean’s and BSI parameters have low capacity
in predicting community characteristics in the ten intermediate beaches studied
here. The validity of morphodynamic parameters have been generally
demonstrated when a full range of beach types are included in the analysis, i.e.
from reflective to dissipative (Jaramillo et al., 1993; McLachlan et al. 1993;
Jaramillo and McLachlan, 1993).
On the other hand, when only intermediate beaches are studied, the
different community characteristics seem to be affected by different abiotic
factors. The number of species is better explained by the exposure rating
(although this was not significant when we used Bonferroni´s correction) than
by variables such as Dean’s parameter or even beach slope, while biomass is
only affected by mean grain size. This confirms that a greater ensemble of
variables should be taken into account in the ecology of sandy beach
macroinfauna, as previously suggested by McLachlan et al., 1996 and Brazeiro
2001. Hence, this shows that communities of sandy beach invertebrates are
limited by more different ecological factors than a single key factor.
In the case of RTR (Fig.3.), there was a significant correlation with
number of species; so when the tide range becomes more significant than wave
energy, number of species increases. Further than this, Dean’s parameter is
smaller in those beaches (Laredo and Hendaya) where RTR reached high
values. Most of the studied beaches showed a broken profile roughly separated
by mean sea level into an upper steep beach, followed by a lower flat
downshore as previously found in beaches from Scotland (Eleftheriou and
Nicholson, 1975) and in the North West coast of Spain (de la Huz, pers.
comm.). The beaches studied have strongly interacting conditions of tide and
wave energy, resulting in broad flat beaches, tide-dominated on the lower
shores but tending towards swash control in the upper intertidal. When beaches
Chapter 2 Environmental factors
86
become increasingly tide dominated, they tend toward tidal flats and become
highly dissipative, where intertidal fauna is rich, while the high tidal zones are
reflective and poorer in fauna (Brown and McLachlan, 1990). No significant
correlation was found between swash amplitude and any of the biotic variables
in the 10 studied beaches.
In conclusion, the intertidal benthic macrofauna inhabiting intermediate
sandy beaches of northern Spain could not be fully related to beach
characteristics studied because of the limited range of beaches studied. There is
no unique key factor affecting benthic macrofauna, but several ecological
factors influence to the different community variables. More studies covering a
complete spectrum of beach types, environmental variables and exposure rates
are needed to check trends and general patterns in the intermediate type of
beaches, which is the dominant morphodynamic type along the northern coast
of Spain. We also need to check McLachlan & Turner’s (1993) predictions in
relation to morphodynamics where intermediate situations are likely to be the
optimum conditions for the development of an abundant interstitial fauna.
Acknowledgments
We thank K. Aerts for helping in laboratory works and C. de la Huz,
M. Incera, J. López, M. Pita and J.G. Rodríguez for field assistance. This
research was supported by The University of Vigo (64102C859) and the
Autonomous Government of Galicia (XUGA30105A98).
2.2.5. References
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Davies, J. L. 1972 Geographic variation in coastal development. Longmans.
London (204 pp.)
Defeo, O., Jaramillo, E., Lyonnet, A. 1992 Community structure and intertidal
zonation of the macroinfauna on the Atlantic coast of Uruguay. Journal
of Coastal Research. 8, 830-839.
Chapter 2 Environmental factors
87
Degraer, S., Mouton, I., De Neve, L., Vincx, M. 1999 Community structure and
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Dugan, J., Hubbard, D.M., McCrary, M.D., Pierson, M.O., 2003. The response
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Emery, K. O. 1961 A Simple Method of Measuring Beach Profiles. Limnology
and Oceanography. 6, 90-93.
Folk, R. L. 1980 Petrology of sedimentary rocks. Hemphill Publishing
Company. Austin, TX. (182 pp.).
Gibbs, R. J., Matthews, M. D., Link, D. A. 1971 The relationship between
sphere size and settling velocity. Journal of Sedimentary Petrology. 41,
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Hacking, N. 1998 Macrofaunal community structure of beaches in northern
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Holm, S. 1979 A simple sequentially rejective multiple test procedure Scandinavian Journal of Statistics. 6, 65-70.
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of species richness in exposed sandy beaches. Marine Ecology
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McLachlan, A. 1980 The definition of Sandy Beaches in Relation to Exposure:
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McLachlan, A. 1983 Sandy beach ecology. A review. In A. McLachlan & T.
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McLachlan, A. 1989 Water filtration by dissipative beaches. Limnology and
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McLachlan, A. 1990 Dissipative beaches and macrofauna communities on
exposed intertidal sands. Journal of Coastal Research. 6, 57-71.
McLachlan, A. 1996.Physical factors in benthic ecology: effects of changing
sand particle size on beach fauna. Marine Ecology Progress Series.
131, 205-217.
McLachlan, A., Wooldridge, T.,Dye, A. H. 1981 The ecology of sandy beaches
in southern Africa. South African Journal of Zoology. 16, 219-231.
McLachlan, A., Erasmus, T., Dye, A. H., Wooldridge, T., van der Horst, G.,
Rossouw, G., Lasiak, T. A., McGwynne, L. 1981 Sand beach
Chapter 2 Environmental factors
88
energetics: an ecosystem approach towards a high energy interface,
Estuarine Coastal and Shelf Science. 13, 11-25.
McLachlan, A., Turner, I. 1993 The interstitial environment of Sandy Beaches.
Marine Ecology. 15(3/4), 177-211
McLachlan, A., Jaramillo, E., Donn, E., Wessels, F. 1993 Sandy Beach
Macrofauna Communities and their Control by the Physical
Environment: A Geographical Comparison. Journal of Coastal
Research. 15, 27-38.
McLachlan, A., Jaramillo, E. 1995 Zonation on sandy beaches. Oceanography
and Marine Biology: An annual review. 33, 305-333.
McLachlan, A., de Ruyck, A., Hacking, N. 1996 Community structure on
sandy beaches: patterns of richness and zonation in relation to tide
range and latitude. Revista Chilena de Historia Natural. 69, 451-467.
McLachlan, A., Fisher, M., Al-Habsi, H. N., Al-Shukairi, S. S., Al-Habsi, A.
M. 1998 Ecology of sandy beaches in Oman. Journal of Coastal
Conservation. 4, 1-10. Masselink, G., Short, A.D. 1993 The effect of tide range on beach
morphodynamics and morphology: a conceptual beach model. Journal
of Coastal Research. 9(3): 785-800.
Rodríguez, J. G., Lastra, M., López, J. 2003 Meiofauna distribution along a
gradient of sandy beaches in northern Spain. Estuarine Coastal and
Shelf Science. 56, 1-7.
Short, A. D., Wright, L. D. 1983 Physical variability of sandy beaches. A.
McLachlan and T. Erasmus (Eds.) Sandy beaches as ecosystems. 133-
144. Junk. The Hague.
Chapter 3. Community structure and intertidal zonation
of the macroinfauna in intermediate sandy beaches
in temperate latitudes: North coast of Spain.
Rodil, I.F., Lastra, M., and Sánchez-Mata, A.G.
Published in Estuarine, Coastal and Shelf Science (2006). 67: 267-279
Chapter 3 Community structure
90
Abstract
Nineteen intermediate exposed sandy beaches, located along the
northern coast of Spain, were sampled during the summer of 1999. Data from
ten of the beaches, located at the eastern part of this coast, was previously
reported to evaluate environmental factors affecting benthic macrofauna. Data
from nine of the beaches, located at the western part of this coast, was included
to compare community structure and intertidal zonation of the macroinfauna on
intermediate sandy beaches in temperate latitudes. Morphodynamic parameters
such as Dean’s parameter (Ω), Beach State Index (BSI) and relative tide range
(RTR) were estimated at each beach. Beach length, width, intertidal slope,
medium grain size, sorting, swash amplitude and wave characteristics were also
analysed. The highest macroinfaunal densities and biomass occurred at the mid
and lower shore levels of each beach. Crustaceans, mainly cirolanid isopods,
were the dominant group found on these beaches, whereas molluscs were the
least representative. In general, the relationship between community structure
and beach morphodynamics was similar to that found for the macroinfauna
worldwide; suggesting that macroinfauna in intermediate sandy beaches is
affected, in the same way, by the physical processes associated with different
beach types. Histograms and kite diagrams representing the intertidal
distribution of the macroinfauna and multivariate analysis were used to show
the zonation pattern on these exposed beaches. Intertidal slope values and
beach profile pattern was found similar in all the beaches sampled. We
hypothesized that this particular beach profile could influence the pattern of
macroinfauna zonation. All the nineteen beaches have two zones in common:
the supralittoral zone of air breathers present on all shores at and above the drift
line and the littoral zone extending from the drift line down the midshore to just
above the water table outcrop. Ordination analyses identified two possible
zones within the lower beach levels on seven of the beaches, but this can not be
clearly established. The Monte Carlo permutation test was used to select beach
slope, length and wave height as the best predictor variables of macroinfaunal
Chapter 3 Community structure
91
characteristics and it seems that the species most affected by the main variables
showed the clearest zonation on the beaches.
Keywords: intermediate sandy beaches; benthic macrofauna; intertidal
zonation; beach morphodynamics; swash climate; northern Spain.
2.3.1. Introduction
Sandy beaches are the most dynamic of soft bottom habitats
(McLachlan et al., 1996) and dominate the world’s temperate and tropical
shorelines (Davies, 1972). Despite their uniform appearance and comparative
poverty, intertidal zones of exposed beaches harbour a marine fauna of great
ecological diversity. Crustacea, Polychaeta and Bivalvia rank among the most
common macroinfaunal taxa (Brown and McLachlan, 1990), while Nematoda,
Harpacticoidea, Plathelmintha and Oligochaeta dominate meiofaunal groups on
sandy beaches (McLachlan, 1980).
Macrofaunal zonation on sandy beaches is a distinctive and well-
described phenomenon of intertidal zones (McLachlan and Jaramillo, 1995);
several attempts have been made to construct zonation schemes for sandy
beach macroinfauna. Two general zonation schemes have been commonly used
to determine distributions of organisms on sandy beaches: Dahl (1952) defined
three biological zones in terms of a typical crustacean fauna inhabiting each
zone, and Salvat (1964) defined four physical zones. These zones can be
recognised by the species found, and Dahl’s zonation pattern can easily been
superimposed on Salvat’s scheme. This scenario only represents the position
during low tide and, because of the highly mobile fauna, such zones would not
be expected to have sharp boundaries and, in fact, they often overlap
(McLachlan, 1983; Degraer et al., 1999).
It has been shown that beach type can be used as a reliable predictor of
species richness, abundance and biomass of the macroinfauna (e.g. McLachlan,
1990; McLachlan et al. 1993, Jaramillo and McLachlan, 1993). Swash
characteristics, which are distinctive for each type of beach (e.g. McArdle and
McLachlan, 1992), may also influence the community structure of the
macroinfauna (e.g. Jaramillo et al., 1993). Slope is closely related to swash
Chapter 3 Community structure
92
climate, which becomes less harsh as the beach face slope flattens (McArdle
and McLachlan, 1992). Environmental changes, associated with the
morphodynamic gradient, seem to have a relevant consequence on the intertidal
macroinfauna and on the zonation patterns. The relationship between species
richness and beach morphodynamics is supported by one common
generalization in sandy beach ecology: the macroinvertebrates decreasing along
a morphodynamic gradient from the dissipative to the reflective conditions
(sensu Short and Wright, 1983) (e.g. Defeo et al., 1992; Jaramillo and
McLachlan, 1993; McLachlan, et al., 1996; Brazeiro, 1999). Intermediate
beaches belong to the morphodynamic sandy beach type produced by moderate
to high waves, fine to medium sand, and long wave periods with intermediate
surf zones characterized by bars, troughs and rip currents (Wright and Short,
1983). The importance of understanding the ecology of intermediate sandy
beaches derives from the fact of there being the most common morphodynamic
beach type (Short, 1996; Alongi, 1998) and one of the most extended intertidal
systems worldwide.
The pioneering studies carried out on intermediate beaches in northern
Spain found no relationships between morphodynamic state and species
richness, biomass or abundance of macroinfauna (Rodil and Lastra, 2004) and
meiofauna (Rodríguez et al., 2003). In larger geographical studies, including
sandy beaches from areas with different oceanographic conditions and other
variables such as Chlorophyll-a concentration in the water column could be a
key factor explaining macrofaunal patterns. A key physical characteristic
typical of these beaches was a profile with a steep foreshore followed by a flat
lower shore, also found on Scottish beaches (Eleftheriou and Nicholson, 1975)
and on the North West coast of Spain (de la Huz, pers. comm.). This profile
creates a reflective character for the upper part of these beaches, while the
lowest part of the shores exhibits dissipative properties. We hypothesized that
this particular profile could give rise to a zonation other than that expected for
intermediate sandy beaches with a more regular or monotonic profile; at the
same time, the idea that such beaches may support more species due to the
variation in swash climate across the beach profile could be investigated. In
Chapter 3 Community structure
93
fact, this factor should be predicted to be more important for species that
interact directly with the swash than for those that inhabit the supralittoral dry
zones. Clear population responses to beach type have not been observed in
supralittoral macroinfauna (Contreras et al., 2003, Defeo and Martínez 2003),
which seems to be less influenced by the swash climate. To examine this
hypothesis, results were analysed from nineteen intermediate sandy beaches,
located in the northern coast of Spain, to evaluate the zonation of intertidal
macrofauna and compared with results from other intermediate beaches
worldwide. This paper provides a description of faunal zonation, composition
and density of the macroinfauna on intermediate morphodynamic beaches
along the northern shoreline of the Iberian Peninsula. Changes in community
structure along the beach profile and factors influencing these patterns are also
considered.
2.3.2. Material and methods.
2.3.2.1. Study area
Nine sandy beaches along the Northwest coast of Spain; Peñarronda,
Otur, San Pedro, Xagó, Xivares, La Espasa, Vega, Toranda and Andrín were
sampled in order to establish a reliable zonation scenario in intermediate sandy
beaches including the data previously obtained from ten eastern beaches on this
coast (Rodil and Lastra, 2004); Oyambre, Liencres, Langre, Berria, Laredo,
Salvaje, Bakio, Laga, Zarautz and Hendaya (Fig. 1). All beaches were located
from 43º 25’ N, 7º 00’ W to 43º 44’ N, 1º 50’ W and spanned a total of 800 Km
of coastline.
Sampling was carried out during spring low tides of September 1999 to
avoid variability linked to seasonal cycle (as community dynamics, species life
cycle, water temperature, storm events, accretion-erosion dynamics, etc) (Lima,
et al., 2000; Jaramillo et al., 2001; Brazeiro, 2001; Defeo and Rueda, 2002).
Tides on this coast are semidiurnal and mesotidal, with a medium tidal range of
three meters.
Chapter 3 Community structure
94
Figure 1. Location of the 19 intermediate sandy beaches studied on the northern coast
of Spain.
2.3.2.2 Sampling design
For all 19 beaches, macrofauna sampling was carried out at six
replicated transects haphazardly separated at the central area of each beach
during low tide. At each transect, 10 equally spaced shore levels extending
from above the drift line (level 10) to the low swash zone (level 1) were
sampled. Previous studies of macroinfauna on exposed beaches (Bally, 1983)
showed that the highest abundances are usually found in the first 15-20 cm
depth. Thus, samples were collected with 25 cm diameter metal cylinders
penetrating 15 cm deep into the substrate. An area of 0.3 m2 was sampled at
each level, the sediment was sieved through 1 mm mesh and the residue was
Zar autz
Lar edo
B err ia
Lan g re
Lien cre s
An dr in
Veg a
Xiv ares
Xag óPeñ arro nd a
San Ped ro
La E sp asa
Tor and a Oy amb re
Salv aje Lag a
B akio
Hen day a
Otu r
Chapter 3 Community structure
95
preserved in 4% formalin. The result was 3 m2 of total sampling surface on
each beach; this being sufficient surface to collect a high percentage (90%) of
the total number of species and abundance in temperate beaches (Jaramillo, et
al., 1995). The individuals were later sorted from the sediments, identified and
counted in the laboratory.
Shell-free biomass of all the species was determined by drying at
100ºC for 24 hours and then at 500ºC for 6 hours, obtaining ash free dry weight
values. Abundance and biomass per running meter (i.e. estimates of total values
in an intertidal across shore transect 1 m wide) were obtained by linear
interpolation between sampling levels, after obtaining mean values per m2.
Three samples of sediment for grain size analyses were collected at
each level by inserting a 3 cm diameter metal corer to a depth of 15 cm. Grain
size of sand was analysed using a Coulter LS 200 laser diffraction particle size
analyser, and the coarser fraction (> 2 mm) by dry sieving (Folk, 1980). Wave
height was estimated by measuring the height of breaking waves with
graduated poles against the horizon. Beach slope at each site was determined
by Emery’s profiling technique (Emery, 1961). From the average wave height
(Hb), wave period (T) and sand fall velocity of particles (values estimated
using the mean grain-size from the swash zone and conversion tables given by
Gibbs, et al., 1971) dimensionless Dean’s parameter (Ω) was calculated (Short
and Wright, 1983). The wave period was the time interval between breakers
and swash environment was estimated measuring maximum swash amplitude,
calculated as the distance between the highest and the lowest turning point of
the upswash and backswash respectively, within a five-minute period. Beach
State Index (BSI), from McLachlan et al. (1993), was also calculated in order
to analyse differences due to differing tide range on the nineteen beaches
studied. The rating system proposed by McLachlan (1980) was used to
categorize the beaches in relation to the wave exposure rate.
2.3.2.3. Statistical analysis
To aid interpretation of species zonation, density values (abundances
per square meter) were calculated and used to plot histograms ands kite
Chapter 3 Community structure
96
diagrams to describe distribution patterns across the beach face. Non-metric
multidimensional scaling ordinations (MDS), with the Bray-Curtis similarity
index, and Cluster analysis (Bray-Curtis index, group-average linkage) were
performed in order to elucidate faunistic belts on the beaches studied.
Measurement of goodness-of-fit of the MDS ordination was given by the stress
value (S); where low stress factor (S<0.2) corresponds to a good ordination
with no real prospect of a misleading interpretation (Clarke and Warwick,
1994). The presence of highly abundant species was standardized with a double
square root transformation. Pairwise analysis of similarities (ANOSIM, Clarke
1993) was carried out to test the null-hypothesis that there were no differences
(at α = 0.05) in the composition of the macroinfaunal assemblages at different
beaches. This was also applied for each beach location separately to assess the
significance of possible macroinfaunal zonation among levels. R is
approximately zero if the null hypothesis is true and close to one when the
lowest similarity appears to occur. MDS, Cluster analysis and ANOSIM were
performed using the PRIMER 5 software package (Clarke and Warmick 1994).
Also, in order to explore any potential relationship between measured
environmental parameters and densities of the macroinfaunal major species, the
technique of Canonical Correspondence Analysis (Hill’s scaling,
downweighting of rare major species) was performed. A previous Monte Carlo
permutation test was first performed to select the environmental variables,
which significantly explained the variability in the abundance of the
macroinfauna (α = 0.05 after 1999 permutations). Canonical correspondence
analysis (CCA) and the Monte Carlo permutation tests were carried out with
CANOCO 4.5 for Windows (ter Braak 1995). The variance explained by the
CCA model was calculated as the sum of eigenvalues axes (Borcard, et al.,
1992). Species with a higher than 20% presence of the overall macroinfauna
identified were selected from the beaches sampled to perform the CCA model.
Macroinfauna densities and environmental values were standardized prior to
analysis to reduce extreme values and to provide better canonical coefficient
comparisons (ter Braak, 1986 and Zar, 1996).
Chapter 3 Community structure
97
2.3.3. Results
2.3.3.1. Physical environment
Physical characteristics of all 19 beaches analysed are shown in Table
1. The characteristics of the nine western beaches are similar to those found for
the ten eastern beaches, which were analysed in Rodil and Lastra (2004), in
terms of sediment substrate (t17 = 1.86, p = 0.08), tide range (t17 = 1.8, p = 0.09)
and beach slope (t17 = 0.51, p = 0.62). Furthermore, all the nineteen
intermediate sandy beaches showed a general decrease in mean grain size at the
upper part of the shoreline (MGS [μm] = 403 - 6.5 x distance to shoreline [m];
R2 = 0.691, p < 0.001).
Eastern beaches were found longer than beaches at the western part of
the coastline (t17 = 2.77, p = 0.013). Six beaches from the western part
(Peñarronda, Otur, San Pedro, La Espasa, Vega and Andrín) share the same
peculiar broken profile as Oyambre, Liencres, Langre, Bakio, Laga, and
Zarautz in the eastern part (Rodil and Lastra, 2004): the upper levels, with a
steep foreshore, differing further from more dissipative levels on the lowest flat
part of the beach profile.
The values of dimensionless Dean’s parameter and BSI values (Table
1) generally categorized all of these beaches as intermediate in morphodynamic
state (sensu Short and Wright, 1983), following the comparative studies from
McLachlan et al. (1993). Dean (t17 = -2.19, p = 0.042) and BSI (t17 = -3.05, p <
0.01) values were significantly higher in beaches located at the western part of
the coastline. The rating system proposed by McLachlan (1980) classified all
the beaches from exposed (11 to 15) to very exposed (16 to 20). Beaches at the
eastern part of the coastline were found to be significantly more exposed (t17
=4.4, p < 0.01) than those located at the western part.
Chapter 3 Community structure
98
Wav
es
Bea
ch
L
(m)a
W
(m)b
Inte
rtid
al
slo
pe
Med
ian g
rain
size
(µ
m)c
So
rtin
gc
Per
iod (
s)d
Hb
(m
)
Dea
n´s
par
amet
er
RT
R
Sw
ash
amp
litu
de(
m)
BS
I
Exp
osu
re
rati
ng
e
Peñ
arro
nd
a 6
00
2
18
1/4
5
36
7±
78
2
.0±
0.2
1
1.5
0
.92
1
.1
4.5
2
5
0.9
1
1[2
,2,2
,4,0
,1]
Otu
r 6
00
2
00
1/3
2
35
5±
1
.0±
0.2
1
3
1.0
2
1.6
4
2
2
1
11
[2,2
,2,4
,0,1
]
San
Ped
ro
34
0
18
7
1
/35
2
66
±8
1
.0±
0.0
1
0.7
0
.86
2
4
.8
14
1
.1
12
[2,2
,2,5
,0,1
]
Xag
ó
83
0
22
6
1
/46
2
70
±6
0
1.0
±0.2
8
.2
1.1
5
2.8
0
.5
24
1
.2
11
[3,1
,2,4
,0,1
]
Xiv
ares
8
00
2
36
1/5
2
27
2±
34
1
.3±
0.0
1
2.6
0
.96
1
.5
4.3
1
9
1
12
[2,2
,2,5
,0,1
]
La
Esp
asa
11
50
18
2
1
/34
4
27
±8
6
1.5
±0.3
1
5.3
2
.07
2
.7
0.3
3
3
1.2
1
2[4
,1,2
,4,0
,1]
Veg
a
14
40
23
0
1
/45
3
09
±2
0
1.3
±0.0
1
3.1
1
.71
2
.6
2.4
2
5
1.1
1
1[4
,1,2
,3,0
,1]
Tora
nd
a 3
00
1
35
1/2
8
24
3±
13
1
.3±
0.0
1
2.6
1
.49
3
2
.7
29
1
.2
11
[3,1
,2,4
,0,1
]
And
rín
24
0
15
6
1
/37
3
18
±2
9
1.3
±0.0
1
1.8
1
,9
3.2
2
.2
11
1
.3
12
[4,1
,2,4
,0,1
]
Oyam
bre
1
80
0
20
0
1
/48
3
44
±7
9
1.7
±0.1
1
2
1.2
5
1.9
2
3.2
2
5
1.0
2
16
[3,1
,2,6
,3,1
]
Lie
ncr
es
28
00
18
0
1
/34
5
27
±4
1
1.6
±0.1
1
5
2.0
9
2.4
1
.9
18
1
.11
1
9[4
,1,2
,7,4
,1]
Lan
gre
8
00
1
94
1/4
5
40
0±
57
1
.6±
0.1
1
2
0.9
1
1.3
6
4.3
2
1
0.8
9
15
[2,0
,2,6
,4,,1
]
Ber
ria
20
00
26
0
1
/56
2
60
±2
1
1.6
±0.1
1
4
1.1
7
2.2
4
3.5
2
2
1.0
9
16
[2,1
,2,6
,4,,1
]
Lar
edo
4
25
0
24
3
1
/48
2
70
±1
7
1.7
±0.1
1
6
0.3
1
0.4
9
13
.2
13
0
.54
1
2[1
,1,2
,5,2
,1]
Sal
vaj
e 7
52
2
00
1/3
2
43
8±
46
1
.6±
0.0
1
4.5
2
.8
1.1
8
3.8
3
9
0.8
3
17
[4,1
,2,7
,3,1
]
Bak
io
54
0
11
5
1
/22
5
64
±4
0
1.5
±0.1
1
6
1.4
1
.16
2
.8
16
0
.83
1
7[3
,1,2
,6,4
,1]
Lag
a 5
74
1
78
1/4
2
54
2±
61
1
.7±
0.1
1
2
0.8
3
1.0
9
4.8
1
6
0.8
3
16
[2,0
,2,7
,4,1
]
Zar
autz
2
50
0
18
0
1
/38
4
57
±2
8
1.6
±0.1
1
3.3
3
.21
1
.92
2
.64
4
9
1.0
2
19
[4,1
,2,7
,4,1
]
Hen
day
a 3
00
0
14
5
1
/47
3
15
±3
9
1.8
±0.0
17
0
.38
0
.51
1
0.4
1
9
0.5
4
10
[1,0
,1,5
,2,1
]
Ta
ble
1.
Ph
ysic
al
chara
cte
risti
cs o
f 1
9 n
ort
hern
beaches o
f S
pain
. a L
en
gth
of
beach.
b W
idth
of
beach
c M
ean ±
SD
of
the m
easure
d v
alu
es a
t each s
am
ple
d t
ran
sect.
d M
ean ±
SD
of
the m
easure
d v
alu
es d
uri
ng l
ow
tid
e (
n>
30
)
e s
ensu M
cL
achla
n´s
(1
98
0)
rati
ng s
yste
m (
i.e.
[w
ave a
cti
on,
surf
zo
ne w
idth
, %
very
fine s
and
, m
ed
ian p
art
icle
dia
mete
r a
nd
slo
pe,
dep
th o
f
red
uced
layers,
sta
ble
burr
ow
s .
]
Chapter 3 Community structure
99
2.3.3.2. Composition and abundance of the Macrofauna
Macroinfauna was dominated by crustacean species (84%), Isopoda
(62.6%) and Amphipoda (17.7%) being the main components of this group.
Polychaetes (11.2%) and molluscs (2.6%) were also present but in lower
abundances. In the supralittoral zone, a mixture of terrestrial and marine
adapted animals was present. Hence, a variety of coleopterans, dipterans and
pupae of uncertain origin, found above the drift line, were excluded from the
final analysis due to low occurrence in all the nineteen beaches sampled.
Oniscoidean isopods and talitrid amphipods were included instead, due to the
high abundances found in the supralittoral part of the beaches. Number of
species, abundance and biomass of macroinfauna of the nineteen beaches are
shown in Table 2. Macroinfauna biomass (from 0.056 to 0.452 g.m-2) and
number of species (from 9 to 15) found in the nine western beaches were
similar to the values from the ten eastern beaches reported in Rodil and Lastra,
2004.
Beach
Number of
species Abundance Biomass
(ind.m-1) (ind.m-2)a (gm-1) (gm-2)
Peñarronda 13 29990 125±71 25 0,106
Otur 11 17172 71±33 52 0,214
San Pedro 10 81829 338±148 54 0,222
Xagó 13 99484 409±387 46 0,452
Xivares 14 95695 395±369 42 0,172
La Espasa 14 43212 180±132 13 0,056
Vega 15 44260 182±121 40 0,162
Toranda 12 38778 160±71 68 0,125
Andrín 9 87714 363±164 27 0,112
Oyambre 14 22954 106±37 23 0.121
Liencres 13 4962 31±17.2 25 0.128
Langre 16 11563 60±9.7 9 0.044
Berria 16 17110 70±55.5 49 0.199
Laredo 29 35245 143±13.2 61 0.278
Salvaje 10 71228 329±98.7 15 0.072
Bakio 10 9157 76±14.2 3 0.03
Laga 14 7549 45±9.6 5 0.027
Zarautz 11 28904 155±32.3 11 0.058
Hendaya 16 17902 105±25 26 0.178
Table 2. Characteristics of the macrofauna at the northern beaches studied. a Mean’s ± SD of the values at each sampled transect.
Chapter 3 Community structure
100
Macroinfauna abundance from the western beaches (from 71 to 409 ind.m-2)
was found significantly higher (t17 = -2.88, p = 0.01) than the abundance found
in the eastern part of the coastline (from 31 to 329 ind.m-2).
MDS analysis (S < 0.2), performed by pooling the sampling levels on
each beach, suggested that the macrofauna communities from the beaches
sampled could be grouped into two broad categories: beaches from the western
part (except Otur; O) and eastern beaches (Fig. 2). The low stress value (S =
0.15) found in the MDS analysis (Fig. 2a) gives a potentially useful two-
dimensional picture, although additional information about the overall structure
would be desirable. The combination of clustering and ordination analyses can
be an effective way of checking the representations (Clarke and Warwick,
1994). Thus, in Figure 2b, the two geographical groups of beaches detected by
the cluster analysis were found to be superimposed on the MDS ordination,
with a Bray Curtis Similarity higher than 40%, which ensures that both plots
(Fig. 2a and b) are an accurate representation of the relationship among the
beaches. ANOSIM results also established a difference (as noted in the MDS
from Fig. 2) between western and eastern beaches, (R = 0.585; p<0.01). This
result must be interpreted with caution since the low R value does not mean
really low similarity between beaches. Laredo showed lower similarity
compared with eastern beaches (R = 0.754; p<0.05) and the lowest with
western beaches (R = 0.948; p<0.05).
2.3.3.3. Intertidal zonation of the macroinfauna
The distribution of the macroinfauna in the lower part of the beaches
was more variable along the East to West gradient than the community
patterns above. Intertidal variability as total abundance (density values
per m2) of the macroinfauna (averaged for all the19 beaches) and the
across-shore distribution of the major species was calculated to plot
histograms (with error bars) and kite diagrams to describe zonation
patterns (Figs. 3 and 4). Total abundance and biomass showed no high
Chapter 3 Community structure
101
across-shore variability even though a peak of abundance was noted at
the upper part of the saturation zone and at the retention zone.
Figure 2. a) Biplot resulting from the multidimensional beach analyses of the
macroinfauna total abundance (density values per square metre).b) Dendogram
resulting from hierarchical cluster analyses of the macroinfauna density values.
(Pe:Peñarronda,O:Otur,SP:SanPedro,Xg:Xagó,Xi:Xivares,Es:Espasa,V:Vega,To:Toran
da,A:Andrín,Oy:Oyambre,Li:Liencres,Lgr:Langre,Be:Berria,Lar:Laredo,Sv:Salvaje,Bk
:Bakio,Lg:Laga,,Z:Zarautz, H:Hendaya).
The upper zone of the beaches was characterised by talitrid amphipods
such as Talitrus saltator (33±16 ind.m-2), Talorchestia brito (2±1ind.m-2) and
Talorchestia deshayesii (1±0 ind.m-2). Air-breathing isopod Tylos europaeus
(2±1 ind.m-2) was also found at the drying beach level (D). Retention zone (Rt)
was mainly characterised by the cirolanid isopods Eurydice pulchra (91±9
ind.m-2) and E. affinis (26±7 ind.m-2), which were also found at the drying zone
in high abundances (65±60 ind.m-2 and 47±40 ind.m-2 respectively), and by the
amphipod Haustorius arenarius (26±7 ind.m-2). Bathyporeia pelagica was also
found at this part of the intertidal zone (2±1ind.m-2). Ophelia bicornis was the
most common member of the polychaeta group at the Rt (19±6 ind.m-2) and D
zones (18±9 ind.m-2).
O y
L i
L g r
B e
L a r
S vB k
L gZ
H
P
O
S P
X g
X v
E sV
T
A
S tre s s : 0 ,1 5
L a rH
L g r
L g
L iO y
B eOZ
S v
B kTP
S PX v
X gA
E sV
2 0 4 0 6 0 8 0 1 0 0
B r a y C u r t i s S i m i l a r i t y
w e s t e r n
b e a c h e s
e a s t e r n
b e a c h e s
a) b)
western beaches
eastern beaches
Chapter 3 Community structure
102
Figure 3. Histograms showing intertidal variability as total abundance (density values
per m2) of the macroinfauna (averaged from all the nineteen beaches).a) Macroinfauna
species found in the saturation zone of the beaches b) Macroinfauna species from the
resurgence and retention part of the beaches (Donax trunculus was found in both
levels). c) Macroinfauna species from the dry upper zones of the beaches. d) Cirolanid
isopods of the genus Eurydice (mean abundances) were found to span throughout the
intertidal. Values of total averaged density and number of species found in all the
nineteen beaches were also plotted.
Cum
opsis
fagei
Dis
pio
sp
Drilo
nere
is f
ilum
Eocum
a d
ollfu
si
Gastr
osaccus s
pin
ifer
Gastr
osaccus s
anctu
s
Hid
robia
ulv
ae
Nephty
s c
irro
sa
Spio
phanes b
om
byx
Scole
lepis
squam
ata
Ponto
cra
tes a
renarius
Avera
ged d
ensity (
ind.m
-2)
0
25
50
75
100
125
150
175
200
Port
um
nus la
tip
es
Sphaero
ma r
ugic
auda
Angulu
s t
enuis
Donax t
runculu
s
Bath
ypore
ia p
ela
gic
a
Hausto
rius a
renarius
Ophelia
bic
orn
is
Avera
ged d
ensity (
ind.m
-2)
0
20
40
60
80
100
120
140
a) b)
c) d)
Eury
dic
e p
ulc
hra
Eury
dic
e a
ffin
is
Tota
l density
n s
pecie
s
Avera
ged d
ensity (
ind.m
-2)
0
250
500
750
1000
1250
1500
1750
2000
2250
2500
Tylo
s e
uro
paeus
Talo
rchestia
deshayesii
Talo
rchestia
brito
Talitr
us s
altato
r
Avera
ged d
ensity (
ind.m
-2)
0
10
20
30
40
50
60
Chapter 3 Community structure
103
Figure 4. Distribution of the macroinfaunal densities and biomass of the main species
in morphodynamic type intermediate beaches on the north coast of Spain. Density
values are expressed in ind.m-2 and biomass values in g.m-2 (averaged from all the
nineteen beaches). Lines separate the physical zones of the intertidal (sensu Salvat
1964); D = dry zone; Rt= retention zone; Rs = resurgence zone; S = swash zone).
The Resurgence (Rs) and saturation (S) zones were also completely
dominated by crustaceans. Cirolanid isopods of the genus Eurydice were once
again the dominant organisms (E. pulchra: 75±33 at Rs and 88±21 ind.m-2 at
S). The amphipod Pontocrates arenarius (17±4 at Rs and 29±8 ind.m-2 at S
zone) and the isopod, Sphaeroma rugicauda (9±2 at Rs and 12±5 ind.m-2 at S)
Sphaeroma rugicauda
Scolelepis squamata
Donax trunculus
Gastrosaccus sanctusOphelia bicornis
Pontocrates arenarius
Haustorius arenarius
Talitrus saltator
Eurydyce pulchra
130
130
35
35
35
35
35
35
35
300Total indiv.
Drilonereis filum
Talorchestia deshayesii
Tylos europaeus
5
5
5
Bathyporeia pelagica
Nepthys cirrosa 5
5
Spiophanes bombyx5
35
S Rs Rt D
Talorchestia brito
Eurydyce affinis
DRtRsS
m above low tide m above low tide
0.25 Total biomass
5
35Number of species
1 42 3 1 42 3
Chapter 3 Community structure
104
were found at this part of the beach. The polychaetes Drilonereis filum (2±0 at
Rs and 1±0 ind.m-2 at S) and carnivorous Nepthys cirrosa (2±1 at Rs and 4±0
ind.m-2 S) were also found at these levels; meanwhile, the spionids Scolelepis
squamata (27±1 ind.m-2) and Spiohpanes bombyx (4±2 ind.m-2) were mostly
abundant toward the swash zone of the beach. Benthoplanktonic mysids of the
genus Gastrosaccus are good indicators of the lower shore, corresponding to
the saturated lower and subtidal parts of the beach. Gastrosaccus sanctus was
restricted to the lowest tidal level (14±1 ind.m-2). Donax trunculus was the
main species representing the Mollusc group from the retention to saturation
levels; the highest abundance was found at the retention zone (11±1 ind.m-2)
and decreasing downshore (5±2 ind.m-2 at Rs).
Biplots resulting from the MDS analysis for total macroinfauna
abundances (Fig. 5) show that macroinfauna assemblages were quite similar in
all the sampled beaches. A measure of goodness-of-fit of the MDS ordination
was given by the low stress value (S < 0.1). All of the beaches appeared to split
into two distinct zones; at least the upper part of the beach (levels 9 and 10,
sometimes with level 8) seems to differ from the lower shoreline levels.
Statistical values of R in ANOSIM analysis indicate the degree of
discrimination between the levels. The R statistic itself is a useful comparative
measure of the degree of separation of sites (Clarke and Warwick, 1994;
Legendre and Legendre, 1998). ANOSIM results, for differences among levels
at each sampled beaches, revealed a significant difference in community
composition between the upper (a) and the lower part (b) of the shoreline
(Table 3). All the beaches sampled showed this simple and clear separation,
and only some of them (San Pedro, Xivares, Vega, Toranda, Oyambre,
Liencres and Laredo) showed a possible third division (b1 for the levels closer
to the dry zone and b2 for the lowest levels downshore) separating the lower
part of the shoreline where Rt, Rs and S levels occur, but without any clear
zonation pattern.
Chapter 3 Community structure
105
2.3.3.4. Relationships between macroinfauna and environmental
variables.
An ordination biplot for the major species of macroinfauna (Fig. 6) was
obtained using Canonic Correspondence Analysis (CCA) to evaluate the
relationship between environmental variables and macroinfauna densities. The
Monte Carlo permutation test showed that the macroinfauna community
changed significantly with beach length (p < 0.001), slope (p < 0.05) and wave
height (p < 0.05) after 1999 permutations. Arrows represent environmental
variables and the length of them shows the importance of each variable (ter
Braak, 1986). The direction of arrowheads represents increasing values for
environmental variables, and the projection of the species onto the arrows
shows the environmental preference of the biota (ter Braak, 1986). This gives
an approximation of the weighted averages of the species with respect to
environmental variables (ter Braak, 1995; Legendre and Legendre, 1998).
These environmental variables explained about 45.8% of the macroinfauna
density variation. The first and second axis, explained by the environmental
variables, accounted for 57% of the species-environment correlations. The sum
of all canonical eigenvalues was 80% (F = 3.076, p< 0.001). The position of the
macroinfauna groups in the biplots reflects the contribution of each group to
the variance explained by the first two axes (ter Braak, 1986). Thus, the
numbers of Scolelepis squamata, Pontocrates arenarius, Gastrosaccus sanctus,
Eurydice pulchra, E. affinis, Sphaeroma rugicauda, Nephtys cirrosa,
Haustorius arenarius, Portumnus latipes and Talitrus saltator were the least
explained by the environmental variables since their positions in the CCA
model were close to the origin (plotted with triangles in Figure 6).
Thus, Donax trunculus reaches the highest densities at beaches with
longer shoreline and with medium-high wave height (Hb) values. Cumopsis
fagei and Bathyporeia pelagica show the highest density values at beaches with
medium-high values of either Hb or beach length. High density values of
Nepthys cirrosa and Portumnus latipes were noted with medium-high Hb
values. Talorchestia brito and Ophelia bicornis show the highest density values
on beaches with low slope values.
Chapter 3 Community structure
106
2.3.4. Discussion
2.3.4.1. Macrofaunal characteristics
The macroinfauna values recorded in the nine eastern beaches (Table
2) seem to be in accordance with the range of values obtained in the ten
western beaches (Rodil and Lastra, 2004) and with those values obtained in
morphodynamic intermediate beaches worldwide (e.g. Defeo et al., 1992;
Jaramillo et al., 1993; McLachlan, et al., 1996, Hacking, 1998). We have found
that macroinfauna abundances (ind.m-2) are significantly higher in the western
than in the eastern beaches, but no difference in biomass or number of species
was found within this geographical gradient.
Molluscs, crustaceans and polychaetes have been reported to be the
three most abundant macrofaunal taxa on sandy beaches worldwide (Pichon,
1967; McLachlan, 1983). Crustaceans (amphipods and isopods) were the most
diverse and abundant group, in abundance and species number, on the beaches
studied here, while molluscs were the least abundant group. The cirolanid
isopod Eurydice pulchra was the most common species occurring on every
beach, spanning the entire intertidal zone. The intertidal distribution of the
majority of macroinfauna species was more restricted than that of Eurydice
pulchra. Most species encountered were concentrated in the lower and middle
levels of the beaches, corresponding to the Saturation and Resurgence beach
zones, with some intrusions into the Retention zone (sensu Salvat 1964).
2.3.4.2. Zonation patterns of the macroinfauna
Several zonation schemes have been proposed for macroinfauna of
sandy beaches (e.g. Dahl, 1952; Salvat, 1964; Pichon, 1967; Trevallion et al.,
1970); but classification and ordination techniques have been recently used to
examine intertidal distributions in many areas of the world (e.g. Donn and
Crockcroft, 1989; McLachlan, 1990; Raffaeli, et al., 1991; Defeo, et al., 1992;
McLachlan, et al., 1996; McLachlan et al., 1998).
Chapter 3 Community structure
107
A1A
2
A3
A4A
5
A6
A7
A8
A9
A10
2D
Str
ess: 0.0
5
BK
1
BK
2B
K3
BK
4
BK
5
BK
6
BK
7B
K8
BK
9B
K10
2D
Str
ess: 0.0
9
BE
1BE
2
BE
3
BE
4B
E5
BE
6
BE
7 BE
8B
E9
BE
10
2D
S
tress: 0.03
H1H
2
H3
H4
H5
H6H7
H8
H9
H10
2D
Str
ess: 0.0
4
LG
1LG
2LG
3
LG
4LG
5LG
6
LG
7
LG
8
LG
9
LG
10
2D
Str
ess: 0.0
3
ES
1E
S2
ES
3E
S4
ES
5E
S6
ES
7E
S8
ES
9E
S10
2D
Str
ess: 0.0
1
LG
R1
LG
R2
LG
R3
LG
R4
LG
R5
LG
R6
LG
R7
LG
R8
LG
R9
LG
R10
2D
S
tress: 0.01
LR
1
LR
2
LR
3
LR
4
LR
5 LR
6LR
7LR
8
LR
9LR
10
2D
S
tress: 0.06
LI1
LI2
LI3
LI4LI5
LI6
LI7
LI8
LI9
LI1
0
2D
S
tress: 0.04
O1
O2
O3
O4
O5
O6
O7
O8
O9
O10
2D
S
tress: 0.06
OY
1
OY
2O
Y3
OY
4O
Y5
OY
6O
Y7
OY
8
OY
9O
Y10
2D
S
tress: 0.01
P1
P2
P3
P4P5
P6
P7
P8
P9
P10
2D
S
tress: 0.04
SV
1S
V2
SV
3S
V4
SV
5
SV
6S
V7
SV
8
SV
9S
V10
2D
S
tress: 0.03
SP
1S
P2
SP
3S
P4
SP
5S
P6
SP
7S
P8S
P9
SP
10
2D
S
tress: 0.01
TO
1
TO
2T
O3
TO
4T
O5
TO
6
TO
7T
O8
TO
9
TO
10
2D
S
tress: 0.08
VG
1V
G2
VG
3V
G4
VG
5
VG
6
VG
7
VG
8V
G9
VG
10
2D
S
tress: 0.05
XV
1
XV
2X
V3
XV
4X
V5
XV
6XV
7
XV
8
XV
9
XV
10
2D
Str
ess: 0.0
5
Z1
Z2
Z3
Z4
Z5
Z6
Z7
Z8
Z9
Z1
0
2D
Str
ess: 0
XG
1
XG
2 XG
3X
G4
XG
5
XG
6
XG
7
XG
8
XG
9
XG
10
2D
S
tress: 0.08
ba a
b
a
b
b
a
ab
a
b2
b1
a
b
b
a
a
b2
b1
a
b
bb
2
b1
a
b
a
b2
b1
b
b
a
a
b
b
b2
b1
b
a
a
b
a
b
bab
a
Fig
ure
5.
Bip
lots
result
ing
fr
om
th
e
mu
ltid
imen
sio
nal
scali
ng
analy
sis
o
f th
e
macro
infa
una (d
ensit
y valu
es exp
ressed
as in
d.m
-2) b
each
zo
nati
on o
n each b
each.
Lett
ers i
nd
icate
beach
nam
es (
as i
n F
igure 2
) w
hil
e n
um
bers r
ep
resent
sam
pli
ng l
evels
(1
-10
).L
ett
er “a” gro
up
up
per b
each le
vels
and
“b
” th
e rest
of
the d
ow
nsho
re le
vels
.
Furth
er d
ivis
ion (b
1 and
b
2) rep
resents
p
ro
bab
le zo
nati
on d
ow
nsho
re (see T
ab
le 3
fo
r
sig
nif
icant
co
rrela
tio
ns).
Chapter 3 Community structure
108
The beaches that we studied along the northern coast of Spain (Rodil
and Lastra, 2004) showed a broken profile roughly separated by mean sea level
into an upper steep beach, followed by a lower flat downshore, as was
previously found in Scottish beaches (Eleftheriou and Nicholson, 1975) and on
the North West coast of Spain (de la Huz, pers. comm.). The main consequence
of this profile is that the Rs level covers a broad zone of the beaches, which is
characterised by high macroinfauna abundance. Moreover, this situation does
not help to make a clear separation between Rs and Rt zones on some of the
sampled beaches, and these levels seem to be the same on some beaches, such
as Zarautz, Langre and Espasa.
Sharp boundaries in macroinfauna zonation were not found in these
beaches; zonation on sandy beaches has been considered as an artificial
division of a continuum, with overlap between adjoining zones (Degraer et al.,
1999). The intertidal distribution of the macroinfauna on the sandy beaches
studied here showed a great complexity since most common species are able to
occupy different tidal levels with a variety of conditions. However, we found
some evidence for the occurrence of major biological zones on the
beaches sampled. Histograms (Fig. 3) and kite diagrams (Fig. 4) representing
the intertidal distribution of the macroinfauna and the multivariate analysis
(Fig. 5) showed that intertidal zonation was not clear in the beaches studied and
it was not possible to fit our results with the previously described general
patterns of zonation on sandy beaches (Dahl or Salvat’s zonation). The
ordination analysis found two zones with clear separation between supratidal
levels (9 and 10, occasionally including level 8) and the lower beach levels.
The high shore zone was clearly evident as a group, and MDS analysis
indicated a boundary between high and low shore assemblages for these
beaches; apart from this, other major biological zones were difficult to discern
(Fig 4). Our results suggest that intermediate beaches with this particular
profile generally display a typical macroinfaunal zonation divided into two
main zones: a narrow high-shore assemblage of air-breathing species below
which there is a wide zone of water-breather species (e.g. Brown and
McLachlan 1980). The special profile of the intermediate sandy beaches
Chapter 3 Community structure
109
studied here seems to fit well with this zonation scenario. Rafaelli et al., 1991
found the same zonation trend on Scottish beaches. We believe that is not
possible to establish a clear delimitation pattern in the lower part of the
intertidal for beaches with this particular profile, even though the ordination
and clustering analyses identify two possible different zones within the lower
beach part (b1 closer to the supralittoral levels of the beach and b2 in the lower
part) on a few of the beaches studied (San Pedro, Xivares, Vega, Toranda,
Oyambre, Liencres and Laredo). In general, this separation is much less
marked than that found between the upper (a) and lower zones (b1 and b2).
Thus, although we can elucidate a trend in some of the beaches for lower shore
zonation, the general pattern showed that zonation appeared unclear and
blurred in the lower shore levels (McLachlan and Jaramillo, 1995).
The zonation patterns described for intermediate beaches of Northern
Spain could be roughly related to Dahl’s scheme (1952), with a supralittoral
zone dominated by talitrid amphipods, considered indicative of the
subterrestrial fringe on exposed sandy beaches (McLachlan, 1983; McLachlan,
1988; Defeo et al., 1992; McLachlan et al., 1998). The intertidal zone, which
includes Rt and Rs zones, has a diverse macroinfauna, mainly cirolanid isopods
and haustoriid amphipods, and includes a lower saturation zone, directly
affected by the swash climate, where the spionid Scolelepis squamata and the
mysid Gastrosaccus sanctus occur. These species or congeners are frequently
found in the swash environment of most of the beaches studied worldwide
(Hayward and Ryland, pers. comm.; McLachlan, et al., 1981; McLachlan et al.,
1998). The lower zone of the studied beaches also harboured the highest
species richness and the highest abundances. This is a characteristic found on
the lower shore of sandy beaches in the United States (McLachlan, 1990),
South Africa (Bally, 1983; Wendt and McLachlan, 1985) and Chile (Jaramillo,
et al., 1993). Different works suggest a positive relationship between
abundance (density per m2) and species richness of macroinfauna and water
content of the sediment (Bally, 1983; Wendt and McLachlan, 1985; Defeo, et
al., 1992).
Chapter 3 Community structure
110
Ea
ster
n b
each
esO
YL
iL
gr
Be
Lr
Sv
Bk
Lg
ZH
R%
R%
R%
R%
R%
R%
R%
R%
R%
R%
Glo
bal
tes
t R
0.9
72
0.1
**0
.75
63
.6*
0.9
98
2.2
*0
.71
40
.5*
0,8
0.2
**-
--
--
--
--
-
Bea
ch l
evel
s
a-b
0.8
97
2.2
*0
.60
32
.2*
--
--
0.8
36
2.2
*0
.58
70
.5**
0.5
87
0.5
**0
.89
30
.8**
0.6
38
2.2
*0
.91
42
.2*
a-b
10
.99
84
.8*
0.8
13
3.6
*-
--
-0
.97
93
.6*
--
--
--
--
--
b1-b
20
.93
81
.8*
0.7
53
.6*
--
--
0.6
46
3.6
*-
--
--
--
--
-
Wes
tern
bea
ches
PO
SP
Xg
Xv
Es
Vg
To
A
R%
R%
R%
R%
R%
R%
R%
R%
R%
Glo
bal
tes
t R
--
--
0.9
48
0.1
**
--
0.8
40
.1**
--
0.7
63
0.6
**
0.7
82
0.2
**
--
Bea
ch l
evel
s
a-b
0.9
78
2.2
*0
.71
62
.2*
0.6
72
2.2
*0
.79
72
.2*
0.8
52
.2*
0.7
56
2.2
*0
.60
31
.7*
0.8
36
2.2
*0
.95
72
.2*
a-b
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Chapter 3 Community structure
111
-1.0 1.0
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Bath
SphaerE pulE aff
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Figure 6. Biplot resulting from the Canonical Correspondence Analysis. Full line
arrows for the environmental variables. Circles for the species most affected by
environmental parameters. The least affected species were plotted with triangles. Data
obtained from the averaged abundance values for all the beaches. (Talorc: Talorchestia britto, Ophelia: Ophelia bicornis, Gast: Gastrosaccus sanctus, Neph:
Nephtys cirrosa, Port: Portumnus latipes, Donax: Donax trunculus, Bath: Bathyporeia pelagica,
Cumop: Cumopsis fagei, Haut: Haustorius arenarius, Scolp: Scolelepis squamata, Sphaer:
Sphaeroma rugicauda, Talit salt: Talitrus saltator, E pul: Eurydice pulchra, E aff: Eurydice
affinis).
Some of the species of sandy beach macroinfauna exhibit some degree
of differential zonation of size classes worldwide (e.g. Dexter, 1977; Haley,
1982). Donax trunculus was found to show zonation by size on the Atlantic
coast (Ansell and Lagardère, 1980; de la Huz et al, 2002), with the smallest
individuals highest on the shore, and the largest confined to the lower saturated
zone in several temperate shorelines. The result of having the high numbers of
Donax trunculus at the Rt zone of the sampled beaches (11±1 ind.m-2) could be
related to the preference and zonation pattern of this species in the intertidal
zone. This also has been shown in other latitudes with Donax serra (Lastra and
McLachlan, 1996; Soares et al., 1996). Medium grain size showed a decrease
Chapter 3 Community structure
112
in all the nineteen intermediate sandy beaches at the upper part of the shoreline
(see Results section) which could explain this intraspecific zonation due to the
sediment preference (de la Huz et al., 2002).
2.3.4.3. Relationships between macroinfauna and environmental
variables.
Macroinfauna abundance and distribution in sandy beaches depend on
several physical and biological factors. Studies on United States, Australia and
South African sandy shores (McLachlan et al., 1993) and beaches from Chile
(Jaramillo and McLachlan, 1993) suggest that beach face slope and mean grain
size were the dominant patterns in community composition. Thus, there is a
general trend of decreasing species richness with increasing particle size and
beach face slope (steeper beaches), and increasing from reflective to dissipative
conditions. Short (1996), suggested that variables such as wave height and
period, sand size, beach slope and embayment dimensions can provide the key
elements in a global sandy beach classification. Furthermore, McArdle and
McLachlan (1992) suggested beach slope and wave height as the most
important factors controlling swash climate. Thus, swash climate on the beach
profile is the most important aspect of the environment by animals inhabiting
exposed sandy beaches, as McLachlan et al. (1993) subsequently refined in
their “swash exclusion hypothesis”. The pioneering studies carried out on
intermediate beaches on the northern coast of Spain found no significant trends
between the swash climate or the morphodynamic state with the macroinfauna
(Rodil and Lastra, 2004), confirming that communities in this type of beach are
controlled by several ecological factors rather than by a single key factor
(McLachlan et al., 1996; Brazeiro, 2001).
Mean grain size and beach face slope showed no significant variation
along the West to East beach gradient. In spite of the geographical continuum
formed by all the sampled beaches, water mass characteristics along the North
coast of Spain are determined by variations in coastal productivity at different
spatial scales. We believe that macroinfauna differences (ind.m-2) found
between the two groups of beaches arise from the chlorophyll-a concentration
Chapter 3 Community structure
113
gradient rather than from physical differences between beaches. The existence
of the upwelling event that is common along the eastern boundary of the North
Atlantic between 10º and 44ºN (Wooster et al., 1976) and focused in the North
west coast of Spain (Molina, 1972) can be involved in this gradient. Upwelling
favourable winds tend to increase the residual flows into the estuaries and rías
(Blanton et al., 1984; Prego and Fraga, 1992) and, consequently, the net influx
of nutrient-rich deeper water. Chlorophyll-a is a good index of the
phytoplankton concentration and food availability in the water column (Menge
et al., 1997). This fertilization leads to the high primary production, which
results in benthic enrichment (López-Jamar et al., 1992) and seems to dilute
when we move eastern through the North coast of Spain (Fernández and Bode,
1991; Teira et al., 2001; Lastra et al., 2006). Thus, it could be argued that
proximity to such upwelling areas leads to higher macroinfaunal abundance
values because of greater food availability due to the increase in productivity.
Canonical analysis (Fig. 6) indicates that environmental parameters
such as slope, beach length (long) and wave height (Hb) are the most important
factors explaining variability in the species density. In general terms, there is a
negative correlation between macroinfauna density and increasing beach face
slope, while no positive correlation with grain size was found. Species whose
density was not well explained by the environmental variables (found close to
the axis origin in Fig. 6) were generally found spanning the whole beach profile
(Figs. 3 and 4). Species broadly ordinated along the first CCA axis (Donax
trunculus, Bathyporeia pelagia and Cumopsis fagei) were found mainly at the
Rt and Rs zones (Fig. 4) and positively correlated with beach length and wave
height (Fig. 6). Other species such as Talorchestia brito and Ophelia bicornis,
found mainly at the upper levels, reached higher density values in beaches with
lower values of the three environmental variables (Fig. 6). The species with the
clearest zonation had the most significant relations with the environmental
variables. An increase in beach length together with more dissipative
conditions (low slope and high wave height) seems to affect these species
positively. Talitrus saltator was another invertebrate harbouring the upper part
of the beach but, in this case, no relations were found with any of the
Chapter 3 Community structure
114
environmental variables in the CCA. It seems that this kind of amphipod is not
affected by morphodynamic conditions. The abundances of Donax trunculus,
which also showed an intraspecific zonation, Bathyporeia pelagica and
Cumopsis fagei, which were found mainly at the lowest part of the shore, were
well explained by wave height and beach length but were not well explained by
beach slope. In general terms, variations in the environmental variables and
particular conditions of the beaches will affect macroinfauna densities and
distribution; but it seems that the species most affected by the environmental
variables were also those that showed more distinct zonation. Thus,
supralittoral macroinfauna was the least affected by the beach type while
species harbouring the lower levels, dependent on the swash regime, were more
affected by the main environmental variables.
In conclusion, macrofauna on intermediate exposed sandy beaches
from this geographical area showed no clear intertidal zonation, even though
they had two zones in common: a supralittoral zone (dry zone) and a littoral
zone. Subdivision of the lower part including Rt, Rs and S zones cannot be
clearly established. Community characteristics are affected by physical factors.
Beach length, slope and wave height were found to be the main variables
affecting macroinfauna on intermediate beaches, as previous works have
suggested. But it seems that the species with the clearest zonation were found
to be the best explained by the environmental variables than species with no
sharp boundaries in their distribution along the beach profile. Furthermore, it
seems that community characteristics in the beaches studied are not just, but
also by other factors dependent on oceanographic conditions and coastal
processes, determining critical characteristics such as water temperature and
food availability.
Acknowledgments
We would like to thank K. Aerts for helping with laboratory work and
C. de la Huz, M. Incera, J. López, M. Pita, G. Rodríguez, S. Cividanes and R.
Costas for field assistance. We also thank Dr. J.G. Rodríguez for critically
reading the manuscript and valuable comments and to the anonymous referees
Chapter 3 Community structure
115
who redirected the content of the original manuscript. Thanks also to Ian
Emmett for language revision. This research initiative was supported by the
University of Vigo (64102C859) and the Government of Galicia (XUGA
30105A98).
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PART III. THE IMPORTANCE OF EXPOSURE ON
SANDY BEACH MACROFAUNA: HYDRODINAMIC
CONDITIONS AND FOOD AVAILABILITY.
“What a trifling difference must often determine which shall survive,
and which perish!”
-Charles Darwin
letter to Asa Gray
Content:
Rodil, I.F., Lastra, M. and López, J. 2007. Macroinfauna community
structure and biochemical composition of sedimentary organic matter
along a gradient of wave exposure in sandy beaches (NW Spain).
Hydrobiologia 579: 301-316.
Chapter 4. Macroinfauna community structure and
biochemical composition of sedimentary organic matter
along a gradient of wave exposure in sandy beaches (NW
Spain).
Rodil, I.F., Lastra, M., and López, J.
Published in Hydrobiologia (2007). 579:301-316
Chapter 4 Community structure and biochemical composition
122
Abstract
Six sandy beaches on the North West coast of Spain, exposed to
different wave action, were sampled in order to study the macroinfauna
community and the biopolymeric fraction (proteins, lipids and carbohydrates)
of sedimentary organic matter. According to McLachlan’s rating system
(1980), three of them were classified as sheltered and the other three as
exposed beaches. Sampling was carried out during August 2004 at three tidal
levels: high, medium and low. Macroinfauna community and organic matter
concentrations were found to be significantly different when sheltered and
exposed beaches were compared. Macroinfauna diversity (H’), abundances and
biomass became increasingly enriched along a gradient from exposed to
sheltered beaches. Macroinfauna mean abundance was found higher in
sheltered (ranked from 1535±358 to 15062±5771 ind m-2) than in exposed
beaches (from 150±41 to 5518±1986 ind m-2). Macroinfauna biomass ranged
from 3.2 to 14.7 g m-2 and species richness from 25 to 27 in sheltered localities;
while in exposed beaches, biomass ranged from 0.2 to 2.3 g m-2 and the number
of species from 5 to 14. The biopolymeric carbon concentration (BPC) was
significantly higher in sheltered (from 84.7±44.7 to 163.3±34.8) than in
exposed (from 30.3±7.5 to 78.7±12.3) beaches. The low hydrodynamic
conditions of sheltered beaches favoured the settlement of organic rich fine
sediments, being supported by the higher protein to carbohydrate ratio found in
the exposed (from 23.5±0.9 to 32.7±4.4), rather than in the sheltered localities
(from 6.2±0.7 to 13.6). Mean macroinfauna abundances were higher at medium
and low tidal levels in both sheltered and exposed beaches. Crustacea was
found to be the main group inhabiting the upper part of both types of beaches,
dominating all tidal levels of exposed sandy beaches. Mollusca and Polychaeta
groups were dominant in sheltered beaches at the medium and lower levels.
There was a significant negative relationship between the BPC and the beach
face slope; thus, BPC decreased as the intertidal slope increased. It seems that
exposed sandy beaches are mainly physically-controlled; whereas hospitable
Chapter 4 Community structure and biochemical composition
123
sheltered beaches let other factors, such as biochemical compounds enrich the
benthic fauna scenery.
Keywords: sandy beaches; exposure gradient; macroinfauna;
biochemical composition of sedimentary organic matter; biopolymeric fraction;
intertidal sediments.
3.4.1. Introduction
Sandy beaches are the most dynamic systems of soft bottom habitats
and the most widely distributed intertidal ecosystem, dominating both
temperate and tropical shores. Ecological studies in sandy beaches mostly dealt
with the faunal community structure and their relationship with environmental
conditions (such as wave energy and sand particle size).
It is generally admitted that biological richness, abundance and
biomass differ along a gradient of exposure rating (McLachlan, 1983;
McLachlan et al., 1996). The macrofauna of sandy beaches includes most
major invertebrate taxa, although it has been recognized that Bivalvia,
Crustacea and Polychaeta are the dominant groups (Brown and McLachlan,
1990). There is a trend for crustaceans to be more abundant in exposed beaches
and molluscs to be more abundant in the sheltered intertidal (McLachlan,
1983), although there are many exceptions (Dexter, 1983). In exposed
environments, intertidal fauna is mainly controlled by physical conditions
(McLachlan et al., 1993); it is suggested that the major hydrodynamic stress of
exposed localities limits their biological richness (McLachlan et al., 1996) and
several ecological factors influence the different community variables rather
than a single key factor (Brazeiro, 2001; Rodil and Lastra, 2004). In contrast,
higher macroinfauna abundance, biomass and diversity are found in sheltered
sedimentary environments (Adam, 1990) where biological interactions become
more important due to the higher species number and the higher proportion of
specialists found in those zones (Brown and McLachlan 1990).
It has been shown that food availability is one of the main factors
affecting community structure and benthic metabolism (Pearson and
Rosenberg, 1987; Grant and Hargrave, 1987; Thompson and Nichols, 1988;
Chapter 4 Community structure and biochemical composition
124
Graf, 1989; Dugan et al., 2003). However, little is known about the amount of
food available on the intertidal sediment and its relationship with the
macroinfauna community. Several studies have shown the strong relation
between food availability and the biochemical composition of organic matter
(e.g. Tenore and Hanson, 1980; Danovaro et al., 1993). This biochemical
composition is the result of the equilibrium between external inputs,
autochthonous production and heterotrophic utilisation (Fabiano and Danovaro,
1994). The organic matter plays a major role within the detritus food chain. In
fact, the quality and quantity of organic matter in surface sediments are
recognised as primary nutritional sources affecting benthic fauna dynamics and
metabolism (Brown and McLachlan, 1990; Grant and Hargrave, 1987, Graf,
1989; Fabiano et al., 1995; Colombini et al., 2000). Food resources are one of
the most probable explanations for marine population patchiness (Decho and
Fleeger, 1988); thus, changes of sedimentary organic matter in marine
environments will affect spatial distribution, metabolism and dynamics of all
benthic organisms, from bacteria to macrofauna (Grant and Hargrave, 1987;
Graf, 1989; Duineveld et al, 1997). Organic matter in marine environments is
composed of labile and refractory compounds; however, only the former have
been used to estimate the nutritional value of the sediment (Buchanan and
Longbottom, 1970) because they consist of simple sugars, proteins and fatty
acids that are easily mineralised by bacteria and thus potentially available for
higher trophic levels (Fichez, 1991; Danovaro et al., 1993). Several studies
have estimated the fraction of sedimentary organic matter available for
consumers through the determination of biochemical classes of organic
compounds (i.e. carbohydrates, proteins and lipids), which are assumed to be
easier to digest and assimilate (Fichez, 1991; Danovaro et al., 1993; Fabiano et
al., 1995; Dell’Anno et al., 2000). The large amount of organic matter reaching
the sediments in sheltered intertidal areas are expected to induce a significant
benthic response (Josenfson and Conley, 1997), which could partially explain
the high abundance and diversity of the macroinfauna in these environments
compared to exposed intertidal sediments. Recent studies have pointed out that
the labile fraction of sedimentary organic matter can be used to describe the
Chapter 4 Community structure and biochemical composition
125
trophic state and organic enrichment of marine coastal ecosystems (Dell’Anno
et al., 2002). There is a lack of information concerning the biochemical
composition of intertidal sediments and its direct relation with benthic
macrofauna. Most of the studies of macroinfauna community in sandy beaches
do not include detailed information of the biochemical composition from the
sediment and the influence of this variable on the distribution and abundance of
species. Recently, the origin and biochemical composition of organic matter
have been proposed as one of the key factors, together with the physical
environment (McLachlan, 1990), for the control of the beach fauna (Incera et
al., 2003).
In this paper, we analysed the macroinfauna structure and composition
of sedimentary organic matter over a range of intertidal sediments exposed to a
different degree of wave action (from sheltered to exposed). The aims of this
study are to investigate: (1) the influence of the physical characteristics on the
intertidal macroinfauna community along a gradient of wave exposure; (2) the
biochemical variability of the sedimentary organic matter in beaches with
different hydrodynamic conditions, and also (3) the relationship between
biochemical composition of the sedimentary organic matter and macroinfauna.
3.4.2. Material and methods
3.4.2.1. Study area
Six sandy beaches located on the northwest coast of Spain (Fig. 1) were
sampled during the low spring tides of August 2004. These localities are
influenced by a mesotidal regime with a mean tidal range of ca. 3 m.
According to their geographical situation in the ría system (sensu Méndez and
Vilas, 2005), these sandy beaches were subject to a different degree of wave
exposure. Three of them, namely Broña, Bornelle and Cabanas, located in the
inner part of the ría (from 42º 46’ to 42º 49’ N and from 8º 55’ to 9º 1’ W) were
characterised by low exposure conditions. According to the 20-point rating
system proposed by McLachlan (1980), this group was considered as sheltered
beaches. The others, namely Xeiruga, Baldaio and Niñóns, located in the outer
Chapter 4 Community structure and biochemical composition
126
part of the ría (from 43º 17’ to 43º 18’ N and from 8º 40’ to 8º 54’ W) were
characterised as exposed beaches (McLachlan, 1980).
Figure 1. Location of the study area and localities sampled on the northwest coast of
Spain.
3.4.2.2. Sampling design
Sampling was carried out at six replicated transects (in triplicate),
randomly separated, at the central area of each beach, after ebbing, at three
tidal levels (high, medium and low). Following the traditional sandy beach
zonation; high level correspond to Salvat’s dry zone (1964) and Dhal’s
supralittoral fringe (1952); medium level correspond to Salvat’s retention zone
and Dhal’s midlittoral zone and low level correspond to Salvat’s saturation
N iñó ns X eiruga
Ca ba na s
Broñ a
Born el le
Ba lda io
Chapter 4 Community structure and biochemical composition
127
zone and Dahl’s sublittoral zone. Macroinfauna samples were collected with 25
cm diameter metal corer penetrating 15 cm depth into the substrate. The
sediment was sieved through 1 mm mesh and the residue was preserved in 4%
formalin. The individuals were later sorted from the sediments, identified and
counted in the laboratory. Shell-free biomass of all the species was determined
by drying at 100ºC for 24 hours and then 500ºC for 6 hours, obtaining ash free
dry weight values.
Three sediment samples were collected by hand coring from sediment
surface down to 15 cm depth at the three tidal levels. Each sediment sample
was mixed and subsamples were taken for the analysis of lipids, proteins and
carbohydrates. All subsamples were frozen at -30ºC until further processing.
Moreover, three samples of sediment for grain size analyses and water content
were also collected at each tidal level by inserting a 3 cm diameter corer to a
depth of 15 cm. Shear strength (kPa) of saturated sediments was also
determined with a shear vane tester and measurements were carried out in the
upper 5 cm of the sediment. Grain size analysis was carried out by means of a
Coulter Counter LS200. Beach slope (Slope=1/R; R=intertidal width/ height of
the high intertidal level) estimated for the entire beach was determined by
Emery’s profiling technique (Emery, 1961). Wave height and wave period
were estimated in order to calculate dimensionless Dean’s parameter (Ω)
according to Short and Wright (1983) and Beach State Index (BSI) according
to McLachlan et al., 1993 was also calculated. Finally, the new beach index
(BI) formulated by McLachlan and Dorvlo (2005) was calculated as follows:
[BI = log10 (Mz x TR)/ S]; where TR is the tidal range, S is the beach slope and
Mz is the mean sand particle size expressed in (phi units + 1), to avoid negative
values (McLachlan and Dorvlo, 2005).
3.4.2.3. Biochemical analysis.
All data were normalized to sediment dry weight after desiccation
(60ºC, 24 h) and finely powdered with a pestle (Pulverisette 2, Fritsch). Total
proteins (PRT) were determined using the method of Lowry & Rosebrough
(1951) modified by Markwell et al. (1978). Concentrations are referred as
Chapter 4 Community structure and biochemical composition
128
bovine serum albumin (BSA) equivalents. Total carbohydrates (CHO) were
analysed according to Dubois et al. (1956) and expressed as glucose
equivalents. Total lipids (LIP) were extracted from dried samples using
chloroform and methanol solution according to the method of Bligh and Dyer
(1959) and Marsh and Weinstein (1966) and measured as tripalmitine
equivalents. All analyses were carried out on three replicates (about 0.5-2.5 g
of sediment was used for each analysis). For each biochemical analysis, blanks
were made using the same sediments previously treated in a muffle furnace
(500ºC 6 h).
Protein, carbohydrate and lipid concentrations were converted into
carbon equivalents, using 0.49, 0.40 and 0.75 conversion factors, respectively
(Fabiano et al., 1995). Biopolymeric carbon concentration (BPC) was
calculated according to Fabiano and Danovaro (1994) as the sum of proteins,
carbohydrates and lipid converted to carbon equivalents according to Fichez,
1991. The BPC is considered a reliable estimate of the fraction of total organic
matter readily available to benthic consumers (Fabiano et al., 1995). Protein to
carbohydrate ratio (PRT:CHO) was also calculated and assumed as an
estimation of organic material ageing (Fabiano et al., 1997).
3.4.2.4. Data analysis.
Pearson’s correlation and regression analysis were carried out to test
for relationships between biotic and abiotic variables in all the beaches.
Macroinfauna community and organic matter content were assessed by a two-
way ANOVA analysis, with exposure (sheltered vs. exposed) and tidal levels
(high, medium and low) as factors (Sokal and Rohlf, 1995). When a significant
difference was observed (p<0.05), a Tukey’s pairwise comparison test was also
performed to elucidate possible differences between levels of a factor
(exposition rate and tidal levels). The relationship between BPC and exposure
rate across tidal level was determined by ANCOVA. All these statistical
analysis were performed using SPSS version 12.0.
Primary description of faunal assemblages at high taxonomic level was
performed by normalizing the proportion of the relative abundances of the main
Chapter 4 Community structure and biochemical composition
129
invertebrate taxa; i.e., Crustacea, Mollusca and Polychaeta, were plotted on
ternary graphs arranged as an equilateral triangle with scatter and lines.
Non-metric multidimensional scaling ordination (MDS), with the Bray-
Curtis similarity index, was performed to describe possible changes on the
macroinfauna community between exposed and sheltered beaches and among
different beach tidal levels. Measurement of goodness-of-fit of the MDS
ordination was given by the stress value (S); where low stress factor (S<0.2)
corresponds to a good ordination with no real prospect of a misleading
interpretation (Clarke and Warwick, 1994). The presence of highly abundant
species was standardized with a double square root transformation. Pairwise
analysis of similarities (ANOSIM, Clarke 1993) was carried out to test the null-
hypothesis that there were no differences (at α = 0.05) in the composition of the
macroinfaunal assemblages at different beaches (sheltered vs. exposed) and at
different tidal levels. The nature of the community groupings identified in the
MDS ordinations was further explored by applying the similarity percentages
program (SIMPER), to determine the contribution of individual species to the
average dissimilarity between type of beaches (exposed vs. sheltered) and tidal
levels (Clarke, 1993; Clarke and Warmick, 1994). These analyses were
performed using the PRIMER 5 software package.
3.4.3. Results
3.4.3.1. Physical environment
The profile and the beach face slope for each locality are shown in
Figure 2. Beach profile showed reflective conditions in the exposed group of
beaches (Xeiruga, Baldaio and Niñóns), being narrower and steeper than in
sheltered localities (Broña, Bornelle and Cabanas) (t6=2.83, p<0.05). A full
characterization of physical variables and indices of the sandy beaches
analysed are provided in Table 1. The values of the dimensionless Dean’s
parameter, categorized Broña, Bornelle and Cabanas as reflective (Ω<1) and
Xeiruga, Baldaio and Niñóns as intermediate-reflective (1<Ω<2) in
morphodynamic state. BSI classification included all the beaches in the
Chapter 4 Community structure and biochemical composition
130
intermediate morphodynamic state (0.5<BSI<1) and new BI index classified all
the localities studied as mesotidal intermediate beaches (B.I.>2).
Figure 2. Intertidal beach slope of the studied localities. S: beach slope (intertidal
width/height of the high intertidal level).
The mean grain size (M.G.S.) values obtained in sheltered localities
presented finer grain sand (from 241 to 294 μm) than the exposed intertidal
localities (from 389 to 571 μm) (t6=2.97, p<0.05). Swash amplitude was higher
(from 4 to 8 m) and shear strength was significantly lower (from 3.6 to 5.4
KPa) in the exposed localities (t6=2.8, p<0.05). There is a significant linear
correlation between exposure rate and medium grain size (M.G.S.= 44.65 x
Exposure -123.7; R2=0.740, p<0.05) and Shear strength (Shear strength= 16.4 –
0.88 x Exposure; R2=0.666, p<0.05). Sediment water content decreased
significantly with increasing tidal level (two-way crossed ANOVA F=20.7,
p<0.01; R2=0.704) and Tukey’s post hoc test showed that differences occurred
Distance from low tide level (m)
0 40 80 120 1600
2
4
6
8
Broña
S = 1/27
0
2
4
6
8Xeiruga
S = 1/22
Cabanas
S = 1/30
Bornelle
S = 1/70
Heig
ht
ab
ove lo
w t
ide level (m
)
0
2
4
6
8Baldaio
S = 1/14
Niñóns
S = 1/12
0 40 80 120 160
Chapter 4 Community structure and biochemical composition
131
between high and low levels (p=0.01) and between high and medium levels
(p<0.01); while no significant water content differences occurred between
medium and low levels and between localities (exposed vs. sheltered).
Table 1. Physical characteristics of the six sandy beaches. a Length of beach. b Width of beach c Mean ± SD of the measured values at each sampled transect. d Mean of the measured values during low tide (n> 30) e Wave height (n>30) f sensu McLachlan´s (1980) rating system (i.e. [wave action, surf zone width,% very
fine sand, median particle diameter and slope, depth of reduced layers, stable
burrows.])
3.4.3.2. Composition and abundance of the macroinfauna
The number of species, mean abundance and biomass (Table 2 and Fig.
3) were found higher in sheltered localities. Number of species was found
significantly higher in sheltered rather than in exposed beaches (Table 3) and
also the interaction between tidal level and exposure rate was found
significantly different (p=0.03) for this variable. Hence, species richness
showed a different pattern of variability between tidal levels in the beaches.
The number of species dropped sharply with decreasing tidal level in the
exposed beaches and rose in sheltered localities (Figure 3). Polychaeta and
Mollusca abundances increased significantly from exposed to sheltered beaches
(Table and Fig. 3). Figure 4 shows mean total abundance (ind m-2) of the main
groups of macroinfauna at each tidal level in the two types of beaches.
Mollusca (p<0.01) and Polychaeta (p<0.05) mean abundances were found to be
significantly higher (Tukey’s post hoc test) at the low part of the beaches rather
than at the upper levels (Fig. 4). Interaction between exposure and tidal level
Beach L (m)a
W (m)b
Slope (1/S) Shear strengthc
M.G.S (μm)c
Swash (m) Ω BSI B.I. Exposure ratingf
T (s)d
Hb (m)e
Broña 490 88 1/27 9.3±1.3 241±18 6.5 0.1 2.5 0.5 0.5 2.41 8 [1,0,2,4,1,0]
Bornelle 550 170 1/70 9.7±0.7 294±24 7.9 0.24 3 0.52 0.52 2.84 10 [0,0,2,7,1,0]
Cabanas 255 100 1/26 6.02±2.0 277±80 5 0.11 3.1 0.59 0.55 2.34 10 [0,0,2,7,1,0]
Xeiruga 490 86 1/22 5.4±2.5 389±76 8.4 0.7 7.6 1.56 0.9 2.27 12 [1,0,2,7,1,1]
Baldaio 3650 55 1/14 3.6±1.9 398±53 8.7 0.7 8 1.33 0.84 2.10 13[1,0,2,7,2,1]
Niñóns 170 50 1/12 5.1±2.0 571±31 6.6 1.1 4 1.89 0.98 2.01 14 [1,1,2,7,2,1]
Waves
Chapter 4 Community structure and biochemical composition
132
was significant for Polychaeta group, meaning that the increase in Polychaeta
abundances was stronger in sheltered conditions (Table 3). The abundance of
macroinfauna is remarkably low at the medium tidal level differing from other
results (i.e. Brown and McLachlan, 1990; Degraer et al., 1999; Janssen and
Mulder, 2005). Biomass values (g m-2) were significantly higher in sheltered
condition, but no differences among tidal levels were found. On the other hand,
mean abundance values did not display significant differences between exposed
and sheltered conditions (Table 3). Sheltered sandy beaches were dominated by
Crustacea at the high tidal levels (99% of the mean total abundance) and by
Polychaeta at medium (84.4%) and low (76.3%) levels. Exposed sandy beaches
were completely dominated by Crustacean at high (100%) and medium
(76.6%) tidal levels, whereas Polychaeta dominated low levels (94.5%).
Mollusca were the less abundant macroinfauna group in all the beaches
sampled and dominated in none of the tidal levels (Fig. 5). Macroinfauna
diversity (H’) was also significantly and inversely correlated with the exposure
rating (H’= 3.46 – 0.142 x Exposure, R2=0.45; p<0.01).
Beach
Species
richness Abundance (ind.m-2)a Biomass (g.m-2) H’b Jc
Broña 25 1535±358 3.2±2 2,9 0.62
Bornelle 26 15062±5771 14.7±11 2,1 0.46
Cabanas 27 5261±1597 7.2±7 2,4 0.5
Xeiruga 8 1475±488 1±0.9 2,2 0.73
Baldaio 5 150±41 0.2±0.1 1,5 0.63
Niñóns 14 5518±1986 2.3±1.9 1,9 0.51 Table 2. Macroinfauna characteristics at the studied beaches.
a Mean’s ± SD of the values at each sampled transect. b Shannon-Wiener diversity index (calculated using neperian logarithms). c Evenness was calculated using Pielou’s J (J = H’/H’max.).
3.4.3.3. Intertidal distribution of the macroinfauna
The one-way ANOSIM (Table 4) found significant differences in
community macroinfauna structure between exposed and sheltered beaches
(global test, p<0.01); significant differences were also found when medium and
low tidal levels were compared between localities (exposed vs. sheltered).
ANOSIM test showed differences in each locality between high and the rest of
Chapter 4 Community structure and biochemical composition
133
the tidal levels (Table 5). MDS ordination analysis of the macroinfauna
community assessed the relationships between localities and tidal levels. High
tidal levels, from both morphodynamic types (exposed and sheltered), were
found closer related than other tidal levels, forming an aggregated group
separated from the rest of the tidal levels sampled (Table 4 and Fig. 6).
Finally, similarity-percentages analysis (SIMPER) of square-root
transformed macroinfauna data, showed that macroinfauna differences between
medium tidal levels from sampled beaches (exposed vs. sheltered) were due to
the high abundance contribution of both Polychaeta, Scolelepis squamata and
Ophelia bicornis (15.5 and 15.2% respectively) in sheltered beaches. The
analysis between lower levels from the localities (exposed vs. sheltered)
showed that the high abundance of the Polychaeta Malacoceros fuliginosa
(18.1%) in sheltered beaches, contributed to the main dissimilarity at this level
(see Appendix A-D, Part III).
3.4.3.4. Organic matter composition
Significant differences were noted in the biochemical compounds
concentrations (i.e. protein, carbohydrate and lipid) between exposed and
sheltered sandy beaches (Table 6). Thus, in the sheltered intertidal sediments,
protein, carbohydrate and lipid concentrations were higher than in the exposed
ones (mean concentrations at the three tidal levels). Proteins were the dominant
compound in both groups of beaches (63.4% and 80.2% for sheltered and
exposed localities respectively), followed by lipids (30 and 17%) and
carbohydrates (7 and 3%). Protein concentrations ranged from 104±38 to
239.5±61 and from 64.7±33.5 to 117.1±49 μg g-1 dry weight (d.w.) in sheltered
and exposed sediments respectively. Carbohydrates ranged from 11.8±4.2 to
22.5±12.5 and from 2.4±1.3 to 4.4±2.1 μg g-1 d. w. and lipid concentrations
ranged from 41.5±40.5 to 114.2±38 and from 16.2±10.8 to 20.3±12.6 μg g-1 d.
w., respectively (Figure 7). PROT:CHO ratio was significantly higher in the
exposed (values from 23.5±0.9 to 32.7±4.4) than in the sheltered
conditions(from 6.21±0.7 to 13.6±5.73).
Chapter 4 Community structure and biochemical composition
134
Figure 3. Mean total macroinfauna abundance (ind m-2) and biomass (g m-2) expressed
as ash free weight dry and species richness in sheltered (closed bars) and exposed (open
bars) localities at the three tidal levels (high, medium and low). Mean ± standard error
(SE) is presented.
Abu
ndan
ce (i
nd m
- 2)
0
5
10
15
A.F
.D.W
. (g
m- 2
)
0
2000
4000
6000
8000
10000
Tidal level
Num
ber
of s
peci
es
0
5
10
15
20
High Medium Low
Chapter 4 Community structure and biochemical composition
135
Table 3. Summary of two-way crossed ANOVA results of exposure (exposed vs.
sheltered) and tidal level (high, medium, low) effect on macroinfauna abundance
(ind.m-2) and biomass (g.m-2).
*Data were converted using a log (X +1) transformation prior to the analysis as
described by Clarke (1993). Bold values indicate significant differences (P < 0.05).
The BPC fraction was found to be significantly higher in the sheltered
intertidal (Table 6) and those values were also found to be higher at the low
than at the high tidal level of the intertidal (p<0.05, Tukey’s post hoc test). No
significant difference was found between medium and low or medium and high
tidal levels. There was a significant negative relationship between BPC mean
concentrations (μg g-1 d.w.) at the three tidal levels and beach slope (S),
meaning that BPC concentrations become increasingly impoverished as the
intertidal slope increased (along the gradient from sheltered to exposed
beaches). Interaction between tidal level and intertidal slope was not significant
[ANCOVA; tidal level effect: F2,11=14.08, p=0.001; intertidal slope
(covariable): F1,11=5.35, p=0.041; tidal level*intertidal slope: F2,11=1.185,
p=0.342 (n.s.)]; thus, the relationship described above was similar in all the
tidal levels analysed in all the beaches. There was also a significant and inverse
correlation between BPC and the exposure rate (BPC=3.35 – 0.13 x Exposure,
R2= 0.723; p<0.05) and a direct correlation between PRTO:CHO and the
exposure rate (PROT:CHO=3.91 x Exposure – 24.63, R2=0.89; p<0.05).
Correlation between PROT:CHO and intertidal slope was found not to be
significant.
Biomass* Crustacean Polychaeta Mollusca Species
abundance* abundance* abundance* richness
F ratio p F ratio p F ratio p F ratio p F ratio p
Exposure 9,34 0.01 0.016 0.9 15.87 0.002 5.91 0.032 72 0.02
Tidal level 0.625 0.55 0.55 0.59 5.12 0.025 9.34 0.004 1.88 0.195
Exp x tid lev 1.02 0.39 0.48 0.62 5.12 0.02 0.81 0.47 4.81 0.03
Chapter 4 Community structure and biochemical composition
136
Figure 4. Mean total abundance (ind m-2) ± SE of the main macroinfauna groups in
sheltered and exposed sandy beaches at the three tidal levels.
Results showed a significant and direct relationship between organic
matter compounds and macroinfauna community (mean values obtained at the
three tidal levels in all the beaches). Thus, there were an increase in
macroinfauna diversity (H’), species richness and in the abundance of some of
Sheltered beaches
Abu
ndan
ces
(ind
m-2
)
0
1000
4000
6000
8000
Exposed beaches
Tidal level
High Medium Low
Abu
ndan
ces
(ind
m-2
)
0
1000
4000
5000
6000 Crustacea
Mollusca
Polychaeta
Others
Chapter 4 Community structure and biochemical composition
137
the taxonomic groups (log transformed data) with proteins [(Species
richness=9.7 + 0.061 x prot; R2=0.23, p<0.05); (Polychaeta abundance=0.01 x
prot. – 0.643; R2=0.61, p<0.01)], carbohydrates [(H’=0.03 x cho + 1.87;
R2=0.437, P<0.01), (Species richness=1.94 – 0.015 x cho; R2=0.61, p<0.01),
(Polychaeta abundance=0.05 x cho – 0.1; R2=0.44, p<0.01)], lipids [(Mollusca
abundance=0.71 + 0.02 x lip; R2=0.31, P<0.05), (Polychaeta abundance = 0.1 –
0.043 x lip; R2 = 0.4, p<0.01)] and BPC [( Species richness=1.9 – 0.002 x BPC;
R2=0.45, p<0.01), (Polychaeta abundance=0.01 x BPC – 0.52; R2=0.62,
p<0.01) ] concentration values.
Figure 5. Ternary plot in three axis of the relative abundances (%) from the main
macroinfauna groups in sheltered (filled circles) and exposed (open circles) localities at
the three tidal levels (H: high, M: medium, L: low). 100% corresponds with the whole
sum of the Crustacea, Mollusca and Polychaeta percentage.
Crustacea
0 10 20 30 40 50 60 70 80 90 100
Mollusca
0
10
20
30
40
50
60
70
80
90
100
Polychaeta
0
10
20
30
40
50
60
70
80
90
100
M L
L M
H
Chapter 4 Community structure and biochemical composition
138
Table 4. Results of the ANOSIM and pair-wise tests for difference on macroinfauna
community structure between tidal levels (exposed vs. sheltered).
Table 5. Results of the ANOSIM and pair-wise tests for difference on macroinfauna
community structure between tidal levels of exposed and sheltered beaches.
3.4.4. Discussion
3.4.4.1. Macroinfauna characteristics in a gradient of exposure
Results obtained in this study suggest that macroinfauna community, in
terms of abundance, biomass and species richness, was more complex and
diverse in sheltered than in exposed sandy beaches. This has been the general
trend found in other studies where an exposure increase led to a decrease in
biotic variables (Dexter, 1992; McLachlan et al., 1993; Jaramillo and
McLachlan, 1993; McLachlan et al., 1996; Rodil and Lastra, 2004). Correlation
and regression analysis showed a direct effect of exposure rating on
morphodynamic beach conditions. Thus, M.G.S and shear strength were
R p
Global test 0.884 0.001
Levels compared (exp. vs. shelt.)
High-high 0.963 0.1
Medium-medium 0.833 0.002
Low-low 0.98 0.003
Exposed beaches Sheltered beaches
R p R p
Global test 0.352 0.04 0.528 0.036
Levels compared
High-Medium 0.75 0.03 0.98 0.03
High-Low 0.996 <0.01 0.996 <0.01
Medium-Low 0.607 0.13 0.786 0.06
Chapter 4 Community structure and biochemical composition
139
significantly related to exposure. There was a positive relationship between
water content and macroinfauna (two-way ANOVA F=20.7, p<0.01), meaning
that the lower tidal level, with higher water content, harboured a richer
macroinfauna community due to the lower desiccation time, lower temperature
change and the higher feeding time available for the organisms (Wendt and
McLachlan, 1985). Supratidal levels, where environmental conditions are harsh
for truly marine macrofauna, showed lower number of species and were
dominated exclusively by crustaceans such as talitrid amphipods and cirolanid
isopods. The ability of this macroinfauna to utilize the upper levels of sandy
beaches must relate to their adaptations to avoid desiccation (McLachlan, 1990;
Little, 2000). Exposed sandy beaches with short swashes and steep slopes
harbour a rich macrofauna community which find a more stable environment in
the supralittoral zone (Defeo and Gómez, 2005); meanwhile, the number of
species inhabiting the lower part diminished sharply. No significant differences
in the biotic variables were found when supralittoral community from exposed
and sheltered localities were compared. Most of the species at this level (talitrid
amphipods, isopods and insects) have been considered wrack-associated
macrofauna and they largely depend on allochthonous inputs associated with
oceanographic processes (Colombini and Chelazzi, 2003; Dugan et al, 2003).
Sheltered beaches, with more favourable environmental conditions and
sediment stability, showed higher significant values of macrofauna abundance,
biomass and species richness than in exposed intertidal when medium and low
tidal levels, from both environments, were compared. Low macroinfauna
values obtained at the medium tidal level in both, exposed and sheltered
beaches could be due to the special beach profile. These beaches showed a
broken profile roughly separated by mean sea level into an upper steep beach
followed by a lower flat downshore, as was previously found on beaches from
the north coast of Spain (Rodil and Lastra, 2004). Medium tidal level was
located close to this broken profile where hydrodynamic forces occurred
directly during tidal flow affecting macroinfauna zonation and probably
macroinfauna abundance and biomass (Rodil et al., 2006).
Chapter 4 Community structure and biochemical composition
140
Figure 6. Biplots resulting from the multidimensional scaling analysis of the
macroinfauna (density values expressed as ind m-2) and species richness on each beach.
[(Sheltered localities: filled circles; Br: Broña, Bo: Bornelle, Ca: Cabanas; Exposed
localities: open circles; Ni:Niñóns, Ba: Baldaio, Xe: Xeiruga). (Capital letters indicate
tidal level: A: high, B: medium; C: low)].
Hydrodynamic and beach morphodynamic effect on biotic variables is
now considered a paradigm in ecology of sandy beaches at the community
level (Defeo and McLachlan, 2005). Swash climate and sand particle size will
define the response of the macroinfauna due to the increasing harshness in
these factors. The macroinfauna biomass and species richness in the studied
localities diminished significantly when the exposure rating increases (coarse
sediment and short and turbulent swashes). Mollusca and Polychaeta mean
abundances diminished significantly with the exposure rating and there were
also significant differences between tidal levels (Table 3). Both faunistic
groups increased their mean abundances significantly at the medium and low
tidal levels where a significant increase in water content also occurs. This part
of the beach is considered to be under optimal conditions of sand moisture,
BrA
BrB
BrC
BoA
BoB
BoC
CaA
CaB
CaC
XeA
XeB
XeC
NiA
NiB
NiC
BaA
BaB
BaC
Stress: 0,06
Chapter 4 Community structure and biochemical composition
141
penetrability and temperature, following the Habitat Favourability Hypothesis,
(Defeo et al., 2001). Thus, high densities of truly marine species will be able to
occupy this part of the sandy beaches, where more gentle physical conditions
are found, competing for space and food. Mollusca was the least abundant of
all the macroinfauna groups found in sheltered localities, and the bivalves
Cerastoderma edule and Donax trunculus were the main components. Species
belonging to this group were not found in any of the exposed localities. This
kind of intertidal locality, with harsher physical conditions and coarser
sediment, can have a negative effect on burrowing and respiration rate and
growth of filter feeder D. trunculus (de la Huz et al., 2002). Sheltered sandy
beaches, with lower hydrodynamic conditions will favour accumulation of
organic matter potentially available to benthic deposit-feeders. Abundance
variation of Polychaeta moving downshore was different in both groups of
beaches. There was an increase in the mean abundance values of this group in
the medium and low tidal levels of the beaches, but it was only significant in
sheltered conditions. Most of the species belonging to this group were deposit-
feeders being favoured by the settlement of organic rich sediments. Dexter’s
(1983) work suggests that crustaceans and polychaetes dominate the most
exposed and sheltered beaches respectively, with molluscs reaching maximum
abundance in intermediate situations. It is generally admitted in sandy beach
ecology that the number of species, macrofauna density and biomass increase
along a morphodynamic gradient from reflective to dissipative conditions
(Defeo et al., 1992, Jaramillo and McLachlan, 1993, McLachlan et al., 1996)
and also, sandy shores show an increase in the biotic variables as exposure
decreases (McLachaln, 1990). On the other hand, Crustacea mean abundances
did not change significantly in any of the situations mentioned above and this
group was found almost exclusively at the high tidal levels of all the sampled
localities (Fig. 4). Supralittoral forms are less influenced by the swash climate
and generally have autonomous active movement on this part of the beaches.
Chapter 4 Community structure and biochemical composition
142
Table 6. Summary of two-way crossed ANOVA results of exposure (exposed vs.
sheltered) and tidal level (high, medium, low) effect on organic sedimentary compounds.
Bold values indicate significant differences at p< 0.005
BPC: biopolymeric carbon concentrations
3.4.4.2. Biochemical composition of sedimentary organic matter
The amount of biopolymeric fraction that can be found in coastal
sediments is a minor fraction of the organic carbon pool found in the water
column (Danovaro and Fabiano, 1997). The quality and quantity of organic
matter in surface sediments have been considered to of particular importance in
determining the amounts of material potentially available to consumer
organisms, thus affecting community structure and benthic metabolism
(Thompson and Nichols, 1988; Graf, 1989). In this study, biochemical
compounds concentrations of sedimentary organic matter showed significant
differences between sheltered and exposed beaches. Thus, biochemical
concentrations were higher in sheltered localities, probably related to the
morphodynamic and physicochemical characteristics of this kind of sandy
beaches. This suggests that BPC concentrations could be one of the factors
responsible for the increase of benthic macrofauna in sheltered localities. The
lack of relationship between some of the macrofaunal descriptors and sediment
biochemical composition could be due to the snapshot sampling design. We are
aware that these results could change when considering longer temporal scales
but the observed patterns of macrofauna and biochemical compounds seem to
be better related in sheltered beaches than in exposed ones. The low
hydrodynamic conditions of sheltered localities favour accumulation of organic
matter in addition to the settlement of fine sediments which limit the renewal of
interstitial water. The relative contribution of the biochemical compounds to
Proteins Carbohydrates Lipids BPC PROT:CHO
F ratio p F ratio p F ratio p F ratio p F ratio p
Exposure 9.497 0.01 1.438 0.003 1.188 0.005 2.123 0.001 28.1 0.01
Tidal level 3.849 0.051 0.891 0.436 1.7 0.224 4.861 0.02 2.43 0.6
Exposure x tidal level 2.295 0.143 0.545 0.593 1.317 0.304 2.961 0.2 0.59 0.25
Chapter 4 Community structure and biochemical composition
143
the total organic pool was clearly dominated by proteins, followed by lipids and
carbohydrates. BPC concentrations were also significantly higher at medium
and low tidal levels, in all the beaches sampled, compared with the supralittoral
level (Table 6 and Fig. 7).
Figure 7. Overall mean protein, carbohydrate and lipid concentrations at the three tidal
levels and different exposure (sheltered: closed bars; exposed: open bars). Standard
deviation is represented.
The intertidal slope of the beach is one of the parameters used to
estimate the degree of hydrodynamic forces on intertidal sandy beaches
(McLachlan, 1980) and this factor usually increases with increasing exposure.
Lipids
Tidal level
0
30
60
90
120
150
Carbohydrates
Bio
po
lym
eri
c c
arb
on
co
nc
en
tra
tio
ns
(µ
g g
-1 d
ry w
eig
ht)
0
10
20
30
40
Proteins
0
50
100
150
200
250
300
350
High Medium Low
Chapter 4 Community structure and biochemical composition
144
The exposed sampled localities showed a significant increase in the reflective
slope conditions (t6=2.83, p<0.05) due to the harsher morphodynamic
conditions. BPC concentrations were found significantly and inversely
correlated with the intertidal slope from all the beaches; although no significant
differences in the BPC concentration was found among the three tidal levels of
the sandy beaches. Thus, it seems that biopolymeric concentrations follow a
similar pattern that is shown by organisms increasing from exposed intertidal
with steeper slopes to sheltered sandy beaches with flatter slopes.
Organic matter availability is the result of the interactions between
physical and biological processes. A significant and inverse correlation
between BPC concentrations and the exposure rate was also found, which
confirms the drop of material potentially available to consumer organisms
when we move through a gradient of sandy beach exposure. It seems that the
control of beach fauna is complex and determined not only by the physical
environment but also by several ecological factors including the biochemical
composition of the organic matter in the sediments.
The protein to carbohydrate ratio (PROT:CHO) has been used to assess
the ‘age’ of sediment organic matter (Cauwet, 1978). Since proteins are more
readily used by bacteria than carbohydrates (Newell and Field, 1983), high
PROT:CHO ratios (>1) are generally associated with recently produced organic
matter. By contrast, low ratios suggest the presence of aged organic matter and
the role of proteins as a potentially limiting factor for benthic consumers
(Danovaro et al., 1993; Fabiano et al., 1995). In this study, average
PROT:CHO ratios and biochemical compounds obtained were similar to other
intertidal works (Cividanes et al., 2002; Incera et al., 2003) but they ranked
high when compared with the subtidal ratios reported in the literature
(Danovaro et al., 1993; Fabiano et al., 1995). Carbohydrate concentrations in
other works were found to be higher in the deep-sea (Danovaro et al., 1993),
being a characteristic of highly oligotrophic or detritic environments. Our
results suggest that most of the sedimentary organic matter in these beaches
was recently produced and that protein is not a limiting factor for consumer’s
growth.
Chapter 4 Community structure and biochemical composition
145
Figure 8. Relationship between intertidal slope (S) and biopolymeric carbon
concentrations (μg g-1 d.w. of sediment) of sedimentation at the three tidal levels.
Sheltered localities are presented as filled circles and exposed localities as open circles.
[ANCOVA; tidal level effect: F2,11 = 14.08, p = 0.001; intertidal slope (covariable):
F1,11 = 5.35, p = 0.041; tidal level*intertidal slope: F2,11 = 1.1815, p = 0.342 (n.s.)].
High tidal level
0 20 40 60 80 100
0
20
40
60
80
100
120
140
Low tidal level
Slope
0 20 40 60 80 100
60
80
100
120
140
160
180
200
220
Medium tidal level
0 20 40 60 80 100
Ca
rbo
n o
f th
e b
iop
oly
me
ric
fra
cti
on
20
40
60
80
100
120
140
160
180
Xeiruga
Xeiruga
Niñons
Baldaio
Cabanas
Broña
Bornelle
Xeiruga
Baldaio
Baldaio
Niñons
Niñons
Broña
Broña
Bornelle
Bornelle
Cabanas
Cabanas
Chapter 4 Community structure and biochemical composition
146
The higher ratios found in exposed rather than in sheltered sandy beaches
indicate that there is little dead organic matter accumulation in exposed
localities, probably due to the strong hydrodynamic conditions. It seems that
with decreasing exposure, beaches tend to behave as storage sites of organic
matter (Little, 2000), with a higher accumulation rate. The high PROT:CHO
ratio, together with the high concentrations of BPC classified these beaches as
eutrophic systems (sensu Dell’Anno et al., 2002). Moreover, since proteins
constituted the main dominant fraction of BPC (on average, 63.4% and 80.2%
for sheltered and exposed localities respectively) and carbohydrates showed the
lowest values measured in all the beaches, the organic matter seems to be
mostly of ‘newly-generated’ detritus and autochthonous origin. Although the
high organic matter concentrations found in the sheltered intertidal could be
better explained by the influence of temporal allochthonous inputs of carbon
and organic material since little primary production occurs on the beach itself
(Brown and McLachlan, 1990).
Thus, the results obtained showed that the dominant species in
sheltered beaches belong to the deposit-feeder group (above all from
Polychaeta group), which base their feeding on organic sedimentary
assimilation (Brown and McLachlan, 1990; Knox, 2000). Subterrestrial species
dominate the upper tidal levels of all the beaches; they will be the main
macroinfauna group in the exposed localities since they do not depend on the
swash climate but upon allochthonous inputs such as wrack macroalgae. It has
been suggested in the literature that fauna decreasing along a gradient from
sheltered to exposed beaches is caused by the increase in harsh swash climate
and coarser grain size (McLachlan et al., 1996). In this study we have
confirmed this fact but moreover, the biochemical compounds and the BPC
concentrations decreasing along the same gradient of exposure, suggests
largely that food quality could be a main factor affecting macroinfauna
community in the intertidal.
Acknowledgements
We are extremely grateful to S.Gil and M.Lago for helping us with
laboratory work and for their invaluable assistance during sampling. This
Chapter 4 Community structure and biochemical composition
147
research was supported by the Government of Spain (Ministerio de Medio
Ambiente; CICIT, REN2002-03119) and the Regional Government of Galicia
(Augas de Galicia and XUGA PGIDIT02RMA30101PR). Funds to I.F. Rodil
were provided by a Ph.D. grant from the Xunta de Galicia (Predoctorales Xunta
P.P. 0000 300S 140.08). We wish to thank two anonymous referees for kindly
advising us on some details of this paper.
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PART IV. THE ROLE OF FOOD AVAILABILITY IN
SANDY BEACHES: SPATIAL AND TEMPORAL
PATTERNS.
“We may infer from these facts, what havoc the introduction of any new
beast of prey must cause in a country, before the instincts of the
aborigines become adapted to the stranger’s craft or power.”
-Charles Darwin
Journal of Researches
Contents:
Rodil, I.F., Cividanes, S., Lastra, M. and López, J. Seasonal variability
in the vertical distribution of benthic macrofauna and sedimentary
organic matter in an estuarine beach (NW Spain). Estuaries and coasts
(accepted, in press).
Rodil, I.F., Olabarria, C., Lastra, M. and López, J. Differential effects
of native and invasive algal wrack on macrofaunal assemblages
inhabiting exposed sandy beaches. Journal of Experimental Marine
Biology and Ecology (accepted, in press).
Chapter 5. Seasonal variability in the vertical distribution
of benthic macrofauna and sedimentary organic matter in
an estuarine beach (NW Spain).
Chapter 5 Seasonal variability in an estuarine beach
153
Abstract.
This study was designed to investigate seasonal changes on food
available for benthic consumers in relation to tidal levels and sediment depth in
an estuarine beach. The relationships between the biochemical characteristics
of sedimentary organic matter and benthic macrofauna were analysed quarterly
over two years (from January 1997 to January 1999), in an estuarine soft
intertidal zone from the NW coast of Spain (42º 64’ 04’’N; 8º 88’ 36’’W).
Sediment samples were collected in order to provide a two-dimensional view of
macroinfauna distribution in the intertidal zone and its relationship with the
quantity and quality of the organic matter. The nutritional value of organic
matter (i.e., lipid, protein and carbohydrate) and the content of chlorophyll a of
the sediment were measured. Macrofaunal assemblages and food availability in
the sediment were studied at three tidal levels on the shore: two intertidal and
one supratidal.
Macroinfauna and biochemical compounds showed a clear vertical
stratification with the highest macrofaunal abundance at the superficial layer of
the sediment, where redox potential discontinuity was also observed.
Crustaceans were found mainly inhabiting the supratidal level of the estuarine
beach, while, polychaetes and molluscs occupied the intertidal level. Food
availability, measured as biopolymeric carbon, and also chlorophyll a from the
sediment were better related to macroinfauna abundance, biomass and
abundance of main taxonomic groups. Macrofauna assemblages showed
particular distribution in both vertical and horizontal ranges suggesting specific
preferences to several abiotic factors. No clear seasonal pattern was found in
macrofauna and sedimentary organic characteristics suggesting that
macrofaunal assemblages are controlled by complex and unpredictable factors,
including small scale changes in substrate and hydrological characteristics.
Keywords: Estuarine beaches; macroinfauna; spatial and temporal patterns;
biopolymeric carbon; food availability; sedimentary organic matter; NW Spain.
Chapter 5 Seasonal variability in an estuarine beach
154
4.5.1. Introduction
Intertidal macroinfauna is regarded as an important component of
marine communities, occupying a key role in the breakdown and incorporation
of organic matter into sediments in coastal ecosystems (Levin et al., 2001).
Intertidal invertebrate communities show temporal and spatial patterns which
are the result of the ability of species to cope with changes in physical and
biological factors associated with major environmental gradients, such as tidal
influence, exposure rate and water and substrate characteristics. Soft sediments
present important biotic and abiotic variations, not only at spatial and temporal
scales, but also in terms of vertical distribution. Several sediment
characteristics such as compactness, water content or grain size are able to
influence the vertical distribution of the macroinfauna.
The organic matter in the sediment, as well as dead material, plays a
major role within the detritus food chain because it includes living organisms
such as bacteria and microalgae, which have been considered one of the most
nutritive food sources (Grémare, 1994; McIntyre et al., 1996). Quantity and
quality of organic matter in surface sediments are recognised primary factors
affecting benthic fauna dynamics and metabolism as well as community
structure (Fabiano et al., 1995; Dugan et al., 2003). The distribution of benthic
communities in sandy intertidals is well known (e.g. Peterson, 1991, Dittmann,
2000). Little is known, however, about the characteristics of food available and
its relationship with the macroinfauna community in the intertidal zone.
Food availability is related to the biochemical composition of organic
matter and several studies have estimated the fraction of sedimentary organic
matter available for consumers by determining the biochemical classes of
organic compounds (i.e. carbohydrates, proteins and lipids), which are assumed
to be easier to digest and assimilate (Fabiano et al., 1995). The concentration of
biochemical compounds and the percentage of total organic matter (TOM) have
been used to estimate the nutritive value of the sediment. Chlorophyll a
concentration in the sediment has been measured as a surrogate of microalgae
biomass and has been widely used in the literature (e.g. Fabiano et al., 1995;
Grémare et al., 1997).
Chapter 5 Seasonal variability in an estuarine beach
155
The large amount of organic matter reaching the intertidal zone in
sheltered areas is expected to induce a significant benthic response which could
partially explain the high abundance and diversity of the macroinfauna in these
environments compared to other coastal ecosystems such as exposed sandy
beaches (e.g. Incera et al., 2006; Rodil et al., 2007). The nutritive value of
sedimentary organic matter may show marked seasonal changes and low values
have often been found in late spring and summer (Grémare et al., 1997; Rossi,
2002). Furthermore, the availability of food resources could be important in
regulating the dynamics of benthic macrofauna (Rossi et al., 2001).
Much of the previous macroinfauna research on soft intertidals is
restricted to general considerations of the factors influencing individual species
and macroinfauna assemblages, while analyses of vertical and horizontal
zonation are scarce. The main purpose of this study was to characterise a two-
dimensional view of macroinfauna distribution along a tidal gradient in an
estuarine beach in order to understand its relationships with environmental
parameters and food availability. Data on the sedimentary organic matter and
environmental parameters from 1997 was previously published in Cividanes et
al., 2002. This study provides longer term seasonal data for the vertical and
horizontal distribution of substratum characteristics and macrofaunal species.
In this paper, we test hypotheses regarding influences on macrofaunal
assemblages inhabiting an estuarine beach. In particular, we test the hypothesis
that (1) the environmental conditions vary between the supratidal and the
intertidal zones and through sediment depth, (2) the quality and quantity of
sedimentary organic matter, i.e., food available, differ over the tidal level,
through sediment depth and over time and, as a result, (3) macrofauna
assemblages vary over time and space in the estuarine beach. Furthermore, we
predicted that macrofauna variability and distribution are strongly related to
specific factors such as food availability.
Chapter 5 Seasonal variability in an estuarine beach
156
Figure 1. Location of the estuarine beach (Barraña) on the NW coast of Spain. a)
Relative position of Galicia and the intertidal b) Intertidal slope and temporal changes
observed throughout the study period (1997-1999). Approximate situation of the three
levels on the shore (HTL: high tidal level; MTL: medium tidal level; LTL: low tidal
level).
4.5.2. Material and methods.
4.5.2.1. Study area
The study site is located in the Ria of Arousa, on the NW coast of the
Iberian Peninsula (Figure 1a). Barraña is a sheltered beach, 2150 m long,
influenced by a mesotidal regime with a mean tidal range of 3 m. This sandy
intertidal zone is located in the inner part of the ria (sensu Méndez and Vilas,
2005) delimited by a local river mouth and characterised by low wave
exposure, shallow reduced sediment layers and the presence of macrofaunal
burrows. This ria is tide-dominated and the beach studied was flushed
Barraña
a
Distance (m)
0 100 200 300
He
igh
t (m
)
0
1
2
3
4
5
b
HTL
MTL
LTL
Chapter 5 Seasonal variability in an estuarine beach
157
regularly. The intertidal profile was measured (Fig. 1b) and no significant
differences were found over time (F8,15 = 0.067, p > 0.05). Barraña is affected
by large amounts of allochthonous organic matter. In this study, algal mats
were present throughout the entire intertidal range (350 m long), but lower on
the shore, as they moved about with tides and waves.
4.5.2.2. Sampling design
From January 1997 to January 1999, sediment samples were collected
quarterly during spring low tide. Sampling was carried out at three replicated
transects, randomly separated, at the central area of the beach at three tidal
levels; one supratidal (high) and two intertidal (medium and low). Due to beach
morphology, medium tide level appeared covered with some water resembling
a pond during ebbing, which created a unique environment (Figure 1b).
Macroinfauna samples were collected with a 15.5 cm diameter metal corer
penetrating 25 cm deep into the substrate (n = 3) at each transect (188.7 cm2
surface area). The samples were divided into 5 layers (0-5, 5-10, 10-15, 15-20,
20-25 cm depth). The sediment was sieved through 1 mm mesh and the
individuals were sorted from the sediments, identified and counted in the
laboratory. Shell-free biomass of all the species was determined by drying at
100ºC for 24 hours and then 500ºC for 6 hours, obtaining ash free dry weight
values.
Sediment samples for biochemical and chlorophyll a analyses were
collected in three replicates by hand coring (15.5 cm inner diameter core) at the
three tidal levels. Samples were also vertically sliced into five layers; each
layer was homogenized by hand mixing and subsamples (frozen at -30 ºC) were
taken for the analysis of sedimentary organic matter, grain size and water
content. Mean grain size was performed by means of a Coulter Counter LS 200
and sediment shear strength by means of a shear vane meter. Sediment water
content was estimated as the difference between wet and dry weight (60 ºC, 72
h) and expressed as a percentage. Temperature (ºC) and redox potential (Eh)
were measured at 5 cm intervals down to 25 cm sediment depth.
Chapter 5 Seasonal variability in an estuarine beach
158
4.5.2.3. Biochemical composition of the sedimentary organic matter
Biochemical compounds of organic matter were evaluated by
spectrophotometric analyses of lipid, carbohydrate and protein concentration in
the sediment. For all analyses, 0.5-2.5 g of sediment was used (data normalised
to sediment dry weight; sed dw). All biochemical analyses were conducted on
sediment samples previously oven dried at 60 ºC until weight was constant and
finely powdered with a pestle. Total lipids (Bligh and Dyer, 1959),
carbohydrates (Dubois et al., 1956) and proteins (Markwell et al., 1978) were
analysed. The sum of the main biochemical classes; i.e. the nutritional value,
was reported as the biopolymeric carbon (BPC sensu Fabiano et al., 1995),
assumed as a reliable estimate of the labile fraction available to benthic
consumers. The protein to carbohydrate ratio (PROT:CHO) was also calculated
to assess the age of the organic material. A detailed description of the analyses
is reported in Cividanes et al. (2002).
Total sediment carbon (TOC) and nitrogen (TN) were determined on
sediment subsamples (15-20 mg) in order to obtain BPC:TOC (%) and C:N
ratio, which were used as a food and quality index respectively . The residual
fraction of the organic carbon (complex organic matter, COM; Fichez, 1991)
was determined as the difference between TOC and BPC. Analyses of dry
weight sediment chlorophyll a (Chla, μg g-1) were extracted following
Lorenzen (1967). The chlorophyll a content was assessed by homogenizing
samples from all five depth layers.
4.5.2.4. Data analysis
Data from macrozoobenthic communities were analysed in terms of
number of species, abundance (ind m-2) and biomass (g m-2). Relative
contribution of the major macrobenthic groups (i.e. Crustacea, Mollusca and
Polychaeta) and also contribution of five major trophic groups (i.e. subsurface
and surface deposit feeders, suspension feeders, carnivores and others) as
percentage of the total individual numbers were tested to elucidate dominance
and trophic characteristics of the macroinfauna (Pearson and Rosenberg, 1987).
Chapter 5 Seasonal variability in an estuarine beach
159
Temporal and spatial fluctuations in biochemical and macrofauna
variables were assessed by a four-factor orthogonal analysis of variance with
year (1997 and 1998), month (January, April, July and October), tidal level
(high, medium and low) and depth (0-25 cm) as fixed factors (Sokal and Rohlf,
1995). When necessary, transformations were used to achieve the assumptions
of homogeneity and normality. A posteriori Tukey’s pairwise comparison test
was also performed to elucidate possible differences between levels of a factor
(p < 0.05). Multivariate analyses were used to determine temporary differences
in the species composition of the benthic assemblage and to assess which
species mainly contributed towards the seasonal differences. Data was carried
out on transformed data (4th square root) using the Bray-Curtis index and
group average linkage for non-metric multidimensional scaling (MDS). The
discrimination of fauna assemblages along tidal levels and over time was tested
with one-way ANOSIM. Species typifying assemblages were identified using
the SIMPER program (Clarke, 1993). The link between the biotic pattern and
abiotic variables was explored using the biological environmental gradients
(BIO-ENV) procedure, which aimed to select the environmental variables
subset that maximises the rank correlation (ρ) between biotic and abiotic
similarity matrix (PRIMER). Whenever possible, general patterns among
particulate organic matter, biochemical characteristics, environmental variables
and benthic macrofauna were assessed using principal component analysis
(PCA; CANOCO 4.5). A generalised linear model (GLM) with a log-linear
model (Poisson error term and forward multiple logistic-regression analysis)
was used to compare the relationships between biotic and abiotic variables.
This model is more flexible and better suited for analysing ecological
relationships which can be poorly represented by classical Gaussian
distributions (Guisan et al., 2002). The significance of the independent
variables was tested using the χ2-test (Wald statistic; Statistica 6.0).
Chapter 5 Seasonal variability in an estuarine beach
160
Table 1. Summary of analyses of variance of the effect of time (Year: 1997 and 1998;
Month: January, April, July, October), tidal level (i.e. high, medium and low) and
sediment depth (0-25 cm) on several environmental variables. (N = 360). Data from
1999 (one month) was not included. M.G.S.: mean grain size, S.S.: shear strength; Eh:
redox potential T: Temperature; W.C.: water content. Significance levels: *: p < 0.05;
**: p < 0.01; ***: p < 0.001; ns: p > 0.05. +log transformed data
4.5.3. Results.
4.5.3.1. Environmental characteristics.
Mean grain size (M.G.S.) and shear strength (S.S.) showed significant
differences over the tidal level and through sediment depth (Table 1) but this
pattern was not consistent over time (i.e., significant Y x M x L x D
interaction). M.G.S. and S.S. increased with sediment depth (Tukey’s post hoc
test). Grain size was coarser at the high tidal level (HTL) than at the mid
(MTL) and low tidal levels (LTL) and S.S. was lower at the supratidal level.
Compactness was lower in January, while sediment was coarser in July and
October (post hoc test). Positive values of redox potential (Eh) were found at
the HTL, although they became negative at the intertidal levels through
sediment depth (post hoc test). Redox potential discontinuity (RPD) was
observed at 5-10 cm depth at the intertidal and this pattern was consistent over
space and time (i.e., no significant Y x M x L x D interaction). Water content
and temperature showed a seasonal pattern, between months, ranging from
16% (July 1997, HTL, 15-20 cm) to 25% (January 1997, LTL, 5-10 cm depth)
Source of variation M.G.S.+ S.S.
+ Eh T W.C.
d.f. p p p p p
Year (Y) 1 n.s n.s *** *** n.s.
Month (M) 3 *** *** *** *** ***
Tidal level (L) 2 *** *** *** *** ***
Depth of the sediment (D) 4 *** *** *** n.s. ***
Y*M 3 ** *** *** *** ***
Y*L 2 * *** *** *** *
M*L 6 *** *** *** *** ***
Y*M*L 6 ** *** *** *** ***
Y*D 4 n.s. *** ** n.s. *
M*D 12 ** ** * * n.s.
Y*M*D 12 *** * n.s. *** n.s.
L*D 8 *** ** *** *** **
Y*L*D 8 *** n.s. n.s. n.s. n.s.
M*L*D 24 * ** n.s. *** n.s.
Y*M*L*D 24 * *** n.s. n.s. n.s.
Chapter 5 Seasonal variability in an estuarine beach
161
and from 10.9 ºC (January 1998, HTL, 0-5 cm) to 22 ºC (July 97, HTL, 20-25
cm) respectively. These patterns were consistent over space and time (no
significant Y x M x L x D interaction).
4.5.3.2. Macrobenthic community.
All the biotic variables varied significantly over the tidal level and
through sediment depth (Table 2) but this pattern was not consistent over time
(i.e. significant Y x M x L x D interaction). Macrofauna abundance was higher
in July and October than in April and January and biomass and the number of
species were higher in July (post hoc tests). As regards vertical distribution
(Figure 2), abundance, biomass and number of species were found to be higher
in the superficial sediment level (0-15 cm, post hoc test). The MTL presented
the highest macroinfauna abundances (17124±4931 ind m-2, October 1997),
biomass (2.061±0.202 g m-2, April 1997) and species values (26, July 1997)
and the HTL the lowest values (18±16 ind m-2, April 1998; 0.001±0.001 g m-2,
January 1998 and 1 species, April 1998). Biotic variables obtained from MTL
were found to be significantly higher than those from LTL (post hoc test).
The contribution of the main macroinvertebrate groups changed at the
three tidal levels and with sediment depth and there was some temporal
variation (Table 2 and Figure 3). Polychaeta and Mollusca were the most
representative groups in the overall intertidal macroinfauna accounting for 53%
and 36%, respectively. Polychaeta showed no significant differences between
months (post hoc test) but was found to be significantly higher at the intertidal
(MTL>LTL>HTL) and in the sediment surface (5>10>15=20=25 cm depth).
This pattern was not consistent over space and time (i.e., significant Y x M x L
x D interaction). The relative contribution of this group accounted for 28%
(January 1999) to 98% (April 1998) at the MTL and from 56% (July 1998) to
91% (July 1997) at the LTL. The density of molluscs was also higher at the
intertidal level (MTL>LTL>HTL) and in the sediment surface (0-15 cm) in
July and January (post hoc test) and this pattern was consistent over time
(Table 2).
Chapter 5 Seasonal variability in an estuarine beach
162
Ta
ble
2.
Su
mm
ary o
f anal
yse
s o
f var
iance
of
the
effe
ct o
f ti
me
(Yea
r: 1
99
7 a
nd
19
98
; M
onth
: Ja
nuar
y,
Ap
ril,
July
, O
cto
ber
), t
idal
lev
el
(i.e
. hig
h,
med
ium
and
lo
w)
and
sed
iment
dep
th (
0-2
5 c
m)
on m
acro
infa
una
abu
nd
ance
(in
d m
-2),
bio
mas
s (g
m-2
), n
um
ber
of
spec
ies
and
abund
ance
of
the
thre
e m
ain t
axo
no
mic
gro
up
s. D
ata
fro
m 1
99
9 w
as n
ot
inclu
ded
. (N
= 3
60
). S
ignif
ican
ce l
evel
s: *
: p
< 0
.05
;
**:
p <
0.0
01
; ***:
p <
0.0
01
; ns:
p >
0.0
5. +
log t
ransf
orm
ed d
ata
A
bu
nd
an
ce
Sou
rce
of
vari
ati
on
Ab
un
dan
ce+
Bio
mass
S
pec
ies
Poly
chaet
es
Moll
usc
s C
rust
ace
an
s+
d.f
. p
p
p
p
p
p
Yea
r (Y
) 1
***
***
***
*
n.s
. **
*
Month
(M
) 3
***
**
***
n.s
. n.s
. **
*
Tid
al l
evel
(L
) 2
***
***
***
***
***
**
*
Dep
th o
f th
e se
dim
ent
(D)
4
***
***
***
***
***
n
.s.
Y*M
3
n.s
. *
n.s
. **
n.s
. **
Y*L
2
***
***
***
**
n.s
. **
*
M*L
6
***
n.s
. **
***
n.s
. **
Y*M
*L
6
***
n.s
. ***
***
n.s
. **
*
Y*D
4
n.s
. n.s
. n.s
. ***
n.s
. n
.s.
M*D
12
**
n.s
. n.s
. **
*
n.s
.
Y*M
*D
12
*
**
*
***
n.s
. *
L*D
8
***
***
***
***
***
**
Y*L
*D
8
n.s
. n.s
. n.s
. **
n.s
. n
.s.
M*L
*D
24
**
*
n.s
. ***
**
n.s
.
Y*M
*L
*D
24
**
*
*
***
n.s
. n
.s.
Chapter 5 Seasonal variability in an estuarine beach
163
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ab
un
da
nc
e (
ind
/m2
)
05
00
01
00
00
15
00
02
00
00
20-2
5
15-2
0
10-1
5
5-1
0
0-5
J 9
7
A 9
7
O 9
7
O 9
7
Sediment depth
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ju
97
20-2
5
15-2
0
10-1
5
5-1
0
0-5
A 9
7
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Bio
ma
ss
(g
/m2
)
24
68
J 9
7
Ab
un
da
nc
e (
ind
/m2)
01000
2000
3000
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Bio
ma
ss
(g
/m2
)
10
20
30
MT
LH
TL
Ju
97
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ab
un
da
nc
e (
ind
/m2
)
02
00
04
00
06
00
08
00
0
20-2
5
15-2
0
10-1
5
5-1
0
0-5
J 9
7
A 9
7
Bio
ma
ss
(g
/m2
)
36
91
21
5
LT
L
Ju
97
O 9
7
Fig
ure 2
. V
ert
ical
dis
trib
uti
on
of
the a
bu
nd
ance (
m-2
±sd
) an
d b
iom
ass
(g.m
-2±
sd)
of
the m
acro
infa
una a
t th
e t
hre
e t
idal
levels
(HT
L.
MT
L a
nd
LT
L)
over
tim
e (
J: J
anuary
. A
: A
pri
l. J
u.
July
. O
: O
cto
ber
fro
m 1
99
7 t
o 1
99
9).
Chapter 5 Seasonal variability in an estuarine beach
164
Bio
mass (
µg
/m2
)
51
01
52
02
5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Sediment depth
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ab
un
dan
ce (
ind
/m2)
05
00
01
00
00
15
00
02
00
00
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ab
un
dan
ce (
ind
/m2)
02
00
04
00
06
00
08
00
0
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Bio
mass (
µg
/m2)
10
20
30
J 9
9
20-2
5
15-2
0
10-1
5
5-1
0
0-5
O 9
8
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Ju 9
8
20-2
5
15-2
0
10-1
5
5-1
0
0-5
A 9
8
20-2
5
15-2
0
10-1
5
5-1
0
0-5
Bio
mass (
µg
/m2
)
24
68
J 9
8
Ab
un
dan
ce (
ind
/m2
)
05
00
10
00
15
00
20
00
20-2
5
15-2
0
10-1
5
5-1
0
0-5
HT
LM
TL
LT
L
A 9
8
J 9
8
O 9
8
Ju 9
8
O 9
8
Ju 9
8
A 9
8
J 9
8
J 9
9
J 9
9
Fig
ure 2
. V
ert
ical
dis
trib
uti
on
of
the a
bu
nd
ance (
m-2
±sd
) an
d b
iom
ass
(g.m
-2±
sd)
of
the m
acro
infa
una a
t th
e t
hre
e t
idal
levels
(HT
L.
MT
L a
nd
LT
L)
over
tim
e (
J: J
anuary
. A
: A
pri
l. J
u.
July
. O
: O
cto
ber
fro
m 1
99
7 t
o 1
99
9).
Chapter 5 Seasonal variability in an estuarine beach
165
This group accounted for about 3% (April 1997) to 71% (January 1999) at the
MTL and from 2% (October 1997) to 41% (January 1998) at the LTL. Most of
the crustaceans (mainly Talitrid amphipods) were found at the supratidal (post
hoc test) with significant seasonal variability (July=October>January=April),
accounting for 5% (January 1998) to 100% (October 1998) of the overall
macroinfauna at this level.
Figure 3. Temporal changes in the abundance of the three taxonomic groups
(Polychaetes. molluscs and crustaceans) and number of species with tidal levels and
sediment depths. Mean average (ind.m-2) and standard deviation are shown.
0-5 cm 5-10 cm 10-15 cm 15-20 cm 20-25 cm depth
HTL
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
Ab
un
dan
ce P
oly
ch
aeta
(in
d/m
2)
0
1000
2000
3000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
Ab
un
dan
ce C
rusta
cea (
ind
/m2
)
0
1000
2000
3000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
Ab
un
dan
ce M
oll
usca (
ind
/m2
)
0
1000
2000
3000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
nu
mb
er
of
sp
ecie
s
0
5
10
15
MTL
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
0
2000
4000
6000
8000
10000
12000
14000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
0
2000
4000
6000
8000
10000
12000
14000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
0
2000
4000
6000
8000
10000
12000
14000
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
0
5
10
15
LTL
Ja97A97Ju97O97Ja98A98 J98O98Ja99
0
2000
4000
6000
8000
10000
Ja97A97Ju97O97Ja98A98 J98O98Ja99
0
2000
4000
6000
8000
10000
Ja97A97Ju97O97Ja98A98 J98O98Ja99
0
2000
4000
6000
8000
10000
Ja97A97Ju97O97Ja98A98 J98O98Ja99
0
5
10
15
Chapter 5 Seasonal variability in an estuarine beach
166
A classification of the macrobenthic organisms into five different
trophic groups (see Appendix IV) gave a numerical dominance of subsurface
and surface deposit-feeders at the MTL (87%, April 1998 and 72%, January
1999) and LTL (62%, April 1997 and 93%, July 1997). The trophic group
classified as “others” as the main dominant at the HTL and carnivores
accounted for 29% at the LTL (April 1998).
Figure 4. Non-metric multidimensional scaling (MDS) analysis of the macroinfauna
(ind m-2). Letters indicate months (J: January; A: April; Ju: June; O: October) and
numbers indicate years (1997. 1998, 1999). : high tidal level; : medium tidal
level; low tidal level.
The macroinfauna assemblage showed significant differences over time
(ANOSIM global test; R = 0.594, p < 0.05). The MDS analysis for total
macroinfauna abundances and species (Figure 4) presented the intertidal levels
clearly separated (R = 0.802, p < 0.001). Macrofauna assemblage from HTL
showed significant differences with MTL (R = 0.892, p < 0.001) and LTL (R =
0.942, p < 0.001) and also significant dissimilarity was found between MTL
and LTL (R=0.737, p < 0.001). The organisms mainly responsible for the tidal
level differences (SIMPER) were the talitrid Talorchestia deshayesii (33% of
J97
J97
J97
A97A97
A97
JU97
JU97
JU97
O97
O97
O97
J98
J98
J98
A98
A98
A98
JU98 JU98
JU98
O98
O98
O98
J99
J99
J99
2D Stress: 0,12
Chapter 5 Seasonal variability in an estuarine beach
167
the total contribution) and several insect larvae (28.8%) at the HTL; the
polychaeta Capitella sp. (22.4%) and the gastropod Hydroid vulvae (16%) at
the MTL and the polychaeta Spoil falconries (19.3%) and the bivalve Lories
luminaries (14.7%) at the LTL. The abundance of Capitella sp. (7.2 %) and
Hydroid vulvae (6.7%) were the most responsible for the dissimilarities over
time (complete list of species in Appendix IV).
4.5.3.3. Organic matter composition and chlorophyll a content.
The annual average concentration during the study period for
carbohydrate, lipid and protein was 289±224, 596±496 and 1226±1060 μg g-1
sed dw, respectively (Figure 5). The statistical analyses revealed that the
nutritive value of the sediment displayed significant variability (Table 3)
although it was not consistent over space and time (i.e., significant Y x M x L x
D interaction). Maxima concentrations were found at the MTL and diminished
with sediment depth (post hoc test). Protein concentrations were higher during
winter and spring than in summer (April>January=October>July), while
carbohydrate and lipid concentrations were higher in summer and autumn (post
hoc test). The BPC showed a similar trend to protein pattern (this figure is
therefore not shown) with maximum values in April at the MTL (significant M
x L x D interaction). PROT:CHO ratio showed significant variability (Table 3)
but this pattern was not consistent over space and time (i.e., significant Y x M x
L x D interaction). This ratio was higher at the beginning of the year
(January>April>July=October) and significant differences were found among
tidal levels (MTL>LTL=HTL).
Seasonal variations of the elemental composition of sedimentary
organic matter across space were plotted in Figure 6. Total organic carbon
(TOC), complex organic matter (COM) and total nitrogen (TN) presented
significant variability (Table 3) but this pattern was not consistent over space
and time (i.e., significant Y x M x L x D interaction).
Chapter 5 Seasonal variability in an estuarine beach
168
The composition of sedimentary organic matter reached the highest values at
the MTL (post hoc test). TOC and COM concentrations were found lower in
winter (January<April=July=October) and in the sediment surface
(5=10=15=20<25 cm). TN showed seasonal variability with higher values at
the end of the summer (October>July=April>January) and in the sediment
surface (5=10>15=20>25 cm).
Figure 5. Temporal variations in the concentrations of carbohydrates, proteins and
lipids with tidal levels and sediment depths. Values are given as micrograms per gram
sediment dry weight (µg g-1 sed d.w. ± sd).
The BPC: TOC ratio indicated that BPC accounted for a relevant fraction of the
total organic carbon (44%). Higher C:N ratio values were recorded at the MTL,
ranging between 4.4 (January 1997, 0-5 cm) and 22.5 (January 1998, 20-25
cm). Chlorophyll a (Chl a; 4.55±4.18 μg g -1 sed dw on annual average)
0-5 cm 5-10 cm 10-15 cm 15-20 cm 20-25 cm depth
Carbohydrates (µg g-1 sed d.w.)
0
200
400
600
800
1000
HTL
0
1000
2000
3000
4000
5000
Ja97A97 J97 O97Ja98A98 J98 O98Ja99
0
500
1000
1500
2000
Proteins (µg g-1 sed d.w.)
0
200
400
600
800
1000
0
1000
2000
3000
4000
5000
Ja97A97 J97 O97Ja98A98 J98 O98Ja99
0
500
1000
1500
2000
MTL
LTL
Lipids (µg g-1 sed d.w.)
0
200
400
600
800
1000
0
1000
2000
3000
4000
5000
Ja97A97 J97 O97Ja98A98 J98 O98Ja99
0
500
1000
1500
2000
Chapter 5 Seasonal variability in an estuarine beach
169
showed seasonal variability (Fig. 6 and Table 3) but this pattern was not
consistent over space and time (i.e., significant Y x M x L x D interaction).
Higher concentrations were found in summer and late summer
(October>July>April=January) at the intertidal (MTL>LTL=HTL) in the
sediment surface.
4.5.3.4. Relationships between sedimentary organics and benthic fauna.
According to BIO-ENV (Table 4), the best correlations (ρs) were found
with sediment grain size and water content and also with some biochemical
compounds such as BPC, prot:cho, C:N, TOC, COM and Chl a. Although this
procedure does not give the direction of such correlations, it can indicate that
these variables possibly influence the differences in community structure. The
projection of variables based on environmental, biochemical and faunal
parameters recorded during the time of study was plotted in Figure 7. The first
and second axes accounted for 63.0% and 15.1% of the variance respectively.
The positive axis linked several faunal characteristics such as number of
species, biomass and abundance of polychaetes to the biochemical compounds
(BPC) and Chl a. Macroinfauna abundance appeared to be associated with the
same biochemical variables. Furthermore, biomass of the macroinfauna showed
high positive values associated with TOC, TN and BPC:TOC. Faunal
parameters were also associated with environmental parameters such as water
content. The abundance of crustaceans was positively associated to some of the
environmental parameters such as Eh, M.G.S. and S.S. These results were
further supported by multiple regression analysis (Table 5).
Chapter 5 Seasonal variability in an estuarine beach
170
Sou
rce
of
vari
ati
on
Pro
tein
+
Carb
oh
yd
rate
+
Lip
id+
BP
C†
TO
C
CO
M†
TN
p
rot:
cho
C
hlo
rop
hyll
a+
d.f
. p
p
p
p
p
p
p
p
p
Yea
r (Y
) 1
***
***
***
***
***
**
***
***
***
Month
(M
) 3
***
***
***
***
***
***
***
***
***
Tid
al l
evel
(L
) 2
***
***
***
***
***
***
***
***
***
Dep
th o
f th
e se
dim
ent
(D)
4
***
***
***
***
***
***
***
***
***
Y*M
3
***
***
***
***
**
***
***
***
***
Y*L
2
***
n.s
. n.s
. *
n.s
. n.s
. ***
***
n.s
.
M*L
6
***
***
***
***
***
***
***
***
***
Y*M
*L
6
***
***
***
***
***
***
***
***
***
Y*D
4
***
**
*
n.s
. n.s
. n.s
. n.s
. n.s
. ***
M*D
12
***
*
n.s
. n.s
. n.s
. n.s
. n.s
. n.s
. ***
Y*M
*D
12
n.s
. n.s
. n.s
. n.s
. *
**
n.s
. **
***
L*D
8
***
**
n.s
. *
***
***
***
*
***
Y*L
*D
8
***
n.s
. n.s
. n.s
. ***
***
n.s
. n.s
. n.s
.
M*L
*D
24
***
***
n.s
. *
***
**
n.s
. **
***
Y*M
*L
*D
24
***
**
*
n.s
. ***
***
*
*
***
Ta
ble
3.
Su
mm
ary o
f anal
yse
s o
f var
iance
of
the
effe
ct o
f ti
me
(Yea
r: 1
99
7 a
nd
199
8;
Mo
nth
: Ja
nuar
y,
Ap
ril,
July
, O
cto
ber
), t
idal
lev
el (
i.e.
hig
h,
med
ium
and
lo
w)
and
sed
iment
dep
th (
0-2
5 c
m)
on t
he
org
anic
mat
ter
com
po
siti
on (B
PC
: b
iop
oly
mer
ic ca
rbo
n;
TO
C:
tota
l o
rgan
ic
carb
on;
CO
M:
co
mp
lex o
rganic
mat
ter;
TN
: to
tal
nit
rogen)
and
chlo
rop
hyll
a c
once
ntr
atio
ns.
Dat
a fr
om
19
99
was
no
t in
clud
ed (
N =
36
0).
Sig
nif
icance
lev
els:
*:
p <
0.0
5;
**:
p <
0.0
01
; ***:
p <
0.0
01
; ns:
p >
0.0
5.
†B
PC
(i.
e.,
the
sum
of
pro
tein
s, c
arb
oh
yd
rate
s an
d l
ipid
s);
CO
M (
i.e.
, th
e d
iffe
ren
ce b
etw
een T
OC
and
BP
C).
+lo
g t
ransf
orm
ed
dat
a
Chapter 5 Seasonal variability in an estuarine beach
171
Figure 6. Temporal variations in total organic carbon (TOC), total nitrogen (TN),
complex organic matter (COM) and Chl a concentrations (µg g-1 sed d.w. ± standard
deviation) with tidal levels and sediment depths. (+Chl a data was log-transformed).
4.5.4. Discussion
4.5.4.1. Benthic macrofauna community.
Analysis of distribution of benthic macrofauna from the studied beach
demonstrated that the tidal levels sampled were characterised by distinct faunal
densities and species composition. Polychaetes and molluscs occurred mainly
at the intertidal level and crustaceans tended to occur higher on the shore as
they are less susceptible to desiccation. Abundance, biomass and number of
species were negatively related to sediment depth. Differences in depth
0-5 cm 5-10 cm 10-15 cm 15-20 cm 20-25 cm depth
HTL
MTL
LTLLTL
Ja97 A97J97O97Ja98 A98J98 O98Ja99
Chl a+ (µg g-1 d-1 sed d.w.)
0,01
0,1
1
10
0,01
0,1
1
10
0,01
0,1
1
10
Ja97 A97J97O97Ja98 A98J98 O98Ja99
COM (µg g-1 sed d.w.)
0
2000
4000
6000
8000
10000
12000
14000
0
2000
4000
6000
8000
10000
12000
14000
0
2000
4000
6000
8000
10000
12000
14000
TOC (µg g-1 sed d.w.)
0
2000
4000
6000
8000
10000
12000
14000
0
2000
4000
6000
8000
10000
12000
14000
0
2000
4000
6000
8000
10000
12000
14000
Ja97 A97J97O97Ja98 A98J98 O98Ja99
TN (µg g-1 sed d.w.)
0
200
400
600
800
1000
1200
1400
0
200
400
600
800
1000
1200
1400
0
200
400
600
800
1000
1200
1400
Ja97 A97J97O97Ja98 A98J98O98Ja99
Chapter 5 Seasonal variability in an estuarine beach
172
distribution of organisms could be related to differences in sediment
characteristics that conditioned organism’s ability to burrow. Variations in
mean grain size and compactness with sediment depth (higher M.G.S and S.S.)
and tidal level (lower M.G.S and higher S.S. at the MTL) could influence
macroinfauna distribution in the intertidal. Sediment characteristics, however,
were not able to explain macroinfauna variation alone. Several works have
noted that vertical zonation could be further controlled by the position of the
Redox Potential Discontinuity (RPD) layer since animals are dependent on
dissolved oxygen for their respiration (Rosenberg et al., 2003; Steyaert et al.,
2003). The RPD was found in the intertidal level at the 5-10 cm depth and
macroinfauna was mainly concentrated on the sand surface or subsurface
(~75%).
The intertidal levels on sheltered beaches are considered to be under
optimal environmental conditions in terms of humidity, temperature and food
supply for marine macroinfauna. These beaches are not as physically controlled
environments as exposed beaches and benthic macrofauna will be favoured by
accumulations of organic matter (Defeo et al., 2001; Incera et al., 2006; Rodil
et al., 2007). Maximum concentration of BPC; i.e., food available, was found at
the MTL. The presence of larger amounts of organic matter (macroalgae
coverage), higher biochemical concentrations and water content could promote
higher macroinfauna abundances and species richness at the MTL rather than at
the LTL.
Most of the species inhabiting the intertidal level belonged to the
deposit-feeder’s group, favoured by organic rich supply on the sediment
surface during winter and spring. Deposit-feeders are able to rapidly exploit
food resources and conspicuous abundance of this trophic group has been
related to a marked increase in proteins (Rossi et al., 2001). The occurrence of
suspension feeders was restricted to the lower intertidal level, probably because
they can only feed at high tide and they cannot exist where submergence is
brief (Dittman, 2000). Bivalves were scarce in April, probably due to the local
clam gathering activities during the previous months. The increase in mollusc
density and biomass in July could be explained by the obligatory close season
Chapter 5 Seasonal variability in an estuarine beach
173
starting in April (see http://www.pescadegalicia.com). Clam and cockle
collection by hand is a common activity in this area which involves regular
sediment disturbance and also macroalgae removal. Some of the changes
presented over time in the macroinfauna community from Barraña could be an
echo of disturbance effects rather than of trophic responses.
Despite the constant dominance of few abundant species on this beach,
high variability of the community was observed throughout the study period.
Several works have suggested that further control of the structure and dynamics
of the macroinfauna community from the intertidal could be related to
fluctuations in the availability of food resources (e.g. Rossi et al., 2001).
4.5.4.2 Spatial and temporal changes in organic matter composition and
Chl a content.
The high concentrations of biochemical compounds recorded in the
sediment could be related to the specific characteristics of this beach; i.e.
sheltered conditions favour accumulation of organic matter in the intertidal
(Nordström, 1992, Cividanes et al., 2002).
From analysis of the biochemical composition of organic matter, the
BPC accounted for about 44% of TOC and proteins were the dominant fraction
of BPC (58%). A significant fraction of the BPC (42%) was presented as
material of a more refractory composition but the overall organic matter can be
considered of recent production. The PROT:CHO ratio, displayed high values
(5.2), indicating that protein availability should not be considered as a limiting
factor for benthic consumers (Fabiano et al., 1995). The rise in proteins meant
an increment in the quality of food available and the particularly high protein
values recorded in winter could be related to allochthonous inputs, reflecting
the characteristics of a eutrophic system (Danovaro, 1996).
Chapter 5 Seasonal variability in an estuarine beach
174
Table 4. Summary of results from BIO-ENV. Combination of n environmental
variables, k variables at a time (1,2,3,…n), giving largest rank correlations (ρs) between
biotic and abiotic similarity matrices for each k. Bold indicates best combination
overall. MGS: Mean grain size; WC: water content; BPC: biopolymeric carbon; TOC:
total organic carbon; COM: complex organic matter; Chl a: chlorophyll a.
Barraña is located at the inner part of the ria where the deposit of
terrigenous and anthropogenic material was present along the intertidal level
(Cividanes et al., 2002). This could to some extent, be related to the seasonal
variability found in the organic matter availability. There was a decrease in the
PROT:CHO ratio in summer and at the beginning of autumn, probably because
of the lack of sea input, low river flux, high temperatures and solar radiation
which usually characterise this season. During this period of the study, less
amount of algal detritus (field observation) and high values of refractory
organic matter were found, suggesting scarce availability and low quality of
food resources. The progressive decomposition of this debris during summer
could cause a rapid depletion of the labile fraction and an accumulation of the
most refractory components such as carbohydrates and lipids (Danovaro et al.,
2002). This suggests the presence of aged organic matter with a largely detritic
origin caused by the algal-wrack decomposition. Carbohydrate concentrations
were higher in July and October, which could be related to the macroalgae
accumulation and consistent decomposition process; while, proteins displayed
higher values in winter and spring.
k Best variable combinations (ρs)
1 TOC
(0.475)
2 WC; TOC BPC; TOC
(0.487) (0.483)
3 WC; BPC; TOC WC; TOC; COM
(0.486) (0.477)
4 WC; BPC; TOC; COM WC; BPC; TOC; C:N
(0.487) (0.506)
5 MGS; prot:cho; TOC;COM;C:N WC; BPC; TOC; COM; C:N MGS; BPC; TOC; COM; Chl a
(0.514) (0.510) (0.473)
Chapter 5 Seasonal variability in an estuarine beach
175
Inte
rcep
t M
GS
E
h
WC
B
PC
T
OC
C
OM
C
:N
Ch
loro
ph
yll
a
Abundan
ce
Est
imat
e 1.5
7
-0.0
01
-0
.001
0.0
5
0.4
5
0.4
7
-0.1
4
0.0
7
-0.0
01
S
tandar
d e
rror
0.5
4
0.0
01
0.0
00
0.0
2
0.1
2
0.0
6
0.0
6
0.0
1
0.0
4
W
ald s
tati
stic
8.6
1.2
24.9
7.1
2
15.1
66.8
6.1
5
159.4
1
0.0
01
AIB
+
Est
imat
e 4.0
4
-0.0
1
0.0
01
-0.0
5
-0.6
7
0.1
7
0.1
8
-0.0
2
0.4
8
S
tandar
d e
rror
0.8
9
0.0
01
0.0
00
0.0
3
0.2
0
0.0
9
0.0
8
0.0
1
0.0
5
W
ald s
tati
stic
20.5
6
37.4
2
2.5
5
2.6
0
11.0
1
3.4
6
4.7
2.4
3
81.5
Ab
ud
an
ce o
f m
ain
gro
up
s
Poly
chae
ta
Est
imat
e 0.8
1
-0.0
03
-0
.001
0.0
8
1.2
6
0.0
5
0.2
2
0.0
7
0.1
1
S
tandar
d e
rror
0.7
9
0.0
01
0.0
00
0.0
3
0.1
7
0.0
8
0.0
9
0.0
1
0.0
5
W
ald s
tati
stic
1.0
5
11.0
7
22.0
4
8.7
7
52.6
1
0.3
4
5.9
0
78.4
1
4.7
2
Moll
usc
a E
stim
ate
-7.8
1
0.0
05
-0
.001
0.3
1
-0.1
3
0.5
1
0.1
1
0.0
9
-0.3
2
S
tandar
d e
rror
1.0
8
0.0
01
0.0
00
0.0
4
0.1
7
0.0
8
0.0
8
0.0
11
0.0
7
W
ald s
tati
stic
52.0
4
20.9
7
1.3
1
65.1
0.6
2
39.1
2
1.5
7
64.5
19.4
Cru
stac
ea
Est
imat
e 19.4
-0
.01
-0
.02
-0.4
1
2.9
4
2.0
4
-3.6
7
0.1
1
0.0
9
S
tandar
d e
rror
2.0
3
0.0
02
0.0
02
0.0
7
1.2
3
0.3
8
0.4
7
0.0
2
0.1
2
W
ald s
tati
stic
91.2
29.6
3
108.3
36.3
5.6
27.9
61.3
27.1
0.5
7
T
ab
le 5
. S
um
mar
y o
f th
e gener
alis
ed l
inea
r m
od
els
(Po
isso
n d
istr
ibuti
on)
ind
icat
ing
var
iab
les
that
wer
e si
gnif
ican
t (i
n b
old
). M
.G.S
.: m
ean
gra
in s
ize;
Eh:
red
ox p
ote
nti
al;
W.C
.: w
ater
co
nte
nt;
BP
C:
bio
po
lym
eric
car
bo
n;
TO
C:
tota
l o
rgan
ic c
arb
on;
CO
M:
com
ple
x o
rganic
matt
er.
+T
he a
ver
age i
nd
ivid
ual
bio
mass
(A
IB)
in e
ach
sam
ple
was
calc
ula
ted
as
bio
mas
s d
ivid
ed b
y a
bund
ance
per
sp
ecie
s (m
g m
-2 d
ry w
eig
ht)
and
it
was
use
d a
s an e
stim
atio
n o
f th
e av
erag
e o
rgan
ism
siz
e
Chapter 5 Seasonal variability in an estuarine beach
176
High TOC concentrations and low BPC:TOC ratio supported these
findings related to the carbohydrate increase during summer. Allochthonous
inputs are usual incidents during winter, due to weather conditions, which
promote accumulation of dead seaweed on the beach face and therefore
introduce new organic matter in the intertidal. Some benthic animals may
indeed benefit from drifting algal mats as a key resource; i.e food and/or
refuge, and its availability can affect diversity and abundance of intertidal
animals including shorebirds (e.g. Norkko and Bonsdorff, 1996; Colombini and
Chelazzi, 2003; Dugan et al., 2003; Kelaher and Levinton, 2003). Intermediate
amounts of drift algae increase the nutrient levels and it is under such
conditions that macrofauna are most likely to utilise the extra organic material
(Norkko and Bonsdorff, 1996; Nordström, et al., 2006). Although low BPC
concentrations were found at the HTL, the high BPC:TOC percentage at the
supratidal suggests an improvement of the organic matter quality which will
benefit macroinfauna dwelling at this level. These findings were also supported
by the low C:N ratio found which points to a high nutritive organic matter.
Chlorophyll a concentrations in the sediment are used as a proxy of the
amount of organic matter produced by benthic microalgae. Large fluctuations
in the concentration of Chl a were found in January, in line with the literature
which reported frequently peaks during winter and spring (e.g. Trueblood et al.,
1994; Rossi, 2002). The particularly high values of Chl a observed in January
1997 at the MTL are difficult to explain. High deposition of algal detritus and a
low decomposition rate over the winter period can create an ideal environment
for microbial productivity with a subsequent increase in photosynthetic activity
(Kelaher and Levinton, 2003). The following months were characterised by
high macroinfauna abundance and biomass when temperatures increase. The
increased availability of microbial biomass could further increase the
abundance and biomass of the macroinfauna such as deposit-feeding
invertebrates inhabiting the intertidal during that time. Overall mean values of
Chl a were low because of the low concentrations found at the supratidal level,
but data from the mid-low tidal levels (4.65±2.1 and 7.6±5.2 µg g-1 sed dw)
Chapter 5 Seasonal variability in an estuarine beach
177
PCA Axis I
PC
A A
xis
II
-0.6 1.0
-0.4
0.6
Tidal level
Sed dept
MGS
Shear strength
Eh
T
Water contentprot
cho
lip
prot:cho
BPC
TOC
BPC:TOC
TN
C:N
Chl-a
implied a very important contribution of autochthonous primary production and
classified this beach as organic marine rich system (Fabiano et al., 2004).
Figure 7. Projection of the considered variables (i.e., environmental variables,
sedimentary organic matter and biochemical compounds and macroinfauna
characteristics) in the first plane of the PCA based on the measurements carried out
during the study period.( : average individual biomass;
: biomass; : number of species;
: mean abundance; : abundance of crustaceans;
: abundance of polychaetes; : abundance of
molluscs). The average individual biomass was calculated as biomass divided by
abundance per species and it was used as an estimation of the average organism size
4.5.4.3. Relationships between environmental variables and benthic
macrofauna.
This study showed the importance of food availability in a benthic
macrofauna community that relied on seasonal deposition of sedimentary
organic matter at the intertidal. Food quality and quantity have the potential to
cause substantial spatio-temporal variation in the structure of macrofauna
Chapter 5 Seasonal variability in an estuarine beach
178
assemblages in estuarine beaches. This conclusion is supported by PCA and
multiple regression analysis which indicated that biochemical compounds and
Chl a were the main factors explaining benthic macrofauna distribution in the
intertidal level. Macroinfauna characteristics and abiotic factors such as organic
matter and Chl a, were always found to be higher at the intertidal level, where
swash action occurs, than at the supratidal. The swash zone has been
considered a key area controlling macroinfauna from the intertidal and the
importance of the swash climate on the macrofaunal assemblages and on the
food available present in sediments of sandy beaches has been recently stated
(Incera et al., 2006). Although it was shown that inputs of microalgae biomass
can occur in winter and contribute to increase the nutritional value of the
sediment, a general pattern of increasing resources of food in winter and/or in
spring and decreasing in summer and autumn is not possible to refer to here.
We can elucidate that there was an increase in quality of the food available in
winter due to the higher protein concentrations meaning that the organic matter
was recently produced at that time. However, in summer and late summer there
was an accumulation of aged organic matter.
Multiple regression analysis were in line with the PCA and BIO-ENV
results and a positive correlation between sedimentary organics and
macroinfauna characteristics, such as biomass, macrofauna abundance and
abundance of polychaetes and crustaceans, was found. These analyses showed
the existence of tight relationships between macroinfauna and food quality but
the distributions of factors such as pigment and nutrients are often depth
dependent. Therefore, caution is called for when correlating depth profiles of
different variables. There is a positive relationship between BPC and
macroinfauna, but GLM showed some lack of fit between biochemical
compounds and quantitative characteristics of macroinfauna. This could be
related to the concentrations of carbohydrates (14%) and to the lipids (28%)
which are compounds with a more refractory composition than proteins.
The conclusions from this study should be treated as predictions that
point to the most important experimental manipulation to be conducted next.
This study showed that macrofauna from estuarine sheltered beaches is not just
Chapter 5 Seasonal variability in an estuarine beach
179
driven by physical forces (e.g. level of dryness, wave action) but also by the
distribution of its primary food sources. Macrofauna organisms showed
preferences both in vertical and horizontal ranges suggesting a specific
distribution which is related to specific sensitivity by several abiotic factors,
including food availability. In relation to this, the assessment of vertical and
horizontal variability and the relative structure of the macroinfauna community
displayed a strong heterogeneity over time, suggesting that macrofauna in
estuarine beaches can be related to complex and unpredictable factors.
Acknowledgements
The authors thank the “Benthos Team” from the University of Vigo for
their assistance during sampling. We are grateful to three anonymous
reviewers, whose critical and constructive comments strengthened this paper.
This research was supported by the Regional Government of Galicia
(PGIDIT02RMA30101PR) and the University of Vigo (C505 122F 64102). I.F.
Rodil was supported by a Ph.D. grant from the Xunta de Galicia (programa
María Barbeito).
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cultrifera and their resources of food in a Mediterranean mudflat.
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deposit-feeder assemblage and sedimentary organic matter in a
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Vincx, M. 2003. The importance of fine-scale, vertical profiles in
characterising nematode community structure. Estuarine Coastal and
Shelf Science 58:353-366.
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Limnology and Oceanography 39: 1440-1454.
Chapter 6. Differential effects of native and invasive algal
wrack on macrofaunal assemblages inhabiting exposed
sandy beaches.
Chapter 6 Effect of native and invasive algal wrack
183
Abstract
Many sandy beaches worldwide receive large amounts of drift seaweed,
known as wrack, from offshore algal beds and closer rocky intertidal shores.
Despite the important influence of algal wrack on macrofaunal assemblages from
different coastal systems, relatively little attention has been paid to the
macrofaunal responses in sandy beaches to macrophyte wrack supplies. Algal
wrack is a key resource, i.e. for food and/or refuge, for beach invertebrates while
its availability can affect diversity and abundance of intertidal animals including
shorebirds, but the role of certain types of wrack and its location on the shore has
not been examined experimentally to date. In this paper, we use experimental
manipulation of two species of brown seaweeds, i.e. artificial wrack patches made
up of the native macroalgae Saccorhiza polyschides (Lightfoot) Batters and the
invasive species Sargassum muticum (Yendo) Fensholt, to test hypotheses about
influences on macrofaunal assemblages inhabiting the drift line and supratidal
levels of exposed beaches. Results pointed out that different types of wrack
deposits were not used uniformly by invertebrates. Nutritional value differed
between the two species of wrack. In most cases, the carbohydrates, lipids and
organic carbon content were greater in patches of S. muticum than in patches of S.
polyschides. Data also provided evidences that nutritional content and
microclimatic conditions of wrack deposits, i.e. temperature and humidity,
affected macrofaunal assemblages.
Keywords: invasive species; experimental manipulation; macrofaunal
assemblages; macroalgal wrack; sandy beaches.
4.6.1. Introduction
Many sandy beaches worldwide receive large amounts of drift seaweed
from offshore algal beds and closer rocky intertidal shores (Inglis, 1989; Rossi
and Underwood, 2002; Dugan et al., 2003). Macrofauna inhabiting exposed
sandy beaches is basically dependant on phytoplankton and marine
macrophytes inputs because of the scant primary production occurrence on this
Chapter 6 Effect of native and invasive algal wrack
184
habitat itself (Inglis, 1989; Dugan et al., 2003; McLachlan and Brown, 2006).
The importance of beach accumulations of wrack on the ecology of sandy
beaches has been previously documented in the literature (see Colombini and
Chelazzi, 2003 and references therein). Algal wrack deposits represent the
main food resource for upper shore detritus feeders such as talitrid amphipods,
tylid and oniscoid isopods besides tenebrionid and staphylinid beetles
(Colombini et al., 2000; Dugan et al., 2003). Wrack also acts as a refuge for the
supralittoral fauna, mainly terrestrial and semiterrestrial arthropods, providing
an opportunity to study seaweed debris both as a food resource and shelter
habitat (Inglis, 1989; Colombini et al., 2000; Jędrzejczak, 2002a, b; Olabarria
et al., 2007).
Despite the important influence of algal wrack on macrofaunal
assemblages from different coastal systems, relatively little attention has been
paid to the macrofaunal responses in sandy beaches to macrophyte wrack
supplies (see Olabarria et al., 2007). Algal wrack is a key resource for beach
invertebrates and its availability can affect diversity and abundance of intertidal
fauna including shorebirds (Dugan et al., 2003; McLachlan and Brown, 2006),
but the role of type of wrack and its location on the shore has not been
examined experimentally so far. On sandy beaches, wrack is deposited
throughout the entire intertidal range creating a patchy scenario of bare and
wrack occupied areas (Valiela and Reitsma, 1995; Colombini et al., 2000;
Rossi and Underwood, 2002). Sandy beaches are by no means homogeneous
habitats. Not only they reflect macroinvertebrate patchiness, but also reflect
important changes in structure and biodiversity of assemblages along their
slope (see McLachlan and Jaramillo, 1995). The spatial distribution of wrack
debris along the beach profile should be a very important factor since the
higher the seaweed is located on the beach the longer it is presumably present
on the intertidal zone. Close to the swash zone, in the lower part of the
intertidal, mats of wrack are mainly driven by the physical forces of waves,
tides and sediment movement during the entire period of stranding. Wrack
deposits at the supratidal undergo dehydration, ageing and finally become
covered by wind-blown sand. After a period of decomposition and decay,
Chapter 6 Effect of native and invasive algal wrack
185
wrack will release nutrients, particularly N and P, which can enhance benthic
microalgae and stimulate growth of aerobic and anaerobic bacteria. Processes
are complex and depend on the amount and taxonomic composition of wrack
(Rossi and Underwood, 2002; Jędrzejczak, 2002a). For example, different
seaweeds may vary in physical structure (levels of branching, toughness),
nutritional values and decomposition rates which could potentially influence
wrack-associated macrofauna. Different physical structures of seaweeds may
also modify microclimatic conditions, i.e. temperature and humidity of wrack
deposits. Therefore, different types of wrack might influence the structure and
function of animal assemblages and determine taxonomic composition, number
and turnover of species. In fact, several studies indicate that population
densities, behaviour and feeding rates of invertebrates on sandy beaches are
likely affected by the type of macroalgal wrack arriving to the intertidal (e.g.
Valiela and Rietsma, 1995; Colombini et al., 2000; Pennings et al., 2000;
Goecker and Kåll, 2003).
Accumulations of dead seaweed on the beach face are a ubiquitous
feature of Galician sandy beaches (NW Spain), where heaps of macroalgae
frequently stranded, mainly consisting of brown macrophytes such as
Saccorhiza polyschides, Sargassum muticum, Fucus spp., and Laminaria
saccharina (Olabarria et al., 2007). The amount and type of stranded material
also vary at different spatio-temporal scales. In summer, for example,
considerable amounts of S. polyschides and S. muticum are stranded on beaches
creating a mosaic of bare and wrack affected areas (pers. obs.). In this context,
it would be interesting to take heed of the effect of both species on the
macrofaunal assemblages inhabiting exposed sandy beaches. Another
important point to consider is the origin of both species, since S. polyschides is
a native seaweed species, whereas S. muticum is an invasive species. This
species is native to SE Asia, but its actual distribution as invasive algae is
spanned all through the world, including Europe, the Mediterranean Sea and
the west coast of North America (Britton-Simmons, 2004). This seaweed has
been first reported in Spain in 1985 (Casares et al., 1987) invading rapidly the
highly productive rocky shores or macroalgae beds. It was first observed on the
Chapter 6 Effect of native and invasive algal wrack
186
Galician coast in 1986 (see Pérez-Cirera et al. 1989) and has successfully
colonised most of the Galician estuaries increasing its abundance rapidly. The
rapid spread of S. muticum might have important effects on the composition,
structure and organization of local assemblages on rocky shores and sandy
beaches (via stranded seaweed). In fact, exotic species have been reported to
have strong impacts on local ecosystems, changing species diversity, trophic
structure and dynamics of populations, negatively affecting ecosystem
processes (Carlton, 1996). So far, no studies have compared the effects of types
of stranded seaweed (native versus exotic species) on macrofaunal assemblages
dwelling on exposed sandy beaches.
In this paper, we used experimental manipulation of two types of
brown seaweeds, i.e. artificial wrack patches comprising the native macroalgae
S. polyschides and the invasive species S. muticum, to test hypotheses about
influences on macrofaunal assemblages inhabiting the drift line and supratidal
zone (i.e. dune) at two different sites along an exposed sandy beach. In
particular, we test the hypothesis that (1) the microclimatic conditions, i.e.
temperature and humidity, vary between both types of wrack, (2) the nutritional
content of the two types of wrack is different, (3) abundance of colonizing
individual and species differ in the two types of wrack, (4) succession varies
between wrack types, and (5) as a result, macrofaunal assemblages are different
in each type of wrack. Furthermore, we predicted that responses in wrack
patches located at the drift line would differ from the patches located at the
supratidal because wrack patches placed at this level remain longer on the
beach. Finally, we predicted that responses could differ among sites because of
their slightly different environmental conditions.
4.6.2. Methods
4.6.2.1. Study area
The study site of Ladeira (42º 34’ 33’’N; 9º 3’ 16’’ W) is an
intermediate exposed sandy beach about 1400 m long and 130 m wide (low
spring tide), sheltered by a large and active dune system, located in the
Chapter 6 Effect of native and invasive algal wrack
187
Corrubedo beach-lagoon complex. This beach is influenced by a mesotidal
regime with a medium tidal range of 3 m.
Two sites about 500 m apart were chosen for this experiment (Site A
and Site B, hereafter). Site A was located at the northern part of the beach,
while site B was located at the southern part. The environmental characteristics
of the two sites differed slightly in terms of the slope, granulometry,
temperature and wind exposure. The slopes varied between 1/27 (Site A) and
1/24 (Site B). Sand was mainly made of fine fraction ranging from 251.2±24.8
(Site B, Drift) to 182.4±1.34 µm (Site A, Drift) and sediments were well sorted
varying between 1.34±0.07 and 1.56± 0.02 φ at Sites A and B respectively.
Temperature in the sediment underneath wrack patches ranged from 30.6±0.47
(Site A, Dune) to 31.6±0.94 ºC (Site B, Dune), whereas temperature in bare
sediment ranged from 29.7±0.94 (Site A, Dune) to 30.1±0.73 ºC (Site B,
Dune). The predominant wind was from northerly (F3,3= 12.26; P< 0.05) being
more intense at Site A (F1,64= 8.71; P< 0.01; SNK tests, P< 0.05).
4.6.2.2. Experimental design
The experiment started on 13 June 2006 and lasted for 21 days.
Manipulative experiment was performed at Sites A and B. The day before
starting the experiment, 250 kg of fresh seaweeds, S. polyschides and S.
muticum, were collected by hand from surrounding rocky intertidal areas, taken
to the laboratory, weighed and separated in plastic bags of 2.5 kg ±0.50 g. At
the field, medium squared-patches (0.25 m2; 2.5 kg ±0.50 g wet weight) of the
two types of seaweed (twelve patches of each type) were haphazardly placed
on the highest mark of the drift line and on the base of the dune parallel to the
shoreline, i.e. 24 patches per tidal level (N= 48 per site). Each patch was placed
1 to 2 metres apart and its location on the beach determined by calculating a
random distribution on the computer.
On days 3, 7, 12 and 21 of the experiment, three randomly chosen
replicate patches of each type of wrack were collected at each site from the
dune and also from the drift line. The associated fauna was retained by
enclosing each patch within a 50 x 50 sieve of 1 mm mesh size. Then
Chapter 6 Effect of native and invasive algal wrack
188
insecticide was sprayed to prevent mobile fauna, such as adult dipterans and
coleopterans, from escaping, and after 5 minutes, the seaweed and any visible
fauna transferred to a plastic bag. Macrofauna underneath each wrack patch
was also collected with a 10 cm diameter stainless-steel corer penetrating 20
cm depth into the substratum (n = 3). Samples were taken from the centre of
the patches to avoid possible edge effects. Three control replicates (3 cores per
replicate), 50 cm apart from the wrack patches and separated by 1 m, were also
taken at each site in order to measure the normal abundance of invertebrates in
nearby bare sediment.
Subsamples of wrack (± 5 g) for biochemical composition analysis
were collected (n=3) at each time and frozen at -30ºC until further processing.
In addition, temperature (˚C) was measured inside the wrack patches (n=3).
Four aeolian sediment traps were buried vertically with their rims flush with
the beach surface in the dune of both sites surrounding the wrack patches. An
inlet and an outlet tube, connected to the chamber trap, were exposed and
orientated to the main wind directions. These devices were designed as
sediment collectors in order to assess the intensity of aeolian processes and to
measure horizontal sediment transport by wind (Goossens and Offer, 2000).
The amount of sand collected on sampling days was measured as relative total
grain mass (g day-1) and the predominant wind direction was established.
During the whole experiment none of the sediment traps were found totally
filled up by wind action.
4.6.2.3. Laboratory analysis
Sediment samples (n=3) from underneath wrack patches were weighed
and then oven-dried at 60ºC until a constant weight was obtained. Sediment
water content; i.e. humidity, was estimated as the difference between wet and
dry weight.
Wrack patches were collected, washed and sieved through a 1 mm
mesh. The retained macrofauna was sorted and identified to the lowest possible
taxonomic level. The total organic matter of wrack was measured as the
difference of dried seaweed (60ºC to a constant weight) before and after
Chapter 6 Effect of native and invasive algal wrack
189
ignition in a muffle furnace at 500 ˚C for 4 hours. Estimating total organic
matter content in wrack does not provide a good indication of the portion
available for consumers. Therefore, the nutritional value of the wrack during
the decay process was done through the determination of the main biochemical
classes of organic compounds (i.e. carbohydrates, proteins and lipids) which
are assumed to estimate the food potentially available for consumers, either
bacteria (Fichez, 1991; Fabiano et al., 1995; Dell’Anno et al., 2000) or higher
trophic levels (Dugan et al., 2003). For all analyses, about 0.15-0.2 g of
seaweed frond subsamples were used for each analysis (data normalized to
seaweed dry weight). All biochemical analyses were conducted on samples
previously oven dried at 60 ºC until constant weight was achieved and finely
powdered with a pestle. Total lipids (Bligh and Dyer, 1959; Marsh and
Weinstein, 1966), carbohydrates (Dubois et al., 1956) and proteins (Markwell
et al., 1978) were analysed and measured as μgg-1. The sum of the main
biochemical classes was reported as the biopolymeric carbon (BPC sensu
Fichez, 1991) assumed as a reliable estimate of the labile fraction available to
benthic consumers. Analyses of dry weight samples (n=3) of Chlorophyll a
(Chl a, μg g-1) from seaweed fronds were extracted following Lorenzen (1967).
Chl a can be used as a surrogate of benthic microalgae biomass (Rossi and
Underwood, 2002).
4.6.2.4. Statistical analysis
Changes in number of individuals, number of species, abundance of
main representative species and diversity (Shannon-Weaver index) were
analysed using a 4-factor orthogonal analysis of variance. Moreover, changes
in the content of organic matter, carbohydrates, lipids, proteins and chlorophyll
a in the wrack were also analysed following the same model. Type of wrack (2
levels), Height on the shore (2 levels), Time (4 levels) were fixed factors and
Site (2 levels) was random. Any interaction that was sufficiently small with a
probability ≥0.25 was pooled. Before analysis, the homogeneity of variances
was evaluated with Cochran’s test (Winer et al., 1991) and data were
Chapter 6 Effect of native and invasive algal wrack
190
transformed when necessary. A posteriori multiple comparisons were done
using Student-Newman-Keul’s (SNK) tests (α= 0.05).
Four factor orthogonal non-parametric multivariate analyses of
variance (PERMANOVA) were used to test the hypothesis about differences
among wrack-associated macrofaunal assemblages (Anderson, 2001). Only
significant effects (p<0.05) were further investigated through a series of pair-
wise comparisons using the appropriate terms in the model. This statistical
method was used because experiment designs were relatively complex
(involving four factors) and because, similar to most other studies on
assemblages, the data did not meet the assumptions of traditional multivariate
statistical analyses (e.g., MANOVA). This method improves on previous ones
because it allows the direct additive partitioning of variation, which enables
tests of multivariate interactions in complex experimental designs. The statistic
test (pseudo-F) is calculated from a symmetric dissimilarity matrix. P-values
are then obtained by permutation tests. Here, the P-values for each term in the
model were generated using 5,000 permutations. To graphically visualize
multivariate patterns in assemblages, non-metric multidimensional scaling
(nMDS) was used to produce two-dimensional ordination plots. Species that
mostly contributed to the dissimilarity/similarity among the two types of wrack
were identified using SIMPER analysis (Clarke, 1993). The BIO-ENV analysis
(PRIMER) was used as an exploratory tool to define suites of abiotic variables
that best determine the macrofaunal assemblages. For that purpose, biotic and
abiotic matrices were constructed using Bray-Curtis dissimilarity (square-root
transformed) and Euclidean distances, respectively.
To compare the relationships between presence/absence of main taxa,
total number of individuals, total number of species, diversity and abiotic
variables, two types of regression models were used. Firstly, we used the
logistic regression model, which falls within the general framework of GLMs
(McCullagh and Nelder, 1989), to analyse the relationship between a binary
response variable (presence/absence) and several explanatory variables (abiotic
predictors). All variables were simultaneously used in a forward multiple
logistic-regression analysis to derive a multivariate model that would predict
Chapter 6 Effect of native and invasive algal wrack
191
the presence or absence of main taxa. The odds of an event occurring (i.e. the
probability an event occurs relative to its converse) were calculated in order to
know if there was a relationship between the presence of the species and each
of the predictor variables. Secondly, we used a GLM with a Poisson error term
and a log link function, known as a log-linear model, which can be used
effectively when the predictors are continuous and the response variable is a
count (Quinn and Keough, 2002). This model is more flexible and better suited
for analyzing ecological relationships that can be poorly represented by
classical Gaussian distributions (Guisan et al., 2002 and references therein).
The significance of the independent variables was tested using the χ2-test
(P<0.05) on the Wald statistic (Statistica 6.0).
Source Humidity Temperaturea,b
df MS F MS F
Wrack (W) 1 1027.75 84.81 0.0092 49.33
Site (S) 1 0.938 1.08 0.0701 54.86***
Height (H) 1 1.281 0.29 0.0013 0.77
Time (T) 3 3.61 0.95 0.0429 0.86
W X S 1 12.119 14.01*** 0.0002 0.15
W X H 1 1.629 0.40 0.0006 19.70
W X T 3 2.491 4.85 0.0297 14.40*
S X H 1 4.459 5.16* 0.0017 1.31
S X T 3 3.795 4.39*** 0.0500 39.14***
H X T 3 0.284 0.22 0.0000 0.00
W X S X H 1 4.046 4.68* 0.0000 0.02
W X S X T 3 0.513 0.59 0.0021 1.61
W X H X T 3 0.393 1.49 0.0154 2.77
S X H X T 3 1.322 1.53 0.0016 1.26
W X S X H X T 3 0.264 0.31 0.0055 4.33**
Residual 64 0.864 0.0013
*p<0.05
**p<0.01
***p<0.001 a ln (x+1) tranformed data bsignificant differences with control data (bare sediment)
Table 1. Summary of analyses of variance for Temperature (ºC) and Humidity (%) in
wrack patches at the different sites and heights on the shore.
Chapter 6 Effect of native and invasive algal wrack
192
4.6.3. Results
4.6.3.1. Microclimatic conditions of wrack patches: humidity and
temperature
Humidity varied between wrack patches, but the variation was not
consistent across heights on the shore and sites (i.e. a significant Wrack x Site x
Height interaction, P< 0.05; Table 1). Humidity was higher in patches of S.
polyschides than S. muticum, but only in the dune at Site A (SNK tests, P<
0.05). Temperature measured inside the patches differed between wrack types,
but, once again, differences were not consistent over space and time (i.e.
significant Wrack x Site x Height x Time interactions; Table 1). For example,
at site A, temperature in patches of S. polyschides was higher than in patches of
S. muticum, but only in the dune on day 12 and in the drift line on day 3 (SNK
tests, P< 0.05). At site B, temperature in patches of S. polyschides was higher
than in patches of S. muticum in the drift line on days 3 and 12 and in the dune
on day 12 at Site B.
4.6.3.2. Analysis of the total organic matter and nutritional value
Total organic matter varied significantly among wrack types (Table 2),
but this variation was not consistent between sites and heights on the shore (i.e.
a significant Wrack x Site x Height interaction, P<0.05). The total organic
matter was greater in patches of S. muticum than in S. polyschides at all sites
and heights on the shore (Figs. 1a, b, c, d). However, there was more organic
content in patches of S. muticum in the dune at Site A than at Site B (Fig. 1a, b;
SNK tests, P< 0.05). In contrast, patches of S. polyschides in the dune had more
organic content at site B than at Site A. (Fig. 1a, b; SNK tests, P< 0.05).
Chapter 6 Effect of native and invasive algal wrack
193
S
ou
rce
Org
an
ic m
att
er
P
rote
ins
b
C
arb
oh
yd
rate
sa,b
Lip
ids
a,b
B
PC
b
Ch
l a
df
MS
F
MS
F
MS
F
MS
F
MS
F
MS
F
Wra
ck (
W)
1
5006
73
46.3
374.0
6
925.9
6**
* 2.2
5
178.1
+
0.7
5
123.5
+
6096
570
.5
429.8
*
1411
89.4
199.9
*
Site (
S)
1
1485
.8
4.4
5*
6688
1.8
12.3
2**
* 0.0
1
0.9
2
0.0
5
2.1
4
1551
02.0
5
6.3
4*
1273
2.8
6.8
*
Heig
ht (H
) 1
1530
.5
1.1
2
2195
64.6
3.3
3
0.3
5
354.3
*
0.1
3
3.1
0
6331
01.8
3.6
2
1513
.7
0.4
1
Tim
e (
T)
3
2376
.8
14.1
4*
1754
970
.4
95.8
***
6.3
7
40.7
4**
* 6.6
4
104.6
**
8756
419
.6
252.1
***
5437
16.7
681.7
***
W X
S
1
1080
6.2
32.3
***
0.0
76
0.0
0
0.0
1
1.1
2
0.0
1
0.2
5
2509
.11
0.1
0
706.3
3
0.4
W X
H
1
3521
.3
1.3
5411
6.7
6.0
1
0.0
8
2.2
7
0.1
8
4.4
5
1174
52.3
0.7
4
2285
.4
21.9
4
W X
T
3
469.5
0.7
2
1495
1.1
0.9
9
0.3
1
29.1
1*
0.1
1
13.7
2*
9545
17.5
25.9
3*
2837
3.6
81.1
**
S X
H
1
1361
.3
4.1
6597
6.9
12.2
***
0.0
01
0.0
9
0.0
4
1.8
4
1749
17.1
5
7.2
**
3690
.24
1.9
6
S X
T
3
168.0
4
0.5
1832
2.7
3.4
*
0.0
1
0.5
4
0.0
6
2.6
5+
7441
4.5
3.0
4*
797.5
8
0.4
2
H X
T
3
70.1
1.9
4999
.72
0.1
1
0.0
5
9.0
1+
0.2
9
8.1
+
2911
6.9
0.2
4
1386
.94
0.1
7
W X
S X
H
1
2702
.7
8.1
**
9003
.56
1.7
0.0
4
3.4
0.0
4
1.7
1587
40.7
6.5
*
104.2
0.0
6
W X
S X
T
3
652.6
1.9
5
1507
0.1
2.8
+
0.0
1
0.9
4
0.0
1
0.3
2
3681
4.2
1.5
1
349.8
0.2
W X
H X
T
3
373.6
1.7
1377
.7
0.7
0.0
1
0.5
0
0.0
14
0.6
5584
.2
0.1
5
1633
.9
0.5
S X
H X
T
3
35.2
0.1
1
4398
1.9
8.1
***
0.0
1
0.5
1
0.0
4
1.5
2
1204
42.3
4.9
3**
8364
.8
4.4
5**
W X
S X
H X
T
3
220.9
0.7
1955
.6
0.4
0.0
1
0.9
3
0.0
25
1.1
3670
6.2
1.5
3322
.82
1.7
Resid
ual
64
334.2
5
5427
.9
0.0
1
0.0
24
2444
4.8
1879
.11
+m
arg
ina
lly s
ign
ific
ant
(0.0
4<
p<
0.0
5);
*p
<0
.05
;**p
<0.0
1;*
**p
<0
.00
1; a
ln (
x+1
) tr
an
sfo
rmed
da
ta; b
sig
nific
ant
diffe
ren
ces w
ith
con
tro
l
Ta
ble
2.
Sum
mar
y o
f anal
yse
s o
f var
iance
fo
r th
e o
rganic
mat
ter,
pro
tein
s, c
arb
ohyd
rate
s,li
pid
s, b
iop
oly
mer
ic c
arb
on (
BP
C)
and
Chlo
rop
hyll
a
(C
hl
a) i
n w
rack p
atch
es.
Typ
e o
f w
rack (
W),
Hei
ght
on t
he
sho
re (
H),
Tim
e (T
) ar
e fi
xed
fac
tors
and
Sit
e (S
) is
a r
and
om
Chapter 6 Effect of native and invasive algal wrack
194
.
Figure 1. Mean (±SE; n=3) amount of organic matter (g), in wrack patches
across heights on the shore (Dune and drift levels), sites (A and B) and over
time. Points show an exponential decay model for the two types of wrack: [S.
polyschides: a) y = 197.1e -0.021x R2 = 0.51; b) y = 219.3e -0.026 R2 = 0.77; c) y =
198.5e -0.019x R2 = 0.48; d) y = 216.5e -0.022x R2 = 0.73) and S. muticum: a) y =
378e -0.008x R2 = 0.47; b) y = 354.5e -0.015x R2 = 0.5; c) y = 361.8e -0.014x R2 =
0.53; d) y = 348.9 e -0.013x R2 = 0.4)]. : S. polyschides dune level; : S.
muticum dune level; S. polyschides drift level; S. muticum drift level.
Site A
0 3 6 9 12 15 18 21 24
Org
an
ic m
att
er (
g)
0
100
200
300
400
500
Site B
0 3 6 9 12 15 18 21 24
0
100
200
300
400
500
Time (days)
0 3 6 9 12 15 18 21 24
Org
an
ic m
att
er (
g)
0
100
200
300
400
500
0 3 6 9 12 15 18 21 24
0
100
200
300
400
500
Time (days)
(a)
(c)
(b)
(d)
Chapter 6 Effect of native and invasive algal wrack
195
Nutritional value, i.e. proteins, carbohydrates and lipids, varied
significantly between wrack types, but patterns differed (illustrated by
biopolymeric carbon concentration in Fig.2; Table 2). Protein concentrations
(μg. g-1) were found significantly greater in patches of S. muticum than in S.
polyschides, but this pattern was not consistent across sites and over time (i.e. a
significant Wrack x Site x Time interaction, P<0.05). For example, protein
concentrations were greater in patches of S. polyschides than in S. muticum at
Site B on day 3. Although lipids and carbohydrates tended to be more abundant
in patches of S. muticum than in patches of S. polyschides, this trend was not
consistent over time (i.e. Wrack x Time interaction, P<0.05). Lipids showed
this pattern on days 3, 7 and 21, whereas carbohydrates followed this pattern on
days 12 and 21. The nutritional composition of wrack measured as
biopolymeric carbon concentration (BPC), varied among wrack patches
although this pattern was not consistent over space (i.e. Wrack x Site x Height
interaction, P< 0.05) nor over time (i.e. Wrack x Time interaction, P< 0.05)
(Fig. 2a). There was more BPC in patches of S. muticum than in patches of S.
polyschides, but this trend varied between heights on the shore and sites. For
example, there was more BPC in patches of S. muticum in the dune than in the
drift line at Site A (SNK tests, P< 0.05). Moreover, BPC in patches of S.
muticum was more abundant than in patches of S. polyschides, but only on days
3 and 7 (SNK tests, P< 0.05).
Chorophyll a concentration varied significantly among wrack patches,
but this variation was not consistent over time (i.e. a significant interaction
Wrack x Time interaction, P< 0.01; Table 2). Chlorophyll a was in greater
concentration in patches of S .polyschides than in patches of S. muticum on
days 3, 7 and 12 (SNK tests, P< 0.05 illustrated in Fig 2b by wrack patches
located in the dune).
Chapter 6 Effect of native and invasive algal wrack
196
Fig
ure
2.
Mea
n (
±S
E;
n =
3)
am
ou
nt
of
a) B
iop
oly
mer
ic c
arb
on a
cro
ss s
ites
(A
and
B)
and
hei
ghts
on t
he
sho
re (
Dun
e an
d d
rift
lev
els
) and
b)
Chlo
rop
hyll
a c
once
ntr
atio
ns
in
the
du
ne
level
at
th
e tw
o
site
s o
ver
ti
me.
D
iffe
ren
t le
tter
s re
pre
sent
sig
nif
ican
t
dif
fere
nce
s and
sa
me
lett
ers
rep
rese
nt
no
si
gnif
icant
dif
fere
nce
s.
S
. po
lysc
hid
es
dune;
S
. p
oly
sch
ides
dri
ft;
S. m
uti
cum
dune;
S
. m
uti
cum
dri
ft.
Chapter 6 Effect of native and invasive algal wrack
197
4.6.3.3. Macrofauna abundance, number of species and diversity
Analyses of macrofauna data were based in pooled data, i.e. individuals
in wrack patches and underneath the wrack patches. This decision was made
because (1) there was a very small number of individuals and species in bare
sediment, i.e. controls, (2% of the total number of individuals) and (2)
individuals found in bare sediment and underneath the wrack patches belonged
to the same species that colonised wrack.
A total number of 7,820 individuals belonging to 29 species were
collected in wrack patches (Table 3). Larval stages of different species
accounted for 66% of total number of individuals. Two coleopteran species, the
tenebrionid Phaleria cadaverina and the histerid Hipocacculus rubripes, and
two dipteran species from the family Anthomyiidae in larvae stage accounted
for 90% of the total abundance. The arachnid Arctosa variana and three species
of coleopteran Cercyon littoralis, Hipocaccus dimidiatus maritimus and Cafius
xantholoma accounted for ~ 4% of the total abundance.
Colonisation of all wrack patches was very rapid. Most species
colonised patches within 3 days (25 species) and only a few new species
colonised by day 7 (2 species), 12 (1 species) and 21 (1 species). Abundances
varied significantly between both types of wrack, but this variation was not
consistent between heights on the shore over time (i.e. a significant Wrack x
Height x Time interaction, P<0.05; Table 4). Abundances in patches of S.
polyschides were larger than in patches of S. muticum in the dune on days 3, 7
and 12 and in the drift line on days 3 and 7 (showed in Fig. 3a; SNK tests, P<
0.05). Abundance of larvae was significantly larger in patches of S. polyschides
on day 3 (Fig. 3b; Table 4), whereas the number of larvae in patches of S.
muticum did not vary over time (SNK tests, P> 0.05). Number of species and
diversity varied between wrack types, but this pattern was not consistent over
time (i.e. significant Wrack x Time interactions; Table 3). The number of
species was larger in patches of S. muticum on day 3, whereas it was larger in
S.polyschides than S.muticum on days 7 and 12 (Fig. 3c). Diversity followed
Chapter 6 Effect of native and invasive algal wrack
198
the same trend as the number of species except for day 21 when diversity
varied significantly between wrack types (Fig. 3d).
species S. polyschides S. muticum
Bare
sediment
Phylum Annelida
Cl. Oligochaeta
Enchytraeidae
sp1 1(0.02) 1 (0.06)
Phylum Arthropoda
Supercl. Chelicerata
Ord. Aranei
Lycosidae
Arctosa varinana (C.L. Koch, 1848) 59 (0.95) 5 (0.32) 2 (1.56)
Thomisidae
Xysticus sp. (C.L. Koch, 1835) 1(0.02)
Supercl. Crustacea
Ord. Amphipoda
Talitridae
Talorchestia deshayesii (Audouin,
1826) 36 (0.58) 33 (2.1)
Ord. Isopoda
Tylidae 2 (0.13)
Tylos europaeus (Arcangeli, 1938) 2 (0.03) 1 (0.78)
Cirolanidae Dana, 1852
Eurydice affinis (Hansen, 1905) 5 (0.08) 5 (0.32)
Supercl. Insecta
Ord. Coleoptera
Hydrophilidae
Cercyon littoralis (Gyllenhal, 1808) 107 (1.72) 82 (5.2) 13 (10.2)
Histeridae
Hypocacculus rubripes (Erichson,
1834) 466 (7.47) 251 (15.9) 5 (3.91)
Hypocaccus dimidiatus maritimus
(Stephens, 1830) 162 (2.6) 13 (0.82) 3 (2.34)
Staphylinidae
Aleochara (Emplenota) grisea
(Kraatz, 1856) 2 (0.03)
Cafius (Cafius) xantholoma
(Gravenhorst, 1806) 116 (1.86) 101 (6.4) 2 (1.56)
Phytosus (Phytosus) spinifer (Curtis,
1838) 3 (0.05) 2 (0.13)
sp1 4 (0.06) 4 (0.25)
Tenebrionidae
Phaleria cadaverina (Fabricius, 1792) 2062 (33.05) 990 (62.7) 86 (67.2)
Phylan gibbus (Fabricius, 1775) 5 (0.08) 5 (0.32)
Ord. Diptera
Subord. Nematocera
Chapter 6 Effect of native and invasive algal wrack
199
Infraord. Muscomorpha
sp1 8 (0.13) 4 (0.25)
sp2 3(0.05)
Empididae
sp1 18 (0.29) 9 (0.57) 2 (1.56)
sp2 6 (0.38)
Drosophilidae
sp1 2 (0.03)
Infraord. Calyptratae
Anthomyiidae
sp1 3009 (48.23) 11 (0.7) 1 (0.78)
sp2 99 (1.55) 2 (0.13) 9 (7.03)
Muscidae
sp1 23 (0.37) 20 (1.27)
sp2 2 (0.03) 2 (0.139
Infraord. Tabanomorpha
Fam Tabanidae
sp1 29 (0.46) 20 (1.27) 4 (3.13)
Infraord. Bibionomorpha
Bibionidae
sp1 1 (0.02)
Infraord. Tipulomorpha
Limoniidae
sp1 15 (0.24) 8 (0.51)
Ord. Neuroptera
Myrmeleonidae
Myrmelon (Myrmeleon) formicarius
(Linnaeus, 1767) 4 (0.06) 2 (0.13)
Ord. Orthoptera
Fam. Acrididae
sp1 1(0.02)
Ord. Trichoptera
sp1 1 (0.02) 1 (0.06)
Table 3. Total number and percent composition (in brackets) of macroinvertebrates in
wrack patches.
4.6.3.4. Analysis of variance of selected species: Patterns of colonisation
and succession
Colonisation patterns in the most abundant species varied between
heights on the shore levels, sites and over time. Those species that mostly
contribute to the dissimilarity between wrack patches over time were identified
and analysed separately (Fig. 4). Anthomyiidae sp1 was the most abundant
species (3009 individuals, 48% of the total abundance). This species was more
abundant in patches of S. polyschides contributing with the highest dissimilarity
Chapter 6 Effect of native and invasive algal wrack
200
among wrack types (17.33%), but this pattern was not consistent over time (i.e.
a significant Wrack x Time interaction, P<0.05; Table 5). This species was
more abundant in patches of S. polyschides than in patches of S. muticum only
on days 3 and 7 (SNK tests, P< 0.05; Fig. 4a). The pattern of this variation was
consistent across heights on the shore and sites (i.e. no significant interaction).
The contribution of the rest of the species was very similar between wrack
patches. Adults of P. cadaverina did not show significant differences among
wrack patches consistently over space and time (i.e. no significant interactions;
Table 5). However, abundance of this species varied over time (7
days>21days>12days>3days; SNK tests, P<0.05; Fig. 4b). Larvae of P.
cadaverina followed a different pattern from adults varying between wrack
patches, but inconsistently across heights on the shore (i.e. Wrack x Height
interaction, P<0.05). Larvae were more abundant in patches of S. polyschides
than in S. muticum in the dune, whereas this pattern was the opposite in the
drift line (Fig. 4c). Abundance of C. littoralis varied between wrack patches,
although this variation was not consistent across sites (i.e. significant Wrack x
Site interaction; P< 0.05; Table 5). This species was more abundant in patches
of S. muticum than in S. polyschides, but only at Site B (SNK tests, P< 0.05;
Fig. 4d). H. rubripes varied significantly between wrack patches, but there was
no consistency between heights (i.e. Wrack x Height interaction, P< 0.05;
Table 5), nor over time (i.e. Wrack x Time interaction, P< 0.05; Table 5). This
species was more abundant in patches of S.polyschides than in S. muticum in
the drift line, whereas the pattern was the opposite in the dune (SNK tests, P<
0.05; Fig. 4e). In addition, H. rubripes was more abundant in patches of S.
polyschides on days 3, 7 and 12, whereas the pattern was the opposite on day
21 (SNK tests, P<0.05; Fig. 4e). Abundance of the arachnid A. variana differed
between wrack patches, but this variation was not consistent over space and
time (i.e. significant Wrack x Site x Height x Time interaction, P< 0.05; Table
5). For example, this species was more abundant in patches of S. polyschides
than in patches of S. muticum on day 12 in the drift and dune line at both sites,
and only in the drift line at Site B on day 21 (Fig. 4f).
Chapter 6 Effect of native and invasive algal wrack
201
So
urc
e
T
ota
l A
bu
nd
an
ce
a,b
Larv
ae a
bu
nd
an
ce
a,b
Sp
ecie
s r
ich
ne
ss
b
D
ivers
ity
a,b
En
tire
ass
em
bla
ge
a
df
MS
F
MS
F
MS
F
MS
F
MS
P
seud
o-F
Wra
ck (
W)
1
12.0
3
233.4
*
68.0
2
275.3
5*
18.3
7
12.2
5
0.0
1
0.9
2
1549
5
1.9
Site
(S
) 1
0.9
4
4.1
8*
0.0
3
0.0
8
2.6
6
0.8
7
0.0
5
2.1
7
1243
3
20.9
6**
*
Heig
ht (H
) 1
1.9
8
0.7
3
22.3
2
7.8
4
1.0
4
0.6
9
0.0
3
301.1
*
6485
.1
1.9
1
Tim
e (
T)
3
7.7
1
88.2
4**
12.8
8
44.4
8**
75.2
9
44.4
3**
0.0
16
3.0
5
601
7.8
6**
*
W X
S
1
0.0
5
0.2
3
0.2
4
0.5
4
1.5
0.4
9
0.0
12
0.5
2
8153
13.7
4**
*
W X
H
1
0.6
2
229.3
*
9.8
2
43.8
4
1.0
4
6.2
5
0.0
03
0.8
1591
.5
1.2
6
W X
T
3
3.8
7
25.7
2*
5.3
2
23.8
4*
22.4
6
13.2
5*
0.7
90
42.4
4**
3219
3.5
6*
S X
H
1
2.7
0
11.9
7**
2.8
4
6.2
8*
1.5
0
0.4
9
0.0
00
0.0
0
3402
.4
5.7
3**
*
S X
T
3
0.0
8
0.3
9
0.2
9
0.6
4
1.6
9
0.5
5
0.0
05
0.2
3
457.8
4
0.7
7
H X
T
3
0.0
1
0.0
6
1.2
1
8.6
9+
2.7
9
0.4
4
0.0
27
0.5
3
717.4
5
0.4
1
W X
S X
H
1
0.0
03
0.0
1
0.2
2
0.4
9
0.1
6
0.0
5
0.0
03
0.1
5
1263
.2
2.1
3
W X
S X
T
3
0.1
5
0.6
7
0.2
2
0.4
9
1.6
9
0.5
5
0.0
18
0.8
1
904.8
1.5
2
W X
H X
T
3
0.4
7
27.9
5*
0.9
9
4.4
7
1.6
2
1.2
4
0.0
00
0.0
0
1425
1.5
S X
H X
T
3
0.1
6
0.7
2
0.1
4
0.3
1
6.3
6
2.0
7
0.0
51
2.2
3
1758
2.9
6**
*
W X
S X
H X
T
3
0.0
1
0.0
7
0.2
2
0.4
9
1.3
0
0.4
2
0.0
34
1.4
8
955.2
1.6
1
Resi
du
al
64
0.2
2
0.4
5
3.0
7
0.0
23
593.3
+m
arg
ina
lly s
ign
ifica
nt
(0.0
4<
p<
0.0
5);
*p<
0.0
5;*
*p<
0.0
1;*
**p
<0
.00
1; a
ln (
x+1
) tr
an
sfo
rmed
da
ta; b
sig
nifi
can
t diff
ere
nce
s w
ith c
on
tro
l
T
ab
le 4
. S
um
mar
y o
f anal
yse
s o
f var
iance
(to
tal
nu
mb
er o
f in
div
idual
s, l
arvae
ab
und
ance
, sp
ecie
s ri
chness
and
Sh
anno
n-W
iener
’s d
iver
sity
ind
ex)
and
PE
RM
AN
OV
A (
enti
re a
ssem
bla
ge)
(n =
3).
Typ
e o
f w
rack
(W
), H
eig
ht
on
the
sho
re (
H),
Tim
e (
T)
are
fixed
fac
tors
and
Sit
e (
S)
is a
rand
om
.
Chapter 6 Effect of native and invasive algal wrack
202
Figure 3. Mean (±SE, n = 3) of a) abundance of individuals in the dune and drift levels
at Site A; b) abundance of larvae in the dune at site A; c) number of species in the drift
at site B; d) diversity in the drift level at site B over time. Different letters represent
significant differences and same letters represent no significant differences. S.
polyschides dune; S. polyschides drift; S. muticum dune; S. muticum drift.
4.6.3.5. Analysis of assemblages in wrack patches
Macrofaunal assemblages varied between types of wrack, but the
direction and magnitude of these differences were inconsistent between sites
(i.e. significant Wrack x Site interaction, pseudo-F(1,64)= 18.84; P< 0.001; Table
4) and over time (i.e. significant Wrack x Time interaction, pseudo-F(3,3)= 3.58,
P< 0.01; Table 4). The interactions were caused by variation in direction and
magnitude of differences among wrack patches, which is clearly illustrated in
Ab
un
da
nce o
f in
div
idu
als
0
50
100
150
200
250
300
350
Time (Days)
Sp
ecie
s ric
hn
ess
0
2
4
6
8
10
12
14
Time (Days)
H'
0.0
0.4
0.8
1.2
1.6
2.0(c)
a ba
a ab
b
a
(d)
a
aa
a
b
b
b
b
(a)
cc
b
a
b
a
cb
bb
c a aa
aa Larv
ae a
bu
nd
an
ce
0
50
100
150
200
250(b)
b
a
a
b
ab b
a
3 7 12 21 3 7 12 21
Chapter 6 Effect of native and invasive algal wrack
203
Fig. 5. Another way of illustrating this is by examining Bray-Curtis
dissimilarities (Table 6). First, the dissimilarity between macrofaunal
assemblages in patches of S. polyschides and those in S. muticum was greater at
Site A than B. In other words, macrofaunal assemblages in patches of S.
polyschides were more similar to those in patches of S. muticum at Site B.
Second, the dissimilarity between macrofaunal assemblages in patches of S.
polyschides and those in S. muticum was greater on days 3 and 12 than on days
7 and 21. Finally, the magnitude of change between assemblages in patches of
S. polyschides and S. muticum was similar on days 3 and 12 and on days 7 and
21 (Table 6).
4.6.3.6. Influence of environmental variables on macrofauna
assemblages.
The total organic content of wrack, concentrations of carbohydrates
and Chl a best explained the pattern of macrofaunal assemblages (Table 7).
Carbohydrates content accounted for as much variance alone as when
combined with total organic content and Chl a. Nevertheless, the best
combination overall did not explain a high percentage of variance (ρs= 0.335;
P< 0.01).
For each main species, a multiple stepwise logistic regression was run
with all abiotic variables together (Table 8). Several of the environmental
variables included in this analysis explained variation for five species. For
example, the effect of temperature and chlorophyll a in patches of S.
polyschides on the probability of P. cadaverina larvae being present, were
significant. This means that for a 1% increase in temperature and chlorophyll a
content, a patch of S. polyschides has a 0.436 and 1.014 more chance of having
a larva than not, respectively (Table 8).
Chapter 6 Effect of native and invasive algal wrack
204
Fig
ure
4.
Mea
n n
um
ber
(±
SE
; n
=3
) o
f in
div
idual
s o
ver
tim
e. a
) A
nth
om
yii
dae
sp
1 i
n t
he
dune
level
at
site
A.
b)
P.
cadave
rin
a
aver
aged
in t
he
du
ne
at s
ite
B.
c) P
cad
ave
rin
a (
larv
ae s
tage)
aver
aged
in t
he
dune
and
dri
ft l
evel
s at
sit
e A
. d
) C
. li
tto
rali
s in
the
du
ne
acro
ss s
ites
(A
and
B).
e)
H. ru
bri
pes
in t
he
dune
and
dri
ft l
evel
s at
sit
e B
. f)
A.
vari
an
a a
cro
ss h
eights
on t
he
sho
re a
nd
sit
es.
Dif
fere
nt
lett
ers
rep
rese
nt
sig
nif
icant
dif
fere
nce
s an
d s
am
e le
tter
s m
ean n
o s
ignif
ican
t d
iffe
rence
s.
S.
po
lysc
hid
es d
une;
S.
po
lysc
hid
es d
rift
; S
. m
uti
cum
dune;
S
. m
uti
cum
dri
ft
0
25
50
75
100
125
P. ca
da
veri
na
(la
rvae
)
05
10
15
20
25
30
Tim
e (
Da
ys)
05
10
15
20
A. va
ria
na
Mean (±SE) no. of individual
02468
10
C. li
tto
rali
s
05
10
15
20
25
Sit
e A
Sit
e B
aa
aa
a
a
aa
ab
bb
Sit
e A
Sit
e B
aa
aa
a
a
a
b
ca
b
b
(d)
(f)
0
50
100
150
200
250
An
tho
myi
ida
e sp
1P
. c
ad
ave
rin
a
a
b
a
ba
a
aa
a
a
a
b
aa
a
aa
aa
a
b
a
a
aa
ba
a
b
a
(a)
(b)
(c)
(e)
a
a
a
a
a
a
ab
b
b
b
bb
H. ru
bri
pes
aa
37
12
21
37
12
21
3
7
12
21
37
12
21
37
12
21
3
7
12
21
3
7
12
21
3
7
12
21
Chapter 6 Effect of native and invasive algal wrack
205
Effects of temperature, humidity, chlorophyll a and carbohydrates in patches of
S. muticum on the probability of C. littoralis being present were also
significant. However, only the effect of carbohydrates content in wrack was
relatively stronger on the presence of this species. In general, although the
effects were significant for some environmental predictors, the effect size was
small. In contrast, total abundance of individuals and total abundance of larvae
showed significant effects with most of the environmental predictors in both
types of wrack (see log-linear models; Table 8). However, the environmental
predictors explaining variability of total abundance and abundance of larvae
varied between types of wrack, i.e. lipids content for total abundance and
chlorophyll a for larvae abundance. Results of the log-linear model for total
number of species and diversity were omitted since there were no significant
effects for any of the predictor variables tested.
4.6.4. Discussion
4.6.4.1. Patterns of colonisation and succession
Results indicate that abundances of individuals were significantly
larger in wrack patches than those found in bare sand, i.e. controls located
nearby wrack patches. It is clear that algal wrack indeed promotes an increase
in population abundances of sandy beach macrofauna, either because it
provides their main source of food or refuge from environmental conditions
and/or due to predation (e.g. Inglis, 1989; Colombini et al., 2000).The number
of species found in this study (29) is similar to those reported in previous
studies elsewhere (Jędrzejczak, 2002b, Dugan et al., 2003), but lesser in
number than in a previous wok conducted in an adjacent beach (Olabarria et al.,
2007). In our study, the major components of the algal wrack were dipteran
flies and tenebrionid and staphylinid beetles. Several authors have noticed that
talitrid amphipods are considered primary macroinfaunal colonisers of fresh
algal wrack stranded on sandy beaches (e.g. Griffiths and Stenton-Dozey, 1981;
Inglis, 1989; Colombini et al., 2000).
Chapter 6 Effect of native and invasive algal wrack
206
So
urc
e
A
nth
om
yii
da
e s
p1
P
. c
ad
av
eri
na
P. c
ad
av
eri
na
(la
rva
)
C.
litt
ora
lis
H.
rub
rip
es
A.
va
ria
na
df
MS
F
MS
F
MS
F
MS
F
MS
F
MS
F
Wra
ck (
W)
1
30.8
2
21
.9*
0.7
7
2.8
7
5.7
7
20.2
6
2.3
7
1.6
7
0.1
1
0.4
4
2.5
51.5
Site
(S
) 1
0.5
4
3.9
8
4.7
1
7.3
3*
2.9
3
6,8
9*
0.3
4
1.1
3
0.2
3
0.6
3
0.4
1
6.8
*
He
igh
t (H
) 1
0.3
8
2.1
5
5.3
2
2.0
3
3.2
6
36.6
0.0
8
206
.6**
11.6
25.7
0.5
5
4.3
6
Tim
e (
T)
3
9.2
2
64.4
**
3.6
6
22.8
*
0.2
0.1
1
1.0
9
1.4
9
3.3
5
4.0
0.5
3
1.6
2
W X
S
1
0.1
4
1.0
3
0.2
7
0.4
1
0.2
8
0.6
7
1.4
2
4.7
1*
0.2
4
0.6
5
0.0
5
0.8
W X
H
1
0.0
7
0.5
6
6.2
4
44.1
1.4
3
913
.9*
0.0
8
0.1
7
1.9
4
266
.2*
0.4
3
5.9
W X
T
3
7.8
6
85.8
**
2.9
2.2
8
2.1
8
2.3
1
0.6
1
1.4
7
2.4
7
10.4
*
0.6
2
2.3
0
S X
H
1
0.1
8
1.3
2
2.6
2
4.1
*
0.8
9
2.0
9
0.0
0
0.0
0
0.4
5
1.2
3
0.1
2
2.0
7
S X
T
3
0.1
4
1.0
6
0.1
6
0.2
5
1.7
3
4.0
6*
0.7
4
2.4
5
0.8
4
2.2
7
0.3
3
5.3
9**
H X
T
3
0.0
1
0.4
4
0.7
4
1.9
1.8
9
12.4
1*
0.1
6
0.3
6
0.3
9
6.1
0
0.1
0
0.4
5
W X
S X
H
1
0.1
2
0.8
9
0.1
4
0.2
2
0.0
1
0.0
1
0.4
4
1.4
6
0.0
1
0.0
2
0.0
7
1.2
W X
S X
T
3
0.0
9
0.6
8
1.2
7
1.9
8
0.9
4
2.2
2
0.4
2
1.3
8
0.2
4
0.6
4
0.2
7
4.4
7**
W X
H X
T
3
0.2
2
2.1
8
2.0
1
1.9
5
0.4
4
0.6
8
0.2
5
0.7
5
1.3
9
6.1
3
0.2
4
1.0
8
S X
H X
T
3
0.0
15
0.1
2
0.3
9
0.6
1
0.1
5
0.3
6
0.4
4
1.4
7
0.0
6
0.1
8
0.2
3
3.8
5*
W X
S X
H X
T
3
0.1
01
0.7
5
1.0
3
1.6
0.6
4
1.5
1
0.3
3
1.1
0
0.2
3
0.6
1
0.2
2
3.7
*
Re
sid
ua
l 64
0.1
35
0.6
4
0.4
2
0.3
0.3
7
0.0
6
*p<
0.0
5; **
p<
0.0
1;
***p
<0
.00
1
Ta
ble
5.
Su
mm
ary o
f anal
yse
s o
f var
iance
fo
r ab
und
ance
of
each s
pec
ies.
Typ
e o
f w
rack (
W),
Hei
ght
on t
he
sho
re (
H),
T
ime
(T)
are
fixed
fac
tors
and
Sit
e (S
) is
a r
and
om
. D
ata
wer
e ln
(x+
1)
tran
sfo
rmed
.
Chapter 6 Effect of native and invasive algal wrack
207
The scarcity of these amphipods in the area of study might be related to the
specific environmental conditions in the beach during the sampling period,
when high temperatures and very strong winds following the first sampling day
dried off most of the wrack patches. In fact, previous studies have shown that
locomotory behaviour of talitrids is strongly influenced by weather conditions
such as relative humidity of air, sand temperature and moisture (e.g. Colombini
et al., 1998; Fallaci et al., 1999).
The pattern of colonisation varied between wrack types. The total
number of individuals was larger in patches of S. polyschides than in patches of
S. muticum. This difference in abundance became more evident within 3 days
and diminished over time, although the sharpest differences occurred in the
abundance of several larvae species. It is interesting to highlight that the
number of species and diversity reached higher values in patches of S. muticum
than in S. polyschides on day 3, but this pattern was reverted from day 7
onwards. On day 3, the largest abundances in native wrack patches were related
mainly to larvae belonging to the same species, i.e. Anthomyiidae sp 1. Thus,
dominance of larvae, can explain the small number of species and low diversity
found in native patches at that time. After day 3, larvae abundance dropped,
and both number of species and diversity increased to reach higher values in
patches of S. polyschides than those in S. muticum. Reproduction, larval
settlement or recruitment can be stimulated by an increase in food (Ford et al.,
1999, Bolam et al., 2000). In the case of flies, adults are insignificant
consumers of algae-exuded substances, but lay eggs in wrack which may
contribute greatly to the breakdown of kelp tissue as a result for their own
feeding activity and through the spread of microorganisms (Griffiths and
Stenton-Dozey, 1981; Inglis, 1989). Within the first days of experiment, the
increase in number of fly larvae could be related to the movements of adults
towards patches of S. polyschides, which can offer a more suitable habitat and
constitute a source of food for these species (see Norkko and Bonsdorff, 1996).
For example, the physical structure and/or specific microclimatic conditions in
native wrack patches might favour chiefly dipteran oviposition and breeding.
Chapter 6 Effect of native and invasive algal wrack
208
Figure 5. Non-metric multidimensional scaling (nMDS) for differences in assemblages
among wrack patches across heights on the shore (dune and drift), sites (A and B) and
over time (n = 3). :S. muticum dune; :S. muticum drift; :S. polyschides; :S.
polyschides drift.
Most species (87%) colonised the wrack patches within 3 days.
Different species showed different patterns of colonisation suggesting that life-
history attributes, such as their colonising and competitive abilities, and
mobility of different taxa, may be important factors contributing to explain
such patterns (see Wilson, 1994). Changes in habitat quality also affect
dynamics of local populations (Bonte et al., 2003). Variations in trophic
habitats of different species may play an important role in pattern of succession
together with different qualitative stages of decomposition and ageing of wrack
(Olabarria et al., 2007). Herbivorous species such as C. littoralis rapidly
colonised all the patches and remained present over time. The scavenger P.
cadaverina that feeds on different sources of organic debris (Jaramillo et al.,
2003) peaked on day 7. Carnivorous species such as the histerid H. rubripes
and the spider A. variana were early colonisers in both types of wrack, but their
abundances were larger on days 7 and 21. This increase in abundance of
predators may be related to the increase in abundance of larvae and immature
3 days
Site A
Site B
7 days 12 days
Stress: 0,06Stress: 0,06
21 days
Stress: 0,08Stress: 0,08
Stress: 0,11Stress: 0,11
Stress: 0,07Stress: 0,07
Stress: 0,13Stress: 0,13
Stress: 0,12Stress: 0,12
Stress: 0,15Stress: 0,15
Stress: 0,14Stress: 0,14
Chapter 6 Effect of native and invasive algal wrack
209
individuals which are likely to serve as food source. Apart from Anthomyiidae
sp1 that was clearly more abundant in patches of S. polyschides on day 3,
abundances of rest of species showed differences between wrack types, but this
trend was not consistent over space and/or over time. This suggests that other
factors, apart from the type of wrack, are influencing the patterns of
colonisation and succession. For example, variation may be related to
progressive microclimatic changes of wrack accumulations due to their
different position across the beach, i.e. dune and drift at the two sites slightly
varied in environmental conditions (e.g. Colombini et al., 2002; Jędrzejczak
2002a,b). In fact, several studies have pointed out that responses of
macrofaunal assemblages to wrack deposits vary depending on sites located a
few metres or kilometres apart (Rossi and Underwood, 2002; Colombini and
Chelazzi, 2003; Dugan et al., 2003) and on seasonality (Ford et al., 1999).
Time (days) Dissimilarity (%) between wrack
3 61
7 55
12 61
21 50
Site
A 63
B 52 Pairwise comparisons from PERMANOVA; 4999 permutations of raw data.
Data were square root transformed.
Table 6. Mean Bray-Curtis dissimilarities (%) between wrack patches.
(S. muticum vs. S. polyschides).
4.6.4.2. Abiotic factors affecting macrofaunal assemblages
There were some evidences to support the hypothesis that macrofaunal
assemblages changed in response to the wrack type, but patterns varied over
space and over time. Results indicated that carbohydrates, organic matter and
chlorophyll a variables best described the observed patterns in macrofaunal
assemblages. Moreover, temperature and humidity had some influence on the
presence of some species in wrack patches (see Table 8).
Chapter 6 Effect of native and invasive algal wrack
210
Different types of wrack can offer different quality and/or quantity of
food availability for macrofauna, which leads to complex patterns of
macrofaunal response (Ford et al., 1999; Rossi and Underwood, 2002). Results
indicated that nutritional value of wrack (mostly carbohydrates, lipids and
organic matter content) differed between the two types of wrack. In most cases,
the carbohydrates, lipids and organic content were greater in patches of S.
muticum than in patches of S. polyschides. In contrast, the chlorophyll a
concentration (used as a proxy of benthic microalgae biomass) was greater in
patches of S. polyschides than in patches of S. muticum in most cases. Benthic
microalgae may account for a large proportion of the carbon budget of a detrital
food-web and may play an important role in moderate fluxes of carbon in
coastal sediments (e.g. Herman et al., 2000). In fact, a greater concentration of
benthic microalgae in S. polyschides might be related to a lesser content of
polyphenols in laminarian seaweeds since the colonisation process in these
organisms is related to the polyphenol content (Van Alstyne et al., 1999).
k Best variable combinations (ρs)
1 CHO
(0.326)
2 O.M., CHO Chl a, CHO
(0.335) (0.316)
3 O.M., CHO, Chla H, O.M., CHO
(0.323) (0.307)
4 H, O.M., CHO, Chla
(0.309)
Table 7. Combinations of environmental variables, taken k at a time, giving
largest rank correlation ρs between biotic and abiotic similarity matrices; bold
indicates best combination overall. CHO: carbohydrate; O.M.: organic matter; Chl a: chlorophyll a; H: humidity.
In this context, the role of microphytobenthos in the flux of nutrients in
sediment is very important. Nutrients can be released from wrack patches and
are likely to be used by microphytobenthos, which may play a major role in the
flux of nutrients in the sediments, representing a direct or indirect source of
food for some invertebrates (Rossi and Underwood, 2002). Strong variation in
patch quality, i.e. nutritional value, may give rise to source-sink dynamics
Chapter 6 Effect of native and invasive algal wrack
211
affecting the local macrofaunal assemblages inhabiting patches of wrack (see
Bonte et al., 2003).
Although temperature and humidity influenced the presence of some
species (e.g. C. littoralis and H. rubripes in patches of S. muticum, total
abundance in the two types of patches; Table 8) the effect was not very strong.
Temperature and humidity varied between the two types of wrack although
inconsistently over space and time. Slight differences in these parameters could
affect colonisation by different invertebrate species. In fact, variation in
microclimatic conditions of wrack deposits has been considered an important
factor affecting behaviour, locomotory activity and distribution of several
arthropod species inhabiting beach-dune systems (e.g. Colombini et al., 1998;
Fallaci et al., 1999).
Apart from differences in nutritional value and microclimatic
conditions between the two types of wrack, differences in structure, i.e.
complexity, of wrack patches might play an important role in variability of
macrofaunal assemblages. Different structures due to morphological
differences of seaweeds cause variability in habitat quality, i.e. shelter from
predation (e.g. Vandendriessche et al. 2006). In some cases, preference of
invertebrates for certain seaweed species seems to be related to factors such as
availability, habitat provision or refuge from predation rather than nutritional
value (e.g. Wakefield and Murray, 1998).
Chapter 6 Effect of native and invasive algal wrack
212
Sa
cch
ori
za p
oly
sch
ides
S
arg
ass
um
mu
ticu
m
Lo
gis
tic r
egress
ion
In
terc
ep
t T
H
O
.M.
pro
t ch
o
Lip
C
hl
a
In
terc
ep
t T
H
O
.M.
pro
t ch
o
Lip
C
hl
a
An
tho
myii
dae s
p1
E
stim
ate
4
8.9
8
0.7
3
-0.7
2
0.0
84
-0
.03
0
.00
2
-0.0
04
0
.00
4
6
0.9
-0
.4
-0.4
7
-0.0
01
-0
.01
0
.00
1
-0.0
01
-0
.01
W
ald
st.
0
.66
2
.41
0
.96
2
.29
4
.58
0
.33
4
0.2
01
0
.14
1
0
.19
5
1.4
5
0.1
1
0.0
01
2
.86
0
.91
0
.05
6
0.7
7
o
dd
s ra
tio
-
2.0
8
0.4
8
1.0
9
0.9
71
1
.00
1
0.9
96
1
.00
4
-
0.6
7
0.6
25
0
.99
9
0.9
9
1.0
01
0
.99
9
0.9
93
P.
ca
da
veri
na
E
stim
ate
2
1.3
-0
.83
0
.76
-0
.03
-0
.01
-0
.00
0
-0.0
01
0
.01
4
-8
.44
0
.57
-0
.18
0
.01
4
0.0
1
0.0
01
-0
.00
1
-0.0
5
(lar
vae s
tage)
Wald
st.
3
.97
4
.23
0
.41
0
.25
2
0.9
83
0
.00
1
0.0
21
3
.87
0.0
14
1
.47
0
.07
0
.27
0
.98
0
.14
0
.04
3
3.5
5
o
dd
s ra
tio
-
0.4
4
2.1
4
0.9
7
0.9
93
0
.99
9
0.9
99
1
.01
4
-
1.7
7
0.8
35
1
.01
4
1.0
1
1.0
00
0
.99
9
0.9
55
C.
litt
ora
lis
Est
imate
6
.87
-0
.11
-0
.07
0
.02
1
0.0
01
0
.00
1
-0.0
02
-0
.01
17
6.9
-0
.73
-1
.62
-0
.05
-0
.01
0
.00
2
-0.0
01
-0
.02
W
ald
st.
0
.03
0
.53
0
.02
5
0.6
81
0
.03
2
0.5
35
0
.23
9
1.9
41
4.3
9
5.4
0
3.8
7
2.1
1
2.2
1
4.7
8
0.1
61
4
.93
o
dd
s ra
tio
-
0.9
0
.93
2
1.0
21
1
.00
0
1.0
01
0
.99
8
0.9
94
- 0
.48
4
0.1
97
0
.95
2
0.9
92
1
.00
2
0.9
98
0
.98
3
H.
rub
rip
es
Est
imate
9
1.4
5
-0.3
-0
.79
-0
.05
-0
.01
0
.00
1
0.0
08
-0
.03
48
4.7
0
.19
9
-4.8
1
-0.2
04
-0
.03
0
.00
2
0.0
1
-0.0
2
W
ald
st.
2
.03
1
.51
1
.42
2
1.3
1
1.3
23
0
.06
0
.83
5
5.0
8
6
.87
0
.28
4
6.6
9
7.4
0
5.5
2
3.5
41
1
.65
2
.57
o
dd
s ra
tio
-
0.7
4
0.4
67
0.9
51
0
.99
2
1.0
00
1
.01
0
.97
2
-
1.2
2
0.0
1
0.8
15
0
.97
2
1.0
02
1
.01
0
.98
A.
va
ria
na
E
stim
ate
2
1.5
2
-0.0
1
-0.3
3
0.0
2
0.0
01
0
.00
2
-0.0
02
-0
.01
23
0.5
0
.66
-2
.41
-0
.13
-0
.00
1
0.0
01
0
.00
5
-0.0
2
W
ald
st.
0
.53
0
.01
0
.8
0.7
62
0
.02
5
.1
0.3
12
2
.01
1.1
9
1.6
3
1.2
41
1
.79
0
.00
3
0.0
63
0
.40
4
2.5
63
o
dd
s ra
tio
-
0.9
9
0.7
2
1.0
2
1.0
1
.00
2
0.9
98
0
.99
4
-
1.9
3
0.1
0
.88
0
.99
9
1.0
1
.00
5
0.9
8
Lo
g-l
inear m
od
el
Ab
un
dan
ce
Est
imate
1
1.1
3
-0.0
4
0.0
06
-0.0
4
0.0
01
-0
.00
0
.00
0
.00
1
-1
.54
-0
.09
0
.07
0
.01
-0
.00
1
0.0
0
-0.0
01
-0
.00
1
W
ald
st.
2
37
8.7
3
7.9
0
.21
2
11
63
.1
96
.7
72
.2
2.2
1
46
.41
0.1
17
2
9.9
2
.43
1
8.0
2
13
.91
6
.64
1
7.1
1
0.8
5
Ab
un
dan
ce
Est
imate
-1
5.4
0
.03
0
.16
1
0.0
12
0
.00
1
-0.0
0
0.0
01
0
.00
3
4
3.6
5
0.0
26
-0
.39
-0
.02
-0
.02
0
.00
0
.00
1
-0.0
01
(lar
vae s
tage)
W
ald
st.
4
4.2
1
7.7
4
3.4
4
12
4.3
1
8.4
5
4.8
1
40
.4
21
1.5
34
.02
0
.98
2
6.3
2
47
.3
19
.4
10
.6
15
.33
1
.21
Ta
ble
8
. S
um
mar
y o
f th
e G
ener
aliz
ed li
nea
r m
od
els
ind
icat
ing var
iab
les
that
w
ere
signif
ican
t (i
n b
old
). T
:tem
per
ature
; H
: h
um
idit
y;
O.M
: o
rgan
ic m
atte
r; p
rot:
pro
tein
s;
cho
: ca
rbo
hyd
rate
s; l
ip:
lip
ids;
Chl
a:
chlo
rop
hyll
a
Chapter 6 Effect of native and invasive algal wrack
213
In summary, this study indicates that the different wrack deposits, i.e. native
versus invasive algal wrack, were not used uniformly by invertebrates. Data
also provides evidences that nutritional content and microclimatic conditions of
wrack deposits, i.e. temperature and humidity, affected macrofaunal
assemblages. It is important to emphasize that since correlation does not prove
causation, the conclusions from this study should be treated as predictions that
point to the most important experimental manipulation to be conducted next,
not as conclusions to be set in stone. Experimental manipulation to test
hypotheses regarding the physical structure of wrack and stable isotope
analyses to provide clues about the origin of invertebrate’s food sources and
trophic flows in beaches are the next step. In addition, results indicate that
replacement of native wrack deposits by exotic wrack may have important
effects on macrofaunal assemblages on sandy beaches. A change in the type (or
amount) of seaweed wrack entering a beach may alter the macrofaunal
assemblages and ecosystem function. Thus, the effect of the invasive seaweed
S. muticum may have an effect that is spread away from the points of invasion,
i.e. intertidal and subtidal rocky shores. An assessment of impact on different
marine ecosystems may be important criteria in assessing the impact of this
invasive species and the prioritization of exotic management.
Acknowledgments
We thank the authorities of the Corrubedo Nature Park for funding,
permission and technical assistance as well as to all the colleagues who assisted
us in field work. This research has also been supported by the Spanish Ministry
of Education and Science (CGL2005-02269). Funds to I.F.Rodil were provided
by a Predoctoral grant (XUGA, P.P. 0000 300S 140.08).
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PART V. GENERAL DISCUSSION.
“Tell me and I will forget. Show me and I may remember. Involve me and I
will understand”.
-Confucius
Part V General Discussion
218
5.7.1. The ecology of sandy beaches in the northern coast of the
Iberian Peninsula.
During the time of this thesis, we have investigated a wide range of
beaches along a major part of Spain’s Atlantic coastline. These beaches were
sampled quantitatively which enables us to make a general description of the
macrofauna community structure from this European region. Most of the
beaches from this coast are highly exposed (sensu McLachlan, 1980) to the
ocean processes; subjected to a mesotidal regime (2 and 4 m.), which is quite
different from most of the traditional studies in microtidal sandy beaches (e.g.
Jaramillo et al., 1993; McLachlan et al., 1993). In terms of beach typology,
sandy beaches from this region can predominantly be classified as intermediate,
with average slopes of 1/22-1/52. Sediment size is medium and not very well
sorted becoming progressively finer on the supratidal.
When starting to work in a region where little to no research has been
done, it is important to construct a baseline study that can be used as a
reference for future work. The first and second part of this thesis (see Chapters
1, 2 and 3) analyse the basic characteristics of the Spanish sandy beach
macrofauna, such as species composition and richness, the spatial distribution
and zonation of the macrofauna or the main environmental factors affecting
benthic macrofauna. Although no temporal study was followed in this part of
the thesis, the comparative snapshot sampling of 19 sandy beaches of the same
type and from the same region, allows a fundamental and representative
analyses of the macrofauna structure. The emphasis of this part of the thesis
was put on spatial, short-term effects. However, there is growing evidence that,
at least on microtidal beaches, the temporal scale is very important in sandy
beach ecology (e.g. Brazeiro and Defeo, 1996; Degraer et al., 1999; Dugan et
al., 2004). The lack of replication in time of several of the ecological studies
(Chapters 2, 3 and 4) is one of the, if not the most important limitation of this
thesis. Although the results from these chapters suggest that macrofauna is
primarily structured spatially, the information is far too limited to state that the
temporal scale is less important on mesotidal, temperate beaches. The results
Part V General Discussion
219
from various chapters of this thesis make us confident, however, that tackling
the appropriate spatial scale is at least as important as using an adequate
temporal scale.
5.7.1.1. Environmental factors affecting benthic macrofauna.
The results obtained in Chapter 2 showed that the number of species
was the biotic parameter most affected by the abiotic factors, increasing
linearly with tide range and diminishing with exposure rate. Other important
biotic factors such as biomass decreased exponentially with increasing average
grain size. This supports one common generalisation in sandy beach ecology:
the macroinvertebrates decreasing along a morphodynamic gradient from the
dissipative to the reflective conditions and from sheltered to exposed beaches.
Mean grain size was negatively related to biotic factors such as species richness
or biomass. There are a number of reasons to assume that this relationship is a
causal event. For instance, many species find it difficult or nearly impossible to
burrow in coarse sediment (Lastra and McLachlan, 1996; de la Huz et al.,
2002), thereby seriously hampering their survival chances. A long burial time
increases the predation risk and the probability to be swept away by the next
incoming swash. Furthermore, coarse sand provides a less stable anchoring
substrate, increasing the chance to be washed out of the sediment. Sediment
grain size indirectly impacts the fauna through its influence on swash and sand
bed permeability. Grain size variation, within the same beach, may promote
intraspecific zonation such as in the case of the bivalve Donax trunculus. The
smallest individuals were found highest on the shore, and the largest confined
to the lower saturated zone coping with swash climate and coarser sand.
Morphodynamic variability in a sandy beach is determined by sediment
range and wave regime but it is also important to include the effect associated
to the tides. Tide range has not been included in beach classification parameters
because traditional studies were carried out in microtidal beaches. However,
tide range is an important agent in mesotidal beach formation, and when tide
range becomes more significant that wave energy, the number of species
increases. Dean’s parameter does not take tides into account, and therefore is
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220
inadequate to cover meso or macrotidal situations. Another index was used to
compare beaches subjected to differing tide ranges. BSI gave good correlations
when a wide range of beach types were considered (Hacking, 1997). Our study
was concentrated on a limited geographic region, in which only part of the
spectrum of conditions are present. In this region, Dean’s parameter or BSI
have a low capacity to identify the roles of the various individual physical
factors controlling beach communities. New indexes such as BSI or BI (see
McLachlan and Dorvlo, 2005) will be more effective in macroscale
comparisons. The recent availability of comparable results of quantitative
beach surveys from many regions, however, allows for a database to be
compiled that covers most beach types and latitudes to enabling a broader
comparison of global trends (e.g. McLachlan and Dorvlo, 2005; Defeo and
McLachlan, 2005).
When only intermediate beaches are studied, the different community
characteristics seem to be affected by different abiotic factors. The number of
species in sandy beaches from this region is better explained by the exposure
rate than by traditional morphodynamic parameters or even beach slope. This
confirms that a greater ensemble of variables should be taken into account in
the ecology of sandy beach macrofauna and that communities of sandy beach
invertebrates are limited by a wider range of ecological factors rather than a
single key factor.
5.7.1.2. Community structure and macrofauna zonation
Crustaceans were the most abundant macrofaunal group, in abundance
and species number, while molluscs and polychaetes were the least abundant
groups (Chapters 2 and 3). The general cross-shore pattern observed in beaches
from this region confirms the current knowledge in sandy beach ecology:
species richness increases downshore (e.g. McLachlan and Brown, 2006).
Intertidal zonation is a well-studied phenomenon and although general patterns
have been established in some particular cases (see 1.1.2.4. for details), there is
no clear zonation pattern and in most of the cases it is considered an artificial
division of a continuum with an overlap between adjoining zones (McLachlan
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221
and Jaramillo, 1995; Degraer et al., 1999). However, results obtained in this
study suggest an elementary, but also widely applicable, zonation scheme for
sandy shores. This divides the studied beaches in two zones: a zone of air-
breathers at and above the driftline and a zone of water breathers below this.
The special profile of the intermediate sandy beaches studied here seems to fit
well with this zonation scenario. These beaches showed a broken profile
roughly separated by mean sea level into an upper steep beach, followed by a
lower flat downshore which has to cope with swash and wave climate. Zones
are clearest and narrowest at the top of the shore and become increasingly
blurred and wide moving downshore. The supralittoral zone of air breathers,
present on all shores, is typically inhabited by crustaceans. True intertidal
species dwell in the littoral zone, present on all except the harshest reflective
beaches, extending from the drift line down the midshore to just above the
water table outcrop (Defeo and McLachlan, 2005). Although we can elucidate a
trend in some of the beaches for lower shore zonation, the general pattern
shows that zonation appears unclear and blurred in the lower shore levels.
5.7.1.3. Relationship between macroinfauna and environmental variables
Macroinfauna abundance and distribution in sandy beaches depend on
several physical and biological factors. Beaches can be described by a set of
physical parameters such as tide range, sediment grain size, exposure rate,
swash climate and/or accretion-erosion dynamics, which could be potential
structuring factors for sandy beach macrofauna (Brazeiro, 2001, McLachlan
and Dorvlo, 2005). Results obtained in this study indicate that environmental
parameters such as slope, beach length and wave height were the most
important factors explaining variability in the species density. These patterns
are tightly related to beach morphodynamics. Sandy beaches with higher slope
and wave height present coarser sediment size and reflective characteristics.
Within one geographical region, the general pattern in sandy beach macrofauna
shows a decrease in species richness, abundance and biomass when moving
from dissipative to the reflective beach state. This pattern, which is found at
any latitude, is now considered one of the paradigms in sandy beach ecology
Part V General Discussion
222
(Defeo and McLachlan, 2005). Furthermore, McArdle and McLachlan (1992)
suggested beach slope and wave height as the most important factors
controlling swash climate, which is the most important aspect of the
environment by fauna inhabiting exposed sandy beaches. Those species with
the clearest zonation were found to be the best explained by the environmental
variables than species with no sharp boundaries in their distribution along the
beach profile.
It seems that community characteristics in the beaches studied are not
just determined by beach morphodynamics, but also by other factors dependent
on oceanographic conditions and coastal processes, determining critical
characteristics such as food availability. In spite of the geographical continuum
formed by all the 19 studied beaches, water mass characteristics along the north
coast of Spain are determined by variations in coastal productivity at different
spatial scales. We believe that macroinfauna differences found between
beaches arise from the chlorophyll concentration gradient rather than from
physical differences between beaches. The existence of an upwelling event,
common along the eastern boundary of the North Atlantic between 10º and 44º
N and focused on the North West coast of Spain (Wooster et al., 1976) can be
related to the macrofauna differences found along this beach gradient (west-
east). There is a net influx of nutrient rich deeper water and this fertilisation
leads to the high primary production, which results in benthic enrichment and
seems to dilute to the east through the north coast of Spain (Lastra et al., 2006).
It could be argued that proximity to such upwelling areas leads to higher
macroinfaunal abundance values because of greater food availability due to the
increase in productivity.
5.7.2. The importance of exposure on sandy beach macrofauna:
hydrodynamic conditions and food availability.
Macrofauna communities inhabiting sandy beaches are supported
almost entirely by allochthonous inputs of organic materials because little
primary production occurs on the beach itself. In many temperate regions, the
major sources of allochthonous organic material to sandy beach macrofauna are
Part V General Discussion
223
phytoplankton and marine macrophytes. Depending on food quality and
quantity in the intertidal, macrofauna community structure and trophic relations
can vary. Beaches lack attached macrophytes except in rare cases of sheltered
beaches with seagrass meadows extending onto the lower shore. Food chains
mainly begin and end in the sea but the land can also play a relative main role
in food availability. Results obtained in Part II of this thesis (Chapter 4) suggest
that macroinfauna community, in terms of abundance, biomass and species
richness, is more complex and diverse in sheltered environments than in
exposed sandy beaches. This reflects the general trend found in traditional
studies where an exposure increase led to a decrease in biotic variables (e.g.
Jaramillo and McLachlan, 1993; McLachlan et al., 1993).
5.7.2.1. Macrofauna characteristics in a gradient of exposure
Supratidal levels, where environmental conditions are harsh for truly
marine macrofauna, showed lower number of species and were dominated
exclusively by crustaceans, mainly talitrid amphipods. The ability of this kind
of organisms to utilise the upper levels of sandy beaches must relate to their
adaptations to avoid desiccation (McLachlan, 1990). Exposed sandy beaches
with short swashes and steep slopes harbour a rich macrofauna community
which find a more stable environment in the supralittoral zone (Defeo and
Gómez, 2005); while the number of species inhabiting the lower part
diminished sharply. In fact, no significant differences in the biotic variables
were found when comparing supralittoral community from exposed and
sheltered localities. Most of the species at this level have been considered
wrack-associated macrofauna and they largely depend on allochthonous inputs
associated with oceanographic processes (see Chapter 6). Sheltered beaches,
with more favourable environmental conditions and sediment stability, showed
higher significant values of biotic factors than exposed beaches when mid and
low tide levels were compared. The results from this study support the “Swash
Exclusion Hypothesis”, which states that the decrease in species richness,
abundance and biomass is caused by increasing harshness of the swash (see
section 1.1.2.3), but no significant effect was found at the supratidal, where
Part V General Discussion
224
swash climate is barely perceptible. Moreover, it is suggested that species
living at the supratidal level show relative independence of swash climate
effects with no clear response to beach type, and those species that follow
predictions of the SHE are mainly represented by intertidal forms (Defeo and
Gómez, 2005).
Swash climate and sand particle size may define the response of the
macroinfauna. Molluscs and polychaetes diminished significantly due to the
increasing harshness and exposure rate of the exposed intertidal. Both faunistic
groups increased their mean abundances significantly at the mid and low tidal
levels in sheltered beaches, where more stable physical conditions are found,
following the Habitat Favourability Hypothesis (Defeo et al., 2001). The
exposed intertidal, with harsher physical conditions and coarser sediment can
have a negative effect on burrowing, respiration rate and growth of filter feeder
bivalves, such as Donax trunculus. Sheltered sandy beaches, with lower
hydrodynamic conditions will favour accumulation of organic matter
potentially available to benthic deposit-feeders, mainly polychaetes, which are
the dominant trophic group in this type of intertidal.
5.7.2.2. Effect of the biochemical composition of sedimentary organic
matter on macrofauna
In Chapter 4, biochemical compounds concentrations of sedimentary
organic matter showed significant differences between sheltered and exposed
beaches. This can be related to the morphodynamic and physicochemical
characteristics of sandy beaches. Furthermore, a significant inverse correlation
between slope, exposure rate and BPC concentration was found. The exposed
sandy localities showed a significant increase in the reflective slope conditions
due to the harsher morphodynamic conditions. It seems that biopolymeric
concentrations follow a similar pattern that was also shown by organisms,
increasing from exposed intertidal with steeper slopes to sheltered sandy
beaches with flatter slopes.
Proteins constituted the main dominant fraction of the biochemical
composition of sedimentary organic matter in sheltered and exposed localities.
Part V General Discussion
225
This was even more important downshore close to the swash climate. The fact
that proteins were the main dominant fraction of BPC and carbohydrates
showed the lowest values measured in all the localities, indicate that the
organic matter may be mostly of newly generate origin. The PROT:CHO ratio
has been used to assess the “age” of sediment organic matter. This ratio was
found high enough to suggest that most of the sedimentary organic matter in
these beaches was recently produced and that protein is not a limiting factor for
consumer’s growth (Fabiano et al., 1995). However, protein concentrations, on
average, were lower in sheltered (63.4%) than in exposed (80.2%) sandy
beaches, but there was a higher concentration of organic matter in sheltered
localities. This could be better explained by the influence of temporal
allochthonous inputs since little primary production occurs on the beach itself.
It seems that the low hydrodynamic conditions of sheltered localities favours
accumulation of organic matter (see Chapter 5), while exposed sandy beaches
depend much more on the episodic inputs such as wrack debris (see Chapter 6).
The food available in the intertidal may be the result of the interaction
and equilibrium between physical and biological processes. There is enough
evidence to suggest that macrofauna sandy beaches are not just physically
controlled (although this can be a main factor) but other ecological factors,
including biochemical composition of sedimentary organic matter, may have
relevant influence in the macrofauna community structure of sandy beaches.
5.7.3. The role of food availability in the macrofauna community
structure of sandy beaches: spatial and temporal patterns.
Two sandy beaches, with different exposure rate, were studied
separately in part IV of this thesis in order to know the effect of food available
on macrofauna assemblages. In Chapter 5, the relationships between the
biochemical characteristics of sedimentary organic matter and benthic
macrofauna were analysed over two years in one estuarine sandy beach from
the NW coast of Spain. Due to the importance of exogenous organic input in
sandy beaches, Chapter 6 dealt with the relevant influence of algal wrack on
macrofaunal assemblages in one exposed sandy beach from NW coast of Spain.
Part V General Discussion
226
With these two studies we tried to identify the role of the organic matter
contribution in the observed intertidal macrofauna variability.
5.7.3.1. Seasonal variability in the benthic macrofauna distribution and
food availability in a sheltered estuarine beach.
Analysis of distribution of benthic macrofauna from Barraña (Chapter
5) demonstrated that the tidal levels sampled were characterised by distinct
faunal densities and species composition. Polychaetes and molluscs occurred
mainly at the intertidal level, while crustaceans tended to occur higher on the
shore (see 5.7.2.1.). Abundance, biomass and number of species were
negatively related to sediment depth. In addition to the horizontal level,
significant differences in depth distribution of macrofauna were found. This
could be related to differences in sediment characteristics, such as grain size or
compactness, which may condition organism’s ability to burrow. Sediment
characteristics, however, were not able to explain macroinfauna variation
alone. Vertical zonation could be further controlled by the presence and
position of the Redox Potential Discontinuity (RPD) layer since fauna is
dependent on dissolved oxygen for their respiration The RPD was found in the
intertidal at the 5-10 cm depth and macroinfauna was concentrated on the sand
surface or subsurface (~75%).
The intertidal levels on sheltered beaches are considered to be under
optimal environmental conditions in terms of humidity, temperature and food
supply for marine macroinfauna. Benthic macrofauna will be favoured by
accumulations of organic matter (Defeo et al., 2001) because of the lower
hydrodynamic conditions in sheltered beaches. Maximum concentrations of
food available, macrofauna abundance and species richness were found at the
medium tidal level. The peculiar profile of this beach, together with more
gentle environmental conditions, increased the amount of organic matter and
water content in the medium tidal level. These particular conditions may
promote macrofauna abundance and species richness in this part of the
intertidal, compared to the supratidal or downshore. Most of the species
inhabiting the intertidal level belonged to the deposit-feeder’s group, favoured
Part V General Discussion
227
by organic rich supply on the sediment surface during winter and spring.
Deposit-feeders are able to rapidly exploit food resources and conspicuous
abundance of this trophic group has been related to a marked increase in
proteins (Rossi et al., 2001). The occurrence of suspension feeders was
restricted to the lower intertidal level, probably because they can only feed at
high tide and they cannot exist where submergence is brief.
Despite the constant dominance of few abundant species on this beach,
high variability of the community was observed throughout the study period,
which could be related to fluctuations in the availability of food resources.
From analysis of the biochemical composition of organic matter, the labile
fraction accounted for an important part of the organic matter accumulated in
the intertidal and proteins were the dominant fraction. The rise in proteins
meant an increment in the quality of food available. The particularly high
protein values recorded in winter could be related to allochthonous inputs,
which are more common at this time of the year. There was a decrease in the
PROT:CHO ratio in summer and at the beginning of autumn, probably because
of the lack of sea input, high temperatures and solar radiation which usually
characterise this season. During this period of the study, less algal detritus and
high values of refractory organic matter were found, suggesting scarce
availability and low quality of food resources. The progressive decomposition
of this debris during summer could cause a rapid depletion of the labile fraction
of the organic matter. This suggests the presence of aged organic matter with of
a largely detritic origin caused by the algal-wrack decomposition.
Allochthonous inputs are usual incidents during winter, which promote
accumulation of dead seaweed on the beach face and therefore introduce new
organic matter in the intertidal. Some benthic animals may indeed benefit from
drifting algal mats as a key resource.
Chlorophyll a concentrations in the sediment reported frequent peaks
during winter and spring, with the particularly high values of Chl a that may be
related to the high deposition of algal detritus and a low decomposition rate
over the winter period. This can create an ideal environment for microbial
Part V General Discussion
228
productivity with a subsequent increase in photosynthetic activity (Kelaher and
Levinton, 2003).
This study showed the importance of food availability in a benthic
macrofauna community that relied on seasonal deposition of sedimentary
organic matter at the intertidal. Food quality and quantity have the potential to
cause substantial spatio-temporal variation in the structure of macrofauna
assemblages in estuarine beaches. The statistical analyses indicated that
biochemical compounds and Chl a were the main factors explaining benthic
macrofauna distribution in the intertidal level. Macroinfauna characteristics and
abiotic factors, such as organic matter and Chl a, were always found to be
higher at the intertidal level, where swash action occurs, than at the supratidal.
The swash zone has been considered a key area controlling macroinfauna from
the intertidal and the importance of the swash climate on the macrofaunal
assemblages and on the food available present in sediments of sandy beaches
has been recently stated (Incera et al., 2006).
Multiple regression analyses were in line with the results obtained, a
positive correlation between sedimentary organics and macroinfauna
characteristics, such as biomass, macrofauna abundance and abundance of
polychaetes and crustaceans, was found. These analyses showed the existence
of tight relationships between macroinfauna and food quality but the
distributions of factors such as pigment and nutrients are often depth
dependent. Therefore, caution is called for when correlating depth profiles of
different variables. The conclusions from this study should be treated as
predictions that point to the most important experimental manipulation to be
conducted next. This study showed that macrofauna from estuarine sheltered
beaches is not just driven by physical forces but also by the distribution of its
primary food sources. Macrofauna organisms showed preferences both in
vertical and horizontal ranges suggesting a specific distribution which is related
to specific sensitivity by several abiotic factors, including food availability. The
assessment of vertical and horizontal variability and the relative structure of the
macroinfauna community displayed a strong heterogeneity over time,
Part V General Discussion
229
suggesting that macrofauna in estuarine beaches can be related to complex and
unpredictable factors.
5.7.3.2. Effect of invasive algal wrack in macrofauna assemblages in an
exposed sandy beach
Several studies have examined macrophytes brought to beaches by the
sea and stay temporally as wrack debris in the intertidal. These may be salt-
marsh grasses from estuaries, seagrasses from sheltered subtidal sands, or
macroalgae from rocky shores and subtidal reefs. Most beaches receive a small
amount of such inputs, but in some situations the input may be substantial,
especially after winter storms. Wrack is fed upon directly by some organisms
associated with the dune and drift line, such as talitrids amphipods, isopods,
and insects. This material dominates the sandy beach food chains (for review,
see Colombini and Chelazzi, 2003). However, much decomposition is
accomplished by bacteria, and breakdown can be completed in days to weeks,
depending on the debris (Griffiths et al., 1983; Jędrzejczak, 2002). Wrack also
acts as a refuge supply for the supralittoral fauna, ovoposition and larval
development, either for terrestrial or marine invertebrates.
It is clear that algal wrack indeed promotes an increase in population
abundances of sandy beach macrofauna, either because it provides their main
food source or refuge from environmental conditions and/or predation. In
Chapter 6, the major components of the algal wrack were dipteran flies (mainly
larvae) and tenebrionid and staphylinid beetles. Talitrid amphipods are
considered primary macroinfaunal colonisers of fresh algal wrack stranded on
sandy beaches. The scarcity of these amphipods in the area of study might be
related to the specific environmental conditions during the sampling period,
when high temperatures and very strong winds following the first sampling day
dried off most of wrack patches. Previous studies have shown that locomotory
behaviour of talitrids is strongly influenced by weather conditions such as
relative humidity of air, sand temperature and moisture (e.g. Colombini et al.,
1998; Fallaci et al., 1999).
Part V General Discussion
230
The presence of wrack made of invasive macroalgae (Sargassum
muticum) and wrack made of native macroalgae (Saccorhiza polyschides)
promote two different colonisation patterns. The total number of individuals
was larger in patches of S. polyschides than in patches of S. muticum. This
difference in abundance became more evident within 3 days and diminished
over time, although the sharpest differences occurred in the abundance of
several larvae species. It is interesting to highlight that the number of species
and diversity reached higher values in patches of S. muticum than in S.
polyschides on day 3, but this pattern was reverted from day 7 onwards. At the
beginning of this study, the largest abundances in native wrack patches were
related mainly to larvae belonging to the same species, i.e. Anthomyiidae sp 1.
This dominance can explain the small number of species and low diversity
found in native patches at that time. After day 3, larvae abundance dropped,
and both number of species and diversity increased to reach higher values in
patches of S. polyschides than those in S. muticum. Reproduction, larval
settlement or recruitment can be stimulated by the presence of the wrack debris
(Bolam et al., 2000). In the case of flies, adults are insignificant consumers of
algae-exuded substances, but lay eggs in wrack which may contribute greatly to
the breakdown of kelp tissue as a result for their own feeding activity and
through the spread of microorganisms. It seems that wrack made of native
macroalgae is a more suitable habitat and represent a very important feeding
source. Maybe the physical structure and/or specific microclimatic conditions
in native wrack patches might favour chiefly dipteran oviposition and breeding.
Most species colonised the wrack patches quickly but different species
showed different patterns of colonization suggesting that life-history attributes,
such as their colonising and competitive abilities, and mobility of different
taxa, may be important factors contributing to explain such patterns.
Herbivorous species such as Cercyon littoralis colonised all the patches rapidly
and remained present over time. The scavenger P. cadaverina that feeds on
different sources of organic debris peaked on day 7. Carnivorous species (H.
rubripes and A. variana) were early colonisers in both types of wrack, but their
abundances were larger on days 7 and 21. This increase in abundance of
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231
predators may be related to the increase in abundance of larvae and immature
individuals which are likely to serve as food source. Although the species
found in the two types of wrack patches are different there was not a consistent
trend across space and/or time. This suggests that other factors apart from type
of wrack are influencing the patterns of colonization and succession. For
example, variation may be related to progressive microclimatic changes of
wrack accumulations due to their different position across the beach.
There were some evidences to support the hypothesis that macrofaunal
assemblages changed in response to wrack type, but patterns varied across
space and time. Results indicated that carbohydrates, organic matter and
chlorophyll a variables best described the observed patterns in macrofaunal
assemblages. Moreover, temperature and humidity had some influence in the
presence of some species in wrack patches. Slight differences in these
parameters could affect colonization by different invertebrate species, because
variation in microclimatic conditions of wrack deposits have been considered
an important factor affecting behaviour, locomotory activity and distribution of
several arthropod species inhabiting beach-dune systems (Colombini et al.,
1998). Nutritional value of wrack (mostly carbohydrates, lipids and organic
matter content) differed between the two types of wrack. In most cases, the
carbohydrates, lipids and organic content were greater in patches of S. muticum
than in patches of S. polyschides. In contrast, the chlorophyll a concentration
(used as a proxy of benthic microalgae biomass) was greater in patches of S.
polyschides than in patches of S. muticum in most cases. In fact, a greater
concentration of benthic microalgae in S. polyschides might be related to a
lesser content of polyphenols in laminarian seaweeds since process of
colonization in these organisms is related to the polyphenols content. Brown
algal polyphenolic compounds protect plants from pathogens or damage by UV
radiation, while deterring feeding by herbivores (Van Alstyne et al., 1999).
Nutrients can be released from wrack patches and are likely to be used by
microphytobenthos, which may play a major role in the flux of nutrients in the
sediments, representing a direct or indirect source of food for some
invertebrates (Rossi and Underwood, 2002).
Part V General Discussion
232
Apart from differences in nutritional value and microclimatic
conditions between the two types of wrack, differences in structure, i.e.
complexity, of wrack patches might play an important role in variability of
macrofaunal assemblages. Different structure due to morphological differences
of seaweeds causes variability in quality of habitat, i.e. shelter from predation.
In some cases, preference of invertebrates for certain seaweed species seems to
be related to factors such as availability, habitat provision, or refuge from
predation rather than nutritional value (Wakefield and Murray, 1998).
The results obtained in this study indicate that replacement of native
wrack deposits by exotic wrack may have important effects on macrofaunal
assemblages on sandy beaches. A change in the type or amount of seaweed
wrack entering a beach may alter the macrofaunal assemblages and ecosystem
function.
5.7.4. Open questions.
The most prominent question that arises from this study on sandy beach
macrofauna reported in this thesis is what happens at different temporal scales.
As faunal zonation is dynamic, temporal studies are needed for a full picture of
zonation patterns (Chapters 2, 3, and 4), requiring intensive sampling; f.i.
bimonthly during a year, to provide unbiased estimates. Although the sampling
load would be very high, temporal replication, following seasonal trends, is a
main factor to have in mind when variability is found in the results. In fact,
there might be as much variability from one week to another as from one
season to another. The simplest solution is to sample more often, either to
detect the temporal trend or to create replication while sampling in an attempt
to avoid confusion in the interpretation of the data.
Concerning macrofauna distribution through the intertidal, the cross-
shore variability of benthic community of sandy beaches was well
accomplished in Chapter 3. The along shore distribution of macrofauna on a
beach is one of the least studied topics in sandy beach research, and only
limited information is available. In general, macrofaunal populations are most
developed in the middle of a beach, with a unimodal bell-shaped distribution
Part V General Discussion
233
towards both sides. Although the sites chosen within each beach studied can be
considered representatives of the whole intertidal, a selection of different sites
within the same beach could underline some of the causes of macrofauna
zonation variability. Once again, sampling load would be excessive.
In Chapter 4, along-shore distribution was widely covered due to the
short length of the intertidal studied. Concerning horizontal distribution, three
representative tide levels were chosen. Two intertidal affected by the swash
climate, and one supratidal not affected by the swash climate. By sampling
these three levels we were able to study specific aspects of the three most
representative environments of the beach: the low swash environment, having
an assemblage of typically intertidal species; the truly intertidal part of the
beach; and the supratidal zone, where only resistant and semiterrestrial species
are present. It is important to point out that both exposed and sheltered beaches
are geographically associated, exposed at North and sheltered at South (Chapter
4). With this design, spatial and exposure effects may be confounded. Although
there is an obvious geographical separation between sheltered and exposed
beaches, previous studies indicated that the values for number of species,
biomass and chlorophyll a were higher in beaches from the NW coast of Spain
due to the influence of the seasonal upwelling event located in this same area of
the Iberian Peninsula (Lastra et al., 2006). However, a thorough study of sandy
beaches with different exposure rate should include intertidal habitats with the
same exposure rate in the same area of study. For instance, it would be
interesting to include three exposed and three sheltered sandy beaches from the
same location and compare them with the same number and type of beaches
from another location. Furthermore, the lack of fit between some biochemical
compounds and quantitative characteristics of macroinfauna may be clarified
when including seasonal sampling.
The lack of seasonal sampling in previous Chapters was partially
solved in Chapter 5, where seasonal variability in benthic macrofauna
distribution and food availability was studied. However, no clear seasonal
pattern was found in macrofauna and sedimentary organic characteristics
suggesting that macrofaunal assemblages are controlled by complex and
Part V General Discussion
234
unpredictable factors. The influence of anthropogenic impacts, very difficult to
assess or predict, can be main factors influencing seasonal variability. It would
be more desirable to study locations without direct human impacts, in “wild
conditions”, or select a cluster of beaches, with the same morphodynamic
conditions from different geographical locations to clarify natural seasonal
variability from more complex external effects.
Studying the impact of a long-term change on macrofauna is
logistically very difficult. A field monitoring campaign over many years, with a
reasonable resolution (monthly or bimonthly), should be combined with
mesocosmos experiments on indicator species. Additionally, keeping
macrofauna in laboratory conditions might prove very valuable for additional
studies. Studying environmental factors in situ, such as swash climate, cannot
reveal all of the information about the mechanisms behind the behaviour and
distribution of sandy beach macrofauna. To understand the underlying
mechanisms, it is crucial to have independent control over the different
physical parameters, which explains the need for laboratory experiments. So
far, experimental work on macrofauna using aquariums or tanks allow work on
crucial factors such as type of sediment, beach slope, swash climate (period,
velocity) or indicator species. For instance, estimates of the feeding rates and
food preferences of different macrofauna species would be beneficial from
laboratory experiments. The pioneer studies carried out in Lastra et al., 2007 (in
press) showed a first attempt to estimate the feeding rates and preferences of
Talitrid amphipods and their impact on food sources. This was accomplished
by a series of field and laboratory experiment evaluating different factors such
as wrack species, consumers size and temperature effect. This study elucidated
species behaviour from different geographical areas to compare the specific use
of food sources such as wrack macroalgae by these organisms. Experimental
manipulation to test hypotheses about physical structure of wrack and stable
isotope analyses to provide clues about the origin of invertebrate’s food sources
and trophic flows in beaches may be the next step.
It is important to have in mind the effect of invasive species in future
studies because the replacement of native species by exotic organisms may
Part V General Discussion
235
have important effects on macrofaunal assemblages on sandy beaches. The
effect of the invasive seaweed S. muticum may have an effect that is spread
away from the points of invasion, i.e. intertidal and subtidal rocky shores. An
assessment of impact on different marine ecosystems may be important criteria
in assessing the impact of this invasive species and the prioritization of exotic
management (see Chapter 6).
The assemblages supported by beach-cast macrophytes are important
prey sources commonly exploited by a number of shorebirds and, therefore, are
a basic element of food webs acting as an important link between marine and
terrestrial ecosystems (Hubbard and Dugan, 2003; Orr et al., 2005). Wrack-
cleaning activities done on beaches used as recreational areas might have
important cascading effects on the species diversity and abundance, and
consequently affect both marine and terrestrial habitats.
It is important to emphasise that since correlation does not prove
causation, the conclusions from this thesis should be treated as predictions that
point to the most important experimental manipulation to be conducted next,
not as conclusions to be set in stone.
5.7.5. List of references.
Bolam, S.G., Fernandes, T.F., Read, P., Raffaelli, D., 2000. Effects of
macroalgal mats on intertidal sandflats: an experimental study. Journal
of Experimental Marine Biology and Ecology 249, 123-137.
Brazeiro, A., Defeo, O., 1996. Macroinfauna zonation in microtidal sandy
beaches: it is possible to identify patterns in such variable
environments. Estuarine, Coastal and Shelf Science 42: 523-536.
Brazeiro, A. 2001. Relationship between species richness and morphodynamics
in sandy beaches: what are the underlying factors? Marine Ecology
Progress Series. 224: 35-44.
Colombini, I., Aloia,A., Fallaci,M., Pezzoli,G., Chelazzi,L., 1998. Spatial use
of an equatorial coastal system (East Africa) by an arthropod
community in relation to periodically varying environmental
conditions. Estuarine, Coastal and Shelf Science 47: 633-647.
Colombini, I., Chelazzi, L., 2003. Influence of marine allochthonous input on
sandy beach communities. Oceanography and Marine Biology: An
Annual Review 41, 115-159.
De la Huz, R., M. Lastra, M., López, J. 2002. The influence of sediment grain
size on burrowing, growth and metabolism f Donax trunculus L.
(Bivalvia: Donacidae): Journal of Sea Research 47: 85-95.
Part V General Discussion
236
Defeo, O., Gómez, J., Lercari, D. 2001 Testing the swash exclusion hypothesis
in sandy beach populations: the mole crab Emerita brasiliensis in
Uruguay. Marine Ecology Progress Series 212: 159-170.
Defeo, O., Gómez, J. 2005. Morphodynamics and habitat safety in sandy
beaches: life-history adaptations in a supralittoral amphipod. Marine
Ecology Progress Series. 293: 143-153.
Defeo, O., McLachlan, A. 2005 Patterns, processes and regulatory mechanisms
in sandy beach macrofauna: a multi-scale analysis. Feature article:
Review. Marine Ecology Progress Series. 295: 1-20.
Degraer, S.,Mouton, I., de Neve, L., Vincx, M. 1999. Community structure and
intertidal zonation of the macrobenthos on a macrotidal, ultra-
dissipative sandy beach : summer-winter comparison. Estuaries 22:
742-752.
Dugan, J., Jaramillo, E., Hubbard, D.M., Contreras, H., Duarte, C., 2004.
Competitive interactions in macroinfaunal animals of exposed sandy
beaches. Oecologia 139: 630-640.
Fabiano, M., Danovaro, R., and Fraschetti, S. 1995. A 3-year time series of
elemental and biochemical composition of organic matter in subtidal
sandy sediments of the Ligurian Sea (northwestern Mediterranean).
Continental Shelf Research 15: 1453-1469.
Fallaci, M., Aloia, A., Audoglio, M., Colombini, I., Scapini, F., Chelazzi, L.,
1999. Differences in behavioural strategies between two sympatric
talitrids (Amphipoda) inhabiting an exposed sandy beach of the French
Atlantic Coast. Estuarine Coastal and Shelf Science 48: 469-482.
Griffiths, C.L., and Stenton-Dozey, J.M. 1981. The fauna and rate of
degradation of stranded kelp. Estuarine Coastal and Shelf Science 12:
645-653.
Hacking, N. 1998. Macrofaunal community structure of beaches in northern
New South Wales, Australia. Marine Freshwater Research 49: 47-53.
Hubbard, D.M., Dugan, J.E., 2003. Shorebirds use o fan exposed sandy beach
in southern California.Estuarine, Coastal and Shelf Science 58S: 41-54.
Incera, M., Lastra, M., and López, J. 2006. Effect of swash climate and food
availability on sandy beach macrofauna along the NW coast of the
Iberian Peninsula. Marine Ecology Progress Series 261: 85-97.
Jaramillo, E., McLachlan, A. 1993. Community and population response of the
macroinfauna to physical factors over a range of exposed sandy
beaches in south-central Chile. Estuarine and Coastal Shelf Science.
37: 615-624.
Jaramillo, E., McLachlan, A., Coetzee, P., 1993. Intertidal zonation patterns of
macroinfauna over a range of exposed sandy beaches in south central
Chile. Marine Ecology Progress Series 101, 105-118.
Jędrzejczak, M.F., 2002. Stranded Zostera marina L. vs wrack fauna
community interactions on a Baltic sandy beach (Hel, Poland): a short-
term pilot study. Part I. Driftline effects of fragmented detritivory,
leaching and decay rates. Oceanologia 44(2): 273-286.
Kelaher, B.P. and Levinton, J.S. 2003. Variation IN detrital enrichment causes
spatio-temporal variation in soft-sediment assemblages. Marine
Ecology Progress Series 261: 85-97.
Part V General Discussion
237
Lastra, M., McLachlan, A., 1996. Spatial and temporal variations in
recruitment of Donax serra Röding (Bivalvia: Donacidae) on an
exposed sandy beach of South Africa. Revista Chilena de Historia
Natural 69: 631-639.
Lastra, M., de La Huz R., Sánchez-Mata, A.G., Rodil I.F., Aerts K., Beloso S.,
López J., 2006. Ecology of exposed sandy beaches in northern Spain:
environmental factors controlling macrofauna communities. Journal of
Sea Research 55: 128-140.
Lastra, M., Dugan, J., Page, M., Hubbard, D., Rodil, I.F., (in press). Processing
of allochthonous macrophyte subsidies by sandy beach consumers:
estimates of feeding rates and impacts on food resources. Marine
Biology.
McArdle, S., McLachlan, A., 1992. Sand beach ecology: Swash features
relevant to the macrofauna. Journal of Coastal Research. 8: 398-407.
McLachlan, A., 1980. The definition of sandy beaches in relation to exposure:
simple rating system. South African Journal of Science 76: 137-138.
McLachlan, A. 1990. Dissipative beaches and macrofauna communities on
exposed intertidal sands. Journal of Coastal Research 1: 57-71.
McLachlan, A., Jaramillo, E., Donn, E., F. Wessels 1993. Sandy beach
macrofauna communities and their control by the physical
environment: a geographical comparison. Journal of Coastal Research
15: 27-38.
McLachlan, A., Jaramillo, E., 1995. Zonation on sandy beaches. Oceanography
and Marine Biology 33, 305-335.
McLachlan, A., Dorvlo, A. 2005. Global patterns in sandy beach macrobenthic
communities. Journal of Coastal Research 21(4): 674-687.
McLachlan, A., Brown, A.C., 2006. The ecology of sandy shores. Acad. Press,
Amsterdam.
Orr, M., Zimmer, M., Jelinski, D.E., Mews, M., 2005. Wrack deposits on
different beach types: spatial and temporal variation in the pattern of
subsidy. Ecology 86: 1496-1507.
Rossi, F., Como, S., Corti, S. and Lardicci, C. 2001. Seasonal variation of a
deposit-feeder assemblage and sedimentary organic matter in a
brackish basin mudflat (Western Mediterranean, Italy). Estuarine
Coastal Shelf Science 58: 353-366.
Rossi, F., Underwood, A.J. 2002. Small-scale disturbance and increased
nutrients as influences on intertidal macrobenthic assemblages:
experimental burial of wrack in different intertidal environments.
Marine Ecology Progress Series 241: 29-39.
Van Alstyne, K.L., McCarthy, J.J., Hustead, C.L., Duggins, D.O., 1998.
Geographic variation in polyphenolic levels of Northeastern Pacific
kelps and rockweeds. Marine Biology 133: 371-379.
Wakefield, R.L., Murray, S.N., 1998. Factors influencing food choice by the
seaweed-eating marine snail Norrisia norrisi (Trochidae). Mar. Biol.
130, 631-642.
Wooster, W.S., Bakun, A., McLain, D.R., 1976. The seasonal upwelling cycle
along the eastern boundary of the North Atlantic. Journal of Marine
Research 34(2): 131-141.
PARTE V. DISCUSIÓN GENERAL.
(Según el acuerdo de 18/06/04 firmado por la Comisión de Doctorado de la
Universidad de Vigo acerca del idioma en que puede escribirse la Tesis doctoral).
Parte V Discusión general
239
5.7.1. La ecología de playas de la costa norte de la Península Ibérica.
Durante el periodo de este estudio, se ha investigado un amplio número
de playas a lo largo de la línea costera del norte de España. Estas playas han
sido muestreadas de forma cuantitativa lo que nos ha proporcionado la
información básica para obtener una descripción general de la estructura de la
comunidad macrofaunística de las playas de esta región. La gran mayoría de
playas que nos encontramos en esta costa son intermareales expuestos (sensu
McLachlan, 1980) a la acción oceánica; sometidas a un régimen mesomareal
(entre 2 y 4 m.), lo cual lo aleja de la gran mayoría de estudios tradicionales de
playas micromareales (e.g. Jaramillo et al., 1993; McLachlan et al., 1993). En
términos de tipología, las playas expuestas de esta región son
predominantemente intermedias con un promedio de pendiente muy variable
(1/22 a 1/52) y un tamaño de grano de tipo medio no muy bien clasificado que
se va haciendo progresivamente más fino a medida que nos dirigimos a la zona
supralitoral de las playas.
La costa Norte de la Península Ibérica es una región donde se han
llevado a cabo muy pocos estudios de ecología de playas. Uno de los objetivos
de la presente tesis es establecer una base de investigación que sirva como
referencia para futuros trabajos y experimentos. La primera y segunda parte de
esta tesis (ver Capítulos 1, 2 y 3) analizan las características principales de la
ecología y de la estructura de la macrofauna; tales como la riqueza y
composición de especies, la distribución espacial y zonación de la macrofauna
o los efectos de las principales variables ambientales que afectan a la
macrofauna bentónica. Aunque no se ha realizado un seguimiento temporal de
la comunidad macrofaunística de estas playas, lo cual le puede restar algo de
fiabilidad al estudio, el muestreo instantáneo comparativo de diecinueve playas
del mismo tipo y de una misma región nos ofrece un análisis representativo
fundamental de la estructura faunística. El énfasis en el análisis de las variables
ambientales en este estudio se ha centrado en el efecto espacial o en los efectos
que se producen en un periodo corto de tiempo. Sin embargo, hay una
evidencia clara, al menos en las playas micromareales, de que la escala
Part V Discusión general
240
temporal es muy importante en el estudio de la ecología de playas (e.g.
Brazeiro y Defeo, 1996; Degraer et al., 1999; Dugan et al., 2004).
Probablemente la pérdida de replicación en el tiempo de alguno de los capítulos
de este estudio (Capítulos 2, 3 y 4) sea una de las más importantes limitaciones
de esta tesis. Aunque los resultados de estos capítulos sugieren que la
macrofauna está principalmente estructurada en el espacio, la información
obtenida está demasiado limitada como para establecer que la escala temporal
es menos importante en un rango mesomareal de playas de regiones templadas.
Sin embargo, los resultados de los primeros capítulos de esta tesis nos
proporcionan la suficiente confianza como para asumir que abordar estos
estudios con la escala espacial adecuada es al menos tan importante como usar
la escala temporal adecuada.
5.7.1.1. Factores ambientales que afectan a la macrofauna bentónica.
Los patrones de variación de, por ejemplo, la riqueza específica se
explican mejor por el grado de exposición de las distintas playas. Los
resultados obtenidos muestran que el número de especies es el parámetro
biológico más afectado por los parámetros ambientales, aumentando de forma
lineal con el rango mareal y disminuyendo con el aumento en el grado de
exposición. Otro factor biótico importante como es la biomasa de la
macrofauna disminuye exponencialmente con un aumento del tamaño medio
del sedimento. Esto demuestra una de las características de los intermareales
arenosos más y mejor documentadas: la disminución de los factores bióticos
(i.e., riqueza específica, abundancia y biomasa de la macrofauna) cuando
pasamos de un estado de playa disipativo a otro reflectivo (i.e., condiciones de
mayor pendiente y tamaño de grano), así como a una mayor exposición. El
tamaño de grano se vio negativamente relacionado con factores bióticos tales
como la riqueza específica o la biomasa. Hay varias razones para asumir que
esta relación es de tipo causal. Por ejemplo, muchas especies pueden encontrar
difícil o incluso ser incapaces de enterrarse en arenas gruesas (Lastra y
McLachlan, 1996; de la Huz et al., 2002) y por tanto verse en dificultades para
sobrevivir debido al aumento de las posibilidades de ser depredado o barrido
Parte V Discusión general
241
por el swash. Además, el sedimento más grueso proporciona un sustrato mucho
menos estable y, de forma indirecta, afecta a la fauna debido a su influencia en
el swash y a la permeabilidad del sedimento. La variación del tamaño de grano
dentro de una misma playa puede provocar una zonación intraespecífica como
en el caso del bivalvo Donax trunculus. Los individuos más jóvenes y
pequeños de esta especie se distribuyen más hacia la zona supralitoral con
sedimentos más finos mientras que los adultos, más grandes, lo hacen hacia la
zona baja del intermareal afectada por el swash y con sedimentos más gruesos.
La variabilidad morfodinámica de una playa está determinada por el
rango de sedimento y el cambio en el oleaje pero también hay que incluir el
efecto asociado a las mareas. El rango mareal no se ha incluido en los estudios
tradicionales porque éstos se han venido realizando en playas micromareales.
Sin embargo, en las playas mesomareales de este estudio, este parámetro
influye decisivamente en la estructura de la comunidad. A medida que aumenta
el rango mareal y se hace significativamente más importante que la energía del
oleaje, el número de especies también aumenta. Comprobamos que la
morfodinámica descrita por los parámetros Dean y BSI tiene una escasa
capacidad para predecir las características de la comunidad de las playas de
esta región. La validez de estos parámetros morfodinámicos ha sido demostrada
de forma general en estudios donde se incluyen en el análisis un amplio rango
de tipos de playas, i.e. de reflectivas a disipativas, mientras que en el presente
estudio las playas poseen características morfodinámicas y de exposición muy
similares. Además el parámetro Dean ha sido típicamente utilizado en
situaciones micromareales donde la influencia mareal es escasa o inapreciable,
pero parece ser poco eficaz para cubrir situaciones meso o macromareales. Otro
índice muy utilizado en la ecología de playas, el BSI, ha sido probado con éxito
cuando se comparan áreas con diferente rango mareal (Hacking, 1997) y por
tanto no se puede aplicar a cualquier tipo de estudio, ya que la mayor parte de
ellos se concentran en regiones geográficas limitadas en donde sólo una parte
del espectro de condiciones está presente. Quizás el mejor uso de este índice, al
igual que otros nuevos como el BDI o el BI (ver McLachlan y Dorvlo, 2005),
provenga de la disponibilidad actual de resultados de los estudios de playas de
Part V Discusión general
242
distintas regiones, lo que proporciona una base de datos comparable de la
mayoría de tipos de playas y latitudes, a partir de los cuales es posible realizar
estudios de tendencias a un nivel global (e.g. McLachlan y Dorvlo, 2005;
Defeo y McLachlan, 2005).
De forma más general, cuando nos centramos en el estudio de playas de
tipo intermedio, las diferentes características de la comunidad parecen
afectadas por varios factores ambientales. Así, en las playas de este estudio la
variación de la comunidad se explica mejor por el grado de exposición que por
los tradicionales parámetros morfodinámicos o incluso que por la pendiente de
la playa. La exposición representa a varios factores ambientales, confirmando
que la ecología de la macrofauna de playas se ve afectada por un conjunto de
variables y que no existe un único factor ambiental determinante y definitivo.
5.7.1.2. Estructura de la comunidad y zonación de la macrofauna
Los taxones dominantes de estas playas son los comunes a nivel
mundial, siendo los crustáceos el grupo más diverso y abundante, y en menor
número se encuentran los poliquetos y sobre todo los moluscos. El patrón
general de distribución horizontal de la macrofauna confirma el conocimiento
general en ecología de playas: la riqueza de especies aumenta hacia los niveles
inferiores de las playas (e.g. McLachlan y Jaramillo, 1995; McLachlan y
Brown, 2006). La zonación de los intermareales es un fenómeno bastante
estudiado y aunque se han establecido patrones generales para algunos casos
concretos (ver 1.1.2.4. para más detalles) no existe una zonación clara para las
playas y en muchos casos se ha considerado cualquier tipo de división como
artificial en un ambiente que refleja un continuo con superposición de zonas
adyacentes (McLachlan y Jaramillo, 1995; Degraer et al., 1999). Sin embargo
en las playas intermedias de este estudio hemos encontrado alguna evidencia de
una posible división biológica en zonas principales. Quizás el esquema de
zonación más elemental, pero también el más aplicable, se refiera a una típica
zonación dividida en dos zonas principales: una zona estrecha en la parte más
alta de la playa donde se encuentra una típica asociación de especies semi-
terrestres, y por debajo de la cual nos encontramos una zona ocupada por una
Parte V Discusión general
243
asociación de diversas especies verdaderamente marinas (e.g. McLachlan y
Jaramillo, 1995, McLachlan y Brown, 2006). Las características del perfil de
estas playas muestran una influencia directa sobre la estructura y distribución
de las comunidades macrofaunísticas. Las playas estudiadas muestran un perfil
roto de forma abrupta en el nivel mareal medio, que divide el intermareal en
una parte supralitoral de mayor pendiente seguida por una planicie litoral en la
parte baja de la playa supeditada a la acción del oleaje y del swash. La zona
supralitoral es la más evidente y los diversos análisis efectuados indican un
claro límite entre esta parte de la playa y el resto del intermareal siguiendo la
forma del perfil de la playa. Esta zona, que posee una comunidad característica
del supralitoral, es habitual en todas las playas expuestas (McLachlan y
Jaramillo, 1995). El perfil de playa que nos hemos encontrado en este estudio
parece que concuerda bien con esta descripción. Aunque se puede encontrar
alguna subdivisión de la parte baja del intermareal (dos o incluso tres zonas),
creemos que establecer una delimitación clara de zonas no es plausible con este
perfil de playa tan particular.
5.7.1.3. Relación entre la macrofauna y las variables ambientales
La abundancia y distribución de la macrofauna de playas dependen de
varios factores físicos y biológicos. Aquellos factores físicos considerados
tradicionalmente como los más influyentes en la distribución de la macrofauna
serían el rango mareal, el tamaño de grano del sedimento, la exposición, la
acción del swash y la dinámica de acreación y erosión (e.g. Brazeiro, 2001,
McLachlan y Dorvlo, 2005). Todos estos factores están ligados de alguna
manera a la morfodinámica de las playas. Los resultados obtenidos en esta tesis
indican que parámetros ambientales como la pendiente, la altura de la ola y la
longitud de la playa son los factores ambientales que mejor explican la
variabilidad en la densidad de especies. Los dos primeros factores estarían
relacionados con la morfodinámica que determina las características típicas de
una playa expuesta. Las playas con mayor pendiente y altura de ola presentan
un tamaño de grano más grueso y con características de las playas reflectivas.
El efecto en las variables biológicas producido por la hidrodinámica y la
Part V Discusión general
244
morfodinámica de las playas se considera un paradigma en ecología de playas
(Defeo y McLachlan, 2005). Hay una tendencia a la disminución del número de
especies a medida que aumentan las características reflectivas de una playa (i.e.
pendiente más pronunciada y mayor tamaño de grano) y su exposición al oleaje
(Jaramillo y McLachlan, 1993). Además, McArdle y McLachlan (1992) han
sugerido que tanto la altura de la ola como la pendiente de la playa son los
factores más relacionados con las características del swash, el cual a su vez es
el factor ambiental que más afecta a la macrofauna de las playas expuestas.
Parece que las especies con una más clara zonación están también mejor
explicadas por las variables ambientales que aquellas especies con límites de
zonación no tan definidos en su distribución a lo largo del perfil de las playas.
El hecho de no encontrar un patrón claro de influencia de los factores
ambientales sobre la estructura de la comunidad y no encontrar tendencias
significativas entre el swash y el estado morfodinámico con la macrofauna nos
confirma que las comunidades en las playas de esta región están controladas no
sólo por un conjunto de factores ecológicos sino también por otros factores que
pueden ser más dependientes de las condiciones oceanográficas y de los
procesos costeros. A pesar del continuo geográfico que representan las 19
playas de este estudio, las características de la masa de agua a lo largo de la
costa norte española están determinadas por variaciones de la productividad a
diferentes escalas espaciales. Creemos que las diferencias faunísticas
encontradas entre las playas son, en gran parte, debidas al gradiente de
concentración de clorofila de esta región y no sólo a posibles diferencias físicas
de los intermareales. La existencia de un evento de resurgencia común a lo
largo del límite Este del Atlántico Norte en las coordenadas 10º y 44º N y
centrado en el Noroeste de la costa de España (Wooster et al., 1976) puede
estar relacionada con las diferencias faunísticas encontradas a lo largo de
nuestro gradiente de playas (Oeste-Este). La resurgencia tiende a producir un
flujo neto de agua de profundidad rica en nutrientes que llega a la costa norte
española generando un proceso de fertilización que aumenta la producción
primaria y parece que este efecto se ve diluido a medida que nos movemos
hacia el Este a lo largo de la costa norte de España (Lastra et al., 2006). Por
Parte V Discusión general
245
tanto, parece razonable pensar que el aumento de la abundancia
macrofaunística en las áreas próximas a este evento se deba a un aumento de la
disponibilidad de alimento debida al aumento en la productividad.
5.7.2. La importancia de la exposición en la macrofauna de playas:
condiciones hidrodinámicas y disponibilidad de alimento.
Las comunidades macrofaunísticas que viven en los intermareales
arenosos se mantienen casi enteramente gracias a los aportes externos de
materia orgánica ya que muy poca producción primaria se genera en la playa.
En la mayor parte de las regiones templadas, las fuentes principales de materia
orgánica exógena son el fitoplancton y las algas macrófitas. Dependiendo de la
cantidad y calidad del alimento disponible en el intermareal, la estructura de la
comunidad macrofaunística y sus relaciones tróficas puede variar. Las playas
carecen de algas macrófitas asociadas al sedimento que sirvan de alimento y/o
protección a la macrofauna, excepto en casos especiales de playas estuáricas
muy protegidas con praderas de fanerógamas. Las cadenas tróficas en los
intermareales empiezan y acaban principalmente en el mar pero incluso el
ecosistema terrestre puede desarrollar un papel importante en la disponibilidad
de alimento. Los resultados obtenidos en la parte III de esta tesis sugieren que
la comunidad macrofaunística, en términos de abundancia, biomasa y riqueza
específica es más compleja y diversa en playas protegidas que en las más
expuestas siguiendo la premisa tradicional de estudios anteriores que reflejan
una disminución de las variables bióticas con el aumento de la exposición
(Jaramillo y McLachlan, 1993; McLachlan et al., 1993).
5.7.2.1. Características de la macrofauna de playas en un gradiente de
exposición
El supralitoral de las localidades estudiadas muestran una riqueza de
especies baja ya que las condiciones son más duras para la macrofauna
típicamente marina, y el dominio es casi exclusivo de los crustáceos;
básicamente anfípodos talítrido. Este tipo de organismos están adaptados para
evitar la desecación (McLachlan, 1990; Little, 2000) por lo que son mayoría en
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este nivel del intermareal. Además, en el caso de las playas expuestas, estos
crustáceos encuentran en el supralitoral un lugar estable para establecerse
(Defeo y Gómez, 2005) mientras que disminuyen en número hacia el swash.
De hecho, en este estudio, no se han encontrado diferencias significativas entre
los supralitorales de las playas expuestas y los de las protegidas. La mayor
parte de las especies supralitorales han sido consideradas dependientes de las
algas varadas que llegan a las playas asociadas a distintintos procesos
oceanográficos (ver Capítulo 6). Los intermareales protegidos que hemos
estudiado presentan unas condiciones ambientales más favorables y con una
mayor estabilidad que las playas expuestas, lo que se refleja en los valores
significativamente más altos de abundancias, biomasas e incluso de la riqueza
específica cuando se comparan con los niveles medios e inferiores de los
intermareales expuestos. Los resultados obtenidos aquí apoyan la hipótesis de
exclusión del swash, la cual predice que los organismos de los niveles
inferiores de las playas expuestas se verán excluidos por el clima del swash
(ver sección 1.1.2.3), pero no a nivel supramareal donde la acción del swash es
inapreciable. Se ha propuesto además que los organismos de este nivel son
relativamente independientes del régimen del swash, dando lugar a una serie de
respuestas variables a los cambios en el tipo de playa (Defeo y Gómez, 2005).
Tanto las características del swash como del tamaño del sedimento
definirán la repuesta de la macrofauna. El grupo de los moluscos y el de los
poliquetos son los más afectados a medida que aumenta la dureza y la
exposición del sistema intermareal. Ambos grupos aumentan sus abundancias
en los niveles inferiores del intermareal donde se presupone la existencia de
unas condiciones físicas más estables siguiendo la hipótesis del hábitat
favorable (Defeo et al., 2001). En el caso de las playas expuestas estudiadas no
se encontraron especies pertenecientes al grupo de los moluscos y muy pocos
poliquetos. Este tipo de intermareal con condiciones físicas más duras y tamaño
de grano más grueso tienen un efecto negativo en la capacidad de
enterramiento, tasa de respiración y alimento de bivalvos filtradores, como es el
caso de Donax trunculus. En las playas más protegidas, con menor
hidrodinamismo, se ve favorecida la acumulación de materia orgánica,
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fundamentalmente de origen exógeno, disponible para los depositívoros
bentónicos, sobre todo los poliquetos, que se convierten en el grupo dominante
en estos intermareales.
5.7.2.2. Efecto de la composición bioquímica de la materia orgánica en
la macrofauna
En este estudio se han encontrado diferencias significativas en las
concentraciones de materia orgánica entre las playas protegidas y las expuestas,
probablemente relacionado con las características morfodinámicas más suaves
de estos intermareales. Además, se ha encontrado una relación inversamente
proporcional entre la pendiente y el grado de exposición de la playa y la
concentración de BPC en el sedimento. Las playas expuestas de este estudio
muestran un ligero aumento en el tamaño de grano y en la pendiente del
intermareal por lo que parece que las concentraciones de BPC siguen un patrón
similar al de los organismos, que aumentan en número desde las playas
expuestas de pendiente más pronunciada a aquellas más protegidas y con
pendientes más suaves.
La aportación más importante de la composición bioquímica al
sedimento intermareal de este estudio, ya sea expuesto o protegido, se debe a
las proteínas y ocurre de forma más significativa en los niveles inferiores
próximos al swash. El hecho de que las proteínas sean la fracción dominante
del BPC y que los carbohidratos muestren los valores más bajos indica que la
materia orgánica de estas localidades tiene un posible origen de producción
reciente o incluso autóctono. De hecho la relación PROT:CHO, que refleja la
edad de la materia orgánica del sedimento, es lo suficientemente alta como para
suponer que la mayor parte de dicha materia es de producción reciente y que
las proteínas no son limitantes para el crecimiento de los consumidores del
intermareal (Fabiano et al., 1995). Sin embargo, el porcentaje promedio de
proteínas encontrado en las localidades protegidas (63,4 %) es menor que en las
expuestas (80,2 %) mientras que hay una mayor cantidad de materia orgánica
en las playas protegidas, lo que puede indicar una mayor influencia de la
materia orgánica exógena en estos intermareales. Parece que a medida que
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disminuye el grado de exposición del intermareal éste se convierte en lugar de
acumulo de materia orgánica (ver Capítulo 5) mientras que las playas expuestas
dependen más de los aportes externos esporádicos como por ejemplo las algas
varadas en el intermareal (ver Capítulo 6).
La disponibilidad final de materia orgánica será el resultado de la
interacción entre los procesos físicos y biológicos que tengan lugar en el
intermareal. Los resultados de este estudio sugieren que el control de la
macrofauna de playas no está determinado exclusivamente por el ambiente
físico y, aunque éste pueda ser un factor fundamental, otros factores
ecológicos, incluyendo la composición bioquímica de la materia orgánica en el
sedimento van a influir también en la estructura de la comunidad
macrofaunística.
5.7.3. El papel de la disponibilidad de alimento en la estructura de la
comunidad de playas: patrones espaciales y temporales.
En la parte IV de esta tesis se estudiaron en dos playas con diferente
grado de exposición el efecto que tiene la disponibilidad de alimento en la
estructura de la comunidad bentónica. En el Capítulo 5 se discuten los
resultados de un estudio realizado en una playa estuárica protegida a lo largo de
dos años, teniendo en cuenta el valor nutricional de la materia orgánica
sedimentaria y su relación con la macrofauna bentónica. Dada la importancia
de la materia orgánica exógena en las playas, el Capítulo 6 presenta un estudio
de estos aportes en forma de algas varadas y como afectan a la comunidad
faunística de un intermareal expuesto. Con estos dos estudios pretendemos
identificar el papel que tienen los aportes de materia orgánica en la variabilidad
observada en la macrofauna de intermareales.
5.7.3.1. Variabilidad estacional en la distribución de la macrofauna
bentónica y de la disponibilidad de alimento en una playa estuárica
protegida.
El análisis temporal de la distribución de la macrofauna bentónica en
una playa estuárica protegida (Barraña) nos demuestra que los niveles mareales
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estudiados presentan una diferente diversidad faunística. Poliquetos y moluscos
aparecen principalmente en el nivel intermareal y los crustáceos tienden a
situarse en los niveles más altos de la playa ya que son menos susceptibles a la
desecación. Además de a nivel horizontal, se han encontrado claras diferencias
en la distribución vertical de la macrofauna. Esto puede ser debido a las
diferencias en las características del sedimento, como el tamaño de grano o la
compactación, que pueden condicionar la capacidad de enterramiento de los
organismos. Sin embargo, las características del sedimento no son capaces de
explicar por sí solas las diferencias encontradas en la distribución de la fauna
bentónica. La distribución en profundidad de estos organismos podría
explicarse mejor por la presencia y posición de la discontinuidad del potencial
redox (RPD) ya que los organismos bentónicos son dependientes del oxígeno
disuelto para respirar. El RPD en esta playa se encontró en el límite de los 5-10
cm que representaba a su vez la franja de mayor concentración de la
macrofauna (75%).
Los intermareales protegidos presentan óptimas condiciones
ambientales para la macrofauna en términos de humedad, temperatura y aporte
alimenticio. El bajo hidrodinamismo hace que el intermareal protegido sea más
independiente de las condiciones físicas que cualquier playa expuesta y la
macrofauna bentónica se ve favorecida por las acumulaciones de la materia
orgánica (Defeo et al., 2001). El nivel medio de este intermareal es el más rico
en términos de abundancia y riqueza específica y también destaca por la
presencia de concentraciones máximas de BPC; i.e., alimento disponible. El
perfil característico de esta playa, junto a las condiciones ambientales más
favorables aumenta la presencia de la materia orgánica y del contenido en agua
en el nivel medio. Estas condiciones pueden fomentar la abundancia y la
riqueza faunística en este parte de la playa, en comparación con el nivel más
bajo del intermareal o el supralitoral. La mayor parte de las especies que se
encontraron en el intermareal pertenecen al grupo de los depositívoros,
favorecidos por la mayor acumulación de materia orgánica en el sedimento
durante el invierno y la primavera. Los depositívoros son organismos capaces
de explotar los recursos de forma rápida y eficiente y un aumento de su
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abundancia se ha relacionado con un aumento en la concentración de proteínas
(Rossi et al., 2001). Por otro lado, los organismos suspensívoros se encuentran
restringidos a la parte más baja del intermareal ya que no resisten largos
periodos de exposición.
Durante este estudio se ha encontrado una gran variabilidad en la
estructura y dinámica de la comunidad macrofaunística que podría estar
relacionada con las fluctuaciones en la disponibilidad y en la calidad de los
recursos alimenticios. Una parte importante de la materia acumulada en esta
playa pertenece a la porción más lábil y las proteínas, a su vez, fueron la
fracción mayoritaria de dicha porción, lo que implica que la materia orgánica es
en su mayoría de producción reciente. El aumento en proteínas, sobre todo en
invierno, provoca un incremento en la calidad del alimento disponible y se
puede relacionar de forma directa con aportes de origen exógeno que son más
habituales en esta época del año. El descenso en la concentración de proteínas y
de la relación PROT:CHO en la época estival y comienzos del otoño puede
deberse a la disminución en el aporte marino, aumento de las temperaturas y de
la radiación solar típicas de esta estación. Durante este periodo disminuye el
aporte de detritus orgánico en forma de algas y aumenta la fracción refractaria
de la materia orgánica. El aumento de procesos de descomposición en verano
puede ser el responsable principal de la disminución de la fracción más lábil de
la materia orgánica, lo que sugiere una menor disponibilidad de recurso
alimenticio y un aumento de materia orgánica vieja causada por la
descomposición de las algas varadas. Durante el invierno se pueden producir
aportes exógenos episódicos que provocan la acumulación de algas varadas en
los intermareales introduciendo materia orgánica nueva. Algunos animales
bentónicos se benefician de estos a portes clave.
La concentración de clorofila en el sedimento presenta picos de
abundancia en invierno y los valores particularmente elevados podrían
relacionarse con la deposición de algas y las bajas tasas de descomposición
durante este periodo que pueden generar un ambiente ideal para la
productividad microbiana con un consecuente aumento en la actividad
fotosintética (Kelaher y Levinton, 2003). Las grandes variaciones en algunos
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casos (Enero 1997) son difíciles de explicar y puede que tengan una relación
importante con la presencia puntual de un mayor volumen de algas varadas en
el intermareal y con bajas tasas de descomposición en esta época.
Este estudio muestra la importancia de la disponibilidad de alimento
para la comunidad macrobentónica de las playas. Además, la cantidad y la
calidad del alimento tienen la capacidad de producir un cambio sustancial en la
variación espacio-temporal en la estructura de las asociaciones
macrofaunísticas. Los análisis realizados establecen que tanto la disponibilidad
de alimento como la clorofila son los principales factores que explican la
distribución de la macrofauna en los niveles intermareales. Tanto la
macrofauna como la materia orgánica o la clorofila son más abundantes en el
nivel intermareal donde la acción del swash es más efectiva que en el
supramareal. La importancia del alimento disponible y del tipo de swash se han
establecido recientemente como los factores claves en el control de la
macrofauna de los intermareales de fondos blandos (Incera et al., 2006).
Aunque no podemos establecer un patrón estacional claro, podemos
dilucidar que se produce un aumento en la calidad del alimento disponible en
invierno, debido fundamentalmente a la contribución de la concentración de
proteína. En verano y a finales de verano lo que se produce básicamente es una
acumulación de materia orgánica más antigua que disminuye la calidad del
alimento presente en el sedimento.
Los análisis de regresión múltiple corroboran los resultados obtenidos y
muestran una correlación positiva entre la materia orgánica sedimentaria y las
características de la macroinfauna (biomasa, abundancia de la macrofauna,
abundancia de poliquetos y crustáceos). Aunque parece que hay una fuerte
relación entre la macrofauna y la calidad del alimento disponible, no se puede
establecer una causación directa; entre otras cosas porque la distribución de
algunos de los factores, como los pigmentos y los nutrientes, son dependientes
de la profundidad. Las conclusiones obtenidas en esta parte del estudio deben
ser tratadas como predicciones que apunten a la manipulación experimental
como el siguiente paso a dar en el proceso de investigación. Este estudio nos
muestra que la macrofauna de playas estuáricas protegidas no está determinada
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de forma exclusiva por las fuerzas físicas sino que hay una relación
determinada por las fuentes de alimento. La macrofauna en este estudio ha
mostrado una serie de preferencias en su distribución vertical y horizontal en el
intermareal que sugiere que la distribución específica depende de una
sensibilidad concreta hacia varios factores entre los que se incluye la
disponibilidad de alimento. Finalmente, podemos decir que la valoración de la
variabilidad vertical y horizontal y la estructura relativa de la comunidad
macrofaunística muestra una fuerte heterogeneidad temporal lo que sugiere que
la macrofauna de playas estuáricas está relacionada con factores complejos e
impredecibles.
5.7.3.2. Efecto de las algas invasoras sobre la asociación macrofaunística
de una playa expuesta
Varios estudios han examinado el papel de las algas que llegan a las
playas desde el mar y permanecen temporalmente depositadas en el
intermareal. Su origen es diverso, desde praderas de fanerógamas de zonas
estuáricas protegidas a macroalgas procedentes de los intermareales rocosos o
del submareal más próximos. La mayor parte de las playas reciben una pequeña
cantidad de estos aportes, pero en algunas situaciones puede ser sustancial,
especialmente después de las tormentas invernales.
Las algas varadas son usadas como alimento por algunos organismos
asociados a la duna y a la zona de berma de la playa, tales como anfípodos
talítridos, isópodos e insectos, dominando por completo las cadenas tróficas de
las playas expuestas (Colombini y Chelazzi, 2003). Sin embargo la mayor parte
de la descomposición de esta materia la realizan bacterias, lo que puede llevar
mucho tiempo, dependiendo del tipo de material varado en la playa (Griffiths et
al., 1983; Jędrzejczak, 2002). Estos acúmulos de algas pueden servir también
de protección, ovoposición y como lugar de desarrollo de larvas de diversas
especies de invertebrados, tanto marinos como típicamente terrestres.
La abundancia tan significativa de organismos hallados en los
acúmulos de algas en la playa estudiada (Ladeira) demuestra la importancia de
los varamientos en los intermareales expuestos. Los resultados obtenidos
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muestran una abundancia mayoritaria de moscas del orden Diptera
(principalmente larvas) y de coleópteros de las familias Staphylinidae y
Tenebrionidae. Aunque los anfípodos talítridos han sido considerados como los
principales colonizadores y consumidores de las macroalgas varadas (Inglis,
1989; Colombini et al., 2000) nuestro estudio muestra un escaso número de
especies de esta familia. La escasez puede ser debida a las duras condiciones
ambientales que encontramos en la playa durante el periodo de estudio. Las
altas temperaturas y el fuerte viento caracterizaron los días siguientes al
establecimiento del experimento lo que provocó una secado rápido de los
parches de algas. De hecho, estudios previos han demostrado que el
comportamiento de los talítridos está fuertemente influido por las condiciones
climáticas del momento, tales como la humedad del aire y del sedimento así
como la temperatura de la arena (e.g. Scapini et al., 1992; Colombini et al.,
1998; Fallaci et al., 1999).
La presencia de acúmulos de un alga invasora (Sargassum muticum)
frente a los acúmulos conformados por un alga nativa (Saccorhiza polyschides)
promovió dos tipos diferentes de patrones de colonización. En términos de
números totales de individuos los resultados fueron más abundantes en aquellos
parches de S. polyschides que en los parches de S. muticum. Está diferencia fue
muy evidente a los tres días de empezar el experimento y se fue haciendo
menor a medida que pasaba el tiempo y las diferencias más abultadas se
centraron en la abundancia de las especies de larvas. Sin embargo, la diversidad
y el número de especies promedio fueron mayores en los acúmulos de
S.muticum al tercer día, aunque este patrón se revirtió en los días siguientes. Al
comienzo del estudio las mayores abundancias encontradas en los acúmulos de
alga nativa fueron debidas casi exclusivamente a una larva de la misma especie
de mosca, (Anthomyiidae sp 1). Esta dominancia explica el bajo número de
especies y la baja diversidad encontrada en los acúmulos de alga en los
primeros días del estudio. A partir del día tres la abundancia de larvas
disminuyó de forma progresiva y tanto el número de especies como la
diversidad aumentaron hasta alcanzar mayores valores en S. polyschides. La
presencia de estos acúmulos de algas en los intermareales puede estimular la
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reproducción, la puesta de huevos, el establecimiento de larvas o el
reclutamiento de distintas especies (Bolam et al., 2000). En el caso de las
moscas, los adultos son insignificantes consumidores de algas pero encuentran
en estos restos un lugar ideal para la ovoposición. Estos huevos intervendrán
decisivamente en la descomposición de las algas, bien directamente por
consumo de las macrófitas o propagando microorganismos consumidores del
tejido. Por los resultados obtenidos en este estudio, parece que los acúmulos de
algas nativas son un hábitat más apto y constituyen una fuente de alimento para
estas especies. Quizás la estructura física y/o las condiciones microclimáticas
características de esta especie de alga pueden favorecer específicamente la
ovoposición y el desarrollo de larvas de dípteros.
La mayor parte de las especies colonizaron rápidamente los acúmulos
de los dos tipos de algas (87 % en los tres primeros días) pero los patrones de
colonización fueron distintos según la especie y sus hábitos tróficos, siguiendo
las distintas etapas de descomposición y envejecimiento de las algas. Las
especies de herbívoros como el coleóptero Cercyon littoralis colonizan pronto
los dos tipos de parches de algas y permanecieron presentes todo el tiempo de
estudio. Un poco más tarde aparecen especies de carroñeros como el
tenebrionido Phaleria cadaverina y especies de carnívoros (H. rubripes y A.
variana) que presentan su mayor abundancia a los siete días y su presencia se
extiende hasta el final del experimento. Este aumento de especies depredadoras
y carroñeras puede estar directamente relacionado con la abundancia de larvas
e individuos inmaduros que pueden servir de fuente de alimento. Aunque las
especies encontradas en los dos tipos de algas son diferentes, no se ha
encontrado una tendencia consistente a lo largo del tiempo y del espacio. Esto
lo que sugiere es que otros factores además del tipo de alga están influyendo en
los patrones de colonización y sucesión. Por ejemplo, las variaciones
encontradas pueden estar relacionadas con cambios microclimáticos
progresivos debidos a las diferentes posiciones de las algas en la playa; tanto la
zona de duna como la de berma presentan condiciones ambientales variables.
Los resultados de este estudio muestran evidencias suficientes para
apoyar la hipótesis de que la asociación macrofaunística cambia como
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respuesta al tipo de alga presente en el intermareal. Los carbohidratos, la
materia orgánica e incluso la clorofila son las variables que mejor describen los
patrones de asociación de la macrofauna. Además, tanto la temperatura como la
humedad tienen alguna influencia en la presencia de algunas de las especies en
los parches de algas. Pequeñas variaciones de estos parámetros ambientales
pueden afectar a la colonización por diversas especies, ya que las condiciones
microclimáticas de los depósitos de algas han sido consideradas como factores
que afectan de manera importante el comportamiento de varias especies de
artrópodos (Colombini et al., 1998). El valor nutricional de las algas difiere
entre los dos tipos de algas. En la mayoría de los caso, el contenido orgánico
(fundamentalmente lípidos y carbohidratos) es mayor en S. muticum y la
Clorofila a (indicativo de la biomasa de microalga bentónica) en S. polyschides.
El contenido de microalgas bentónicas puede tener un papel importante en la
regulación de los flujos de carbono a los intermareales costeros (Herman et al.,
2000) y, de hecho, una mayor concentración podría relacionarse con un menor
contenido en polifenoles en las hojas de laminarias (S. polyschides). El
contenido en polifenoles de las algas pardas tiene como funciones proteger al
alga de patógenos o rayos UV e incluso para disuadir a los herbívoros (Van
Alstyne et al., 1999). Los nutrientes liberados de los acúmulos de algas pueden
ser utilizados directamente por el microfitobentos que a su vez pueden regular
el flujo de nutrientes al sedimento ya que representan, directa o indirectamente,
una fuente alimenticia para algunos invertebrados (Rossi y Underwood, 2002).
Aparte de las diferencias en el valor nutricional y en las condiciones
microclimáticas de los dos tipos de algas, la distinta estructura y complejidad
de los parches podría jugar un papel importante en la variabilidad encontrada
en la asociación macrofaunística. La distinta morfología y estructura de las
macroalgas provoca una variabilidad importante en la calidad del hábitat que
afectará a la capacidad de protección o la conveniencia del lugar de
ovoposición. En algunos casos, la preferencia de los invertebrados por ciertas
especies de algas pueden estar relacionadas con factores tales como la
disponibilidad y la provisión de hábitat o de refugio más que por el valor
nutricional (e.g. Wakefield y Murria, 1998).
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Los resultados obtenidos en este estudio indican que un
reemplazamiento de los depósitos de algas nativas varados en las playas por
acúmulos de algas alóctonas puede tener efectos importantes en la estructura de
la comunidad de la fauna de invertebrados. Un cambio en el tipo o cantidad de
alga de arribazón que llega a una playa puede alterar la asociación
macrofaunística y por tanto el funcionamiento del ecosistema en su conjunto.
5.7.4. Cuestiones abiertas.
Quizás la cuestión más importante que surge del estudio realizado
sobre la estructura de la comunidad macrofaunística de playas, resumido en
esta tesis, sea el efecto de las diferentes escalas temporales. Debido a que la
zonación de la fauna es dinámica, estudios temporales de los Capítulos 2, 3 y 4
(correspondientes a las partes II y III) nos podría mostrar un patrón de zonación
más claro, lo que requiere un muestreo temporal intensivo, p.ej.
bimensualmente durante un año, que nos proporcione estimaciones imparciales.
La replicación temporal, siguiendo por ejemplo las posibles diferencias
estacionales, es un factor importante al tener en cuenta la variabilidad de los
resultados obtenidos. De hecho, podría encontrarse más variabilidad de una
semana a otra que entre estaciones por lo que en la mayor parte de los estudios
es recomendable muestrear a menudo, tanto para detectar una tendencia
temporal como para crear réplicas de muestreo en el tiempo (Underwood,
1997) que eviten confusiones en la interpretación de los datos.
En cuanto a la distribución de la macrofauna, el trabajo realizado sobre
la zonación en el Capítulo 3 cubre un aspecto importante de la comunidad
bentónica en playas, como es su distribución a través del perfil intermareal.
Otro punto de interés estaría relacionado con la distribución a lo largo de la
playa. Aunque los lugares escogidos dentro de las playas pueden asumirse
representativos del resto del intermareal, una selección de dos o incluso tres
sitios distintos dentro de cada una de las playas muestreadas podría realzar las
posibles diferencias en la distribución espacial de la macrofauna dentro de un
mismo intermareal. Una vez más, el trabajo de muestrear 19 intermareales
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teniendo en cuenta una mayor variación espacial implicaría un diseño
logísticamente muy complicado.
En el Capítulo 4, la distribución longitudinal de la macrofauna en la
playa estuvo bien cubierta debido a la escasa anchura del intermareal estudiado
para la ocasión. En el caso de la distribución horizontal, los tres niveles
mareales escogidos en este estudio son suficientemente representativos de las
características ambientales específicas del gradiente mareal.
Es importante señalar que las playas expuestas y protegidas
seleccionadas en este estudio están asociadas geográficamente. Con este diseño
el efecto espacial y el de exposición pueden confundirse. Aunque hay una
obvia separación geográfica entre los intermareales expuestos y los protegidos,
estudios previos indican que valores de variables ecológicas tan importantes
como el número de especies, la biomasa y la clorofila a son más altos en las
playas del Noroeste de la costa española debido a la influencia de la
resurgencia estacional localizada en esta zona de la Península Ibérica (Lastra et
al., 2006). Sin embargo, un futuro estudio más exhaustivo de estos
intermareales debería incluir playas de la misma exposición en la misma área
de estudio. Un trabajo estadísticamente más preciso debería incluir al menos
tres playas expuestas y tres protegidas de la misma ría y compararlas con otras
tres playas de cada tipo en otra ría distinta. Además, la pérdida de relación
existente entre alguno de los descriptores bióticos y la composición bioquímica
del sedimento podrían haberse clarificado, una vez más, incluyendo la
variación temporal.
El estudio presentado en el Capítulo 5 solventa alguna de las
incertidumbres creadas por la falta de un estudio temporal más completo. Sin
embargo, la estructura de la comunidad o la composición bioquímica de la
materia orgánica del sedimento de la playa de Barraña no presentan un patrón
temporal característico. La influencia de factores antropogénicos de difícil
análisis y predicción pueden haber sido fundamentales a la hora de conformar
un patrón estacional tan poco claro. Un estudio en localidades sin efectos
antrópicos directos o la comparación de localidades de distintas áreas
geográficas podría contribuir a clarificar algo más los resultados obtenidos. En
Part V Discusión general
258
este estudio se refleja también la importancia de tener datos y antecedentes de
aquellos lugares influidos por las actividades antrópicas y también en
condiciones ideales para ver si se los cambios producidos obedecen a patrones
temporales naturales o a otros efectos externos más complejos.
Un seguimiento del trabajo de campo durante varios años, con una
resolución razonable (mensual o bimensual) puede clarificar la falta de patrón
de distribución o de comportamiento faunísticos o la falta de relación entre
factores bióticos y abióticos, pero deberían ser combinados con experimentos
de distinta índole. Así, el uso de especies indicadoras o la manipulación de las
fuentes externas de alimento usando mesocosmos o trabajando en el laboratorio
sería un complemento esencial de los estudios tradicionales de playas.
Estudiar factores ambientales in situ, como por ejemplo el swash, no
revela toda la información sobre los mecanismos que están detrás del
comportamiento y la distribución de la macrofauna de playas. Para entender los
mecanismos que subyacen en la dinámica de playas, es crucial tener un control
independiente sobre los diferentes parámetros físicos, lo que exige la necesidad
de distintos experimentos. Así, el uso de acuarios o tanques pueden
proporcionar resultados valiosos que permitan trabajar con factores tan
cruciales como el tipo de sedimento, la pendiente, regular el efecto del swash
(periodo, velocidad) o trabajar con especies clave. El estudio de preferencias
alimenticias de las distintas especies también se verán beneficiadas de
experimentos en laboratorio o mesocosmos en intermareales. Trabajos como el
de Lastra et al., 2007 (enviado) son pioneros en la manipulación controlada de
especies de talítridos y en el análisis de sus preferencias alimentarias, tanto en
laboratorio como en el intermareal, que permiten elucidar el comportamiento
de especies de la macrofauna bentónica de distintas áreas geográficas y
comparar el uso específico que hacen estos organismos de las distintas fuentes
externas de alimento que llegan a las playas.
La existencia de correlación no prueba causación de ningún tipo, por lo
que las conclusiones que obtenemos de este estudio deben ser tomadas como
predicciones que ayuden a las manipulaciones experimentales como el paso
natural que debe seguir a un estudio descriptivo. En el caso de las algas varadas
Parte V Discusión general
259
y especies invasivas, distintos experimentos en laboratorio podrían comprobar
diversas hipótesis a cerca de la influencia de la estructura física de los distintos
tipos de alga; un análisis de isótopos estables nos proporcionaría las pistas
necesarias sobre el origen y las preferencias de las fuentes alimenticias de los
invertebrados así como de los flujos tróficos en playas. Es importante tener en
cuenta el efecto de las especies invasoras para el futuro de los estudios en
ecología de playas ya que pueden afectar irreversiblemente a la comunidad
faunística y al funcionamiento del ecosistema. El efecto provocado por un alga
alóctona como S. muticum puede extenderse rápidamente de sus puntos de
invasión originales, ya sea el intermareal o submareal rocoso, a los
intermareales arenosos más cercanos. Es importante, por tanto, mantener un
estudio de valoración de los impactos que se producen en los distintos
ecosistemas marinos como criterio básico para valorar el impacto directo de
especies alóctonas que pone en evidencia la necesidad de una gestión prioritaria
de los efectos de las distintas especies invasoras en los ecosistemas costeros.
Las asociaciones macrofaunísticas que aparecen en los depósitos de
algas varadas en las playas expuestas son también recursos importantes para
numerosas especies de aves y, por lo tanto, son una parte básica de la red
trófica actuando como un nexo de unión fundamental entre los ecosistemas
marino y terrestre (Hubbard y Dugan, 2003; Orr et al., 2005). Actividades tan
comunes, en zonas costeras con gran concentración turística, como la limpieza
de playas puede provocar efectos irreversibles que determinen la diversidad y
abundancia de especies, afectando consecuentemente a estos dos ecosistemas.
PART VI. GENERAL CONCLUSIONS
Part VI General Conclusions
261
1. The intertidal benthic macrofauna inhabiting intermediate sandy beaches of
northern Spain cannot be fully related to morphodynamic beach characteristics
because of the limited range of beaches studied. The number of species is better
explained by the beach exposure rate and tide range rather than by traditional
variables such as Dean’s parameter or beach slope.
2. There is a trend in the sandy beaches studied where an exposure increase leads
to a decrease in biotic variables due to the increase in hydrodynamic
conditions, i.e. harsh swash climate and coarser grain size. There is no unique
key factor affecting benthic macrofauna but several ecological factors influence
the different community variables.
3. Community characteristics from intermediate sandy beaches are affected by
several physical factors. Beach length, slope and wave height are the main
variables affecting macroinfauna assemblages. An increase in beach length
together with more dissipative conditions, i.e. low slope and high wave height,
affect species positively. It seems that macrofauna community characteristics in
sandy beaches are not just determined by beach morphodynamics, but also by
other factors dependent on oceanographic conditions and coastal processes,
determining critical characteristics such as food availability.
4. Macrofauna from intermediate exposed sandy beaches shows no clear intertidal
zonation although two specific zones can be established: a narrow dry high-
shore assemblage of air-breathing species, i.e. the supralittoral zone, below
which there is a wide zone of water-breather species, i.e. the littoral zone.
Species with the clearest zonation pattern are the best explained by the
environmental variables than species with no sharp boundaries in their
distribution along the beach profile.
5. Analyses of distribution of benthic macrofauna along the intertidal demonstrate
that the tidal levels are characterised by distinct faunal densities and species
composition. Macroinfauna community, in terms of abundance, biomass and
species richness is more complex and diverse in sheltered than in exposed
sandy beaches. Crustaceans, mainly talitrids amphipods and cirolanid isopods,
are the dominant group in the supratidal level of both, exposed and sheltered
beaches; while polychaetes and molluscs occupy the intertidal level in sheltered
Part VI General Conclusions
262
intertidals with more favourable environmental conditions, sediment stability
and organic matter accumulation.
6. Macroinfauna and biochemical compounds showed a clear vertical
stratification with the highest values and concentrations at the superficial layer
of the sediment, where redox potential discontinuity was also observed.
Macrofauna organisms showed preferences both in vertical and horizontal
ranges suggesting a specific distribution which is related to specific sensitivity
to several abiotic factors, including food availability. This emphasizes how
complex the ecology of organisms inhabiting this apparently simple intertidal
habitat might be.
7. The relative structure of the macroinfauna community display a strong
heterogeneity over time, suggesting that macrofaunal assemblages in estuarine
beaches are controlled by complex and unpredictable factors, including small
scale changes in substrate and hydrological characteristics. The existence of a
strong anthropogenic influence may add an important variability factor in the
sedimentary organic distribution and macrofauna community structure of the
intertidal.
8. There is evidence to suggest that food quality can be a main factor, together
with the hydrodynamic conditions, affecting macroinfauna community in the
intertidal. The distribution patterns of macroinfauna beach assemblages result
from a combination of biotic (such as food availability) and abiotic (such as
beach slope, sand particle size or swash climate) factors. It seems that exposed
sandy beaches are mainly physically controlled, whereas hospitable sheltered
beaches let other factors, such as food availability, enrich the benthic fauna
scenery. The observed patterns of macrofauna and biochemical compounds
seem to be better related in sheltered beaches than in exposed ones.
9. Macroinfauna distribution and trophic structure are directly related to the
quantity and quality of the sedimentary organic matter of the intertidal. The
main trophic group inhabiting sheltered intertidal zones belonged to the deposit
feeders, basically formed by polychaetes. This group seems to be regulated by
the availability of sedimentary food resources. Most of the subterrestrial
species at the supratidal level have been considered wrack-associated
Part VI General Conclusions
263
macrofauna and they depend on allochthonous inputs associated with
oceanographic processes rather than on the swash climate.
10. It is important to consider macrophyte wrack supply together with physical
factors in order to better understand the processes that influence community
structure on sandy beaches. There is some evidence to support that macrofaunal
assemblages change in response to time, and different responses at different
sites may be related to different environmental conditions. Wrack deposits are
important in determining spatial and temporal patterns of macrofaunal
distribution on exposed sandy beaches.
11. Different types of wrack deposits, i.e. native versus invasive algal wrack, are
not used uniformly by invertebrates. There is evidence to support that
nutritional content and microclimatic conditions of wrack deposits affect
macrofaunal assemblages of exposed beaches. The replacement of native wrack
deposits by exotic wrack may have important effects on macrofaunal
assemblages on sandy beaches. A change in the type or amount of seaweed
wrack entering a beach may alter the macrofaunal assemblages and ecosystem
function.
12. The effect of the invasive seaweed S. muticum may have an effect that is spread
away from the points of invasions, i.e. intertidal and subtidal rocky shores. An
assessment of impact on different marine ecosystems may be important criteria
in assessing the effect of this invasive species and the prioritization of exotic
management.
PART VII. APPENDIX
Part VII Appendix
265
PART II: Chapters 2 and 3.
Appendix A. List of macrofauna collected in all the sandy beaches sampled. (+
Presence).
Sp
ecie
s
Peñ
arr
on
da
O
tur
S. P
ed
ro
Xag
ó
Xiv
are
s
Esp
asa
Veg
a
To
ran
da
A
nd
rín
Mollu
sca
Donax tru
nculu
s
+
Cru
sta
cea
Bath
yp
ore
ia p
ela
gic
a
+
Cum
opsis
fa
gei
+
Dio
genes p
ug
ilato
r
+
Eury
dic
e p
ulc
hra
+
+
+
+
+
+
+
+
+
Eury
dic
e a
ffin
is
+
+
+
+
+
+
+
+
+
Gastr
osaccus n
orm
an
i
Gastr
osaccus s
anctu
s
+
+
+
+
+
+
+
Gastr
osaccus s
pin
ifer
+
Hasto
rius a
renari
us
+
+
+
+
+
+
+
+
+
Mysid
acea
in
det.
+
Ponto
cra
tes a
renari
us
+
+
+
+
+
+
+
+
+
Port
um
nus latipes
+
+
+
+
+
Sph
aero
ma h
oo
keri
+
Sph
aero
ma r
ug
icau
da
+
+
+
+
+
+
+
+
+
Talit
rus s
alta
tor
+
+
+
+
+
Talo
rchestia b
rito
+
+
Talo
rchestia d
eshayesii
+
Tylo
s e
uro
peaus
+
+
Uro
thoe
pu
lche
lla
+
Part VII Appendix
266
Sp
ecie
s (
co
nti
nu
ati
on
) P
eñ
arr
on
da
O
tur
S. P
ed
ro
Xag
ó
Xiv
are
s
Esp
asa
Veg
a
To
ran
da
A
nd
rín
Poly
cha
eta
Dis
pio
uncin
ata
+
Ete
one lo
nga
+
Mala
coero
s fu
ligin
osu
s
+
Nephty
s ci
rrosa
+
+
+
+
+
+
+
+
Ophelia
bic
orn
is
+
+
+
Ph
yllo
doci
dae in
det.
+
Sco
lele
pis
squ
am
ata
+
+
+
+
+
+
+
+
Sig
alio
n m
ath
ildae
+
+
Oth
ers
Hym
eno
pte
ra
+
+
+
Nem
ert
ea
+
+
+
+
+
+
+
+
+
Olig
ach
aeta
Ara
ne
i +
+
+
Dip
tera
+
+
+
+
+
+
+
+
+
Cole
opte
ra
+
+
+
+
Part VII Appendix
267
Sp
ecie
s (
co
nti
nu
ati
on
) O
yam
bre
L
ien
cre
s
La
ng
re
Be
rria
L
are
do
S
alv
aje
B
ak
io
La
ga
Z
ara
utz
H
en
da
ya
Mollu
sca
An
gu
lus t
en
uis
+
Do
nax t
run
cu
lus
+
+
+
Hyd
rob
ia u
lva
e
+
+
Cru
sta
ce
a
Ba
thyp
ore
ia p
ela
gic
a
+
+
+
+
Cu
mo
psis
fa
gei
+
+
+
Dio
ge
ne
s p
ug
ila
tor
+
+
Eo
cu
ma
do
llfu
si
+
Eu
ryd
ice
pu
lch
ra
+
+
+
+
+
+
+
+
+
+
Eu
ryd
ice
aff
inis
+
+
+
+
+
+
Ga
str
osa
ccu
s n
orm
an
i
+
Ga
str
osa
ccu
s s
anctu
s
+
+
+
+
+
+
+
+
+
Ga
str
osa
ccu
s s
pin
ife
r
+
+
+
Ha
sto
riu
s a
ren
ari
us
+
+
+
+
+
+
+
Idoth
ea n
eg
lecta
+
Mic
rode
uto
pus d
am
no
nie
nsis
+
Mic
rode
uto
pus s
p.
+
Mysid
ace
a in
det.
+
+
Pa
raja
ssa
pe
lag
ica
+
Po
nto
cra
tes a
ren
ari
us
+
+
+
+
+
+
+
+
+
Po
rtu
mnu
s la
tip
es
+
+
+
+
+
+
Sp
ha
ero
ma r
ug
ica
ud
a
+
+
+
+
+
+
+
Ta
litr
us s
alta
tor
+
Ta
lorc
hestia
bri
to
+
+
Ta
lorc
hestia
de
sh
aye
sii
+
Uro
tho
e b
revic
orn
is
+
Part VII Appendix
268
Sp
ecie
s (
co
nti
nu
ati
on
) O
yam
bre
L
ien
cre
s
Lan
gre
B
err
ia
Lare
do
S
alv
aje
B
akio
L
ag
a
Zara
utz
H
en
da
ya
Uro
thoe
pose
idonis
+
Poly
cha
eta
Dis
pio
uncin
ata
+
Drilo
nere
is filu
m
+
Gly
cera
tridacty
la
+
Lum
bri
neri
s s
p.
+
Nephty
s c
irro
sa
+
+
+
+
+
Ophelia
bic
orn
is
+
+
+
+
Ophelia
neg
lecta
+
Para
done
is s
p.
+
Scole
lepis
squ
am
ata
+
+
+
+
+
+
Sig
alio
n m
ath
ildae
+
Sig
alio
n s
quam
atu
m
+
+
Spio
phan
es b
om
byx
+
Syl
lidae ind
et
+
Oth
ers
Insecta
+
+
+
+
Nem
ert
ea
+
+
+
+
+
+
+
Olig
achaeta
+
+
+
+
+
Ara
ne
i
+
+
Dip
tera
+
Cole
opte
ra
+
+
+
Pla
the
lmin
tes in
det.
+
Echin
ocard
ium
sp
.
+
Part VII Appendix
269
PART III: Chapter 4.
Appendix A. List of macrofauna collected in all the sandy beaches sampled.
Trophic group: suspension feeders: f; surface detritus feeders: s; subsurface
detritus feeders: b; carnivores: c; others: o (+ Presence).
Taxa Sheltered beaches Exposed beaches
Trophic group Broña Bornelle Cabanas Xeiruga Baldaio Niñons
Nemertea + + +
Polychaeta
Arenicola marina b + + +
Eteone longa c + + +
Glycera tridactyla c + +
Leptonereis glauca c +
Malacoceros fuliginosa s +
Nereis diversicolor c +
Nereis pelagica c +
Nereis spp. c + + +
Nephtys cirrosa c +
Ophelia bicornis b + +
Ophelia radiata b +
Ophelia sp. b +
Perinereis cultrifera o +
Phyllodoce laminosa c + +
Scololepis squamata s + + + + + +
Spiophanes bombyx s +
Spio filicornis s +
Mollusca
Calionymus maculatus o +
Cerastodema edule f + + +
Donax trunculus f + +
Tapes decussatus f +
Tellina tenuis s +
Venerupis rhomboides f +
Crustacea
Atylus guttatus s +
Bathyporeia pelagica s +
Caprella penanitis o +
Carcinus maenas c + +
Crangon crangon o +
Eurydice affinis c + + +
Eurydice pulchra c + + + + +
Gammarus locusta s +
Gammarus salinus s +
Gammarus sp. s +
Gastrosaccus spinifer o +
Haustorius arenarius s + +
Part VII Appendix
270
Taxa (continuation) Sheltered beaches Exposed beaches
Trophic group Broña Bornelle Cabanas Xeiruga Baldaio Niñons
Crustacea
Idotea baltica o +
Idotea emarginata o +
Idotea metallica o +
Idotea neglecta o + +
Idotea pelagica o + +
Isaea montagus o +
Lembos websteri s + Pontocrates
arenarius s + Sphaeroma
rugicauda o + +
Talitrus saltator o + + +
Talorchestia britto o + + + + + Talorchestia
deshayesii o + +
Tylos europaeus o + + + +
Urothoe elegans s +
Platyhelminthes o +
Insecta
Coleoptera spp. o + + +
Diptera spp. o +
Hymenoptera spp. o + +
Aranei o + +
Part VII Appendix
271
Appendix B. Summary of SIMPER analysis comparing sheltered and exposed
sandy beaches. δi: contribution of species i to the Bray-Curtis similarity matrix
between both groups of beaches. Σδi: accumulative percentange.
Average similarity: 41,03
Sheltered Average Exposed Average
Species abundance abundance δi(%) Σδi (%)
Talorchestia britto 2975.91 933.5 11.44 11.44
Idotea pelagica 5.55 1383.0 6.30 17.74
Talorchestia deshayesii 249.75 801.42 5.78 23.53
Tylos europaeus 906.87 79.92 5.34 28.87
Haustorius arenarius 175.38 0.00 4.37 33.24
Nemertea spp. 177.60 0.00 4.05 37.30
Eurydice affinis 0.00 101.01 3.85 41.15
Scololepis squamata 513.93 218.67 3.85 44.99
Ophelia bicornis 250.86 250.86 3.19 48.18
Nereis spp. 79.92 0.00 2.93 51.11
Malacoceros fuliginosa 103.53 0.00 2.86 53.97
Talitrus saltator 341.88 8.88 2.85 56.82
Glycera tridactyla 93.24 0.00 2.67 59.50
Cerastoderma edule 55.50 0.00 2.33 61.82
Arenicola marina 46.62 0.00 2.26 64.09
Crangon crangon 38.85 0.00 2.18 66.27
Gammarus locusta 36.63 0.00 1.96 68.23
Eteone longa 25.53 0.00 1.79 70.02
Eurydice pulchra 34.41 71.04 1.73 71.75
Gammarus salinus 26.64 0.00 1.59 73.34
Donax trunculus 29.97 0.00 1.57 74.91
Gammarus sp. 36.63 0.00 1.56 76.47
Idotea metallica 24.42 0.00 1.44 77.91
Angulus tenuis 22.20 0.00 1.32 80.64
Ophelia sp. 12.21 0.00 1.32 80.64
Nereis diversicolor 22.20 0.00 1.29 81.93
Idotea emarginata 25.53 0.00 1.28 83.21
Idotea neglecta 21.09 4.44 1.20 84.41
Carcinus maenas 7.77 0.00 1.07 85.48
Sphaeroma rugicauda 4.44 18.87 0.00 86.47
Perinereis cultrifera 7.77 0.00 0.98 87.45
Urothoe elegans 9.99 0.00 0.93 88.38
Spiophanes bombyx 5.55 0.00 0.83 89.21
Leptonereis glauca 6.66 0.00 0.80 90.01
Part VII Appendix
272
APPENDIX C Summary of SIMPER analysis comparing high and medium
and high and low tidal levels in sheltered sandy beaches.
Average dissimilarity: 97.04
High average abundance
Medium average abundance δi(%) Σδi (%)
Tylos europaeus 2713.95 0.00 8.23 8.23
Talorchestia britto 8904.42 3.33 7.94 16.18
Scololepis squamata 0.00 1521.81 7.63 23.81
Talitrus saltator 1015.65 0.00 7,21 31.02
Talorchestia deshayesii 742.59 0.00 6.88 37.90
Ophelia bicornis 0.00 702.63 6.83 44.73
Haustorius arenarius 0.00 276.39 5.86 50.58
Glycera tridactyla 0.00 239.76 5.71 56.29
Nereis spp. 0.00 116.55 4.96 61.26
Donax trunculus 0.00 69.93 4.44 65.70
Eurydice pulchra 0.00 46.62 4.02 69.72
Eteone longa 0.00 43.29 3.95 73.67
Cerastoderma edule 0.00 29.97 3.57 77.24
Crangon crangon 0.00 23.31 3.32 80.56
Ophelia sp. 0.00 16.65 2.99 83.55
Carcinus maenas 0.00 6.66 2.12 85.67
Sphaeroma rugicauda 0.00 6.66 2.12 87.79
Ophelia radiata 0.00 3.33 1.53 89.32
Spiophanes bombyx 0.00 3.33 1.53 90.84
Average dissimilarity: 98.07
High average abundance
Low average abundance δi(%) Σδi (%)
Talorchestia britto 8904.42 0.00 6.11 6.11
Malacoceros fuliginosa 0.00 3083.58 5.40 11.51
Talitrus saltator 1015.65 0.00 4.65 16.17
Talorchestia deshayesii 742.59 0.00 4.44 20.61
Tylos europaeus 2713.95 3.33 4.33 24.94
Haustorius arenarius 0.00 239.76 3.69 28.62
Cerastoderma edule 0.00 136.53 3.31 31.93
Arenicola marina 0.00 136.53 3.31 35.24
Nereis spp. 0.00 123.21 3.24 38.48
Gammarus sp. 0.00 109.89 3.16 41.65
Gammarus locusta 0.00 103.23 3.12 44.77
Crangon crangon 0.00 89.91 3.03 47.80
Gammarus salinus 0.00 76.59 2.92 50.73
Idotea emarginata 0.00 69.93 2.86 53.59
Nereis diversicolor 0.00 66.60 2.83 56.42
Idotea metallica 0.00 59.94 2.76 59.19
Idotea neglecta 0.00 49.95 2.64 61.83
Ophelia bicornis 0.00 46.62 2.60 64.43
Idotea baltica 0.00 36.63 2.44 66.86
Angulus tenuis 0.00 33.30 2.38 69.24
Part VII Appendix
273
Eteone longa 0.00 33.30 2.38 71.62
Glycera tridactyla 0.00 29.97 2.31 73.92
Urothoe elegans 0.00 26.64 2.23 76.15
Perinereis cultrifera 0.00 19.98 2.05 78.20
Donax trunculus 0.00 16.65 1.93 80.13
Leptonereis glauca 0.00 16.65 1.93 82.06
Carcinus maenas 0.00 16.65 1.93 83.99
Idotea pelagica 0.00 13.32 1.79 85.78
Spiophanes bombyx 0.00 9.99 1.61 87.39
Venerupis decussata 0.00 9.99 1.61 89.00
Phyllodoce laminosa 0.00 6.66 1.37 90.37
APPENDIX D. Summary of SIMPER analysis comparing high and medium
and high and low tidal levels in exposed sandy beaches.
Average dissimilarity: 52.81
High average abundance
Medium average abundance δi(%) Σδi (%)
Idotea pelagica 4145.85 0.00 21.62 21.62
Talorchestia deshayesii 2397.60 3.33 16.39 38.01
Scololepis squamata 0.00 143.19 12.90 50.91
Talorchestia britto 2770.56 29.97 11.66 62.58
Atylus guttatus 13.32 0.00 6.91 69.49
Talitrus saltator 13.32 0.00 6.91 76.39
Idotea neglecta 13.32 0.00 6.91 83.30
Sphaeroma rugicauda 53.28 3.33 6.56 89.86
Eurydice affinis 29.97 209.79 4.98 94.84
Average dissimilarity: 80.62
High average abundance
Low average abundance δi(%) Σδi (%)
Idotea pelagica 414.585 0.00 15.89 15.89
Talorchestia britto 2770.56 0.00 15.12 31.00
Talorchestia deshayesii 2397.60 0.00 14.84 45.85
Scololepis squamata 0.00 512.82 11.90 57.75
Tylos europaeus 93.24 0.00 8.67 66.42
Sphaeroma rugicauda 53.28 0.00 7.62 74.04
Atylus guttatus 13.32 0.00 5.08 79.11
Talitrus saltator 13.32 0.00 5.08 84.19
Idotea neglecta 13.32 0.00 5.08 89.27
Eurydice affinis 29.97 306.36 4.38 93.64
Part VII Appendix
274
T
rophic
January
A
pri
l
Ju
ly
Oct
ober
Speci
es
gro
up
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
Poly
cha
eta
Are
nic
ola
mari
na
b
- +
+
-
+
+
- +
+
-
+
+
Arici
ida
e in
det.
o
- -
- -
- -
- -
+
- -
+
Bocc
ard
ia s
p.
o
- -
- -
- -
- +
-
- -
-
Capite
lla c
apita
ta
b
+
+
+
- +
+
-
+
+
+
+
+
Cirra
tulid
ae in
det.
b
- -
+
- -
- -
- -
- -
-
Ete
one lo
nga
c
- +
+
-
+
+
- +
+
-
+
+
Gly
cera
tid
act
yla
c
- -
+
- +
+
-
+
- -
+
+
Hete
rom
ast
us
filifo
rmis
b
- -
- -
- -
- -
- -
- +
Lan
ice c
onch
ilega
s
- -
+
- -
+
- -
- -
- +
Mala
coce
ros
fulig
inosu
s s
- +
+
-
+
- -
+
- +
+
+
Nephty
s ca
eca
c
- -
- -
- +
-
- -
- -
-
Nephty
s h
om
berg
ii c
- -
+
- -
- -
- -
- +
-
Nephty
s in
cisa
c
- -
- -
- -
- -
+
- -
-
Nepth
ys s
p.
c -
- +
-
- +
-
+
+
- -
-
Nere
is d
ivers
icolo
r c
- +
+
-
+
+
- +
-
+
+
+
Nere
is s
p.
c -
- -
- +
-
- +
-
- -
-
Orb
iniid
ae in
det.
o
- +
+
-
- -
- -
+
- -
+
Pect
inari
a k
ore
ni
b
- -
+
- -
- -
- -
- -
-
Phyl
lod
oce
lam
inosa
c
- -
+
- -
+
- -
+
- +
+
Phyl
lod
oce
sp.
c -
- +
-
+
+
- -
+
- -
-
Pra
eg
eria
rem
ota
o
- -
- -
- -
- -
- -
- -
Pse
ud
opo
lydora
sp.
s -
+
- -
- -
- -
+
- +
+
PART IV: Chapter 5.
Appendix A. List of species collected in the estuarine beach sampled
(Barraña). Trophic group: suspension feeders: f; surface detritus feeders: s;
subsurface detritus feeders: b; carnivores: c; others: o (+ Presence).
HTL: high tidal level; MTL: medium tidal level; LTL: low tidal level.
Part VII Appendix
275
T
rophic
January
A
pri
l
July
O
cto
ber
Specie
s
gro
up
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
Pygospio
ele
gans
s
- +
-
- +
-
- +
+
+
+
-
Scolo
plo
s a
rmig
er
b
- -
- -
- +
-
- -
- -
-
Spio
filic
orn
is
s
- +
+
-
+
+
- +
+
-
+
+
Spio
phan
es b
om
byx
s
- +
-
- +
-
- -
- -
+
+
Str
eb
losp
io c
f. d
ekhuyzen
i s
- -
- -
- -
- -
- -
- -
Cru
sta
cea
Aori
dae in
det.
c
- +
-
- -
- -
- -
- -
+
Carc
inus m
aen
as
c
- +
-
- +
-
- +
+
-
- +
Cra
ngo
n c
rang
on
o
- +
-
- +
-
- +
+
-
+
-
Cope
pod
a inde
t.
o
-
+
- -
- -
- +
-
- -
Cum
acea inde
t.
o
- -
- -
- -
- +
+
-
- -
Cum
opsis
go
odsir
i o
- -
- -
- -
- +
+
-
- -
Cum
opsis
long
ipes
o
- -
- -
- -
- +
-
- -
-
Cyath
ura
cari
nata
s
- +
-
- +
-
- +
+
-
+
-
Eury
dic
e a
ffin
is
c
+
- -
- -
- -
- -
+
- -
Eury
dic
e n
aylo
ri
c
- -
- -
- -
- -
- -
- -
Gam
maru
s s
alinus
s
- +
+
-
- -
- +
-
+
- -
Gastr
osaccus s
anctu
s
o
- +
+
-
+
- -
+
+
- -
+
Hausto
rius a
ren
arius
s
- -
- -
- -
- -
+
- -
-
Hete
rota
na
is b
ers
tedi
o
- -
- -
- -
- -
+
- -
-
Hyale
sp.
c
- -
- -
- -
- +
+
-
- -
Idote
a m
eta
llic
a
o
- -
- -
- -
- -
- +
-
-
Idote
a n
egle
cta
o
- -
- -
- +
-
+
- -
- -
Iphin
oe
trisp
inosa
s
- -
- -
- -
- +
+
-
- -
Jassa falc
ata
o
- -
- -
- -
- -
+
- -
-
Mic
rode
uto
pus g
ryllo
talp
a
s
- -
- -
- -
- -
- -
+
+
Mysid
ae in
det.
o
- +
+
-
- +
-
- +
-
- -
Para
mysis
helleri
o
- +
-
- -
- -
+
- -
- -
Talitr
us s
alta
tor
o
+
- -
+
- -
+
- -
+
+
-
Part VII Appendix
276
T
rophic
January
A
pri
l
July
O
cto
ber
Specie
s
gro
up
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
HT
L
MT
L
LT
L
Talo
rchestia b
ritto
o
- -
- -
- -
+
- -
- -
-
Talo
rchestia d
eshayesii
o
+
- -
+
- +
+
-
+
+
+
+
Tylo
s e
uro
paeus
o
+
- -
- -
- -
- -
- -
-
Uro
thoe
pose
idonis
s
- -
+
- -
+
- -
- -
- +
Mollu
sca
Abra
tenu
is
s
- +
-
- -
- -
- -
- -
-
Ang
ulu
s ten
uis
s
- -
+
- -
+
- -
+
- -
-
Cera
sto
derm
a e
du
le
f -
+
+
- +
+
-
+
+
- +
+
Donax v
ari
ega
tus
f -
- -
- -
- -
- +
-
- -
Ensis
ensis
f
- -
+
- -
- -
- -
- -
-
Hydro
bia
ulv
ae
s
+
+
- -
+
- +
+
+
+
+
-
Lorip
es lucin
alis
s
- +
+
-
- +
-
- +
-
- +
Scro
bic
ula
ria p
lan
a
s
- +
+
-
+
- -
+
- -
+
-
Tapes d
ecussatu
s
f -
+
- -
- +
-
- -
- +
-
Telli
na te
nuis
s
- -
+
- -
- -
- -
- -
-
Telli
nacea
ind
et.
s
- +
+
-
- -
- -
- -
+
-
Ven
eru
pis
pu
llastr
a
f -
- -
- -
- -
+
- -
- -
Oth
ers
Insecta
inde
t o
+
- +
+
-
- +
-
- +
-
-
Cole
opte
ra larv
ae
o
+
- -
- -
- -
- -
+
- -
Dip
tera
larv
ae
o
+
- -
- -
- -
- -
- -
-
Nem
ert
ea ind
et.
c
- +
-
- +
-
- +
+
-
- +
Olig
ochaeta
inde
t.
o
+
+
+
+
+
- +
+
-
+
+
+
Part VII Appendix
277
Appendix B. Summary of SIMPER analysis comparing tidal levels from
Barraña. δi: contribution of species i to the Bray-Curtis similarity matrix
between both groups of beaches. Σδi: accumulative percentange. HTL: high
tide level; MTL: medium tide level; LTL: low tide level.
Average dissimilarity: 86.52
HTL Average abundance
MTL Average abundance δi(%) Σδi (%)
Capitella capitata 0.00 467.00 12.37 12.37
Hydrobia ulvae 2.00 706.00 10.99 23.36
Taorchestia deshayesii 77.00 0.00 8.76 32.12
Nereis diversicolor 0.00 75.00 8.71 40.84
Spio filicornis 0.00 49.00 7.87 48.71
Malacoceros fuliginosus 0.00 48.00 7.83 56.54
Talitrus saltator 26.00 0.00 6.63 63.17
Cerastoderma edule 0.00 13.00 5.31 68.48
Arenicola marina 0.00 10.00 4.82 73.30
Insect larvae 7.00 0.00 4.18 77.48
Eteone longa 0.00 6.00 3.91 81.40
Abra tenuis 0.00 3.00 2.79 84.19
Tellinacea indet. 0.00 2.79 2.79 89.76
Pygospio elegans 0.00 2.79 2.79 89.76
Aoridae indet. 0.00 3.00 2.79 92.55
Average dissimilarity: 86.93
HTL Average abundance
LTL Average abundance δi(%) Σδi (%)
Capitella capitata 0.00 115.00 11.56 11.56
Taorchestia deshayesii 77.00 0.00 10.60 22.16
Spio filicornis 0.00 70.00 10.37 32.53
Talitrus saltator 26.00 0.00 8.02 40.55
Urothoe poseidonis 0.00 24.00 7.83 48.38
Phyllodoce sp 0.00 20.00 7.41 55.79
Loripes lucinalis 0.00 17.00 7.03 62.82
Gastrosaccus sanctus 0.00 5.00 4.36 67.18
Bivalvia indet. 0.00 3.00 3.37 70.55
Insect (larvae) 7.00 1.00 3.37 73.92
Mysidae indet. 0.00 2.00 2.67 76.59
Hydrobia ulvae 2.00 0.00 2.67 79.27
Eteone longa 0.00 2.00 2.67 81.94
Lanice conchilega 0.00 2.00 2.67 84.61
Nephtys hombergii 0.00 2.00 2.67 87.28
Tylos europaeus 0.00 0.00 1.69 88.97
Insect 0.00 1.00 1.69 90.66
Part VII Appendix
278
Average dissimilarity: 66.23* Appendix B
(continuation) MTL Average abundance
LTL Average abundance δi(%) Σδi (%)
Hydrobia ulvae 706.00 0.00 13.01 13.01
Nereis diversicolor 75.00 0.00 8.59 21.60
Urothoe poseidonis 0.00 24.00 6.38 27.98
Malacoceros fuliginosus 48.00 1.00 6.34 34.32
Phyllodoce sp 0.00 20.00 6.04 40.36
Loripes lucinalis 0.00 17.00 5.73 46.09
Cerastoderma edule 13.00 0.00 5.23 51.32
Arenicola marina 10.00 0.00 4.75 56.07
Gastrosaccus sanctus 0.00 5.00 3.55 59.63
Capitella capitata 467.00 115.00 2.77 62.39
*Results from the main species with the highest dissimilarity.
Appendix C. Summary of SIMPER analysis comparing two years in Barraña.
δi: contribution of species i to the Bray-Curtis similarity matrix between both
groups of beaches. Σδi: accumulative percentange.
Average dissimilarity: 46.84*
1997 Average
abundance 1998 Average
abundance δi(%) Σδi (%)
Talitrus saltator 116.50 49.25 4.90 4.90
Malacoceros fuliginosus 69.00 3.00 4.57 9.47
Hydrobia ulvae 746.50 559.50 4.38 13.84
Oligochaeta indet. 45.50 15.50 3.90 17.74
Pygospio elegans 46.00 0.50 3.62 21.36
Talorchestia deshayesii 117.00 41.00 3.42 24.78
Urothoe poseidonis 20.50 3.75 2.43 27.21
Phyllodoce laminosa 0.00 4.50 2.21 29.42
Glycera tidactyla 5.50 0.25 2.16 31.59
Capitella capitata 947.25 461.00 2.08 33.67
Cerastoderma edule 14.50 95.25 1.98 35.65
Spio filicornis 53.25 161.50 1.92 37.57
Tapes decussatus 1.75 0.00 1.78 39.36
Decapod indet 14.25 0.00 1.78 41.13
Scrobicularia plana 14.50 3.00 1.77 42.90
Nephtys hombergii 10.25 0.25 1.76 44.66
Crangon crangon 0.25 2.00 1.73 46.39
Nereis diversicolor 64.25 24.75 1.69 48.09
Cyathura carinata 2.50 0.25 1.69 49.78
*Results from the main species with the highest dissimilarity.
Part VII Appendix
279
Appendix D. Environmental variables from January 97 to October 97. (HTL: high tidal level; MTL:medium tidal level; LTL: low tidal level).
Mea
n g
rain
siz
e (μ
m)
Sh
ea
r
st
re
ng
th
(
kP
a)
R
ed
ox
p
ot
en
ti
al
(
mV
)
Wa
te
r
co
nt
en
t
(%
)
Tem
per
ature
(ºC
)
De
pt
h
(c
m)
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
0
-5
3
40
.6
±1
0.
4
23
9.
7±
44
2
04
.5
±3
.9
3
.3
±0
.4
4
.5
±1
.3
5
.1
±1
.3
2
24
.7
±2
2.
2
57
.3
±4
3
40
±5
6.
6
21
.3
±0
.5
2
3±
1.
3
25
±0
.3
1
3.
3±
0.
1
12
.1
±0
.2
1
3.
2±
0.
2
5
-1
0.
3
38
.4
±1
2.
5
26
4.
7±
23
.8
1
98
.3
±4
.9
1
1.
3±
1.
7
6.
7±
1.
4
7.
5±
1.
4
22
6.
7±
17
.2
-
66
.3
±3
7.
2
-
15
8.
5±
40
2
0±
2
23
.5
±1
.7
2
5±
1
13
.2
±0
.1
1
2±
0.
1
12
.8
±0
.1
Ja
nu
ar
y
97
1
0-
15
.
34
4.
5±
34
3
11
.2
±4
8.
1
19
3.
2±
3.
8
17
.1
±1
.2
7
.8
±1
9
.9
±2
.1
2
31
.7
±1
9
-1
03
.7
±1
9
-2
09
.5
±8
1
8.
3±
1
24
±1
2
4±
0.
2
13
.1
±0
.1
1
1.
8±
0.
1
12
.7
±0
.1
1
5-
20
4
17
.4
±3
3.
3
34
6.
1±
28
.7
1
97
.3
±9
.8
2
0.
7±
0.
7
12
.9
±1
.4
1
3.
4±
1.
9
24
2.
5±
3.
5
-1
17
±1
0.
6
-
22
6±
15
.6
1
8.
3±
1
23
±1
.2
2
4±
0.
3
12
.9
±0
.2
1
1.
7±
0.
1
12
.5
±0
.1
2
0-
25
4
03
.1
±8
8
37
7.
7±
96
.5
2
19
.7
±1
5.
4
-
-
-
24
2±
4
-1
17
±1
0.
6
-
22
6±
15
.6
1
9.
2±
1
23
±1
.3
2
4.
7±
0.
5
-
-
-
0
-5
3
18
±1
3.
2
23
2.
7±
12
.3
2
11
.9
±6
.4
3
.2
±0
.6
4
.1
±0
.8
4
.6
±0
.5
1
78
±5
9
-
16
3.
5±
10
1
-
11
9±
15
1
21
±1
2
2±
1
24
±1
1
9.
3±
0.
1
16
.7
±0
.1
1
4.
4±
0.
2
5
-1
0.
3
28
±1
0
24
7.
8±
12
2
02
.4
±2
.8
5
.3
±1
.4
6
.2
±1
.2
1
1±
1.
4
21
1±
35
-
34
8±
12
4.
5
-4
15
±3
3
20
±0
2
2±
1
23
±0
.4
1
9.
9±
0.
1
16
.5
±0
.2
1
4.
3±
0.
1
Ap
ri
l
97
1
0-
15
.
34
6.
8±
5.
3
28
4.
7±
15
1
97
.7
±6
.2
1
0.
1±
2.
7
9.
9±
1.
5
16
±1
.5
2
26
±1
9
-
34
7±
21
2.
5
-
50
6±
43
.4
1
9+
0.
5
21
.6
±1
2
3±
0.
2
20
.2
±0
.3
1
6.
4±
0.
1
14
.5
±0
.1
1
5-
20
3
59
±2
3
39
.6
±3
0
20
5.
5±
8.
7
14
±2
1
3.
8±
1.
1
22
±2
.3
2
63
±1
8
-4
44
±1
13
-
53
0±
5
18
±0
.4
2
2±
1
23
±0
.5
1
9.
4±
0.
3
16
±0
.2
1
4.
7±
0.
1
2
0-
25
4
03
.6
±2
8.
7
40
7.
5±
58
.8
2
10
±7
.3
-
-
-
2
76
±2
0
-4
79
±7
7
-
53
2.
3±
14
1
8.
3±
0.
5
22
.4
±1
.2
2
3.
6±
0.
4
18
±0
.3
1
5.
7±
0.
1
14
.9
±0
.1
0
-5
3
68
.3
±1
2
21
7.
9±
10
.8
1
91
.2
±4
.2
2
.3
±1
3
.8
±0
.6
3
.4
±0
.7
1
86
.5
±5
9
-1
55
±1
01
-
12
5±
15
1
19
.2
±0
.3
2
2±
0.
7
24
±1
1
8.
6±
0.
3
15
.8
±0
.3
1
7.
9±
0.
2
5
-1
0.
3
66
.4
±1
3.
3
25
0.
2±
9.
7
18
8.
6±
3.
3
5.
9±
2
6.
5±
1.
5
8.
7±
1.
1
20
0±
35
-
36
5±
12
4.
5
-
39
4.
3±
33
1
8.
5±
0.
7
21
±1
.5
2
3±
0.
5
20
.1
±0
.6
1
5.
5±
0.
2
16
.8
±0
.2
Ju
ly
9
7
10
-1
5.
3
55
.8
±3
.1
2
59
.7
±1
6.
8
18
9.
4±
6
8.
5±
2.
8
9.
2±
1.
3
14
.3
±1
.8
2
37
.3
±1
9
-
33
0±
21
2.
5
-
53
1±
43
.4
1
8±
0.
8
22
±0
.3
2
4±
0.
2
21
.3
±0
.5
1
5.
4±
0.
2
16
.1
±0
.2
1
5-
20
3
98
±6
.6
3
17
.5
±1
8.
2
19
1.
5±
5
12
.2
±3
.1
1
2.
4±
1.
1
18
.1
±1
.7
2
50
±1
8
-4
66
±1
12
-
50
3.
5±
5
16
±0
.3
2
2±
0.
2
23
±1
2
1.
9±
0.
4
15
.7
±0
.2
1
5.
9±
0.
1
2
0-
25
4
03
.3
±3
7.
5
40
2.
4±
25
.7
2
22
±2
4.
7
-
-
-
28
9.
8±
20
-
45
5±
77
-
55
9±
13
.7
1
7.
7±
2
23
.5
±2
.2
2
3.
4±
5
22
.2
±0
.2
1
6±
0.
2
15
.9
±0
.1
0
-5
3
59
.4
±5
0.
1
23
8.
9±
14
.7
2
13
.4
±6
.3
3
.3
±0
.4
5
.2
±1
.1
3
.2
±1
.3
2
10
±1
3.
2
-1
76
±2
4
-2
82
.3
±7
2
0±
1.
5
21
.5
±1
2
1.
5±
1.
5
17
.3
±0
.2
1
7.
4±
0.
1
17
.6
±0
.1
5
-1
0.
3
34
.7
±2
2.
6
26
4.
9±
11
.6
2
21
.1
±5
.6
5
.7
±1
.6
8
.5
±1
.7
9
.3
±1
.3
2
05
±1
3.
2
-2
28
±1
1.
5
-0
5±
13
.2
1
9±
0.
5
21
±2
2
2±
2
17
.5
±0
.1
1
7.
4±
0.
1
17
.6
±0
.1
Oc
to
be
r
97
1
0-
15
.
40
2.
9±
50
.8
3
14
.4
±1
9.
5
22
0.
2±
5.
8
7.
3±
1.
5
11
±2
1
3.
5±
1.
7
22
2±
10
.4
-
23
2±
3
-
31
3.
3±
13
1
7±
0.
6
21
.4
±1
.5
2
2±
1
17
.5
±0
1
7.
5±
0.
1
17
.8
±0
.1
1
5-
20
3
66
.9
±1
7.
8
37
8.
5±
30
.3
2
38
.3
±1
4.
9
11
.7
±1
.8
1
2.
9±
2.
5
18
.1
±2
.1
2
28
±1
2.
6
-2
62
±3
3.
3
-
31
8.
3±
13
1
7.
4±
1
21
.5
±1
.2
2
2.
5±
1.
7
17
.6
±0
1
7.
5±
0.
1
17
.8
±0
.1
20
-2
5
41
3.
9±
60
.6
4
51
.8
±3
6.
7
26
2±
0.
1
-
-
-
22
5±
13
-
27
8.
3±
34
-
32
7±
3.
5
18
±1
2
2.
6±
1
22
±2
1
7.
6±
0
17
.6
±0
.1
1
7.
7±
0.
1
Part VII Appendix
280
Me
an
gra
in s
ize
(μ
m)
S
he
ar
s
tr
en
gt
h
(k
Pa
)
Re
do
x
po
te
nt
ia
l
(m
V)
W
at
er
c
on
te
nt
(
%)
T
em
pe
ratu
re (
ºC)
De
pt
h
(c
m)
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
H
TL
M
TL
L
TL
0
-5
4
08
.8
±1
1.
3
22
0.
6±
13
.3
2
14
.3
±1
.2
4
.9
±0
.5
2
.6
±1
1
.8
±0
.1
2
15
±7
.1
-
21
8±
9
-1
77
±5
1.
3
21
±0
.6
2
3±
1.
1
24
±0
1
0.
9±
0.
1
12
.7
±0
.3
1
3.
5±
0.
1
5
-1
0.
4
08
.7
±2
9
24
2.
4±
16
2
07
.7
±3
.5
7
.7
±0
.5
6
.1
±0
.6
5
.4
±0
.8
2
25
±7
.1
-
40
5±
30
.4
-
38
7±
15
.3
1
9±
0.
5
22
.5
±0
.2
4
24
±1
1
1.
3±
0.
1
13
±0
.2
1
3.
4±
0
Ja
nu
ar
y
98
1
0-
15
.
39
5.
1±
30
.5
2
60
.9
±1
2.
2
21
2.
7±
4.
2
8.
4±
0.
5
7±
0.
7
8±
1
22
0±
0
-4
51
±1
6.
5
-4
70
±0
1
9±
1.
1
22
±0
.5
2
3±
0.
4
11
.5
±0
.1
1
3.
1±
0.
2
13
.4
±0
1
5-
20
3
79
.4
±3
3
37
6.
8±
23
.1
2
07
±2
.8
8
.9
±0
.4
8
.3
±0
.6
1
0.
2±
1.
6
22
0±
0
-4
73
±1
5.
3
-5
12
.5
±1
1
19
±2
2
2±
1.
5
23
.5
±0
.2
1
1.
7±
0.
1
13
.1
±0
.1
1
3.
5±
0
2
0-
25
4
08
.1
±1
3.
7
34
0.
5±
68
.5
2
09
.1
±1
-
-
-
2
07
.5
±1
8
-4
70
±1
4
-5
30
±1
4
18
±1
.2
2
1.
5±
1
24
.1
±0
.5
1
1.
8±
0.
1
13
.1
±0
.1
1
3.
6±
0
0
-5
3
63
.5
±1
2
23
0.
7±
6
18
8.
7±
1
5±
1
4.
1±
0.
5
2.
9±
0.
5
16
3.
3±
21
-
24
3.
3±
55
-
85
±2
1
21
±0
.1
2
1±
1
24
.6
±2
1
5.
4±
0.
1
15
.5
±0
1
5.
7±
0.
1
5
-1
0.
3
68
.2
±4
0.
7
25
2±
11
.8
1
91
.1
±1
1
8.
6±
0.
5
7.
2±
0.
6
8.
5±
0.
6
14
3.
7±
31
-
36
0±
44
.4
-
16
5±
49
.5
1
9±
2
21
±1
2
4.
5±
4
15
.5
±0
.1
1
5.
6±
0
15
.7
±0
.1
Ap
ri
l
98
1
0-
15
.
35
2.
3±
19
.8
2
79
.8
±9
8.
1
19
5.
6±
13
.1
9
.8
±1
1
0.
1±
1.
7
10
.5
±0
.7
1
66
.7
±3
8
-4
17
±3
2
-2
85
±2
1
20
.5
±1
.1
2
1±
1.
2
23
±3
.6
1
5.
7±
0.
1
15
.6
±0
.1
1
5.
7±
0.
1
1
5-
20
3
29
.7
±1
3
43
4±
84
.5
1
86
.2
±8
.3
1
1.
3±
1.
7
11
.9
±1
.9
1
2.
4±
1.
8
16
6.
7±
46
.2
-
45
5±
38
-
36
7.
5±
81
1
9±
0.
3
20
.7
±1
.5
2
5.
5±
4.
6
15
.8
±0
1
5.
7±
0
15
.8
±0
.1
2
0-
25
3
98
.3
±2
7.
7
35
7.
3±
31
.4
2
19
.1
±3
6.
8
-
-
-
-
-4
77
±3
2.
1
-4
22
.5
±3
2
17
.4
±0
.4
2
0.
7±
3
25
.5
±3
-
1
5.
7±
0
15
.7
±0
0
-5
4
08
.7
±2
1.
7
24
9.
4±
11
.1
1
98
.4
±7
.4
4
±0
.4
3
.1
±0
.5
4
.2
±0
.7
2
20
±2
8
-1
48
.3
±5
0
-1
15
±3
5.
4
19
.4
±0
.3
2
2.
2±
0.
5
24
±0
1
6.
4±
0.
1
16
±0
.1
1
9.
8±
0.
3
5
-1
0.
3
83
.1
±2
1.
8
23
6±
2.
5
19
8.
2±
8.
8
11
.1
±1
.9
7
.2
±0
.9
9
.4
±2
.4
2
25
±2
1
-2
92
±9
4
-2
80
±7
1
18
±0
.6
2
1.
5±
1.
3
24
.3
±1
1
6.
8±
0.
1
15
.8
±0
.1
1
7.
9±
0
Ju
ly
9
8
10
-1
5.
3
80
.9
±1
2.
3
34
6.
2±
74
.2
1
92
.6
±2
.8
1
8.
9±
5.
8
11
.6
±1
.1
1
4.
1±
2.
7
22
5±
21
-
40
6.
3±
70
-
38
0±
42
.4
1
8±
0.
4
22
±1
2
3±
1
17
.3
±0
.1
1
5.
8±
0.
2
17
±0
1
5-
20
4
03
.4
±1
4.
3
52
4.
2±
18
5.
6
18
8±
2.
6
26
.6
±3
.8
1
2.
1±
1
18
.8
±3
.5
2
35
±7
-
45
8±
27
.5
-
46
5.
21
.2
1
7.
7±
1
20
.5
±1
2
2.
6±
1.
5
17
.8
±0
.1
1
5.
9±
0.
2
16
.5
±0
.1
2
0-
25
3
81
.9
±3
6.
7
44
1.
2±
19
.1
2
04
.7
±5
-
-
-
2
35
±1
4
-4
77
±2
5.
2
-4
90
±7
.1
1
7.
3±
1
21
±1
.3
2
3±
1
18
.3
±0
1
6±
0.
2
16
.2
±0
0
-5
3
35
.6
±2
.8
2
15
.4
±1
4.
1
18
8.
9±
2.
7
3.
7±
0.
6
4.
2±
0.
7
4.
3±
0.
3
21
7±
7.
6
-2
43
.3
±5
5
-9
5±
7.
1
17
.8
±1
.2
2
4±
1
24
±0
1
4±
0.
2
16
.2
±0
.2
1
7.
5±
0.
2
5
-1
0.
3
72
±1
3.
5
23
6.
6±
13
1
73
.3
±2
.6
7
.6
±1
.2
7
.8
±1
.6
9
.6
±0
.8
2
25
±5
-
36
0±
44
.4
-
30
1.
7±
69
1
8±
0.
5
23
.6
±2
2
4±
0.
3
14
.8
±0
.2
1
6.
4±
0.
1
17
.3
±0
.1
Oc
to
be
r
98
1
0-
15
.
35
8.
7±
8.
6
31
7.
4±
19
.1
1
79
.5
±6
.2
1
1.
7±
3
11
±1
.1
1
5.
6±
1.
6
22
5±
5
-4
17
±3
2
-3
87
±7
5
18
.4
±1
2
3±
2
24
±1
1
5.
2±
0.
2
16
.6
±0
.1
1
7.
3±
0
1
5-
20
3
70
.7
±3
2.
2
40
9.
7±
79
.3
1
85
.3
±1
1
9.
9±
4.
5
13
.5
±3
.2
1
6.
5±
1.
3
22
7±
6
-4
55
±3
8
-4
37
±5
8
17
.7
±0
.3
2
2±
1
24
.3
±1
1
5.
4±
0.
2
16
.8
±0
.1
1
7.
3±
0
2
0-
25
4
23
.1
±1
2
42
0.
4±
50
.3
3
91
.7
±7
8.
4
-
-
-
21
8±
16
-
47
7±
32
.1
-
46
3.
3±
38
1
7.
5±
1.
2
24
±5
+5
.3
2
4.
2±
0.
6
15
.6
±0
.1
1
6.
9±
0.
1
17
.4
±0
.1
0
-5
4
87
±5
5
24
6.
2±
25
2
26
±4
.5
6
.3
±0
.7
4
±0
.7
3
±0
.6
2
20
±9
-
37
.5
±1
0.
6
-4
67
±1
1.
5
20
±2
.2
2
1±
0.
5
24
±0
.5
1
1.
5±
0.
1
11
.8
±0
.1
1
2.
4±
0.
1
5
-1
0.
7
42
.6
±4
8.
7
24
2.
1±
3
23
4.
1±
20
1
6.
5±
1.
2
7.
8±
0.
6
7.
5±
1.
1
21
8±
7.
6
-1
73
.3
±2
9
-2
40
±3
6
18
.3
±1
.1
2
2±
1.
4
23
.2
±0
.5
1
1.
6±
0
11
.7
±0
.1
1
2.
4±
0
Ja
nu
ar
y
99
1
0-
15
.
35
6.
5±
55
2
76
.3
±2
1.
1
21
3.
1±
3.
4
17
.9
±1
.9
1
0.
5±
1.
7
14
±2
.5
2
02
±3
-
31
7±
25
.2
-
37
3.
3±
50
2
0±
1.
5
22
±1
2
3.
3±
0.
4
11
.7
±0
.1
1
1.
7±
0
12
.4
±0
.1
1
5-
20
3
63
.5
±6
8.
2
39
5.
8±
10
5.
6
22
4.
7±
19
.3
1
9.
9±
2.
3
13
.4
±2
.3
1
7.
7±
1.
6
20
3±
6
-3
67
±3
1
-4
53
±3
1
18
.1
±0
.3
2
2.
3±
1.
3
24
.2
±0
.5
1
1.
8±
0.
1
11
.7
±0
.1
1
2.
5±
0
2
0-
25
4
54
.9
±1
08
.5
4
89
.5
±4
9.
7
20
6.
3±
8.
2
-
-
-
21
0±
0
-3
80
±2
0
-4
95
±3
1.
2
17
.6
±1
.2
2
3±
1.
1
23
±1
1
1.
9±
0.
1
11
.8
±0
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1
2.
5±
0
Part VII Appendix
281
Appendix E. Relative contribution of the major macrobenthic groups to the individual densities at the three tidal levels sampled during the period of study. Values are presented as percentages of the respective total abundance [n: abundance (ind.m2) ± sd; number of species is presented in brackets] of three replicated samples per tidal level. A full circle being 100%.
n = 1210±338 n = 107±71n = 6533±979
Polychaetes
Crustaceans
Molluscs
Others
J97
Ap 97
O97
Ju97
J 98
A98
O98
Ju98
J99
n = 1655±463 n = 8402±1638 n = 765±267
HTLMTLLTL
n = 1673±481n = 12442±6693n = 7725±1602
n = 409±320n = 6764±1887n = 4130±1851
n = 125±71n = 11445±570n = 908±231
n = 1869±445n = 17124±4931n = 2563±463
n = 534±285n =6497±3880n = 5465±2314
n = 3168±1157n = 552±160
n =2261±587n = 4948±2955n = 534±338
n = 18±16
Part VI Appendix
282
Appendix F. Contribution of four major trophic groups in percentage of the total individual numbers at the three tidal levels from Barraña. (sb: subsurface deposit-feeder; s: surface deposit-feeder; sf: suspension feeder; c: carnivore; o: others). HTL: high tidal level; MTL: medium tidal level; LTL: low tidal level.
MTL
0
20
40
60
80
100
sb
s
c
o
sf
HTL
% f
ee
din
g t
yp
e
0
20
40
60
80
100
LTL
Ja97A97Ju97O97Ja98A98 J98 O98Ja99
0
20
40
60
80
100