macroalgae in the intertidal zone of cantabrian sea: richness, cover of characteristic and...

AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. 21: 7–16 (2011)

Published online 23 November 2010 in Wiley Online Library(wileyonlinelibrary.com). DOI: 10.1002/aqc.1157

Macroalgae in the intertidal zone of Cantabrian Sea: richness,cover of characteristic and opportunistic species

PILAR GARCIA, LUIS MIGUEL GUTIERREZ PESQUERAa and EVA ZAPICO REDONDO�

Institute of Natural Resources and Land Use Planning (INDUROT), University of Oviedo, C/Gonzalo Gutierrez Quiros s/n, 33600,

Asturias, Spain

ABSTRACT

1. Macroalgae are one of the biological parameters considered in the European Water Framework Directive(WFD) for establishing the ecological status of coastal water bodies. In order to test the metric used to assess thiselement in the Cantabrian coast, the quality of rocky bottoms (CFR) index was applied to 164 transects at 28sites on the coast of Asturias (northern Spain) in the summers of 2007 and 2008.2. At each sampling point, three variables were measured: species richness, cover of characteristic and opportunistic

macroalgae, and in 2008 the percentage of the area occupied by each characteristic species was also estimated.3. Application of the Shapiro–Wilk test to the variables ‘cover of characteristic macroalgae’ and ‘cover of

opportunistic algae’ revealed that the data were not normally distributed (Po0.001). A Kolmogorov–Smirnov testrevealed: (a) significant differences (Po0.01) between the exposed and semi-exposed sites, for the three variablesstudied; (b) significant differences in cover, for six species depending on the type of exposure; and (c) significantdifferences (Po0.01) in opportunistic macroalgal cover in relation to the two subtypes of water bodies in the studyarea. However, no significant differences were observed for overall macroalgal cover or species richness.4. According to the results obtained, new reference conditions and class boundaries are proposed for the

implementation of the CFR index in Asturian coastal waters. The ranges proposed for the CFR index in thepresent study provide better discrimination for evaluating the ecological status of the studied area.5. The results of SIMPER and MDS analyses reinforced the conclusion that the type of exposure and the

degree of human impact are the factors that best explain the degree of similarity between the sites sampled.Copyright r 2010 John Wiley & Sons, Ltd.

Received 21 January 2010; Revised 20 September 2010; Accepted 30 September 2010

KEY WORDS: Water Framework Directive; CFR index; macroalgae; ecological status; Cantabrian Sea

INTRODUCTION

Since the start of the implementation of the EU WaterFramework Directive (WFD) 2000/60/EC (European

Commission, 2000), there has been increased interest inmonitoring the composition and abundance of macroalgae(among other biological parameters) on European coasts.Different methods have been applied in several countries to

classify the status of their coastal waters: RSL (ReducedSpecies List) (Wells et al., 2007), EEI (Ecological EvaluationIndex) (Orfanidis et al., 2001, 2003), P-MarMAT (Portuguese

Marine Macroalgae Assessment Tool) (JRC, 2008), CARLIT(Cartography of Littoral areas) (Ballesteros et al., 2007) andCFR (Quality of Rocky Bottoms) (Juanes et al., 2008). The

latter index is being used to estimate water quality on the basis

of the status of macroalgae on the Spanish Atlantic coast.The initial version of the CFR comprised four indicators:

species richness, cover of characteristic macroalgae, cover of

opportunistic macroalgae and physiological status (Juaneset al., 2008). Later, in intercalibration exercises amongdifferent Spanish teams belonging to the North-east AtlanticGeographical Intercalibration Group (NEA GIG), it was

agreed to omit the physiological parameter as it wasconsidered a subjective measure and difficult to implement(Guinda et al., 2008; JRC, 2008).

The first approach did not take into account possibledifferences due to the geographical position (west–east) of thecoast. However, the exposure factor was considered in the

*Correspondence to: Eva Zapico Redondo, Institute of Natural Resources and Land Use Planning (INDUROT), University of Oviedo, C/GonzaloGutierrez Quiros s/n, 33600, Asturias, Spain. E-mail: [email protected]

Copyright r 2010 John Wiley & Sons, Ltd.

different scores for the observed values of richness and coverby characteristic macroalgae, but not for the opportunisticmacroalgae. This measure was designed to be applied to both

intertidal and subtidal communities, with different scoresdepending on the depth.

The Cantabrian coast (northern Spain) is included in the

warm-temperate area of the Atlantic region (Alvarez et al., 1988).Different studies carried out in the Bay of Biscay havedemonstrated the influence of geographical position (along the

west–east axis) on macroalgal composition and abundance(Anadon and Niell, 1981; Anadon, 1983; Arrontes, 1993). Suchvariations may be due to differences in natural conditions as aresult of differences in the topographical, geological or

geographical situation, or to changes induced by human pressures.The Iberian Poleward Current (IPC) (Frouin et al., 1990;

Haynes and Barton, 1990; Ambar and Fiuza, 1994) transports

subtropical waters that are warmer, more saline and poorer innutrients than the surrounding waters. This is a frequent event,particularly in winter (between November and February), and

varies in intensity from year to year (Llope, 2005). The IPCinvolves the formation of mesoscale structures (fronts), whichhave important biological implications, and also modifies the

hydrographic properties (thermohaline and nutrients) of thecore waters (Fernandez et al., 1993; Bode et al., 2002; Huskinet al., 2003; Isla and Anadon, 2004).

Another mesoscale phenomenon described in the area is

coastal upwelling (Botas et al., 1990; Llope, 2005). This has afertilizing effect on phytoplankton and encourages its growth.Upwelling events are frequent in summer, these are unequally

distributed in the Cantabrian Sea. The presence of Cape Penasenhances the effect of western winds and significantly increasestheir intensity. The distribution of the emerged water mainly

affects the western coast (as an extension of the Galicianupwelling system) and the process is less intense on the eastcoast. This differential distribution is of great ecological

significance. Cape Penas (Figure 1) has been considered as aboundary between the two subtypes of water bodies: NEA1/26a (North-east Atlantic without upwelling) and NEA1/26e(North-east Atlantic with weak upwelling) (JRC, 2008).

Another remarkable feature, which may affect macroalgae,is the existence of a thermal gradient along the coast in thesummer (Fischer-Piette, 1957; Koutsikopoulos et al., 1998;

Alcock, 2003). In the inner zone of the Bay of Biscay, thecontinental influence is more evident than at the western(Galician coast) and northern (Brittany coast) extremes. As a

result, the inner waters of the gulf warm up much more than atthe edges, thereby creating a spatial thermal gradient.

The coastline of Asturias (northern Spain) is more than600 km long (total length of Cantabrian coast is 2080 km) and

is surrounded by the Bay of Biscay.The most important human pressures in Asturias are

derived from specific sources of contamination (urban and

industrial sewage, ‘thermal dumping’, etc.). These havedecreased in recent years as the result of the installation ofseveral waste treatment plants, decreased levels of emission

through the modernization of production processes and theinstallation of emission systems designed to prevent the mostserious impacts. However, there remain some contamination

foci on the coast and in estuaries, with the most common beingdischarges of urban waste (from sewage treatment plants) andmost importantly, industrial waste. The largest and mostabundant emissions occur in the vicinity of the Aviles estuary

and at Abono (Figure 1), and to a lesser extent at the mouth of

the river Navia (Consejerıa de Medio Ambiente del Principadode Asturias, 2005, unpublished data). Such emissions mayaffect the state of macroalgae in the surrounding areas. Thedischarge of the most important Cantabrian river (Nalon

River) could also be a threat due its nutrients load and othercontaminants.

One of the aims of the WFD is to establish reference

conditions for biological parameters on the basis of the type ofwater body.

The effects of the variables: type of exposure and type

of water body (NEA1/26a and NEA 1/26e) over the threeindicators considered in the CFR index were investigated.Reference conditions were also determined from the data

available. Finally, the effects of anthropogenic pressures wereanalysed in relation to the results obtained.

METHODS

Sampling

Sampling was carried out in summer, in 2007 and 2008.The summer period is considered the most suitable forapplication of the CFR as it coincides with maximumdevelopment of most algal populations in temperate seas.

A total of 27 sampling points were included in the 2007 survey,and an additional point was included in 2008. The 28 samplingpoints were distributed along the coast (Figure 2). At each

point, three transects were established in accordance with themethod described by Juanes et al. (2008). Although the index isdesigned for application to intertidal and subtidal zones, in the

present study it was applied only to the intertidal zone,

Figure 1. Study area.

P. GARCIA ET AL.8

Copyright r 2010 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 21: 7–16 (2011)

including the fringe usually colonized by macroalgae, from themid-littoral to the infralittoral. In each transect, the following

variables were measured: species richness, cover ofcharacteristic macroalgae, and cover of opportunisticmacroalgae. In 2008, the percentage of the area of the

transect occupied by each characteristic species was alsoestimated visually. Characteristic macroalgae are understoodto be those perennial or late successional macroalgae that form

well defined conspicuous populations occupying more than1% of the area studied (Juanes et al., 2008).

The cover by characteristic macroalgae is expressed as a

percentage of the total area of the transect occupied by latesuccessional or perennial algae, whereas the cover byopportunistic species is a relative measure expressed as thepercentage occupied by such species (mainly green algae)

relative to the area occupied by characteristic macroalgae(Juanes et al., 2008). Both types of cover were independentlyestimated visually (in situ) by two experts. The mean value of

the two observations was calculated in order to reduce thesubjectivity factor. Richness was measured as the number ofcharacteristic macroalgae observed (not including invasive or

opportunistic species). Whenever possible, the transects wereorientated perpendicular to the coastline so that they includedthe entire intertidal area.

Data analysis

The field data obtained in each transect (species richness,cover by characteristic and by opportunistic macroalgae)

were stored in an SPSS file (version 15.0.1, 2006) (Perez,2001) along with additional information such as exposure ofthe transects, the type of water body to which they belong

(WFD) and the geographical position relative to Cape Penas(Figure 1).

The Shapiro–Wilk’s test for normality was applied to thecontinuous variables studied (cover by characteristic and

opportunistic macroalgae). This test was carried out withSPSS, and the graphs and summary statistics were obtainedwith the same program. Species richness is a discrete variable

and therefore the test for normality is not applicable.As the variables studied were not normally distributed,

non-parametric tests for comparing independent samples

were used.

To test for the existence of possible differences betweenvariables (species richness, cover by characteristic and

opportunistic macroalgae) in relation to the factor exposure,the Kolmogorov–Smirnov Z test was applied (as the criterionof normality required for use of the ANOVA test was not met),

also with SPSS.For the cover estimated in 2008, the mean values for the

three transects and each site were calculated and the data were

later included in the SPSS file. The Kolmogorov–Smirnov Ztest was used to analyse the difference between each variable(species) at each type of location (exposed/semi-exposed).

In addition, differences between the two types of coastalwater bodies NEA1/26a (North-east Atlantic withoutupwelling) and NEA1/26e (North-east Atlantic with slightupwelling) as regards the variables studied were determined by

use of the Kolmogorov–Smirnov Z test.The class boundaries proposed for the CFR index (Juanes

et al., 2008) were revised. Pearson’s correlation coefficients

were used to compare the final scores obtained with CFR andnew proposed limits, and Kendall’s Tau b was used forqualitative comparison of the ecological status.

A sample-variable matrix was constructed with the meanvalues of cover for each species found in the three transects ateach location in 2008. PRIMER computer software (Clarke and

Warwick, 1994) was used for hierarchical grouping of thelocations (cluster analysis) and multidimensional scaling (MDS)was applied, with Bray–Curtis distances on untransformed datato analyse the degree of similarity between the macroalgae

communities. Similarity percentage analysis (SIMPER) was usedto determine the contribution of each taxon to dissimilaritiesbetween groups obtained by cluster and MDS analysis.

RESULTS

Sample description

Analysis of the data obtained (from 164 transects) revealed thatthe mean cover of the characteristic macroalgae was 71% with a

standard deviation of 19%. In most of the sites studied themean cover of characteristic macroalgae was higher than 80%,but at a few it was very low. The mean of opportunistic

macroalgae cover was 8% with a standard deviation of 12%.

Figure 2. Location of the sampling sites (northern coast of Spain).

MACROALGAE IN THE INTERTIDAL ZONE OF CANTABRIAN SEA 9


The values for richness were high in comparison with those

established as reference conditions (JRC, 2008), with a meanrichness of 11 species. The species richness ranged between 2and 20. A total of 29 characteristic species of macroalgae were

found during sampling. Additional species were also identified(in total 62 taxa), including invasive species (Table 1).

Application of the Shapiro–Wilk test to the variables cover

by characteristic macroalgae and cover by opportunistic algaerevealed that the data were not normally distributed (Po0.001).

Analysis of the variables species richness, cover by

characteristic macroalgae and cover by opportunistic

macroalgae, in relation to exposure

Before establishing the reference conditions, possible

differences between exposed and semi-exposed sites wereexplored, as any such differences would justify the use ofdifferent reference conditions for each case. Such differences

were already assumed in elaboration of the CFR index (Juaneset al., 2008), but the analysis was carried out to confirm anydifferences in this particular case.

The results of the Kolmogorov–Smirnov test revealed

significant differences (Po0.01) between the exposed andsemi-exposed sites, for the three variables studied (Figure 3).Other descriptive statistics for the exposed and semi-exposed

sites are shown separately in Table 2.The values of the three variables were higher in the

semi-exposed areas than in the exposed areas: the mean

macroalgal cover in the semi-exposed areas was 72.54%,compared with 63.97% in the exposed areas. The differenceswere even greater when compared with the median values

(another measure of central tendency), found to be a goodindicator of reference conditions (REFCOND, 2003), withmedian values of 80.00 and 60.00, for semi-exposed andexposed sites, respectively. The mean species richness in the

semi-exposed sites was 12.09, compared with 8.69 for theexposed sites. The mean values for cover by opportunisticmacroalgae were generally low (less than 10% in both types of

areas) but nevertheless higher in the semi-exposed sites(9.40%) than in the exposed sites (1.97%). Most valuesoutside the range (Figure 3) correspond to those transects

with the worst biological status and in which opportunistic

species were abundant, probably as a result of anthropogenic

pressures.

Analysis of species composition in exposed and semi-exposed

areas

The differences in cover of the different characteristic specieswere also investigated separately for the two degrees ofexposure. The results of the Kolmogorov–Smirnov test

revealed significant differences in cover, for six species:Bifurcaria bifurcata (Po0.01), Caulacanthus ustulatus(Po0.01), Cladostephus spongiosus (Po0.01) Cystoseiratamariscifolia (Po0.01), Stypocaulon scoparium (Po0.01)

and Leathesia difformis (Po0.05) (Table 3).The species B. bifurcata, C. spongiosus, C. tamariscifolia,

S. scoparium and L. difformiswere more abundant in semi-exposed

areas than in exposed areas, and cover values were also higherin the semi-exposed areas. In contrast, the alga C. ustulatus wasmore abundant at the most exposed sites (Table 3).

No significant differences were found for the other speciesconsidered (Table 3), and cover by these species was similar inboth types of areas. Some of these species were equally abundantat both types of sites (semi-exposed/exposed): Codium spp.

(5.93/7.72%), Corallina officinalis (31.78/40.55%), Lithophyllumincrustans (25.71/39.77%), Gelidium corneum (3.13/1.55%) andGelidium pulchellum (3.60/5.05%). Other species were less

abundant or less common, such as for example: Codiumadhaerens (1.81/0%) and Nemalion helminthoides (1.73/2.33%).The low cover by species such as Pelvetia canaliculata and species

of the genus Fucus (less than 5%) was unexpected, as these speciesare traditionally considered to comprise the upper belt on shelteredcoasts (Anadon, 1983). During sampling these species were found

to be abundant at only a few locations such as Banugues (site 16),Castello (site 3) and San Lorenzo (site 19). At other locationswhere these species occurred, they were usually poorly developed,which made their identification to species level difficult.

Differences between water body subtypes NEA1/26a and

NEA1/26e

As also carried out for other biological parameters

(JRC, 2008), differences in opportunistic macroalgal cover

Table 1. List of species of macroalgae present in the intertidal zone

List of the main macroalgae found on the Asturian coast

Asparagopsis armata Codium adhaerens� Gigartina pistillata� Padina pavonicaAsperococcus sp. Codium spp.� Gracilaria multipartita Pelvetia canaliculata�

Bifurcaria bifurcata� Colpomenia peregrina Halurus equisetifolius Plocamium cartilagineumBryopsis plumosa�� Corallina elongata � Hildenbrandia rubra Plumaria elegansCalliblepharis ciliata Corallina officinalis L.� Himanthalia elongata Polysiphonia sp.Callithamnion sp. Cystoseira baccata� Laminaria ochroleuca� Porphyra umbilicalisCaulacanthus ustulatus� Cystoseira tamariscifolia� Laurencia hybrida� Pterocladiella capillaceaCeramium virgatum�� Dictyopteris membranacea Laurencia pinnatifida� Pterosiphonia complanataChaetomorpha aerea�� Dictyota dichotoma Leathesia difformis� Saccorhiza polyschides�

Champia parvula Eudesme virescens Liagora viscida Sargassum muticumChondracanthus teedi� Fucus spiralis� Lithophyllum byssoides� Sphaerococcus coronopifoliusChondracantus acicularis� Fucus vesiculosus� Lithophyllum incrustans� Stypocaulon scoparium�

Chondria coerulescens Gastroclonium ovatum Lomentaria articulata Taonia atomariaChondrus crispus� Gelidium latifolium� Mastocarpus stellatus� Ulva sp.��

Cladophora spp.�� Gelidium corneum� Nemalion helminthoides�

Cladostephus spongiosus� Gelidum pulchellum� Nitophyllum punctatum

�Species characteristic.��Opportunistic species, non-native/invasive species are underlined.

P. GARCIA ET AL.10


were investigated in relation to the two subtypes of waterbodies (NEA1/26a and NEA1/26e), and were found to besignificant (Po0.01) (Figure 3). The mean cover by

opportunistic species was 4.2% in subtype NEA1/26e incomparison with 11.5% in subtype NEA1/26a. However, nosignificant differences were observed for overall macroalgalcover or species richness.

Furthermore there were no significant differences in thecover by the main species found either side of Cape Penas.

Reference conditions

Given the existence of differences between exposed and semi-exposed areas as regards the variables studied, different

reference conditions (RC) are proposed for each. Althoughthere were also differences in the distribution of theopportunistic species in water body subtypes NEA1/26a and

NEA1/26e, when the 10th percentile was calculated andapplied in the analysis, the variations were found to be small(approximately 1%), and therefore reference conditions were

not established for this factor.Reference conditions can be established by the following

methods: (1) use of data from monitoring sites (to providespatially based reference conditions); (2) predictive modelling;

(3) use of either historical data, palaeo-reconstruction or acombination of both (to provide temporally based referenceconditions); (4) expert judgement; and (5) a combination of

the above approaches. The mean or median values from thedistribution of reference site values are considered themost robust values for use as the reference values in

classification of ecological status (relatively few data/sites arerequired for sufficient confidence in RC) (REFCOND, 2003).In light of the difficulty in finding sites that can be consideredpristine, and the lack of historical data, we opted to use

statistical modelling based on the best of our own data, toestablish the particular reference conditions, and selected the90th percentile for the cover by characteristic species and

Table 2. Descriptive statistics for the semi-exposed and exposed sites

Percentage coverby characteristicmacroalgae

Richness Percentage coverby opportunisticmacroalgae

Semi-exposed (N5 125)

Mean 72.54 12.09 9.40Standard error 1.74 0.30 1.13Standard deviation 19.47 3.34 12.6410ile 48.00 7.60 1.00

90ile 95.00 16.00 20.00

Exposed (N5 39)

Mean 63.97 8.69 1.97Standard error 2.41 0.65 1.09Standard deviation 15.05 4.06 6.8010ile 40.00 4.00 0.00

90ile 90.00 14.00 5.00

Figure 3. (A) Cover of characteristic macroalgae in semi-exposed and exposed areas; (B) cover of opportunistic macroalgae in semi-exposed andexposed areas; (C) species richness in semi-exposed and exposed areas; (D) comparison of cover by opportunistic macroalgae in NEA 1/26e

and NEA 1/26a.



richness, and the 10th percentile for cover by opportunisticspecies (Table 4).

These conditions differ considerably from those established

in the latest intercalibration report (JRC, 2008) for the entireCantabrian coast (Table 4), which indicates possibledifferences between the different regions. These referenceconditions proved too wide-ranging for the study area,

particularly as regards species richness, the value of whichwas below the 10th percentile for the semi-exposed areas(7.60).

Application of the CFR index

The results obtained from the application of the CFR index(Table 5) are different depending on the applied thresholds.The class boundaries proposed by Juanes et al. (2008) areshown in Table 6 while the thresholds proposed in the present

study are shown in Table 7. In both cases assignation of thebiological status was established from the scores listed inTable 8.

The ranges for the variables macroalgal cover and richness(Table 7) were established on the basis of the referenceconditions proposed in the present study, and deviations of

15% (very minor disturbance) were calculated for theHigh–Good status, of 30% (low levels of disturbance) forGood–Moderate status, 60% (intermediate level of

disturbance) for Moderate–Poor status, and 80% (severedisturbance) for Poor–Bad status, as outlined in Annex V ofthe WFD.

Although differences in the cover by opportunistic species

depended on the degree of exposure, the reference conditionswere very similar (Table 4) and therefore we used the sameranges in both cases. For the ranges of cover by opportunistic

species, the suggestions made by Scanlan et al. (2007) weretaken into account.

In general the ecological status scores obtained by

considering the proposed reference conditions were lowerthan the scores obtained with the reference conditionsproposed by Juanes et al. (2008). In both cases, intermediate

correlations were obtained: Pearson’s coefficient, R2 5 0.56(Po0.01); Kendall’s Tau b5 0.428 (Po0.01) (Figure 4).

With the reference conditions proposed by Juanes et al.(2008) the values of the index for the study areas ranged

between 50 and 100; with the reference conditions proposed inthe present study, the values ranged between 33 and 98, thusproviding better discrimination of the ecological status. Thus

with the previously proposed reference conditions, 26 of the 27sites were classified as of High ecological status in 2007, and 24of 28 sites in 2008. With the thresholds proposed in the present

study, the corresponding numbers were 12 in 2007 and 9 in2008; the most frequent ecological status was Good (14 in 2007and 17 in 2008). The number of sites that achieved Moderateecological status also increased.

The final scores show mean differences higher than 15 pointsin 9 of the 28 studied sites depending on the class boundariesapplied. Some of these sites are in water bodies influenced by

river discharge or industrial pressures (Sites 4 and 5 on theNavia coast; 11 and 12 on the Nalon coast; 15 on the Avilescoast and 24, very close to the Ribadesella coast). Furthermore,

site 18 is 2 km away from the mouth of the Abono River,subject to one of the most significant industrial pressures in thearea studied. The differences between final scores are higher in

those sites inside water bodies under significant pressures and atthese sites the final score is lower when class boundaries asproposed in this study are used instead of the class boundariesproposed by Juanes et al. (2008).

Cluster analysis and multidimensional scaling (MDS)

The cluster analysis grouped the samples into seven differentgroups for a level of similarity of 50%, of which threewere significant (a5 0.05). The three significant groups are

shown: a group comprising only one site (site 3), a group

Table 3. Average cover of characteristic and opportunistic macroalgae(underline) in the two environments studied (exposed and semi-exposed),and results of the Kolmogorov–Smirnov test

Species Semi-exposed

Exposed Z Kolmogorov–Smirnov

P

Bifurcaria bifurcata 18.48 0.22 1.78 0.004��

Caulacanthus ustulatus 1.42 10.27 1.78 0.004��

Cladostephus spongiosus 5.68 0.00 1.87 0.002��

Cystoseira tmariscifolia 2.51 0.00 1.58 0.014�

Stypocaulon scoparium 5.41 0.05 1.68 0.007��

Leathesia difformis 5.30 1.11 1.51 0.021�

Chondria coerulescens 0.49 2.22 1.32 0.063Chondrus crispus 2.46 5.00 0.69 0.726Codium adhaerens 1.81 0.00 0.69 0.726Codium spp. 5.93 7.72 0.69 0.726Colpomenia peregrina 0.04 0.00 0.20 1.000Corallina officinalis 31.78 40.55 0.79 0.56Dictyopterismembranacea

0.10 0.00 0.59 0.874

Dictyota dichotoma 0.18 0.05 0.23 1.000Fucus spp. 5.07 0.05 1.18 0.121Gelidium corneum 3.13 1.55 0.30 1.000Gelidium pulchellum 3.60 5.05 1.18 0.121Chondracanthusacicularis

0.22 0.00 0.59 0.874

Halurus equisetifolius 0.01 0.55 0.36 0.999Hildenbrandia rubra 2.74 2.27 0.30 1.000Laurencia hybrida 0.69 0.00 0.49 0.968Laurencia pinnatifida 0.27 0.88 0.53 0.945Liagora viscida 0.10 0.05 0.20 1.000Lithophyllum incrustans 25.71 39.77 1.09 0.189Lithophyllum byssoides 10.13 12.11 0.69 0.726Mastocarpus stellatus 0.13 1.39 0.62 0.829Nemalion helminthoides 1.73 2.33 0.36 0.999Pelvetia canaliculata 0.16 0.00 0.20 1.000Plocamium cartilagineum 0.84 0.55 0.26 1.000Pterocladia capillacea 0.48 3.66 0.53 0.945Ralfsia verrucosa 1.93 8.94 1.05 0.218Ulva spp. 9.09 3.88 1.35 0.0531

�Significant results Po0.05.��Highly significant Po0.01.1Result almost significant PE0.05.

Table 4. (1) Previously established reference conditions (RC) (JRC,2008), and (2) reference conditions calculated from data obtained inthe present study

Indicators (1) (2)

RC semi-exposed

RCexposed

Cover by characteristic macroalgae (%) 70 95 90Population richness (N) 6 16 14Relative cover by opportunistic species (%) 9 1 0

P. GARCIA ET AL.12


formed by 13 sites (13–28), and a group formed by eight sites

(15–25) (Figure 5).There does not appear to be any longitudinal geographical

gradient that determines the grouping of the study sites or theirdistribution in the results of the MDS analysis. Neither the

geographical position relative to Cape Penas nor classificationin one of the two water body subtypes (NEA 1/26a, NEA1/26e) appears to explain the grouping of the sites.

Table 5. Results of applying the CFR index to the central shores in the study area: (1) results obtained with the original ranges proposed by Juanes et al.(2008); (2) results obtained by application of the ranges proposed in the present study; (3) mean differences between scores obtained with 1 and 2

Beach (1) (2) (1) (2) (1) (2) (1) (2) (3)2007 2007 2008 2008 2007 2007 2008 2008

Punta de la Cruz — — High High — — 100 90 10.0Mexota High High High High 100 98 100 93 4.5Castello High Good High High 90 78 90 85 8.5Arnelles High Good High Good 93 63 100 65 32.5Del Moro High Good High Good 97 63 98 68 32.0Fabal High High High Good 97 93 90 78 8.0La Escaladina High High High Good 100 92 93 78 11.5Quintana High High High High 97 97 97 83 7.0La Gairua High High High Good 100 93 97 80 12.0Las Llanas High High High Good 93 85 87 65 15.0La Guardada High Good High Good 90 73 93 78 16.0Sablon de Bayas High Good High Good 100 68 97 67 31.0Bainas High Good High High 93 75 100 97 10.5Arnao High High High Good 100 90 83 73 10.0El Cuerno High Good High Good 88 58 97 67 30.0Banugues High Good High Good 83 77 87 67 13.0Les Huelgues High Good High High 90 77 100 95 9.0El Tranqueru Good Moderate Good Moderate 67 45 70 55 18.5San Lorenzo High High Good Good 93 90 82 63 11.0El Rinconın High Good High High 87 78 97 82 12.0La Griega High Good Good Good 83 77 75 63 9.0El Viso High Good High Good 93 80 90 70 16.5Punta del Pozo High High Moderate Moderate 100 87 50 33 15.0La Atalaya High Good High Good 97 78 93 77 17.5La Huelga High High High High 100 82 100 92 13.0Valle/Sevalle High High High High 93 85 100 97 5.5Vidiago High Good High Good 87 68 87 72 17.0El Vivero High High High Good 88 83 87 72 10.0

Table 6. Class boundaries and scores assigned in Juanes et al. (2008) for application of the CFR index

Cover by characteristic macroalgae Species richness Cover by opportunistic macroalgae

Score Int. Semi-exp. Int. Exposed Score Int. Semi-exp. Int. Exposed Score Intertidal

45 70–100% 50–100% 20 45 43 35 o10%35 40–69% 30–49% 15 4–5 3 25 10–19%20 20–39% 10–29% 10 2–3 2 15 20–29%10 10–19% 5–9% 5 1 1 5 30–69%0 o10% o5% 0 0 0 0 70–100%

Table 7. Class boundaries and scores according to the current proposal

Biological status Cover by characteristic macroalgae Richness Cover by opportunistic macroalgae�

Score Int. Semi-exp. Int. Exposed Score Int. Semi-exp. Int. Exposed Score Intertidal

High (�15% RefCond) 45 480% 475% 20 X14 X12 35 o5%Good (�30% RefCond) 35 80–6% 75–60% 15 13–10 11–8 25 5–15%Moderate (�60% RefCond) 20 64–40% 59–35% 10 9–6 7–5 15 16–25%Poor (�80% RefCond) 10 39–20% 34–20% 5 5–3 4–3 5 26–75%Bad (4�80% RefCond) 0 o20% o20% 0 o3 o3 0 475%

�Ranges proposed by Scanlan et al. (2007).

Table 8. Ranges for the establishment of ecological status based on thefinal score of the CFR

Final score (addition of three indicators) Ecological status

81–100 High57–80 Good33–56 Moderate9–32 Poor0–8 Bad



Groups [13–28] and [15–25], designated S and E in theMDS graph (Figure 5) include most of the sites studied andcorrespond to semi-exposed (S) and exposed (E) sites. Site 2 is

the only semi-exposed site included in group E. As alreadydemonstrated, exposure is one of the factors that determinesthe macroalgal composition at the sites studied, as well asthe variables richness and cover by characteristic and

opportunistic macroalgae.The sites that appear separated from the others display

certain peculiarities: site 3 is a semi-exposed site with

an abundant presence of Fucus (Figure 6). As corroboratedin the SIMPER analysis (similarity percentages – speciescontributions one-way analysis), Fucus spp. is the taxon that

accounts for most of the differences between this site and theothers (21.16% dissimilarity from group S and 22.24%dissimilarity from group E).

In some transects at sites 18, 19, 21 and 23 (Figure 5), excludedfrom the two main groups, a high cover by opportunistic specieswas observed. Sites 18 and 23 correspond with the worstbiological status.

Site 23 is a semi-exposed site with a high presence ofopportunistic macroalgae (35%) and low overall cover (59%)and consequently the genera Corallina and Ulva (Figure 6)

account for most of the differences from groups S and E (23.3and 17.92% dissimilarity, respectively, for Corallina; 21.09 and16.71 for Ulva).

At site 19, a semi-exposed site, Fucus spp. is wellrepresented (40%), but unlike at site 3, opportunistic speciesare also abundant (22%). In comparison with the sites in

groups S and E, at site 19 there was less cover by Corallina(8.33%).

The groups formed by sites (18, 21) and (11,16) differfundamentally from groups S and E in the lower cover by

Corallina and Bifurcaria (Figure 6), whereas the taxa thatbest explain the differences between these two groups areStypocaulon scoparium (10.20% dissimilarity) and the

opportunist Ulva (10.03%), which were most abundant atsites 18 and 21.

DISCUSSION

The biological status of most of the sites with respect tomacroalgae is Good, fulfilling the environmental objectives ofthe WFD. These results are consistent with those obtained

for other biological parameters analysed, such as physico-chemical (Garcia et al., 2010) phytoplankton and benthicmacroinvertebrates (INDUROT, 2009 – Unpublished data).

In general, high values were obtained for cover and richness,and only a few sites were classified as of Moderate ecologicalstatus, generally due to a lower degree of overall cover bymacroalgae in some of the transects and a higher presence of

opportunistic species such as at sites 18 and 23 (Figure 6).According to the WFD, a programme of corrective

measures must be presented by 2015, for water bodies with

less than Good status. Site 18 (Tranqueru beach) is close to thebusy port of Musel (Gijon), and to the mouth of the riverAbono (Figure 1), and is a site of industrial and ‘thermal’

dumping. Site 23 (Punta el Pozu), close to the mouth of theRibadesella estuary (Figure 1), is also subjected to a range ofcontaminants, mainly sewage discharges. Although these sitesare affected to a certain degree by anthropogenic pressures,

it is difficult to attribute the results obtained exclusively tothese pressures, as many of the sites in the central zone arerecreational beaches close to highly populated areas, and are

classified as of Good or High ecological status, without anyapparent negative effects on the macroalgae communities.The characteristics of the coastline under study, i.e. steeply

sloping shelf, high degree of exposure and short residence time,probably favour dissipation of the effects of human pressures.

There were differences between exposed and semi-exposed

sites as regards application of the CFR index. In addition toaffecting the results for overall cover and number of speciespresent, already taken into account in the index, the exposurealso affected the cover by opportunistic species. The lower

exposure to waves in semi-exposed areas favoured settlementof macroalgae. The cover and richness data were thereforehigher in sheltered areas. In contrast, in exposed areas, the

values of these variables were lower (Wells, 2006). However,the most exposed conditions also hampered proliferation ofopportunistic species. Given that the differences in the 10th

percentile are small for cover by opportunistic species,

Figure 4. Linear regression of the mean scores obtained for the twoCFR indices. CFR_1 values were obtained with ranges proposed byJunes et al. (2008), CFR_2 values were obtained with the ranges

proposed in the present study.

Figure 5. MDS ordenation plot. ‘S’ indicates the semi-exposed sitesand ‘E’ the exposed sites. The contours around the groups identified in

the cluster analysis (50% similarity).

P. GARCIA ET AL.14


establishment of similar ecological quality ratios (EQR) forboth types of coast may be acceptable. The ranges proposed byScanlan et al. (2007) appear to be more closely related to the

conditions of the study area (with only 1% of opportunisticspecies considered as reference conditions) particularly for thehigher status classes, and were therefore used for assessment of

opportunistic macroalgae.Despite the oceanographic differences between the two

types of water body and the different floristic composition

described by other authors (Anadon and Niell, 1981), therewere no significant differences between subtypes NEA1/26aand NEA1/26e as regards the overall cover by characteristic

species, or species richness, although opportunistic specieswere more abundant in NEA1/26e waters. We opted not to usedifferent reference conditions for the two types of water body.In the case of the opportunistic species, the differences were

very small for the metric used (10th percentile), therefore theestablishment of similar EQR for both types of water bodiescould be acceptable.

The cover by each species also did not differ in the twowater body types. It is likely that the cover has altered in recentyears, given the clear decrease in the abundance of some

species of Boreo-Atlantic distribution, such as the generaFucus (Figure 6), Pelvetia canaliculata and Himanthaliaelongata, as well as the disappearance of the genera

Laminaria and Saccorhiza from the intertidal zone. This isconsistent with the predictions made by Alcock (2003) asregards the gradual decrease in the area of distribution of theFucacea in the Bay of Biscay.

The results of the cluster analysis and MDS reinforced theconclusion that the type of exposure and the degree of humanimpact – and not the geographical west–east gradient – are the

factors that best explain the degree of similarity between thesites sampled. There was a clear separation between exposedand semi-exposed sites, groups E and S, respectively, in Figure 5

and other sites (with the exception of site 3), where lowercover by Corallina (Figure 6) and greater abundance of thegenus Ulva (Figure 6) were detected. According to Orfanidis

et al. (2001, 2003) and Littler and Littler (1984), and consideringthat Corallina is representative of late successional stages, thedisappearance of the latter, along with the abundant presence of

opportunistic species would classify these sites as of worseecological status than the other sites, probably as a result of theaction of some type of human pressure (eutrophication is themain cause known in the case of opportunistic species).

The reference conditions proposed for the CFR index in theeastern zone of the Bay of Biscay, and the ranges (Juanes et al.,2008) appear to be too wide for application to the coastal areas

in the central Bay of Biscay; this may be due to the east–westdifferences already mentioned, and therefore new referenceconditions and ranges were established for classification of the

ecological status of these areas. The ranges proposed for theCFR index in the present study provide better discriminationfor evaluating the ecological status of a site. Acceptance of the

results obtained with the original ranges would lead toclassification of all sites studied as pristine or almost pristine,including sites that are clearly affected by human pressures, asidentified by the application of the new ranges and thresholds.

Figure 6. Abundance of populations in the studied transects for different species: (A) Fucus spp.; (B) Ulva spp.; (C) Bifurcaria bifurcata;(D) Corallina sp.



ACKNOWLEDGEMENTS

This study was financed by the Consejerıa de Medio AmbienteOrdenacion del Territorio e Infraestructuras del Gobiernodel Principado de Asturias. We are grateful to staff fromINDUROT who participated in the collection and handling of

field data: Eneko Aierbe, Cristina Amez, Carlos Guardado andJuan Rodrıguez. We also thank Dr Ana Colubi for resolvingour doubts about the statistical treatment of the data.

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