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LONG-TERM MONITORING OF COASTAL ECOSYSTEMS 143

Revista Chilena de Historia Natural 83: 143-157, 2010 © Sociedad de Biología de Chile

SPECIAL FEATURE: LONG-TERM RESEARCH

REVISTA CHILENA DE HISTORIA NATURAL

Long-term monitoring of coastal ecosystems at Las Cruces, Chile:Defining baselines to build ecological literacy in a world of change

Monitoreo de largo plazo en el ecosistema marino costero de Las Cruces, Chile: Defi-niendo líneas base para construir alfabetización ecológica en un mundo que cambia

SERGIO A. NAVARRETE*, STEFAN GELCICH & JUAN C. CASTILLA

Estación Costera de Investigaciones Marinas, Center for Advanced Studies in Ecology and Biodiversity, & LaboratorioInternacional de Cambio Global (LINCGlobal, CSIC-PUC) Pontificia Universidad Católica de Chile, Casilla 114-D,

Santiago, Chile* Corresponding author: [email protected]

ABSTRACT

Marine coastal habitats are being increasingly impacted by human activities. In addition, there are dramaticclimatic disruptions that could generate important and irreversible shifts in coastal ecosystems. Long-termmonitoring plays a fundamental and irreplaceable role to establish general baselines from which we canbetter address current and future impacts and distinguish between natural and anthropogenic changes andfluctuations. Here we highlight how over 25 years of monitoring the coastal marine ecosystem within the no-take marine protected area of Las Cruces has provided critical information to understand ecologicalbaselines and build the necessary ecological literacy for marine management and conservation. We arguethat this understanding can only be gained with simultaneous monitoring of reserves and human-impactedareas, and the development of complementary experimental studies that test alternative hypothesis aboutdriving processes and mechanisms. In this contribution we selected four examples to illustrate long-termtemporal fluctuations at all trophic levels including taxa from algae to sea birds. From these examples wedraw a few general lessons: a) there is co-occurrence of rapid- and slowly- unfolding ecological responses tothe exclusion of humans within the same rocky shore community. The sharp differences in the pace at whichdepleted populations recover is at least partly related to differences in life history (dispersal capabilities) ofthe targeted species. b) Long-term monitoring of the supply-side of marine communities is critical to evaluatethe potential feedback effects of local changes in abundance into the arrival of new individuals and tocorrectly evaluate environmental and human-induced perturbations. c) Unexpected changes in localpopulation dynamics can occur in “independent” and apparently non-interactive modules of the marineecosystem, such as roosting sea birds inside the reserve. In addition we discuss the way in which ecologicaldata generated from long-term monitoring at marine reserves was institutionalized in a national marinemanagement policy. At the same time, we highlight the mismatch between the gained scientific informationand principles from these studies and the current concept of marine protected areas that is beingimplemented by some government agencies in Chile. Information from long term monitoring programs hasproved essential to understand how marine environments respond to anthropogenic and/or naturaldisturbances, however funding these schemes, which generally have no short term gains for fundingagencies in both developing and developed countries, still remain a major challenge.

Key words: community structure, conservation, keystone species, marine reserves, policy.

RESUMEN

Los ambientes marinos costeros están siendo impactados en forma creciente por las actividades humanas.Además, perturbaciones asociadas a cambios climáticos pueden producir cambios dramáticos e irreversiblesen estos ecosistemas. El monitoreo de largo plazo juega un rol fundamental e irremplazable para establecerlíneas-base sobre las cuales podemos establecer impactos actuales y futuros y distinguir entre cambiosantropogénicos y fluctuaciones naturales. En este estudio resaltamos cómo el monitoreo de más de 25 añosen la reserva marina costera no extractiva de Las Cruces ha entregado información crítica sobre líneas-basesecológicas y ha ayudado a comprender ecosistemas costeros para su manejo y conservación. Planteamos queeste conocimiento solo puede ser adquirido a través del monitoreo simultáneo en zonas de reservas y enzonas impactadas por el humano (de libre acceso), en conjunto con estudios experimentalescomplementarios para poner a prueba hipótesis acerca de los procesos y mecanismos que subyacen a lospatrones observados. En este artículo seleccionamos cuatro ejemplos para ilustrar patrones temporales de

144 NAVARRETE ET AL.

largo plazo en todos los niveles tróficos, incluyendo taxa que van desde las macroalgas a las aves marinas.De estas experiencias surgen algunas lecciones generales: a) existe una coocurrencia de respuestasecológicas rápidas y lentas frente a la exclusión de humanos en la misma comunidad costera rocosa. Lasmarcadas diferencias entre las tasas de recuperación de poblaciones afectadas son al menos en partedependientes de las historias de vida (capacidad de dispersión) de estas. b) El monitoreo de largo plazo del“abastecimiento” de nuevos individuos (reclutamiento) en comunidades marinas es crítico para evaluar lapotencial retroalimentación de cambios en abundancia local sobre la llegada de nuevos individuos y de estaforma evaluar correctamente perturbaciones ambientales o antrópicas. c) Cambios inesperados en dinámicaspoblacionales pueden ocurrir en módulos aparentemente independientes del ecosistema litoral, como lo sonlas aves marinas que descansan o anidan al interior de la reserva. Adicionalmente, discutimos la forma en lacual datos ecológicos generados a partir de monitoreos de largo plazo fueron institucionalizados en unartículo de la ley de pesca y acuicultura. Al mismo tiempo resaltamos el desfase entre el conocimientoadquirido de los estudios de largo plazo en reservas marinas e instrumentos de conservación marinaimplementados por algunas agencias de gobierno en Chile. Concluimos señalando que la informaciónproveniente de monitoreos de largo plazo ha resultado esencial para comprender cómo los ambientesmarinos responden a disturbios naturales o antropogénicos, sin embargo el financiamiento de estosprogramas, que generalmente no tienen grandes ganancias en el corto plazo para las agencias definanciamiento, continúa siendo un gran desafío tanto en países desarrollados como los en vías de desarrollo.

Palabras clave: conservación, especies clave, estructura comunitaria, legislación, reservas marinas.

INTRODUCTION

One of the important scientific questions todayis not whether marine coastal ecosystems havebeen profoundly transformed by humans overthe past hundreds of years, but whether wecan understand how they have changed, whatcomponents and features have experiencedirreversible changes, and how we use scientificknowledge to go from here and minimize pastand future losses.

The notion of a bountiful ocean withendless buffer capacity that many of us learnedof in high school is long gone. Today, policymakers and resource managers are forced toset targets for conservation and managementexercising the “short-term memory” approach,which in a world of slowly but ever slidingbaselines (Pauly 1995, Dayton et al. 1998,Jackson et al. 2001, Myers & Worm 2003)makes us feel more optimistic about the stateof coastal ecosystems and the success ofconservation and management practices. Thisis an admittedly bleak scenario; one that somemarine ecologists might not agree with. Yet,we argue that if we are to provide usefulecological information about conservation,management and biotic responses to climaticdisruptions, it is better to face the fact thatmarine ecosystems, from the intertidal zonedown to the abyssal ocean, are likely verydifferent to the ones before Homo sapiens (L.)developed the first tools and used the coastalocean for subsistence. This realization posesmonumental challenges when we try to

identify the benchmarks against which naturaland anthropogenic changes must be discernedand quantified (Dayton et al. 1998). In thisthorny and often polemic endeavor (e.g. Wormet al. 2006, Jaenike 2007, Murawski et al. 2007,Worm et al. 2007), long-term monitoring ofecosystems plays a fundamental andirreplaceable role.

Long-term data on physical or biologicalecosystem-state variables of marine coastalhabitats along the southeastern Pacific arescarce at best. Beyond the obvious limitationsto undertake long-term studies imposed bygranting agencies, which typically support 2-4yr long projects, and the increasingly stringentrequirements for short PhD dissertations (Dye1998b), it appears that other issues have alsoplayed a role in the scarce interest paid bymarine ecologists (including Chilean) ingenerating, compiling, or analyzing long-termdata (but see, Bustamante & Castilla 1987,Duarte et al. 1996, Moreno & Rubilar 1997,Vásquez et al. 2006, for Chilean examples). Webelieve that the strong emphasis inexperimental manipulations and null -hypothesis testing, particularly among rockyshore ecologists (Moreno 1984, Camus & Lima1995, Underwood 2000), has sometimes beenviewed as contradictory, rather than criticallycomplementary to quantitative monitoring ofbiological systems (Castilla 2000, Moreno2001). Indeed, long-term monitoring in coastalsystems is fundamental for several practicalreasons, but one of them is to assess theaccuracy and limitations of our ecological


models, most of which are based on long-termnear-equilibrium expectations, but are typicallyevaluated against short-term ‘snapshop’ data.The often, longer-term dynamics of speciesand species interactions that are fundamentalto ecosystem structuring and functioningsimply cannot be detected or assessed withsuch short-term studies. Yet, development ofcomplementary, well designed and replicatedexperiments are essential to test alternativehypothesis about the driving processes andmechanisms underplaying the temporalchanges. As longer term data becomesavailable, these hypotheses will likely need tobe reformulated and evaluated through newexperiments. As stated above, long-term datais our only hope to establish meaningful,though imperfect benchmarks against whichthe current ecosystem-state of the coastalocean can be compared and targets formanagement and conservation could be set.Here, the establishment and monitoring ofMarine Protected Areas (MPA), whencompared with long-term information onexploited (open-access) shores, gives us anopportunity to discern natural change inenvironmental variables from direct impactscaused by human exploitation (Castilla 1999,Carr 2000, Castilla 2000, Castilla et al. 2007a,Barrett et al . 2009). Finally, long-termbiological information and simultaneousenvironmental data represent the only way tocorrectly identify transient behavior fromlonger-term trends and cycles (Dye 1998a),and to uncouple internal system dynamicsfrom climate-driven fluctuations (Stenseth etal. 2002, Stenseth et al. 2003).

In this contribution, we use examples fromthe no-take MPA reserve site of the EstaciónCostera de Investigaciones Marinas (ECIM) atLas Cruces to illustrate the importance of long-term observations in the coastal ocean andhighlight the need to create, maintain andmonitor no-take marine protected areas in thecoast of Chile. Since we cannot attempt tosummarize here the wealth of ecologicalinformation generated at Las Cruces since itscreation in 1982, we selected four examples oftemporal fluctuations that include all trophiclevels, including taxa from algae to sea birds.For the sake of space, we only sparsely cite theexperimental work that support ourinterpretation of the changes observed in the

reserve, but the importance of this work couldnot be over-stated. We discuss how knowledgegenerated from this long-term monitoringprogram was institutionalized in marinemanagement and conservation policies.Information from long-term monitoringprograms has proved essential to buildecological l i teracy on how marineenvironments respond to anthropogenic and/or natural disturbances and how these couldbe managed. However, f inancing theseschemes which generally have no short termgains for funding agencies in both developingand developed countries still remains a majorchallenge.

Las Cruces Marine Protected Area: 25 years ofmonitoring a no-take reserve in Chile

The no-take marine reserve of ECIM is astretch of about 500 m of wave-exposed rockyshore and 10 hectares of subtidal rocky reefsthat was closed to fishers and tourists inOctober 1982. The main changes that ensuedin the rocky shore communities after theexclusion of humans have been amplyreported (Castilla & Durán 1985, Oliva &Castilla 1986, Durán & Castilla 1989, Castilla1993, Botsford et al. 1997, Castilla 1999,Cornelius et al. 2001, Loot et al. 2005), andhave some similarit ies with those thatoccurred at another, University-owned marineprotected area in Mehuín, near Valdivia insouthern Chile (Jara & Moreno 1984, Morenoet al. 1984, Godoy & Moreno 1989). Moreno(2001) provides a review of the main ecologicalchanges observed in the Mehuin reserve, withseveral examples of unprecedented andunanticipated changes that were documentedonly because of the existence of historicalrecords. Unfortunately, the marine reserve ofMehuín was terminated in 1991 (Fernandez &Castilla 2005). This means that the protectedarea of Las Cruces is the only existing andeffective marine reserve in Chile for whichthere is ecological information and long-termmonitoring.

The rapid and long-lasting effects of local processes

One of the clearest changes that took placeinside the ECIM reserve after the exclusion ofhumans was the increase in density and overall


biomass of the muricid gastropod Concholepasconcholepas (Brugiére) (“loco”), a highlyprized species that is intensively collected byfishers in open access areas and a topcarnivore that feeds preferentially on intertidalmussels (Castilla & Durán 1985, Castilla &Paine 1987, Durán & Castilla 1989). The 4-5times higher density of Concholepas inside thereserve of ECIM compared to areasimmediately outside (Fig. 1) led to the rapidintertidal decline of what were extensive beds(monocultures) of the competitively dominantmussel Perumytilus purpuratus (Lamarck),which released bare rock surface forcolonization and establishment of other sessilespecies, particularly two species of chthamalidbarnacles, Jehlius cirratus (Darwin) andNotochthamalus scabrosus (Darwin), whichquickly settle and covered most of the freedrock surface (Fig. 2). The majority of these

changes occurred swiftly after closure tohumans and with comparatively short delaysthroughout the coastline protected by thereserve. By late 1985, the seascape in the midintertidal zone inside the reserve wasdramatically different to the one outside.There, where fishers continually removedwhat turned out to be a keystone predator(Power et al. 1996, Navarrete & Castilla 2003),mussels continued to dominate the midintertidal zone and barnacles and other sessilespecies (not shown here) remained restrictedto sparse patches within the mussel bedmonoculture (Fig 2). Details of this story ofcascading interactions and indirect effectsaffecting all trophic levels of the intertidalcommunity have been presented in severalpublications (Castilla & Durán 1985, Oliva &Castil la 1986, Durán & Castil la 1989,Bustamante & Castilla 1990, Castilla 1999).

Fig. 1: Abundance of the intertidal carnivore gastropod Concholepas concholepas in spring-summermonths between 1981 and 2000 at 7-10 sites inside the ECIM marine reserve and in adjacent,‘open access’ areas to the south (outside ECIM). Data correspond to mean density (± SE) ofindividuals (juveniles and adults pooled together) in 1 m2 quadrats haphazardly distributed at 7-10wave exposed sites amongst and immediately above the holdfasts of the kelp Lessonia nigrescensin the low intertidal zone. Vertical dashed line indicates the time the marine reserve was establis-hed and humans were excluded. Details of methods can be found in Castilla & Durán (1985) andDurán & Castilla (1989).

Abundancia del gastrópodo intermareal carnívoro Concholepas concholepas en meses de primavera-verano entre1981 y 2000 en 7-10 sitios al interior de la reserva marina de ECIM y en zonas adyacentes de “acceso abierto” al sur(afuera de ECIM). Los datos corresponden a densidad (± EE) de individuos (juveniles y adultos juntos) en cuadran-tes de 1 m2 dispuestos azarosamente en 7-10 sitios expuestos al oleaje entre los discos e inmediatamente por sobreel alga Lessonia nigrescens en la zona intermareal baja. La línea segmentada vertical indica el momento en que lareserva fue establecida y los seres humanos se excluyeron. Detalles de los métodos se pueden encontrar en Castilla& Durán (1985) y Durán & Castilla (1989).


Fig. 2: Average cover (% ± SE) of the mussel Perumytilus pupuratus and chthamalid barnacles(Jehlius cirratus and Notochthamalus scabrosus pooled together) in spring-summer months at theintertidal zone of the ECIM marine reserve (inside) and in the ‘open access’ shore to the south(outside). Between 1981 and 2000 cover was estimated using 4-8 1 m2 quadrats (81 intersectionpoints), haphazardly positioned on gently sloping (< 45°) wave exposed platforms. After year 2000cover was estimated with 10-12 0.25 m2 quadrats haphazardly positioned in the same platforms.Vertical dashed line indicates the time the marine reserve was established and humans were exclu-ded. The dotted connecting lines indicates years when data were not collected in spring-summermonths and were not included for consistency. Details of methods can be found in Castilla & Durán(1985) and Castilla et al. (1993). The two inserts show monthly recruitment rates of barnacles (toppanel) and mussels (mid panel) at high and mid intertidal platforms, respectively, at sites inside andoutside the ECIM marine reserve between 1997 and 2007. Recruitment data are expressed here asthe logarithm of the number of individuals found per artificial collector (5 plates for barnacles, 5Tuffy scrubbing pads for mussels) per day, by dividing by the number of days collectors were in thefield (usually 25-45 days). Data for barnacle includes only spring-summer months since no recruit-ment occurs in winter time. Data for mussels include all months of the year and presented here as 3-month moving averages. Details of recruitment methods and data treatment can be found in Nava-rrete et al. (2002), Navarrete et al. (2005) and Navarrete et al. (2008).

Cobertura promedio (% ± EE) del mitílido Perumytilus purpuratus y cirripedios chthamalidos (Jehlius cirratus yNotochthamalus scabrosus agrupados) en meses de primavera- verano en la zona intermareal al interior de la reservade ECIM (inside) y en zonas de acceso abierto (outside) al sur. Entre 1981 y 2000 la cobertura se estimó mediante4-8 cuadrantes (81 puntos de intersección) dispuestos azarosamente en plataformas expuestas al oleaje y de bajainclinación (< 45°). Después del año 2000 la cobertura se estimó mediante 10-12 cuadrantes de 0.25 m2 posiciona-dos azarosamente en las mismas plataformas. La línea vertical segmentada indica el momento en que se establecióla reserva marina y los seres humanos fueron excluidos. La línea punteada conectando las observaciones indica losaños en que no se recolectaron datos en primavera-verano y no fueron incluidos para mantener la consistencia.Detalles de los métodos pueden ser encontrados en Castilla & Durán (1985) y Castilla et al. (1993). Los dos gráficosinsertos muestran la tasa de reclutamiento de cirripedios (arriba) y mitílidos (central) en la zona intermareal alta ymedia, respectivamente, en sitios al interior y afuera de de la reserva marina de ECIM entre 1997 y 2007. Los datosde reclutamiento son expresados en logaritmo del número de individuos observados por colector artificial (5 placaspara cirripedios, 5 Tuffy para mitílidos) por día, a través de dividir por el número de días que los colectoresestuvieron en terreno (usualmente 25-45 días). Los datos de cirripedios incluyen solamente primavera-verano puesno ocurre reclutamiento en invierno. Los datos de mitílidos incluyen todos los meses del año y se presentan aquícomo promedios móviles de una ventana de 3 meses. Detalles de métodos para cuantificar reclutamiento se encuen-tran en Navarrete et al. (2002), Navarrete et al. (2005) y Navarrete et al. (2008).


Continued monitoring of the coastalecosystem of Las Cruces for the past 25 yearsshowed a remarkable persistence of thismodified, some might say ‘natural’ state insidethe reserve. First, the abundance (cover) ofbarnacles within the reserve declined from amaximum of about 80 % to around 50-60 % by1989 (Fig. 2), partly as a response tocompetition with macroalgae and partly due tointensified predation on barnacles by locos andother predators once mussels were harder tofind (Durán & Castilla 1989, Castilla 1999).After 1989 barnacle cover has fluctuated,without a clear cycle or periodicity, at aroundthis 50-60 % for the past 18 years and there areno signs of declines (Fig. 2). After the nearelimination of mussel beds inside the reserve,dropping from complete dominance to lessthan 10 % by 1984, mussels have neverrecovered in these 23 years, despiteconsiderable fluctuations in the abundance ofConcholepas inside the reserve (Fig. 1) and thepersistence of high mussel cover immediatelyoutside (Fig. 2). After year 2000 there was asmall decline in mussel bed cover outside thereserve (Fig. 2), but this change could be duein part to slight changes in the protocolfollowed to quantify mussel cover (from fixedpoints to random quadrants).

The stunning persistence of the seascapeinside the reserve begs the question ofwhether this ca. 500 m of coastline representswell the ecosystem state before humansstarted to extract Concholepas and many otherinvertebrates and algae, i.e. whether themarine reserve is a “baseline” of what anatural system looked like. This we can notknow for certain, largely because of thelimited and single spatial scale provided bythe ECIM reserve. Glimpses into the pastobtained by studying shell middens of pre-Columbian subsistence gatherers suggestthat large bodied gastropod and limpets werecommon (Jerardino et al. 1992), but it is hardto re-construct patterns of abundance of non-edible species, such as small mussel andbarnacles.

A different explanation for the persistentseascape inside the reserve is that the rapidresponse by the keystone predator pushed thesystem into an alternative, possibly stable state(sensu Lewontin 1969), different to the onefound in pre-historic times (e.g., Scheffer et al.

2001). This would mean that even ifConcholepas and other invertebrates werereduced to levels observed outside, the currentstate of system inside the reserve wouldpersist through local feedback mechanisms.For instance, considering the spatial extentand dramatic changes in overall mussel andbarnacle population sizes inside the reserve, isit possible that these changes have affectedthe rates of arrival of new individuals? If lowmussel abundance leads to low musselrecruitment and high barnacle abundanceleads to increased recruitment rates, then thereserve ecosystem would have some criticalfeedback mechanisms. Considering thatmussels and barnacles have free swimmingpelagic larvae that develop in the plankton fora few weeks (Thorson 1950, Roughgarden etal. 1988), it is difficult to imagine that changesat the scale of the reserve affect recruitmentrates, yet this proposition should be evaluatedthrough additional observations andexperiments.

Mussel and barnacle recruitment: The supplyside of marine communities

In 1997 we began monitoring monthlyrecruitment of mussels, barnacles and severalother invertebrate species at sites inside theECIM reserve, outside the reserve and 14other localities along the coast of central Chile(Navarrete et al. 2002, Navarrete et al. 2005).The use of the same, replicated artificialcollectors, which are replaced monthly at allsites and examined under the microscope (seeMartínez & Navarrete 2002, Navarrete et al.2002, Navarrete et al. 2008, for details) permitsan estimation of the rate of arrival of newindividuals at a given site. Results illustrateseveral issues.

First, while mussel abundance declinedrapidly and remained at low levels for 23 yearsfollowing the increase in Concholepas, musselrecruitment rates to this shore have been ashigh or higher than recruitment to nearbyopen-access areas, at least over the past 10years (Fig. 2 inserts). This reinforces theimportance of humans as top predators(Castilla 1993) that can control the importanceof key local processes (predation), which canthen cascade down to mussels and the generalstructure of the entire local community, even


Fig. 3: Average biomass (± SE) of adult Durvillaea antarctica (“cochayuyo”) kelp in the lowintertidal zone of ECIM (white bars) and in adjacent open access areas to the north (black bars)during spring low tides between 1981 and 2002. Data correspond to the total biomass of adultplants found along 500 m long transects of variable width conducted inside and outside the ECIMreserve. The gray line represents the differences in biomass between ECIM and the open accessareas with spline smoothing to better capture longer-term trends. Details of the methods can befound in (Castilla et al. 2007a).

Promedio de biomasa (± EE) de adultos del alga parda Durvillaea antarctica (“cochayuyo”) en la zona intermarealbaja de la ECIM (barras blancas) y de zonas adyacentes de libre acceso hacia el norte (barras negras), durantemareas bajas de primavera entre 1981 y 2002. Los datos corresponden al total de plantas adultas encontradas a lolargo de transectos de 500 m de largo y ancho variable realizados al intertior y afuera de la reserva marina deECIM. La línea grís respresenta la diferencia en biomasa entre ECIM y la zona de acceso abierto con un suavizado“spline” para capturar mejor tendencias de largo plazo. Detalles de métodos pueden encontrarse en (Castilla et al.2007a).

when there is abundant mussel larvae torecover the prey population.

Second, long-term recruitment data clearlyshow that the near elimination of mussel bedsfrom the ca. 500 m coastline inside the marinereserve, has had no negative effects on theavailability of larvae in the water column andpotential recruitment of young. Similarly,increased abundance of barnacles does notappear to have produced increased barnaclerecruitment inside the reserve as compared tonearby areas (Fig. 2 insert). This clearlyindicates that the dispersal scales of musseland barnacle larvae are way beyond the scalesof this marine reserve and adjacent habitats.This is probably an obvious result for manymarine ecologists. Nonetheless it is one oftremendous relevance when assessing theseparate and combined effects of marinereserve size, rates of larval replenishment andinternal species interactions (e.g., predator-

prey interactions) including demographicfeedbacks, on the structure and dynamics ofecosystems (Carr & Reed 1993, Botsford et al.2001, Shanks et al. 2003, Navarrete et al. 2005,Wieters et al. 2008). Thus, we cannot envisionany coastal long-term monitoring programwithout quantitative evaluation of recruitmentrates.

The long-term trend in loco following the exclu-sion of humans

When examining long-term data on Concholepasabundance inside and outside the marinereserve, it is apparent that densities haveremained generally higher inside than outside,but also that this gastropod undergoes periodicfluctuations in abundance that are not observedin the abundance of its mussel and barnacleprey on the same shore (Figs. 1 and 2). Lack oflocal bottom-up effects from prey to predators’


abundance and dependence of predatorpopulations on their own recruitment rates is anexpected result of predator-prey interaction inspecies with pelagic larvae (Gaines & Lafferty1995, Wieters et al. 2008) and this could well bean example of such dynamics. Indeed, there is ahighly significant temporal correlation inConcholepas abundance inside and outside thereserve (r = 0.81, P < 0.001), despite contrastingpatterns of prey abundance. But a detailedanalysis of Concholepas population fluctuationsis beyond the scope of this paper. We only wantto highlight here the need to monitor localabundances as well as recruitment of species atdifferent trophic levels if we are to understandlong-term fluctuations in coastal communities.

The edible kelp Durvillaea antarctica (Chamis-so) “cochayuyo”: Slow recovery of a short-distan-ce disperser

The rocky, low-shore kelp Durvil laeaantarctica (cochayuyo) , a short-distancedisperser (Hay 1977, Buschmann 1984, Taylor& Schiled 2005), is an important edible speciesused for local human consumption, along thecentral and southern coast of Chile (Gelcich etal. 2006). When the Las Cruces marine coastalstation was closed to human intervention 25years ago, extraction of “cochayuyo” wasintensive along the coast and it was thereforehypothesized that the protection of the initiallydepleted population would recover via self-replacement, first inside the no-take area, andthen would expand to adjacent non-protected(exploited) areas through seeding effects.

Data on adult biomass of cochayuyocollected over 20 years (1981-2002), bothinside the Las Cruces no-take reserve and inadjacent harvested (Fig. 3) areas show that:(a) At the time of the establishment of ECIM(1982), the species had an extremely depletedpopulation of less than 0.05 kg m-2, comparableto the abundance observed outside. (b) Adultcochayuyo populations slowly but steadilyrecovered to ca. 0.5 kg m-2 inside the reservein a period of about 5-7 years. During thissame period, cochayuyo biomass remained low(ca. 0.1 kg m-2) in open access areas. (c) In1992 and particularly 1993, the populationreached the highest biomass per unit area inthe no-take reserve (up to 2.5 kg m-2), andthereafter naturally decreased to intermediate

levels (ca. 0.5 - 1 kg m-2), probably as a resultof intra-specific competition or other densitydependent processes (Castilla et al. 2007 a).Abundance of cochayuyo remained at this levelfor at least 8 years (1995-2002). Importantly,re-colonization processes followed in open –access areas outside of the reserve. In factduring the 1995-2002 period, cochayuyobiomass in open access areas reached similarvalues to those inside. These long-term resultssuggest cross-boundary “seeding effects”between ECIM reserve and nearby openaccess grounds, however these results mightbe confounded by a decrease in cochayuyoharvesting activities from open access areassince 1989 (see Castilla et al. 2007a, for furtherdiscussion on this topic).

The cochayuyo example highlights theneed for long-term monitoring inside andoutside MPAs to detect and correctly interpretthe relative population dynamics of sessilespecies with short distance propaguledispersal. Indeed, long-term data provedcritical to document population recoveries thattook place over at least 13 years. The contrastwith the rapid dynamics of mussels andbarnacles described above, which occurred onthe very same rocky shore, is particularlyenlightening.

Unsuspected effects beyond the marine realmand fishers: Roosting seabirds

The examples selected above illustrate thegreat contrast in the temporal dynamics ofimportant components of the rocky intertidalcommunity that coexist within the same stretchof coastline. At least in part, these differencesmust be related to the differences in lifehistories of the species (modes of developmentand dispersal capabilities) and the size of themarine reserve. But just a few tens of metersaway from the intertidal rocks another stronginteraction was slowly unfolding. In November1997 we began monitoring, twice a day, thenumber of birds resting on the rocks inside theECIM reserve. At that time, 15 years after theclosure of the reserve, sea gulls (Larusdominicanus Lichtenstein) were slightly moreabundant than cormorants (Phalacrocoraxolivaceus [Humboldt]) during spring-summerdays (Fig. 4). In late 1999 we observed the firstsea gulls nesting inside the reserve and ever


since the numbers of chicks hatching hassteadily increased. As the reserve became anesting site for sea gulls, their numbersdramatically increased and surpassedcormorants by 2001, to stabilize at high levelsonly after 2006 (Fig. 4). At the same time, thenumber of cormorants within the same area hassteadily declined year after year, apparentlybecause of interference with the aggressivenesting sea gulls. Sea gulls regularly feed onrocky intertidal organisms in open access areasas well as the marine reserve Castilla & Paine(1987), Navarrete & Castilla (1990), Wieters etal. 2009) and, therefore, the increase observedin the reserve does not seem to be aconsequence of changes that occurred in theintertidal zone (Cornelius et al. 2001). Instead,sea gulls seem to recognize the reserve as asafe nesting site simply because people wereprevented from walking along the shore(Cornelius et al. 2001). No data exist frombefore 1997 and roosting birds are only rarelyobserved in adjacent areas outside the reserve(and are not counted), so we have no data for

comparison. We know that gulls never nestedon this shore before, but we can only assumethat cormorants were as, or more, abundantthan sea gulls before 1999. What otherchanges in the littoral community can betriggered by this drastic but slow shift in birdabundance and composition of birds inside thereserve? On the coast of Maine, (Ellis et al.2006) documented changes in soil nutrientcomposition and the structure of thevegetation following changes in relativeabundance of other species of cormorants andsea gulls. These changes might have alreadytaken place within the ECIM reserve but goneundocumented because we do not havemonitoring of vegetation in the reserve.

On hypothesis testing as a continuous processguided by long-term monitoring

Undoubtedly one of the most influentialconceptual developments originating fromexperimental manipulations in marine systemswas the idea that a single “keystone” species

Fig. 4: Mean number (± SE) of sea gulls (Larus dominicanus) and common cormorants (Phalacro-corax olivaceus) roosting on rocks in the littoral zone of ECIM reserve during spring-summermonths from 1997-2009. Number of birds are counted twice a day at four points inside the reservethroughout the year. Standard errors are based on differences among months.

Número promedio (± EE) de gaviotas (Larus dominicanus) y cormorán común (Phalacrocorax olivaceus)descansando en las rocas de la zona litoral de la reserva de ECIM durante los meses de primavera-verano desde1997 hasta 2009. Los números de aves son estimados por conteos realizados dos veces al día en cuatro puntos deobservación al interior de la reserva a través del año. Errores estándar son basados en diferencias entre meses.


can be responsible for the maintenance ofpatterns of community structure, speciescoexistence and local diversity. Thedemonstration that the seastar Pisasterochraceus (Brandt) was a “keystone predator”,conducted by (Paine 1966) on the coast ofWashington, USA, spurred a series ofexperiments around the world designed to testthe hypothesis that a single carnivore predator,usually an asteroid species, could play a pivotalrole on local species diversity. The waveexposed coast of central Chile was one of thoseshores that helped generalize the keystoneconcept. Through an experimental manipulationconducted in the early 80’s, Paine and Chileaninvestigators (Paine et al. 1985) demonstratedthat the seastar Heliaster helianthus (Lamarck)was a keystone species that controled theabundance of the competitively dominantintertidal mussel. Few researchers know thatthe rocky benches where Paine et al. (1985)experiments were conducted are located in LasCruces, “inside” what later became the marinereserve of ECIM. At the time of Paine et al.’sexperiments, fishers had free access to theshore and kept the biomass of the “other”(perhaps the “real”) keystone predator in thesystem, Concholepas concholpeas, at very lowlevels. Thus, after the profound transformationof the seascape triggered by Concholepas whenthe ECIM reserve was established (see above),the demonstrated role of Heliaster as a uniquekeystone predator had to be revised. Clearly therole of Concholepas had been under-estimatedand it seemed that at least two predator speciescould play major roles in this rocky shore.Indeed, further experiments (Navarrete &Castilla 2003) have shown that Heliaster andConcholepas can play major roles in thesecommunities and their effects are far largerthan those of the many other benthic predatorsthat coexist in this system. Or at least that’s thelevel of our understanding so far.

What have we learned for marine managementand conservation policies?

Ecological literacy is the ability to understandthe natural system that makes life on earthpossible; to understand the principles behindthe functioning of ecosystems and use thoseprinciples for creating sustainable futures (Orr1992). As noted in the above sections of this

paper, information from long-term monitoringprograms within and outside of a marinereserve at Las Cruces has greatly enhanced ourunderstanding of unexpected pathways inecosystem dynamics and the role of humansinfluencing these processes. This informationprovides basic building blocks, the necessaryecological literacy, for current and futuremanagement and conservation of marineenvironments. In the specific case of Chile,scientific knowledge generated in Las Crucesreserve triggered a learning process which waseventually institutionalized and converted into anational marine fisheries and managementpolicy. There have been important attempts tosummarize this institutionalization of ecologicalknowledge in Chile (see Castilla et al. 2007b,Castilla & Gelcich 2008, for different aspects ofthis process) and it is beyond the scope of thispaper to summarize these findings. We will justmention two key points that relate directly tothe role of ecological literacy, which stemmedfrom long-term monitoring programs.

In essence, research from long-termstudies (> 5 years) in Las Cruces providedinformation on natural restocking of fisheryresources (Castilla & Durán 1985), rates ofresource recovery (Castilla & Bustamante1989, Castilla et al. 1998, Castilla et al. 2007b)and multi-scale ecosystem dynamics (Castilla1999). Similar experiences in the nowterminanted marine reserve of Mehuín insouthern Chile supported the notion that rapidrecovery of over-exploited invertebratepopulations was possible, repeatable andoccurred even in small sections of the coast(Moreno et al. 1984, Moreno et al. 1986,Moreno 2001). Unfortunately, with terminationof this reserve, the opportunity to assess thegenerality of patterns detected in the ECIMreserve or geographic variation of suchpatterns can no longer be assessed. It must benoted that ECIM is a very small marinereserve (and so was Mehuin) of just about 500m linear coastline and so the dynamics insideare expected to be influenced by thesurrounding environment. Nonetheless, eventhese small MPA’s revealed the influence ofhuman activities with sharp and rapid (1-3years) recovery of invertebrate populations,contrasting sharply with patterns recentlyreported for marine reserves in Tasmania(Barret et al. 2009). It was precisely this rapid


recovery that made it possible to demonstratethe value of the reserve as a tool for coastalconservation and fisheries management. As aresult, these studies allowed the articulation oflinks between basic research (i.e., ecologicalprinciples) and applied science, therebybuilding the science foundations needed tosupport informed decision-making regardingmarine sustainable management.

Knowledge from the recovery and themonitoring of Las Cruces and other areas wasdisseminated to non-scientists, principallygroups of artisanal fishers. This knowledgeprompted the necessary dialogue betweenscientists and fishers to establish a co-learningexercise (Gelcich et al. 2005). Fishers andscientists established joint experimental no-take areas in order to minimize inaccuracies ofthe Las Cruces data at broader scales, therebyfostering ecological literacy under the premisethat the participation of resource users isimportant not only in the management ofresources, but also in research orientedtoward the generation of information andinnovations (Edwards-Jones 2001, Gelcich etal. 2006, Gelcich et al. 2008). Finally, researchfrom Las Cruces was used by scientists andother stakeholders (i.e., fishers) in takingproactive positions that promoted infusion ofsound science into policy implementation(Castilla & Gelcich 2008).

The boundaries between science and policyare not fixed; rather, they are routinelyrenegotiated by various stakeholders inparticular contexts and in regards to particularissues (Gray & Campbell 2009). Thus, a keychallenge is to strengthen and expand theconstructive role that science has contributedto the management of coastal resources toinform the design and management for marinebiodiversity. Long-term ecological monitoringprogrammes seem a fundamental componentfor the task, as they provide the necessarybaselines to build ecological literacy and indoing so, motivate the necessary dialogue andinnovations for adaptations (Folke 2006).

Funding challenges and the need to implement anetwork of effective no-take marine reserves

The Chilean Innovation Council forCompetitiveness (CNIC) aims to doubleChile’s Gross Internal Product by 2020

through investing strongly in innovation,knowledge, and human competences (CNIC2006). It considers that this strategy should beapplied mainly to those productive sectors thathave the highest potential for developmentsuch as mining, agriculture-based foodproducts, special interest tourism andaquaculture (CNIC 2006). Additionally, theCNIC has selected the “environment” as one offive critical crosscutting supporting services toachieve these development goals. In thiscontext, long-term marine ecologicalmonitoring is fundamental to provide Chilewith timely information that facil itatesincreasingly adaptive policies and prioritysetting. It also identifies changes and trendsoccurring in marine ecosystems and, as aresult, policy makers are better able to makedecisions related to development, conservationand sustainability.

In this article we have shown how longterm ecological monitoring within and outsidea marine reserve at Las Cruces and relatedresearch programs provide the necessarybenchmarks, knowledge and dialogue toconfront marine management and conservationissues under global environmental changescenarios. The examples also illustrate theimportance of not only creating, but actuallyextensively monitoring and effectivelymaintaining no-take marine reserves along thecoast of Chile. Historically, Chilean legislation(Fisheries and Aquaculture Law) hasemployed marine reserves for the purpose ofconserving genetic diversity of economicallyimportant biological resources and onlyrecently the ecosystems that support suchresources. Such reserves are managed by theUndersecretary of Fisheries. The no-takereserve of Las Cruces is an exception (forothers see Fernández & Castilla 2005), whichhas been financed privately and with little legalsupport, for 23 years, by ECIM, of the P.Universidad Católica de Chile. Only five yearsago the legislation allowed the creation ofprotected areas for conservation purposes inChile, under the name of “Areas MarinasCosteras Protegidas” (AMCP), and in 2005 LasCruces was officially declared an AMCP.However, this new model of protected areasthat emerged in Chile, under theadministration of the National Commission forthe Environment (CONAMA), is not the one


we fostered and benefited from the LasCruces’ experience. Instead, the concept ofAMCP’s in Chile (except for the one in LasCruces) is one of multiple-uses, which includeareas for biodiversity conservation, regulatedfisheries, tourism and education, usuallywithin a very large section of coast (> 15 kmcoastline). This makes maintenance andmonitoring difficult or impossible to achieve. Itis important to highlight that AMCP are onlyone tool for marine conservation and that abroader integrated network for marineconservation in which comparatively largesustainable use Management and ExploitationAreas for Benthic Resources (MEABRs) andsmaller no-take marine reserves (such as theone of Las Cruces) and sanctuaries arefundamental elements. Thus, although AMCPmight be a step forward, we mustunfortunately say that in Chile the need tocreate no-take marine reserves with efficientmonitoring programmes, still remains, despitecontinuous claims from the scientif iccommunity over the past 30 years (Castilla1976, 1986, Moreno & Vega 1988, Castilla1996, 2002).

Funding of long-term monitoring programsremains an important challenge in developingcountries such as Chile. Thus there is a need toincorporate ecological literacy as a basicelement of Chile’s development agenda. Oneimportant strategy could be to frame ecologicalliteracy as a building block within Chile’sexisting innovation and competitivenessstrategies. To date, however, the generation ofmarine long-term monitoring data in Chile (e.g.,Duarte et al. 1996, Moreno & Rubilar 1997,Vásquez et al. 2006, Castilla et al. 2007a) hasnot been valued and has been dependent on thework of a few key stewards, researchers whohave maintained monitoring initiatives, as thosepresented in this paper, through self-funded,short-term research grants. Thus, a long-termmonitoring scheme of linked social-ecologicalsystems in Chile should become a nationalpriority and the only way to achieve theproposed 2020 development target. Thisscheme should take the form of a network(Vaughan et al. 2001) and must include long-term multi-disciplinary monitoring along thecoast, through core variables (e.g., ecology,sociology, oceanography) of social-ecologicalsystem change. This network would include a

number of cooperative dispersed monitoringinitiatives in order to deliver the necessaryknowledge to determine baselines from whichecological literacy can be built upon.

SUPPLEMENTARY MATERIAL

The Spanish version of this article is availableas online Supplementary Material at http://rchn .b io log iach i le . c l/suppmat/2010/1/SM_Navarrete_et_al_2010.pdf

ACKNOWLEDGEMENTS

Collecting data over many years and fromdisparate components of coastal communitiesis a monumental task that cannot be achievedby single individuals and certainly this is notan exception. The authors of this contributionhave merely summarized the efforts of manyfriends, colleagues, students, postdocs andresearch assistants. It would be impossible tolist them all here. To all them we are verygrateful for their continuous enthusiasm andfor making possible the existence of ECIMreserve and its small but productive scientificcommunity. Several granting agencies havemade these studies possible. We’ll be remisednot to mention Fondecyt Regular, Inititationand Postdoctoral grants to the authors of thiscontribution over the past decades. Yet, manyof these long-term monitoring programswould have been l i teral ly impossible tomaintain without the support the InternationalDevelopment Research Council, Canada, theAndrew Mellon Foundation, and the FondapFondecyt 15001-001 grant to the Center forAdvanced Studies in Ecology and Biodiversity(CASEB). More recently, the LaboratorioInternacional de Cambio Global (LINCGlobalCSIC-PUC) has supported the continuationand valued the importance of these researchprograms.

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Invited Associate Editor: Christopher AndersonReceived July 9, 2009; accepted February 8, 2010

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