Biodivers ConservDOI 10.1007/s10531-008-9555-5ORIGINAL PAPER

Community involvement in management for maintaining coral reef resilience and biodiversity in southern Caribbean marine protected areas

Carolina Camargo Jorge H. Maldonado Elvira Alvarado Roco Moreno-Snchez Sandra Mendoza Nelson Manrique Andrs Mogolln Juan D. Osorio Alejandro Grajales Juan Armando Snchez

Received: 16 February 2008 / Accepted: 27 November 2008 Springer Science+Business Media B.V. 2008

Abstract Climate change is posing new challenges to conservation because managementpolicies on protected coral reefs are less eVective than they were before the current ecosys-tem degradation. Coral reefs, the most diverse and complex marine ecosystem provide eco-nomic services for millions, but are seriously threatened worldwide because reef-buildingcorals are experiencing bleaching phenomena and a steady decline in abundance. Theresources of a Marine Protected Area (MPA) in Cartagena, Colombia, are in constantdecline, despite a current management plan and on-site staV, urging new conservationactions. A multidisciplinary team gathered to evaluate management eVectiveness includingbiophysical, socioeconomic and governance indicators. Coral cover and Wsh diversity andabundance were low both inside and outside the MPA, which suggests a limited eYciencyof management. Currently, the MPA is a reef with low coral cover and high algae cover aswell as large dead coral areas, which are generally signs of highly degraded reef habitats.Live coral cover in the MPA was represented by pioneer coral species such as Agariciatenuifolia and Porites astreoides. Nonetheless, 35% of the scleractinian species sampled inthe area harbored more than one zooxanthellae symbiont, which suggests potential resis-tance and resilience against coral bleaching. Maintenance of trophic structure and func-tional diversity is an important endeavor that should be a priority for management in orderto allow ecosystem resilience. Social and governance indicators showed low-income levelsand few opportunities for communities living in and around the park, low governability,

C. Camargo N. Manrique A. Grajales J. A. Snchez (&)Departamento de Ciencias Biolgicas-Facultad de Ciencias, Laboratorio de Biologa Molecular Marina-BIOMMAR, Universidad de los Andes, P.O. Box 4976, Bogot, Colombiae-mail: juansanc@uniandes.edu.co

Present Address:C. CamargoDepartamento Biologa y Microbiologa, Universidad de Boyac, Tunja, Colombia

J. H. Maldonado R. Moreno-Snchez S. Mendoza A. Mogolln J. D. OsorioFacultad de Economa-CEDE, Universidad de los Andes, Bogot, Colombia

E. AlvaradoFacultad de Ciencias Naturales, Universidad Jorge Tadeo Lozano, Bogot, Colombia1 C

Biodivers Conservweak communication among stakeholders and with authorities at diVerent levels. As aresult, problems related to over exploitation of resources were commonplace in the MPA.These results reXect low adaptive capacity of communities to comply with restrictiveconservation rules, showing that establishment of a protected area is a necessary but insuY-cient condition to guarantee conservation goals. Ignoring the role of local communitiesonly will exacerbate the problems associated with natural resources. Involvement ofcommunities in strategic ecosystems management appears to be a requisite to improveeVectiveness of protected areas, and participatory strategies, such as co-management, oVeropportunities to improve governability while letting communities adapt to MPA needs.

Keywords Caribbean Colombia Coral reefs Management eVectiveness Marine protected areas Zooxanthellae Socialecological systems Symbiodinium Participatory methods, experimental economic games Community involvement, comanagement

Introduction

Coral reefs are the most productive and diverse ecosystem in the seas, due in part to thesymbiotic relationship between corals (Anthozoa: Cnidaria) and zooxanthellae (Symbiodi-nium spp.; Dinophyta) (Muscatine and Porter 1977). Because of the energy provided bytheir symbiont, corals can achieve high growth rates forming gigantic reef structures (e.g.,the Mesoamerican Reef or the Great Barrier Reef). Despite comprising

Biodivers Conservelements to assess past behavior and future needs in order to turn current practices intoadaptable management. The present study, including biological, socioeconomic and gover-nance components, is the Wrst evaluation of management eVectiveness carried out inColombia, and it is intended to oVer stakeholders tools for improving the decision-makingaround MPA performance and the standard of living for communities.

Study site

The National Natural Park Rosario and San Bernardo Corals (NNP-RSBC; 1015 and935N, 7547 and 7550W) established in 1977, presents an extensive MPA as well asthe most diverse and developed coral reefs in the Colombian continental platform. NNP-RSBC also includes mangrove communities associated with coastal lagoons and extensivesea grass. About 40 islands and cays form both archipelagos, whose geological originswere mud diapirism (e.g., Vernette et al. 1992) (Fig. 1). Resources have diminishedabruptly in the MPA since 1950, when colonization of the islands began; coral cover hasdeclined during the last two decades mostly because of coral bleaching, disease, overWsh-ing, increase in human population and building in the coastal areas, and consequentincreases in suspended sediment discharges (runoV and sewage) (e.g., Restrepo et al.2006). In addition to 16 reef sites within this MPA, eight reef sites outside the protectedarea in the proximity of Bar island (see Snchez 1999) were chosen for comparison withareas without management. Despite a current management plan and being the oldestmarine national park in Colombia, governability and enforcement capacity are low and, asa result, resources are diminishing and call for new and urgent conservation actions to turncurrent management policies into an adaptive management.

Fig. 1 Biophysical sampling sites inside and outside the MPA (stars)1 C

Biodivers ConservMethodology

Biophysical assessment

A team of 12 scientists and technicians from diVerent Colombian institutions conductedsurveys to collect the biophysical data following Pomeroy et al. (2005). Sampling siteswere geo-referenced and located with GPS. Two Weld trips were made, one in May 2006when 16 sites were surveyed, eight outside and eight inside the park, and another duringSeptember 2006, when another eight stations were surveyed inside the park. Sites outsidethe MPA were used as control sites, where there was no formal management. To increaseinformation on biophysical indicators but incorporating enough simplicity for managementinterpretation, all the indicators were grouped into either focal species abundance orcommunity structure (Table 1).

Focal Wsh species

Fish populations (in just three economically important families: Scaridae, Lutjanidae andSerranidae) were estimated by visual surveys along a 50 m by 2 m wide transect for a totalof 100 m2 (including body size estimates, e.g., Friedlander et al. 2003). In each of the 24sampling sites two observers swam two 50 m transects to perform the Wsh survey. At eachstation, percentages of commercial families were determined. In addition, bootstrap resam-pling (1,000 replicates) was done to examine heterogeneity within each group of sites (e.g.,inside and outside the MPA). Non-parametric tests were conducted to assess diVerencesbetween these values. Species richness, uniformity and diversity indexes were calculated.Cluster techniques were used for assessing relationships between stations using log(x + 1)transformed data.

Coral species/cover

To monitor populations of the critically endangered coral species, Acropora palmata andA. cervicornis, sixty 1 m2 photo sequences were taken from belt-transects (30 m long and2 m wide) laid beside Wsh transects in each of the sampling sites. Other coral species notendangered but potentially vulnerable, Siderastrea siderea and Diploria labyrinthiformis,were chosen as indicators of sedimentation loads (e.g., Ginsburg et al. 2001), and surveyedin the same way as the endangered species.

Community composition and structure of coral reefs

In the same 60 m2 photo sequences, species richness, dominance and diversity (Pomeroyet al. 2005) were estimated using Image J software (NIH) after size distortion correctionusing the quadrant frame in Photoshop (Adobe). Cluster analysis was done to observe sim-ilarity among sites both inside and outside the MPA (Snchez et al. 2005). To obtain moreaccurate mean values and to check the heterogeneity of the stations, a bootstrap resamplingapproach (100 replicates) was done as well. Non-parametric tests (KruskalWallis) wereconducted to assess diVerences between protected and unprotected sites. The diversity anddistribution of zooxanthellae was determined by collecting tissue samples from coloniesinside and outside the MPA. Coral samples were screened using a set of molecular biologytechniques to identify zooxanthellae types (e.g., LaJeunesse 2002; Santos et al. 2003;Granados et al. 2008).1 C

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Biodivers ConservSocioeconomic and governance assessment

Replicate teams evaluated the success of management and conservation objectives, using16 socio-economic indicators and 16 governance indicators grouped into Wve categorieseach (see details in Table 1). Socioeconomic categories were:

1. Local marine resource use patterns and socioeconomic conditions2. EVect on resources3. Formal and informal knowledge about resources4. Leadership in environmental management5. Values associated to the park

Governance categories were:

1. Institutions, administrative resources, and existence and knowledge of a managementplan

2. ScientiWc research3. Legislation, norms, rules and enforcement4. Resource conXict5. Participation

To collect information for these indicators, several methodological approaches were imple-mented, all of them based on Weldwork with stakeholders (Fig. 2). Most relevant methodsare described below.

Participative rural diagnostic

The Wrst stage of the socioeconomic research was the elaboration of a participative ruraldiagnostic (PRD) involving several communities living either adjacent or within the MPAin the study area. Several tools from PRD were used to characterize the community status,to triangulate information from structured, semi-structured surveys and economic experi-mental games (EEG), and to collect general information about local ecological knowledge.Some of the PRD applied tools and the corresponding collected information is presented in

Fig. 2 Structure of the research methodology to collect socio-economic and governance information1 C

Biodivers ConservTable 2. Three workshops for PRD activities were carried out in focal groups with about100 participants.

Interviews with park staV

Following the PRD, personal, semi-structured interviews with MPA staV of the Rosarioand San Bernardo Corals Natural National Park Unit (RSBC-NNPU) were conducted.Interviews included all 23 park staV, and included open and multiple choice questionsregarding their perception about selected governance indicators.

Economic valuation of the protected area

In addition, an environmental economic valuation of the park was conducted. In this valua-tion, 816 tourists were surveyed. The questionnaire was designed and applied in two citiesclose to the park (Cartagena and Tol). The survey was designed not only to determine theeconomic value of the park, but also to collect socioeconomic and governance informationfrom tourists visiting the protected area. The economic methods used in the valuationincluded contingent valuation and travel cost. In parallel, tour operators using the park asmain attraction were interviewed; out of 29 detected Wrms, 26 of them were surveyed. Thissurvey collected economic information about oVered tourism packages, Wrm size, percep-tions about the park andto determine the value of the parkreferendum questions forcontingent valuation were included, as well as a direct measurement of total beneWts.

Economic experimental games

Finally, EEG were performed in eight of the most representative communities in the parkand its area of inXuence, Wve of them located adjacent to the MPA and three of themlocated inside the area. These activities are called economic games because they aredesigned in a way such that the participants play a game, emulating real life situationsinvolving economic decisions and, at the end, participants obtain gains from playing. Inthis case, the game consisted on emulating Wsh extraction. Gains depend on their extractionbehavior, which was exhibited through individual extraction decisions. This activity is away of obtaining information about the behavior of the resource users under diVerentmanagement alternatives for the MPA (controlled treatments), while compiling socio-economic, demographic and governance information from those communities. A total of

Table 2 Main tools used in the PDR and information that they provided

PDR tool Main information collectedProductive proWle Main income-generating activitiesSocial cartography Spatial distribution of extractive activities and other activities

involving marine resourcesSeasonal analysis of productive activities Patterns of Wsh extraction along the yearSubmarine proWle Local knowledge about location of marine resourcesHistorical analysis Events that have shaped the evolution of the community,

resources and MPAConXict institutional analysis Presence of institutions (park authorities, NGOs,

social assistance, academics, etc.)Relationships between community and institutions

Problems and opportunities matrix List of perceived community problems and opportunities1 C

Biodivers Conserv235 participants played the games and completed the survey. In order to evaluate ifattitudes of participants about resource extraction diVered depending on location, commu-nities were divided between those located inside the limits of the park and located outsideof the park, but using resources provided by it. A total of 130 players located outside thepark and 105 located inside participated. Players started with a baseline (control) to observebehavior under open access; that phase included 10 rounds similar to all participants. In thesecond phase, players were randomly assigned to diVerent treatments:

1. Baseline. Some participants continued playing under baseline, to have a control(25 outside and 20 inside).

2. Communication. Some participants had the opportunity to talk and construct strategiesbased on their ability to cooperate in the use of the resource. With this rule, internalregulation eVectiveness was evaluated (15 inside and 25 outside).

3. Regulation. Some participants received a rule about extraction, which was imposedexternally. However, players had the opportunity of cheating under an imperfect moni-toring setting. A Wne was applied to those monitored and caught violating the rule.Every participant had a 10% chance of being monitored. No communication amongplayers was allowed. With this rule, external regulation eVectiveness was evaluated(45 outside and 25 inside).

4. Co-management. Other group of participants had the chance of receiving informationfrom a real park ranger, who tried to convince them to reduce extraction. After receiv-ing that information, participants had the opportunity to talk among them and toarrange strategies according to their own perceptions and the information provided bythe ranger. With this treatment, a combination of external non-coercive interventionand internal regulation was evaluated (45 outside and 35 inside).

With these games, the hypothesis to test was whether diVerent approaches to social partici-pation generated diVerent responses on resource extraction.

This information obtained from the socioeconomic and governance assessment wasorganized to answer the selected indicators (Fig. 2). The advantage of using severalmethods was to let us compare and triangulate diVerent points of view about the manage-ment of the resources from groups of stakeholders obtaining diVerent beneWts in type andmagnitude.

Results

Biophysical indicators

Focal species

Overall, abundance values from the families Lutjanidae, Scaridae, and Serranidae were lowboth inside and outside the MPA (Table 3) but the diVerences were not signiWcant(ANOVA, P > 0.05). ClassiWcation analysis using the data from Wsh families showed clus-ter patterns independent of the management classiWcation, i.e., inside or outside the MPA(Fig. 3a). Community indexes corroborated the same pattern S: 13.62 (720, minimummaximum) inside the area and 12.62 (917) outside; J: 0.66 (0.510.75) inside and 0.65(0.590.72) outside; and H: 0.96 (0.751.10) inside and 0.96 (0.861.06) outside.Bootstrapping, to examine the eVect of heterogeneity in the results, showed no diVerencesbetween the original and resampled values (Fig. 4).1 C

Biodivers ConservAbundance of focal species (A. palmata, A. cervicornis, D. labyrinthiformis and S. siderea)

In general, the number of colonies of the four coral species was higher inside the MPA thanoutside of it, e.g., A. cervicornis (56 colonies inside, 54 outside), A. palmata (118-32),D. labyrinthiformis (109-102) and S. siderea (427, 156). Nevertheless, when densities werecompared between the zones, no signiWcant diVerences were found regardless of the spe-cies (P > 0.05, KolmogorovSmirnov test). The same was true for the class-size structureas we found no signiWcant diVerences between skewness and kurtosis in size distribution ofthe four species found inside or outside of the MPA (P > 0.05, KolmogorovSmirnov test).Although there were diVerences between sites, the populations of the four species werepositively skewed, therefore dominated by small size colonies. S. siderea and D. labyrinth-iformis can be regarded as common species as they were present in all (n = 28) or most ofthe sampled sites (28, 22, respectively). A. palmata and A. cervicornis were rare (7, 16sites, respectively).

Community composition and structure of coral reefs

Averaged live coral cover was greater inside the MPA, whereas algae, sponges, and gorgo-nians were higher outside MPAs (Table 3). The sampled sites did not have signiWcantdiVerences, as dead coral and rubble were the predominated substrate. Live coral cover wasrepresented mainly by Agaricia tenuifolia and Porites astreoides in most sites. There wereno diVerences between observed and resampled data (Fig. 4) and no signiWcant diVerencesbetween managed and unmanaged areas were observed (KruskalWallis, P > 0.05). Classi-Wcation analyses with coral abundance data showed slight diVerences with respect to theirmanagement status but no clear aggregations of stations were observed (Fig. 3). Similarityvalues were overall high among sites (80%), and most stations inside the MPA formedone cluster.

Diversity and distribution of zooxanthellae

A total of 280 samples of coral belonging to 37 coral species were collected and screened inthe laboratory for molecular identiWcation of zooxanthellae. Four Symbiodinium clades

Table 3 Community composition

Substrate cover (percentage) and Wsh mean density (within 100 m2 transects) in 24 sampled sites (16 insidethe MPA and 8 outside the MPA)

Group Inside MPA Outside MPA

Benthic (cover) Average Minimum Maximum Average Minimum Maximum

Coral 25.7 21.2 29.8 27.6 25.1 28.9Algae 27 24.2 31.1 30.9 24.8 34.1Sponges 7.9 5.1 10.8 8.6 5.3 11.1Gorgonians 2.2 1.8 2.9 4 3.1 4.3Fish (densities per 100 m2)

Lutjanidae 3.8 1 8.6 3.9 1 7.4Scaridae 9.11 2.6 12.1 8.9 2.8 10.8Serranidae 1.76 1.3 3.1 1.26 1.8 2.81 C

Biodivers Conservwere identiWed according to SSU Taq1-RFLP patterns, which included at least 10 ITS2-types (Table 4). Fifteen species (35%) included more than one clade, both by intra (e.g.,simultaneously) or intercolony (e.g., diVerent individual) variation. The most polymorphicspecies was P. astreoides (clades A, B, and C) followed by Millepora alcicornis (A, C, andE) and Montastraea faveolata (A, C, and E).

Fig. 3 Cluster analyses (BrayCurtis) of sampling sites. a ClassiWcation analysis of Wsh abundance. b Clas-siWcation analysis for the benthic community1 C

Biodivers ConservSocioeconomic indicators

Socioeconomic indicators are presented for each of the Wve categories in which indicatorswere grouped.

Pattern of use of local marine resources and socioeconomic conditions

Surveys to participants in EEG showed that main income-generating activities by inhabitantswere Wshing (72%), tourism services (6%) and handcrafting (5%). This Wnding highlights

Fig. 4 Mean abundances and deviations from a benthic organisms and b Wsh, inside and outside the MPA.Resampling percentages were obtained generating bootstrapped matrices from the original data set (100 replicates)1 C

Biodivers Conservthe relative dependency of communities on natural resources. Those resources were mainlyused to satisfy the demand for seafood by tourists, as well as coral and other invertebrates forcraftsmanship and souvenirs, and, for the subsistence of local communities (non-monetaryincome). Over 56% of households earn less than the equivalent to a Colombian monthlyminimum wage (about US$180), and around 34% of households receive between 1 and 2monthly minimum wages (from US$180 to US$360). Assuming an average family size of5.5 persons, 90% of families were living below the line of poverty, and 56% below the lineof extreme poverty, according to the criteria of one dollar daily per capita, established by theWorld Bank.

Table 4 Coral host sampled and genetic identity of zooxanthellae (Symbiodinium spp.) in the NNP-CRSBand nearby areas

Coral host Number of samples

Genetic identity Depth (m)

18S(SSU) ITS2

Acropora cervicornis 2 A A3 810Acropora palmata 1 A 10Agaricia agaricites 20 C 3 822Agaricia fragilis 2 C 20Agaricia tenuifolia 15 C 3 836Agaricia undata 2 C 822Colpophyllia natans 8 C, B 722Dichocoenia stokesii 1 C 22Diploria c1ivosa 5 B B1 722Diploria labyrinthiformis 5 C 722Diploria strigosa 9 C 822Eusmilia fastigiata 6 C 822Favia fragum 2 C 722Isophyllastrea rigida 2 C 10Isophyllia sinuosa 2 B 10Leptoseris cucullata 17 C 3 823Madracis decactis 2 C 8Meandrina meandrites 10 C-B C3-B1 822Millepora alcicornis 20 A-B-C-D A4-B1-C1 822Millepora complanata 1 A 8Montastrea annularis 25 A 812Montastrea annularis 25 C 1222Montastraea cavernosa 10 C 822Montastraea faveolata 20 A 812Montastraea faveolata 20 C-E 1222Mussa angulosa 2 C-B 10Mycetophyllia aliciae 5 C-B 822Mycetophyllia lamarckiana 5 C 10Porites astereoides 20 A-B-C A4-B1-C3 836Porites colonensis 10 C 822Porites porites 5 C 822Scolymia cubensis 2 C 20Scolymia lacera 2 C 20Siderastrea siderea 10 C-B 822Solenastrea bournoni 2 B 20Solenastrea hyades 5 C-B 20Stephanocoenia intercepta 5 B 201 C

Biodivers ConservThe communities in the northern region of the park (Rosario islands) were highly inte-grated to the market, especially to the tourist industry. This area is close to Cartagena and isan important tourist destination, as it oVers beaches, snorkeling and SCUBA diving sitesand is a source of seafood, especially snapper, lobster, crab, and shellWsh (queen-conch), aswell as handicrafts. In the southern region (San Bernardo islands) there was less tourismpressure but more exports of Wsh and shellWsh to interior markets.

Impact on resources

During PRD focal groups and from surveys to participants in EEG, we observed that localcommunities were aware of environmental and resource problems in the area. From theidentiWed problems related with natural resources, 38% of stakeholders reported situationsassociated with Wshing (mainly the use of destructive Wshing techniques and overWshing).They also recognized coral reef damage as an important problem (20%), and perceived theimpact on land-based factors, including erosion (8%), deforestation (12%) and pollution(10%). From the park staV surveys, it was evident that park authorities have implementedsome environmental education activities with communities since 1998, and have estab-lished a formal environmental education program since 2006, which enhances awarenessamong Wshers about the need of protecting marine resources.

Historical analyses let us identify some events and situations that since 1950 havealtered the availability of natural resources and have generated changes in the MPA land-scape. Such events and situations included arrival of new settlers, construction of recrea-tional houses and hotels along the beach, marine water pollution, increase in the use ofgunpowder and other types of destructive Wshing techniques, overWshing, extraction ofbiological material, coral bleaching and massive and disorganized/unregulated tourism.

Formal and informal knowledge about natural history and resources

Communities inside the park were established there, on average, 80 years ago; thereforethey identiWed the main events that have shaped the natural history of the zone. DuringPRD focal groups, we identiWed local knowledge about marine resources such as spatialdistribution patterns of commercial species, seasonality of Wshing, types of commercial Wshclassify by meat type, migratory issues, shortage times and reproductive seasons.

On the other hand, we found, from park staV surveys, Wsherman surveys and focalgroups, that dissemination of formal knowledge has been mainly performed by a team fromthe park authority, which is in charge speciWcally of community education and training.The park authority also had an environmental educational program to spread formal knowl-edge to the community. Its eVectiveness was not investigated here though.

Values associated to the protected area

Stakeholders gave high importance to marine resources. Most participants in the EEGconsidered corals, mangroves, and beaches as very important (82, 81 and 79%, respec-tively) and expressed a high degree of intergenerational altruism, declaring their interest forconservation of the MPA for future generations (96%). Fisherman communities recognizedthe biological and ecological importance of the MPA.

Tourists also perceived the beneWts of the MPA for tourism and recreation. Contingentvaluation of tourists showed a willingness to pay for maintaining the current conditions ofthe park of $5.34 per person for entering into the MPA. This individual willingness to pay1 C

Biodivers Conservgenerated an annual Xow of beneWts of US$1,315,718. The travel cost method generated aXow of beneWts from tourism and recreation of US$10,158,927.

Contingent valuation applied to tour operators showed a willingness to pay of $2.09 percustomer (tourist) taken into the MPA, equivalent to an aggregated annual Xow of beneWtsof US$515,138 from using the park as an input in the recreation and tourism industry.Additionally, income generated from tourism activity in the MPA accounted forUS$10,592,128 annually. Accordingly, the total Xow of beneWts from tourism, consideringuse and non-use values added up to US$22,064,445 annually.

Governance indicators

Institutions, administrative resources, and existence/adoption of a management plan

The park authority had a management plan designed for the period 20072011. The man-agement plan includes diagnostics, conservation goals and rules for resource-users (e.g.,MPA zoning). Additionally, a strategic plan of action was established where speciWcprojects and activities were deWned for those 5 years. Nevertheless, according to the PRDfocal groups, most of the inhabitants in the region were not aware of the existence of amanagement plan at the time of the meetings.

ScientiWc research

Since it is not part of its duties, the NNP-RSBC did not have a formal scientiWc researchprogram, but it did deWne research guidelines and support initiatives (logistically) to vari-ous research groups. According to the staV, scientiWc research should be focusedalmostequallyin two main areas: (1) biological, including monitoring of coral reefs, Wshingresources, mangroves, birds and turtles; and (2) social, including local community issues,tourism and Wshing management.

Legislation, norms, rules and enforcement

An ample set of laws, decrees and other rules existed aimed to conserve MPA naturalresources. During PRD focal groups, communities recognized the existence of some formalregulations such as minimum catch sizes, closed seasons for Wshing, minimum mesh sizes,and other regulation on Wshing activity. Moreover, stakeholders considered that these regu-lations should be enforced. However, due to the common pool resources (CPR) nature,stakeholders did not Wnd incentives to protect natural resources. Even though rules wererecognized, behavior of participants during the EEG showed that they were not evenlyaccepted or adopted. Figure 5 presents the average extraction decisions of communitiesaccording to the rules imposed. Baseline exhibited the higher extraction compared to treat-ments, showing that rules were eVective in reducing extraction. These rules, however, gen-erated diVerent impacts on communities. Communication and external regulation, althougheYciently in reducing extraction, were more eVective in communities located inside thepark. Under external regulation, where participants were supposed to extract one unit as theexternal rule, those located outside the MPA extracted, on average, 4.1 units, and thoselocated inside, 2.9. A co-management rule was the most eVective rule for reducing extrac-tion of resources, and, surprisingly, was even more eVective among outside communities.

With respect to tourists responses, we found a gap between the information that visitorsshould know when entering the MPA and what they really knew about regulations to1 C

Biodivers Conservfollow in the park. Although 74% of visitors knew they were visiting a protected area only35% admitted knowing about the existence of regulations associated with visiting the park,and just 24% declared knowing the rules included in such legislation. With respect toenforcement, the MPA staV stated that although a monitoring and control program, budgetrestrictions limit the capability of the staV in completing all of scheduled activities. ParkstaV declared that established rules are useful in meeting conservation goals in the MPA(64%) and that they are suYcient (51%). However, they mentioned that these rules arediYcult to enforce (86%). These Wndings show that although existent legislation is aimed toenact de jure property rights to park authorities, in practice, stakeholders in the park use theprotected area as a de facto open access, where non-exclusive but rival resources lead to theproblems of a typical CPR.

Level of resource conXict

The use of CPR generates a divergence between collective interests and private interests asindividual Wshermen obtain gains from each unit extracted but assume merely the privatecosts, ignoring social costs of extraction. This divergence is typical of Wsheries; extraction inthis MPA is not an exception where several stakeholders converge. From PRD and surveys tostakeholders, we observed that extracting activities inside the MPA generate conXicts atdiVerent levels and among diVerent stakeholders. Below we summarize those issues.

1. The use of destructive Wshing methods (as gunpowder use, catch of small Wsh andsmall mesh sizes) and over Wshing, which were reported by park staV as among themain issues aVecting the MPA (13% each), were maybe the most important source ofconXict between communities and park authorities. Although during PRD, focal Wshergroups recognized that behavior as an important source of conXict they justiWed itgiven their socioeconomic situation: Wshing is their main income generating activityand they do not have any income alternative with which to switch. The average incomeof Wsherman households in the inXuence zone of the MPA was very low, which aggra-vates the authoritiesWshers conXict.

2. The presence of Wshers from outside the MPA generates conXict with Wshers locatedwithin its limits. During focal groups surveys, it was evident a competition betweenthese two groups of Wshermen; insiders blamed outsiders for using destructive Wshing

Fig. 5 Average extraction decisions from experimental economic games (EGG)1 C

Biodivers Conservmethods that do not to comply with MPA regulations. Within communities, individualsalso declared conXicts mainly with respect to the use of illegal Wshing techniques.

3. A presence of industrial Wshing was detected inside the MPA. During social cartog-raphy exercises, individuals outlined the presence of industrial Wshing ships inside theMPA and reported the damage of Wshing nets from industrial ships. When analyzingproblems and opportunities, Wshermen also mentioned that authorities did not apply thesame control and penalties to industrial Wshing, which is supposed to be completelybanned. Those perceptions worsen conXicts and reduce governability at the MPA.

From the MPA staV perspective, the most important threats to the natural park that alsoaggravated conXicts between park authorities, and between direct and indirect resourceusers were as follows:

Governance issues (33%): including diYculty in enforcing the management plan, lack ofenvironmental education, lack of dissemination, lack of joint work with communities,lack of law compliance, and lack of income-generating alternatives.

Pollution issues (21%): water pollution from continental sources, and solid wastedisposal.

Fisheries issues (17%): inadequate Wshing arts and overWshing. Massive and disorganized tourism (12%). Lack of attachment with their own lands by communities within and outside the MPA. Overuse of recreation areas. Unorganized ship transit.

Participation

Some community organizations had emerged to deal with environmental and socialproblems in the MPA, including Wshermen associations, environmental education groups,eco-tourism groups, and solid-waste management organizations, which in part were sup-ported by the park authorities. The degree of interaction between authorities and communi-ties was low, e.g., lack of knowledge of the management plan by local communities, albeitthere was an ongoing environmental educational program. The same management plan,however, recognized the importance of enhancing the relationship with local communities.So far, the relationship between authorities and local communities has been mainly unilate-ral and focused on environmental education; participation of communities was marginal.According to staV interviews, MPA authorities had established strategic alliances withdiVerent public institutions in order to train communities in organization and participation.However, there were no records of these activities. Although 60% of surveyed stakeholdersdeclared voluntary work participation in activities led by park authorities and aimed at con-servation activities, there were no direct channels designed to promote such joint work.Involvement of communities in surveillance, monitoring and enforcement was marginal.

Discussion

Comparison of biophysical indicators within the MPA to those of unmanaged nearby coralreefs suggested that management actions have limited eVectiveness. Currently, reefs in theMPA have low coral cover, high algae cover, and large areas of dead coral resulting fromthe mass mortality of Acropora spp.; these are signs of highly degraded reef habitats (e.g.,Knowlton et al. 1990; Nystrm et al. 2000). Live coral cover in the MPA was represented1 C

Biodivers Conservby pioneer coral species such as A. tenuifolia and P. astreoides, which may indicate a phaseshift in the community structure (e.g., Gardner et al. 2003). In addition, the widespreadpresence of S. siderea may indicate high sedimentation loads in the study area (Ginsburget al. 2001; Vermeij and Bak 2002). Low abundances of lutjanids, scarids and serranidswere found in Wsh surveys, which are indications of high Wshing pressure within the MPA.The trophic integrity of the MPA has been greatly compromised because the low abun-dance of scarids. This creates conditions unsuitable for coral settlement and coral reef resil-ience (Mumby et al. 2006). In addition, low rates of Wsh bioerosion and increased coralmortality have enhanced the phenomenon of large areas of intact dead coral skeletons(Bellwood et al. 2004) such as the Acropora zones in the MPA. Protection of herbivorousspecies such as parrotWsh and surgeonWsh must be urgently enforced, because of theirimportant role in the ecosystem dynamics (Bellwood et al. 2004). Maintenance of trophicstructure and functional diversity is a vital task for managers, in order to allow ecosystemresilience (Nystrm et al. 2000). Ecosystem integrity cannot be achieved in the MPA ifWshing targets ecosystem engineers such as parrotWshes. This situation suggests that man-agement actions have not yet achieved the expected eVects on the ecosystems; albeit longerperiods are usually needed to monitor and achieve conservation goals (Tuya et al. 2000,Pomeroy et al. 2005).

Finding a higher proportion of polytypic coral colonies, i.e., harboring more than onezooxanthellae type simultaneously enhances the potential for resistance and resilienceagainst bleaching events. Since each type of zooxanthellae is adapted to speciWc environ-mental conditions, symbiotic Xexibility is one facet of the resilience for an ecosystemfacing environmental changes (e.g., Baker 2003; Van Oppen and Gates 2006; Hoegh-Guld-berg et al. 2007). However, it is alarming that the worldwide pattern is that most coralspecies have a single symbiont preference (Goulet 2006). The proportions of scleractinianspecies sampled in our study that harbored more than one symbiont was 35%, which ishigher in comparison to other Caribbean locations, which have a maximum of 25% (Goulet2006). In addition, in the same MPA parallel studies have found the presence of at leastthree types of free-living zooxanthellae associated with macroalgae (Porto et al. 2008) andthe unexpected presence of clade G for the Wrst time in the Atlantic Ocean associated withexcavating sponges from the genus Cliona (Granados et al. 2008). Those Wndings corrobo-rated the value of the conservation objects at this coral reef MPA.

Valuation of the MPA reXects the importance of these strategic ecosystems for society.The observed value was similar to important reefs in the Caribbean and higher than othervaluations of reefs elsewhere (Mogolln 2008). Nevertheless, the MPA is threatened byconXicts between conservation goals and the use of goods and services that emerge from:

Use by communities from inside and outside the MPA. Use by tourists, tour operators, hotels, occupants, etc. Industrial Wshing in areas near the MPA.

High poverty levels of local communities and lack of alternative income sources compelpeople to guarantee its sustenance mainly from natural resources and from the environmen-tal services supplied by the area. The increasing demand of tourism services results in over-harvesting of marine resources (Lovejoy 2006). Several members of the community wereaware of the diminishing supply of natural resources and its consequences for future gener-ations, which can be the starting point for creating solutions (Mow et al. 2007). However,the MPA was seen as an open access, common-pool resource where non-exclusion andrivalry act together to intensify the overuse of marine resources.1 C

Biodivers ConservOur evaluation of governance found that the park staV is making substantial improve-ments in its performance. However, policymaking is dispersed and ambiguous along thelocal, regional, and national scales, which generates conXicts or diYculties when executingpolicy at local level. In addition, communication channels with the community remainweak. As a result, management and conservation goals are neither totally understood norfully supported by the community; more cooperative work is a primary need of adaptivemanagement (Pinto da Silva 2004). Lack of governance turns this MPA into a de factoopen access resource. Therefore, the establishment of the MPA is insuYcient for conserv-ing the valuable resources that it hosts. Further eVorts are needed, such as improving gover-nance by incorporating communities in decisions and responsibilities. Additional researchapproaches are needed, not only in biological and ecological areas, but also in socioeco-nomic and community-based initiatives. Themes such as the socioeconomic conditions ofinhabitants, alternative income generation sources, and governance of tourism must bepriority items.

Although our research was not intended to evaluate the degree of adaptive capacity ofWshing communities at NNP CRSB, the generalized low levels of socioeconomic andgovernability indicators might reXect low adaptive capacity of local communities. AsMcClanahan et al. (2008) argue, in a MPA, where no-take zones are imposed, communitieswith low adaptive capacity may be unable to comply with regulations about access to anduse of resources. According to our results, some community-based rules are better suited toreduce extraction patterns and should be considered against other more restrictive ones.Following McClanahan et al. (2008), current restrictive management strategies for theMPA should be combined with social and public investments, including basic infrastruc-ture provision and income-generating alternatives that enhance performance in conserva-tion of the MPA. Such strategies must be designed to increase the capacity of localcommunities in adapting to protected areas restrictions, and taking advantage of conserva-tion at low social costs. In resource user communities characterized by poverty, manage-ment strategies should focus on improving the quality of life of people before conservationparadigms may be adopted (Cinner and Pollnac 2004). Co-management strategies, under-stood as a combination of external regulation and internal ability and capacity to participatein making decisions about management of protected areas, oVer opportunities to improvegovernability of the protected area, and let the communities adapt to changes and improvequality of life of populations. Therefore, Wnding ways to secure improvement of livingstandards for communities directly related to the use of resources in and around the pro-tected area should be in the agenda of authorities. These approaches should be reinforcedwith building capacities to increase stakeholders understanding of the social importance ofprotected areas. Several studies have mentioned the relevant role of community involve-ment in MPA management (Scholz et al. 2004; Cinner 2005; Cinner et al. 2005a, b).Involvement of communities in strategic ecosystems management appears as a necessarycondition to improve the eVectiveness of protected areas.

In the case of the NNP CRSB, the Wrst step is to improve the communication channelsbetween authorities and the community, in order to establish rights and duties for each ofthe involved parties, so that conservation objectives can be achieved and people inhabitingthe area can improve their welfare. Experimental economic games showed that people fromcommunities were willing to participate in activities involving shared responsibility in theMPA management (Maldonado and Moreno-Snchez 2008; Moreno-Snchez and Maldo-nado 2008). Such initiatives should deWne rights and duties for each participant involved(e.g., stakeholders and managers) and should be self-monitored, even if external institu-tions can promote or encourage these initiatives. EEG Wndings showed diVerences, in terms1 C

Biodivers Conservof extraction decisions between communities located outside and inside the park; therefore,management strategies encouraging community participation should also be diVerentiated.Adaptive capacities might be lower in communities outside the park, as they have been lessexposed to the park authorities eVorts and programs. In addition, communities located out-side the MPA responded much better to co-management strategies than external regulationrules, making co-management the most suited rule for those communities. So far, a pro-posal for performing a controlled natural experiment implementing a co-managementscheme for the use of natural resources is the next step for moving these results intopractical implementation that improves management and sustainability use of coral reefs inprotected marine areas.

Acknowledgments This study was funded by NOAA-Coral Grants (NA05NO54631013), a COLCIEN-CIAS grant (Project No. 1204-09-17774), and University of the Andes (Sciences and Economics Faculties).We are very grateful to the park authority in Colombia (UAESPNN) and all the staV from NNP CRSB inCartagena (I. Pineda, D. Bedoya, W. Gmez, Y. Ortodosgoitia, L.A. Correa). The Minister of Environment,Household and Territorial Development of Colombia granted access to genetic resources to J.A. Snchez forthe DNA analyses included in this paper (Contract 007, resolution 634, 14 March 2007). We are thankful toLa Tortuga Dive Shop (C. Martnez), INVEMAR (C. Reyes, G. Duque, D. Gil, P. Castillo), Universidad JorgeTadeo Lozano (A.M. Giraldo, D. Salazar, S. Teillaud), UniAndes (J. Mcallister, C. Aguilar, J. Lpez-Angarita),Universidad Nacional (A. Acero) and C. Flrez for their cooperation and assistance. Comments by JackFrazier, Thomas Shirley, and two anonymous reviewers are greatly appreciated.

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Community involvement in management for maintaining coral reef resilience and biodiversity in southern Caribbean marine protected areasAbstractIntroductionStudy siteMethodologyBiophysical assessmentFocal Wsh speciesCoral species/coverCommunity composition and structure of coral reefs

Socioeconomic and governance assessmentParticipative rural diagnosticInterviews with park staVEconomic valuation of the protected areaEconomic experimental games

ResultsBiophysical indicatorsFocal speciesAbundance of focal species (A. palmata, A. cervicornis, D. labyrinthiformis and S. siderea)Community composition and structure of coral reefsDiversity and distribution of zooxanthellaeSocioeconomic indicatorsPattern of use of local marine resources and socioeconomic conditionsImpact on resourcesFormal and informal knowledge about natural history and resourcesValues associated to the protected area

Governance indicatorsInstitutions, administrative resources, and existence/adoption of a management planScientiWc researchLegislation, norms, rules and enforcementLevel of resource conXictParticipation

DiscussionReferences

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