1. Biodivers Conserv
DOI 10.1007/s10531-008-9555-5
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ORIGINAL 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 ·
Rocío Moreno-Sánchez · Sandra Mendoza · Nelson Manrique ·
Andrés Mogollón · Juan D. Osorio · Alejandro Grajales ·
Juan Armando Sánchez
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 management
policies 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-building
corals are experiencing bleaching phenomena and a steady decline in abundance. The
resources of a Marine Protected Area (MPA) in Cartagena, Colombia, are in constant
decline, despite a current management plan and on-site staV, urging new conservation
actions. A multidisciplinary team gathered to evaluate management eVectiveness including
biophysical, socioeconomic and governance indicators. Coral cover and Wsh diversity and
abundance were low both inside and outside the MPA, which suggests a limited eYciency
of management. Currently, the MPA is a reef with low coral cover and high algae cover as
well 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 Agaricia
tenuifolia and Porites astreoides. Nonetheless, 35% of the scleractinian species sampled in
the 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 order
to allow ecosystem resilience. Social and governance indicators showed low-income levels
and few opportunities for communities living in and around the park, low governability,
C. Camargo · N. Manrique · A. Grajales · J. A. Sánchez (&)
Departamento de Ciencias Biológicas-Facultad de Ciencias, Laboratorio de Biología Molecular
Marina-BIOMMAR, Universidad de los Andes, P.O. Box 4976, Bogotá, Colombia
e-mail: juansanc@uniandes.edu.co
Present Address:
C. Camargo
Departamento Biologa y Microbiologa, Universidad de Boyac, Tunja, Colombia
J. H. Maldonado · R. Moreno-Sánchez · S. Mendoza · A. Mogollón · J. D. Osorio
Facultad de Economía-CEDE, Universidad de los Andes, Bogotá, Colombia
E. Alvarado
Facultad de Ciencias Naturales, Universidad Jorge Tadeo Lozano, Bogotá, Colombia

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weak communication among stakeholders and with authorities at diVerent levels. As a
result, problems related to over exploitation of resources were commonplace in the MPA.
These results reXect low adaptive capacity of communities to comply with restrictive
conservation rules, showing that establishment of a protected area is a necessary but insuY-
cient condition to guarantee conservation goals. Ignoring the role of local communities
only will exacerbate the problems associated with natural resources. Involvement of
communities in strategic ecosystems management appears to be a requisite to improve
eVectiveness of protected areas, and participatory strategies, such as co-management, oVer
opportunities to improve governability while letting communities adapt to MPA needs.
Keywords Caribbean · Colombia · Coral reefs · Management eVectiveness · Marine
protected areas · Zooxanthellae · Social–ecological 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 the
symbiotic relationship between corals (Anthozoa: Cnidaria) and zooxanthellae (Symbiodi-
nium spp.; Dinophyta) (Muscatine and Porter 1977). Because of the energy provided by
their symbiont, corals can achieve high growth rates forming gigantic reef structures (e.g.,
the Mesoamerican Reef or the Great Barrier Reef). Despite comprising <0.5% of the ocean
Xoor, coral reefs harbor almost a third of all marine Wsh species (Samoilys et al. 2007). On
a global scale, coral reefs face diverse threats including overexploitation, habitat destruc-
tion, pollution and climate change (e.g., Wilkinson 1996; Hoegh-Guldberg et al. 2007).
Climate change through the production of elevated oceanic temperatures and high radiation
and increased coastal development, have generated, separately or in conjunction, sporadic
bleaching phenomena or the expulsion of zooxanthellae that often results in partial or total
coral mortality (see reviews in: Hoegh-Guldberg 1999; Coles and Brown 2003; Douglas
2003; Hughes et al. 2005).
In all countries, strengthening the relationship between conservation actions and human
welfare is necessary. Marine protected areas (MPAs) are intended to protect species,
marine habitats, biodiversity, restore Wsheries, manage tourist activities, and reduce con-
Xicts among users (Pomeroy et al. 2005). Hence, the global goal is to cover 10% of all
marine ecological regions with MPAs, including both multiple use and strictly protected
areas (Wells et al. 2007). MPAs are beneWcial (e.g., Aguilar-Perea et al. 2006; Branch and
Clark 2006; Claudet et al. 2006; Hiddink et al. 2006; Pérez-Ruzafa et al. 2006; Shears et al.
2006; Russ et al. 2008) for increasing in economically important Wsh assemblages (e.g.,
sizes, diversity and abundance of commercial species: Halpern 2003) and replenishment of
eggs and larvae by increasing spawner biomass (e.g., Castilla and Bustamante 1989). In
addition, the MPA spillover eVect may improve Wsheries outside reserves (e.g., Branch and
Odendaal 2003; Russ et al. 2008). One way in which MPAs, health of coral reef ecosys-
tems, and the welfare of Wshing communities are linked is that by protecting the coral reef,
coral cover and Wsh abundance and diversity inside the MPA, increases in Wsh abundance
outside the MPA promote higher catches for Wshermen (e.g., Gjertsen 2005). Conse-
quently, MPAs are used both for habitat protection and as a Wsheries management tool
(Campbell and Hewitt 2006). Nonetheless, MPA eVectiveness greatly depends on proper
management actions and policies (e.g., Halpern and Warner 2002; Fraschetti et al. 2005;
McClanahan et al. 2008). Evaluation of management eVectiveness considers objective

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elements to assess past behavior and future needs in order to turn current practices into
adaptable management. The present study, including biological, socioeconomic and gover-
nance components, is the Wrst evaluation of management eVectiveness carried out in
Colombia, and it is intended to oVer stakeholders tools for improving the decision-making
around MPA performance and the standard of living for communities.
Study site
The National Natural Park Rosario and San Bernardo Corals (NNP-RSBC; 10°15Ј and
9°35ЈN, 75°47Ј and 75°50ЈW) established in 1977, presents an extensive MPA as well as
the most diverse and developed coral reefs in the Colombian continental platform. NNP-
RSBC also includes mangrove communities associated with coastal lagoons and extensive
sea grass. About 40 islands and cays form both archipelagos, whose geological origins
were mud diapirism (e.g., Vernette et al. 1992) (Fig. 1). Resources have diminished
abruptly in the MPA since 1950, when colonization of the islands began; coral cover has
declined during the last two decades mostly because of coral bleaching, disease, overWsh-
ing, increase in human population and building in the coastal areas, and consequent
increases 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 protected
area in the proximity of Barú island (see Sánchez 1999) were chosen for comparison with
areas without management. Despite a current management plan and being the oldest
marine national park in Colombia, governability and enforcement capacity are low and, as
a result, resources are diminishing and call for new and urgent conservation actions to turn
current management policies into an adaptive management.
Fig. 1 Biophysical sampling sites inside and outside the MPA (stars)

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Methodology
Biophysical assessment
A team of 12 scientists and technicians from diVerent Colombian institutions conducted
surveys to collect the biophysical data following Pomeroy et al. (2005). Sampling sites
were geo-referenced and located with GPS. Two Weld trips were made, one in May 2006
when 16 sites were surveyed, eight outside and eight inside the park, and another during
September 2006, when another eight stations were surveyed inside the park. Sites outside
the MPA were used as control sites, where there was no formal management. To increase
information on biophysical indicators but incorporating enough simplicity for management
interpretation, all the indicators were grouped into either focal species abundance or
community structure (Table 1).
Focal Wsh species
Fish populations (in just three economically important families: Scaridae, Lutjanidae and
Serranidae) were estimated by visual surveys along a 50 m by 2 m wide transect for a total
of 100 m2
(including body size estimates, e.g., Friedlander et al. 2003). In each of the 24
sampling sites two observers swam two 50 m transects to perform the Wsh survey. At each
station, 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 diVerences
between 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 and
A. cervicornis, sixty 1 m2
photo sequences were taken from belt-transects (30 m long and
2 m wide) laid beside Wsh transects in each of the sampling sites. Other coral species not
endangered but potentially vulnerable, Siderastrea siderea and Diploria labyrinthiformis,
were chosen as indicators of sedimentation loads (e.g., Ginsburg et al. 2001), and surveyed
in 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 (Pomeroy
et al. 2005) were estimated using Image J software (NIH) after size distortion correction
using the quadrant frame in Photoshop (Adobe). Cluster analysis was done to observe sim-
ilarity among sites both inside and outside the MPA (Sánchez et al. 2005). To obtain more
accurate mean values and to check the heterogeneity of the stations, a bootstrap resampling
approach (100 replicates) was done as well. Non-parametric tests (Kruskal–Wallis) were
conducted to assess diVerences between protected and unprotected sites. The diversity and
distribution of zooxanthellae was determined by collecting tissue samples from colonies
inside and outside the MPA. Coral samples were screened using a set of molecular biology
techniques to identify zooxanthellae types (e.g., LaJeunesse 2002; Santos et al. 2003;
Granados et al. 2008).

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Table1IndicatorsselectedfortheMPAeVectivenessassessmentbasedonworkshopresults
GroupIndicatorMethods
Biophysical
Focalspeciesabundanceand
structure
Fish:commercialspeciesandherbivoresVisualtransects
AbundanceofAcroporapalmata,A.cervicornis,
D.labyrinthiformisandS.siderea
Phototransectdata
Size-structureDirectmeasurements
CommunitystructureCompositionandabundancePhototransectdata
ZooxanthellaediversityandhostdistributionSSU,ITS2,DGGEandDNAsequencing
Socioeconomic
Localmarineresourceusepatterns
andsocioeconomicconditions
LocalmarineresourceusepatternsPRD,productiveproWle
PerceptionofseafoodavailabilityPRD,seasonalanalysis
HouseholdincomedistributionbysourcePRD,productiveproWleandEEGsurvey
HouseholdoccupationalstructurePRD,productiveproWleandEEGsurvey
NumberandnatureofmarketsPRD,productiveproWle
ImpactonresourcesLevelofunderstandingofhumanimpactsonresourcesPRD,problemsandopportunitiesmatrix,
EEGsurvey,parkstaVinterviews
PerceptionoflocalresourceharvestPRD,productiveproWle,socialcartography,
seasonalanalysisandsubmarineproWle
Formalandinformalknowledge
aboutresources
StakeholderknowledgeofnaturalhistoryPRD,historicalanalysis
DistributionofformalknowledgetocommunityParkstaVinterviewsandEEGsurveys
LeadershipinenvironmentalmanagementPercentageofstakeholdergroupinleadershippositionsEEGsurveys
AssociatedvaluestotheparkLocalvaluesandbeliefsaboutmarineresourcesEEGsurveysandPRDsocialcartography
Perceptionofnon-marketandnon-usevalueEconomicvaluation(touristsandtour-operators)
andEEGsurveys
Governance
Institutions,administrativeresources,
andexistenceandknowledgeofaEMP
Existenceofdecision-makingandmanagementbodyParkstaVinterviews
Existenceandadoptionofanenvironmental-management-plan(EMP)ParkstaVinterviews,EEGsurveys,tourist
surveys,andtouroperatorssurveys
AvailabilityandallocationofMPAadministrativeresourcesParkstaVinterviews
ScientiWcresearchExistenceandapplicationofscientiWcresearchandinputParkstaVinterviews
Legislation,norms,rulesandenforcementLocalunderstandingofMPArulesandregulationsEEGsurveys,touristsurveys
ExistenceandadequacyofenablinglegislationParkstaVinterviews

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Table1continued
GroupIndicatorMethods
ClearlydeWnedenforcementproceduresParkstaVinterviews
EnforcementcoverageParkstaVinterviewsandEEGsurveys
ResourceconXictLevelofresourceconXictPRD,conXictinstitutionalanalysisandproblems
andopportunitiesmatrix,parkstaVsurveys,tourist
surveys,touroperatorssurveys
ParticipationExistenceandactivitylevelofcommunityorganizationsPRDinstitutionalanalysis,EEGsurveys
DegreeofinteractionbetweenmanagersandstakeholdersPRDinstitutionalanalysis,EEGsurveys,park
staVsurveys
ProportionofstakeholderstrainedinsustainableuseEEGsurveys,parkstaVsurveys
LeveloftrainingprovidedtostakeholdersinparticipationEEGsurveys,parkstaVsurveys
Levelofstakeholderparticipationandsatisfaction
inmanagementprocessesandactivities
EEGsurveys,parkstaVsurveys
Levelofstakeholderinvolvementinsurveillance,
monitoringandenforcement
EEGsurveys,parkstaVsurveys
Degreeofinformationdisseminationtoencourage
stakeholdercompliance
EEGsurveys,parkstaVsurveys

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Socioeconomic and governance assessment
Replicate teams evaluated the success of management and conservation objectives, using
16 socio-economic indicators and 16 governance indicators grouped into Wve categories
each (see details in Table 1). Socioeconomic categories were:
1. Local marine resource use patterns and socioeconomic conditions
2. EVect on resources
3. Formal and informal knowledge about resources
4. Leadership in environmental management
5. Values associated to the park
Governance categories were:
1. Institutions, administrative resources, and existence and knowledge of a management
plan
2. ScientiWc research
3. Legislation, norms, rules and enforcement
4. Resource conXict
5. 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 methods
are described below.
Participative rural diagnostic
The Wrst stage of the socioeconomic research was the elaboration of a participative rural
diagnostic (PRD) involving several communities living either adjacent or within the MPA
in 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 information

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Table 2. Three workshops for PRD activities were carried out in focal groups with about
100 participants.
Interviews with park staV
Following the PRD, personal, semi-structured interviews with MPA staV of the Rosario
and San Bernardo Corals Natural National Park Unit (RSBC-NNPU) were conducted.
Interviews included all 23 park staV, and included open and multiple choice questions
regarding 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 cities
close to the park (Cartagena and Tolú). The survey was designed not only to determine the
economic value of the park, but also to collect socioeconomic and governance information
from tourists visiting the protected area. The economic methods used in the valuation
included contingent valuation and travel cost. In parallel, tour operators using the park as
main attraction were interviewed; out of 29 detected Wrms, 26 of them were surveyed. This
survey collected economic information about oVered tourism packages, Wrm size, percep-
tions about the park and—to determine the value of the park—referendum questions for
contingent 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 park
and its area of inXuence, Wve of them located adjacent to the MPA and three of them
located inside the area. These activities are called economic games because they are
designed in a way such that the participants play a game, emulating real life situations
involving economic decisions and, at the end, participants obtain gains from playing. In
this case, the game consisted on emulating Wsh extraction. Gains depend on their extraction
behavior, which was exhibited through individual extraction decisions. This activity is a
way of obtaining information about the behavior of the resource users under diVerent
management 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 collected
Productive proWle Main income-generating activities
Social cartography Spatial distribution of extractive activities and other activities
involving marine resources
Seasonal analysis of productive activities Patterns of Wsh extraction along the year
Submarine proWle Local knowledge about location of marine resources
Historical analysis Events that have shaped the evolution of the community,
resources and MPA
ConXict 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 opportunities

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235 participants played the games and completed the survey. In order to evaluate if
attitudes of participants about resource extraction diVered depending on location, commu-
nities were divided between those located inside the limits of the park and located outside
of the park, but using resources provided by it. A total of 130 players located outside the
park and 105 located inside participated. Players started with a baseline (control) to observe
behavior under open access; that phase included 10 rounds similar to all participants. In the
second 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 strategies
based on their ability to cooperate in the use of the resource. With this rule, internal
regulation eVectiveness was evaluated (15 inside and 25 outside).
3. Regulation. Some participants received a rule about extraction, which was imposed
externally. 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 among
players 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 information
from 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 to
arrange strategies according to their own perceptions and the information provided by
the ranger. With this treatment, a combination of external non-coercive intervention
and 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 was
organized to answer the selected indicators (Fig. 2). The advantage of using several
methods 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 and
magnitude.
Results
Biophysical indicators
Focal species
Overall, abundance values from the families Lutjanidae, Scaridae, and Serranidae were low
both 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 SЈ: 13.62 (7–20, minimum–
maximum) inside the area and 12.62 (9–17) outside; JЈ: 0.66 (0.51–0.75) inside and 0.65
(0.59–0.72) outside; and HЈ: 0.96 (0.75–1.10) inside and 0.96 (0.86–1.06) outside.
Bootstrapping, to examine the eVect of heterogeneity in the results, showed no diVerences
between the original and resampled values (Fig. 4).

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Abundance 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 than
outside 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 were
compared between the zones, no signiWcant diVerences were found regardless of the spe-
cies (P > 0.05, Kolmogorov–Smirnov test). The same was true for the class-size structure
as we found no signiWcant diVerences between skewness and kurtosis in size distribution of
the four species found inside or outside of the MPA (P > 0.05, Kolmogorov–Smirnov test).
Although there were diVerences between sites, the populations of the four species were
positively 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 of
the sampled sites (28, 22, respectively). A. palmata and A. cervicornis were rare (7, 16
sites, 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 signiWcant
diVerences, as dead coral and rubble were the predominated substrate. Live coral cover was
represented mainly by Agaricia tenuifolia and Porites astreoides in most sites. There were
no diVerences between observed and resampled data (Fig. 4) and no signiWcant diVerences
between managed and unmanaged areas were observed (Kruskal–Wallis, P > 0.05). Classi-
Wcation analyses with coral abundance data showed slight diVerences with respect to their
management status but no clear aggregations of stations were observed (Fig. 3). Similarity
values were overall high among sites (»80%), and most stations inside the MPA formed
one cluster.
Diversity and distribution of zooxanthellae
A total of 280 samples of coral belonging to 37 coral species were collected and screened in
the 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 inside
the 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 28.9
Algae 27 24.2 31.1 30.9 24.8 34.1
Sponges 7.9 5.1 10.8 8.6 5.3 11.1
Gorgonians 2.2 1.8 2.9 4 3.1 4.3
Fish (densities per 100 m2
)
Lutjanidae 3.8 1 8.6 3.9 1 7.4
Scaridae 9.11 2.6 12.1 8.9 2.8 10.8
Serranidae 1.76 1.3 3.1 1.26 1.8 2.8

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were 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 polymorphic
species was P. astreoides (clades A, B, and C) followed by Millepora alcicornis (A, C, and
E) and Montastraea faveolata (A, C, and E).
Fig. 3 Cluster analyses (Bray–Curtis) of sampling sites. a ClassiWcation analysis of Wsh abundance. b Clas-
siWcation analysis for the benthic community

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Socioeconomic indicators
Socioeconomic indicators are presented for each of the Wve categories in which indicators
were grouped.
Pattern of use of local marine resources and socioeconomic conditions
Surveys to participants in EEG showed that main income-generating activities by inhabitants
were 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)

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the relative dependency of communities on natural resources. Those resources were mainly
used to satisfy the demand for seafood by tourists, as well as coral and other invertebrates for
craftsmanship and souvenirs, and, for the subsistence of local communities (non-monetary
income). Over 56% of households earn less than the equivalent to a Colombian monthly
minimum wage (about US$180), and around 34% of households receive between 1 and 2
monthly minimum wages (from US$180 to US$360). Assuming an average family size of
5.5 persons, 90% of families were living below the line of poverty, and 56% below the line
of extreme poverty, according to the criteria of one dollar daily per capita, established by the
World Bank.
Table 4 Coral host sampled and genetic identity of zooxanthellae (Symbiodinium spp.) in the NNP-CRSB
and nearby areas
Coral host Number of
samples
Genetic identity Depth (m)
18S(SSU) ITS2
Acropora cervicornis 2 A A3 8–10
Acropora palmata 1 A 10
Agaricia agaricites 20 C 3 8–22
Agaricia fragilis 2 C 20
Agaricia tenuifolia 15 C 3 8–36
Agaricia undata 2 C 8–22
Colpophyllia natans 8 C, B 7–22
Dichocoenia stokesii 1 C 22
Diploria c1ivosa 5 B B1 7–22
Diploria labyrinthiformis 5 C 7–22
Diploria strigosa 9 C 8–22
Eusmilia fastigiata 6 C 8–22
Favia fragum 2 C 7–22
Isophyllastrea rigida 2 C 10
Isophyllia sinuosa 2 B 10
Leptoseris cucullata 17 C 3 8–23
Madracis decactis 2 C 8
Meandrina meandrites 10 C-B C3-B1 8–22
Millepora alcicornis 20 A-B-C-D A4-B1-C1 8–22
Millepora complanata 1 A 8
Montastrea annularis 25 A 8–12
Montastrea annularis 25 C 12–22
Montastraea cavernosa 10 C 8–22
Montastraea faveolata 20 A 8–12
Montastraea faveolata 20 C-E 12–22
Mussa angulosa 2 C-B 10
Mycetophyllia aliciae 5 C-B 8–22
Mycetophyllia lamarckiana 5 C 10
Porites astereoides 20 A-B-C A4-B1-C3 8–36
Porites colonensis 10 C 8–22
Porites porites 5 C 8–22
Scolymia cubensis 2 C 20
Scolymia lacera 2 C 20
Siderastrea siderea 10 C-B 8–22
Solenastrea bournoni 2 B 20
Solenastrea hyades 5 C-B 20
Stephanocoenia intercepta 5 B 20

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The 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 is
an important tourist destination, as it oVers beaches, snorkeling and SCUBA diving sites
and is a source of seafood, especially snapper, lobster, crab, and shellWsh (queen-conch), as
well as handicrafts. In the southern region (San Bernardo islands) there was less tourism
pressure 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 local
communities were aware of environmental and resource problems in the area. From the
identiWed problems related with natural resources, 38% of stakeholders reported situations
associated with Wshing (mainly the use of destructive Wshing techniques and overWshing).
They also recognized coral reef damage as an important problem (20%), and perceived the
impact on land-based factors, including erosion (8%), deforestation (12%) and pollution
(10%). From the park staV surveys, it was evident that park authorities have implemented
some environmental education activities with communities since 1998, and have estab-
lished a formal environmental education program since 2006, which enhances awareness
among Wshers about the need of protecting marine resources.
Historical analyses let us identify some events and situations that since 1950 have
altered 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 of
gunpowder and other types of destructive Wshing techniques, overWshing, extraction of
biological 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; therefore
they identiWed the main events that have shaped the natural history of the zone. During
PRD focal groups, we identiWed local knowledge about marine resources such as spatial
distribution patterns of commercial species, seasonality of Wshing, types of commercial Wsh
classify by “meat type”, migratory issues, shortage times and reproductive seasons.
On the other hand, we found, from park staV surveys, Wsherman surveys and focal
groups, that dissemination of formal knowledge has been mainly performed by a team from
the 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 EEG
considered corals, mangroves, and beaches as very important (82, 81 and 79%, respec-
tively) and expressed a high degree of intergenerational altruism, declaring their interest for
conservation of the MPA for future generations (96%). Fisherman communities recognized
the biological and ecological importance of the MPA.
Tourists also perceived the beneWts of the MPA for tourism and recreation. Contingent
valuation of tourists showed a willingness to pay for maintaining the current conditions of
the park of $5.34 per person for entering into the MPA. This individual willingness to pay

15. Biodivers Conserv
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generated an annual Xow of beneWts of US$1,315,718. The travel cost method generated a
Xow 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 per
customer (tourist) taken into the MPA, equivalent to an aggregated annual Xow of beneWts
of 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 for
US$10,592,128 annually. Accordingly, the total Xow of beneWts from tourism, considering
use 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 2007–2011. 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 speciWc
projects and activities were deWned for those 5 years. Nevertheless, according to the PRD
focal groups, most of the inhabitants in the region were not aware of the existence of a
management 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 research
program, but it did deWne research guidelines and support initiatives (logistically) to vari-
ous research groups. According to the staV, scientiWc research should be focused—almost
equally—in two main areas: (1) biological, including monitoring of coral reefs, Wshing
resources, 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 natural
resources. During PRD focal groups, communities recognized the existence of some formal
regulations 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 were
recognized, behavior of participants during the EEG showed that they were not evenly
accepted or adopted. Figure 5 presents the average extraction decisions of communities
according 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, although
eYciently in reducing extraction, were more eVective in communities located inside the
park. Under external regulation, where participants were supposed to extract one unit as the
external rule, those located outside the MPA extracted, on average, 4.1 units, and those
located 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 visitors
should know when entering the MPA and what they really knew about regulations to

16. Biodivers Conserv
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follow in the park. Although 74% of visitors knew they were visiting a protected area only
35% 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 to
enforcement, the MPA staV stated that although a monitoring and control program, budget
restrictions limit the capability of the staV in completing all of scheduled activities. Park
staV 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 are
diYcult to enforce (86%). These Wndings show that although existent legislation is aimed to
enact de jure property rights to park authorities, in practice, stakeholders in the park use the
protected area as a de facto open access, where non-exclusive but rival resources lead to the
problems of a typical CPR.
Level of resource conXict
The use of CPR generates a divergence between collective interests and private interests as
individual Wshermen obtain gains from each unit extracted but assume merely the private
costs, ignoring social costs of extraction. This divergence is typical of Wsheries; extraction in
this MPA is not an exception where several stakeholders converge. From PRD and surveys to
stakeholders, we observed that extracting activities inside the MPA generate conXicts at
diVerent levels and among diVerent stakeholders. Below we summarize those issues.
1. The use of destructive Wshing methods (as gunpowder use, catch of small Wsh and
small mesh sizes) and over Wshing, which were reported by park staV as among the
main issues aVecting the MPA (13% each), were maybe the most important source of
conXict between communities and park authorities. Although during PRD, focal Wsher
groups recognized that behavior as an important source of conXict they justiWed it
given their socioeconomic situation: Wshing is their main income generating activity
and they do not have any income alternative with which to switch. The average income
of Wsherman households in the inXuence zone of the MPA was very low, which aggra-
vates the authorities–Wshers conXict.
2. The presence of Wshers from “outside” the MPA generates conXict with Wshers located
within its limits. During focal groups surveys, it was evident a competition between
these two groups of Wshermen; insiders blamed outsiders for using destructive Wshing
Fig. 5 Average extraction decisions from experimental economic games (EGG)

17. Biodivers Conserv
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methods that do not to comply with MPA regulations. Within communities, individuals
also 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 the
MPA and reported the damage of Wshing nets from industrial ships. When analyzing
problems and opportunities, Wshermen also mentioned that authorities did not apply the
same control and penalties to industrial Wshing, which is supposed to be completely
banned. Those perceptions worsen conXicts and reduce governability at the MPA.
From the MPA staV perspective, the most important threats to the natural park that also
aggravated conXicts between park authorities, and between direct and indirect resource
users were as follows:
• Governance issues (33%): including diYculty in enforcing the management plan, lack of
environmental 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 waste
disposal.
• 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 social
problems 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, albeit
there 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 with
diVerent public institutions in order to train communities in organization and participation.
However, there were no records of these activities. Although 60% of surveyed stakeholders
declared 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 coral
reefs suggested that management actions have limited eVectiveness. Currently, reefs in the
MPA have low coral cover, high algae cover, and large areas of dead coral resulting from
the mass mortality of Acropora spp.; these are signs of highly degraded reef habitats (e.g.,
Knowlton et al. 1990; Nyström et al. 2000). Live coral cover in the MPA was represented

18. Biodivers Conserv
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by pioneer coral species such as A. tenuifolia and P. astreoides, which may indicate a phase
shift in the community structure (e.g., Gardner et al. 2003). In addition, the widespread
presence of S. siderea may indicate high sedimentation loads in the study area (Ginsburg
et al. 2001; Vermeij and Bak 2002). Low abundances of lutjanids, scarids and serranids
were 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 coral
mortality 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 herbivorous
species such as parrotWsh and surgeonWsh must be urgently enforced, because of their
important role in the ecosystem dynamics (Bellwood et al. 2004). Maintenance of trophic
structure and functional diversity is a vital task for managers, in order to allow ecosystem
resilience (Nyström et al. 2000). Ecosystem integrity cannot be achieved in the MPA if
Wshing targets ecosystem engineers such as parrotWshes. This situation suggests that man-
agement actions have not yet achieved the expected eVects on the ecosystems; albeit longer
periods 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 one
zooxanthellae type simultaneously enhances the potential for resistance and resilience
against bleaching events. Since each type of zooxanthellae is adapted to speciWc environ-
mental conditions, symbiotic Xexibility is one facet of the resilience for an ecosystem
facing 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 coral
species have a single symbiont preference (Goulet 2006). The proportions of scleractinian
species sampled in our study that harbored more than one symbiont was 35%, which is
higher in comparison to other Caribbean locations, which have a maximum of 25% (Goulet
2006). In addition, in the same MPA parallel studies have found the presence of at least
three types of free-living zooxanthellae associated with macroalgae (Porto et al. 2008) and
the unexpected presence of clade G for the Wrst time in the Atlantic Ocean associated with
excavating 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 other
valuations of reefs elsewhere (Mogollón 2008). Nevertheless, the MPA is threatened by
conXicts 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 compel
people 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 were
aware 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 and
rivalry act together to intensify the overuse of marine resources.

19. Biodivers Conserv
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Our evaluation of governance found that the park staV is making substantial improve-
ments in its performance. However, policymaking is dispersed and ambiguous along the
local, regional, and national scales, which generates conXicts or diYculties when executing
policy at local level. In addition, communication channels with the community remain
weak. As a result, management and conservation goals are neither totally understood nor
fully supported by the community; more cooperative work is a primary need of adaptive
management (Pinto da Silva 2004). Lack of governance turns this MPA into a de facto
open 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 research
approaches are needed, not only in biological and ecological areas, but also in socioeco-
nomic and community-based initiatives. Themes such as the socioeconomic conditions of
inhabitants, alternative income generation sources, and governance of tourism must be
priority items.
Although our research was not intended to evaluate the degree of adaptive capacity of
Wshing communities at NNP CRSB, the generalized low levels of socioeconomic and
governability indicators might reXect low adaptive capacity of local communities. As
McClanahan et al. (2008) argue, in a MPA, where no-take zones are imposed, communities
with low adaptive capacity may be unable to comply with regulations about access to and
use of resources. According to our results, some community-based rules are better suited to
reduce extraction patterns and should be considered against other more restrictive ones.
Following McClanahan et al. (2008), current restrictive management strategies for the
MPA 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 local
communities 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 conservation
paradigms may be adopted (Cinner and Pollnac 2004). Co-management strategies, under-
stood as a combination of external regulation and internal ability and capacity to participate
in making decisions about management of protected areas, oVer opportunities to improve
governability of the protected area, and let the communities adapt to changes and improve
quality of life of populations. Therefore, Wnding ways to secure improvement of living
standards 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 reinforced
with building capacities to increase stakeholders understanding of the social importance of
protected 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 necessary
condition to improve the eVectiveness of protected areas.
In the case of the NNP CRSB, the Wrst step is to improve the communication channels
between authorities and the community, in order to establish rights and duties for each of
the involved parties, so that conservation objectives can be achieved and people inhabiting
the area can improve their welfare. Experimental economic games showed that people from
communities were willing to participate in activities involving shared responsibility in the
MPA management (Maldonado and Moreno-Sánchez 2008; Moreno-Sánchez 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 terms

20. Biodivers Conserv
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of 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 less
exposed to the park authorities’ eVorts and programs. In addition, communities located out-
side the MPA responded much better to co-management strategies than external regulation
rules, making co-management the most suited rule for those communities. So far, a pro-
posal for performing a controlled natural experiment implementing a co-management
scheme for the use of natural resources is the next step for moving these results into
practical implementation that improves management and sustainability use of coral reefs in
protected 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 in
Cartagena (I. Pineda, D. Bedoya, W. Gómez, Y. Ortodosgoitia, L.A. Correa). The Minister of Environment,
Household and Territorial Development of Colombia granted access to genetic resources to J.A. Sánchez for
the DNA analyses included in this paper (Contract 007, resolution 634, 14 March 2007). We are thankful to
La Tortuga Dive Shop (C. Martínez), INVEMAR (C. Reyes, G. Duque, D. Gil, P. Castillo), Universidad Jorge
Tadeo Lozano (A.M. Giraldo, D. Salazar, S. Teillaud), UniAndes (J. Mcallister, C. Aguilar, J. López-Angarita),
Universidad Nacional (A. Acero) and C. Flórez for their cooperation and assistance. Comments by Jack
Frazier, Thomas Shirley, and two anonymous reviewers are greatly appreciated.
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