Status and conservation of coral reefs in Costa Rica

8/8/2019 Status and conservation of coral reefs in Costa Rica.

1/18

33Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 58 (Suppl. 1): 33-50, May 2010

Status and conservation of coral reefs in Costa Rica

Jorge Corts1, 2, Carlos E. Jimnez1, Ana C. Fonseca1, 3 & Juan Jos Alvarado11. Centro de Investigacin en Ciencias del Mar y Limnologa (CIMAR), Ciudad de la Investigacin, Universidad de

Costa Rica, San Pedro, 11501-2060 San Jos, Costa Rica; [email protected]. Escuela de Biologa, Universidad de Costa Rica, San Pedro, San Jos, Costa Rica.3. World Wildlife Fund (WWF), San Jos, Costa Rica, Interlink #718, P.O. Box 02-5635, Miami, Florida 33102, USA.

Received 30-VIII-2009. Corrected 03-X-2009. Accepted 12-XII-2009.

Abstract: Costa Rica has coral communities and reefs on the Caribbean coast and on the Pacific along the coastand off-shore islands. The Southern section of the Caribbean coast has fringing and patch reefs, carbonate banks,and an incipient algal ridge. The Pacific coast has coral communities, reefs and isolated coral colonies. Coral reefshave been seriously impacted in the last 30 years, mainly by sediments (Caribbean coast and some Pacific reefs) and

by El Nio warming events (both coasts). Monitoring is being carried out at three sites on each coast. Both coastssuffered significant reductions in live coral cover in the 1980s, but coral cover is now increasing in most sites. Thegovernment of Costa Rica is aware of the importance of coral reefs and marine environments in general, and inrecent years decrees have been implemented (or are in the process of approval) to protect them, but limited resourcesendanger their proper management and conservation, including proper outreach to reef users and the general public.Rev. Biol. Trop. 58 (Suppl. 1): 33-50. Epub 2010 May 01.

Key words: coral reefs, Costa Rica, monitoring, GCRMN, conservation, management.

Costa Rica has coral reefs on the Carib- bean coast and on the Pacific side (coastand off-shore islands). The Caribbean coast is212km long and consists mainly of high-energysandy beaches that on the Southern section areinterrupted by carbonate promontories (Fig. 1).These promontories are made up primarily offossil reefs (Pleistocene, Holocene), and beach-rock in some sections. Extant reefs develop on

top of these rocky outcrops (Corts & Guzman1985, Corts & Jimnez 2003a). Three coral reefareas are recognized on the Caribbean coast:1) fringing reefs between Mon and Limn, 2)fringing and patch reefs, and carbonate banks atCahuita National Park, and 3) fringing and patchreefs, carbonate banks, and incipient algal ridgebetween Puerto Viejo and Punta Mona (Fig. 1).Seasonal variability is minimum along this coast,with rains year round and no upwelling. Most of

the touristic activity on the Southern Caribbean

coast of Costa Rica is oriented toward the reefs,as are also the fisheries.

The Pacific coast of Costa Rica is 1 160kmlong, and has a high diversity of habitats: rockyshores of a wide variety of rock types, sandy beaches of several compositions and grainsize, mangrove forests, estuaries, a tropicalfjord, islands of various sizes, and several gulfsand bays (Fig. 2). The northern section of the

coast (Gulf of Papagayo) is characterized bya dry tropical forest, with a very dry seasonfrom December to April, and a rainy seasonfrom May to November. This part of the coastis exposed to seasonal upwelling (McCrearyet al. 1989) during the dry season due to thecrossing the isthmus of Trade Winds. The cen-tral and southern coast is covered with tropicalrain forest, with a transition zone in between inthe Central Pacific coast. Coral communities,

reefs and isolated coral colonies can be found


2/18

34 Rev. Biol. Trop. (Int. J. Trop. Biol. ISSN-0034-7744) Vol. 58 (Suppl. 1): 33-50, May 2010

Fig. 1. Caribbean coast of Costa Rica, monitoring sites and Marine Protected Areas. Codes: PNC=Parque Nacional Cahuita;REGAMA=Refugio Nacional de Vida Silvestre Gandoca-Manzanillo.

along the Pacific of Costa Rica, which has beendivided into eight regions (Corts & Jimnez2003b): 1) Santa Elena, in the Northern section

of the coast next to the border with Nicaragua;2) Baha Culebra, to the South of Santa Elenaand North of Pennsula de Nicoya; 3) Pennsulade Nicoya, mainly the seaward side of the pen-insula, since the inner section is an estuarineenvironment with very little coral growth; 4)Pacfico Central, extends from the East end ofGolfo de Nicoya to the largest mangrove areaof Costa Rica, the Sierpe-Trraba complex; 5)Pennsula de Osa, the outer section and part of

the entrance to Golfo Dulce; 6) Golfo Dulce,includes the reefs within the gulf; and offshoreislands: 7) Isla del Cao, 15km from the coast,and 8) Isla del Coco, more than 500km fromthe coast (Fig. 2).

STATUS OF THE CORAL REEF BENTHOSCARIBBEAN

Mon-Limn: Fringing reefs and carbon-

ate platforms are found in this section of the

coast which is subject to heavy wave action,with the largest reefs growing on the leewardside of the islands. This area is exposed to

freshwater runoff, sewage, petroleum pollu-tion and solid wastes from the main ports onthe Caribbean (Mata et al. 1987, Guzman &Jimnez 1992, Guzman & Garca 2002, Acu-a-Gonzlez et al. 2004). The coast betweenMon and the Port of Limn is bordered by acarbonate platform that extends from above theupper tidal zone down to 15m depth (Corts& Guzman 1985). The submerged platformis covered with algae, hydroids, sponges and

isolated corals. The most abundant corals in1983, when the area was surveyed, were: P.astreoides and A. agaricites forma purpurea(Corts & Guzman 1985). Beyond 15m depththe bottom consisted of soft mud (Corts 1998).Isla Uvita is off the Port of Limn (Fig. 1), buta strong current separates it from the port andits pollution. So, it is possible to observe well-developed reefs around the island. The eastside had an extensive carbonate platform, with

microatolls ofSiderastrea siderea in the lagoon


3/18


that was further exposed with the 1991 LimnEarthquake (Corts et al. 1992). A monitoringstation was established in 2005 in the west side,coral cover was very low and sponges weredominant (Fonseca et al. 2006a).

Cahuita: The largest fringing reef of theCaribbean in the country is located at ParqueNacional Cahuita (Fig. 1). This reef consists ofthree barriers; the outer barrier, stretching for5km from the Western side of Punta Cahuita, tothe Eastern side, it is separated from the coast between 100m and 2km. Between this barrierand the coast there is a small fringing reef, about500m long and within 100m from the shore,called the inner crest. Finally, a 100m barrier is

located of the Western end of the reef (Corts

& Risk 1984, 1985, Corts & Guzman 1985).Partch reefs are found within the lagoon and car-bonate banks off shore. The coral reef at Cahuitahad been degrading during the last 30 years dueto siltation, other anthropogenic impacts andnatural causes (some of them exacerbated by

human activity): massive death of organisms,earthquake, and warming events. Live coral cov-erage decreased from 40% in the early 1980s to10% in the early 1990s (Corts 1994). Usingthe AGRRA surveying protocol, live coral was2-3% in the late 1990s (Fonseca 2003). Thereef of Cahuita has been monitored since 1999using the CARICOMP monitoring protocol, andin recent years with funding from the South-ern Tropical America-Global Coral Reef Moni-

toring Network (STA-GCRMN) node. At the

Fig. 2. Pacific coast of Costa Rica, monitoring sites and Marine Protected Areas. Codes: ACG= rea de ConservacinGuanacaste; ACM Isla del Coco= rea de Conservacin Marina Isla del Coco; ACOPAC= rea de Conservacin PacficoCentral; ACOSA= rea de Conservacin de Osa; ACT= rea de Conservacin Tempisque; PNC= Parque NacionalCorcovado; PNMA= Parque Nacional Manuel Antonio; PNMB= Parque Nacional Marino Ballena; PNSR= Parque Nacional

Santa Rosa; RACB= Reserva Absoluta Cabo Blanco; RB Isla del Cao= Reserva Biolgica Isla del Cao.


4/18


CARICOMP site, live coral increased slightlyfrom around 15% to 17% in 2004, however turfalgal cover has increased significantly (Fonsecaet al. 2006a, Fig. 3).

The populations of the black sea urchin, Diadema antillarum, which were decimatedin the early 1980s in Costa Rica and widerCaribbean (Lessios et al. 1984, Murillo &Corts 1984) are recovering. Before the 1983mass mortality densities were 3.6 to 8.8 ind/m2(Valdez & Villalobos 1978), after the mortalitydensities were 0.25 to 2 ind/m2. By 1992 it hadreached 0.001 ind/m2 (Corts 1994) and in 2004,0.3 to 0.7 ind/m2 (Alvarado et al. 2004, Fonsecaet al. 2006a). The increase in Diadema may becontributing to the recovery of the reef at Cahu-

ita (Wyckoff & Corts unpubl. data). Similarobservations were done by Myhre & Acevedo-Gutirrez (2007) in Manzanillo, in which livecoral cover has increased. Mean while, Echi-nometra viridis decreased significantly between1999 and 2004, from 2 to 0.07 ind/m2 at theCARICOMP site (Fonseca et al. 2006a).

Puerto Viejo-Punta Mona: Around PuertoViejo the reefs are mostly dead due to siltation,

coral extraction for curio-trade, sewage and solidwastes. The reef at Punta Cocles (Fig. 1) had5% live coral cover in 1983, with S. siderea asthe dominant species (Corts & Guzman 1985);in 1988 live coral cover was 12.75% whilein 1995 it was 13.23.6% (Jimnez & Cortsunpbl. data). Live coral cover has continued toincrease and by 2002 it was 16% (Fernndez &Alvarado 2004). This increase was probably dueto the natural and anthropogenic protection ofthe reef; it is located far from any large sedimentsource or rivers and the local people close to thereef protect it because they consider it as partof their homes (Fernndez & Alvarado 2004).From Punta Uva to Punta Mona, the coral reefsare within the Refugio Nacional de Vida Sil-

vestre Gandoca-Manzanillo (Fig. 1), and eventhough live coral cover is low, reef conditions,in terms of species diversity and health, aregood. Fringing reefs are located around the mainrocky points, such as Punta Uva, and patch reefsin the lagoons and protected areas from directwave action. The reef off the town of Manzanilloconsisted of an incipient algal ridge (R. Steneckpers. comm.). In 1988, live coral cover overallwas around 8%; by the early 1990s, coral cover

Fig. 3. Average benthic cover (standard deviation) at Meagershoal, Cahuita National Park. Modified from Fonseca et al.

(2006a).


5/18


decreased (ca. 1%) on the algal ridge than inother sections of the reef (3.4-9%) (Jimnez &Corts unpubl. data). Offshore carbonate banksconsisted of hard substrate surrounded by sand(Corts 1992). Deep offshore walls (>25m deep)are present off Manzanillo and are colonizedby a profusion of octocorals (e.g.Ellisela spp.), platty stony corals ( Leptoseris cuculata) and barrel sponges (Xestospongia spp.) (Jimnez& Corts unpubl. data, Fonseca pers. obs.). In1999, using the AGRRA protocol, live coralcover at the forereef platform of Manzanillo wasonly 2%, recent mortality was 3%, old mortalitywas 10% and incidence of diseases was 15%(Fonseca 2003). In 2003 using the CARICOMPprotocol live coral cover at Manzanillo was just

over 7% (Table 1).

PACIFIC COAST ANDOFFSHORE ISLANDS

Baha Salinas: Located on the North Pacif-ic extreme of Costa Rica and exposed to theseasonal upwelling, the area around Salinas hasisolated, but relatively large coral communitiesmade up by Pavona gigantea. Other zooxan-

thellate corals found were Porites panamensisand a few colonies of Pavona varians. Manyazooxanthellate corals have been found: Tubas-trea coccinea, Cladopsammia eguchi, Oulangia

bradleyi, several species ofAstrangia and onespecies of Phyllangia (Corts unpubl. data).Many species of algae, octocorals, mollusks and polychaetes have been collected and are nowbeing studied.

Santa Elena: Coral reefs and communi-

ties North and South of Pennsula de SantaElena (mostly within the rea de ConservacinGuanacaste, Fig. 2) were described by Cor-ts (1996/1997). Corals found in low densitiesin other parts of the Eastern Pacific, formedsmall patch reefs there, for example Pocil-lopora eydouxi andPavona gigantea. Relativelylarge reefs frameworks built up by Pocilloporadamicornis have been found on the North sideof Pennsula de Santa Elena. Coral communi-

ties formed by mixed assemblages of species

are located on the South of Pennsula de SantaElena, protected from the full impact of the sea-sonal upwelling in the region, and from strongwave action. Live coral cover ranged from 47.5to 95.2% in 1993-94. Pocillopora damicornis predominated in the shallow sections, while Psammocora stellata predominated the deepersections.

Transects have been done on a Pocillopora

reef off Isla San Pedrillo, Islas Murcilago. Thistype of reef was characterized by very high coralcover. Data from 1995, 1996, 1997 and 2001are presented in Figure 4. Live coral cover hasstayed in the upper 80% throughout with a slightdecrease in 1997 (Jimnez unpubl. data).

Baha Culebra: The coral reefs and com-munities of this area (Fig. 2) were succinctlydescribed by Glynn et al. (1983) and by Corts& Murillo (1985), and in more detail by Jimnez

(1997, 1998, 2001a), Jimnez et al. (2001), andJimnez & Corts (2003a). Coral reefs and com-munities have been variably disturbed by natural(El Nio) and anthropogenic impacts (siltation,divers, fishers). Several coral species that werefound abundantly in Baha Culebra in the early1980s, have become rare because of extractionfor aquarium trade (Corts & Murillo 1985).Baha Culebra had rare and unique coral com-munities and reefs. One in particular, a Lepto-

seris papyracea reef suffered a high mortality

TABLE 1Average benthic cover ( standard deviation) at

Manzanillo in 2003, Gandoca-Manzanillo National Wildlife

Refuge. Modified from Fonseca (2003)

Manzanillo (n=5)

Live coral 7.243.41

Coralline algae 6.053.79

Non-coralline algae 68.808.09

Total algal cover 74.858.80

Corallimorpharians 0.000.00

Zoanthids 0.000.00

Milleporids 0.670.13

Octocorals 0.960.89

Sponges 3.420.60

Others 12.864.54


6/18


associated to the 1997/98 El Nio (Jimnez et

al. 2001), but it is recovering (Jimnez unpubl.data).

One of the reefs in Baha Culebra has beenmonitored since 1994 (Fig. 5). Average live coralcover at three depths was generally higher beforethe warming and bleaching cycle of 1997/98and didnt change significantly in the follow-ing years. The impact of the warming eventwas also evident with increasing dead coral andmacroalgae covers, with the only exception at

12m depth.Since 2003 the green algae Caulerpa sertu-lariodeshas been spreading aggressively in BahaCulebra, smothering and killing corals (Fernn-dez & Corts 2005, Jimnez unpubl. data). Theimpact ofCaulerpa on the corals was previouslyobserved in 2001 at Baha Ocotal, 6km South ofBaha Culebra, (Jimnez & Corts unpubl. data).Thick mats ofCaulerpa extended (ca. 1ha) overlive corals between 7 and 15m depth, producingbleaching and mortality of colonies. Two years

later, Caulerpa reached Baha Culebra producingextensive mortality of the corals in several areas(Jimnez et al. 2003, Fernndez 2007) , and ofthe coralPsammocora in La Penca reef (Bezy etal. 2006). Live coral cover decreased there from42.720.8% in 1995 (Jimnez 2001a) to 12.64.9% after the Caulerpa invasion (Jimnez etal. unpubl. data). In March 2005, live cover atLa Penca was still low (10.37.2%) (Bezy et al.2006). Fernndez (2007) found that the patches

of C. sertularioides increased in size during

the upwelling period, and decreased during thenon-upwelling period. But, possibly related toeutrophication, the patches were not shrinkingmuch during the non-upweeling period, cover-ing more area every year, and expanding over

the entire bay.

Pennsula de Nicoya: This large sectionof the coast has coral communities, and a fewcoral reefs (Corts & Murillo 1985). Most ofthe coast is exposed to strong wave action thatmay preclude the development of coral reefs.However, sheltered from the SW swells, there isan extensive reef, Matapalo (about 1.7km long)at the vicinities of Punta Gorda, 12km south

from Baha Culebra. Matapalo reef is dominated

Fig. 4. Average benthic cover and standard deviation on thePocillopora reef off Isla San Pedrillo, Islas Murcilago.

Fig. 5. Average benthic cover and standard deviation atGiri-giri, Baha Culebra.


7/18


by branching coral species (Pocillopora spp.),which on average have a high live cover (>50%),similar to that of Baha Culebra and Islas Mur-cilagos (Jimnez in prep.).

In another section of the coast, at Smara,small Pocillopora, and Porites lobata patchreefs had been observed. Octocorals were abun-dant on rocky outcrops, and on islands andislets off Pennsula de Nicoya. Patch reefs andcoral communities have been observed betweenCabo Blanco and the Islas Negritos (Fig. 2), insome areas growing over very extensive deadreefs. Octocorals are abundant on the IslasNegritos. Freshwater runoff in Golfo de Nicoya(Fig. 2) prevents the development of corals inits inner section of the gulf (Corts & Jimnez

2003b). Islands in the middle section of the gulf,that many years ago had corals dont have anymore because of the increase in freshwater dueto water deviation projects in the watershed.

Pacfico Central: The central section of thePacific coast of Costa Rica has few reefs (Cor-ts & Murillo 1985). Isolated corals and smallcoral communities can be found on rocky out-crops along the coast, including Parque NacionalManuel Antonio (Fig. 2). Patch reefs ofPavonaclavus have been observed to the South.

Rich coral communities have been observedand studied at Parque Nacional Marino Ballena(Alvarado 2004, 2006, Alvarado et al. 2005,2009). The main reef-builder species wasPoriteslobata, with a high live coral cover (40%) insome sites, follow by Pavona clavus (Fig. 6).Since 1992, the coral communities have beenmonitored (Fig. 7), showing a decrease in livecoral cover due mainly to the El Nio events dur-

ing the 1990s (Jimnez & Corts 2001, 2003b).After 2001, a slow recovery in coral cover hasbeen observed but also a decrease or absence ofspecies that are less resistant to sedimentation(Alvarado unpubl. data). The large fresh waterlens between Parque Nacional Marino Ballenaand Pennsula de Osa from the Trraba-Sierpemangrove complex (Fig. 2) inhibits the develop-ment of corals in that area.

Pennsula de Osa: The second largest pen-insula on the Pacific coast of Costa Rica isPennsula de Osa, on the Southeastern part ofthe country (Fig. 2). The coral communities andreefs on Pennsula de Osa were described byCorts & Jimnez (1996). A 250m2Pocillopora

Fig. 7. Percentage average live coral coverage (standarddeviation) at Rocas las Tres Hermanas, Parque NacionalMarino Ballena, 2003-2005. n= total number of transects.t= number of transects where the species was found. 0=species not found in the transects. Belt transects with 1m2

quadrat (2003-2005). Table taken from Alvarado et al.(2005).

Fig. 6. Percentage average live coral coverage (standarddeviation) at Punta Uvita, Parque Nacional Marino Ballena,1992-2005. n= total number of transects. t= number oftransects where the species was found. 0= species notfound in the transects. Chain transects (1992, 1994, 2001:Jimnez & Corts 2001, 2003), belt transects with 1m2

quadrat (2003-2005). Table taken from Alvarado et al.

(2005).


8/18


patch-reef was studied at one site and it consistedof close to 100% live coral cover ofPocilloporadamicornis in 1994. Exposed rocky substrateswere covered by octocorals, and isolated coralswere found on all rocky outcrops. The area hasnot been visited since the mid 1990s.

Golfo Dulce: This gulf is located on theSouthern part of Costa Rica, and it is about 50kmlong by 10 to 15km wide, oriented NW to SE(Fig. 2). It is an enclosed embayment of tectonicorigin, with a 60m deep sill and depths of 200min the inner section (Hebbeln et al. 1996) that areanoxic. For this reason it is described as a tropi-cal fjord (Hebbeln & Corts 2001). Several typesof coral reefs and coral communities have been

found in the gulf, and they can be divided intotwo groups, the ones of the inner section of thegulf, and the ones from the outer section (Corts1990a, b). The inner Gulf reefs are characterizedby live and deadPorites lobata on the reef frontand deadPocillopora damicornis andPsammo-cora stellata on the reef flat. Coral diversity islow and topographic relief high, with steep reef-fronts and sides. Live coral cover ranged fromless than 1% to 8% in 1987. The outer Gulf reefs

are characterized by a relatively high live coralcoverage (range from 29 to 46%), high coraldiversity, and low topographic relief (Corts1990b, Corts & Guzman 1998).

The reef structure at Punta Islotes startedgrowing 5 500 years ago over a basaltic sub-strate. Between 2 500 and 500 years ago reefgrowth was high, accumulation most of thestructure. Around 500 years ago, due to tectonicactivity, two rivers started flowing into the innerpart of Golfo Dulce, retarding and in some areas

stopping reef accretion. In the last 50 years, reefgrowth has ceased due to the increase in ter-rigenous sedimentation product of coastal andinland alteration (Corts et al. 1994).

Between 1992 and 1996 live coral cover atSndalo (outer reef) decreased from 29 to 17%,while at Punta Islotes (inner reef) it increasedfrom 2 to 10%. Dead coral dominates the sub-strate. The reef at Sndalo was greatly affectedby the sedimentation due to Hurricane Caesar

in 1996 (Fonseca et al. 2006b). The structural

balance of these reefs was negative, since bio-erosion rates were higher, 0.71kg/m2.y1 in PuntaIslotes and 2.61kg/m2.y in Sndalo, than con-struction rates, 0.41kg/m2.y in Punta Islotes and0.56kg/m2.y in Sndalo, resulting in a net reef production of -0.3kg/m2.y in Punta Islotes and-2.05kg/m2.y in Sndalo. If prevailing condi-tions continue the reef of Punta Islotes will becompletely destroyed in 6 400 years (Fonseca1999).

Isla del Cao: This island is located 15kmoffshore from Pennsula de Osa (Fig. 2), and thecoral reefs were studied by Guzman (1986). Theisland had five coral reef flats, ranging in sizefrom 0.8 to 4.2hectares. These fringing reef flats

were mainly built by dead pocilloporid corals,covered by crustose coralline algae, isolatedlive colonies of pocilloporids and poritids, andmicroatolls ofPorites lobata. The reef slope andbase was dominated by the massive coralPoriteslobata, which was the predominant species ofthe island. The shallow sections of the reef werestructured mainly by physical factors: waveaction, temperature and salinity fluctuations, andlow tide exposure. While the deeper sections

were controlled by biological interactions: bio-erosion, damselfish algal lawns, and corallivores(Guzman 1988, Guzman & Corts 1989). Thesereefs were impacted by the 1982-83 El Nio,with lost of up to 50% of the live coral coverage(Guzman et al. 1987) followed by phytoplankton blooms that killed shallow pocilloporid reefs(Guzman et al. 1990). Again, during the 1992and the 1997-1998 El Nio there was extensive bleaching but lower mortality, less than 5%.Pulses of recruitment have been observed after

the 1982-83, 1992 and 1997-98 El Nio events(Guzman & Corts 2001).

Between 1992 and 1996, live coral at asite on the North side of the island, 10m deep,decreased from 30 to 24%, and dead coralwas the dominant substrate category (Fonsecaet al. 2006b). However, this reef was still aconstructive reef with a net production of2.76kg CaCO3/m

2/year, and bioerosion ratesbeing very low 0.002kg CaCO3/m

2/year (Fon-

seca 1999).


9/18


Isla del Coco: This island is approximately500km southwest of Costa Rica mainland (Cor-ts 2008). It had the highest number of zooxan-thellate corals (17 spp.) on the Pacific of CostaRica (Corts & Guzman 1998). Isla del Cocoalso had the highest number of azooxanthellatecorals, but more than half of this corals werecollected in deep waters (Cairns 1991, Cortsunpubl. data). Fringing reefs ranging in sizefrom less than one hectare to more than 50 hect-ares grew around Isla del Coco. Most of the reefswere constructed byPorites lobata (Bakus 1975,reported as Porites californica) but there werealso extensive zones of agariciids: Pavona spp.and Gardineroseris planulata. Macintyre et al.(1992) found that the largest colonies ofPorites

lobata were between 25050 and 43080 yearsold, but it is probaly an underestimation of theage the bases of the large colonies bioeroded.Most of the coral died during the 1982-1983 ElNio, in 1987 live coral cover was between 2.6and 3.5% (Guzman & Corts 1992). The feedingand erosional activity of the sea urchinDiademamexicanum was concentrated on surviving indi-viduals of the 1982-83 El Nio.

In 2002, Isla del Coco was visited again.Reefs that previously had high densities ofD.mexicanum were almost complete bioeroded,while reefs that in the 1980s had a high numberof coral recruits and had high coral cover in2002. Live coral cover of several species hasincreased to 23% (Fig. 8) and one species, Lep-toseris scabra, not seen before, was present andvery abundant in some reefs (Guzman & Corts2007).

Populations of corallivores were evaluatedin the late 1980s and again in 2002. The density

ofA. planci did not exhibit a significant change between surveys while the density ofAro-thron meleagris increased significantly overall between 1987 and 2002. The overall averageofD. mexicanum significantly decreased at allreefs, from 14.5 ind/ha in 1987 to 0.84 ind/ha in2002 (Guzman & Corts 2007) (Fig. 9).

STATUS OF CORAL REEF FISHES

Caribbean: Using a rapid visual tech-nique, Phillips & Perez-Cruet (1984), found 49species of reef fishes at Cahuita. They indicatedthat diversity was lower at Cahuita than at otherCaribbean reefs, and attribute this differenceto the declining state of the reef at Cahuita.Fonseca & Gamboa (2003) found 35 species

Fig. 8. Mean percent live coral cover (standard error) bygenera in 1987 and 2002 at Isla del Coco (adapted fromTable 1 in Guzman & Corts 2007).

Fig. 9. Population mean (SE) density comparisons of thecorallivores Acanthaster planci and Arothron meleagris(ind/ha1) and of the sea urchin Diadema mexicanum (ind/m2) in 1987 and 2002 at Isla del Coco (adapted from Table2 in Guzman & Corts 2007). Sample size units (n) arenumber of censuses for corallivores, m2 forDiadema, andnumber of reefs for grand mean.


10/18


of reef fishes in transects done at Cahuita. Fishdensity, size and diversity were higher in theshallow sites that have higher structural com-plexity, coral cover and macroalgae abundance(Fonseca & Gamboa 2003, AGRRA protocol,sampling done in 1999). Damselfishes (mainlyStegastes fuscus andAbudefduf saxatilis) werethe most abundant species in shallow (


11/18


drop in coral cover from 1980 to 1993 (Wyck-off & Corts unpubl. data).

Pollution:The coastal zone between Porteteand Limn (Fig. 1) are polluted with fecal wastesand garbage, mainly from banana plantations andcoastal towns. Analysis between 1981 and 1985of petroleum pollution indicated that the levelswere relatively low, with sporadic events of highconcentrations. The highest concentrations werefound in the port areas (Mata et al. 1987). In astudy done between 2000 and 2002 in the Limnarea, the level of petroleum pollution was stilllow (Acua-Gonzlez et al. 2004). High levelsof heavy metal pollution in coral skeletons andsediments from reefs, even in pristine reefs

were found by Guzman & Jimnez (1992). Thesources of the heavy metals may be natural, butmainly they are of anthropogenic origin, includ-ing sewage discharges, oil spills (from refineriesand tankers), the misuse of agricultural chemi-cals and fertilizers, and topsoil erosion (Guzman& Garca 2002). Garca-Cspedes et al. (2004)studying trace metals in several coastal areasof Costa Rica, found highest levels of lead inLimn, and intermediate levels of iron, zinc, andcopper. Concentrations of PBCs are low in theLimn area (Spongberg 2004).

Impact of tourism: Tourist visitation to theCaribbean coast of Costa Rica, as well as coastaldevelopment has increased enormously in thelast two decades. This activity has had an impacton the coral reefs of the region, due to tramplingof corals and other organisms on the lagoon, andkicking of corals during diving (Corts 1994,Gove & Corts unpubl. data).

PACIFIC COAST ANDOFFSHORE ISLANDS

Siltation: Terrigenous sediments haveaffected several reefs on the Pacific coast (Cor-ts & Murillo 1985), at Baha Culebra (Jimnez1998), at Parque Nacional Marino Ballena(Alvarado 2006) and at Golfo Dulce (Corts1990a, b, 1991, Corts et al. 1994, Fonseca

1999, Fonseca et al. 2006b). Sedimentation

has increased because of deforestation of thewatersheds, road and tourist complexes con-structions, and inappropriate agricultural prac-tices (Corts 1990a, b, Jimnez 1998, Alvarado2004, 2006). A significant reduction in reefaccretion can be observed in reef cores fromGolfo Dulce (Fig. 2), and it has been attributedto recent terrigenous sedimentation (last 50years) as the area was deforested for bananaplantation (Corts et al. 1994, Fonseca 1999).

Extraction of reef organisms: Some spe-cies of corals had been extracted for the localcurio trade. The populations ofPocilloporaeydouxi and ofP. meandrina, both very attrac-tive branching coral have been reduced because

of exploitation (Glynn 1979, Corts & Murillo1985). Extraction of reef fish has severelyimpacted the populations of some regions(Dominici-Arosemena 1999, Dominici-Arose-mena et al. 2005).

Tourism: Coral reefs on the Pacific sideof Costa Rica have become important for div-ing tourism. Touristic activity has direct andindirect effects on the coral reefs (Corts &Murillo 1985, Jimnez 1997, 2001a). Directeffects included: coral extraction and damageto colonies by divers and boat anchors. Indirecteffects included: over-exploitation of resources(fish, lobster, mollusks) increased sewage andincreased sediment loads from coastal altera-tion (urbanization, road construction).

Pollution: Levels of pollution, e.g. PCB,trace metals and petroleum hydrocarbons arelow in Isla del Cao, Baha Culebra, and Golfo

Dulce, with the exception of PCBs, which werehigh in Golfo Dulce (Acua & Murillo 1987,Acua-Gonzlez et al. 2004, Garca-Cspedeset al. 2004, Spongberg 2004).

CURRENT AND POTENTIALCLIMATE CHANGE IMPACTS

In June 1983 water temperatures along theCaribbean coast of Costa Rica were between

29 and 35C, causing bleaching and death of


12/18


reef organisms (Corts et al. 1984). One of themost affected species was Acropora palmata,which combined with a Caribbean-wide whiteband epidemic, eliminated most colonies fromthe region (Gladfelter 1982, Brukner 2003). InCahuita, most of the colonies died and recov-ery has been slow (Corts et al. 1984, Corts1992). More bleaching events were observedin 1992, 1995, 1998, and 2005 (Fonseca &Nielsen unpubl. data), all coincident with highwater temperature. The 1995 bleaching eventwas particularly severe, affecting and killingseveral coral species (Jimnez 2001b).

The main natural disturbance affecting coralreefs of the Pacific of Costa Rica had been El Nio warming events. During the 1982-83 El

Nio there was extensive coral bleaching (Cortset al. 1984), resulting in coral death of up to 50%at Isla del Cao (Guzman et al. 1987), and around90% at Isla del Coco (Guzman & Corts 1992).The localities with higher mortality had greatersea surface temperature anomalies, longer lengthof warming, and faster rate of warming (Glynnet al. 1988). Again in 1992 and 1997-1998 therewas extensive bleaching of corals, due to warm-ing events. But, in both occasions mortality was

lower and recovery was faster than in 1982-83(Guzman & Corts 2001, Jimnez et al. 2001,Jimnez & Corts 2001, 2003b).

Coral reefs at Isla del Cao (Fig. 2) wereaffected during severe phytoplankton blooms in1985, maybe associated with La Nia. Mass mor-tality of corals occurred during the bloom downto a depth of 3m. Mortality due to the dinofla-gellate bloom completely eliminated some coralspecies from shallow reef zones (Guzman et al.1990). Also related to phytoplankton blooms,

extensive bleaching and partial mortality wereobserved in 2004 at Baha Culebra where thebloom affected mostly pavoniid corals (Jimnezet al. unpubl. data) and at Santa Elena, wheremortality of pocilloporids were observed aftera bloom produced mainly by Cochlodinoiumpolykrikoides (Vargas et al. in prep.).

Mid-day low tidal exposure of EasternPacific reefs during La Nia years causes exten-sive mortality of reef-flat organisms (Eakin &

Glynn 1996). Mortality due to low tides had

been observed at Isla del Cao (Guzman 1986)and Corcovado (Corts & Jimnez 1996).

MARINE PROTECTED AREAS,MONITORING, AND CONSERVATION

MANAGEMENT CAPACITYCARIBBEAN

Marine Protected Areas on the Caribbeancoast with coral reefs are: Parque NacionalCahuita (National Park) and Refugio Nacio-nal de Vida Silvestre Gandoca-Manzanillo(National Wild Life Refuge) (Fig. 1). Monitor-ing of the Cahuitas seagrasses and coral reefshas been going on since 1999 following the

CARICOMP protocol Level I (Fonseca et al.2006a). Monitoring has been initiated at thereefs at Gandoca-Manzanillo and Isla Uvitawith funding from the STA-GCRMN node.

Within the protected areas there is noextraction of corals or live rock, but artisanalfishing is still active in some cases due to localsocial problems, and in others due to lack ofcontrol. Tourism activities began their regula-tion at Parque Nacional Cahuita, but not forother areas.

PACIFIC

There are only three protected areas onthe Pacific coast of Costa Rica with the marineenvironment as their main focus of protec-tion, Parque Nacional Marino Las Baulas (LasBaulas National Marine Park), Parque Nacio-nal Marino Ballena (Ballena National MarinePark) and rea de Conservacin Marina Isla

del Coco (Isla del Coco Marine ConservationArea) (Fig. 2). Other coral reefs areas are pro-tected in the marine portions of parks or con-servation areas, from North to South: , ParqueNacional Santa Rosa, Reserva Absoluta CaboBlanco (Absolute Reserve), Parque NacionalManuel Antonio, Reserva Biolgica Isla delCao (Biological Reserve), and Parque Nacio-nal Corcovado (Fig. 2).

Monitoring is going on at Isla del Cao,

Parque Nacional Marino Ballena, and is starting


13/18


at Isla del Coco. Another area that is beingmonitored is Baha Culebra (Fig. 2), and thereare plans to monitor the reefs of Golfo Dulce inthe South, but these last two are not protectedareas. A national coral reef monitoring plan isbeing developed at the present time (2009).

Within the protected areas there is noextraction of corals or live rock, but there isstill reef fish extraction fishing going on atrea de Conservacin Guanacaste. Commer-cial fishing has been controlled in most parks,but it still goes on at the outer marine limits ofthe protected areas, that should be consideredas buffer zones. Tourism is being regulatedat Isla del Cao and Isla del Coco, but not inother areas.

GOVERNMENT POLICIES,LAWS AND LEGISLATION

The Costa Rican government does nothave any specific policy regarding coral reefs(Cajiao- Jimnez 2003) or monitoring activi-ties. There are laws regulating the activityin the coastal zone, pollution inland and sea,fisheries, wildlife protection, and biodiver-

sity use and conservation. All touch coralreefs indirectly, which is the first problem,and second, each one is enforced by a dif-ferent government institution. This results inlack of enforcement, institutional overlap andnegligence. Only the Ministerio de Ambientey Energa (MINAE, Ministry of the Environ-ment), through its Sistema Nacional de reasde Conservacin (SINAC, National System ofConservation Areas) protects the coral reefsinside protected areas.

A decree banning the extraction of coralsand other reef organisms in Costa Rican waterswas drafted and submitted in September 2005but has not been signed. If this decree is signedcorals and many other reefs organisms, e.g.sponges, non-commercial molluscs, and octoc-orals, among others, could only be collected forscientific research.

GAPS IN CURRENT MONITORING ANDCONSERVATION CAPACITY

Coral reef monitoring is restricted to onesite on the Caribbean (Parque Nacional Cahu-ita) and two on the Pacific coast: Baha Culebra

and Isla del Cao. But on the Caribbean, twonew reefs at Refugio Nacional de Vida Silves-tre Gandoca-Manzanillo and Isla Uvita werestarted. On the Pacific, the reefs at Islas Mur-cilago, Golfo Dulce, and at Isla del Coco needto be included. A national coral reef monitoredprogram should be implemented and financialsupport included.

Conservation capacity is moderate becauseof finite funding. With the exception of Isla del

Coco, protection of coral reefs is restricted tothe immediate areas that the park rangers canwatch from the post. To aggravate the problemof coral reef conservation, in many cases thecauses of reef degradation originate outsidethe parks boundary, e.g., sediments comingdown from deforested mountains of adjacentwatersheds; or coral death is due to El Niowarming events.

CONCLUSIONS ANDRECOMMENDATIONS FORCORAL REEF CONSERVATION

Costa Rica has coral reefs on the Caribbeanand Pacific coasts (coast and off-shore islands).Most reefs are within protected areas, but man-agement and conservation is limited because ofinadequate funding, and because some of themain problems are natural (warming events)or originate outside the protected areas (sedi-

ments from adjacent watersheds). Outside theprotected areas there are regulations to improveland use, for example, the need of keeping abelt of forest along rivers, but this is not alwaysapplied. This has resulted in degraded reefs inseveral areas due to chronic siltation, for exam-ple, Cahuita, Parque Nacional Marino Ballenaand Golfo Dulce. In other areas, especially on


14/18


the Pacific live coral has been significantlyreduced in the last two decades due to El Nio.In general terms the coral reefs of Costa Ricaare recovering, but the degree of human activ-ity directly affect this recovery.

Extraction of any kind of reef organisms,including the so called live rock must becompletely prohibited and banned in all reefareas, or at least within the protected areas.

Tourism and fishing in coral reefs areasmust be regulated and dive sites designatedfollowing scientific criteria to define the carry-ing capacity. Reef sites should be permanentlymarked with mooring buoys. A diving eti-quette, with coral conservation and protectionas its main objective, must be elaborated and

implemented. Fishing of any kind should notbe allowed in protected areas.New marine conservation projects should

include the surrounding areas or buffer zones,specially the large watersheds, to stop or reducethe input of sediments and pollutants. Also,more outreach to the general public, directand indirect users of the reef, and governmentofficials is needed. The categories of marineprotection should be redefined or updated from previous management plans, considering thecurrent knowledge on integrated coastal andmarine management. The conclusions of theconservation gap analysis recently published(SINAC 2009) must be implemented, withthe expansion and creation of new marineprotected areas, and the implementation of thenew protection categories (Executive Decree34433). Governamental jurisdiction outsidemarine protected areas, inland and offshore,should be defined in order to acquire a higher

institutional compromise.

ACKNOWLEDGMENTS

Funding was provided by the Vicerrec-tora de Investigacin, Universidad de CostaRica; Consejo Nacional de InvestigacionesCientficas y Tecnolgicas (CONICIT); UNEPCaribbean Monitoring Project through theSTA-GCRMN node at INVEMAR, Colom-

bia; Ecodesarrollo Papagayo; and M. Tupper.

Logistic support was provided by the Centrode Investigacin en Ciencias del Mar y Lim-nologa (CIMAR, UCR); Hotel Ecoplaya; Ins-tituto Costarricense de Turismo (ICT); SistemaNacional de reas de Conservacin (SINAC);and UnderSea Hunter. The reviews by Ian G.Macintyre, Tim Rixen, and especially HctorGuzman are geatly appreciated.

RESUMEN

Costa Rica tiene comunidades coralinas y arrecifes enla costa Caribe y del lado Pacfico a lo largo de la costa yen islas mar afuera). Arrecifes de franja y de parche, bancoscarbonatados y una cresta de algas coralinas incipiente estn

presentes en la seccin sur de la costa Caribe. Comunidadescoralinas, arrecifes y colonias de coral aisladas se encuentran

a lo largo de todo el Pacfico de Costa Rica. Los arrecifescoralinos han sido impactados seriamente en los ltimos 30aos, principalmente por sedimentos en el Caribe y algunosarrecifes del Pacfico, y por el calentamiento durante elFenmeno de El Nio-Oscilacin Surea en el Pacfico. Tressitios en el Caribe y otros tres en el Pacfico estn siendomonitoreados. Despus de reducciones significativas en lacobertura de coral vivo en la dcada de 1980, tanto en elCaribe como en el Pacfico, la mayora de los arrecifes se estrecuperando. El gobierno de Costa Rica es consciente de laimportancia de los arrecifes coralinos y de otros ecosistemasmarinos, y en aos recientes han implementado (o estn en

proceso de aprobacin) varios decretos para la proteccin delos arrecifes. Pero, hay limitacin de fondos y personal parasu adecuado manejo y proteccin. Se necesita ms divulga-cin de informacin sobre los arrecifes coralinos al pblicoen general y usuarios de los mismos; de nuevo, la limitacinde fondos restringe lo que se puede hacer.

Palabras clave: arrecifes coralinos, Costa Rica, monito-reo, GCRMN, conservacin, manejo.

REFERENCES

Acua, J.A. & M.M. Murillo. 1987. La contaminacin porhidrocarburos de petrleo en la Isla del Cao. Ing.Cienc. Qum. 11: 95-98.

Acua-Gonzlez, J.A., J.A. Vargas-Zamora, E. Gmez-Ramrez & J. Garca-Cspedes. 2004. Hidrocarburosde petrleo, disueltos y dispersos, en cuatro ambientescosteros de Costa Rica. Rev. Biol. Trop. 52: 43-50.

Alvarado, J.J. 2004. Descripcin de las comunidades arre-cifales del Parque Nacional Marino Ballena, Pacficocentral-sur de Costa Rica. Tesis de Licenciatura, Uni-

versidad de Costa Rica. San Pedro, Costa Rica.


15/18


Alvarado, J.J. 2006. Factores fsico-qumicos y biolgicosque median en el desarrollo de los arrecifes y comuni-dades coralinas del Parque Nacional Marino Ballena,Pacfico sur, Costa Rica. Master Thesis, Universidadde Costa Rica. San Pedro, Costa Rica.

Alvarado, J.J., J. Corts & E. Salas. 2004. Status of the sea

urchinDiadema antillarum Philippi (Echinodermata:Echinoidea) at Cahuita National Park (1977-2003),Costa Rica. Carib. J. Sci. 40: 257-259.

Alvarado, J.J., J. Corts, C. Fernndez & J. Nivia. 2005.Coral communities and reefs of Ballena Marine

National Park, Pacific coast of Costa Rica. Cienc.Mar. 31: 641-651.

Alvarado, J.J., C. Fernndez & J. Corts. 2009. Water qua-lity conditions on coral reefs at the Marino Ballena

National Park, Pacific Costa Rica. Bull. Mar. Sci.84: 137-152.

Bakus, G.J. 1975. Marine zonation and ecology of CocosIsland, off Central America. Atoll Res. Bull. 179:1-11.

Bezy, M.B., C. Jimnez, J. Corts, A. Segura, A. Len, J.J.Alvarado, C. Gilln & E. Meja. 2006. Contrasting

Psammocora-dominated coral communities in CostaRica, Tropical Eastern Pacific. Proc. 10th Int. CoralReef Symp. 1: 376-381.

Bruckner, A.W. 2003. Proceedings of the CaribbeanAcro-

pora Workshop: Potential application of the U.S.endangered species act as a conservation strate-gy. NOAA Technical Mem. NMFS-OPR-24, SilverSprings, Maryland, USA.

Cairns, S.D. 1991. A revision of the ahermatypic Scleractiniaof the Galpagos and Cocos Islands. Smithson. Contr.Zool. 504: 1-33.

Cajiao-Jimnez, M.V. 2003. Rgimen legal de los recursosmarinos y costeros en Costa Rica. Editorial IPECA,San Jos Costa Rica.

Corts, J. 1981. The coral reef at Cahuita, Costa Rica, a reefunder stress. Master Thesis, McMaster University,Hamilton, Ontario, Canada.

Corts, J. 1990a. Coral reef decline in Golfo Dulce, CostaRica, Eastern Pacific: anthropogenic and natural dis-turbances. Ph.D. Dissertation, University of Miami,Miami, Florida, USA.

Corts, J. 1990b. The coral reefs of Golfo Dulce, Costa Rica:Distribution and community structure. Atoll Res. Bull.344: 1-37.

Corts, J. 1991. Los arrecifes coralinos de Golfo Dulce,Costa Rica: aspectos geolgicos. Rev. Geol. Amr.Central 13: 15-24.

Corts, J. 1992. Los arrecifes coralinos del Refugio Nacionalde Vida Silvestre Gandoca-Manzanillo, Limn, CostaRica. Rev. Biol. Trop. 40: 325-333.

Corts, J. 1994. A reef under siltation stress: a decade ofdegradation, p. 240-246.In R.N. Ginsburg (compiler).Proc. Colloquium on global aspects of coral reefs:Health, hazards and history, 1993. RSMAS, Universityof Miami, Miami, Florida, USA.

Corts, J. 1996/1997. Comunidades coralinas y arrecifes delrea de Conservacin Guanacaste, Costa Rica. Rev.Biol. Trop. 44/45: 623-625.

Corts, J. 1998. Componente Marino, p. 1-24. In J.A.

Vargas (ed.) Planificacin y manejo de bahas y reascosteras fuertemente contaminadas del Gran Caribe.Estudio de caso: Puerto Limn, Costa Rica. InformeFinal, Proyecto Regional GEF/RLA/G41.

Corts, J. 2008. Historia de la investigacin marina de laIsla del Coco, Costa Rica. Rev. Biol. Trop. 56 (Suppl.2): 1-18.

Corts, J. & H.M. Guzman. 1985. Arrecifes coralinos de lacosta Atlntica de Costa Rica. Brenesia 23: 275-292.

Corts, J & H.M. Guzman. 1998. Organismos de los arreci-

fes coralinos de Costa Rica: Descripcin, distribucingeogrfica e historia natural de los corales zooxantela-dos (Anthozoa: Scleractinia) del Pacfico. Rev. Biol.Trop. 46: 55-92.

Corts, J. & C.E. Jimnez. 1996. Coastal-marine environ-ments of Parque Nacional Corcovado, Puntarenas,Costa Rica. Rev. Biol. Trop. 44: 35-40.

Corts, J. & C.E. Jimnez. 2003a. Past, present and futureof the coral reefs of the Caribbean coast of CostaRica, p. 223-239. In J. Corts (ed.). Latin American

Coral Reefs. Elsevier Science B.V., Amsterdam, TheNetherlands.

Corts, J. & C.E. Jimnez. 2003b. Corals and coral reefsof the Pacific of Costa Rica: History, research andstatus, p. 361-385.In J. Corts (ed.). Latin Americancoral reefs. Elsevier Science B.V., Amsterdam, The

Netherlands.

Corts, J. & M.M. Murillo. 1985. Comunidades coralinas yarrecifes del Pacfico de Costa Rica. Rev. Biol. Trop.33: 197-202.


16/18


Corts, J. & M.J. Risk. 1984. El arrecife coralino del Parque Nacional Cahuita, Costa Rica. Rev. Biol. Trop. 32:109-121.

Corts, J. & M.J. Risk. 1985. A reef under siltation stress:Cahuita, Costa Rica. Bull. Mar. Sci. 36: 339-356.

Corts, J., M.M. Murillo, H.M. Guzman & J. Acua. 1984.Prdida de zooxantelas y muerte de corales y otrosorganismos arrecifales en el Atlntico y Pacfico deCosta Rica. Rev. Biol. Trop. 32: 227-231.

Corts, J., R. Soto, C. Jimnez & A. Astorga. 1992. Deathof intertidal and coral reef organisms as a result of a7.5 earthquake. Proc. 7th Int. Coral Reef Symposium1: 235-240.

Corts, J., I.G. Macintyre & P.W. Glynn. 1994. Holocenegrowth history of an Eastern Pacific fringing reef,Punta Islotes, Costa Rica. Coral Reefs 13: 65-73.

Corts, J., A.C. Fonseca, M. Barrantes & P. Denyer. 1998.Type, distribution and origin of sediments of the Gan-doca-Manzanillo National Wildlife Refuge, Limn,Costa Rica. Rev. Biol. Trop. 46: 251-256.

Dominici-Arosemena, A. 1999. Estructura poblacional delos peces de arrecifes del Golfo de Papagayo, Gua-nacaste, con nfasis en las especies de mayor impor-tancia comercial como ornamentales. Master Thesis,University of Costa Rica, San Pedro, Costa Rica.

Dominici-Arosemena, A., E. Brugnoli-Olivera, J. Corts- Nez, H. Molina-Urea & M. Quesada-Alpzar.2005. Community structure of Eastern Pacific reeffishes (Gulf of Papagayo, Costa Rica). Tecnociencia7: 19-41.

Eakin, C.M. & P.W. Glynn. 1996. Low tidal exposure andreef mortalities in the Eastern Pacific. Coral Reefs15: 120.

Fernndez, C. 2007. Propagacin del alga Caulerpa sertu-larioides (Chlorophyta) en Baha Culebra, Golfo dePapagayo, Pacfico norte de Costa Rica. Master The-sis, University of Costa Rica. San Pedro, Costa Rica.

Fernndez, C. & J.J. Alvarado. 2004. El arrecife coralinode Punta Cocles, costa Caribe de Costa Rica. Rev.Biol. Trop. 52: 121-129.

Fernndez, C. & J. Corts. 2005. Caulerpa sertularioides,a green alga spreading aggressively over coral reefcommunities in Culebra Bay, North Pacific of CostaRica. Coral Reefs, Reef Site 24: 10.

Fonseca E., A.C. 1999. Bioerosin y bioacrecin en arreci-

fes coralinos del Pacfico sur de Costa Rica. Master

Thesis, University of Costa Rica, San Pedro, CostaRica.

Fonseca E., A.C. 2003. A rapid assessment at CahuitaNational Park, Costa Rica, 1999 (Part 1: stony coralsand algae). Atoll Res. Bull. 496: 248-257.

Fonseca E., A.C. & C. Gamboa. 2003. A rapid assessmentat Cahuita National Park, Costa Rica, 1999 (Part 2:reef fishes). Atoll Res. Bull. 496: 258-267.

Fonseca E., A. C., E. Salas & J. Corts. 2006a. Monitoreodel arrecife coralino Meager Shoal, Parque NacionalCahuita (sitio CARICOMP). Rev. Biol. Trop. 54:755-763.

Fonseca E., A.C., H.K. Dean and J. Corts. 2006b. Non-colonial macro-borers as indicators of coral reefstatus in the South Pacific of Costa Rica. Rev. Biol.

Trop. 54: 101-115.

Garca-Cspedes, J., J.A. Acua-Gonzlez & J.A. Vargas-Zamora. 2004. Metales traza en sedimentos de cuatroambientes costeros de Costa Rica. Rev. Biol. Trop.52: 51-60.

Gladfelter, W.B. 1982. White-band disease in Acroporapalmata: implications for the structure and growth ofshallow reefs. Bull. Mar. Sci. 32: 639-643.

Glynn, P.W. 1979. Climatic cycles may affect reef growth.

Smithsonian Tropical research Institute, Cont. Res26: 4.

Glynn, P.W., E.M. Druffel & R.B. Dunbar. 1983. A deadCentral American coral reef tract: possible link with theLittle Ice Age. J. Mar. Res. 41: 605-637.

Glynn, P.W., J. Corts, H.M. Guzman & R.H. Richmond.1988. El Nio (1982-83) associated coral mortality andrelationship to sea surface temperature deviations inthe Tropical Eastern Pacific. Proc. 6th Int. Coral ReefSymposium 3: 237-243.

Guzman, H.M. 1986. Estructura de la comunidad arrecifalde la Isla del Cao, Costa Rica, y el efecto de perturba-ciones naturales severas. Master Thesis, University ofCosta Rica, San Pedro, Costa Rica.

Guzman, H.M. 1988. Distribucin y abundancia de organis-mos coralvoros en los arrecifes coralinos de la Isla delCao, Costa Rica. Rev. Biol. Trop. 36: 191-207.

Guzman, H.M. & J. Corts. 1989. Coral reef communitystructure at Cao Island, Pacific Costa Rica. P.S.Z.N.I:

Mar. Ecol. 10: 23-41.


17/18


Guzman, H.M. & J. Corts. 1992. Cocos Island (Pacific ofCosta Rica) coral reefs after the 1982-83 El Nio dis-turbance. Rev. Biol. Trop. 40: 309-324.

Guzman, H.M. & J. Corts. 2001. Changes in reef commu-nity structure after fifteen years of natural disturban-ces in the Eastern Pacific (Costa Rica). Bull. Mar.

Sci.: 69: 133-149.

Guzman, H.M. & J. Corts. 2007. Reef recovery 20-yr afterthe 1982-83 El Nio massive mortality. Mar. Biol.151: 401-411.

Guzman, H.M. & E.M. Garca. 2002. Mercury levels in coralreefs along the Caribbean coast of Central America.Mar. Poll. Bull. 44: 1415-1420.

Guzman, H.M. & C.E. Jimnez. 1992. Contamination ofcoral reefs by heavy metals along the Caribbean coastof Central America (Costa Rica and Panama). Mar.

Poll. Bull. 24: 554-561.

Guzman, H.M., J. Corts, R.H. Richmond & P.W. Glynn.1987. Efectos del fenmeno de El Nio-OscilacinSurea 1982/83 en los arrecifes de la Isla del Cao,Costa Rica. Rev. Biol. Trop. 35: 325-332.

Guzman, H.M., J. Corts, P.W. Glynn & R.H. Richmond.1990. Coral mortality associated with dynoflagellate

blooms in the eastern Pacific (Costa Rica and Panama).Mar. Ecol. Prog. Ser. 60: 299-303.

Hebbeln, D. & J. Corts. 2001. Sedimentation in a tropicalfjord: Golfo Dulce, Costa Rica. Geo-Mar. Lett. 20:142-148.

Hebbeln, D., D. Beese & J. Corts. 1996. Morphology andsediment structure in Golfo Dulce, Costa Rica. Rev.Biol. Trop. 44: 1-10.

Jimnez, C.E. 1997. Corals and coral reefs of Culebra Bay,Pacific coast of Costa Rica: anarchy in the reef. Proc.8th Int. Coral Reef Symposium 1: 329-334.

Jimnez, C.E. 1998. Arrecifes y comunidades coralinas de

Baha Culebra, Pacfico norte de Costa Rica (Golfode Papagayo). Master Thesis, University of CostaRica, San Pedro, Costa Rica.

Jimnez, C.E. 2001a. Arrecifes y ambientes coralinos deBaha Culebra, Pacfico de Costa Rica: aspectos

biolgicos, econmico-recreativos y de manejo. Rev.Biol. Trop. 49: 215-231.

Jimnez, C.E. 2001b. Bleaching and mortality of reeforganisms during a warming event in 1995 at theCaribbean coast of Costa Rica. Rev. Biol. Trop. 49:233-238.

Jimnez, C.E. & J. Corts. 2001. Effects of the 1991-92El Nio on scleractinian corals of the central Pacificcoast of Costa Rica. Rev. Biol. Trop. 49: 239-250.

Jimnez, C.E. & J. Corts. 2003a. Growth of seven speciesof scleractinian corals in an upwelling environment ofthe eastern Pacific (Golfo de Papagayo, Costa Rica).

Bull. Mar. Sci. 72: 187-198.

Jimnez, C.E. & J. Corts. 2003b. Coral cover changeassociated to El Nio, eastern Pacific, Costa Rica,1992-2001. P.S.Z.N.: Mar. Ecol. 24: 179-192.

Jimnez, C.E., J. Corts, A. Len & E. Ruiz. 2001. Coral bleaching and mortality associated with El Nio1997/98 event in an upwelling environment at theEastern Pacific (Gulf of Papagayo, Costa Rica). Bull.Mar. Sci. 69: 151-169.

Jimnez, C., J. Corts & E. Ruiz. 2003. Re-evaluacin

de los ambientes coralinos de Baha Culebra (1994-2003). Ecodesarrollo Papagayo, unpubl. rept. 27 p.

Lessios, H.A., D.R. Robertson & J.D. Cubit. 1984. SpreadofDiadema mass mortality through the Caribbean.Science 226: 335-337.

Macintyre, I.G., P.W. Glynn & J. Corts. 1992. Holocenereef history in the Eastern Pacific: mainland CostaRica, Cao Island, Cocos Island, and GalpagosIslands. Proc. 7th Int. Coral Reef Symp. 2: 1174-1184.

Mata, A., J.A. Acua, M.M. Murillo & J. Corts. 1987. Lacontaminacin por petrleo en el Caribe de Costa Rica:1981-1985. Carib. J. Sci. 23: 41-49.

McCreary, J.P., H.S. Lee & D.B. Enfield. 1989. Theresponse of the coastal ocean to strong offshorewinds, with application to circulations in the Gulfs ofTehuantepec and Papagayo. J. Mar. Res. 47: 81-109.

Murillo, M.M. & J. Corts. 1984. Alta mortalidad en la poblacin del erizo de mar Diadema antillarum enel Parque Nacional Cahuita, Limn, Costa Rica. Rev.

Biol. Trop. 32: 167-169.

Myhre, S. & A. Acevedo-Gutirrez. 2007. Recovery of seaurchin Diadema antillarum populations is correlatedto increase coral cover and reduced macroalgal cover.Mar. Ecol. Prog. Ser. 329: 205-210.

Phillips, P.C. & M. Perez-Cruet. 1984. A comparison surveyof reef fishes in Caribbean and Pacific Costa Rica. Rev.Biol. Trop. 32: 95-102.

Risk, M.J., M.M. Murillo & J. Corts. 1980. Observacionesbiolgicas preliminares sobre el arrecife coralino en el


18/18


Parque Nacional Cahuita, Costa Rica. Rev. Biol. Trop.28: 361-382.

SINAC (Sistema Nacional de reas de Conservacin). 2009.GRUAS II: Propuesta de Ordenamiento Territorial

para la conservacin de la biodiversidad en Costa Rica.Vol. III. Anlisis de vacos en la representatividad e

integridad de la biodiversidad de los sistemas marinosy costeros. San Jos, Costa Rica. 60 p.

Spongberg, A.L. 2004. PCB Contamination in surfacesediments in the coastal waters of Costa Rica. Rev.Biol. Trop. 52: 1-10.

Valdez, M.F. & C.R. Villalobos. 1978. Distribucinespecial, correlacin con el sustrato y gradode agregacin en Diadema antillarum Philippi

(Echinodermata: Echinoidea) Rev. Biol. Trop. 26:237-245.

Documents

Status and conservation of coral reefs in Costa Rica