Annual Review of WCS Coral Reef Programs 2003-04

Prepared by - T.R. McClanahan

The Wildlife Conservation Society (WCS) has maintained programs in coral reef conservation science since 1981 and currently has three major regions of study: the western Indian Ocean, with most projects focused on the fringing reefs of Kenya; the Meso-American Barrier Reef, with projects focused on Glovers reef atoll Belize; and the high diversity reefs in Indonesia and Papua New Guinea.  A program in Madagascar has recently been in development and is part of the western Indian Ocean program. In addition the Society has a coral research lab at the Osborne Aquarium and Columbia University in New York City.  The major objectives of the programs are: 1) to determine the effects of marine parks, global climate change, fishing, and indigenous management on fisheries catches and species diversity and reef ecology, 2) to develop methods to restore coral reefs that have been degraded by over fishing, pollution, or coral bleaching, 3) to assist the organization of relevant government agencies and social organizations in developing sustainable resource use for coral reefs, 4) to foster the professional development and training of marine scientists in coral reef ecology and management practices, and 5) contribute to the coordination and general development of coral reef conservation and science in the tropics. Depending on the major threats and needs for conservation science in each region these foci differ slightly between study sites and over time.   Below is a brief description of the major foci and some findings from each of the regions in the 2003-2004 fiscal year followed by a list of research published during this year. 

Kenya’s fringing reef

Coral reefs in Kenya have been monitored since 1987 and work this year continued to focus on the response of these reefs to the 1998 coral bleaching and mortality and the 2002 “fungal disease” events.  This included studies of the response of the algae, coral, and fish taxa to the coral mortality and the factors that influence recovery. The work in Kenya continued the long-term goals of monitoring coral reefs in the marine parks and fished reefs, monitoring water quality and coral tissue, and monitoring fish catch in southern Kenya.  Short-term projects during this year included field surveys of northern Tanzania and Mauritius to evaluate the status of fisheries management systems in these two areas and the effects of coral bleaching and climate change.  Short-term projects included a survey of marine park stakeholders, evaluation of an offshore fishing alternative, the ring net, and effects of shipwrecks on fish enhancement and catches.  Below is a brief description of some of the key findings.

Climate change and reef ecology

An ongoing study is examining the changes in the algal symbionts that live in corals associated with background and changing water temperatures.  Samples are being monitored quarterly in Kenya and collected along geographic and environmental gradients in many regions of the world.  Samples are being stored for future analyses and developing a global database on coral symbionts. A study of symbiont taxa in regions with different background and without bleaching found that Symbiodinium Clade D is the dominant taxa in reefs with high temperatures and histories of coral bleaching.  This symbiont group may reduce the level of mortality in reefs with climate change and these studies will provide insight into the resilience of corals.

Coral bleaching and mortality are expected to increase with climate warming and algae are expected to replace corals when herbivory is low, which is frequently influenced by fisheries management and marine protected areas (MPAs).  Studies of herbivory and coral and algal growth, abundance, and diversity in 7 fished and 5 unfished reef sites were undertaken six years before and after the most severe warm-water anomaly in Kenya in recent history.  Herbivory on experimental assays was around 20 times higher and increased across the disturbance in unfished reefs.  Nonetheless, the effects of the disturbance was larger within these reefs; undergoing a temporary transition from dominance by hard and soft coral to turf and frondose algae to calcifying algae by the end of the study.   The fished reefs changed least but had greater cover of turf and frondose algae and sponge after the disturbance.  Herbivory reduced the abundance and persistence of frondose algae in the MPA reefs and created space and appropriate substratum for recruiting corals but annual rates of coral recovery were low and not different between the management systems.  Consequently, the positive effect of reduced competition with frondose algae and open and appropriate space for coral colonization may have been compensated for by higher predation and mortality of corals in the MPAs.  Reef communities in MPAs are more diverse and complex than fished reefs and the lack of background fishing disturbances makes them less resilient to rare climatic disturbances.

Response to background temperatures

Examination of changes in coral assemblages in four back reef locations across the warm 1998 El Niño Southern Oscillation (ENSO) event was undertaken three years before and after this event.  The physical locations of the reefs differed such that there was a 120-275% warm season range in the Standard Deviations but minor differences in mean temperatures, based on two non-ENSO years.  Our studies tested the predictions that rare warm-water events would 1) produce fewer coral assemblage changes in unstable than stable temperature environments and 2) after the disturbance the stable would more closely resemble the unstable temperature coral assemblages.  The 1998 event did produce fewer changes in coral cover and the community similarity of the assemblages in the high than the low temperature variation reefs.  Despite the initially lower taxonomic richness in the unstable temperature assemblage, there was an additional loss of taxonomic richness in the high and none in the stable temperature reefs.  There was some evidence for taxonomic convergence with a general loss of some of the branching taxa such as branching Porites and Stylophora and relative increase in massive Porites and Favia.  There was, however, moderate site specificity that did not produce true convergence but a general movement in all sites to massive Porites and Favia dominance.  The unstable temperature assemblages maintained the basic “community structure” but lost taxonomic richness and the opposite was true for the stable temperature assemblages.

Disease studies

 In early 2002 coral mortality occurred along 600 km of coastline from Tanzania to Kenya.  Astreopora, Echinopora, and Montipora species were severely affected, with Montipora being nearly eliminated from Kenyan reefs.  Acropora, Platygyra, Goniopora, and massive Porites were also affected; however, Porites and Goniopora rarely died and often recovered, whereas death for most other species occurred within two weeks.  In Echinopora and Montipora, a dull ashy tissue color and brittle skeletons characterized the early stages of this event with a mucus layer on the tissue surface evident in intermediate stages.  Mucus and embedded debris then disappeared and surfaces were left covered in a white calcareous dust that sometimes capped a black layer.  Astreopora tissues became dull and pale, seldom produced mucus, and eventually the skeleton became bare and white.  Either a colorless translucent or brownish thin margin of tissue was visible between living tissue and bare skeleton, depending on coral species.  Scanning electron micrographs of affected corals revealed the presence of fungi.  Histology and staining showed that the fungi were observed mostly in the three genera that died from the syndrome and it may be that fungi invaded and killed corals weakened by another unidentified pathogen.

Glovers Reef Atoll, Belize

Work in Glovers reefs included continued monitoring and experiments on herbivory and nutrients to determine restoration alternatives for reefs dominated by frondose algae.   Coral cover is declining and frondose algal cover is increasing and, therefore, experimental studies are underway to determine the causes of these changes.   Additionally, a study documenting the distribution and abundance of the most economically valuable species in this atoll, including spiny lobsters Panulirus argus, queen conch Strombus gigas, Nassau grouper Epinephelus striatus, black grouper Mycteropercus bonaci, hogfish Lachnoliamus maximus, mutton snapper Lutjanus analis, and queen triggerfish Balistes vetula has been ongoing over the past 7 years.  Studies have shown that significant changes have occurred in protected populations and models have been developed that have significant predictive power to determine potential cost:benefit outcomes under various conditions.   Finally a comparative species inventory of communities occupying different reef physiographic zones and water current flow in the reef zones has been undertaken.

Nutrient and herbivory studies

Studies of herbivory and nutrient interactions of algae growing on dead coral and live coral condition using replicate open, closed, fertilized and unfertilized cages in a two level and factor design during the summer in Glovers reef lagoon.  Herbivory negatively influenced wet, dry and decalcified biomass of algae while nutrients marginally and positively influenced wet algal but not dry and decalcified biomass.  Total and turf algal cover was, however, influenced by both herbivory and nutrients.  Turf algal cover was more positively influenced by nutrients than negatively by herbivory.  Brown frondose algal cover was negatively influenced by both herbivory and nutrients.  There were more algal taxa and higher dominance in low compared to high herbivory treatments.  Crustose coralline cover declined in all treatments but least in the high nutrients and herbivory treatment and calcareous greens were never more than 1% of the cover.  Two species of Porites fragments placed in the cages survived well in all treatments but developed a dark coloration in the fertilized and paled in the unfertilized cages.   Our studies found that turf algae does well under both high nutrient and herbivory while frondose algae did best under both low herbivory and  appeared to be inhibited by nutrients. Our findings suggest that low herbivory and not high nutrients must be responsible for the high levels of brown frondose algae reported on the reefs in this region.  Stony corals did sufficiently well in all conditions that it was not possible to determine their optimal conditions and elevated nutrients may provide them resistance to warm-water associated bleaching.

Indonesian Marine Protected Areas: Evaluation of fishing gear

In Indonesia, the regulation of fishing effort is difficult, as local fisheries agencies do not have adequate resources to monitor and collect information on effort, numbers, and distribution of fishing communities. The major gears used in Indonesia are purse seine and drift nets but a variety of gears are used on coral reefs, including hook and line, spearguns, hand spears, traps, gill nets, and muro-ami. Muro-ami involves the use of divers to drive fish into a large seine-like net and is widespread throughout Karimunjawa National Park in the Indonesian province of Central Java.  Species selectivity and catch composition among gears was determined by examining species diversity, fish size, and mean trophic level of the catches for each major gear type in a multi-species fishery in central Indonesia. Two hundred and four fish species from 37 families were recorded from 187 landings. Net fisheries caught the most species (127 species d-1) while hand spears caught the least number of species (14 species d-1). Muro-ami fishing, a method using large set nets accounted for the highest numbers of fish landed per fisherman (11.2 ± 4.4 individuals per day) and the smallest size fish (28.3 ± 0.64 cm). During a single fishing trip net fisheries caught a mean of 12 species d-1 while other gears caught 4-6 species d-1. Predatory fish species caught by hand lines and gill nets had the highest trophic diversity (3.82 and 3.78 respectively) while spear guns had the lowest (2.69). The mean trophic level of fish caught by muro-ami (3.39) suggests that muro-ami captures a variety of species. The high numbers of individuals and species and low size of fish caught by muro-ami indicates a selective gear but with high species overlap with other gear types, notably traps, and is, therefore, a gear that is likely to compete with other more benign gear and be unsustainable. Interviews with 119 local fishers showed that 80% of fishers supported regulations to abolish muro-ami fishing, a restriction that will both reduces catch of small fish and species overlap in selectivity among gears used. 

Traditional Management in Papua New Guinea

An integrated socioeconomic and ecological assessment of coastal communities and coral reefs was undertaken throughout Papua New Guinea (PNG).  The major objectives of this project were to build the capacity of local scientists, identify threats to coral reef ecosystems, and to begin to determine which management strategies were effective in achieving coral reef conservation and which socioeconomic factors influenced the success or failure of these strategies.  A number of significant threats to coral reefs were identified and documented during this study and found to be very specific in their magnitude.  These include destructive fishing methods, overharvesting of invertebrates, and the perceptions of community members regarding their effects on coral reefs. 

The effectiveness of management regimes in countering threats to coral reefs was examined. Management regimes studied included: i) national park systems; ii) community-based protected areas (created and/or managed with the input of outside experts); iii) traditional management systems (instigated and managed by the community as part of their culture); and iv) customary marine tenure regimes (where enforced ownership over the reefs existed but no other management regimes were present). Reef ecosystems were assessed at replicate sites located inside and outside managed areas. In addition, reefs within the tenure or fishing grounds of communities with management regimes in place were paired with environmentally similar, nearby control reefs/fishing grounds where communities had no system of management in place. The condition of reef ecosystems was quantified using underwater visual surveys of reef fish communities, reef substratum and target invertebrates, as well as indicators of disturbances to reef communities caused by anthropogenic and natural factors. Socio-economic information was gathered from communities with management regimes in place, as well as from paired control communities that had no system of management. This information was gathered using several techniques, including household surveys, resource user key informant interviews, community leader key informant interviews, women’s focus groups, oral histories and participation in fishing trips.

The most significant finding of this study was that management appeared ineffective in promoting the condition of reef ecosystems throughout the majority of sites examined. The majority of ecosystem variables, such as coral and fish diversity, coral cover and total fish abundance, showed little difference in magnitude inside versus outside protected areas across any of the management sites. However, two variables (fish biomass and average fish size) appeared to respond strongly to management regulations, and were found to be higher in magnitude inside than outside protected areas at four of the management sites examined.  Three of the four sites that were effective in improving fish stocks were traditional management regimes. This result was surprising, given that none of the traditional management regimes examined contained permanent reef closures (each involved periodic closures, whereby protected reefs were periodically opened to fishing, either briefly or for extended periods of time), and one of these systems actually allowed line fishing inside the protected area throughout the entire year. In addition, these communities were provided with no external assistance to either instigate or maintain these systems of management. Despite the non-permanent nature of these protected areas, these systems still appeared to have significant conservation benefits for reef fish stocks. The fourth site to display a strong difference in fish stock parameters was a community-based protected area involving a system of permanent reef closure. This community received significant external assistance to establish and maintain the management regime in the form of funding, awareness and education programs and community support programs. One national park site displayed significantly greater average fish size and hard coral cover within the protected area compared to surrounding reefs, however, these differences were only marginal.

Socioeconomic data suggested that the success of management regimes was due largely to factors driving compliance. The results suggested that management regimes that had high levels of acceptance and awareness resulted in greater compliance and consequently were more effective. Greater compliance in the successful community-based management site may have stemmed from the significant input of resources to awareness programs and community support in this community. For the successful traditional management sites, greater awareness and acceptance of the management was likely to have resulted from the integrated nature of the regime in the communities’ cultures and traditions. Greater compliance in traditional systems was also likely to have been influenced by the ability of communities to periodically fish these areas and reap the benefits of the management system, thus meeting more community goals than systems of permanent closure. In an ideal situation, permanently closed marine protected areas provide a good solution to conserving reef resources. However, in countries that lack the resources to properly enforce management regulations, these results suggest that alternative regimes, such as those seen in traditional systems of management, may be valuable conservation tools. This program was successful in identifying and documenting significant and specific threats to coral reef ecosystems and identifying management regimes that were, and were not, effective in conserving reef resources at a number of sites. Traditional management regimes showed significant conservation benefits for coral reef fishes. In countries lacking the resources to properly enforce management regulations, traditional management regimes may prove to be very effective conservation tools.

Annual Publications

1) Acosta, C. A., and D. N. Robertson. 2003. Comparative spatial ecology of fished spiny lobsters Panulirus argus and an unfished congener P. guttatus in an isolated marine reserve at Glover's Reef atoll, Belize. Coral Reef 22:1-9.

2) Baker A.C. (2003) Flexibility and specificity in coral-algal symbiosis: Diversity, ecology and biogeography of Symbiodinium. Annual Review of Ecology and Systematics, 34, 661-689

3) Baker, A. C., C. J. Starger, T. R. McClanahan, and P. W. Glynn. 2004. Corals' adaptive response to climate change. Nature 430:741.

4) Buddemeier, R. W., A. C. Baker, D. G. Fautin, and J. R. Jacobs. 2004. The adaptive bleaching hypothesis. Pages 427-444 in E. Rosenberg and Y. Loya, editors. Coral Health and Disease. Publisher, Berlin.

5) Baker, A. C. 2004. Symbiont diversity on coral reefs and its relationship to bleaching resistance and resilience. Pages 177-194 in E. Rosenberg and L. Y., editors. Coral Health and Disease. Springer-Verlag, Berlin.

6)  Cros, A., and T. R. McClanahan. 2004. Coral transplants damage under various management conditions in the Mombasa Marine National Park, Kenya. Western Indian Ocean Journal of Marine Science 2(2): 127-136.

7) Mangi, S., McClanahan, T.R. 2003.  The effect of marine protected area and the exclusion of beach seines on coral reef fisheries.  In Coastal Ecology of Kenya, Coastal Ecology Series, African Studies Center, Leiden.  Pp. 171-184.

8) McClanahan, T. R., and J. Maina. 2003. Response of coral assemblages to the interaction between natural temperature variation and rare warm-water events. Ecosystems 6: 551-563

9) McClanahan, T.R.  2003.  Disturbance, recovery and restoration of Kenyan coral reefs.  In Coastal Ecology of Kenya, Coastal Ecology Series, African Studies Center, Leiden.  Pp. 21-34.

10) McClanahan, T. R., E. Sala, P. Stickels, B. A. Cokos, A. Baker, C. J. Starger, and S. Jones. 2003. Interaction between nutrients and herbivory in controlling algal communities and coral condition on Glover's Reef, Belize. Marine Ecology Progress Series 261: 135-147.

11) McClanahan, T.R., Sala, E., Mumby, P.J., Jones, S. 2004 Phosphorus and nitrogen enrichment do not enhance brown frondose “macroalgae”.  Marine Pollution Bulletin 148(1-2): 196-199

12) McClanahan, T.R. 2003. Sea urchin reduction as a restoration technique in a new marine park.  Proceedings of the 9th Coral Reef Symposium, Bali 2: 947-953

13) McClanahan, T.R. 2004. The limits to Beyond Boundaries. Aquatic Conservation: Marine and Freshwater Ecosystems 14(1): 1-4

14) McClanahan, T. R., A. H. Baird, P. A. Marshall, and M. A. Toscano. 2004. Comparing bleaching and mortality responses of hard corals between southern Kenya and the Great Barrier Reef, Australia. Marine Pollution Bulletin 48: 327-335.

15)  McClanahan T.R. & Mangi S. 2004. Gear-based management of a tropical artisanal fishery based on species selectivity and capture size. Fisheries Management and Ecology 11: 51-60

16) McClanahan, T.R. (ed, special issue) 2004. Food webs of shallow subtidal marine ecosystems. Ecosystems 321-322.

17) McClanahan, T. R. 2004. Coral bleaching, diseases and mortality in the western Indian Ocean. Chapter 7, pp. 157-176. in E. Rosenberg and Y. Loya, editors. Coral Health and Disease. Springer-Verlag, Berlin.

18) McClanahan, T.R. 2004.  The relationship between coral bleaching and mortality. Marine Biology 144 (6): 1239-1245.

19) McClanahan, T. R., K. R. Moothien Pillay, and H. Terashima. 2003. Mauritius: a small refuge with potential? Reef Encounters 32: 56 –59

20) Muthiga, N.A. 2003. Coexistence and reproductive isolation in the sympatric echinoids Diadema savignyi (Michellin) and Diadema setosum (Leske) on Kenyan coral reefs.  Marine Biology 143: 669-677