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Symbiosis, Fisheries and Economic Development on Coral Reefs

Symbiosis, Fisheries and Economic Development on Coral Reefs

Cheilinus undulatus to 87 kg). - reef generally grow at a rate less than , and economic one kg per year in the diverse and highly development on coral reefs competitive coral-reel . The intensity of on coral reels is Charles Birkeland indicated by the disproportionate prevalence and diversity of predators in the community structure8, and the ratio of juveniles to adults Life-history traits of commercially important species, physiological attributes of the in populations on coral reels is much less than framework species, and characteristics of ecosystem processes make coral reefs in neighboring or beds. especially vulnerable to export of . Organisms in driven by Although even smaller coral-reef fishes can and terrestrial nutrient input are more amenable to biomass yield. live for decades once they reach adulthood, the Nonexportive approaches to resource management, exemplified by Palau, survivorship of juvenile fishes in their first are compatible with the attributes of coral-reef ecosystems; they satisfy year is as low as 0.007 (Acanthurus lineatus in to a greater degree the economic demands and pressures of growing human American Samoa, central Pacific )9 or 0.008 populations, and they provide motivation to manage. (Haemulon Ilavolineatum at St Croix, Caribbean)10. The uncertainty of survival in a Charles Birkeland is at the tightly competitive system with high rates of Marine Laboratory, University of Guam, Mangilao, GU 96923, USA. predation probably contributes to selection for large size, longevity and multiple reproduction. These traits of coral-reel species reflect the low rates of population turnover and vulnerability to overharvest11 in , oral reefs have been touted as having the biomass yield per unit gross primary prod- giant clams, spiny lobsters and sea turtles. greatest gross primary and uctivity of the ecosystem than can coral-reef C These life-history traits of coral-reel animals highest standing stock biomass of marine fishes (Fig. 1 ). Tropical pelagic fishes search have recently contributed to the conclusion ecosystems. It has been calculated that the widely for dense concentrations of food, that marine protected areas are the most coral reefs of the world can produce a feeding intensely in ‘foamers’ or ‘boils’ when practical and effective method for sustainable fisheries yield of 20-35 million they find concentrations, consuming as much management of coral-reef fisheriesll-13. metric tonnes per year1.2. as 25% of their own body weight in one day. But high yields have not been sustained They can grow to 5kg (skipjack, Katsuwonus when the fisheries are exploited commer- pelamis), 9kg (mahimahi, Coryphaena Ecosystem processes cially. Although average annual fisheries hippuros) or 14 kg (yellowfin, Thunnus There are also fundamental differences at yields have been documented to be as high as albacares) within their first two years7, the level of ecosystem processes between 26.6 metric tons per km-2 yr-1 for some coral although they do tend to have short lifespans coral reefs and regions subjected to pulses of reefs, the yields on these same coral reefs (skipjack and mahi-mahi live for a maximum concentrated nutrient input. Oceanographic eventually demonstrate a decrease of up to of four or five years). When finding a dense processes such as upwelling are the major 70% , a decrease of 75% patch of food, feeding activity by is driving forces in large-scale current in number of per hectare, and a major sometimes so intense that the body ecosystems (Humboldt, Benguela, Oyashio, shift in relative abundances among species, temperature can rise above that of the Kuroshio), while species interactions (e.g. with a drastic decrease in the species preferred surrounding seawater and cause ‘burns’ in the predation) are a major controlling factor in by fishermen3. There are a number of muscle tissue that lower the market value of coral-reef eco-systemsl4-16. The complexity of examples of coral-reef fisheries being found to the catch. Thus, the tropical pelagic fishes that these interactions has contributed to the be more vulnerable to commercial search out and feed on patchy concentrations conclusion that a holistic approach to fisheries overexploitation than predicted by the initial of abundant resources are characterized by fast management such as marine protected areas is standing stock or potential yield calculated for growth, early reproduction and rapid the most practical and effective method for the system4. This special vulnerability is population turnover, traits that are relatively management of coral-reef fisheries11-13. largely from the life-history characteristics of favorable for the adjustment of their by humans does not in- the important species (Table 1) and the populations to exploitation. fluence the process of upwelling. On coral characteristics of the ecosystem (Fig. 1). Although some coral-reef fishes can grow reefs, in contrast, overfishing can have large- Although pelagic fishes can also be to a great size (the Epinephelus scale, long-term. ecosystem-level effects14-16. overharvested6, they can support a greater itajara can grow to 300 kg and the In recent recognition of the

364 Copyright © 1997. Elsevier Science Ltd. All rights reserved 0169-5347/97/$17.00 PII: S0169-5347(97)01099-9 TREE vol. 12. no 9 September 1997 PERSPECTIVES importance of taking basic characteristics of the ecosystem into account, the National Oceanic and Atmospheric Administration's (NOAA) National Marine Fisheries Service (NMFS) is presently establishing an advisory panel to explore the application of ecosystem principles in conservation and management. Although coral reefs have high gross primary productivity, the fisheries yield and net system productivity are rela- tively low (Fig. 1). Fisheries yield per unit gross primary productivity for the Peruvian upwelling is about 10 to 60 times greater than this ratio for coral reefs (Fig. 1). For coral-reef systems, the net system productivity averages very close to 2 zero . Far less than one percent of the gross primary productivity is converted to production that is meaningful for human 2 consumption . This is partially a result of the proportion of energy lost in transfers among trophic levels. The concentration of standing stock biomass is lower in food webs character- ized by high rates of nutrient input. The major increase in the world fisheries yield of the 1950s and 1960s was largely a result of concentrated harvesting effort on fishes lower on the , such as and . On coral reefs, the presently rampant live coral-reef fish trade of over a billion dollars a year17, is the establishment of others in response to about 10µM destabilize the symbiosis of concentrated on serranids and other large light, temperature or other factors19. In and intracellular by fishes such as Cheilinus undulatus, high contrast to the free-floating single-celled enhancing the growth rates of the in the food web. Upwelling regions of the zooxanthellae18. The corals may respond algae in the of upwelling world have short food-webs with only one areas, regulatory processes within the to this physiologically destabilizing or two steps between and a rapid increase in intracellular algal complex physiological adaptations of reef major source of food for man, while there animals tend to dampen the responses of density by expelling ‘excess’ cells. are up to six substantial trophic levels in intracellular algae to pulses of nutrient Furthermore, the intracellular algae coral reefs. input. within a single species of coral may be a Physiological symbioses between Constraints of physiological complex of species in which the animals and the algae within their tissues complexity coral may expel some and allow are

Complex interactions at the physio- logical level also put constraints on the yield of the ecosystem. In systems of Table 1. Comparison of life-history traits of large tropical pelagic fishes abundant nutrient input (such as in areas and coral-reef fishes of upwelling), relatively simple, free- Tropical pelagic fishes Coral-reef fishes floating, phytoplankters such as diatoms and naked flagellates can respond rapidly (e.g. Thunnus albacares, (e.g. Epinephelus cruentatus, Katsuwonus pelamis, Epinephelus itajara, Epinephelus guttatus, and increase in population density. Coryphaena hippurus) Cheilinus undulates, Sphyraena )

Feeding rates of herbivorous Rapid growth 1-4.5 kg per year, 3-14 kg by Slow growth, rarely over 0.5 kg per year increase as phytoplankton becomes the second year densely available, and the gross growth Early sexual maturity Postponed first reproduction efficiencies of herbivorous marine in upwelling regions are at least Periodically abundant recruitment Irregular recruitment success twice the 10% usually quoted for Relatively short life (Coryphaena and Katsuwonus Long adult life (often decades) terrestrial communities. have a life span of only about 4-5 years) Life histories adapted to multiple reproduction In contrast to the swift and large- scale response of free-floating single- Live in schools or dense aggregations Adults often territorial and solitary celled algae to nutrient input in upwelling Wide ranging: individuals can travel from Sedentary post-settlement life-history stages regions, the response of single-celled the Philippines to Hawaii or further algae within the tissues of corals and other Rapid population turnover Low mortality of adults; high mortality of juveniles animals is inhibited by the complex physiological accommodations between the host and the symbiont. There is some indication that levels of dissolved nitrogen exceeding

TREE vol. 12. no. 9 September 1997 365 PERSPECTIVES funda mental to the characteristics of cor- were deteriorating. the Government of reefs if economies on tropical islands are based on the al reefs at the ecosystem level. Coral reefs Bermuda offered payment of up to $75 000 natural attributes of the species and ecosystem, i.e. ar e often depicted as oases in nutrient- per fisherman. in addition to compensation recycling and low amounts of export. should be poor waters, and organisms characteris- for hardware such as pots and winches. in exported mainly from ecosystems with abundant nutrient tic of coral reefs are often involved in order to close the coral reefs of Bermuda to input, such as upwelling, and continental shelves. interactions that facilitate capture and re- pot fishing22. The fishermen were where the populations of organisms are more amenable to cycling of materials. Symbiotic relation- encouraged to use their boats for more being harvested. ships of a variety of single-celled primary lucrative endeavors in tourism. producers (e.g. dinoflagellates, chloro- It likewise became clear in Palau that References phytes, diatoms, cyanobacteria and Pro- exporting fishes was in competition with 1 Crossland. C.J., Hatcher. B.G. and Smith. S.N.Inc (1991) ch/oron) with disparate classes of animals and far less profitable than subsistence The role of coral reefs in global

(e.g. ciliates, foraminiferans, radiolarians, , recreational fishing, tourism and carbon production. Coral Reefs 10.55-64 dem osponges, hydrocorals, actinians, the sale of fishes to local restaurants and 2 Hatcher. B.G. (1997) Organic production and scler actinians, octocorals, scyphozoans, hotels. In view of the more sustainable decomposition. in Life and Death of Coral Reefs (Birkeland. C., ed). pp 140-174. turbellarians, bivalves, gastropods and economic use of resources in subsistence Chapman & Hall ascidians) provide novel metabolic capa- and tourism than in the export of biomass, 3 Craig. P., Green. A. and Saucerman. S. (1995) bilities and mechanisms for the capture the Government of Palau passed the troubles in American Samoa. SPC and recycling of nutrients20. Since a large ‘Marine Protection Act of 1994’ to phase Fisheries Newsletter 72.33-34 proportion of primary production in out the export of fishes. Currently, the com- 4 Birkeland. C., ed (1997) Life and Death of coral-reef ecosystems is from intracellu- mercial export from Palau of fishes is Coral Reefs. Chapman & Hall lar symbioses (rather than phytoplank- illegal between the months of March and 5 Nixon. S.W. (1982) Nutrient dynamics. ton), complex physiological responses July, which corresponds to the spawning primary production and fisheries yields of probably lead to a dampening of a posi- seasons for most species; . Oceanologica Acta SP. 357-371 tive response of the coral-reef system to cannot be exported unless produced by 6 Safina.C. (1995) The world’s imperiled fish. Scientific increased harvesting. aquaculture. American. November. 46-53 7 Anon. (1995) Important Pelagic Fishes of the It takes at least an order of magnitude Bermuda and Palau Pacific, Western Pacific Regional Fishery Management more fish to support a few commercial Coral reefs have supported subsistence Council fishermen on oceanic islands than it does to fishing for hundreds or perhaps thou- support the same number of people by 8 Hixon. M.A. (1991) Predation as a process structuring 21 coral reel fish communities. in sands of years . However, as the Asian subsistence fishing. This is because most of The Ecology of Fishes on Coral Reefs (Sale. P.F., economy grows and the dollar value of the proceeds from the sale of fishes goes ed.). pp 475-508. Academic Press reef resources overrides management, toward marketing and transportation costs. 9 Craig. P. (1995) Life history and harvest of tradi- tion and law. as human populations Coral-reef resources can sustain a much the surgeonfish Acanthurus lineatus in grow beyond the carrying capacity of greater number of people or careers in the American Samoa, Biol. Rept. Ser. No. 77. Dept. coral reefs, and as urbanization and world economy if used in the nonextractive, Mar. Wildlife Resources, American Samoa immigration of people change the culture service-oriented approaches of Bermuda 10 Ogden. J.C. (1997) Ecosystem interactions in from subsistence to participation in the and Palau. These approaches are the tropical coastal seascape, in Life and international cash economy, compelling compatible with the attributes of coral-reef Death of Coral Reefs (Birkeland. C., ed.). and lucrative alternative sources of pp 288-297. Chapman & Hall species and ecosystems, and with the de- income must be found for the majority of 11 Bohnsack. J.A. (1994) How marine fishery reserves can mands of the growing human populations, fishermen living near coral reefs. The growing economies and urbanization. improve reef fisheries, in Proceedings of the 43rd Gulf and Caribbean life-history characteristics of coral-reef The money exchanged in world tourism Fisheries Institute. pp 217-241 organisms and the relatively closed nature in 1992 was $1.9 trillion, over 27 times the 12 Polunin. N.V.C. and Roberts. C.M. (1996) Reef Fisheries. of the ecosystem make it unrealistic to $70 billion of the world marine fisheries Chapman & Hall expect reef communities to continue to revenue23. To participate in the world 13 Roberts. C.M. (1997) Ecological advice for the global produce enough food to meet these economy, the islands of Oceania can be fisheries crisis, Trends Ecol. Evol. 12. increasing population and commercial highly competitive for the high spenders in 35-38 demands. Radically new approaches to tourism, while geography (transportation 14 Sherman. K. (1994) Sustainability, biomass resource management have been initiated costs), ecology (low yield, effects of over yields, and health of coastal ecosystems: an ecological by Bermuda and Palau for sustainable fishing on ecosystem processes) and perspective, Mar. Ecol. Prog. Ser. inco me from coral reefs. biology (life-history and physiological 112.277-301 The number of people employed and characteristics of the species) work against 15 Hughes. T.P. (1994) Catastrophes, phase shifts, and large-scale degradation of a the economics of extractive reef-fisheries commercial export fisheries on coral reefs. Caribbean coral reef, Science 265, 1547-1551 were small in Bermuda compared to the The expenditures for commercial fisheries 16 Roberts. C.M. (1995) Effects of fishing on the econo my supported by tourism. Tourism are more risky than the commitments to ecosystem structure of coral reels. Conserv. and recreation-related commerce in ecotourism. The cost of airfares are paid by Bermuda grossed more than $9 million in the tourists themselves, in contrast to the Biol. 9.988-995 17 Johannes. R.E. and Riepen. M. (1995) 1988. There was widespread concern that costs of fisheries shipping and marketing Environmental, economic, and social because of commercial fishing the coral which are subtracted from the profit on implications of the live fish trade in Asia and reefs in Bermuda were deteriorating and exported fish sales. It is remarkable that coral reefs in the western Pacific. Report to the nature that algae were replacing living coral. The regions of low nutrient input, such as on Conservancy and the South Pacific Forum hotel owners, charter-boat fishermen, dive in the Pacific gyre, are able to support Fisheries Agency and tour-boat operators and other busi- such concentrations of high biomass and 18 Muller-Parker. G. and D’Elia. C.F. (1997) nesses concluded that the incomes of diversity .It is analogous that a greater Interactions between corals and their m any were threatened by the activities of number of people and diversity of careers symbiotic algae, in Life and Death of Coral a few fishermen. In 1990, after can be supported sustainably by coral Reefs (Birkeland. C., ed.), pp 96-113. Chapman & Hall considering evidence that the catches were declining substantially and that the reef communities

366 Tree vol. 12 no. 9 September 1997 PERSPECTIVES

19 Buddemeier. R.W. and Fautin. D.G. (1993) Coral 21 Dalzell. P. and Adams. T.J.H. Sustainability and a tragedy of the commons averted? bleaching as an adaptive mechanism. management of reef fisheries in the Pacific Environment 35.7-41 BioScience 43. 320-326 islands, in Proceedings of the 8th International 23 Weber, P. (1993) Reviving coral reefs, in State 20 Douglas. A.E. (1994) Symbiotic Interactions. Coral Reef Symposium, Panama (in press) of the world 1993 (Brown. L.R., ed.). pp 42-60. Oxford University Press 22 Butler. J.N. et al. (1993) The Bermuda fisheries: W.H. Norton

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