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CORAL REEF FISH ASSEMBLAGES AT BANCO CHINCHORRO, MEXICAN CARIBBEAN Rosa Maria Loreto, Mario Lara’ and Juan J. Schmitter-Soto ABSTRACT As pat ofthe characterization studies forthe management plan ofthe Banco Chinchotro biosphere reserve, an atoll-lke ref off the Caribbean coast of Mexico, fish assemblages and abundances by trophie groups were analyzed. Over the course of three years 384 ‘visual censuses, in 20 x 2-m transects, were conducted in a series of strata previously defined by coral structure and development. The known (mainly non-cryptic) ichthyo- fauna of Chinchorro consists of 163 species. Twenty-four of these (in ten families, con tributing 329% of the recorded individuals) are regularly captured by fishery cooper tives operating within Chinchorro, Deep or shallow zones with good reef development tended to have more species and a higher fish density; these zones are located in fou (out Of 17) regions, which have been proposed for conservation, Six trophic groups were sistinguished: benthophagous fishes (Haemulidae, Labridae) were the most abundant group (37.6%), followed by planktivores (27.4%) and omnivores (20.09%) (mainly Pomacenttidae). Herbivores (Acanthuridee, Searidae) were intermediate in abundance ) and higher trophic levels (piscivores and iehthyobenthophagous fishes: Serranide, Lutjanidae, Carangidae) had the lowest densities (below 2%), Overfishing ‘may have affected fish communities at Chinchorr: this was inferred because commer- cial fish populations are scarce and individuals are smal. Ecological evaluation of habitats isan integral part of the development of management plans and programs for the use and conservation of large ecosystems, such as coral reef. The analysis of emergent properties of communities and populations of reef organisms provides criteria and judgment elements to be weighed as possible indicators of the con- servation status of these complex ecosystems, As the main component of nekton, fishes have a great importance in coral ree, from the ecological and human use points of view. Moreover, they provide valuable tools for ‘gauging the conservation status of reef ecosystems, because they may he very sensitive to ‘environmental changes. Although this virtue has been explored more thoroughly in fresh- water (Fausch et al., 1990), fishes have been included in such reef health monitoring protocols as the Atlantic and Gulf Rapid Reef Assessment (AGRRA) Program (Ginsburg, 2000). Chactodontid abundance, for example, has been correlated with coral density or diversity (Birkeland and Neudecker, 1981; Findley and Findley, 1985). One of the most striking attributes of reef fish communities is their species diversity which is the result of two interrelated processes: 1) differential distribution, i. efficient habitat use inthe coral reef, and 2) morphologic and trophie specialization (Anderson et al, 1981; Gladfelter et al., 1980; Sale et al., 1984; Williams, 1986). The understanding of these processes requires a knowledge of pattern in reef fish communities. Banco Chinchorro is an atoll-ike reef off the southem Caribbean versant of Mexico (Fig. 1). This is the most comprehensive report on the fish assemblages of Chinchorr, ‘The only antecedent is Garduio’s (1988) thesis (results published by Chiivez, 1997, and Gardunto and Chavez, 2000), describing composition, diversity, and trophic groups of ‘Deceased while paper in review. The surviving authors dedicate the finished work to his memory 153 1s BULLEN MARINESCIENCE YL. 7.NO. 1.20) Figure |. Location and map of the Banco Chinchorro Biosphere Reserve illustrating limits of 17 reef regions described according to ref stricture development and reef zonation, and sampled sites. S= Slope, OR = Outer Ridge, OT ~ Outer Terrace, IR Inner Ridge, IT~ Inner Terrace, LE = Leeward Fuge, RR = Reef Ring, RHC = Ridge’High Cover, RLC ~ Ridge/Low Cover, Di Deep Heads, SH Shallow Heads. GE = Gorgonians and Sponges, SP= Sand and Patches, BR = Back Reef, BZ ~ Breaker Zone, RCE = Reef Crest Edge, IF = Inner Forereet, OF ~ Outer Forerce, DF = Deep Forerect. Living tissue cover: A~ high, B= medium, C= low. Conservation prioity: 1 igh, 2= medium, 3= low (ftom Loreio and Lara, 2000). reef fishes, based on 24 10-min transects within Chinchorro, and comparing them to other coral reefs around Yucatin Peninsula. Other studies that have provided fish records for Chinchorro, albeit no community studies, include Bohlke and MeCosker (1973), BOhike sand Randall (1968), Gilmore (1997), Greenfield and Johnson (1981), and Smith-Vaniz, and Palacio (1974). Cayo Norte, the northernmost key within Chinchorro, is the type locality for Gobiosoma illecebrosum (Bablke and Robins, 1968). {Loo ETAL: COAL REE FISHAT BANCO CHINCHORRO 1s ‘The aim of this study is to consider some properties ofthe trophie structure of the non- cexyptie fish assemblages at the Banco Chinchorro Biosphere Reserve. This is part of the characterization studies used as input for the management plan of the reserve. Meniops ‘We evaluated cach reef region and zone onthe basis of species richness, Fish density, and relative abundance of trophic groups. The data originated from three cruises cated out in May 1997, July 1998, and July 1999 on board the R/V Oceanus Building on the work of Jordin and Merino (1987), Loreto and Lara (2000) defined 17 reef ‘regions in Chinchorro according to coral development (Fig. 1). These egions bear the designations XXXIV to L, because they continue a series of 33 regions defined for other coastal (Palla et al. 1992; Gutiérrez et al, 1993, 1995, 1999) and insular (Garcia and Loreto, 2000) reefs inthe Mexi- can Caribbean. In the eastern margin, inner frontal reef regions XXXV and XL, located in the southern and northern ends of the bank, respectively, have coral heads about 5 m high; regions XXXVLand XXVIII have coral heads up 0 3 m high; region XXXVI has low coral heads, about | m high, and in region XXX1X coral heads develop on a slope and terrace. On the westem margin, regions XLI and XLIII have one slope with coral heads, and regions XLIl and XXXIV have two slopes with coral heads. In the inner bank, region XLIV has greatly developed Moniastrea heads. In ‘he inner fringe ofthe ref, from south to north, repion XLV has punctuated massifs of Montastrea \with low coral cover and a lage cover of brown algae. In region XLVI gorgonians ate dispersed. ‘over sand, In region XLVI there is only sand, In egion XLVIIL, near the center ofthe bank, there are dispersed coral heads up to 8m deep. 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Vu. 72,N01 283 The outer forereef presented the highest species richness and fish density. This ten- dency occurred inall ref regions, except region XL, which was tcherin the inner forereet (53 species). Both subzones attained their maximum development in regions XXXV and XL, in the extreme southern and northern ends of the ato, respectively, with coral mas- Sif up 0 6 m high. Discussion (Our figure of 136 species sighted by visual census is very similar to the 138 species found in Banco Chinchorro by Garduflo (1988) and the 134 species seen by Nitlez and Arias (1998) near the mainland, Mahahual. With the new records, the checklist for Chinchorro reaches 163 species. This is below the 393 species listed for the total reef adult fish fauna in the Mexican Caribbean (Schmitter-Soto eta, 2000) of the 240 species of Belize (Harborne etal, 1998), but a revision of the eryptic species from Chinchorr already collected and deposited in several museums should drastically increase that num- ber. Cryptic species ean increase the richness of reef ichthyofaunas by 50% (Allen etal, 1992), and they may comprise the majority of fish species in well-developed coral reefs (Robins, 1991). We agree with Garduio (1988) about the dominance of Th. bifasciatum, C. cyanea, C. parrae, H. garnoti, 8 partitus, and S. planifrons, which are also the predominant fish in Mahahual (Niiez and Arias, 1998). On the other hand, Garduiio (1988) did not observe Coryphopterus, which we found to be the sixth most abundant fish in Chinchorro; per- haps he dismissed it a priori as a cryptic species. On the other hand, his fifth most abun- dant species is 0. chrysurus, which we did not find to be as dominant (Chromis eyanea was the dominant species also in Cozumel Island (Fenner, 1991), both before and after Hurricane Gilbert (1988). After the hurricane, another dominant species, C. parrae, became even more abundant; on the contrary, H. garnoti and S. partitus be- came less common. ‘The availability of shelter isa crucial factor in tropical marine ecosystems. The defen- sive mechanisms of most fish species are related to shelter. Therefore, trophic relation- ships, diversity, composition, and density of reef fishes are closely related to the com- plexity of the coral reef (Claro and Gareia-Arteaga, 1994), On the other hand, overfishing is one of the most frequent forces that provoke changes in the pattern of fish communi- ties, and one of its first symptoms is the change in size structure of the populations of exploited species (Nikolsky, 1974). The reef lagoon, reef erest and forereef of Chinchorro are easily accessible, even without SCUBA, and are located within the capture arcas of the fishing cooperatives. Although the mentioned concordance of our results and Gardutio’s (1988) could imply a lack of change in community structure during the last 12 yrs, the effect of overfishing is inferrable because species of the higher trophic levels are rare; ‘moreover, their individual sizes are small, though this observation remains to be sus- tained with the pertinent fishery studies for each species. Garduiio and Chavez (2000) pointed out thatthe higher equitability of the Chinchorro ichthyofauna, in comparison with other coral reefs around Yucatin Peninsula, implied a ‘more even distribution of resources atthe bank, According to Claro and Garvia-Arteaga (1994, the pattern to be expected in a well-conserved Caribbean reef is that herbivore and planktivore fishes, the base of the trophic chain, have a lower biomass than carni- vvores, considering that the abundance of live coral cover under these conditions is greater Lower0 8 a: CORAL REE FLAT WANCO CHINCHORRD 161 than the abundance of plant cover. Moreover, harpoon fishing can also induce an over- abundance of herbivores, released from their predators because othe fishery bias toward large piscivores (Chavez, 2000). At Chinchorto live coral cover was usually over 15%, and as much as 35% (pers. obs.) abundance of herbivores was low, even in those sites within the reef lagoon where coral ridges are made mainly of dead coral with brown algae, not palatable to fishes. On the other hand, planktivores eould be expected to be scarce because of the low biomass levels of plankton in tropical waters, the importance of zooplankton forthe juve niles of several species notwithstanding; however, this ideal pattern was not observed at Chinchorro, where planktivores were the sevond trophic group in importance, particu- Jarly on the leeward slope, Gardufto and Chaver (2000) found planktivores tobe the most, Important trophic group in Chinehorro, followed by omnivores; however, they found herbivores to be quite abundant (about 14%), mainly because of the dominance of O. chrysurus (nearly 8%), which we, as already mentioned, did not find as important. Polunin and Roberts (1993) reported that in protected unexploited sites in Belize and Netherlands Antilles large Lutjanidae and Haemulidae, as well as Scaridae, were com- ‘mon; they further assumed that this was the situation in exploited areas before intensive fishing began. In Cozumel, Fenner (1991) observed that, after eight yrs of protection from fishing, large serranids became common. Koslow etal. (1988) compared three reef fish communities in Jamaica before and after a period of 14-17 yrs, when heavy fishing exploitation began for two ofthe sites. They found that carnivores, especially large preda- tors, declined most clearly, along with other commercially relevant fishes (Haemulidae). ‘When these sites were virtually unexploited, benthophagous fishes were dominant, as is now the case in Chinchorro; however, before exploitation, herbivores (Scaridae, some Balistidae) also were very abundant, unlike Chinchorvo, This abundance of herbivores in some sites was already noted by Randall (1963) inthe Virwin Islands, and it seems to be expected: herbivores are at the base of the food web, and for energetic reasons their biomass should largely exceed that of first-order camivores, However, plant biomass is usually very low compared to animal biomass in coral reefs, a fact that may explain this apparent anomaly (Sierra et al., 1994), urthermore, Choat (1991) cautioned against considering herbivorous fishes as an ecologically uniform group; for example, the abundance of searids, which are able to rode coral, isnot equivalent to the abundance of Kyphasus, which depends on macroalgae and macrophytes. Moreover, the role of channelling primary production may be fulfilled by benthic invertebrates; this would explain the observed abundance of benthophagous fishes. Jones etal. (1991) reviewed a number of studies and found that herbivorous fishes comprise only 7-26% of reef ichthyofaunas, compared against 438% for piscivores, 4~ 38% for planktivores, and 27-36% for benthophagous fishes. On the other hand, Chinchorro, as an atoll-ike reef, is rather isolated. Bardach (1959) stated that herbivores should predominate in large reefs, but earivores in isolated reef patches, Randall (1963) and Sierra etal, (1994) found more carnivores in artifical than in natural reefS. Galzin (1987) detected a significant increase in herbivores and carnivores after an eight-yr period in French Polynesian reefs; he attributed the change to a a de- crease in coral cover and an increase in algze, but could not explain this environmental variation, It may prove difficult to separate direct human pressure (i.e. fishing) from natural or human-induced climatic change. 168 BULLETIN OF MARINESCIENCE YL, 7.0.32 The species in the upper trophic levels—omnivores, benthophagous. ichthyobenthophagous fishes and piscivores—large, colorful fishes important for tou ism and fishery have a wide feeding spectrum. In Chinchorro, omnivores are the third most important trophic group, whereas benthophagous fishes re the most abundant: how- «ver, ichthyobenthophagous fishes and piscivores are scarce, possibly as a result of over fishing. In Chinchorro there has been an intense fishery, more than 40 yrs old, based on two main resources: queen conch (Sironibus gigas) and spiny lobster (Pants argus), for both of which there are egal restrictions that impede their overexploitation: however, the capture of fishes has been considered incidental, taking place slong with the fishing ‘of eoneh or lobster, during the period when the closed seasons ofboth resources overlap (May and June), or during the reproductive aggregations of Nassau grouper (Epinephelus siriats), jewish (Epinephelus tajara), hoglish (Lachnolaimus maximus), or aniberjacks (Seriota spp.), among others. According to official data (SEMARNAP, 2000), the most relevant fish species captured in Chinchorro. with more than I ton per yr from 1990- 1997, were Epinephelus spp, Lutjanus spp.,Sphyraena barracuda, Gerres cinereus, and Seriota spp. their joint volume fel between 1990-1999 from 77.74 to 23.23 tons, During our field work, however, we were able to observe boats capturing exclusively fishes, even during the open season for lobster or conch, including species such as pomacanthids and tetraodontid, which offer few yield but are easy to take. legal fishing is continu ‘us problem that irritates authorized fishermen. Fishing is the only formal economic activity in Chinchorro. Tourism is stil incipient and sporadic, but itis expected to increase in the coming years. The pattems in fish assemblages may be used asa baseline for monitoring both fisheries and tourism, ACKNOWLEDGMENTS: Financial support: Goldman and Packard Foundations through The Nature Conservancy. Feld work: J. Estrada, L. Mendoza, J.C. Huitron, A. Vega and A. Huitron. Map: A. Loreto and J. L. Jiménez, Amigos de Sian Ka’an: J. Bezaury,G. Garcia, C. Lopez and L. Gomez. Boat operator: M Coll. Lireravure Cire Allen, G., LS. Bouvier and R.E, Jensen, 1992, Abundance, diversity, and seasonality of eryptic fishes and their contribution to a temperate ref fish assemblage off Santa Catalina Island, CCaliornia. Bull South, Calif, Acad, Sei, 91: 55-69. Anderson, G. R.V.,A.1. Ehrlich, PR, Ehrlich, J D, Roughgarden, B. C. Russell and FH. Talbot 1981. The community structure of coral ref fishes. Am. Nat 117: 476-495. Birkeland, Cand . Neudecker. 1981, Foraging behavior of two Caribbean chastodontids; Chacon ceapisirams and C. aculeatus. Copeia 1981: 169-178 Bohlke, J. E, and J. E. McCosker. 1973, Two additional West Atlantic gobies (genus Gobiosoma) that remove ectoparasites from other fishes. Copeia 1973: 609-610. and J. E. Rendall, 1968. A key to the shallow-water West Atlantic cardinalfishes ‘Apogonidae), with descriptions of five new species. Proc. Acad. Nat. Sei, Phila, 120: 175-206, and C. R, Robins. 1968. Wester Atlantic seven-spined gobi, with deseriptions of Tei new species and a new genus, and comments on Pacific relatives. Proc. Acad, Nat, Sci Phila 120: 43-174, Brock, V-E. 1954. preliminary report on a method of estimating ree fishes populations, J Wil “Manage. 18: 297-308, LORETO ETAL: CORAL REEF FSH AT BANCO CHINCHORRO 169 (Chavez, E.A. 1997. Sampling design for the study of Yucatin refs, nothwestern Caribbean, Proc. Sih nt. Coral Reef Symp. 2: 1465-1470, 2000. Perspectives of conservation and use of the Meso-American barrier reef sys ‘em Pages 112-120 nO, AburtoO. and. A, Sinchez-Oni, eds, Reef resources ofthe Gull of California. Management strategies forthe marine omate species. Centro Interdissilinario de Ciencias Marinas, La Paz, Mexico, Choa, JH. 1991. The biology of herbivorous fishes in coral refs, Pages 120-155 in PF. Sale, ed ‘The ecology of fishes on coral reefs. Academic Press, San Diego. Claro, Rand J, P Garcia-Arteaga, 1994, Esirucura de ls comunidades de peces en Tos arrecites ‘el gropo insular Sabana-Camagiiey. Cuba. Avicennia 2: 83-107. Fausch, K-D.,J. Lyons, J. R. Karr and PL. Angermeier. 1990, Fish communities as indicators of environmental degradation. Am. Fish, Soe. Symp. 8: 123-144, Fenner, D. P, 1991. Effects of hurricane Gilbert on coral ree, fishes and sponges at Corum, ‘Mexico, Bull. Mar, Sci. 48: 719-730. Findley, J.S.and M.'T Findley. A search for patter in butterfly fish communities. Am. Nat. 126: 800-816, Galzin, R. 1987, Structure of fish communities of French Polynesian coral reefs, 1: Temporal scales. Mar. Eeol. Progr. Ser. 71: 137-148. Garcia, G. and R. M. Loreto. 2000. Caracterizacin de los arecifescoralinos dela isla de Cozumel, ‘Quintana Roo, México. Sian Kaan Set: Dac. 7: 1-42. Gardufo, M. 1988. Distribucién de la ictiofauna asociada a los arrecifes del Caribe mexicano (M.Sc. Thesis, Centr de Investigacign y Estudios Avanzados, Mérida, Mexico. 81 p. and E. A. Chavez. 2000, Fish resource allocation in coral reefs of Yucatin Peninsula Pages 367-381 fr M, Munawar, S, G. Lawrence, I. . Munawar and D. F. Malley, eds. Aquatic evosystems of Menico: status and scope. Backhuys, Leiden, Gilmore, RG. 1997. Lipogramma robins, 3 new basset from the tropical westem Atlantic, with descriptive and distributional notes on L. flavescens and L. amabantoides (Perciformes: Grammatidae). Bull. Mar. Sei. 60: 782-788. Ginsburg, RN. 2000. AGRRA homepage:

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