Proceedings 9th International Coral Reef Symposium, Bali, Indonesia 23-27 October 2000, Vol. 1.
Species richness and endemism levels of the Southwestern Atlantic reef fish fauna R. L. de Moura1 and I. Sazima 2 ABSTRACT A qualitative synopsis of the Southwestern Atlantic (Brazilian) reef-fish fauna is presented based on extensive recent collections and literature records. Species richness is higher than previously reported, but considerable lower than that of the Caribbean region. A species/area relationship may explain the lower species richness of the Southwestern Atlantic, besides other historical and ecological factors. Levels of endemism within reef fish families are highly variable (0-100%), showing a negative association with dispersion capabilities. The wide taxonomic spectrum of fishes bearing Brazilianendemic species indicates that major cladogenetic events isolated some groups in the Southwestern Atlantic. PlioPleistocene sea-level fluctuations account for breaking gene flow between the Caribbean and the Southwestern Atlantic during regressive periods, but the lack of phylogenetic evidences supporting area relationships complicates biogeographical analyses. Multiple historical factors seem to be responsible for the present composition of the Brazilian reef fish fauna.
Keywords Reef fishes, Species richness, Southwestern Atlantic, Endemism levels Introduction Few estimates of reef fish diversity are available for the Southwestern Atlantic (e.g. Rosa and Moura 1997), a situation that precluded the inclusion of this area in previous interoceanic faunistic comparisons (e.g. Thresher 1991, Sale 1996, Bellwood 1997, Ormond and Roberts 1997, Robertson 1998). As Greenfield (1988, 1989) predicted, an increasing number of Brazilian-endemic shore fishes have been recognized as a result of revisionary studies of widespread West Atlantic groups. Recent and ongoing taxonomic work show that the Southwestern Atlantic harbors a considerable number of endemics (e.g. Moura 1995, Sazima et al. 1998, Heiser et al. 2000, Moura et al. 2001), many of them previously identified as Caribbean congeners. The present paper contributes to recent efforts to analyze the composition of the Southwestern Atlantic’s reef fish fauna (Moura et al. 1999a, Floeter and Gasparini 2000). We provide a checklist of Brazilian-endemic species and update previous estimates of species richness that were unsubstantiated by museum specimens. The smaller reef area of the SWA is suggested as the primary factor accounting for its low species richness, besides other historical and ecological factors. Methods Species richness estimates are primarily based on recent and extensive fieldwork (1997-2000). Surveys involving 2
1 2
to 4 fish taxonomists, for at least 15 days in each locality, were conducted at Manoel Luís Reefs (00°52’S, 44°15’W), Southern Ceará (04°17’, 37°17’W), João da Cunha Reefs (04°44’S, 36°57’W), Fernando de Noronha Archipelago (03°50’S, 32°25’S), Rocas Atoll (03°52'S, 33°50'W), Tamandaré (08°22'S, 35°05'W), Abrolhos (17°57'S, 38°41'W), Espirito Santo (20°40’S, 40°20’W), Rio de Janeiro (23°00’S, 41°50’W) and São Paulo (24°00', 45°40'W). The resulting database is available at http://www.mnrj.ufrj/pronex/. Voucher specimens are deposited at Museu de Zoologia da Universidade de São Paulo (MZUSP), Museu de História Natural da Universidade Estadual de Campinas (ZUEC) and National Museum of Natural History, Washington, DC (USNM). Species richness and endemism levels were analyzed using a consensus list of families (ie. families present at all coastal localities). The families Carcharhinidae, Myliobatidae, Elopidae, Moringuidae, Engraulidae, Clupeidae, Belonidae, Hemirhamphidae, Triglidae, Pomatomidae, Echeneidae, Rachycentridae, Eleotridae, Scombridae, and Cynoglossidae were not accounted, as they are primarily associated with non-reef habitats. The consensus list approach (see Bellwood 1997) does not provide a definition of what a reef fish is, but makes comparisons of species richness and endemism levels among areas more comprehensive. For conciseness, only SWA endemics are fully listed, but the total number of species recorded in each family is also provided. Estimates of regional reef areas are from Spalding and Grenfell (1997). Reconstruction of oceanic paleotemperatures and sea-level fluctuations were obtained from CLIMAP (1981) and Woodroff and Grindrod (1991).
Museu de Zoologia, CP 42694 Univ. de São Paulo 04299-970 São Paulo SP Brazil (
[email protected]) Museu de História Natural, CP 6109 Unicamp 13083-970 Campinas SP Brazil
Results and Discussion Species Richness A total of 438 species belonging to the 48 SWA families were recorded from the Brazilian coast (Table 1), approximately 20 percent of these being endemic. Despite being present or even abundant in some
localities, the families Narcinidae, Congridae, Bythitidae, Antennariidae, Syngnathidae, Aulostomidae, Fistulariidae, Gobiesocidae, and Callyonimidae were absent from the consensus list. Endemism levels within these ten nonconsensus list families are generally low (less than 5%), with the probable exceptions of Bythitidae and Syngnathidae, which lack recent revisions.
Table 1. Consensus families of fishes recorded in well-sampled SWA localities. Brazilian-endemic species in each family are listed even when not present in all localities or not being primarily reef-associated. S.W.A. endemic species
Other species recorded in Brazil 4(a)
S.W.A. endemic species
Other species recorded in Brazil
S.W.A. endemic species
Other species recorded in Brazil
Acanthuridae Ginglymostomatidae Ostraciidae 3 none none 1 none Apogonidae Grammidae Pempheridae Apogon americanus 6 Gramma brasilensis 0 none 1 Balistidae Grammistidae Pomacanthidae none 4 None 4 none 5 Batrachoididae Haemulidae Pomacentridae Poric. kymosemeum (3) 7 Haemulon squamipinna 19 Chromis jubauna (2) 5 Poric. porosissimus (2) (3) Boridia grossidens (2) (3 Stegastes fuscus Thal. montevidensis (2)(3) Holocentridae Stegastes pictus Triathala. argentina (2)(3) none 5 Stegastes rocasensis (1) Triathala. lambaloti (2)(3) Kyphosidae Stegastes sanctipauli (1) Blenniidae 3 none 2 Stegastes trindadensis (1) Entomacrod. vomerinus Labridae Stegastes uenfi Hypleuroc. fissicornis (2) Clepticus brasiliensis 11 Stegastes variabilis Lupinoblennius paivai (2) Halichoeres brasiliensis Priacanthidae Ophioblen. a. atlanticus Halichoeres sp. (2) none 3 Scartella sp.1 Halichoeres brasiliensis Scaridae Scartella sp.2 (1) Thalassom. noronhanum Scarus trispinosus 5 Bothidae Xyrichth. incandenscens Scarus sp. none 3 Labrisomidae Sparisoma amplum Carangidae Labrisomus sp.1 3 Sparisoma axillare Trachino. marginatus (3) 34 (b) Labrisomus sp.2 Sparisoma frondosum Chaenopsidae Malacoctenus sp.1 (1) Sparisoma sp. (2) none 1 Malacoctenus sp.2 (1) Sciaenidae Chaetodontidae Paraclinus sp.1 Cynoscion guatucupa (3) 26 (c) Prognathod. obliquus (1) 4 Paraclinus sp.2 Stellifer sp. (3) Prognathod. brasilensis Paraclinus sp.3 Stellifer brasiliensis (3) Cirrhithidae Starksia brasiliensis Umbrina canosai (2)(3) none 1 Starksia sp.1 Scorpaenidae Clinidae Starksia sp.2 Helic. dactylopterus(2)(3) 8 (c) Ribeirocl. eigenmanni (2) 0 Lutjanidae Serranidae Dactylopteridae Lutjanus sp. 13 Acant. brasilianus (2)(3) 26 (c) none 1 Malacanthidae Acant. patachonicus(2)(3) Dactyloscopidae Lopholatilus villarii 2 Anthi. menezesi (3) Gillellus sp. 7 Microdesmidae Anthi. salmopunctatus (1) Storrsia olsoni (1) Microdesmus bahianus 1 Bathyantias roseus (2)(3) Platygillelus sp. Monacanthidae Dules auriga (2)(3) Dasyatidae none 8 Holanthias sp. Dasyatis marianae 5 Mullidae Serranus sp.(2) (3) Diodontidae Mullus argentinae (2) (3) 3 Sparidae Cyclichthys spinosus 4 Muraenidae Diplodus a. argenteus (2) 6 (c) Ephippidae none 15 (c) Calamus mu (2) none 1 Ogcocephalidae Sphyraenidae Gobiidae Ogcocephal. vespertilio 5 none 4 Akko dioneaea (3) 40 (c)(d) Ophichthidae Synodontidae Elacatinus figaro Asarchen. longimanus (3) 22 (c) none 6 (c) Elacatinus sp.1 (1) Letharchus aliculatus (3) Tetraodontidae Elacatinus sp.2 (1) Ophichth. brasiliensis (3) Canthigaster sp. 8 (c) Gobionellus stomatus Opistognathidae Trypterygiidae Lythrypnus brasiliensis Opistognat. brasiliensis 4 (c) Enneanectes smithi (1) 1 Lythrypnus sp. (1) Opistognat. cuvierii. Priolepis dawsoni Opistognat. sp. Legends: (1) endemic to oceanic islands; (2) primarily subtropical or temperate; (3) not a primarily reef-associated fish; (a) one species, A. monroviae, is recently introduced from W. Africa; (b) includes pelagic dwellers; (c) includes soft bottom dwellers; (d) probably underestimated.
Accounting for species absences in a given zoogeographical area is a contentious issue. However, species belonging to at least 32 reef-fish genera, some of which are common and abundant along Florida and the Caribbean, seem to be genuinely absent from the SWA, rather than still unrecorded. These include: Aprognathodon (Ophichthidae), Neoniphon (Holocentridae), Kryptophanaron (Anomalopidae), Opsanus, Sanopus (Batrachoididae), Oligopus, Petrotyx, Calamopteryx (Bythitidae), Emmelichthyops (Inermiidae), Centropristis, Hypoplectrus (Serranidae), Pseudogramma (Grammistidae), Lipogramma (Grammidae), Erythrocles (Emmelichthyidae), Apsilus (Lutjanidae), Lagodon (Sparidae), Chasmodes (Blenniidae), Acanthemblemaria, Chaenopsis, Hemiemblemaria, Coralliozetus (Chaenopsidae), Stahmonotus, Nemaclinus (Labrisomidae), Evermannichthys, Pariah, Varicus, Vomerogobius, Lophogobius, Ginsburgellus, Palatogobius (Gobiidae), Derilissus (Gobiesocidae) and Xanthichthys (Balistidae). Although some of these fishes are small-sized and secretive, notable absences include large and very conspicuous fishes that are unlikely to have been overlooked. In addition to several new records published in recent years (e.g. Moura et al. 1999a), many previous records to Brazil appear to be based on misidentifications. For instance, we were not able to validate literature records (e.g. from Böhlke and Chaplin 1996, Randall 1996, and SmithVaniz et al. 1999) with museum specimens of the following 22 species: Epinephelus striatus (Serranidae), Chaetodon capistratus (Chaetodontidae), Halichoeres garnoti (Labridae), Scarus coelestinus, S. coeruleus, S. iserti, S. taeniopterus, S. vetula, Sparisoma aurofrenatum, S. chrysopterum, S. rubripinne, S. viride (Scaridae), Stegastes leucostictus (Pomacentridae), Paraclinus nigripinnis (Labrisomidae), Canthigaster rostrata (Tetraodontidae), Xanthichthys ringens (Balistidae), Aluterus heudeloti (Monacanthidae), Lactophrys triqueter, L. caudalis (Ostraciidae), Chilomycterus atinga, C. shoepfi (Diodontidae). Species richness in the SWA is considerably lower than that of the Caribbean region (Fig. 1). Considering only consensus families, the SWA has approximately 440 species compared with about 650 for the Caribbean region (estimates from Table 1, Böhlke and Chaplin 1996, Figueiredo and Menezes 1978, 1980, Menezes and Figueiredo 1980, 1985, 2000, Randall 1996, Smith-Vaniz et al. 1999). The sample size of only two biogeographic regions (Caribbean and Brazil) does not allow a regression analysis, but reef fish species richness appears to be strongly related with area (Fig. 1, see Rosensweig 1995). Diversity "anomalies" (see Ricklefs and Lathan 1993) in other tropical communities, such as mangroves, have also been partially explained by species/area relationships (e.g. Ellison et al. 1999).
Besides a species/area relationship, additional historical and ecological factors may have contributed to the impoverishment of the Brazilian reef fauna. Few islands and only underdeveloped seagrass beds occur along the eastern coast of South America (Maida and Ferreira 1997), contributing to its low relative area and habitat diversity. The continental platform along the tropical Brazilian coast is extremely narrow, ranging from 30 to 40 km width, with the notable exception of the Abrolhos Bank, where the platform extends to about 200 km width (Maida and Ferreira 1997). Within SWA, species richness of other reef organisms, such as hermatypic corals, reach maximum values on the Abrolhos Bank (Hetzel and Castro 1994). If only tropical areas are considered, the Abrolhos Bank is also the richest area in terms of reef fish species (190). However, maximum species richness within the SWA is found in a “transition zone” (primarily rocky bottoms with sparse corals between 21°-22°S), where tropical species occur together with subtropical species (Moura et al. 2001, in prep.).
Fig. 1 Relative reef areas (upper) and reef-fish species richness (lower) in the Caribbean and Brazil. Species richness at individual sites along the Brazilian coast also seems to be consistently lower than that of individual sites along the Caribbean. Approximately 470 reef fish species are recorded at the Bahamas (Böhlke and Chaplin 1996), 330 at the Cayman Islands (Burgess et al. 1994) and 270 at Bermuda (Smith-Vaniz et al. 1999). For individual sites on the tropical Brazilian coast we obtained
approximately 100 (Manoel Luís Reefs), 110 (Tamandaré), 190 (Abrolhos), 200 (Espirito Santo) and 190 species (Rio de Janeiro). The species richness pattern for the Western Atlantic appears to be highly influenced by evolutionary and dispersion processes operating on regional spatial scales and historical time scales, rather than the result of local ecological interactions (Caley 1997). Longer-term studies of Brazilian reefs will certainly yield more species records per site, but it is unlikely that any locality will be comparable to Caribbean sites in terms of species richness. Endemism levels Endemism levels within SWA consensus families are closely associated with the restricted dispersal capabilities of demersal spawners, viviparous species, and fishes exhibiting parental care. All groups with low dispersion capabilities (apogonids, pomacentrids, blennioids, gobioids and tetraodontids, cf. Thresher 1991) have endemic species in the SWA. Their endemism levels range from about 10 to 100 percent of the total number of species in the family (Tables 1 and 2). Notable exceptions are Labridae and Scaridae, which exhibit high levels of endemism (40-50%) and broad dispersal capabilities. Faster mutation rates in these labroid lineages may account for their high endemism levels. An exploratory Chi-square test showed that the proportion of families with endemic species is related to the proportion of families with dispersal restrictions (Chi sq.= 18.63, p= .000016, df= 1). Table 2 Summary of frequencies and results of the Chisquare test. Highly capable of Dispersal restricted dispersion Observed Expected Observed Expected Totals freq. freq. Freq. freq. Families w/o SWA endemics Families with SWA endemics
9
16.14
16
8.85
25
22
14.85
1
8.14
23
Implications of sea-level fluctuations The hard bottom formations off the Amazon and Orinoco river mouths are considered the most important zoogeographical "stepping stones" between the Caribbean and Brazil (Collette and Rutzler 1977, Moura et al. 1999b). These “stepping stones” are located in relatively shallow waters, but below hyposaline layers (Fig. 2). The effect of Plio-Pleistocene sea-level fluctuations on these "stepping stones" also accounts for effective isolation of some groups
during regressive periods. For example, the “stepping stones” are essentially eliminated when the AmazonOrinoco freshwater plume covers the entire shallow water habitat (Fig. 2). Lowered sea levels are generally accompanied by lowered temperatures and increased water turbidity, two additional stress factors that could increase speciation rates during regressive periods (see Potts 1984). Another important implication of sea-level fluctuations is that the warm water area of the SWA is severely reduced during regressive periods. In the Caribbean, “pockets” of tropical water remain in scattered areas, and the resultant reef area remains substantially greater than that of the SWA (CLIMAP 1981). Thus, local extinctions in regressive periods were probably more frequent in the SWA than in the Caribbean, just as they were more frequent in the Caribbean than in the Indo-Pacific (Ormond and Roberts 1997). The present winter sea surface isotherm of 20°C is situated at about 32°S, compared to about 20°S during the last glacial maximum (CLIMAP 1981), thus severely reducing distributions of tropical reef organisms in the SWA. Differential extinctions have been suggested by Belwood (1997) as a factor explaining differences in the family-level composition of Caribbean and Indo-Pacific assemblages, and may also account for differences between the Caribbean and Brazil. The West-flowing Equatorial Current seems to constrain the counter-flow dispersion from the Caribbean into the SWA, but at the same time facilitates dispersion from the SWA into the southern Caribbean. Some species occurring on both sides of the Amazon River mouth are not found south of São Roque Cape (the “hump” of Brazil), being restricted to the area under influence of the Equatorial Current. Species in this category include Heteroconger camelopardalis (Congridae), Inermia vittata (Inermiidae), Chromis scotti (Pomacentridae), Lachnolaimus maximus (Labridae), Xyrichthys incandescens and Starksia sp. 2 (Labrisomidae). Several common Brazilian shore fish species are also found in the southern Caribbean, but do not range northward. This assemblage includes Pseudomyrophis frio (Ophichthidae), Thalassophryne nattereri (Batrachoididae), Ogcocephalus notatus (Ogcocephalidae), Opistognathus sp. (Opistognathidae), Trachinotus cayennensis (Carangidae), Anisotremus moricandi (Haemulidae), Centropyge aurantonotus (Pomacanthidae), Scomberomorus brasiliensis (Scombridae), Trinectes microphthalmus, T. paulistanus (Achiridae), Canthigaster sp. and Sphoeroides tyleri (Tetraodontidae). The simplest explanation for this pattern is that some species originated in the SWA and subsequently dispersed into the southern Caribbean, during recent transgressive periods. The alternative (but least parsimonious) explanation is that these species were formerly widespread, but eventually became extinct from northern Caribbean waters.
Carolina V. Minte-Vera for many valuable discussions. We are also grateful to the Instituto Brasileiro do Meio Ambiente e Recursos Naturais Renováveis (IBAMA) for collecting permits, and the Brazilian Navy for many working opportunities in remote localities. The Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Ministério da Ciência e Tecnologia (through FINEP/PRONEX), Conservation International and the Smithsonian Institution provided essential financial support. References
Fig 2. The Amazon River mouth, indicating the points used to construct the depth profile (A, B, C, D). The depth profile (right) shows present-day sea level (PDSL), present-day depth of freshwater plume (PDFW), Plio-Pleistocene minimum sea level (PLSL) and the corresponding depth of the freshwater plume during regressive periods (PLFW). The lack of phylogenetic studies The current lack of species-level phylogenetic studies is a serious obstacle for a better understanding of biogeographic patterns in the Atlantic. Indeed, a major taxonomic impediment for phylogenetic studies of PanAtlantic groups still exists, as West Africa is a key area for reef fish endemism that remains poorly documented, with few published checklists (e.g. Seret 1981) and few specimens available in museums. Also, the recognition of subspecific-level status for allopatric forms with “low” degrees of difference (e.g. Schultz 1968) is a misleading practice accounting for the poor understanding of zoogeographic patterns within the Atlantic (see Gill 1997). West African endemism was recently recognized in cases involving labrid (Heiser et al. 2000) and scarid (Moura et al. 2001) species previously considered as having pan-Atlantic distributions. In at least one case (Clepticus), the African species shared supposedly derived traits with the Brazilian species, indicating that they may represent sister taxa (Heiser et al. 2000). Thus, even if the putative sister-species of some Brazilian-endemics occurs in the Caribbean, other Brazilian-endemics may be more closely related to West African congeners. The subjective allopatric replacements, as well as the Late Pliocene origin of the Brazilian reef fish fauna, both advocated by Floeter and Gasparini (2000), are largely unsubstantiated by phylogenetic evidence. These speculations reflect the deficient knowledge of phylogenetic and biogeographic relationships within Atlantic reef fishes. In fact, there is growing evidence that multiple and nonexclusive historical factors may account for the present composition of the Brazilian reef fish fauna. Acknowledgments We thank Naércio A. Menezes, José Lima de Figueiredo, Ronaldo B. Francini-Filho and
Bellwood DR (1997) Reef fish biogeography: habitat associations, fossils and phylogenies. Proc 8th Int Coral Reef Symp 1: 379-384 Bellwood DR (1998) What are reef fishes? - Comment on the report by D.R. Robertson: Do coral-reef fish faunas have a distinctive taxonomic structure? (Coral Reefs 17: 179-186). Coral Reefs 17: 187-189 Böhlke JE, Chaplin CCG (1996) Fishes of the Bahamas and adjacent tropical waters. 2 nd Edition, Univ Texas Press, Austin: 771 pp. Burgess GH, Smith SS, Lane ED (1994) Fishes of the Cayman Islands. In MA Brunt and JE Davies (eds). The Cayman Islands: natural history and biogeography. Kluwer Academic Publishers: 199- 228 Caley MJ (1995) Reef fish community structure and dynamics: an interaction between local and large scale processes ? Mar Ecol Prog Ser 129: 19-29 Caley MJ (1997) Are local patterns of reef fish diversity related to patterns of diversity at a larger scale? Proc 8th Int Coral Reef Symp 1: 993-998 CLIMAP (1981) Seasonal reconstructions of the Earth’s surface at the last glacial maximun. Geol Soc Am Map and Chart: 36 pp. Collette BB, Rutzler K (1977) Reef fishes over sponge bottoms off the mouth of the Amazon River. Proc 3 rd Int Coral Reef Symp 1:305-310. Ellison AM, Farnsworth, EJ, Merkt RE (1999) Origins of mangrove ecossistems and the mangrove biodiversity anomaly. Global Ecol Biogeogr 8: 95-115 Figueiredo JL, Menezes NA (1978-1980) Manual de peixes marinhos do sudeste do Brasil. Vols II and III. São Paulo, Museu de Zoologia, Univ. São Paulo: 90-110 Floeter SR, Gasparini JL (2000) The southwestern Atlantic reef fish fauna: composition and zoogeographic patterns. J Fish Biol 56: 1099-1114 Gill, AC (1997) Subspecies, geographic forms and widespread Indo-Pacific coral-reef fish species: a call for change in taxonomic practice. Proc Indo-Pacific Fish Conf 5: 79-87. Greenfield DW (1988) A review of the Lythrypnus mowbrayi complex (Pisces: Gobiidae), with a description of a new species. Copeia 1988: 460-470
Greenfield DW (1989) Priolepis dawsoni, n. sp. (Pisces: Gobiidae), a third Atlantic species of Priolepis. Copeia 1989: 397-401 Heiser JB, Moura, RL, Robertson DR (2000) Two mew species of Creole Wrasse (Labridae: Clepticus) from opposite sides of the Atlantic Aqua J Ichth Aq Biol 4: 110 Hetzel B, Castro CB (1994) Corais do sul da Bahia. Ed Nova Fronteira: 189 pp. Maida M, Ferreira BP (1997) Coral reefs of Brazil: an overview. Proc 8th Int Coral Reef Symp 8: 263-276 Menezes NA, Figueiredo JL (1980-2000) Manual de peixes marinhos do sudeste do Brasil. Vols IV, V and VI. São Paulo, Museu de Zoologia, Univ. São Paulo: 96–116 Moura RL (1995) A new species of Chromis (Perciformes: Pomacentridae) from the southeastern coast of Brazil, with comments on other species of the genus. Rev fr Aquariol 21: 91-96 Moura RL, Sazima I, Gasparini JL (1999a) New records and range extensions of reef fishes in the western south Atlantic, with comments on reef fish distribution along the Brazilian coast. Revta Bras Zool 16: 513-530 Moura RL, Francini-Filho RB, Rodrigues MCM, Sazima I (1999b) Unexpected richness of reef corals near the southern Amazon River mouth. Coral Reefs 18: 170 pp. Moura, RL, Figueiredo JL, Sazima I (2001) A new parrotfish (Scaridae) from Brazil, and revalidation of Sparisoma amplum (Ranzani, 1842), S. frondosum (Agassiz, 1831), S. axillare (Steindachner, 1878) and Scarus trispinosus Valenciennes, 1840. Bull Mar Sci: 68 (in press) Ormond RFG, Roberts CM (1997) The biodiversity of coral reef fishes. In: Ormond RFG, Gage JD, Angel MV (eds) Marine biodiversity: patterns and processes. Cambridge Univ Press, Cambridge: 216-257 Potts DC (1984) Generation times and the Quaternary evolution of reef-building corals. Paleobiology 10: 4858 Randall JE (1996) Caribbean reef fishes. 3 rd Edition, TFH Publ Inc, Neptune City: 368 pp. Ricklefs RE, Lathan RE (1993) Global patterns of diversity in mangrove floras. In: Ricklefs RE, Schluter D (eds)
Species diversity in ecological communities. Univ of Chicago Press, Chicago: 215-229 Robertson DR (1998) Do coral-reef fish faunas have a distinctive taxonomic structure? Coral Reefs 17: 179186 Rocha LA, Rosa IL (1999) New species of Haemulon (Teleostei: Haemulidae) from the Northeastern Brazilian coast. Copeia 1999: 447-452 Rosa RS, Moura RL (1997) Visual assessment of reef fish community structure in the Atol das Rocas Biological Reserve, off northeastern Brazil. Proc 8 th Int Coral Reef Symp 1: 983-986 Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge: 436 pp. Sale PF (1996) Structure and dynamics of reef fish communities: a biogeographical comparison. In: ML Cody, JA Smallwood (eds) Long-term studies of vertebrate communities. Academic Press, San Diego: 73-97 Sazima I, Gasparini JL, Moura RL (1998) Gramma brasiliensis, a new basslet from the western South Atlantic (Perciformes:Grammatidae). Aqua J Ichth Aq Biol 3: 39-43 Schultz LP (1868) A new subspecies of parrotfish, Nicholsina ustus colettei, from the eastern Atlantic ocean. Proc U S Nat Mus 124: 1-5. Seret B (1981) Poissons de Mer L’Ouest Africain Tropical. ORSTROM, Paris: 416 pp. Smith-Vaniz WF, Collette BB, Luckhurst BE (1999) Fishes of Bermuda. Amer Soc Icthyol Special Publ 4. Allen Press, Lawrence: 424 pp. Spalding MD, Grenfell AM (1997) New estimates of global and regional coral reef areas. Coral Reefs 16: 225-230 Thresher RE (1984) Reproduction in reef fishes. TFH Publ, New Jersey: 399 pp. Thresher RE (1991) Geographic variability in the ecology of coral reef fishes: evidence, evolution and possible implications. In: PF Sale (ed) The ecology of fishes on coral reefs. Academic Press, San Diego: 401-436 Woodroffe CD, Grindrod J (1991) Mangrove biogeography: the role of Quaternary environmental and sea-level change. J Biogeogr 18: 479-492
