Indo-Pacific coral-reef fishes as indicators of conservation hotspots
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1 Proceedings 9 th International Coral Reef Symposium, Bali, Indonesia October 2000, Vol. 2 Indo-Pacific coral-reef fishes as indicators of conservation hotspots G. R. Allen 1 ABSTRACT The concept of hotspots, or threatened areas of extraordinary endemism and/or biodiversity, has been effectively used to target conservation priorities, although it has been applied mainly to terrestrial systems. In the present study coral reef fishes are used as general hotspot indicators in the Indo-Pacific region. A zoogeographic analysis involving 2051 species reveals 35 sites of local endemism, as well as elucidating regional trends. Indonesia is the leading country for endemism and also boasts the highest overall species diversity. The Hawaiian Islands exhibit the highest percentage of reef-fish endemism, and tiny Malpelo Island, Colombia has the highest concentration of endemics. The hotspots data suggest that Indonesia and the Philippines are worthy of the highest conservation priority due to their extraordinary species diversity, significant endemism, and high degree of threat. Keywords Reef fishes, Zoogeography, Conservation, Endemism, Biodiversity, Indo-Pacific. Introduction Conservation hotspots are limited geographic areas containing extraordinary concentrations of biodiversity and/or endemic plants and animals. This concept has been particularly effective for prioritizing conservation initiatives, given the enormous task of conserving biodiversity with limited funding (Mittermeir et al. 1999). Until now it has been applied mainly to terrestrial systems. Myers et al. (2000) recognized 25 global hotspots based on numbers of endemics and endemic species/area ratios for plants and non-fish vertebrates, as well as habitat loss. Conservation International is currently developing a global conservation strategy involving marine hotspots, with special emphasis on coral-reef areas. Although it is generally accepted that tropical latitudes support the earth s greatest marine biodiversity, knowledge is far from complete for any region. Considering the huge unfilled gaps of taxonomic information for many groups, particularly invertebrates, it is convenient to use relatively well known flagship groups as indicators of overall biodiversity. The present paper utilizes distribution patterns of reef fishes as indicators of coral-reef hotspots. Fishes are finely adapted to a combination of environmental factors, of which the availability of food and shelter are particularly important. Therefore, the local or regional reef fish community is a useful gauge of both habitat and overall biodiversity. A typical coral reef supports a wealth of fishes, which in turn depend on a complex food web involving myriad plants and invertebrates (Sale 1991). Methods The present study involves analysis of reef fish distribution in the Indo-Pacific region for the purpose of identifying hotspots applicable to marine conservation priority setting. The analysis is restricted to shallow reef fishes, which are defined here as species that are wholly or mainly confined to coral reefs and intermingled habitats (sand and rubble patches, adjacent seagrass beds, etc.) less than 60 m deep. The 60 metre depth is near the lower limit of safe scuba diving, and also approximates the limit of most reef-building scleractinian corals. Table 1 Indo-Pacific coral reef fish families a Muraenidae Holocentridae Syngnathidae Scorpaenidae Serranidae Pseudochromidae Cirrhitidae Apogonidae Carangidae Lutjanidae Caesionidae Haemulidae Lethrinidae Nemipteridae Mullidae Chaetodontidae Pomacanthidae Pomacentridae Labridae Scaridae Pinguipedidae Blenniidae Gobiidae Microdesmidae Siganidae Acanthuridae Balistidae Monacanthidae Tetraodontidae a Families in bold print were used for the analysis of endemism (see following section). More than 100 families are represented on Indo- Pacific coral reefs, but a relatively small portion of these constitute the majority of species. The bulk of the fauna is composed of the 29 families listed in Table 1. This is especially true in the species-rich Indo- Australian Archipelago, where these families routinely constitute percent of the total reef fish fauna. Of particular importance are the Gobiidae, Labridae, Pomacentridae, Apogonidae, Blennidae, Serranidae, Chaetodontidae, and Acanthuridae, which collectively comprise more than 50 percent of the fishes on any given reef. Analysis of Endemism Seventeen of the 29 principal families were utilized, containing a total of 2051 species (Table 2). In most cases, the entire family was considered, but for Syngnathidae, Serranidae, Pseudochromidae, and Tetraodontidae the analysis was limited to particular 1 Conservation International, Center for Applied Biodiversity Science, 1919 M Street, NW, Suite 600, Washington, DC 20036, USA. tropical_reef@bigpond.com
2 subfamilies and genera. The various groups were selected not only because they are among the most speciose on coral reefs (and therefore result in high resolution of endemic hotspots), but also because they are relatively well collected and studied. Reproductive biology was another important consideration. Consequently, there is good representation of groups that exhibit parental egg care and have a relatively limited pelagic larval stage (e.g. psedochromids, apogonids, pomacentrids, and blenniids). In general, these groups show a much higher degree of localized endemism compared to fishes with a more lengthy pelagic larval stage. Table 2 Fish groups used for Indo-Pacific hotspots analysis Family/ subfamily/ Species Primary references genus Syngnathinae 175 Dawson 1985 Holocentridae 58 Randall & Greenfield 1996, Randall 1998 Epinephelinae 105 Randall & Heemstra 1991 Pseudochrominae 100 A. Gill pers. comm. Apogonidae 263 Allen in preparation Lutjanidae 45 Allen & Talbot 1985 Caesionidae 20 Carpenter 1987 Chaetodontidae 105 Allen et al Pomacanthidae 70 Allen, et al Pomacentridae 291 Allen 1991 Labridae 330 Parenti & Randall 2000 Scaridae 67 Parenti & Randall 2000 Blenniidae 263 numerous references Microdesmidae 40 Randall & Hoese 1985 Acanthuridae 66 Randall in press Siganidae 21 Woodland 1990 Tetraodontidae (Arothron, Canthigaster) 32 Allen & Randall 1977, Myers, 1999 Both published and unpublished distribution maps and data were consulted for each species. Actual analysis consisted of screening the known distribution of each species, then assigning them to various categories (e.g. Indian Ocean, Western Pacific, Red Sea, Hawaiian Islands, Easter Island, etc.). The resultant information was then used to construct the maps appearing in Figs Analysis of Species Diversity A review of relatively recent published faunal checklists of colleagues was undertaken and combined with the authors personal survey data for Australia, Indonesia, Malaysia, Singapore, Philippines, and Papua New Guinea. In order to maintain consistency, only coralreef fishes (see definition above) were considered. The information from this analysis was used to construct a generalized species contour map for the Indo-Pacific region (Fig.3). Results Analysis of Endemism Results of the analysis reveal both regional and local patterns of endemism. The largest definable endemic areas are consistent with the major biotic provinces that are more or less universally recognized: Indian Ocean, Western Pacific, Pacific Plate, and Eastern Pacific (Fig. 1). The eastern Pacific region clearly supports a highly unique fauna, which is actually more closely related to that of the western Atlantic. This relationship reflects a common ancestry, resulting from the interconnection of the two areas prior to the uplifting of the Central American landbridge, which probably occurred in the early Pliocene. Although few species are common to both regions, there are numerous shared genera and sisterspecies complexes, involving a close relative on each side of the Central American isthmus (Allen and Robertson 1994). Fig. 1 Major biotic provinces of the tropical Indo-Pacific based on reef fish distributions: A Indian Ocean; B Western Pacific; C Pacific Plate, and; D Eastern Pacific. Percentages in parentheses indicate percentage of endemic species in various indicator groups that were utilized. The reef-fish fauna of the Indo-west and central Pacific is remarkably homogenous at the family and generic levels. There are also numerous wide-ranging species in the region. Indeed, the majority of species have relatively wide distributions. However, the present analysis focused mainly on species that are at least restricted to one of the major biotic provinces, or exhibit more restricted ranges. The level of endemism in the Indian and Western Pacific oceans is similar, 25.9 and 28.0 percent respectively. In other words, about one of every four species found in either of these regions is endemic. Although the figure for the Pacific Plate is slightly less, it is nevertheless significant, and the present analysis supports the work of Springer (1982), who recognized the Plate as a discrete sub-unit of the Indo- Pacific region. Although this information may be useful for students of zoogeography it has little practical application in terms of conservation planning. Patterns of local endemism are far more useful for this purpose.
3 The ultimate goal of the present analysis was to identify local patterns of endemism. Fig. 2 shows 35 local hotspots of endemism, basically areas that have three or more endemic species. Although most of the areas represented are relatively confined, consisting in many cases of a single island or small archipelago, the Hawaiian Islands and Red Sea are disparate, occupying much greater areas. Nevertheless, their relative isolation and high levels of endemism set them apart as discrete units of endemism and it serves no useful purpose to resolve them into finer units. Other prominent areas of endemism include the Marquesas, southern Japan, Mascarene Islands, Oman, Great Barrier Reef, Lesser Sunda Islands (Indonesia), Fiji, and Palawan (Philippines). Results of the analysis of endemism can be evaluated in a variety of ways. Three of the most obvious are presented here. The first method, illustrated in Table 3, lists the 10 highest ranking geopolitical areas in terms of total reef fish endemics. Table 3 Top 10 areas for endemic reef fishes based on absolute numbers. Locality Endemic spp. Indonesia 58 Hawaii (USA) 49 Philippines 31 Southern Japan 26 Marquesas (France) 25 Australia 22 Oman 14 Papua New Guinea 12 Mexico 11 Fiji 10 The reader is reminded that the values in this table were determined from selected indicator groups only. to be approximately twice this total judging from two areas (Hawaii and Marquesas) where accurate total figures are available (Randall, pers. comm.). Another way to evaluate the endemism data involves ranking various areas on the basis of their percentage of endemic species in relation to the total reef-fish fauna (Table 4). The highest ranking areas using this methodology are generally isolated outposts (e.g. Pacific islands) or areas that were essentially isolated during past geological episodes (e.g. Red Sea). Table 4 Top 10 coral-reef hotspots based on percentage of endemic reef fishes Locality No. species No. endemics % endemics Hawaiian Is Baja California Easter I Red Sea Marquesas Galapagos Is Clipperton I Isla del Coco Mascarene Is Oman The values shown in Table 4 are based on the overall fauna of each location, rather than being restricted to the indicator groups. The last example ranks various locations on the basis of the number of endemic species per unit area (Table 5). Tiny isolated islands with significant endemism (> 5%) easily outrank other areas in the Indo- Pacific if this approach is used. The total number of endemics for each area is estimated Fig. 2 Hotspots for reef fish endemism in the tropical Indo-Pacific. The coral triangle is indicated by shading.
4 Table 5 Top 10 locations for endemism on the basis of number of endemic fishes per unit area a Locality E/km 2 x 1000 a Malpelo Island, Colombia 250 Clipperton Island 240 Easter Island 200 Isla del Coco 120 Rapa 80 Pitcairn Island 12.5 Christmas Island, Indian Ocean 10 Mauritius 3.5 Komodo Islands, Indonesia 2.5 Réunion 1.8 Togean Islands, Indonesia 1.4 a The ranking was determined by dividing the total endemic species (E) by the area (km 2 ) and multiplying the sum by Analysis of Species Diversity Results for the analysis of species diversity are shown in Fig. 3. The pattern presented here for reef fishes agrees well with other wide-ranging groups such as corals and molluscs (Veron 1995, Briggs 1999), and no doubt reflects diversity trends for other Indo-Pacific marine organisms. Basically, the center of diversity is the area occupied by eastern Indonesia and the southern Philippines. There is an attenuation of the fauna in all directions away from the center, although this trend is less pronounced in a westward direction. Numerous families of reef fishes exhibit similar patterns, for example the highly speciose Pomacentridae (Allen 1975, 1991). Most conservation actions are initiated at the country level or regional level, involving several adjacent countries. Therefore, it is useful to rank individual countries on the basis of overall species diversity (Table 6). The total for each country may at first appear very conservative, compared to various published works involving these areas. However, these figures apply to coral-reef fishes as defined above and do not reflect the total shore fish fauna. Table 6 Top 10 countries for reef-fish diversity Country No. spp. Reference Indonesia 1,820 Allen & Adrim in prep. Australia 1,627 Hoese et al. in press Philppines 1,525 Allen in press Papua New Guinea 1,494 Kailola Republic of Belau 1,254 Myers 1999 Japan 1,315 Masuda et al Taiwan 1,172 Shen et al New Caledonia 1,007 Rivaton et al Fiji 919 Myers 1999 Federated States of Micronesia 900 Myers 1999 The area encompassing Australia, Indonesia, Philippines, and Papua New Guinea (Briggs 1999) contains the largest concentrations of species from the majority of tropical marine fish and invertebrate families. This region is sometimes referred to by zoogeographers as the Indo-Australian Archipelago or East Indian Triangle (Briggs 1999). The area (Fig. 2) has also been tagged the Coral Triangle by conservation biologists (Werner and Allen 1998). Although its extraordinary biological diversity is widely acknowledged, there is still Fig. 3 Map of Indo-Pacific region showing diversity isopleths for tropical reef fishes.
5 a lack of basic taxonomic information for most locations within this huge region. However, unpublished field research on reef fishes by the author and various colleagues indicates that the epicenter of the Coral Triangle may well be situated in eastern Indonesia. Discussion Randall (1998) provided the best overview to date of Indo-Pacific fish zoogeography. His extensive data corroborate those of the present analysis, particularly regarding principal hotspots for endemism. He also offers a plausible explanation for the East Indian center of marine biodiversity, attributing it to the following five factors: 1. relatively stable sea temperatures during ice ages; 2. large area and diversity of habitat; 3. large numbers of shore fishes adapted to nutrient-rich waters of continental and large island shelves; 4. large numbers of species with larvae unable to survive in plankton-poor oceanic seas or having too short a life span in the pelagic realm for long transport in ocean currents, and 5. being an area that is the recipient of immigrating larvae of species evolved in peripheral locations. Randall further suggests that speciation may have occurred in the region as a result of an east-west barrier to fish dispersal caused by sealevel lowering during past glacial periods. He gave 65 examples of possible geminate species pairs that could have evolved as result of this barrier. Certainly on the basis of its extraordinary biodiversity, as well as significant local endemism, the East Indian Coral Triangle should be near the top of the list of marine conservation priority areas. The need for protective measures is especially acute in the Philippines and Indonesia, both of which have experienced a rapid decline in marine resources over the past few decades. Much of the blame is attributed to the widespread use of illegal fishing methods (McAllister 1988). Muroami, cyanide, and explosives are among the most destructive practices resulting in wholesale degradation of coral environments. The muroami method, common in the Philippines involves setting a net over a coral reef into which a group of swimmers drive the fishes. The swimmers are equipped with weighted (usually rocks) lines that are bounced up and down in an effort to break up the corals and drive out the fishes (Carpenter 1988). In the 1980s the use of cyanide emerged as the most effective method of capturing specimens for the aquarium and live food-fish trades. McAllister (1988) conservatively estimated that 75,000 kg or 1,500 drums of cyanide were being sprayed onto Philippines coral reefs each year. Although there are no authenticated cases of recent extinctions involving reef fishes, coral reefs and their myriad inhabitants are increasingly at risk as a result of human activities. Greenhouse emissions and resultant sea temperature increases, destructive fishing practices, and haphazard logging /agricultural methods that lead to erosion and consequent sedimentation of reefs are among the most obvious factors. There is an urgent need to establish an effective network of marine protected areas throughout the Indo-Pacific and other tropical seas. Admittedly, there is still much to learn concerning source-sink relationships of marine larva, but if we wait for researchers to provide this information it may already be too late for many species. It would be far better to implement a strategic network of MPAs as soon as possible. If a conservation umbrella was based on the 35 Indo-Pacific hotspots recognized in Fig. 2 it is conservatively estimated that at least 90 percent of all fishes in the region would receive at least some measure of protection. Most importantly, the rarest elements of the fauna, the highly restricted endemics, would receive maximum attention following this approach. Acknowledgments I am grateful for the assistance of my Conservation International colleagues R. Mittermeier and T. Werner, who encouraged me to undertake this analysis and offered many useful suggestions. I also acknowledge the numerous contributions of J. Randall and V. Springer to our knowledge of Indo-Pacific fish zoogeography. Their works were crucial to this study. Thanks are also due C. Roberts, F. Wells, and J. Veron for their discussions and input concerning Indo-Pacific zoogeography. References Allen GR (1975) Damselfishes of the South Seas. T.F.H. Publications, Neptune City, New Jersey: Allen GR (1991) Damselfishes of the World. Mergus Verlag, Melle, Germany: Allen GR (in press) Reef fishes of the Calamianes Islands, Palawan Province, Philippines. In: Werner TB, Allen GR (eds) A Rapid Marine Biodiversity Assessment of the Calamianes Islands, Palawan Province, Philippines. Bull Rapid Assess Prog 17, Conservation International, Washington, DC. Allen GR, Randall JE (1977) A review of the sharpnose pufferfishes (subfamily Canthigasterinae) of the Indo- Pacific. Rec Aus Mus 30: Allen GR, Robertson DR (1994) Fishes of the tropical Eastern Pacific. Crawford House Press, Bathurst, Australia: Allen GR, Steene R, Allen M (1998) Guide to angelfishes and butterflyfishes. Odyssey Press/Tropical Reef Research, Perth, Australia: Allen G.R, Talbot FH (1985) Review of the snappers of the genus Lutjanus (Pisces: Lutjanidae) from the Indo-Pacific, with description of a new species. Indo-Pacific Fishes 11: Briggs JC (1999) Coincident biogeographic patterns: Indo-west Pacific Ocean. Evol 53: Carpenter KE (1987) Revision of the Indo-Pacific fish family Caesionidae (Lutjanoidea), with descriptions of five new species. Indo-Pacific Fishes 15: Carpenter KE (1988) FAO species catalogue. Vol. 8. Fusilier fishes of the world. An annotated and illustrated catalogue of caesionid species known to date. FAO Fish Synop 125: Dawson CE (1985) Indo-Pacific Pipefishes. Gulf Coast Research Laboratory, Ocean Springs, Mississippi:
6 Hoese D, Bray D, Allen G, Allen C, Cross N, Paxton J (in press) Zoological Catalogue of Australia. Vol. 7 (Part II). Pisces: Mugilidae to Tracanthodidae. Aus Biol Res Stud, Canberra. Kailola PJ ( ) The fishes of Papua New Guinea. A revised and annotated checklist. Vol. 1 Myxinidae to Synbranchidae (1987), Vol 2. Scorpaenidae to Callionymidae (1987), Vol. 3 Gobiidae to Molidae (1991). PNG Dept Fish Mar Resources Bull 41: Masuda H, Amaoka K, Araga C, Uyeno T, Yoshino T (1984) The fishes of the Japanese Archipelago. Tokai Universiy Press, Tokyo: McAllister DE (1988) Environmental, economic, and social costs of coral reef destruction in the Philippines. Galaxea 7: Mittermeir RA, Myers N, Mittermeir CG (1999) Hotspots Earth s biologically richest and most endangered terrestrial ecoregions. Cemex, Mexico City: Myers N, Mittermeir RA, Mittermeir CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 404: Myers RF (1999) Micronesian reef fishes. Third Edition. Coral Graphics, Guam: Parenti P, Randall JE (2000) An annotated checklist of the species of the labroid fish families Labridae and Scaridae. JLBSI Icthyol Bull 68: Randall JE (1996) Revision of the Indo-Pacific squirrelfishes (Beryciformes: Holocentridae: Holocentrinae) of the genus Sargocentron, with descriptions of four new species. Indo-Pacific Fishes 27: Randall JE (1998) Zoogeography of shore fishes of the Indo-Pacific region. Zool Stud 37: Randall JE (in press) A guide to the surgeonfishes of the world. University of Hawaii Press, Honolulu. Randall JE, Greenfield DW (1996) Revision of the Indo- Pacific holocentrid fishes of the genus Myripristis, with descriptions of three new species. Indo-Pacific Fishes 25: Randall JE, Heemstra PC (1991) Revision of Indo-Pacific groupers (Perciformes: Serranidae: Epinephelinae), with descriptions of five new species. Indo-Pacific Fishes 20: Randall JE, Hoese DF (1985) Revision of the Indo- Pacific dartfishes, genus Ptereleotris (Perciformes: Gobioidei). Indo-Pacific Fishes 7: Rivaton J, Fourmanoir P, Bourret P, Kulbicki M (1989) Checklist of the fishes of New Caledonia. Catalogues Sciences de la mer, Orstom, Centre de Noumea: Sale PF (ed) (1991) The ecology of fishes on coral reefs. Academic Press, San Diego: Shen SC, Shao KT, Lee SC, Mok HK, Chen CT, Chen CH (1993) Fishes of Taiwan. National Taiwan University Press, Taipei: Springer VG (1982) Pacific plate biogeography with special reference to shorefishes. Smith Contrib Zool 367: Veron JEN (1995) Corals in space and time. UNSW Press, Sydney: Werner TB, Allen GR (eds.) (1998) A rapid biodiversity assessment of the coral reefs of Milne Bay Province, Papua New Guinea. RAP Working Papers 11, Conservation International, Washington, DC. Woodland DJ (1990) Revision of the fish family Siganidae with descriptions of two new species and comments on distribution and biology. Indo-Pacific Fishes 19:
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