AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) Published online 24 August 2007 in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/aqc.880

Conservation hotspots of biodiversity and endemism for Indo-Pacic coral reef shes
GERALD R. ALLEN*
Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, Perth 6986, Australia ABSTRACT 1. Distribution patterns of 3919 species of Indo-Pacic reef shes were analysed using GIS mapping software for the purpose of conservation prioritization of extraordinary high concentrations (hotspots) of diversity and endemism. 2. Megadiversity countries with more than 1000 coral reef species include Indonesia, Australia, Philippines, Papua New Guinea, Malaysia, Japan, Taiwan, Solomon Islands, Palau, Vanuatu, Fiji, New Caledonia, and the Federated States of Micronesia. 3. The richest area for reef shes is the renowned Coral Triangle, which includes eastern Indonesia, Sabah (Malaysia), Philippines, Papua New Guinea, and the Solomon Islands. The highest concentration of species within this region extends from south-eastern Indonesia to the central Philippines. 4. Occupying only 3% of the surface area of the tropical Indo-west and central Pacic, the heart of the Coral Triangle contains 52% of its total species. 5. The top-ranked areas based on percentage of endemism are Easter Island, Baja California, Hawaiian Islands, Galapagos Islands, Red Sea, Clipperton Island, Marquesas, Isla del Coco, Mascarene Islands, and Oman. 6. The highest concentration of endemics per unit area occurs at remote south-eastern Polynesian and eastern Pacic islands including Clipperton, Isla del Coco, Easter, Rapa, and the Pitcairn Group. Copyright # 2007 John Wiley & Sons, Ltd. Received 2 October 2006; Revised 6 May 2007; Accepted 12 May 2007
KEY WORDS:

species richness; zoogeography; GIS analysis; coral triangle; marine protected areas

INTRODUCTION Hotspot is a term frequently used by conservation biologists to denote a relatively restricted geographic area containing an extraordinary high concentration of biodiversity and endemism. The hotspot concept

*Correspondence to: Gerald R. Allen, Department of Aquatic Zoology, Western Australian Museum, Locked Bag 49, Welshpool DC, Perth, Western Australia 6986. E-mail: tropical reef@bigpond.com

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has been especially eective for prioritizing conservation action when faced with the enormous task of biodiversity conservation with limited nancial resources (Mittermeier et al., 1998, 1999). Until recently, the concept has been applied primarily to terrestrial systems. For example, Myers et al. (2000) recognized 25 global hotspots based on the number of endemic plants and non-sh vertebrates, their area ratios, and threats as indicated by natural habitat loss. Conservation International is currently developing a global conservation strategy that recognizes the importance of marine hotspots with special emphasis on coral reef areas. Although it is generally accepted that tropical latitudes support the Earths greatest marine biodiversity, knowledge is far from complete for any region. Considering the huge unlled gaps of taxonomic information for many groups, particularly invertebrates, it is convenient to use well known agships as indicators of general biodiversity. Fishes are particularly useful in this regard for several important reasons. First and foremost they are highly speciose and exhibit a full range of distribution patterns from wide-ranging circumglobal species to highly restricted local endemics. Unlike most groups of marine organisms the majority of species are easily observed in the eld and by comparison their taxonomy and distribution patterns are relatively well studied. Importantly, it has been shown in a number of studies that there is a strong local correlation between sh diversity and diversity of other organisms such as molluscs (Wells, 2002) and corals (Veron, 2000). Birds have been similarly used to rally conservation support for terrestrial areas subjected to habitat degradation (Statterseld et al., 1998). Like their avian counterparts, shes are nely adapted to a combination of environmental factors, of which the availability of food and shelter are particularly important. Therefore, the local or regional reef sh community is a useful gauge of both habitat and overall biodiversity. A typical coral reef supports a wealth of shes, which in turn depend on a complex food web involving myriad plants and invertebrates (Sale, 1991). Roberts et al. (2002) were the rst authors to embrace the idea of global marine hotspots. Their analysis was based on the distribution patterns of 1700 species of reef shes, 804 species of coral, 662 species of molluscs, and 69 species of lobster. The data were used to rank various centres of endemism, mainly on the basis of concentration of restricted-range endemic species. They recognized 18 hotspots ranging in size from tiny Easter Island in the south-eastern Pacic to the entire Great Barrier Reef of Australia. However, their methodology was questioned by Baird et al. (2002), who emphasized the need for a more balanced approach that does not rely so heavily on the concept of endemism at the expense of overall biodiversity. Moreover, despite the apparently large number of species utilized for the analysis, it was a global study based on insucient numbers from the species-rich Indo-Pacic region. In addition, there have been considerable advances in our knowledge of sh distributions and geographical information systems (GIS) since their data were gathered. Allen (2002) used coral reef shes as indicators of marine conservation hotspots based on distribution patterns of Indo-Pacic coral reef shes. The analysis involved general diversity as well as endemism based on absolute numbers, percentage of endemics, and concentration of endemism according to area size. The present study provides an expansion of these same ideas, but employs a more rigorous GIS approach and a considerably expanded dataset. The ultimate goal of the present analysis is to identify concentrations of diversity and endemism (i.e. hotspots), at varying spatial scales, as an aid for prioritizing marine conservation initiatives. This is accomplished by utilizing a dataset that includes distribution maps of every known species of coral reef sh in the Indo-west and central Pacic. Special emphasis is placed on the Coral Triangle region of South East Asia, an area that supports the greatest global marine biodiversity, but is also among the most threatened (Allen and Werner, 2002; Briggs, 2005). Terrestrial hotspots as previously dened (Myers et al., 2000) are generally areas of exceptional diversity/ endemism that are also highly threatened. However, the current analysis of reef hotspots purposely avoids inclusion of a threat layer. It is acknowledged that coral reefs of certain regions (e.g. South East Asia) are particularly threatened by an extremely high density of human inhabitants and consequent eects of shing
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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pressure and careless land use, but virtually all coral reefs are currently at risk. Certainly the most ominous threat is the disturbing trend of accelerating ocean temperature and the periodic severe coral bleaching events they promote (Hoegh-Guldberg, 1999). Although GIS techniques are employed to analyse the data, this study is strongly inuenced by the authors Indo-Pacic eld experience, totalling more than eight years (i.e. about 4.5 months per year) over a 35 year period, with special focus on the taxonomy, ecology, and zoogeography of the regions reef shes. The past decade was particularly instructive, involving multiple journeys to Fiji, Madagascar, Indonesia, and Papua New Guinea as well as extended single visits to western Thailand, Philippines, Christmas Island (Indian Ocean) Solomon Islands, and the Phoenix Islands.

METHODS The study is restricted to shallow reef shes, which are herein dened as species that are entirely or mainly conned to coral reefs and intermingled substrata (sand/rubble patches, seagrass beds, etc.) less than 60 m deep. The 60 m depth limit is near the lower limit of scuba diving, and also approximates the limit of most reef-building scleractinian corals (Veron, 2000). Distribution patterns of 3919 species of reef shes were analysed to provide more accurate information to set conservation priorities. A distribution map was prepared for every known species of reef sh in the tropical Indo-west and central Pacic from East Africa and the Red Sea to the islands of Oceania. Distribution polygons, bounded by the outermost records of occurrence, were drawn on standard equalarea base maps utilizing ArcView GIS software. The distribution of individual species was represented as a single polygon if numerous collection/visual observation records indicated a more or less continuous distribution (Figure 1). However, for species that appear to have a genuine disjunct distribution or are poorly known and reported from a relatively few scattered locations, two or more polygons or circles were used (Figure 2). The latter category accounts for approximately 40% of the total species. These types of digitized polygons are commonly employed by taxonomic specialists to convey overall distribution patterns for a diverse range of shallow marine taxa from seaweeds and corals to marine mammals (Carpenter and Niem, 19982001; Veron, 2000). Although polygons show broad expanses of deepsea/pelagic habitat, they are constructed on the premise that the species in question occurs within the boundaries only where suitable habitat (e.g. shallow coral reefs) is present. Polygons rather than point distribution records based on actual museum specimens were utilized in order to expedite the completion of the project within a 3 year period. Essentially, the same information (i.e. hotspot delineation) is generated with polygons as with the extremely labour intensive point data. Actual map preparation involved between 5 and 60 min per species, depending on the complexity of the distribution. An accompanying database containing family, genus, and species names, as well as the author(s) and year of publication was prepared with an Excel spreadsheet. The integration of maps and spreadsheet facilitated production of various analytical programs that generated instantaneous listings of either total fauna or total endemics for any polygon, regardless of size, circumscribed on the ArcView basemap. Distribution data were gathered from a variety of sources including personal observations throughout the Indo-Pacic over the past three decades, recent literature (new species descriptions and especially family and generic revisions), regional faunal monographs, collections and collaboration of numerous colleagues who are mentioned in the acknowledgement section. In addition, collections from the following museums were utilized: Australian Museum (Sydney), Bishop Museum (Honolulu), California Academy of Sciences (San Francisco), National Museum of Natural History (Washington, DC), and the Western Australian Museum (Perth).
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Figure 1. Distribution of Abudefduf bengalensis (Pomacentridae).

Figure 2. Distribution of Discordipinna griessingeri (Gobiidae). Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Table 1. Countries with more than 1000 coral reef shes including percentage of the total reef sh fauna of the Indo-west and central Pacic region (IWCP), estimated coral reef area, density based on the number of species per km2, and number of endemics

Country Indonesia Australia Philippines Papua New Guinea Malaysia Japan Taiwan Solomon Islands Republic of Palau Vanuatu Fiji New Caledonia Federal States of Micronesia

Species 2122 1827 1790 1635 1549 1462 1374 1371 1254 1105 1068 1060 1031

Percent IWCP spp. 54.4 46.8 45.9 41.9 39.7 37.5 35.2 35.2 32.2 28.3 27.4 27.2 26.4

Reef Area (km2) 51 020 48 960 25 060 13 840 3600 2900 940 5750 1661 4110 10 020 5980 4340

Spp./km2 0.042 0.037 0.071 0.118 0.430 0.504 1.462 0.238 0.755 0.269 0.107 0.177 0.238

Endemics 78 93 29 22 1 26 7 3 3 2 15 7 7

Reef areas expressed as km2 for various countries in Table 1 were obtained from the World Atlas of Coral Reefs (Spalding et al., 2001). Apparently there are no reliable gures available for reef areas of most small oceanic islands. Therefore, the locations listed in Table 5 were estimated by multiplying the island(s) perimeter in km by 0.5. The multiplier represents the maximum distance from shore (500 m) for most shallow coral reefs at typical island locations as determined by satellite imagery on the NASA world wide website. The gure assumes there is a uniform belt of coral/rocky reef habitat, which of course is not the actual case and many reefs that fringe oceanic islands are narrower than 500 m. Therefore, the estimates are probably higher than the actual reef area for most of the listed locations. Although the tropical eastern Pacic was not included in the current mapping project, data from previous studies by the author and D.R. Robertson (Allen and Robertson, 1994) were utilized, particularly with reference to the analysis of endemic species per unit area.

RESULTS Analysis of species diversity The pattern of diversity for reef shes presented in Figure 3 is compatible with that of marine invertebrates that have been well documented including corals (Veron, 2000) and molluscs (Wells, 2002), and probably is applicable to other major invertebrate groups. Basically, the centre of diversity extends from central Indonesia to Papua New Guinea and the Solomon Islands, and northward to the Philippines. This region (delineated by the darkest shade in Figure 3) is frequently referred to as the Coral Triangle by conservation biologists and is the globes richest area for marine biodiversity (Allen and Werner, 2002). There is general faunal attenuation in all directions from the centre, although this trend is less pronounced towards the west where there is an increase in diversity in the Red Sea and south-western Indian Ocean. Numerous families of reef shes exhibit similar patterns, for example well-studied groups such as Pomacentridae and Labridae, which contain 302 and 361 species respectively in the Indo-west and central Pacic region. Conservation activity is usually implemented at the country level or regional level involving adjacent countries. It is therefore useful to rank individual countries on the basis of overall species diversity. The countries with the highest diversity of reef shes, the exclusive 1000 species club, are indicated in Table 1.
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Figure 3. Map of the Indo-Pacic region showing diversity isopleths for tropical reef shes. The lightest shade represents between 200 and 400 species and the darkest shade between 1300 and 1700 species.

In terms of density of reef sh per unit area, Taiwan and Palau lead all other megadiversity countries due to their comparatively small reef area and rich fauna, which share many elements with the nearby Coral Triangle. Isolated oceanic islands generally have rich concentrations of reef shes. For example, the tiny island nation of Nauru in the western Pacic, with a coral reef area of less than 4 km2, has an exorbitant density of 177 species/km2. The Indonesian Archipelago is the worlds premier area for marine biodiversity, mainly due to its extraordinary wealth of coral reef organisms. Allen and Adrim (2003) recorded 2056 species from Indonesia, and the total of 2122 species recorded during the present study conrms its position as the richest country in the world for reef shes. There is, however, considerable conjecture concerning the location of the highest concentration of species within the Coral Triangle. According to Carpenter and Springer (2005) the centre of the centre for sh diversity is situated in the central Philippines, with a secondary area of high diversity located o north-eastern Sumatra. Utilizing similar methodology as the present study, their conclusions were based on GIS mapping overlays for 2983 marine organisms, including 2047 shore shes. However, unlike the current study, which involves coral reef shes, they utilized mostly common sheries species (including a high percentage of soft-bottom inhabitants), excluding numerous small reef shes that tend to have more restricted ranges. Less than half of the species included in their analysis were coral reef inhabitants. The distributions were mapped by 84 taxonomic specialists for a Food and Agriculture Organization of the United Nations publication (Carpenter and Niem, 19982001). Their analysis was based on comparisons of single 10 km 10 km pixels (i.e. 100 km2 area). Surprisingly, considering the discrepancy in the nature of the databases, the present results corroborate the ndings of Carpenter and Springer. The highest total } 1627 species } within a limited area (100 000 km2) was in the central Philippines (Figure 4), followed by the Raja Ampat Islands (1613 species), Molucca Islands (1573 species), northern Sulawesi (1567 species), and the southern Philippines (1566 species). However, if the area of comparison is increased to a 500 000 km2 grid (Figure 5), there is a shift in the centre of diversity to the Indonesian region between the extreme western end of New Guinea and northern
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Figure 4. Comparison of faunal totals for 100 000 km2 squares superimposed on Coral Triangle region of Southeast Asia.

Figure 5. Comparison of faunal totals for 500 000 km2 squares superimposed on Coral Triangle region of Southeast Asia.

Sulawesi (1705 species), followed by the Sulu Sea (1660 species), central Philippines (1648 species), southeast Banda Sea (1635 species), Lesser Sunda Islands (1628 species), and central Sulawesi (1577 species). Most importantly, the GIS-species distribution data reveal that the heart of the Coral Triangle extends from south-eastern Indonesia to the Philippines (Figure 6). This corresponds with the 1500 species contour and within this area species numbers uctuate narrowly over a range of about 100 species. Realistically, any area within this region could be expected to yield a record-breaking species count given an intense collection eort and provided the full range of reef habitats is present. The heart region occupies about three million km2 or only 3% of the surface area of the tropical Indo-west and central Pacic, yet it contains 52% of the total species from this vast region. Randall (1998) proposed several key factors for the proliferation of reef species in the region including its complex geological history with merging of disparate elements due to tectonic shifting, the stepping-stone nature of the archipelago that tends to prevent local extinctions, a
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Figure 6. The heart of the Coral Triangle.

long history of stable climate, periodic raised/lowered sea levels that form isolating barriers, and its strategic position between the Pacic and Indian Ocean. Although 1500 species appears to be the hallmark of a localized (under 100 000 km2) area within the heart of the Coral Triangle, this gure has never been documented in the eld. It is based on a combination of collection/visual observation records and expected range distributions records. The highest actual totals for the region based on localized eld surveys by the author between 1985 and the present time were obtained at the Raja Ampat Islands, western New Guinea (1119 species), Maumere Bay, Flores (1111 species), and Milne Bay Province, Papua New Guinea (1109 species). The Great Barrier Reef of Australia, although lying just beyond the boundary of the Coral Triangle, is nevertheless one of the globes megadiversity centres for marine organisms. Spanning 14 degrees of latitude and a linear distance of more than 1800 km, the GBR is home to nearly 1500 reef shes, including 34 endemics. Western Australia is also relatively rich with nearly 1400 species of tropical reef shes, including 27 endemics. The current analysis does not support Carpenter and Springers (2005) nding that a secondary centre of diversity is located between peninsular Malaysia and Sumatra, centred on Bintan Island, lying 38 km southeast of Singapore. This is certainly invalid for coral reef shes, where a 100 000 km2 overlay of the same area captures a comparatively modest total of 771 species. Reef development is poor due to an unusually high level of sedimentation. The authors impression of the area, based on a week-long scuba diving survey at Bintan in May 1997, was of a highly impoverished fauna, more akin with species-poor reefs of the
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Kimberley coast of north-western Australia. Moreover, M. Erdmann (personal communication) spent eight months in the area and documented a similarly impoverished stomatopod fauna consisting of only three species, in contrast to totals ranging between 23 and 36 species for localities in eastern Indonesia. Analysis of endemism The largest denable endemic units are consistent with the major biotic realms that are universally recognized (Briggs, 1974): Indian Ocean, Western Pacic, and Pacic Plate (Figure 7). Although not part of the present analysis, the eastern Pacic region possesses a highly unique fauna, which is more closely related to that of the western Atlantic. This relationship reects a common ancestry resulting from the interconnection of the two areas prior to nal closure of the Panamanian land bridge, which occurred about 3.1 million years ago (Coates and Obando, 1996). Few species are common to both the West Atlantic and East Pacic, but numerous genera and sister-species are shared (Allen and Robertson, 1994). The reef-sh fauna of the Indo-west and central Pacic is remarkably homogenous at family and generic levels. There are also numerous wide-ranging species that occur in two or more of the major realms. However, the present analysis is primarily concerned with species that are conned to one of the major realms or exhibit more restricted ranges. Both West Pacic and Indian Ocean realms are characterized by relatively high levels of endemism with approximately one endemic for every 34 species in the respective areas (Table 2). Although the level of endemism for the Central Pacic is considerably less, this analysis supports the ndings of Springer (1982), who recognized the Pacic Plate as a discrete sub-unit of the Indo-Pacic region. Tables 35 present a listing of globally signicant areas for reef sh endemism based on three dierent criteria: absolute numbers, percentage of the overall fauna, and number of endemics per unit area. Most of the locations indicated in Table 3 are well known for their extraordinary high levels of endemism (Randall, 1998), but several have received minimal attention. For example, the Marquesas were omitted by Roberts et al. (2002) in their summary of marine hotspots. These islands harbour a wealth of endemics, recently highlighted by Randall (2005). Similarly, the Lesser Sunda Islands of Indonesia and coastal Oman have

Figure 7. Major biotic realms of the tropical Indo-west and central Pacic region. Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Table 2. Comparison of reef sh diversity and endemism for major biotic realms of the Indo-west and central Pacic region

Realm Indian Ocean West Pacic Central Pacic (Plate)

Total spp. 2086 2989 1403

Endemics 532 938 130

Endemism (%) 25.5 31.4 9.3

Table 3. Highest ranked areas in Indo-west and central Pacic region based on total number of endemic reef shes

Location Hawaiian Islands Mascarene Islands Marquesas Islands Great Barrier Reef FijiTonga Islands Western Australia Northern Red Sea Lesser Sunda Islands Papua New Guinea-Solomon Islands Southern Japan Oman Easter Island Birds Head Peninsula, Indonesia Central Philippines

Endemic spp. 86 37 36 34 29 27 26 25 25 24 22 20 16 14

Total spp. 420 819 507 1455 1115 1302 778 1682 1680 1466 581 87 1230 1653

Table 4. Highest ranked areas based on percentage of endemic reef shes

Locality Easter Island Baja California Hawaiian Islands Galapagos Islands Red Sea Marquesas Islands Clippperton Island Isla del Coco Mascarene Islands Oman

Number of species 87 400 420 300 861 507 103 192 836 581

Number of endemics 20 80 86 35 95 36 8 10 37 22

Endemics (%) 23.0 21.6 20.5 11.7 11.0 7.1 5.8 5.2 4.4 3.8

recently emerged as signicant centres (Randall, 1995; Allen and Adrim, 2003). There is strong justication for uniting Fiji and Tonga into a single area of endemism based on a nucleus of species that are shared by the two countries. Similarly, analysis of the Papua New GuineaSolomon Islands region reveals a signicant number of shared elements. Their close geographic relationship is also indicative of a natural faunal unit. The Birds Head Peninsula of Indonesia, occupying the extreme western end of the island of New Guinea is perhaps the most obscure location on the list. Currently 20, mainly undescribed taxa are believed to be
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Table 5. Highest ranked locations for endemism based on the number of endemic shes per km2 of coral reef habitat

Locality Clipperton Island, E. Pacic Isla del Coco, E. Pacic Easter Island Malpelo Island, E. Pacic Rapa Pitcairn Islands Christmas Island, Indian Ocean Komodo Islands, Indonesia Reunion Mauritius

Area (km2) 13 37 253 12 91 80 230 1600 3500 2800

Number of endemics 6 10 20 3 7 4 2 6 3 12

Reef area (km2) 4 12 33 6 28 24 34 217 103 870

Endemic spp./km2 1.5 0.83 0.61 0.50 0.25 0.16 0.06 0.03 0.03 0.01

restricted to this area and current research by the author and M. Erdmann will most likely increase this total. Within this area, Cenderawasih Bay (due south of the islands of Biak and Yapen), is particularly notable, harbouring at least six endemics. Allen and Erdmann (2006) hypothesized that the bay was essentially isolated for a substantial period over the past ve million years and present day geographic and oceanographic conditions continue to provide a degree of isolation. Table 4 provides a list of the 10 highest ranked hotspots for endemic reef shes based on the percentage of the overall fauna. Easter Island with 23% endemism heads the list in this category and the majority of other locations are relatively remote oceanic outposts where speciation has occurred due to reduced gene ow from outlying areas. Isolated oceanic islands are also the highest ranked locations in terms of the number of endemic shes per unit area (Table 5). Clipperton Island in the eastern tropical Pacic easily heads the list. This tiny atoll, with a shallow reef area of only 13 km2 has an impressive total of six endemics (Robertson and Allen, 1996; Allen and Robertson, 1997). Numerous species are known on the basis of only a few specimens collected at a single location and therefore provisionally qualify as local endemics. If known only from isolated oceanic locations there is an excellent chance their status as a localized endemic is valid in contrast to regions where there are more or less continuous reef areas (e.g. Southeast Asia). In the latter case, the endemic status must be viewed with suspicion until conrmed or denied by considerable collecting/observation eort in adjacent areas. Fishes from tiny oceanic islands such as Malpelo, Clipperton, and Easter, possess some of the smallest known ranges for tropical reef shes. For example, the wrasse species Halichoeres malpelo (Allen and Robertson, 1992) occupies an area of less than 12 km2. Restricted-range endemics from non-oceanic areas generally have more extensive distributions. One of the smallest known ranges in the latter category is that of the pomacanthid angelsh Chaetodontoplus vanderloosi (Allen and Steene, 2004), which is conned to an area of cool-upwelling in south-eastern Papua New Guinea occupying less than 250 km2. Even the distribution of the popular aquarium sh Pterapogon kauderni (Apogonidae), which occupies about 17 000 km2 o the eastern coast of Sulawesi, is considered to be extremely small compared to that of most reef shes (Allen and Steene, 1995; Allen, 2000).

DISCUSSION Many of the hotspots identied by this study have already received considerable conservation attention by local non-governmental organizations (NGOs) or large global organizations such as Conservation
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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Table 6. Frequency of Napoleon wrasse (Cheilinus undulatus) for various locations in the Coral Triangle (G. Allen data)

Location Raja Ampat Islands } 2002 Raja Ampat Islands } 2001 Halmahera (southwest) } 2005 Togean/Banggai Islands } 1998 Calamianes Is., Philippines } 1998 Weh Island, Sumatra } 1999

Number of sites where seen 9 7 4 6 3 0

Percentage of total sites 18.0 15.55 14.8 12.76 7.89 0.00

Approx. number seen 14 7 4 8 5 0

International (CI) and The Nature Conservancy (TNC). The latter two American-based organizations have been particularly active in critical conservation areas throughout the Coral Triangle. Much of their eort is focused on Indonesia and the Philippines, two megadiversity centres that share an acute need for urgent conservation measures. Both countries have experienced a rapid decline in marine resources, particularly over the past three decades. Much of the blame is attributed to the widespread use of illegal shing methods, of which cyanide and explosives are among the most destructive to reef environments. McAllister (1988) conservatively estimated that 75 000 kg or 1500 drums of cyanide were being sprayed onto Philippine coral reefs each year. The insatiable oriental market for shark ns and live reef shes has seriously depleted stocks of groupers (Serrandiae) and other large shes throughout the Coral Triangle. One of the prime targets of the Asian-based live restaurant sh trade is the Napoleon wrasse (Cheilinus undulatus), one of the largest species of reef sh, growing to well in excess of 100 cm. Young sh (under about 50 cm) are generally targeted because they are easier to ship and market. The author has noticed an appreciable decline in this species since his rst visit to Indonesia in 1974. Indeed, data gathered on recent biological surveys in the Coral Triangle indicate that it is rare or absent at most locations (Table 6). This species is now listed in Appendix II of CITES, but illegal trade will no doubt continue as long as the huge demand remains on the Asian market. Conservation hotspots are not necessarily the sole domain of the megadiversity heavyweights highlighted in Table 1. Aside from a few regional pockets of endemism within the species-rich Coral Triangle, this study supports the contention of Hughes et al. (2002) that centres of high species richness and centres of high endemism are generally not concordant. Therefore, a two-pronged strategy embracing both diversity and endemism is essential to the design of any broad-scale marine protected area (MPA) network. Moreover, due to the vagaries of marine dispersal it is vital for all countries throughout the Indo-Pacic region to work together towards the common goal of conserving biodiversity. Unlike terrestrial systems where restricted-range species are an important component of local diversity, marine systems are characterized by prodigious numbers of wide-ranging species. The current analysis reveals an average range of 9,357,070 km2 for Indo-central Pacic reef shes or roughly the size of China. Approximately 40% of species have geographic ranges spanning more than 10,000,000 km2. Even so called limited-range endemics have distributions that frequently cross political boundaries, requiring multi-national conservation initiatives. In general, limited-range marine endemics occupy much larger areas than their terrestrial counterparts, with the exception of those conned to tiny oceanic islands. Reef shes of the Indo-west and central Pacic occupying an area of less than 120,000 km2 or 10.8% of the total species are justiably classed as having restricted distributions and therefore merit conservation attention. The endemic centres listed in Tables 35 can justiably share the conservation limelight with megadiversity areas. Oceanic islands and archipelagos are particularly strong centres of endemism. Genetic studies of reef shes currently in progress by the author and collaborators from Boston University indicate that island endemism may be considerably more prevalent than formerly believed. For example,
Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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recent DNA analysis reveals that six populations from Fiji previously considered as geographic colour variants of wide ranging species are genetically distinct lineages. Although there is only one case involving the recent extinction of a reef sh (Ferreira et al., 2005), coral reefs are increasingly at risk. Coral bleaching, elevated sea temperatures, destructive shing practices, and sedimentation due to careless logging or agricultural practices are among the most obvious threats. There is an urgent need to establish a network of MPAs throughout the Indo-Pacic and other tropical seas. There is still much to learn about life history cycles of reef shes and especially sourcesink relationships of marine larvae, 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 network of MPAs as soon as possible. A logical strategy would be to establish MPA networks focused on the 14 key endemic areas listed in Table 3. This plan would not only provide a refuge for 415 limited range endemics, but if carefully designed could also provide a measure of protection for up to 82% of the total reef sh species in the Indo-west and central Pacic region. Admittedly, this plan may sound over-simplied, especially in light of the argument that most existing MPAs are too small and too far apart to eectively maintain genetic connectivity (Rodrigues and Gaston, 2001). However, such a network would provide a strategic foundation for future MPA expansion that will be necessary once critical information on genetic connectivity is revealed. Moreover, there is increasing evidence (Jones et al., 2005) for highly localized self-sustaining recruitment in reef sh populations. For example, Jones et al. (1999) estimated that 1560% of juvenile damselsh (Pomacentrus amboinensis) self-recruited back to their natal population at Lizard Island on the Great Barrier Reef. Accordingly, Leis (2002) suggested the geographic size of management-conservation units is probably much smaller than previously thought, perhaps on the scale of 10 s of km2. The Birds Head region (far western New Guinea) of Indonesia provides an excellent working example of how grass roots conservation is being implemented in one of the key areas in Table 3. Major biological assessment surveys conducted by CI (McKenna et al., 2002) and TNC (Donnelly et al., 2003) conrmed this region as an exceptionally rich corridor for both diversity and endemism. The urgent establishment of an MPA network was recommended to appropriate local and national agencies on the basis of the rapid assessment ndings. Over the following four-year period government ocials, in consultation with local and international NGOs, formulated a strategic network of seven MPAs (Figure 8), occupying a total surface area of approximately 6540 km2, scheduled for implementation in mid-2007. The combination of

Figure 8. Map of the Birds Head Peninsula of western New Guinea showing proposed MPA network (shaded areas on main map). Abbreviations as follows: CB } Cenderawasih Bay; RA } Raja Ampat Islands; TB } Triton Bay. Copyright # 2007 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc

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the seven Raja Ampat MPAs, an existing national park in Cenderawasih Bay and a proposed MPA at Triton Bay will provide a refuge for 1264 species of reef shes, including at least 20 suspected endemics. The Birds Head conservation initiative represents an important addition to an Indo-Pacic network that currently includes major MPA networks on Australias Great Barrier Reef (347 800 km2) and the north-western Hawaiian Islands (362 580 km2). Hopefully, the remaining 10 regions listed in Table 3 will initiate similar action. The current analysis of reef sh distributions provides crucial baseline information for prioritizing conservation initiatives in the speciose Indo-west and central Pacic region. The next logical step is to expand the database to include the eastern Pacic and Atlantic oceans in order to provide a truly global perspective. The maps generated in this study can also be utilized in the IUCN Red List assessment process, which is currently commencing for Indo-Pacic coral reef shes. Because there is a general scarcity of basic information pertaining to abundance and past population trends, range size will assume extra importance in determining the vulnerability of many reef shes.

ACKNOWLEDGEMENTS
The mapping study and GIS analysis was funded by Conservation International (CI). I am particularly indebted to Roger McManus, Director of Global Marine Programs at CI for his encouragement and support of this project. Robert Waller, formerly employed by CIs GIS laboratory, designed and implemented the analytical programs. Additional technical support was provided by GIS laboratory sta John Musinsky and Erica Ashkenazi. I am also grateful to Tim Werner and Sheila McKenna, past and present directors of CIs Rapid Assessment Program (RAP) for providing eld opportunities for me that helped to ll critical gaps in the distribution data. I thank the following ichthyological specialists for contributing their distributional knowledge of specic families and/or strategic geographic locations: Hans Bath (Blenniidae), Kent Carpenter (Caesionidae and Lethrinidae), Howard Choat (Scaridae), Bruce B. Collette (Belonidae, Hemiramphidae, and Scombridae), Tom Fraser (Apogonidae), Ofer Gon (Apgogonidae), Hans Fricke (Callionymidae and Tripterygiidae), Anthony Gill (Pseudochromidae), David Greeneld (Holocentridae and Fiji), Martin Gomon (Labridae), Douglass Hoese (Gobiidae), Phillip Heemstra (Serranidae and western Indian Ocean), Barry Hutchins (Monacanthidae), Je Johnson (Haemulidae), Leslie Knapp (Platycephalidae), Helen Larson (Gobiidae), Peter Last (Carcharhinidae and Dasyatidae), Je Leis (Diodontidae), Rudie Kuiter (Syngnathidae and Indonesia), John McCosker (Muraenidae and Ophichthidae), Scott Michaels (Hemiscyllidae), Randy Mooi (Plesiopidae), Phillip Munday (Great Barrier Reef and Papua New Guinea), Theodore Pietsch (Antennariidae), Richard Pyle (Pomacanthidae), John Randall (Mullidae, Labridae, Scaridae, Acanthuridae and numerous Indo-Pacic localities), Ross Robertson (tropical Eastern Pacic), Barry C. Russell (Nemipteridae), Werner Schwarzhans (Bythitidae), William Smith-Vaniz (Carangidae and Opistognathidae), Victor Springer (Blenniidae), Jerey Williams (Blenniidae and Trypterygiidae), Richard Winterbottom (Gobiidae and Vietnam), and David Woodland (Siganidae). Finally, I express my sincere thanks to John Briggs, Kent Carpenter, Roger McManus, Russell Mittermeier, and Victor Springer, who critically reviewed the manuscript and oered helpful suggestions for its improvement.

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Aquatic Conserv: Mar. Freshw. Ecosyst. 18: 541556 (2008) DOI: 10.1002/aqc