*David R. Bellwood, School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia. E-mail: email@example.com
Coral reefs exhibit highly congruent patterns of biodiversity, with a prominent hotspot in the Indo-Australian Archipelago (IAA). Unlike many terrestrial systems, the IAA hotspot exhibits extensive latitudinal and longitudinal biodiversity gradients. Conflicting hypotheses have highlighted the importance of the area as a centre of origin, overlap or accumulation, with the location of endemics being used as the primary criterion for testing these hypotheses, by identifying the presumed geographical origins of species. We evaluate the utility of marine endemics for resolving these hypotheses, and examine recent molecular phylogenetic evidence for coral reef species that has revealed the antiquity of the endemics and the other species that make up this hotspot. These analyses emphasize the importance of the IAA in the survival rather than the origins of species.
Hotspots have been delimited in both terrestrial and marine realms (Myers et al., 2000; Roberts et al., 2002). In marine systems, the greatest diversity of marine life is seen on coral reefs, and it is in this system that one can see what is arguably the world’s greatest biodiversity hotspot. The Indo-Pacific represents a single biogeographical region that encompasses approximately two-thirds of the equatorial tropics. Within this region, coral reef biodiversity increases, both latitudinally and longitudinally, as one moves towards a hotspot in the Indo-Australian Archipelago (IAA) (Rosen, 1981; Briggs, 2000, 2005; Roberts et al., 2002; Mora et al., 2003). Known by a wide variety of names, from the Malay Archipelago to the Coral Triangle (the nomenclature is reviewed by Hoeksema, 2007), this area exhibits a distinctive ‘bulls-eye’ pattern of diversity (Fig. 1).
Most major coral reef groups exhibit the same pattern. The IAA contains the highest biodiversity of corals (Hughes et al., 2002), reef fishes (Bellwood & Hughes, 2001), bryopsidale macroalgae (Kerswell, 2006), and several gastropod and crustacean groups (Hoeksema, 2007). Depending on the taxon, the gradient in species richness decreases two- to 50-fold as one moves east from the IAA across the Pacific. Corals, for example, range from over 550 species at sites in Indonesia to c. 150 species in French Polynesia, and just seven on Clipperton Atoll (Glynn et al., 1996; Hughes et al., 2003). This hotspot challenges many evolutionary and ecological theories; for many years it was viewed as the source of new species, that is, the source of heat was thought to be within the hotspot.
Explaining the global marine biodiversity hotspot
Stehli & Wells (1971) first identified the latitudinal and longitudinal bulls-eye pattern in a review of global coral reef genera. Their pattern was extremely convincing, and has proved robust for many disparate groups. Subsequent explanations for its origins have been less convincing. For latitudinal changes, one can draw on the plethora of hypotheses that have been proposed to account for latitudinal tropical–temperate diversity gradients (Willig et al., 2003). However, the marine hotspot exhibits both latitudinal and longitudinal gradients (Bellwood & Hughes, 2001). With no clear physical boundaries, these gradients span over 75° of latitude and 245° of longitude, approximately two-thirds of the equatorial tropics. These strong longitudinal gradients preclude many of the tropical–temperate hypotheses.
In contrast to terrestrial systems, therefore, relatively few models have been proposed to explain this bulls-eye-shaped marine biodiversity hotspot. Over the past 30 years, discussions have revolved around three main alternative, but not mutually exclusive, models: centre of origin, centre of overlap, and centre of accumulation (Rosen, 1981; Potts, 1985; Bellwood & Wainwright, 2002; Hoeksema, 2007). The centre-of-origin model has its roots in Darwinian pre-continental drift ideas, with species arising in a specific location or centre, and dispersing out. Applied to the IAA, this model assumes that species arise within the IAA and that the hotspot is a by-product of the relative dispersal abilities of species (Briggs, 2000; Mora et al., 2003).
Finally, the centre-of-accumulation model (Ladd, 1960; Rosen, 1981; Potts, 1985) suggests that species arise outside the IAA, before expanding or being carried into the IAA. The hotspot is therefore a result of the accumulation of species from outside. Proposed sites of origin include nearby island arcs (Rosen, 1981) or Pacific islands (Ladd, 1960; Paulay, 1997). The critical role of the IAA is in accumulating species (as a museum or refuge), with the species arriving either individually (Ladd, 1960) or as part of entire biotas as a result of the rafting, accretion or suturing of land masses following tectonic events (Remington, 1968; McKenna, 1973; Santini & Winterbottom, 2002). In this model, accumulation may be enhanced by differential rates of extinction, with the area having lower rates of extinction and thus functioning as a centre of survival (Potts, 1985; Barber & Bellwood, 2005).
Theoretical considerations and recent molecular phylogenetic data both suggest that this assumption – that endemics usually mark the site of origin of a species – is not necessarily true, especially for taxa with good dispersal abilities and long evolutionary histories. The critical questions are: (i) are coral reef endemics relatively young (Pleistocene, <2 Ma), and (ii) do they indicate the location where species arise?
The passage of species through time
Within coral reef biogeography, many workers have assumed that sea-level changes during the Pleistocene were important drivers of speciation in coral reef systems and that, with such recent origins, the distribution of endemics is a good basis for identifying areas with exceptionally high rates of origination (Briggs, 2000, 2005; Mora et al., 2003; reviewed by Hoeksema, 2007). However, for widely dispersing taxa there remains a strong possibility that many of these endemics are relictual, especially in non-peripheral locations. In this scenario, as a species’ range contracts the remaining population eventually becomes a relictual endemic (this is testable using fossils: fossils outside extant ranges would indicate relictual species). It is axiomatic that all species are endemics at the point of extinction. In contrast, species will be endemics close to the point of origination only if they are a product of a spatially restricted speciation event (founder effects, peripatry) (Gaston, 2003; Coyne & Orr, 2004). In the taxa that most clearly mark the biodiversity hotspot (characterized by relatively large geographical ranges spanning the IAA hotspot; Connolly et al., 2003), origination without endemicity is likely. Speciation can thus occur without an initial period of endemism if the smaller population following a split (e.g. vicariance event) is greater than the cut-off for defining an endemic (B″ in Fig. 2).
To date, maps of the IAA hotspot have been based largely on those taxa with relatively large geographical ranges that stack up (like a plate of unevenly sized pancakes) in the IAA (Connolly et al., 2003). Taxa with numerous restricted-range species can display exceptional taxonomic diversity, but they do not stack (Meyer et al., 2005). One species per island can yield high gamma diversity but low alpha diversity. It is in these taxa with numerous restricted-range species that endemism may reflect sites of origin; a situation that requires taxa to exhibit exceptional rates of spatially restricted origins and negligible subsequent range expansion. This may be the case for small reef taxa with limited dispersal capabilities, such as patellogastropods and vetigastropods that lack feeding larvae (Paulay & Meyer, 2002; Kirkendale & Meyer, 2004; Meyer et al., 2005). For species with longer dispersal abilities and large geographical ranges, such as fishes, cowries and most spawning corals, endemism may be of limited relevance for marking geographical origins.
Although preliminary, the estimated ages of these fish and cowrie species agree well with a wide range of other reef taxa (e.g. Halimeda, Kooistra et al., 2002; crustaceans, Knowlton & Weight, 1998; fishes, Klanten et al., 2004), taxa in other tropical marine systems (e.g. mangrove snails, Reid et al., 1996; Williams & Reid, 2004), and the fossil record (Renema et al., 2008). This suggests that the early Pliocene to Miocene ages for endemics are not unreasonable. Furthermore, as the ages are based on original estimates using a range of markers and calibration methods, the high levels of congruence among taxa provide some confidence in the resultant patterns.
The source of heat in hotspots
There are two main implications of these recent molecular discoveries. Firstly, they highlight the difficulties in distinguishing between the three alternative hypotheses.
The search for centres of endemism may be futile if one wishes to identify areas of origin in widely dispersing groups. Centres of endemism are just as likely to reflect areas of reliction. By definition, they are areas where restricted-range species persist. They could be either where species arise and remain, or alternatively the last stand of previously widespread species. Endemism can be lost through either population declines (leading to extinction) or range expansion (becoming too widespread to be an endemic). The locations where they persist must be large enough to support viable populations, while limiting range expansion, but they must also be sufficiently isolated to prevent inundation and introgression by the sister species (Paulay & Meyer, 2002). Interestingly, for most groups the majority of endemics lie in peripheral areas (Bellwood & Wainwright, 2002; Hughes et al., 2002; Jones et al., 2002; Roberts et al., 2002; Connolly et al., 2003). These areas are characterized by a high degree of isolation. Their role in supporting endemism therefore may reflect enhanced survival as endemics, rather than supporting exceptional rates of origination (Bellwood & Wainwright, 2002; Hughes et al., 2002).
Despite the difficulty of using endemics on their own, the combination of sister species-range analysis and accurately dated divergences provides an invaluable tool for identifying potential sites of species origination. With increased taxon sampling, robust tree construction, well calibrated species ages and increased geographical resolution, we will be in a position to evaluate critically the relative contribution of the three main models (and their various subdivisions). Indeed, recent molecular phylogeographical and phylogenetic studies in the IAA have opened up a new understanding of the extent and complexity of divergence events within the region (Barber et al., 2006). Increased analyses of disparate groups are breaking up what were once large geographical ranges into smaller pieces, adding more pancakes to the pile. The extent to which sisters’ ranges overlap, the location of these divergence zones, and the extent to which they stack (i.e. are congruent among taxa) will determine the major drivers of diversity in the region. Future emphasis in the IAA on a multiplicity of taxon pairs will help deconstruct the origins of the marine biodiversity hotspot.
Secondly, the ages of the species within the hotspot emphasize the difference between processes that create and those that maintain biogeographical patterns. If the hotspot is a consequence of evolutionary processes (e.g. exceptional origination rates), then the pattern may be viewed as a historical phenomenon; current conditions may be largely irrelevant. Alternatively, evolutionary processes may play no role, the patterns merely arising from an uneven distribution of extant species, with the ongoing persistence of the hotspot reflecting regional-scale ecological processes. Although geographical patterns are undoubtedly shaped by processes operating over all temporal scales (Willis & Whittaker, 2002), the longevity of reef taxa (including endemics), the widespread occurrence of endemics, and the consistent among-taxon congruence in the size, shape and structure of the IAA hotspot all point to the potential of the IAA to maintain species, regardless of their geographical origins.
For widely dispersing taxa (Fauvelot et al., 2003; Bowen et al., 2006; Klanten et al., 2007), with over 4 Myr in which to disperse, the IAA is clearly an exceptional area in which species can, and probably have, accumulated. Precisely why they have accumulated in this area remains unclear. The relative importance of potential factors such as its role as a Pleistocene refuge, its down-current location, exceptional habitat area and heterogeneity, or distance from the mid-domain, may vary among taxa (Paulay, 1997; Connolly et al., 2003; Bellwood et al., 2005; Kerswell, 2006). However, it is sobering to consider that two of these factors (habitat diversity and reef area) can be, and have been, negatively affected by human activities, including global warming (Wilkinson, 2002; Hughes et al., 2003). By our actions, we may have already reduced the capacity of the IAA to support coral reef biodiversity.
With the current emphasis on marine conservation in the IAA (increasingly termed the ‘coral triangle’ in this context), it is important to understand why our conservation efforts are being focused on this area. The assumption that this area is special because it supports an exceptional number of endemics and acts as a source of new species does not appear to be well supported by current data. Indeed, the areas outside the IAA appear to be equally important in this regard. This distinction at a global scale reflects the current problems operating at much smaller, local scales with marine No-take Areas (NTAs) or Marine Protected Areas (MPAs), where it is the status of seascapes outside the protected areas that can underpin the long-term success of these conservation efforts (Hughes et al., 2005). The regional IAA and local MPAs may both exhibit relatively high biodiversity, yet they both appear to rely, to some extent, on input from outside. Be it geological time scales or just a few decades, it is clear that in the marine realm we cannot neglect areas outside designated areas of exceptional richness, whatever the scale. Like a bed of roses in a field of thistles, the potential for exchange is not one way from ‘good’ to ‘bad’. The IAA is part of the Indo-Pacific realm, while rich MPAs are part of the broader seascape. If we fail to recognize the historical and current ecological value of peripheral, lower-diversity areas we may undermine our current conservation goals. It is perhaps with an eye on the past that we may be best able to plan for the future.
This work arose from discussions at the 3rd International Biogeography Society Symposium, Tenerife. We thank M. Dawson and the IBS marine group for stimulating discussions; B. Hoeksema, J. Pandolfi, W. Renema, T. Hughes, S. Connolly, two anonymous reviewers, and ARC Centre of Excellence for Coral Reef Studies colleagues for insightful comments; and C. Read, A. Hoey and S. Wismer for assistance with figures. This work was supported by the Australian Research Council (D.R.B.) and NSF(DEB-9807316 & 0316338, OCE-0221382) (C.P.M.).
David Bellwood is a Professor of Marine Biology at James Cook University. His research focuses on the evolution and ecology of coral reef fishes. The aims are to understand the processes that generate and maintain coral reef biodiversity and to explore the consequences of variation in biodiversity for ecosystem function. He is also interested in the role of fishes on coral reefs and enhancing or maintaining reef resilience in a changing world.
Christopher Meyer is a research zoologist at the Smithsonian National Museum of Natural History in Washington, DC, and Director of the Moorea Biocode Project. He is interested in diversification processes and patterns in marine systems, especially those associated with coral reefs. His other research interests include the use of DNA barcoding to examine diversity in marine communities.