As threats to global biodiversity accelerate while the world’s human population and its resource use continue to grow, and biodiversity conservation resources remain insufficient to reduce biodiversity loss, focusing and prioritizing conservation action is essential. Several biodiversity conservation priority-setting approaches have been proposed. The initial focus was on identifying species of comparatively highest risk of extinction, an approach culminating in the IUCN Red List of Threatened Species (www.iucnredlist.org) and numerous national and regional Red Lists. Soon thereafter, different (although largely compatible) approaches to identify priority conservation areas were developed, tested and adopted, including biodiversity hotspots (Myers 1988, 1990; Mittermeier et al. 1999, 2004; Myers et al. 2000), megadiversity countries (Mittermeier et al. 1997), ecoregions (Olson et al. 2001; Abell et al. 2008), high-biodiversity wilderness areas (Mittermeier et al. 2002), and key biodiversity areas (Langhammer et al. 2007). The underlying premise among these approaches has been that by focusing conservation action in areas with high species richness, high endemism and irreplaceability (Rodrigues et al. 2003), deep phylogenetic diversity, as well as high percentages of threatened species and high levels of systemic threats to the areas (e.g., rates of habitat degradation and loss), the maximum conservation outcome could be achieved per unit conservation effort.

Slightly over half of all turtle species have been assessed as threatened with extinction based on IUCN Red List criteria (official and draft threat assessments by the IUCN Tortoise and Freshwater Turtle Specialist Group; www.iucnredlist.org, www.iucn-tftsg.org), one of the highest percentages of any major group of vertebrates (Turtle Conservation Coalition, 2011; Turtle Taxonomy Working Group [TTWG] 2014). Therefore, turtles clearly represent a global biodiversity conservation priority. Because of their particular value to humans, whether as food, medicine, pets, or as providers of ecological services, and their very slow recovery from (over)exploitation, turtles tend to be at the cutting edge of biodiversity decline and an indicator of ecosystem degradation. The distribution of turtle species and subspecies, and the occurrence of deep phylogenetic lineages, is not uniform across the planet.

Thus, as a contribution to maximizing the effect and efficiency of turtle conservation efforts, we analyze the occurrence of tortoises and freshwater turtles in the priority conservation areas established and refined by Conservation International, the biodiversity hotspots (BHS), the high-biodiversity wilderness areas (HBWA) and other wilderness areas (OWA), and the megadiversity countries. An initial analysis of turtle species richness in BHS, HBWA, and OWA was carried out by Buhlmann et al. (2009:table 3). In this article, we update that analysis in the context of an updated turtle taxonomy (TTWG 2014) and extend it to the level of terminal taxa (subspecies). Numbers of species and taxa occurring in megadiversity countries have been presented in table 3 of TTWG (2014) and are repeated here. Ecoregions hosting unique or near-unique turtle occurrences, as demarcated by distribution ranges defined by hydrologic unit compartments (HUC), were presented by Buhlmann et al. (2009, appendix 1).

Ideally, a global prioritization of turtles should incorporate the IUCN Red List status of individual species and subspecies, as was done for Asia by Stuart and Thorbjarnarson (2003). However, because not all turtle species worldwide have been officially assessed for the Red List, such an analysis is still forthcoming but is planned for when the required data sets are completed.

METHODS

Definitions of BHS and HBWAs were obtained from the most recent reviews of these conservation priority areas (Mittermeier et al. 2002, 2004), including both mapped geographical extent as well as habitat and topographical descriptions and definitions. Turtle Priority Areas (TPA) were defined by Buhlmann et al. (2009). Turtle megadiversity countries were derived from table 3 of TTWG (2014). After an initial determination of taxon richness per predefined priority area, it became evident that two clusters of smaller areas originally defined by exceedingly rich and unique floras (the adjoining Cape Floristic, Maputaland–Pondo–Albany, and Succulent Karoo biodiversity hotspots) and based on ecoregions (the tropical Australian TPA, including the Arnhemland and Cape York Savannah ecoregions) did not rank highly in the global analysis but that each cluster collectively is inhabited by a rich turtle fauna that is largely endemic to the cluster. Therefore, we combined these sets of adjoining priority areas and evaluated the turtle richness of these combined areas, designating them the southern African TPA and the north and east tropical Australian TPA, respectively.

The taxonomy and the numbers of tortoise and freshwater turtle genera, species, and terminal taxa (subspecies) used in this analysis follows TTWG (2014). In cases where TTWG (2014) presented alternate taxonomies of taxon rank (e.g., Chrysemys dorsalis as a full species, or as a subspecies of Chrysemys picta) or genus allocation (e.g., Actinemys or Emys), the rank (species or subspecies) first used in the checklist entry, and the finest genus resolution in the case of split versus combined genera (e.g., Actinemys) was used for the calculations of taxon richness. Extinct species, extirpated national or regional population occurrences, and established populations of recently introduced nonnative species were not included in total richness assessments; marine turtles of the families Cheloniidae and Dermochelyidae were also excluded from the analysis.

Methodology to determine the number of turtle genera, species, and taxa occurring in a particular conservation priority area followed that of Myers et al. (2000). Distribution ranges of turtle species used for this analysis were mapped based on a combination of the locality maps provided by Iverson (1992a), GIS files prepared for the Buhlmann et al. (2009) analysis, and additional data sources listed in the TTWG (2014) checklist. Turtle range maps were included in TTWG (2014), although the current analysis used earlier, preliminary versions. Turtle taxa whose ranges overlapped with BHS, HBWA, and TPA were scored as “present”, and a preliminary species list per priority area was generated. However, a simple overlap of turtle distribution maps and priority areas will create “false positives” in cases where the ecology of the turtle taxon is incompatible with the available habitat, topography, or altitude in the priority area. For example, significant mapping overlap exists between the Madrean Pine–Oak Woods BHS and the distribution range of Kinosternon arizonense, and indeed, this species of the desert floor may occur within sight of the montane “sky islands” of the BHS, but it has never been recorded from this topography. Neither the resolution of the GIS data for the priority area boundaries nor the turtle distribution ranges is adequate to avoid such false positives. Thus, a second pass was made through the data set to evaluate the correctness of the preliminary species lists per priority area, and species whose inclusion or exclusion drew our attention were evaluated in more detail based on a wide range of available information (specimen locality data, published literature, and expert consultation). Based on such evaluations, admittedly subjective and perhaps nonrepeatable to some extent, final species lists were prepared. We consider that the increased resolution and accuracy from this second, expertise-based evaluation more than makes up for the errors inherent in mathematically repeatable but bio-ecologically flawed analysis and results.

If a species has been questionably reported (as indicated by “(?)” in the TTWG 2014 checklist) as native to a particular area, it was counted as part of the turtle fauna (erring on the side of maximum richness). When assessing numbers of endemic species, taxa and genera in a particular country or area, only confirmed occurrences were considered (i.e., an unconfirmed report of occurrence in a neighboring country does not make a species no longer endemic to the single country from which it is confirmed to occur).

RESULTS AND DISCUSSION

Table 1 and Fig. 1 present the numbers of total and endemic species and taxa occurring in the BHS, HBWA, and TPA with highest richness and diversity of turtles, whereas Table 2 and Fig. 2 present corresponding turtle richness numbers for the turtle-rich countries (for the purposes of this analysis, the United States was analyzed and depicted as the contiguous 48 states only, because neither Hawaii nor Alaska have native tortoises or freshwater turtles). As Tables 1 and 2 show, there appeared no natural breaks in numbers of total or endemic species or taxa, and an arbitrary threshold for inclusion was set at 10 species for priority areas and at 15 species for the top turtle megadiversity countries.

Table 1. Taxon richness of living tortoises and freshwater turtles per turtle hotspot, arranged by richness of species and taxa in biodiversity hotspots (BHS), high-biodiversity wilderness areas (HBWA), or turtle priority areas (TPA).

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Table 2. Taxon richness of living tortoises and freshwater turtles of turtle-rich countries, arranged by richness of species and taxa.*  =  Megadiversity countries (Mittermeier et al. 1997).

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Particularly noteworthy is that 83% of species, 79% of all taxa, 84% of genera, and all families are represented in the remaining natural habitats of these 16 TPA, which collectively represent no more than 7.0% of the planet’s land surface. Further analysis and selection of priority areas could increase this already high taxon density even further (e.g., by excluding the Sundaland BHS, a substantial land area would be excluded, but only one genus and two species would be lost from the combined turtle numbers), but for the current analysis total richness per area was used, rather than complementary richness that would add to already selected areas. In general, the broad patterns of turtle distribution, species richness, and species diversity emerging from our analysis correspond closely to the earlier analysis based on geography (Iverson 1992b) and on HUC (Buhlmann et al. 2009).

From this and other analyses of the biogeography, diversity, and species richness of turtles, it is evident that there are 2 major regions of exceptional turtle richness. Buhlmann et al. (2009) identified the Mobile Bay area of Alabama and the Ganges–Brahmaputra confluence region as the two sites globally where 18 or 19 turtle species coexist. Our analysis documents that these two areas are at the center of wider regions of turtle richness and diversity. As one looks at adjoining river systems, faunal turnover becomes apparent, and the total species and taxon richness of these wider regions amounts to multiple times the richness of an individual river system. Specifically, the 18-species Mobile Bay HUC is at the core of the 42-species southeastern US TPA, whereas the Ganges–Brahmaputra confluence is within the 41-species Ganges–Brahmaputra floodplain region, which in turn adjoins the 50-species IndoBurma BHS. Both regions of exceptional turtle richness and diversity share a tropical to subtropical climate and roughly north–south trending of both hill and mountain ridge systems and major river valleys on geologically old and stable land masses.

The wider tropical–subtropical Asian region, extending from the Himalayan foothills and Ganges–Brahmaputra lowlands through monsoonal Southeast Asia into southern China and Sundaland, is characterized by a high number of turtle genera and low number of subspecies compared with the number of species (e.g., Fig. 3C–D). Major breaks between the component BHS and their turtle faunas are associated with north–south trending geological compression zones (i.e., the Arakan range, the Dawna range, and the Annamite mountains, each of which separates turtle faunas which are only partly similar to each other at genus and species level, a pattern that was documented for freshwater fish in this region by Kottelat [1989]). The other region of exceptional turtle species richness is the southeastern United States, connecting to the deserts and tropical lowlands of MesoAmerica. The great taxon richness of the southeastern United States is characterized by dynamic, geologically recent (sub)speciation, particularly in the strictly riverine genera Graptemys and Apalone, evidently associated with river basin separation resulting from sea level changes (Ennen et al. 2010; Ehret and Bourque 2011). Although the southeastern United States has not been identified as a high-diversity wilderness or hotspot area based on vegetation diversity combined with deforestation rates (Myers et al. 2000), its biodiversity significance has been highlighted for freshwater fish and molluscs (Lydeard and Mayden 1995; Olson et al. 2001).

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In contrast, turtles rarely reach exceptional richness in the two areas documented as having the globally highest richness and diversity of amphibians, birds, or mammals, being Amazonia and the tropical Andes, and the forest arc stretching from west Africa through the northern Congo Basin to the east African montane region (Baillie et al. 2004:fig. 5.4). The biogeographical reasons for the modest turtle species richness in these areas are not evident. The excellent connectivity for turtles across these wide ranges by way of the extensive river systems evidently results in sufficient gene flow among and between freshwater turtle populations in rivers and tributaries, and among terrestrial turtle species dispersing during flood events, that a fairly homogenous turtle fauna remains established across these wide regions. However, further phylogenetic research may show that current understanding of turtle taxonomy for these areas underestimates their true turtle diversity and richness (e.g., Cyclemys: Fritz et al. 2008; Lissemys: Praschag et al. 2011; Pelomedusa: Petzold et al. 2014) or conversely may argue that North American and Mediterranean diversity is overemphasized (e.g., Testudo: Parham et al. 2006; Pseudemys: Spinks et al. 2013).

An area of corresponding species richness and diversity for turtles as well as amphibians, birds, and mammals is the MesoAmerica hotspot, stretching from tropical Mexico to Panama. Not only is it the third-richest region for turtles (27 species, 40 taxa), it also has some of the highest numbers and percentages of endemic species (16 species, 59%) and endemic taxa (31, 78%), including being the only priority conservation area to which an entire family is endemic (Dermatemydidae, Fig. 3E), as well as the subfamily Staurotypinae with its two genera.

Adjoining MesoAmerica is the remarkable diversity of the Rio Magdalena basin of northwestern Colombia. Although total species richness in northwestern Colombia is not spectacular (11 species; Fig. 3F), its endemism level is quite high, and it is the only region in the world where seven different turtle families occur together.

It is remarkable that the richest wilderness area for turtles, whether measured by total species, total taxa, or endemic taxa, is the deserts of North America wilderness area, which proves slightly richer than the next-richest wilderness area, Amazonia (Table 1). The geographical isolation of waterbodies in these deserts has stimulated an evolutionary radiation in the genera Trachemys and Kinosternon, many of which are endemic to isolated watercourses. Amazonia is the richest wilderness area in terms of genera and families and nearly equals the North American deserts and New Guinea for the highest number of endemic species (Table 1). These numerical findings contrast sharply with the results of Buhlmann et al. (2009), who documented Amazonia as one of the richest turtle regions and the North American deserts as a species-poor region. The results derive directly from the different ways of calculating local species richness. Buhlmann et al. (2009) calculated the likely number of species per hydrological area within the wilderness area, and nearly all North American desert turtle assemblages consist of no more than 4 taxa per site or HUC (generally a Kinosternon, a Trachemys, and occasionally a third freshwater species, plus often a tortoise or Rhinoclemmys). Nevertheless, when aggregated across the total wilderness area, the combined turtle taxon richness and endemicity are high. A contrasting assemblage is apparent in the environmental stability of Amazonia, where most species range widely throughout the wilderness area, with little or no apparent regional variation or speciation.

Although excluded from this analysis, the distribution of extinct species and subspecies of turtles in a geographical and ecological context is worth comment. A total of 9 species and 2 subspecies of turtles are recorded as having gone extinct in recent history, since 1500 AD (TTWG 2014:table 1). These extinctions have occurred either on small oceanic islands of the Mascarenes (Cylindraspis spp.; Aldabrachelys gigantea daudinii; Pelusios castaneus seychellensis) or Galapagos archipelago (Chelonoidis nigra, Chelonoidis abingdonii, Chelonoidis phantastica) or in “habitat islands,” discrete areas of critical habitat that were degraded, as in the case of Kinosternon hirtipes megacephalum, known from a single desert spring system that dried out.

Comparing and contrasting the different analytical approaches, it becomes evident that tortoises and freshwater turtles do not show globally consistent patterns of richness and endemism at species and terminal taxon rank. To some extent, this is a function of the mapping approach employed, as well as of the size and definition of the priority areas concerned, a finding consistent with the conclusions of Bombi et al. (2011). No single TPA exceeds all other areas in all important prioritization statistics. Each of the most turtle-rich priority areas or megadiversity countries takes first place in some measure of richness at family, genus, species or taxon level or at endemism level. Every turtle taxon, and every region and area, is unique in one way or another and deserves targeted conservation effort. Greatest effects can likely be achieved by focusing efforts on the areas and countries with highest diversity and endemism identified in our analysis.