Results of the global conservation assessment of the freshwater crabs (Brachyura, Pseudothelphusidae and Trichodactylidae): The Neotropical region, with an update on diversity

Abstract The freshwater crabs of the Neotropics comprise 311 species in two families (Pseudothelphusidae and Trichodactylidae) and one or both of these families are found in all of the countries in the Neotropical region (except for Chile and some of the Caribbean islands). Colombia (102 species, 81% endemic) and Mexico (67 species, 95% endemic) are the biodiversity hotspots of freshwater crab species richness and country-level endemism for this region. The results of the IUCN Red List conservation assessments show that 34% of pseudothelphusids and 10% of trichodactylids have an elevated risk of extinction, 29% of pseudothelphusids and 75% of trichodactylids are not at-risk (Least Concern), and although none are actually extinct, 56% of pseudothelphusids and 17% of trichodactylids are too poorly known to assess (Data Deficient). Colombia (14 species), Venezuela (7 species), Mexico (6 species), and Ecuador (5 species) are the countries with the highest number of threatened species of Neotropical freshwater crabs. The majority of threatened species are restricted-range semiterrestrial endemics living in habitats subjected to deforestation, alteration of drainage patterns, and pollution. This underlines the need to prioritize and develop conservation measures before species decline to levels from which they cannot recover. These results represent a baseline that can be used to design strategies to save threatened Neotropical species of freshwater crabs.


Introduction
The Neotropical region occupies the entire South American continent, plus Mexico and Central America, the islands of the Caribbean, and southern Florida. The Nearctic/Neotropical boundary runs through Mexico and passes through the southern parts of Baja California and Sonora, crosses the Meseta Central, and continues to southern Veracruz. The majority of the Neotropical region has a tropical climate with warm water freshwater ecosystems, but the southern part of this region from 10° to 25°S (southern Brazil, Uruguay, Paraguay, Argentina, and Chile) has a subtropical climate with cooler freshwater habitats. Freshwater crabs are found throughout the freshwater ecosystems of the Neotropical region but are notably absent from Baja California and the Yucatan Peninsula (Mexico), southern Florida (USA), some of the Caribbean islands, southern Argentina, and all of Chile.
The objectives of the present study are to describe and update our knowledge of Neotropical freshwater crab diversity of both the Pseudothelphusidae and Trichodactylidae and to describe the patterns of distribution and endemism within these families. We also identify here not only those species that are most vulnerable to extinction, but also those species that are poorly known and obvious candidates for future research attention.

Methods
Comprehensive distributional data for the Neotropical freshwater crabs were compiled from literature and museum records, particularly the major monographs on the Pseudothelphusidae by Rodríguez (1982Rodríguez ( , 1992 and Rodríguez and Magalhães (2005), and  Rodríguez (1992) and Magalhães and Türkay (1996a-c, 2008a-b, 2012). Other regional monographs referred to include those for Colombia (Campos 2005), Ecuador (Rodríguez and Sternberg 1998), Brazil (Magalhães 2003), Peru (Rodríguez and Suárez 2004), and Mexico and Central America (Alvarez and Villalobos 1990, 1994, 1995, 1997, Villalobos et al. 1993, 1999, 2010, Villalobos 2005. Despite these efforts distributional records for most species of freshwater crabs are still likely to be incomplete. Distribution maps presented here are based on specimen-level databases compiled for all species based on all known specimens and includes information from over 2,500 different localities. Individual conservation assessments for all species of Neotropical freshwater crabs assessed by Cumberlidge et al. (2009) using the IUCN Red List categories and criteria at the global scale (IUCN 2003) are provided on the IUCN Red List site (http://www.iucn.redlist.org). Freshwater crab species were assessed for inclusion in one of the Red List categories based on a combination of data on geographic range and/or population levels and related trends (Cumberlidge et al. 2009). The available data were sufficient to make valid assessments of the conservation status of only 150 out of the 298 species known from the Neotropical region at the time, and assessments were not possible for 148 species that were treated as Data Deficient due to a lack of specimens, and of locality and population data (Cumberlidge et al. 2009). Threats were inferred if a species was potentially subject to anthropogenic impacts such as habitat destruction, alteration of drainage patterns, or pollution, especially if it was either not found in a protected area, or if it was found in a protected area for only part of its range. Distribution maps (Figs 1-4) were prepared using ArcView GIS mapping software.

Neotropical freshwater crab families
The Neotropical region has its own distinctly recognizable freshwater crab fauna, with no species occurring in other parts of the world. The Neotropical freshwater crab fauna is not uniformly distributed and species and genus composition changes from country to country (Table 2, Figs 1, 2). The global distributions of all species of the Pseudothelphusidae and Trichodactylidae based on all known localities are shown in figures 1 and 2. The Neotropical freshwater crab fauna today (49 genera, 311 species, 2 families) easily exceeds that of the entire Afrotropical region (18 genera, 145 species, 2 families), but is significantly less diverse than the Palaearctic-Oriental-Australasian region (147 genera, 850 species, 2 families) (Cumberlidge et al. 2009;present work). The Neotropical freshwater crab fauna, which represent 20-22% of the world's freshwater crab species diversity , Yeo et al. 2008, Cumberlidge et al. 2009), is dominated by the highly diverse pseudothelphusids (34 genera, 264 species). Pseudothelphusids are found in 26 out of the 31 countries and reach their highest species richness in South America (Table 2). Pseudothelphusids are found throughout the warmer parts of the Neotropics from Mexico to Central America and the Andes (Venezuela, Colombia, Ecuador, and Peru), and in the Guyanian Shield and Central Brazilian Shield in the Amazon basin ( Fig. 1, Table 2). The majority of pseudothelphusid species live at altitudes greater than 400 m above sea level, with a few Andean species reaching up to 3000 m (Campos 2005).
This family comprises two subfamilies, Epilobocerinae and Pseudothelphusinae . The Epilobocerinae consists of only 9 species in 2 genera (Epilobocera ,   Table 2. Distribution of Pseudothelphusidae (P) and Trichodactylidae (T) in each country in the Neotropical region that has populations of freshwater crabs. First number indicates the number of genera, species, and localities of Pseudothelphusidae, the second number indicates the same data for the Trichodactylidae.

No. GENERA (P, T) No. SPECIES (P, T) South America
Argentina 0 (Rodríguez and Magalhães 2005). The Trichodactylidae is the smallest of all freshwater crab families (15 genera, 47 species) and represents only 4% of the world's freshwater crab diversity. Despite this, the family is widely distributed and has representatives in 16 countries, most of which are in South America (Table 2) (Rodríguez 1992, Yeo et al. 2008, Cumberlidge et al. 2009). The vast majority of trichodactylid species are found below 100 m above sea level in the Magdalena river basin and Lake Maracaibo in Colombia and Venezuela, in the coastal lowlands of the Guyanas and Brazil, and in the lowland river basins of the Amazon, Orinoco, Paraguay, and Parana. A few species of trichodactylids reach up to 900 m above sea level in the Andes foothills (Campos 2005     (Avotrichodactylus constrictus, A. oaxensis, Rodriguezia mensabak, and R. villalobosi) (Magalhães and Türkay 2012); one species (Trichodactylus quinquedentatus) from Colombia and Nicaragua (Smalley and Rodríguez 1972), and one species (Poppiana dentata) from Trinidad (which is also found on the neighboring mainland in Venezuela, Suriname, Guyana, and French Guiana, and in Nicaragua) (Magalhães and Türkay 2008a). The Trichodactylidae includes two subfamilies: the Trichodactylinae, with 3 genera, two from Mexico (Avotrichodactylus and Rodriguezia) and one from South and Central America (Trichodactylus); and the Dilocarcininae, with 9 genera that are found throughout South America (Rodríguez 1992, Magalhães and Türkay 1996a, b, c, 2008a. Interestingly, this classification ) groups together at the subfamily level the four disjunct species of trichodactylids found in Mexico with the genus Trichodactylus that includes species from the Magdalena basin and Amazon slopes in Colombia, a species from Nicaragua and Colombia, species from the Atlantic coastal river systems of southeastern Brazil, and species from the Paraguay and Parana basins in southern Brazil and Argentina.

Hotspots of freshwater crab diversity
Colombia stands out as the most diverse and the most species rich part of the region (21 genera, 102 species, 2 families) ( Table 2) with biodiversity hotspots located in forested mountainous regions where deep valleys and a complex topographical relief are favorable for genetic isolation and allopatric speciation. The pseudothelphusid fauna of Colombia comprises 13 genera and 88 species in one subfamily (Pseudothelphusinae) and four tribes (Hypolobocerini, Strengerianini, Kingsleyini, and Potamocarcinini). There are distinct northern and southern components of pseudothelphusid distribution in Colombia, with the dividing line coinciding with the watersheds of the San Juan, Cauca, and Magdalena river basins. The southern component of this fauna is dominated by Hypolobocera, Lindacatalina, and Moritschus and extends from southern Colombia into Ecuador and Peru, and also includes species from southeast Colombia and the Amazonian and Pacific slopes of Ecuador. The trichodactylid fauna of Colombia comprises 8 genera, 14 species in two subfamilies: Trichodactylinae (one genus) and Dilocarcininae (7 genera).
The next most species-rich country is Mexico (17 genera, 67 species, 2 families) ( Table 2) with a freshwater crab fauna dominated by pseudothelphusids with 15 genera, and 63 species in one subfamily (Pseudothelphusinae) and three tribes (Pseudothelphusini, Potamocarcinini, and Hypolobocerini). Mexico's trichodactylid fauna is much smaller and comprises just 4 species in 2 genera all in the subfamily Trichodactylinae. Freshwater crab diversity in Mexico is highest in the Isthmus of Tehuantepec and Chiapas State, possibly because this is where species from three pseudothelphusid tribes overlap with species of trichodactylids (Villalobos and Alvarez 2010).
The freshwater crab fauna of Ecuador (7 genera, 26 species, 2 families) includes 3 genera and 21 species of pseudothelphusids (all Pseudothelphusinae, Hypolobocerini), and 4 genera and 5 species of trichodactylids (all Dilocarcininae). Finally, Peru (11 genera, 22 species, 2 families) has a fauna dominated by trichodactylids (14 species and 8 genera, in 2 subfamilies Dilocarcininae and Trichodactylinae), with a smaller pseudothelphusid fauna consisting of 8 species and 2 genera (all Pseudothelphusinae in 2 tribes Kingsleyini and Hypolobocerini). Freshwater crabs of both families are completely absent from Chile. Despite warm subtropical climates freshwater crabs are absent in many islands of the Caribbean including Jamaica, The Cayman Islands, The Bahamas, Grenada, Antigua, and Anguilla.
When distribution patterns are considered at the genus level (Table 2) the taxonomic diversity of Neotropical freshwater crabs is again by far the highest in Colombia (21 genera), Venezuela (18 genera), Mexico (17 genera), Brazil (16 genera), and Peru (11 genera). Diversity is lower in Ecuador (7 genera), Guyana, Suriname, Bolivia, Paraguay, French Guiana, Nicaragua, and Guatemala (6 genera), and in Argentina and Panama (5 genera) ( Table 2). Costa Rica, El Salvador and Belize each have 4 genera, Trinidad and Tobago has 3 genera, Honduras and Cuba each have 2 genera, while Uruguay and the other islands of the Greater and Lesser Antilles each have 1 genus.

Widespread species: Pseudothelphusidae
Thirteen (out of 34) pseudothelphusid freshwater crab genera and 28 (out of 283) species have a wide distribution that easily exceeds 20,000 km 2 and includes more than one country. Notably, Fredius reflexifrons is found in six countries (Brazil, French Guiana, Guyana, Peru, Suriname, Venezuela), Potamocarcinus magnus is found in five countries (Mexico, Guatemala, Honduras, El Salvador, Costa Rica), and Kingsleya latifrons (Guyana, French Guiana, Suriname, Brazil)

Distribution patterns and habitat
Freshwater crabs are found in all major habitat types in the Neotropics (Thieme et al. 2005;Abell et al. 2008) including rivers, rapids, swamps, lakes, caves, and mountain streams and species belonging to both families prefer warm-water habitats year round. The Pseudothelphusidae are typically found in small mountain streams above 400 m above sea level, which may in part reflect their ability to breathe air and live a semiterrestrial existence. Pseudothelphusids reach their highest diversity in the rivers and streams that drain the highland areas of the cordilleras of Colombia and Ecuador. In contrast, trichodactylids are most abundant in the vast network of lowland rivers of South America that make up the Amazon, Orinoco, Paraguay, and Parana basins (Cumberlidge et al. 2009). Species diversity tends to be highest where vegetation cover is densest and water availability is highest, and there are fewer, or no species found in the more arid ecosystems and those with colder water temperatures. The pattern of the dominance of Pseudothelphusidae in Colombia, Venezuela, Ecuador, Peru, Mexico, Central America, and the Caribbean, and their absence in Bolivia, Uruguay, Paraguay, southern Argentina, and Chile probably reflects an origin somewhere in Colombia and Venezuela, from where they spread out north to Central America and Mexico, east to the Guyanas and Lesser Antilles, and south as far as Brazil and Peru (Rodríguez 1982(Rodríguez , 1986. Similarly the dominance of Trichodactylidae in the Amazon, Orinoco, Paraguay, and Parana River basins and their absence from Chile and from aquatic ecosystems at high altitudes in the Andes elsewhere in South America reflects their preference for an aquatic, rather than a semiterrestrial life (Rodríguez 1982(Rodríguez , 1986. However, it is harder to explain the presence of trichodactylids in Central America, Mexico, and Trinidad in localities that lie well outside of the major river basins of the South American subcontinent (Rodríguez 1992).
Twenty-four species of neotropical freshwater crabs are found in caves (22 pseudothelphusids and two trichodactylids), and are either fully adapted to a life in caves, or are visitors to caves and have a distribution that also includes surface waters (Table 3). Twelve species of cave-dwelling freshwater crabs are from Mexico, five from Central America (Belize 1, Guatemala 3, and Costa Rica 1), two from the Caribbean (Cuba 1, Puerto Rico, and St. Croix 1), and five from South America (Colombia, 2 and Venezuela 3).

Freshwater crab endemism (Table 4)
The majority of freshwater crab species found in Colombia (81%) are country endemics: 78 species of pseudothelphsids and 5 species of trichodactylids (Cumberlidge et al. 2009). The high degree of endemism in Colombia's freshwater crab fauna at the species level (83 of 102 species, 81%) is also seen to a lesser extent at the genus level (9 of 21 genera, 43%), but not at the family level (neither of the two families are exclusively found in Colombia). Many of the Colombian endemics are found in the isolated mountain streams and in the middle stretches of rivers associated with rainforest (Campos 2005). Mexico's freshwater crab fauna has the next highest number of country endemics (66 of 67 species, 97%) that is also seen at the genus level (13 of 17 genera, 76%), but not at the family level (neither of the two families are exclusively found in Mexico). Many of the Mexican endemics are found in the isolated mountain streams and in the middle stretches of rivers associated with the rainforests and caves  (Villalobos and Alvarez 2010). All species of freshwater crabs found in Cuba and Hispaniola are island endemics.

Conservation status
The conservation status of the 298 species of freshwater crabs known from the Neotropical region in 2009 was evaluated against the IUCN (2003) Red List criteria (version 3.1) and is available on the Red List site (www.iucn.redlist.org). These results were summarized by Cumberlidge et al. (2009). The conservation status of species described since that work (Table 1) has not yet been assessed. Unfortunately, about half of all Neotropical freshwater crabs (148 species) are too poorly known to submit to the assessment protocols and are listed as Data Deficient, notably some 80% of the diverse Mexican fauna (Tables 5, 6). Of the remaining 150 species that could be assessed (belonging to 22 genera and 2 families) the majority (107 species) were found to be of Least Concern, and most of these species either live in rivers, marshy lowlands, or in mountain streams in the forested highlands (Cumberlidge et al. 2009). For the Pseudothelphusidae, 111 out of 251 species were assessed (140 species were data deficient), and of these, 72 species of Least Concern, 2 species were Critically Endan-      (Cumberlidge et al. 2009). Despite the large numbers of specimens available very little information is available on population levels and trends, except for a qualitative estimate (e.g., whether common or rare) based on the number of sites at which a species is present and its relative abundance at each site.
With only 42 out of 298 species of Neotropical freshwater crabs known in 2009 assessed as threatened with global extinction (Tables 5-7), the region's largely endemic freshwater crab fauna (Table 4) does not appear at first sight to be in immediate trouble compared with other aquatic groups found in the same freshwater habitats (e.g., fish, molluscs, and dragonflies) (Collen et al. 2008). The 107 species of Neotropical freshwater crabs judged to be of Least Concern (35 species of trichodactylids, and 72 species of pseudothelphusids) have a wide distribution in rivers, lakes, highland streams and lowland wetlands, and appear to be tolerant of changes in land use that affect aquatic ecosystems.
Threats to Neotropical freshwater crabs include habitat destruction driven by increasing agriculture, the demands of increasing industrial development, and the alteration of fast flowing rivers for the creation of hydroelectric power (Cumberlidge et al. 2009). Even species assessed as Least Concern could suffer a catastrophic decline should there be abrupt changes in land development, hydrology, or pesticide-use regimes. Species with a narrow distribution are vulnerable to extreme population fragmentation and could suffer a rapid decline and even extinction in a relatively short time should dramatic changes in land-use affect their habitat. The 148 species of Neotropical freshwater crabs judged to be Data Deficient are mostly rare species, and their conservation status needs to be re-evaluated once more information comes to light. It is hoped that prioritizing species for conservation action through the Red List assessment process will lead to the development of conservation recovery plans for threatened species in the future.

Conclusions
This study confirms that freshwater crabs are completely absent from all parts of the Nearctic region (even in the neighboring warmer parts of northern Mexico and southern Florida, USA), and that the northern limits of their distribution coincide with the Nearctic/ Neotropical boundary in Mexico and the presence of arid regions lacking permanent freshwaters (i.e., the Sonoran and Chihuahuan Deserts). Species richness of freshwater crabs increases south of this boundary in Mexico and reaches a peak in the States of Veracruz, Tabasco, Oaxaca, and Chiapas. The uneven pattern of species-richness -high in Mexico, low in Central America, and high in Colombia -is difficult to explain by simply invoking an even spread of species out of a center of origin somewhere in Colombia -Venezuela (Rodríguez 1982(Rodríguez , 1992, and further studies are necessary. The relatively low species richness of freshwater crabs in Brazil is unexpected given its vast area and rich biodiversity, and may reflect the dominance of trichodactylids and a general paucity of species-rich pseudothelphusids in the Brazilian fauna. The abundance of freshwater crabs in Colombia, Ecuador, and Peru coincides with a freshwater habitat species diversity hotspot (that is defined by overlapping distributions of stenotopic species based on combined data from vertebrates and invertebrates (Collen et al. 2008)). All countries in the Neotropical region are still in a phase of exploration and steep rises in species numbers of pseudothelphusids are expected once more surveys have been completed.
The Neotropics are the second most diverse region in the world for freshwater crabs, and there are 42 species from 14 countries within this region that may be threatened with extinction. The finding that 34% of pseudothelphusids and 10% of trichodactylids are threatened, and that many others are poorly known, can be used to develop a conservation strategy for these species, and supply a focus for future research efforts (Cumberlidge et al. 2009). Although some species of Neotropical freshwater crabs have been quite well studied a clear majority are known only from either the type locality or from just a few localities, and in these cases further collections are necessary to ascertain their actual distributions. The restricted range of many species from the Neotropics, together with the on-going human induced loss of habitat in many parts of the region, are a cause for concern for the long-term security of elements of this fauna. Conservation activities should therefore be aimed primarily at preserving the integrity of sites and habitats while at the same time closely monitoring key populations. Significant areas of the Neotropics still remain insufficiently explored, and the focus of new efforts should be on new species discovery through increased collection in remote areas and the refinement of taxonomic skills. These efforts should also focus on conserving threatened species, and on seeking out data deficient species. Gathering current data on distribution, natural history, population trends, threats, and endemism of the Neotropical region's highly diverse freshwater crabs will enable the updating of the IUCN Red Lists, and the development of conservation strategies for this understudied diverse and potentially highly threatened fauna.