Rev. Esp. Herp. (2005) 19:33-46
Geographical distribution patterns of South American side-necked turtles (Chelidae), with emphasis on Brazilian species
FRANCO LEANDRO SOUZA
Universidade Federal de Mato Grosso do Sul, Centro de Ciências Biológicas e da Saúde, Departamento de Biologia, 79070-900 Campo Grande, MS, Brazil (e-mail: [email protected])
Abstract: The Chelidae (side-necked turtles) are the richest and most widespread turtle family in South America with endemic patterns at the species level related to water basins. Based on available literature records, the geographic distribution of the 22 recognized chelid species from South America was examined in relation to water basins and for the 19 Brazilian species also in light of climate and habitat characteristics. Species-distribution maps were used to identify species richness in a given area. Parsimony analysis of endemicity (PAE) was employed to verify the species-areas similarities and relationships among the species. For Brazilian species, annual rainfall in each water basin explained 81% of variation in turtle distribution and at a regional scale (country-wide) temperature also influenced their distribution. While rainfall had a significant positive relationship with species number in a given area, a negative but non-significant relationship was identified for temperature. Excepting an unresolved clade formed by some northern water basins, well-defined northern-northeastern and central-south groups (as identified for water basins) as well as biome differentiation give support to a hypothesis of a freshwater turtle fauna regionalization. Also, a more general biogeographical pattern is evidenced by those Brazilian species living in open or closed formations. The geographic distribution of Brazilian chelid species apparently reflects patterns of climate and vegetation physiognomies and can be associated with life- history traits such as low vagility. Since some Brazilian chelid species have a distribution encompassing diversity hotspots, the delimitation of endemism areas could be useful in defining conservation priority areas. Key words: biogeography, Brazil, Chelidae, parsimony analysis of endemicity, South America, turtle.
Resumen: Patrones de distribución geográfica de las tortugas pleurodiras (Chelidae) sud- americanas, con énfasis en las especies brasileñas. – Las tortugas de la familia Chelidae (tortugas pleurodiras de cuello de serpiente) son las más abundantes y ampliamente distribuídas en América del Sur y presentan patrones de endemismo a nivel específico relacionados con las cuencas hidrográficas. Basándonos en la literatura disponible, examinamos la distribución geográfica de 22 especies de Chelidae reconocidas en América del Sur en relación con las cuencas hidrográficas. Para las 19 especies presentes en Brasil estudiamos además la relación con el clima y las características del hábitat. Los mapas de distribución de las especies fueron utilizados para calcular la riqueza de especies en un área determinada. También se empleó un análisis parsimonioso de endemicidad (PAE) para estudiar las semejanzas entre áreas y las relaciones entre especies. Para las especies brasileñas, la precipitación anual en cada cuenca hidrográfica explicó 81% de la variación en la distribución de las tortugas y a escala regional (de todo el país) la temperatura también afecta a su distribución. Mientras que la pluviosidad mostró una relación positiva y estadísticamente significativa con el número de especies en un área determinada, para la temperatura dicha relación fue negativa y no significativa. Con la única excepción de un clado no resuelto formado por algunas cuencas hidrográficas del norte, la existencia de grupos norte-nordeste y centro-sur bien definidos (y coincidentes con las cuencas hidrográficas) y la diferenciación de los biomas apoyan la hipótesis de regionalización de la fauna de tortugas de agua dulce. Además, las especies brasileñas que viven en formaciones abiertas o cerradas ponen de manifiesto 34 F.L. SOUZA un patrón biogeográfico más general. La distribución geográfica de las especies de Chelidae brasileñas aparentemente refleja patrones climáticos y de fisionomía vegetal y podría estar asociada a algunos rasgos de su historia de vida como la escasa vagilidad. Dado que la distribución de algunas especies de Chelidae brasileñas incluye puntos calientes de diversidad, la delimitación de áreas de endemismo puede ser útil para definir áreas prioritarias para la conservación. Palabras clave: América del Sur, análisis parsimonioso de endemicidad, biogeografía, Brasil, Chelidae, tortuga.
INTRODUCTION interesting evolutionary background for research on Brazilian freshwater turtle Around 20% of all 278 extant species of biogeography. For instance, mountainous turtles are found in South America, including regions of southeastern Brazil are reported as representatives of Chelydridae, Emydidae, geographical barriers for mammals Geoemydidae, Kinosternidae, Podocnemididae, (including bats) and reptiles (VANZOLINI, Chelidae, Testudinidae, Cheloniidae and 1973; VANZOLINI & REBOUÇAS-SPIEKER, Dermochelyidae (IVERSON, 1992b). The 1976; DIXON, 1979; SIMPSON, 1979; species diversity among these families is DITCHFIELD, 2000; LARA & PATTON, 2000; varied, the Chelidae (side-necked turtles), MORITZ et al., 2000; SOUZA et al., 2003), with 22 species, being the most speciose one. whereas Amazonian rivers may also play an In contrast with other families that are important role in shaping the distribution restricted to a few water basins (e.g. patterns of a plethora of vertebrate species the Podocnemididae, Geoemydidae, and (see review in MORITZ et al., 2000). On the Chelydridae), chelids are widespread in other hand, complex vegetation habitats, South America, ranging from northern including flooded areas, gallery and evergreen Venezuela and the Guianas to Argentina. forests, and Cerrado physiognomies, can be However, endemism patterns related to water found along the rivers and other water bodies basins can be detected at the species level inhabited by Brazilian freshwater turtles. (PRITCHARD & TREBBAU, 1984; IVERSON, With the only exception of marine turtles and 1992a, b; CABRERA 1998; IPPI & FLORES, representatives of the Podocnemididae 2001; MCCORD et al., 2001). Although (particularly Podocnemis spp.) which exhibit factors driving such local (water basin) and a high dispersal capability (VALENZUELA, regional distribution patterns for these 2001), all other aquatic turtle species from freshwater turtle species are poorly known, Brazil are quite sedentary, with home range they could reflect processes influencing size restricted to a small area and dispersal evolutionary history, including natural limited to a few meters/day (MAGNUSSON et barriers, colonization, and local extinction. al., 1997; SOUZA & ABE, 1997, 2000). These Recognizing species geographical distribution life-history traits in conjunction with a patterns can allow the recognition of the landscape matrix that imposes still more factors responsible for these patterns. dispersal restrictions (e.g. temperature, Extensive variation in ecosystems and vegetation physiognomies, and geographical topography occurs in South America in barriers) could constrain these organisms general and Brazil in particular (e.g. tropical within local areas (SOUZA et al., 2002a, b). and subtropical rainforests, Cerrado vegetation, The family Chelidae consists of mountainous and flat topographies) creates an predominantly aquatic species, generally BIOGEOGRAPHY OF SOUTH AMERICAN CHELIDAE 35 leaving the water only for basking or for BRANDÃO et al., 2002; COLLI et al., 2002; nesting. According to IVERSON (1992b), on a RIBAS & MONTEIRO-FILHO, 2002; KINAS et al., global scale water basins that receive elevated in press). For systematic purposes, recent annual rainfall also exhibit high turtle systematic reviews of the genus Phrynops by richness. While this assertion may apply CABRERA (1998) and MCCORD et al. (2001) globally, such a relationship could be not were followed. Thus, 22 Chelidae species valid at a regional scale because local climate could be assigned to South America and 19 to can be influenced by different environmental Brazil (Table 1). characteristics such as relief and the The geographic distribution of Brazilian landscape matrix (including distinct side-necked turtles was interpreted in relation vegetation physiognomies). In Brazil, tropical to annual rainfall, latitude, longitude, altitude, and subtropical climates are detected in a mean annual air temperature, water basin north-south gradient (NIMER, 1989), area, mean annual precipitation in each water reflecting distinct patterns of temperature and basin, and main biomes (see below). annual rainfall. In turn, this climate gradient Brazilian water basin boundaries were supports a diversity of habitats, from tall tree outlined by ANA (2003) according to forests in lowland and mountainous regions landscape complexity formed by country to, xeromorphic vegetation in the Cerrado to drainage and relief. Thus, we identified 12 grassland. Thus, rainfall, temperature, and major water basins in Brazil: Amazon, habitat characteristics around water basins Atlantic-North eastern (Atl-Ne), Atlantic- could be important factors affecting North eastern Orient (Atl-Ne Orient), distribution patterns in Brazilian chelids. Atlantic-East (Atl-E), Atlantic-South eastern In this paper, the distribution of the (Atl-Se), Atlantic-South (Atl-S), Parnaíba, Brazilian freshwater side-necked turtles Paraná, Tocantins, São Francisco, Paraguay, (Chelidae) was revisited in light of climate and Uruguay (Fig. 1), plus the Orinoco and and habitat characteristics to determine which Magdalena basins for South America. These environmental or physical aspects could be water basins encompass distinct vegetation relevant in shaping the biogeography of this physiognomies (from Atlantic rainforest to taxon. Cerrado), distinct climatic regions (from an equatorial zone to a subtropical province), and different size areas (NIMER, 1989; IBGE, MATERIALS AND METHODS 1993; CUNHA, 2001). The mean annual The geographic distribution of South rainfall in each water basin was compiled American Chelidae was compiled from from CUNHA (2001) and NIMER (1989) that available literature, including systematic provided annual rainfall records from weather reviews (MITTERMEIER et al., 1978; station throughout Brazil. The main Brazilian VANZOLINI et al., 1980; RHODIN et al., 1982, biomes were defined according to IBGE 1984a, b; RHODIN & MITTERMEIER, 1983; (1993). Roughly, these biomes can be PRITCHARD & TREBBAU, 1984; LEMA & represented by Amazon forest, Atlantic FERREIRA, 1990; IVERSON, 1992a; VANZOLINI, rainforest sensu lato (which includes 1994; CABRERA, 1998; MCCORD et al., 2001) physiognomies such as semideciduous forest as well as recent faunistic surveys from in the southeastern inland, and Araucaria poorly known regions (CABRERA, 1995; angustifolia forest in temperate regions), SOUZA et al., 2000; ARGÔLO & FREITAS, 2002; Cerrado (with its distinct physiognomies such 36 F.L. SOUZA as campo limpo, campo sujo and cerradão), annual rainfall, mean temperature, and mean Caatinga, Pantanal, and Southern grasslands. altitude were calculate at the central point of For Brazil, turtle distribution maps were each cell according to records from diverse used to calculate species richness in a given topographical and climate data bases (NIMER, area. The Brazilian territory was divided into 1989; ANA, 2003; CNPM, 2003; IBGE, a 2.5º × 2.5º latitude-longitude grid (ca. 2003). A forward multiple linear regression 90 000 km2) on a 1:16 670 000 map, resulting was performed to determine the influence of in 136 quadrants. For each cell the number of water basin area and mean annual rainfall in turtle species was determined according to each water basin (calculated as above) on the literature. Latitude, longitude, mean turtle species richness in the 12 major
TABLE 1. The data matrix (area × taxon) with distribution (1: presence; 0: absence) of the 22 South American Chelidae species according to 14 water basin and six major Brazilian biomes. Am: Acanthochelys macrocephala, Ap: A. pallidipectoris, Ar: A. radiolata, As: A. spixii, Bd: Batrachemys dahli, Bh: B. heliostemma, Bn: B. nasuta, Br: B. raniceps, Bt: B. tuberculata, Bz: B. zuliae, Bv: Bufocephala vanderhaegei, Cf: Chelus fimbriatus, Hm: Hydromedusa maximiliani, Ht: H. tectifera, Mg: Mesoclemmys gibba, Pp: Platemys platycephala, Pg: Phrynops geoffroanus, Ph: P. hilarii, Pt: P. tuberosus, Pw: P. williamsi, Rh: Ranacephala hogei, Rr: Rhinemys rufipes. Hyphens in biomes denote non-Brazilian species. TABLA 1. Matriz de datos (área × taxón) de distribución (1: presencia; 0: ausencia) de las 22 especies de Chelidae sudamericanas en relación a 14 cuencas hidrográficas y a seis grandes biomas en Brasil. Am: Acanthochelys macrocephala, Ap: A. pallidipectoris, Ar: A. radiolata, As: A. spixii, Bd: Batrachemys dahli, Bh: B. heliostemma, Bn: B. nasuta, Br: B. raniceps, Bt: B. tuberculata, Bz: B. zuliae, Bv: Bufocephala vanderhaegei, Cf: Chelus fimbriatus, Hm: Hydromedusa maximiliani, Ht: H. tectifera, Mg: Mesoclemmys gibba, Pp: Platemys platycephala, Pg: Phrynops geoffroanus, Ph: P. hilarii, Pt: P. tuberosus, Pw: P. williamsi, Rh: Ranacephala hogei, Rr: Rhinemys rufipes. Los guiones en los biomas indican especies no brasileñas.
Species
Basins Am Ap Ar As Bd Bh Bn Br Bt Bz Bv Cf Hm Ht Mg Pp Pg Ph Pt Pw Rh Rr Orinoco 0 0 0 0000101010011101000 Magdalena 0 0 0 0100000000000000000 Amazon 0 0 0 0011100110011101001 Atlantic-Northeastern 0 0 0 0000000000001101000 Parnaíba 0 0 0 0000010000000101000 Atlantic-Northeastern Orient 0 0 0 0000010000000101000 São Francisco 0 0 0 1000010000000100000 Atlantic-Eastern 0 0 1 0000000000000100000 Tocantins 0 0 0 1000000110001100000 Paraguay 1 1 0 0000000100000100000 Paraná 0 0 0 1000000101100100000 Atlantic-Southeastern 0 0 1 1000000001100100010 Uruguay 0 0 0 1000000100100110100 Atlantic-Southern 0 0 0 1000000000100110100
Biomes Amazon forest 0 – 0 0–1110–010011101001 Caatinga 0 – 0 0–0001–000000101000 Pantanal 1 – 0 0–0000–000000100000 Cerrado 0 – 0 1–0000–100000100000 Atlantic rainforest 0 – 1 1–0001–101100110110 Southern grasslands 0 – 0 0–0000–000000010000 BIOGEOGRAPHY OF SOUTH AMERICAN CHELIDAE 37
and a positive relationship between longitude and rainfall. Methods using parsimony algorithms have been used as a biogeographic tool for detecting similarities among areas and establishing relationships among bio- geographic units according to the organisms found in them (MORRONE & ESCALANTE, 2002). A parsimony analysis of endemicity (PAE) (MORRONE, 1994) was employed to verify such species-areas similarities and relationships among South American Chelidae species. PAE defines study units in biogeography by grouping areas based on shared species (MORRONE, 1994; DA SILVA & OREN, 1996; LUNA et al., 1999; IPPI & FIGURE 1. The 12 Brazilian river drainage considered in this study. 1: Amazon, 2: Atlantic-Northeastern, 3: Parnaíba, 4: FLORES, 2001; ROJAS-SOTO et al., 2003). The Atlantic-Northeastern Orient, 5: São Francisco, 6: Atlantic- method is particularly useful for those East, 7: Tocantins, 8: Paraguay, 9: Paraná, 10: Atlantic- organisms with limited dispersal abilities Southeastern, 11: Uruguay, 12: Atlantic-South. Adapted from Brazilian Hydrological Information System (2003). (RON, 2000), such as the Chelidae FIGURA 1. Las 12 cuencas hidrográficas brasileñas (MAGNUSSON et al., 1997; SOUZA & ABE, consideradas en el presente estudio. 1: Amazon, 2: Atlantic- 1997, 2000). For the present purpose, the 14 Northeastern, 3: Parnaíba, 4: Atlantic-Northeastern Orient, identified water basins for South America and 5: São Francisco, 6: Atlantic-East, 7: Tocantins, 8: Paraguay, 9: Paraná, 10: Atlantic-Southeastern, 11: Uruguay, 12: the six Brazilian biomes were defined as Atlantic-South. Adaptado de Brazilian Hydrological geographic provinces for turtle distribution Information System (2003). (Table 1). In PAE, the data set is a matrix of presence (1; analogous to a derived character) or absence (0; primitive character) of species Brazilian basins, and to check the relationship in a given geographic area, with a between turtle richness and the five variables hypothetical area with no taxa (a rooting discerned above (latitude, longitude, mean taxon or outgroup). PAE was performed using annual rainfall, mean temperature, and mean the algorithm implemented in NONA altitude). Prior to these analyses, these (GOLOBOFF, 1999) through Winclada (NIXON, variables were checked for normality, 2002) by applying a heuristic search with skewness, and kurtosis (ZAR, 1999). A 1000 replications on the data matrix. If correlation matrix was created for all five multiple parsimonious trees resulted from the independent variables to check for analyses, they were summarized by means of redundancy. After this analysis, only one a strict consensus tree. variable among a highly correlated pair (r > 0.6) was retained to be included in the RESULTS regression model. Temperature and rainfall were chosen as climate variables since this Magdalena basin has a unique chelid species. prior analysis showed a highly negative The Amazon basin is the richest among all 14 relationship between latitude and temperature South American basins, with ten chelid 38 F.L. SOUZA species, followed by Orinoco (seven species), 2A). Typical coastal areas from southeastern Atlantic-Southeastern and Uruguay (six Brazil (Atlantic-Southeastern and Atlantic- species), Tocantins, Paraná, and Atlantic- South basins) plus Tocantins, Paraguay, South (five species), Paraguay (four species), Uruguay, and Paraná basins distinguish a and the remaining five basins with three central-southern clade. Magdalena basin, as species each. The Atlantic rainforest harbours expected, forms a unique clade, represented 10 species, while nine species are found by its endemic species, Batrachemys dahli. within the Amazon forest. Three species are One single most parsimonious tree of 21 recorded from both the Cerrado and Caatinga steps (consistency index: 90; retention index: biomes, two species from the Pantanal, and 66) was found for the endemicity pattern just one species is found in the Southern related to Brazilian biomes (Fig. 2B). The grasslands (Table 1). Amazon forest shares species with the For Brazilian water basins, only mean Caatinga while the Cerrado and Atlantic annual rainfall in each basin was retained in rainforest exhibit common species. The the multiple linear model (F2,9 = 18.99; P < Pantanal shares species with all other biomes 0.001), explaining 81% of the variation in Brazilian turtle distribution (R2 = 0.808). In A outgroup this model, mean annual rainfall in each basin Magdalena had a positive significant relationship with Parnaíba the number of turtle species (β = 0.68; t = Atl-Ne Orient 3.57; P < 0.01). In a country wide analysis Säo Francisco Atl-L rainfall, temperature, and altitude explained Atl-Ne only 27% of the variation in species richness Amazon 2 Orinoco (F3,132 = 16.67; P < 0.0001; R = 0.274). While Paraguay rainfall had a significant positive relationship Tocantins β with richness ( = 0.452; t = 5.48; P < 0.001), Uruguay a negative non-significant relationship was Atl-S identified for both temperature (β = − 0.144; Paraná t = − 1.82; P = 0.07) and altitude (β = − 0.159; Atl-Se − t = 1.83; P = 0.07). B outgroup PAE showed distinct patterns of Southern grasslands geographic distribution for the South Pantanal Cerrado American Chelidae species at a water basin Atlantic rainforest level and for Brazilian species at a biome Amazon level. In relation to water basins, six most Caatinga parsimonious trees of 32 steps were found. FIGURE 2. The strict consensus tree obtained by the The strict consensus tree (consistency index: parsimony analysis of endemicity with the raw distribution 68; retention index: 66) shows a two resolved of the 22 South American chelid species in relation to water basins (A) and the single most parsimonious tree of the 19 clade formed by Amazon-Orinoco and Brazilian chelid species in relation to Brazilian biomes (B). Atlantic-North eastern basins (a northern- FIGURA 2. Árbol de consenso estricto obtenido mediante un northeastern clade) and Atlantic-East and São análisis parsimonioso de endemicidad de los datos en bruto Francisco basin in a not resolve (polytomy) de distribución de las 22 especies de Chelidae sudameri- canas en relación con las cuencas hidrográficas (A) y árbol branch that also includes Parnaíba, and más parsimonioso de las 19 especies de Chelidae brasileñas Atlantic-North eastern Orient basins (Fig. en relación con los biomas brasileños (B). BIOGEOGRAPHY OF SOUTH AMERICAN CHELIDAE 39 except the Southern grasslands that, in turn, aquatic organisms, freshwater turtle species shares its single species only with the Atlantic may have their geographic distributions rainforest. Excepting the unresolved clade constrained by this life-history trait. Even formed by some northern drainage basins, the though terrestrial excursions are not well-defined northern-northeastern and uncommon in these organisms, especially central-south groups (as identified for drainage during periods of drought or reproduction basins) as well as biome differentiation give (PRITCHARD & TREBBAU, 1984; LEMA & support to the hypothesis of regionalization in FERREIRA, 1990; CABRERA, 1998), such the freshwater turtle fauna. dispersal behaviour is limited. Turtles generally move only to surrounding aquatic habitats such as riparian forests or to nearby DISCUSSION seasonally flooded basins. Like fishes The geographic distribution of South (MENEZES, 1988), different turtle species American and Brazilian chelid species inhabiting the same river or the same drainage apparently reflects the patterns of climate and basin typically occur in the upper and lower vegetation physiognomies found across the reaches of these watercourses. Furthermore, continent. Notwithstanding the possibility geologic, ecologic or climatic barriers (or a that distribution data set could be flawed or combination of these) between suitable incomplete, and the fact that climate data was habitats may impose still more difficulties for averaged for large quadrant areas, we believe species dispersal. This scenario may be true that the results reported here provide a for South American and Brazilian chelids. reasonable preliminary interpretation of The distinct areas of endemism identified Brazilian chelid biogeography. for the Brazilian chelids are similar to those Mean annual rainfall in each drainage found for other taxa, including birds basin was positively related to turtle species (CRACRAFT, 1985), fish (MENEZES, 1988; richness. Rainfall is considered an important VARI, 1988), and distinct lineages of South climate variable in shaping freshwater turtle American turtles (IVERSON, 1992b; IPPI & richness across the world (IVERSON, 1992a), FLORES, 2001). Roughly, two distinct patterns and this is also true at a regional scale, of geographical distribution are found in represented by Brazilian drainage basins. At a Brazilian chelids. Although unresolved, the more local scale, rainfall is again an combined Parnaíba and Atlantic- important correlate, although temperature Northeastern Oriental plus the clades and altitude have some influence. Our including Atlantic Eastern and São Francisco findings illustrate that a single factor (abiotic basins and Amazon, Orinoco, and Atlantic- or geographic) should not be assumed to drive Northeastern basins together with the turtle diversity. On the contrary, the data Magadalena branch identifies a northern- suggest that patterns of endemism together northeastern species group distribution while with both biome and drainage basin effects the remaining six basins encompass a central- better define the biogeography of Brazilian southern distribution. Although the multiple side-necked turtles. linear regression model failed to detect Freshwater aquatic organisms are useful statistical significance for both temperature in reconstructing historical biogeographic and altitude as environmental characteristics patterns since their vagility is restricted to driving geographic distribution patterns for defined linear habitats (VARI, 1988). As Brazilian chelids, some considerations must 40 F.L. SOUZA be noted. There are species typically found in 1988) and is absent only in high latitudes areas exhibiting a mean annual air from southern Brazil that include part of the temperature around 26ºC, including all the Uruguay and Atlantic-South drainage basins Amazon forest, Caatinga, Pantanal and as well as Southern grassland biome. Given Cerrado species, within a geographic the climate gradient and the diversity of distribution encompassing the Amazon, physiognomies encompassed by the drainage Parnaíba, Atlantic-Northeastern, Atlantic- basins across Brazil, it is possible that P. Northeastern Orient, Tocantins, São Francisco, geoffroanus is really a complex of sibling and the northern part of Paraná basin. This species (PRITCHARD & TREBBAU, 1984). broad area harbours 75% of the Brazilian The Amazon forest and Caatinga share chelid fauna. On the other hand, at least seven common species. The Amazon and Orinoco species (Acanthochelys radiolata, A. spixii, basin (equatorial forest) represents an area of Hydromedusa maximiliani, H. tectifera, endemism for seven species (Batrachemys Phrynops hilarii, P. williamsi, and heliostemma, B. nasuta, B. raniceps, B. Ranacephala hogei) can be found in dahli, B. zuliae, Mesoclemmys gibba, and temperate areas of Brazil that experience Rhinemys rufipes) and share, with Atlantic- harsh winters and a mean annual air Northeastern, Atlantic-North eastern Orient, temperature around 22ºC. An altitude Tocantins, and Parnaíba basins three other distribution pattern is also detected for some species (Phrynops tuberosus, Chelus freshwater turtle species where geographic fimbriatus, and Platemys platycephala). In range encompasses mountain areas (“upland addition, endemism is found in the Para- species”). Similar to fish (VARI, 1988), guay (Acanthochelys macrocephala, A. amphibian (GIARETTA et al., 1999), bird pallidipectoris) and Atlantic-Southeastern (MELO et al., 2001), and mammal (BONVICINO (Ranacephala hogei) basins, which encom- et al., 1997) communities, a species pass Pantanal and Atlantic rainforest biomes, replacement mechanism can be observed respectively. Batrachemys tuberculata has a across an altitude gradient in the two geographic distribution ranging from an Hydromedusa spp. in some Atlantic rainforest inland northeastern semi-arid region to the areas of southeastern Brazil. In sympatry, Atlantic-Northeastern basin, and Phrynops Hydromedusa maximiliani inhabits areas tuberosus inhabits coastal and inland areas in above 600 m, whereas H. tectifera is found in the Amazon and Northern-Northeastern lowland areas. In contrast, in areas where one basins (VANZOLINI et al., 1980; IVERSON, of the species is absent, H. maximiliani can be 1992a; MCCORD et al., 2001). Similarly, detected in coastal rivers below 100 m (e.g. despite the generally dry Cerrado São Sebastião Island), whereas H. tectifera is characteristics, this biome exhibits particular reported up to 900 m in upland areas of areas of wetland habitats such as flooded Paraná State (RIBAS & MONTEIRO-FILHO, areas associated with gallery forests. These 2002). Thus, ecological interactions may also vegetation corridors along river edges are an explain some distribution patterns observed important component of Cerrado structure at a local scale. In contrast to most Brazilian influencing the population dynamic of several chelids, the distribution pattern exhibited by vertebrate species (REDFORD & FONSECA, Phrynops geoffroanus is not congruent with 1986; DA SILVA & BATES, 2002). The Atlantic either basins or biomes. The species has a rainforest domains scattered throughout “patternless distribution” (sensu VANZOLINI, inland areas in humid valleys and along BIOGEOGRAPHY OF SOUTH AMERICAN CHELIDAE 41 river systems. Thus, both Cerrado and ecological division into two major groups, Atlantic rainforest biomes are represented in represented by those species living in open- Paraguay and Paraná basins, sharing such or closed-formations. This distribution turtle species as Bufocephala vanderhaegei pattern is similar to those described for and Hydromedusa tectifera. species of frogs (HEYER, 1988) and lizards Life-history traits (mating system, (VANZOLINI, 1988). The closed-formation dispersal ability), historical events (fragmen- group is represented by those species living in tation, range expansion, colonization), and regions with closed forest canopy. In a broad landscape matrix (mountain ridges, sense, this formation is defined by an arc watersheds) are important components in from Amazon rainforest to its linkage with shaping geographic distribution for Atlantic rainforest via northern Brazil and the organisms with low vagility such as Atlantic rainforest, with its distinct freshwater turtles (SCRIBNER et al., 1986; physiognomies from the northeastern coastal WALKER & AVISE, 1998; SCRIBNER & region inland to southeastern and southern CHESSER, 2001; SOUZA et al., 2003). The Brazil. The open-formation group includes combination of these components can those species living in biomes such as the account for the endemism patterns detected Cerrado, Pantanal, and Caatinga. Although for Brazilian chelids. A topographically tree cover along edges of water bodies (e.g. complex region found throughout eastern riparian forests) inhabited by the turtles from Brazil (Atlantic-Eastern, Atlantic- these regions is common, these areas Southeastern, and Atlantic-Southern basins) typically have an open canopy. A diagonal associated with an altitudinal gradient, strip from central to northern Brazil can medium to low temperature, and high rainfall define this open formation. Encompassing clearly identifies areas of endemism in over one quarter of Brazil, the Cerrado, Brazilian Coastal range (e.g. Phrynops Pantanal, and Caatinga biomes harbour hilarii, P. williamsi, Ranacephala hogei, chelids typical of dry areas, such as Hydromedusa maximiliani). In central Brazil, Acanthochelys macrocephala, Bufocephala environmental stochasticity due to a vanderhaegei, Batrachemys tuberculata, and pronounced wet-dry seasonality and specific Phrynops tuberosus. Contact zones between habitat requirements apparently restrict the open- and closed-formation provide suitable geographic distribution of Acanthochelys areas for some species as Acanthochelys macrocephala to some areas of the Pantanal spixii and Hydromedusa tectifera. (RHODIN et al., 1984b; VINCKE & VINCKE, The distribution patterns of organisms can 2001; MAURO et al., 2004). Black water and shed light on historical factors that have clear water rivers as well as flooded and non- shaped biodiversity across a given region. flooded areas from Amazonian rainforest are Besides, it highlights putative areas with important environmental features shaping the common distribution characteristics (RON, geographical distribution of large Amazon 2000; ROJAS-SOTO et al., 2003). Delimiting river turtles (Podocnemididae) and some areas of endemism is useful to prioritising chelid species, including Chelus fimbriatus areas for conservation (IPPI & FLORES, 2001). and Rhinemys rufipes (PRITCHARD & Although many of the Brazilian chelid TREBBAU, 1984). species are found in continuous forests of the A more general biogeographic pattern Amazon region, several species have a evidenced by the Brazilian Chelidae is their distribution restricted to the Atlantic 42 F.L. SOUZA rainforest and Cerrado, two of the most mações Hidrológicas.
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