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Braz. J. Biol. vol.66 no.1a São Carlos Feb. 2006
Padrões distribucionais de primatas Neotropicais (Platyrrhini) baseados na Análise de Parcimônia de Endemismo
Goldani, A.; Carvalho, G. S.; Bicca-Marques J. C.
Faculdade de Biociências, Pontifícia Universidade Católica do Rio Grande do Sul, Avenida Ipiranga, 6681, CEP 90619-900, Porto Alegre, RS, Brazil
The Parsimony Analysis of Endemicity (PAE) is a method of historical biogeography that is used for detecting and connecting areas of endemism. Based on data on the distribution of Neotropical primates, we constructed matrices using quadrats, interfluvial regions and pre-determinated areas of endemism described for avians as Operative Geographic Units (OGUs). We codified the absence of a species from an OGU as 0 (zero) and its presence as 1 (one). A hypothetical area with a complete absence of primate species was used as outgroup to root the trees. All three analyses resulted in similar groupings of areas of endemism, which match the distribution of biomes in the Neotropical region. One area includes Central America and the extreme Northwest of South America, other the Amazon basin, and another the Atlantic Forest, Caatinga, Cerrado and Chaco.
Keywords: Parsimony Analysis of Endemicity, neotropical primates, Platyrrhini, distribution patterns, endemism.
A Análise de Parcimônia de Endemismo (PAE) é um método da biogeografia histórica que é usado para detectar e conectar áreas de endemismo. Baseando-se em dados de distribuição de primatas Neotropicais, construíram-se matrizes de dados utilizando-se quadrículas, regiões entre rios e áreas de endemismo pré-determinadas para aves como Unidades Geográficas Operacionais (OGUs). Codificou-se a ausência da espécie na OGU como 0 (zero) e a presença como 1 (um). Uma área hipotética com ausência total de espécies de primatas foi usada como grupo externo para polarização. Todas as três análises resultaram em grupos similares de áreas de endemismo, coincidindo com a distribuição de biomas na região Neotropical: uma área incluindo a América Central e o extremo Noroeste da América do Sul; outra, a Bacia Amazônica; e, uma terceira, a Mata Atlântica, Caatinga, Cerrado e Chaco.
Palavras-chave: Análise de Parcimônia de Endemismo; primatas neotropicais; Platyrrhini; padrões distribucionais; endemismo.
Biogeographical methods depend on a good knowledge of the distribution and areas of endemism of a particular group of species. In biogeography, an area of endemism is defined as "the congruent distributional limits of two or more species" (Platnick, 1991). Harold & Mooi (1994) define an area of endemism as a geographic region compris-ing the distributions of two or more monophyletic taxa that exhibit a phylogenetic and distributional congruence and having their respective relatives occurring in other such-defined regions. The number of species found in a given geographic area, for example, is directly related to its size, a phenomenon known as "species-area relationship" (Rosenzweig, 1995). Therefore, it is possible that scale affects the results of biogeographical studies. In this paper we test whether the choice of scale influences interpretations of the patterns of distribution of New World primates based on a Parsimony Analysis of Endemicity (PAE) and whether this method can help understanding past patterns of dispersion of the primate fauna within Latin America.
PAE is a method proposed by Rosen (1988) to relate areas historically based on the composition of their biota or part of it. This method is analog to cladistics. In the PAE method the areas (Operating Geografic Units - OGUs) represent the taxa and the taxa represent the characters. Different authors have used different ways for determining OGUs. The most common variation of the method, proposed by Morrone (1994), uses predetermined same-sized quadrats. It has been used in the study of several groups of plants and animals (e.g., Posadas, 1996; Posadas et al., 1997; Cavieres et al., 2002; GarcíaBarros et al., 2002). Craw (1988) sugested the use of predetermined areas of endemism (see also Goldani et al., 2002), whereas Silva & Oren (1996) adopted interfluvial regions as OGUs in a study of Amazonian primates. The size of individual OGUs may vary in these latter two methods.
New World monkeys are good models to test the influence of OGUs size in biogeography because their distribution is relatively well known, and most species present restrict distributions and have limited dispersion abilities. About 34% of the approximately 300 known extant primate species occur in the Neotropics (Rylands & Konstant, 2000). New World monkeys occur in forested habitats from about 30° S in Brazil and Argentina to about 20° N in Mexico (Hirsch et al., 2002).
MATERIALS AND METHODS
Distribution data were obtained mainly from a georeferenced data base available in the internet (BDGEOPRIM; www.icb.ufmg.br/~primatas/home_bdgeoprim.htm). BDGEOPRIM was elabo-rated and is maintained updated by André Hirsch and his colleagues of the Universidade Federal de Minas Gerais (Brazil). The data set was complemented with information from other publications (Silva & Oren, 1996; Collins & Dubach, 2000; Lehman, 2000; Chiarello & Melo, 2001).
Data analysis was based on matrices (OGUs vs. taxa) in which the absence of a taxon in a particular OGU is coded as 0 (zero) and its presence as 1 (one). A hypothetical area (outgroup) in which all taxa are absent (0) was added for polarization (Rosen & Smith, 1988).
Analyses were made using the Hennig86 software (Farris, 1988) with the following comands: mh* and bb* (branching bound), sw (sucessive weighting), ne (strict consensus) and ie (implicit enumeration). In the first analysis (quadrats as OGUs), areas of endemism were established in a cladogram based on the distribution of 106 species (Table 1) in 60 quadrats of 5° longitude by 5° latitude (Fig. 1) (first stage). The relationship among these areas of endemism (second stage) was determined according to the occurrence of 57 species (Table 2). Those species occurring in a single area (autapomorphies) were not included in this analysis.
The second analysis was based on the areas of endemism proposed for Neotropical birds by Cracraft (1985). Those areas with a complete absence of primates (West Peruvian Andean Subcenter, Austral Andean Center, Peruvian Arid Coastal Center, Nothofagus [Chilean Andean] Center and Patagonian Center) were excluded from the analysis, whereas a new OGU was added to the list (Central America - 31) Fig. 2). The original numbering of these areas was maintained in this paper to facilitate comparing the patterns observed with birds and primates: 1) Chocó Rainforest Center; 2) Nechí Rainforest Center; 3) Magdalena Center; 4) Santa Marta Center; 5) Guajiran Center; 6) Parian Center; 7) Venezuelan Montane Center; 8) Meridan Montane Center; 9) Perijan Montane Center; 10A) Gran Sabana Subcenter of Pantepui Center; 10B) Duida Subcenter of Pantepui Center; 11) North Andean Center; 12B) East Peruvian Andean Subcenter; 12C) South Peruvian Andean Subcenter; 14) Tumbesan Center; 16) Marañón Center; 17) Guyanan Center; 18) Imeri Center; 19) North Amazon Napo) Center; 20) South Amazon Inambari) Center; 21) Rondônia Center; 22) Pará Center; 23) Belém Maranhão) Center; 24) Serra do Mar Center; 25) Paraná Center; 26) Caatinga Center; 27) Campo Cerrado Center; and 28) Chaco Center. The relationship among these areas was established based on the distribution of 69 primate species Table 3).
In the last analysis we used interfluvial regions delimited by the main rivers and the Panama Canal as OGUs (Fig. 3). According to Ayres & Clutton-Brock (1992), the main rivers may represent natural geographic barriers for some primates. Data on the distribution of 76 species were used in this analysis (Table 4). Interfluvial OGUs were delimited by: I) Panama Canal; II) Panama Canal and Magdalena river; III) Magdalena and Orinoco rivers; IV) Orinoco and Branco rivers; V) Putamayo and Maranon rivers; VI) Japura and Putamayo rivers; VII) Negro and Amazonas/Japura rivers; VIII) Branco river and Atlantic coast; IX) Maranon and Ucayali rivers; X) Ucayali and Purus rivers; XI) Purus and Madeira/Madre de Dios rivers; XII) Madeira/Guaporé and Tapajós rivers; XIII) Tapajós/Teles Pires and Xingu rivers; XIV) Xingu and Araguaia rivers; XV) Tocantins and São Francisco rivers; XVI) Madre de Dios and Guaporé rivers; XVII) Tapajós and Teles Pires rivers; XVIII) Araguaia and Tocantins rivers; XIX) São Francisco river and Atlantic coast; XX) Paraguai and Paraná/Paranaíba rivers; and XXI) Paraná/Paranaíba rivers and Atlantic coast.
1st analysis Determining areas of endemism and their relationship based on quadrats
One cladogram with 669 steps, ci 0.64 and ri 0.77 was produced in the first stage (Fig. 4). It ena-bled the establishment of eight areas of endemism named A1 to A8 (Fig. 5). In the second stage, one cladogram with 98 steps, ci 0.58 and ri 0.54 was found (Fig. 6). Areas A1 and A3 were grouped by the presence of Ateles hybridus and Saguinus leucopus. Five species justified the grouping of areas A4 and A6: Alouatta guariba, Brachyteles arachnoides, Cebus nigritus, Leontopithecus caissara and Leontopithecus chrysopygus. Whereas eleven primates justified the grouping of A7 and A8 (Ateles belzebuth, Ateles paniscus, Cacajao melanocephalus, Callicebus torquatus, Lagothrix lagotricha, Mico chrysoleucus, Saimiri sciureus, Saguinus bicolor, Saguinus inustus, Saguinus midas, and Pithecia pithecia), the branch (A2(A5(A7,A8))) was justified only by Chiropotes albinasus, Lagothrix cana, and Saimiri ustus.
2nd analysis Determining the relationship among the areas of endemism proposed for birds (modified from Cracraft, 1985) with data on primates
One cladogram with 320 steps, ci 0.72 and ri 0.84 resulted from this analysis (Fig. 7). The branches ((A10B,A18)(A10A(A17(A22,A23)))) and (A5(A2(A1,A11))) were justified by the presence of a single species, Chiropotes satanas and Saguinus oedipus, respectively. Six species grouped A20 and A21: Callicebus hoffmannsi, Mico acariensis, Mico humilis, Mico manicorensis, Mico marcai, and Saguinus mystax. The occurrence of Ateles chamek, Callicebus brunneus, and Lagothrix cana justified the grouping (A12C(A27(A20,A21))). Areas A24 and A26 were grouped for sharing Callithrix jacchus and Cebus xanthosternos.
3rd analysis Determining the relationship among interfluvial areas
A cladogram with 386 steps, ci 0.79 and ri 0.89 was obtained (Fig. 8). A smaller number of species justified the groupings obtained in this analysis: a) Cebus capucinus justified the grouping of areas I and II; b) Calithrix penicillata justified the branch (XVIII(XV(XIX,XXI))); c) Ateles marginatus, Callicebus moloch, and Mico argentatus grouped areas XIII and XIV; d) Saguinus midas and Pithecia pithecia justified the branch (VIII(III,IV)); and e) Callimico goeldii and Pithecia monachus justified the branch (IX(VI(V,VII)(X(XI,XII)))).
The cladograms produced by all three analyses were very similar, and showed the grouping of neighboring areas: a) Central America and the extreme northwest of South America; b) Amazon basin; and c) Atlantic Forest, Caatinga, Cerrado, and Chaco (see Figs 3, 5, 6, and 8). These three large areas are represented by the main biomes in Latin America. Therefore, this pattern of primate distribution suggests that in the recent past species dispersion occurred mainly within those areas than between them, probably because they may have been even less connected (or more isolated) during the Pleistocene ice ages from 1.4 mya to about 10.000 years ago (Chernicoff et al., 1997) than today.
Despite this similarity, the analysis using larger OGUs (interfluvial regions) showed the highest consistency (0.79) and retention (0.89) indices, corroborating studies with Mexican mammals (Morrone & Escalante, 2002). These values mean that the use of different OGUs enable better results with natural areas like interfluvial regions. In spite of the hypothesis that rivers may represent natural geographic barriers for primate dispersion (Ayres & Clutton-Brock, 1992), several species were widely distributed occupying more than a single interfluvial region (such as Alouatta seniculus, Alouatta caraya, Alouatta guariba, Aotus azarae, Ateles chamek, Callimico goeldii, Cebuella pygmaea, Cebus albifrons, Saimiri sciureus, and Pithecia monachus). Whereas some of these species may be good swimmers and overcome these potential barriers (e.g., Alouatta spp.), others may have dispersed before the establishment of some of today's larger rivers, or part of its population may have been transported in natural rafts or due to river dynamics (changes in river course) from one margin to the other.
In sum, this study showed that the use of larger Operational Geographic Units (OGUs) produces more consistent results and that PAE was a useful tool for understanding the patterns of distribution and dispersion of nonhuman primates within South and Central America. Therefore, PAE shall contribute to our knowledge on the patterns of dispersion and distribution of nonhuman primates in the other three biogeographic regions where they occur (namely Africa, Madagascar, and South Asia) since similar analyses are missing.
Acknowledgments We are grateful to André Hirsch and colleagues from Universidade Federal de Minas Gerais for making precious Internet information available to us. This work was partially supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a scholarship granted to the first author (process number 131662/2001-5). Júlio César Bicca-Marques also thanks Cláudia, Gabriel, and Ana Beatriz for their permanent support. And, finally, we also thank the researchers Cláudio José Barros de Carvalho, José Maria Cardoso da Silva and Paula Posadas for the valuable review and suggestions for this paper.
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Faculdade de Biociências
Pontifícia Universidade Católica do Rio Grande do Sul
Avenida Ipiranga, 6681
CEP 90619-900, Porto Alegre, RS, Brazil
Received August 18, 2004 Accepted October 1, 2004 Distributed February 28, 2006