Perbiche-Neves et al. Frontiers in Zoology 2014, 11:36 http://www.frontiersinzoology.com/content/11/1/36 RESEARCH Open Access Historical biogeography of the neotropical Diaptomidae (Crustacea: Copepoda) Gilmar Perbiche-Neves1*, Daniel Previattelli1, Marcio R Pie2, Andressa Duran2, Eduardo Suárez-Morales3, Geoffrey A Boxshall4, Marcos G Nogueira5 and Carlos EF da Rocha1 Abstract Introduction: Diaptomid copepods are prevalent throughout continental waters of the Neotropics, yet little is known about their biogeography. In this study we investigate the main biogeographical patterns among the neotropical freshwater diaptomid copepods using Parsimony Analysis of Endemicity (PAE) based on species records within ecoregions. In addition, we assess potential environmental correlates and limits for species richness. Results: PAE was efficient in identifying general areas of endemism. Moreover, only ecoregion area showed a significant correlation with diaptomid species richness, although climatic factors were shown to provide possible upper limits to the species richness in a given ecoregion. Conclusion: The main patterns of endemism in neotropical freshwater diaptomid copepods are highly congruent with other freshwater taxa, suggesting a strong historical signal in determining the distribution of the family in the Neotropics. Keywords: America, Diaptominae, Diversity, Evolution, GIS, PAE, Richness Introduction the Palearctic and Nearctic regions [5]. It has been as- Diaptomid copepods are among the main trophic links sumed that the colonization of the Neotropics is probably between primary producers and consumers in aquatic much more recent, but no theory has yet received wide webs and represent the dominant family of Calanoida acceptance. According to the scenario hypothesized by in inland waters of Europe, Asia, North America (NA), Boxshall & Jaume [1], the presence of diaptomids at low Africa, and the northern part of South America (SA) [1]. altitudes in the northern and central parts of SA resulted Their origin, diversification, taxonomy, and evolution from a late invasion from NA, occurring after the closure are still poorly understood in the Neotropics - particu- of the Panama gap in the Pliocene about 3 MYA. After larly in South America - and there have been few studies invading from the North, the diaptomids would have dealing with general aspects of the regional biogeog- spread rapidly, colonizing the interconnected lowland raphy of the group (but see [2,3]). Although the origin river systems. In this scenario the rapid colonization of of the order Calanoida is ancient, dating back at least multiple river basins would conceal biogeographical dif- from the Silurian period (439-416 MYA) [4], the initial ferences among regions, as well as a possible N-S gradi- colonization by diaptomids of continental waters from ent in species richness [6], given that the southern areas marine origins is hypothesized to have taken place in would have had less time to accumulate species. In fact, the northern supercontinent of Laurasia sometime after patterns that would be congruent with this scenario can the break-up of Pangaea (around 160 MYA) [1]. The be observed in freshwater cyclopoid copepods [7], but success of this colonization and subsequent diversification they are inconsistent with the remarkably high diversity process is reflected by the fact that nearly half of the of SA diaptomids. Alternatively, Suárez-Morales [2] and current 440 known species in the family are distributed in Suárez-Morales et al. [3] suggested the development of independent diaptomid faunas in Central/North America * Correspondence: [email protected] and in SA, resulting from their long isolation prior to 1Departamento de Zoologia, Universidade de São Paulo – USP, IB, Rua do Matão, travessa 14, n. 321, São Paulo, SP CEP 05508-900, Brazil the closing (in the Pliocene) of the Panama isthmus. Full list of author information is available at the end of the article Such a recent connection would help to explain the © 2014 Perbiche-Neves et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Perbiche-Neves et al. Frontiers in Zoology 2014, 11:36 Page 2 of 8 http://www.frontiersinzoology.com/content/11/1/36 large differences in diversity between the SA diaptomid de Dios Piedmont, Paraguay, Lower Parana, Chaco, and fauna and that of Central America (CA). Guapore Itenez (Figure 1, in purple). A fourth large An understanding of diaptomid biogeography is still in cluster of ecoregions revealed an association of several its infancy. Most studies to date either include restricted ecoregions in the southern Neotropics (Laguna dos geographical regions [3,8] or are based on panbiogeogra- Patos, Lower Uruguay, Cuyan Desaguadero, Mar Chiquita phy [9,10], which has been heavily criticized for its ex- Salinas Grandes, Bonaerensean Drainages, and Upper cessive reliance on ancient vicariance (to the expense of Uruguay), as well as some high elevation areas of the alternative hypotheses) and its limitations in terms of Andes (Amazonas High Andes and Tramandai Mampi- reproducibility (see [11] for a recent discussion). Given tuba, Figure 1, in yellow). Other regions included some the lack of comprehensive phylogenetic information on faunistically unique clusters, such as the Valdivian Lakes, neotropical diaptomids, a valuable first approximation the South Andean Pacific Slopes (Figure 1, in light pink), can be obtained through a Parsimony Analysis of En- and the Magdalena Sinu/North Andean Pacific Slopes demicity (PAE, [12]). One important recent criticism of (Figure 1, in brown). The Central America ecoregions PAE is use of biologically unrealistic limits to areas, such forms a large cluster (Figure 1, in green), which was di- as geopolitical boundaries [13]. Another, criticize the vided into several small groups. Within these clusters, inability of PAE to detect perfect vicariance or dispersal high support was found to group Caribbean ecoregions. to explain biogeographical histories trough phylogenetic Most North American ecoregions were faunistically dis- biogeography [14]. In contrast, one advantage of the tinct from Central American ecoregions (Figure 1, light study of freshwater fauna is that hydrological basins blue). provide natural geographical boundaries between areas Ecoregions varied considerably in their respective num- (e.g. [15]), thus improving considerably the explanatory ber of recorded species (Figure 2). However, such differ- power of the analyses. A detailed discussion for and ences were not structured along a simple latitudinal against the use of PAE can be found at Morrone [16]. gradient. Rather, most diaptomid species are found east of The goal of the present study is to provide a large- the Andes, particularly in the Amazon lowlands and in scale study of the biogeography of neotropical diaptomid the Lower Paraná (Figure 2). Interestingly, of all tested species using the most comprehensive dataset on species candidate correlates, only the area of the ecoregion occurrences compiled to date. Our specific goals are (1) showed a significant association with diaptomid species to use PAE as a tool to provide a general overview of the richness (Table 1, F = 7.97, p = 2.5e-07, adjusted r2 =0.44). biogeographical relationships among diaptomid copepod This is intriguing, given the considerable climatic differ- faunas of different neotropical ecoregions; (2) to map ences between ecoregions. The reason for this result be- the geographical variation in diaptomid species richness comes clear by inspecting the actual scatterplots of each in the Neotropics; (3) to test the role of climatic factors variable against species richness (Figure 3). For instance, as potential correlates of diaptomid species diversity. although ecoregions with low annual temperature were species-poor, higher temperatures include ecoregions with Results an increasingly large variation of species richness. In other The PAE results of the biogeographical relationships words, although colder regions have consistently fewer among ecoregions based on their diaptomid copepod fauna species, warmer conditions include both low and high (Figure 1) revealed strong support for several groups of values of species richness. This suggests that, instead of ecoregions, some of which showed interesting sub- a simple linear relationship between species richness and structuring. A large cluster of ecoregions encompasses environmental variables, the climatic conditions found in a the higher Guiana shield and includes the ecoregions of the given ecoregion might only provide an “upper boundary” Guianas and the Orinoco river (Piedmont, Llanos, Guiana of the total species richness that can be found there. This Shield, delta and coastal drainages), with the Amazon low- inference was supported by our results of the BSS ana- lands (Rio Negro, Amazonas Lowlands, Madeira Brazilian lyses for mean annual temperature (p = 0.002), max- Shield, Tocantins-Araguaia, and Amazonas estuary and imum temperature during the warmest month (p = 0.06), coastal drainages) nested within this cluster (Figure