Accessibility / Report Error

Trans-Amazon dispersal potential for Crotalus durissus during Pleistocene climate events

Potencial de dispersión trans-Amazónica de Crotalus durissus durante el Pleistoceno

Abstracts

Two disjunct distributional areas of Crotalus durissus (Neotropical rattlesnake) are in open habitats north and south of the Amazon Basin and are presently separated by humid rainforest habitats. We used ecological niche modeling to identify and investigate potential dispersal pathways for this species between the two areas during the late Pleistocene. Niches estimated for the two populations did not differ significantly. Our analyses indicated two possible, but a single most likely, potential routes of dispersal during the last glacial cycle. These results are important to understanding the history of Amazon Basin humid forest biotas, as they suggest agents of isolation among putative humid forest refugia in the form of dry forest and scrub, and associated biotas.

Ecological Niche Modeling; Amazon Basin; Biogeography; Forest Refugia; Last Glacial Maximum


Actualmente existen dos áreas de distribución disyuntas de la serpiente de cascabel Crotalus durissus, afín a hábitats abiertos, al norte y al sur de la cuenca del Río Amazonas, separadas por selvas húmedas. Usamos técnicas de modelado de nicho ecológico para identificar corredores potenciales de dispersión para esta especie entre las dos áreas en el Pleistoceno tardío. Los nichos estimados para las poblaciones de cada una de las áreas de distribución no presentaron diferencias significativas. Nuestros análisis identificaron un corredor de dispersión más probable para esta especie durante el Último Máximo Glaciar. Estos resultados tienen implicaciones para el entendimiento de la historia de las biotas de las selvas húmedas del Amazonas, ya que sugieren causas de aislamiento entre refugios potenciales de selva húmeda, en la forma de selva seca y matorral.

Modelado de Nicho Ecológico; Amazonas; Biogeografía; Refugios Pleistocénicos; Último Máximo Glaciar


Introduction

The events leading to the present diversity of species across the Amazon Basin have been pondered since the time of Darwin (Mayr and O’Hara 1986MAYR, E. & O’HARA, R.J. 1986. The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution 40:55-67, doi: 10.2307/2408603
10.2307/2408603...
, Nores 1999NORES, M. 1999. An alternative hypothesis for the origin of Amazonian bird diversity. J. Biogeogr. 26:475-485, doi: 10.1046/j.1365-2699.1999.t01-1-00311.x
10.1046/j.1365-2699.1999.t01-1-00311.x...
, Bush and de Oliveira 2006BUSH, M.B. & DE OLIVEIRA, P.E. 2006. The rise and fall of the refugial hypothesis of Biota Neotrop. 6, doi: http://dx.doi.org/10.1590/S1676-06032006000100002.
http://dx.doi.org/10.1590/S1676-06032006...
). However, effects of past climate shifts on present-day biotic diversity can be difficult to discern because they depend on complex interactions among multiple biotic and abiotic factors. Earliest assumptions were of stable tropical rainforest ecosystems that had remained largely unchanged since the Cenozoic (Fischer 1960FISCHER, A.G. 1960. Latitudinal variations in organic diversity. Evolution 14:64-81., Bush 1994BUSH, M.B. 1994. Amazonian speciation: a necessarily complex model. J. Biogeog. 21:5-17, doi: 10.2307/2845600
10.2307/2845600...
, Nores 1999NORES, M. 1999. An alternative hypothesis for the origin of Amazonian bird diversity. J. Biogeogr. 26:475-485, doi: 10.1046/j.1365-2699.1999.t01-1-00311.x
10.1046/j.1365-2699.1999.t01-1-00311.x...
). This idea was replaced by the Pleistocene Refugium Hypothesis (PRH) beginning in the late 1960s (Haffer 1969HAFFER, J. 1969. Speciation in Amazon forest birds. Science 165:131-137.), and gaining considerable popularity thereafter. Given improved understanding of geologic history and impacts on climate and hydrologic systems, the PRH provided a more adequate explanation of the distribution and diversity of modern taxa in the region.

The PRH posits substantial retractions and fragmentation of humid rainforests in the face of advancing savannahs during the cooler, drier climates of the Last Glacial Maximum (LGM, ∼21,000-18,000 yr BP) and preceding glacial events. This hypothesis has been resurrected and amended in various forms (Mayr and O’Hara 1986MAYR, E. & O’HARA, R.J. 1986. The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution 40:55-67, doi: 10.2307/2408603
10.2307/2408603...
). However, as data from sedimentary core samples from across the Amazon Basin and marine isotope analyses shed light on climatic cycles and likely regional vegetation responses throughout the Quaternary (van der Hammen and Hooghiemstra 2000VAN DER HAMMEN, T. & HOOGHIEMSTRA, H. 2000. Neogene and Quaternary history of vegetation, climate, and plant diversity in Amazonia. Quaternary. Sci. Rev. 19:725-742, doi: 10.1016/S0277-3791(99)00024-4
10.1016/S0277-3791(99)00024-4...
, Bush 1994BUSH, M.B. 1994. Amazonian speciation: a necessarily complex model. J. Biogeog. 21:5-17, doi: 10.2307/2845600
10.2307/2845600...
, Bush and de Oliveira 2006), researchers have suggested more moderate explanations for Pleistocene range fragmentation, such as increased vegetation heterogeneity in the region, perhaps with dry-forest conditions constituting the cool-climate matrix rather than savannah (Nores 1999NORES, M. 1999. An alternative hypothesis for the origin of Amazonian bird diversity. J. Biogeogr. 26:475-485, doi: 10.1046/j.1365-2699.1999.t01-1-00311.x
10.1046/j.1365-2699.1999.t01-1-00311.x...
, Bonaccorso et al. 2006BONACCORSO, E., KOCH, I. & PETERSON, A.T. 2006. Pleistocene fragmentation of Amazon species’ ranges. Divers. Distrib. 12:157-1164, doi: 10.1111/ddi.2006.12.issue-2
10.1111/ddi.2006.12.issue-2...
, Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183., Bush et al. 2011BUSH, M.B., GOSLING, W.D. & COLINVAUX, P.A. 2011. Climate and vegetation change in the lowlands of the Amazon Basin, p. 61-84. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.).

The Pleistocene (∼2.58 My-11.7 Ky BP) saw a series of global cooling events alternating with warmer periods: temperature fluctuations averaged 4-5°C, and precipitation varied by 50-60% (van der Hammen and Hooghiemstra 2000, Bush and de Oliveira 2006, Lawing and Polly 2011LAWING, A.M. & POLLY, P.D. 2011. Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species’ response to climate change. PLoS ONE 6:e28554, doi: 10.1371/journal.pone.0028554
10.1371/journal.pone.0028554...
). Paleoreconstuctions of the Last Interglacial period (LIG; ∼130,000-116,000 yr BP) indicate climates similar to or possibly even warmer than those of the present day (Otto-Bliesner et al. 2008), whereas the LGM (∼21,000-18,000 yr BP) was characterized by cold and dry climates in continental regions worldwide (van der Hammen and Hooghiemstra 2000, Braconnot et al. 2007BRACONNOT, P., OTTO-BLIESNER, B., HARRISON, S., JOUSSAUME, S., PETERCHMITT, J.Y., ABE-OUCHI, A., CRUCIFIX, M., DRIESSCHAERT, E., FICHEFET, T., HEWITT, C.D., KAGEYAMA, M., KITOH, A., LAÎNÉ, A., LOUTRE, M.F., MARTI, O., MERKEL, U., RAMSTEIN, G., VALDES, P., WEBER, S.L., YU, Y. & ZHAO, Y. 2007. Results of PMIP2 coupled simulations of the mid-Holocene and Last Glacial Maximum - part 1: experiments and large-scale features. Clim. Past 3:261-277, doi: 10.5194/cp-3-261-2007
10.5194/cp-3-261-2007...
). Ehlers and Gibbard (2007)EHLERS, J. & GIBBARD, P. 2007. The extent and chronology of Cenozoic global glaciation. Quatern. Int. 164-165:6-20, doi: 10.1016/j.quaint.2006.10.008
10.1016/j.quaint.2006.10.008...
suggested at least 20 glacial cycles over the previous 2.6 My BP, most within the last ∼900,000 yr.

Ecological niche modeling (ENM), in combination with paleoclimatic reconstructions, provides researchers with a powerful tool with which to “retrodict” potential past distributions of species for key points in time (e.g., LIG, LGM), and can be particularly useful for investigating hypotheses such as the PRH (Waltari et al. 2007WALTARI, E., HIJMANS, R.J., PETERSON, A.T., NYÁRI, Á.S., PERKINS, S.L. & GURALNICK, R.P. 2007. Locating Pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS One 2:e563, doi: 10.1371/journal.pone.0000563
10.1371/journal.pone.0000563...
, Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183.). Availability of climatic reconstructions for the Pleistocene allows exploration of paleo-distributional potential of species, including the location and timing of range disjunctions and potential dispersal routes. Although previous ENM studies of Amazon Basin biotas have indicated that distributions of forest species did fragment owing to climate changes (Bonaccorso et al. 2006BONACCORSO, E., KOCH, I. & PETERSON, A.T. 2006. Pleistocene fragmentation of Amazon species’ ranges. Divers. Distrib. 12:157-1164, doi: 10.1111/ddi.2006.12.issue-2
10.1111/ddi.2006.12.issue-2...
, Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183.), few have reconstructed the converse phenomenon of broadened distributions of savannah species (Bonaccorso et al. 2006BONACCORSO, E., KOCH, I. & PETERSON, A.T. 2006. Pleistocene fragmentation of Amazon species’ ranges. Divers. Distrib. 12:157-1164, doi: 10.1111/ddi.2006.12.issue-2
10.1111/ddi.2006.12.issue-2...
, Collevatti et al. 2012COLLEVATTI, R.G., TERRIBILE, L.C., LIMA-RIBEIRO, M.S., NABOUT, J.C., DE OLIVEIRA, G., RANGEL, T.F., RABELO, S.G. & DINIZ-FILHO, J.A.F. 2012. A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a Neotropical seasonally dry forest tree species. Mol. Ecol. 21:5845-5863, doi: 10.1111/mec.12071
10.1111/mec.12071...
).

Here, we use LGM and LIG paleoclimatic reconstructions in an ENM framework to understand possible effects of Pleistocene climatic shifts on Amazon Basin habitats via analysis of an open-habitat species, the rattlesnake Crotalus durissus L., 1758. Despite high diversity of rattlesnakes in North America, C. durissus is the only rattlesnake species to have colonized South America broadly (Tozetti and Martins 2008TOZETTI, A.M. & MARTINS, M. 2008. Habitat use by the South-American rattlesnake (Crotalus durissus) in south-eastern Brazil. J. Nat. Hist. 42:1435-1444, doi: 10.1080/00222930802007823
10.1080/00222930802007823...
). Populations of this species are found across a broad range in Mesoamerica, and in South America north and south of the Amazon Basin. Though predominantly found in the cerrado formations known as campo cerrado and campo sujo, (Wüster et al. 2005aWÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005a. Tracing an invasion: landbridges, refugia and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol. Ecol. 14:1095-1108, doi: 10.1111/j.1365-294X.2005.02471.x
10.1111/j.1365-294X.2005.02471.x...
, Quijada-Mascareãas et al. 2007QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
10.1111/j.1365-2699.2007.01707.x...
), C. durissus populations are also known from fragmented dry forest habitats and disturbed areas (Bastos et al. 2005BASTOS, E.G.M., DE ARAÚJO, A.F.B. & DA SILVA, H.R. 2005. Records of the rattlesnakes Crotalus durissus terrificus (Laurenti) (Serpentes, Viperidae) in the state of Rio de Janeiro, Brazil: a possible case of invasion facilitated by deforestation. Rev. Bras. Zool. 22:812-815, doi: 10.1590/S0101-81752005000300047
10.1590/S0101-81752005000300047...
, Quijada-Mascareãas et al. 2007QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
10.1111/j.1365-2699.2007.01707.x...
, Tozetti and Martins 2008TOZETTI, A.M. & MARTINS, M. 2008. Habitat use by the South-American rattlesnake (Crotalus durissus) in south-eastern Brazil. J. Nat. Hist. 42:1435-1444, doi: 10.1080/00222930802007823
10.1080/00222930802007823...
, Tozetti et al. 2009TOZETTI, A.M., VETTORAZZO, V. & MARTINS, M. 2009. Short-term movement of the South American rattlesnake (Crotalus durissus) in southeastern Brazil. Herpetol. J. 19:201-206.). As a result, a distributional understanding for this species through time may be particularly illuminating as regards the distributional history of Amazonian biotas.

Materials and Methods

1. Input Data

Occurrence data for six disjunct populations of the C. durissus complex across Central and South America were kindly provided by A. Quijada-Mascareãas (pers. comm.). In light of the coarse spatial resolution of available paleoclimatic reconstructions, we focused analyses on the two populations in South America, for which 55 unique occurrences for the northern population and 28 occurrences for the southern population (Figure 1) were available. As these sets of occurrences are distinctly located north and south of the Amazon Basin, their potential for range shifts during Pleistocene cooling events is of particular relevance.

Figure 1
Model calibration regions for Crotalus durissus overlaid on a map of ecoregions (Olson et al. 2001OLSON, D.M., DINERSTEIN, E., WIKRAMANAYAKE, E.D., BURGESS, N.D., POWELL, G.V.N., UNDERWOOD, E.C., D’AMICO, J.A., ITOUA, I., STRAND, H.E., MORRISON, J.C., LOUCKS, C.J., ALLNUTT, T.F., RICKETTS, T.H., KURA, Y., LAMOREAUX, J.F., WETTENGEL, W.W., HEDAO, P. & KASSEM, K.R. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51:933- 938.). Thick black line delineates training regions (M) for northern and southern populations; triangles indicate present-day C. durissus occurrence points used in this study.

Present-day climatic data were acquired from the WorldClim database (Hijmans et al. 2005HIJMANS, R.J., CAMERON, S. & PARRA, J. 2005. WorldClim v.1.3. http://biogeo.berkely.edu/worldclim/worldclim.htm. University of California. Berkeley, CA.
http://biogeo.berkely.edu/worldclim/worl...
). Parallel Late Pleistocene bioclimatic layers (LGM and LIG) were derived from downscaled global climate outputs from the Community Climate System Model (CCSM). LGM data were obtained from the Paleoclimate Modeling Intercomparison Project Phase II (PMIP2, Braconnot et al. 2007BRACONNOT, P., OTTO-BLIESNER, B., HARRISON, S., JOUSSAUME, S., PETERCHMITT, J.Y., ABE-OUCHI, A., CRUCIFIX, M., DRIESSCHAERT, E., FICHEFET, T., HEWITT, C.D., KAGEYAMA, M., KITOH, A., LAÎNÉ, A., LOUTRE, M.F., MARTI, O., MERKEL, U., RAMSTEIN, G., VALDES, P., WEBER, S.L., YU, Y. & ZHAO, Y. 2007. Results of PMIP2 coupled simulations of the mid-Holocene and Last Glacial Maximum - part 1: experiments and large-scale features. Clim. Past 3:261-277, doi: 10.5194/cp-3-261-2007
10.5194/cp-3-261-2007...
); LIG data (∼140,000-120,000 yr BP) were kindly made available by C. Ammann (pers. comm.), based on Otto-Bliesner et al. (2006)OTTO-BLIESNER, B.L., MARSHALL, S.J., OVERPECK, J.T., MILLER, G.H., HU, A. & CAPE LAST INTERGLACIAL PROJECT MEMBERS. 2006. Simulating arctic warmth and icefield retreat in the Last Interglacial. Science 311:1751-1753, doi: 10.1126/science.1120808
10.1126/science.1120808...
, and downscaled and prepared by R. Hijmans (pers. comm.). As a result, we were able to characterize distributional responses to major climatic events over the past 135,000 yr. Because robustness of ENMs is highly dependent on the complexity of the environmental spaces in which they are calibrated (Peterson and Nakazawa 2008PETERSON, A.T. & NAKAZAWA, Y. 2008. Environmental data sets matter in ecological niche modeling: an example with Solenopsis invicta and Solenopsis richteri. Global Ecol. Biogeogr. 17:135-144., Peterson et al. 2011PETERSON, A.T., SOBER=N, J., PEARSON, R.G., ANDERSON, R.P., MARTINEZ-MEYER, E., NAKAMURA, M. & ARÚJO, M.B. 2011. Ecological Niches and Geographic Distributions. Princeton University Press, Princeton.), we took care not to calibrate models in highly dimensional spaces. Seven variables showing low correlations (<0.8) were used in ENM calibration (annual mean temperature, mean diurnal range, maximum temperature of the warmest month, minimum temperature of the coldest month, annual precipitation, and precipitation of wettest and driest months). All analyses were conducted at a spatial resolution of 2.5’, or ∼5 km.

Model calibration regions were delineated carefully, as most presence-only niche modeling algorithms generate background information, or pseudoabsences, based on these areas (Stockwell 1999STOCKWELL, D. 1999. The GARP modelling system: problems and solutions to automated spatial prediction. Int. J. Geogr. Inf. Sci. 13:143-158, doi: 10.1080/136588199241391
10.1080/136588199241391...
, Phillips et al. 2006PHILLIPS, S.J., ANDERSON, R.P. & SCHAPIRE, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190:231-259, doi: 10.1016/j.ecolmodel.2005.03.026
10.1016/j.ecolmodel.2005.03.026...
, Pearson et al. 2007PEARSON, R.G., RAXWORTHY, C.J., NAKAMURA, M. & PETERSON, A.T. 2007. Predicting species’ distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34:102-117, doi: 10.1111/j.1365-2699.2006.01594.x
10.1111/j.1365-2699.2006.01594.x...
, Warren et al. 2010WARREN, D.L., GLOR, R.E. & TURELLI, M. 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607-611, doi: 10.1111/eco.2010.33.issue-1
10.1111/eco.2010.33.issue-1...
). In this step we followed Barve et al. (2011)BARVE, N., BARVE, V., JIMÉNEZ-VALVERDE, A., LIRA-NORIEGA, A., MAHER, S.P., PETERSON, A.T., SOBER=N, J. & VILLALOBOS, F. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol. Model. 222:1810-1819, doi: 10.1016/j.ecolmodel.2011.02.011
10.1016/j.ecolmodel.2011.02.011...
: we attempted to identify areas that had been accessible to the species over relevant time periods, whether suitable or not, in effect a hypothesis of M in the Biotic-Abiotic-Mobility (BAM) framework (Peterson et al. 2011PETERSON, A.T., SOBER=N, J., PEARSON, R.G., ANDERSON, R.P., MARTINEZ-MEYER, E., NAKAMURA, M. & ARÚJO, M.B. 2011. Ecological Niches and Geographic Distributions. Princeton University Press, Princeton.). These hypothesized accessible areas were bounded to the west by the eastern foothills of the Andes and to the east by the Atlantic Ocean. The calibration area for the northern population extended north to encompass the full extent of the coastline; that of the southern population extended south into north-central Argentina. Designation of the accessible area in the Amazon Basin was chosen arbitrarily at roughly half the distance between the known occurrence points of the two populations (Figure 1). We transferred model results to the whole of South America to allow interpretation of potential dispersal routes at a continental scale during LGM.

2. Niche Similarity

As an initial step, we used ENMTools (Version 1.3, http://enmtools.blogspot.com/) to test hypotheses of niche similarity between the two populations. Described in depth by Warren et al. (2010)WARREN, D.L., GLOR, R.E. & TURELLI, M. 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607-611, doi: 10.1111/eco.2010.33.issue-1
10.1111/eco.2010.33.issue-1...
, the program works in conjunction with Maxent (Phillips et al. 2006PHILLIPS, S.J., ANDERSON, R.P. & SCHAPIRE, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190:231-259, doi: 10.1016/j.ecolmodel.2005.03.026
10.1016/j.ecolmodel.2005.03.026...
) to test whether two populations have environmental characteristics of occurrences more or less similar than random expectations. The “background” area specified in this test for each population is the accessible area (M) described above. The program compares niche models via two similarity metrics (Schoener’s D and I) based on known occurrences of one of the two populations with niche models based on points drawn at random from the “background” (M) of the other. This process was repeated 1000 times to create a null distribution of background similarity values. ENMs were generated for each population in Maxent, and thresholded to the least training presence value (Pearson et al. 2007PEARSON, R.G., RAXWORTHY, C.J., NAKAMURA, M. & PETERSON, A.T. 2007. Predicting species’ distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34:102-117, doi: 10.1111/j.1365-2699.2006.01594.x
10.1111/j.1365-2699.2006.01594.x...
). Finally, we compared observed similarity values to the null distribution, rejecting the null hypothesis of similarity if the observed fell below the fifth percentile of the distribution of null values.

3. Ecological Niche Modeling

Because observed values for niche similarity for both similarity metrics were well above the critical values of the null distributions (Figure 2), we were unable to reject the null hypothesis (all P ≥ 0.997); we thus accepted that no significant dissimilarity exists between niches of northern and southern South American populations of C. durissus. In view of these results, occurrences of the two populations were combined (i.e., the two calibration regions and occurrence data) to obtain an overview of likely geographic limits of the distribution of C. durissus through time.

Figure 2
Niche background similarity distributions for one-tailed testing of similarity of niches between northern and southern Crotalus durissus populations for D and I similarity indices. The observed degree of similarity between the two species is shown as a black arrow.

Niches were estimated and paleodistributional projections made using two common ENM algorithms: the openModeller (OM-GARP version 1.1, Muãoz et al. 2011MUÑOZ, M.E.S., GIOVANNI, R., SIQUEIRA, M.F., SUTTON, T., BREWER, P., PEREIRA, R.S., CANHOS, D.A.L. & CANHOS, V.P. 2011. OpenModeller: a generic approach to species' potential distribution modelling. Geoinformatica 15:111-135, doi: 10.1007/s10707-009-0090-7
10.1007/s10707-009-0090-7...
) implementation of the Genetic Algorithm for Rule-set Prediction (GARP, Stockwell 1999STOCKWELL, D. 1999. The GARP modelling system: problems and solutions to automated spatial prediction. Int. J. Geogr. Inf. Sci. 13:143-158, doi: 10.1080/136588199241391
10.1080/136588199241391...
) and a maximum entropy approach (Maxent, Phillips et al. 2006PHILLIPS, S.J., ANDERSON, R.P. & SCHAPIRE, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190:231-259, doi: 10.1016/j.ecolmodel.2005.03.026
10.1016/j.ecolmodel.2005.03.026...
). Both algorithms were set to 1000 bootstrapped runs for up to 1000 iterations of estimation. GARP models were run to a 1% convergence criterion, with extrinsic testing of omission, a relative omission threshold (20% of the distribution), and a 50% commission threshold (Anderson et al. 2003ANDERSON, R.P., LEW, D. & PETERSON, A.T. 2003. Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol. Model. 162:211-232, doi: 10.1016/S0304-3800(02)00349-6
10.1016/S0304-3800(02)00349-6...
), producing 100 final models for interpretation, which were summed to produce a single map of model agreement. Maxent was set for 100 bootstrap replicates; all other settings were left at default. Suitability thresholds for interpretation of models from both algorithms were based on least training presence criteria (Pearson et al. 2006PEARSON, R.G., THUILLER, W., ARAÚJO, M.B., MARTINEZ-MEYER, E., BROTONS, L., MCCLEAN, C., MILES, L., SEGURADO, P., DAWSON, T.P. & LEES, D.C. 2006. Model-based uncertainty in species range prediction. J. Biogeogr. 33:1704-1711, doi: 10.1111/jbi.2006.33.issue-10
10.1111/jbi.2006.33.issue-10...
), modified to consider possible error rates (E) of 0, 1, 5, and 10% (Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183., Peterson et al. 2011PETERSON, A.T., SOBER=N, J., PEARSON, R.G., ANDERSON, R.P., MARTINEZ-MEYER, E., NAKAMURA, M. & ARÚJO, M.B. 2011. Ecological Niches and Geographic Distributions. Princeton University Press, Princeton.).

Finally, to explore responses to key climatic parameters, we developed niche visualizations following a modification of the approaches of Elith et al. (2005)ELITH, J., FERRIER, S., HUETTMANN, F. & LEATHWICK, J. 2005. The evaluation strip: a new and robust method for plotting predicted responses from species distribution models. Ecol. Model. 186:280-289, doi: 10.1016/j.ecolmodel.2004.12.007
10.1016/j.ecolmodel.2004.12.007...
and Owens et al. (2013)OWENS, H.L., CAMPBELL, L.P., DORNAK, L.L., SAUPE, E.E., BARVE, N., SOBER=N, J., INGENLOFF, K., LIRA-NORIEGA, A., HENSZ, C.M., MEYERS, C.E. & PETERSON, A.T. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263:10-18, doi: 10.1016/j.ecolmodel.2013.04.011
10.1016/j.ecolmodel.2013.04.011...
: simple models were constructed based on two generalized bioclimatic variables (mean annual temperature and precipitation) and projected onto a two-dimensional space wherein the x-axis equates to a broad spectrum of mean annual temperatures (-100-100°C) and the y-axis corresponds to a similar spectrum of mean annual precipitation values (0-15,000 mm; see Owens et al. 2013OWENS, H.L., CAMPBELL, L.P., DORNAK, L.L., SAUPE, E.E., BARVE, N., SOBER=N, J., INGENLOFF, K., LIRA-NORIEGA, A., HENSZ, C.M., MEYERS, C.E. & PETERSON, A.T. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263:10-18, doi: 10.1016/j.ecolmodel.2013.04.011
10.1016/j.ecolmodel.2013.04.011...
for further illustration of this approach). ENMs were calibrated using the pooled C. durissus occurrence data and present-day bioclimatic data using GARP and Maxent, as described above.

Results

The niche visualizations (Figure 3) offer a two-dimensional view of temperature and precipitation responses of the species, but also suggest the need for some caution with transferring models onto conditions outside those over which our model was calibrated (Owens et al. 2013OWENS, H.L., CAMPBELL, L.P., DORNAK, L.L., SAUPE, E.E., BARVE, N., SOBER=N, J., INGENLOFF, K., LIRA-NORIEGA, A., HENSZ, C.M., MEYERS, C.E. & PETERSON, A.T. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263:10-18, doi: 10.1016/j.ecolmodel.2013.04.011
10.1016/j.ecolmodel.2013.04.011...
). The two models (GARP and Maxent) differed in the response surface shape reconstructed, although which is more “correct” is not clear.

Figure 3
GARP (left) and Maxent (right) projections of Crotalus durissus occurrences and ecological niche models visualized using a calibration strip. The x-axis expresses mean annual temperature (-100 to 100˚C) and the y-axis shows annual precipitation (0 to 15,000 mm). Circles indicate C. durissus occurrences. Boxes indicate ranges of conditions manifested across the combined (north and south) calibration region.

Model projections onto current conditions emphasized the disjunct nature of the present potential distribution of the species (Figure 4). Paleoprojection outputs indicated a climatically suitable dispersal corridor for C. durissus across the eastern part of the Amazon Basin during the cooler, drier climates of the LGM (Figure 4). GARP further identified a possible corridor from the northwest south along the eastern foothills of the Andes. Both of these corridors were in areas where projections onto LIG and present-day conditions indicated climatic barriers to trans-Amazonian dispersal (Figure 4). Visually, model outputs for the two algorithms showed high agreement as regards general patterns of bioclimatic suitability shifts across time periods. However, whereas Maxent projections showed broader areas of suitability during the transition from the LIG (22.4%) to the LGM (30.5%), GARP projected decreased suitable area from LIG (30.2%) to LGM (24.9%).

Figure 4
Projections of modeled potential distributional areas for Crotalus durissus during the Last Interglacial, Last Glacial Maximum (LGM), and the present day. Black lines indicate climatically suitable dispersal corridors reconstructed at LGM. Suitability is indicated via shading, with white denoting areas of high climatic suitability, light gray moderate suitability, and dark gray low suitability. Black triangles indicate present-day occurrence points.

Discussion

Our paleodistributional reconstructions concur with those of prior ENM-based studies indicating LGM expansion of cerrado and other dry-habitat biomes (Collevatti et al. 2012COLLEVATTI, R.G., TERRIBILE, L.C., LIMA-RIBEIRO, M.S., NABOUT, J.C., DE OLIVEIRA, G., RANGEL, T.F., RABELO, S.G. & DINIZ-FILHO, J.A.F. 2012. A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a Neotropical seasonally dry forest tree species. Mol. Ecol. 21:5845-5863, doi: 10.1111/mec.12071
10.1111/mec.12071...
, Bonatelli et al. 2014BONATELLI, I.A.S., PEREZ, M.F., PETERSON, A.T., TAYLOR, N.P., ZAPPI, D.C., MACHADO, M.C., KOCH, I., PIRES, A.H.C. & MORAES, E.M. 2014. Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol. Ecol. 23:3044-3063, doi: 10.1111/mec.12780
10.1111/mec.12780...
), as well as those which identified LGM barriers for forest that coincide with our reconstructed dispersal corridors for a non-forest species (Bonaccorso et al. 2006BONACCORSO, E., KOCH, I. & PETERSON, A.T. 2006. Pleistocene fragmentation of Amazon species’ ranges. Divers. Distrib. 12:157-1164, doi: 10.1111/ddi.2006.12.issue-2
10.1111/ddi.2006.12.issue-2...
, Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183.). Although projections from niche modeling algorithms presently provide only a single, generalized snapshot of climatic suitability for a given time slice, they illuminate processes affecting the broader distributional potential of C. durissus since the LIG. A variety of studies, including genetic (Wüster et al. 2005aWÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005a. Tracing an invasion: landbridges, refugia and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol. Ecol. 14:1095-1108, doi: 10.1111/j.1365-294X.2005.02471.x
10.1111/j.1365-294X.2005.02471.x...
,bWÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005b. No rattlesnakes in the rainforests: reply to Gosling and Bush. Mol. Ecol. 14:3619-3621, doi: 10.1111/mec.2005.14.issue-11
10.1111/mec.2005.14.issue-11...
, Quijada-Mascareãas et al. 2007QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
10.1111/j.1365-2699.2007.01707.x...
), paleoecological (Prado and Gibbs 1993PRADO, D.E. & GIBBS, P.E. 1993. Patterns of species distributions in the dry seasonal forests of South America. Ann. Mo. Bot. Gard. 80:902-927, doi: 10.2307/2399937
10.2307/2399937...
, Pennington et al. 2000PENNINGTON, R.T., PRADO, D.E. & PENDRY, C.A. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27:261-273, doi: 10.1046/j.1365-2699.2000.00397.x
10.1046/j.1365-2699.2000.00397.x...
, Mayle et al. 2004MAYLE, F.E., BEERLING, D.J., GOSLING, W.D. & BUSH, M.B. 2004. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos. T. R. Soc. Lon. B 359:499-514, doi: 10.1098/rstb.2003.1434
10.1098/rstb.2003.1434...
, Pennington et al. 2004PENNINGTON, R.T., LAVIN, M., PRADO, D.E., PENDRY, C.A., PELL, S.K. & BUTTERWORTH, C.A. 2004. Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philos. T. R. Soc. Lon. 359:515-537, doi: 10.1098/rstb.2003.1435
10.1098/rstb.2003.1435...
, Anhuf et al. 2006ANHUF, D., LEDRU, M.P., BEHLING, H., DA CRUZ JR, F.W., CORDEIRO, R.C., VAN DER HAMMEN, T., KARMANN, I., MARENGO, J.A., DE OLIVEIRA, P.E., PESSENDA, L., SIFFEDINE, A., ALBUQUERQUE, A.L. & DA SILVA DIAS, P.L. 2006. Paleo-environmental change in Amazonian and African rainforest during the LGM. Palaeogeogr. Palaeocl. 239:510-527, doi: 10.1016/j.palaeo.2006.01.017
10.1016/j.palaeo.2006.01.017...
, Cowling 2011COWLING, S.A. 2011. Ecophysiological response of lowland tropical plants to Pleistocene climate, p. 359- 380. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York., Hannah et al. 2011HANNAH, L., BETTS, R.A. & SHUGART, H.H. 2011. Modeling future effects of climate change on tropical forests, p. 411-429. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.), and paleoclimatic (Colinvaux and de Oliveira 2001COLINVAUX, P.A. & DE OLIVEIRA, P.E. 2001. Amazon plant diversity and climate through the Cenozoic. Palaeogeogr. Palaeocl. 166:51-63, doi: 10.1016/S0031-0182(00)00201-7
10.1016/S0031-0182(00)00201-7...
, Wang et al. 2004WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART, P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740-743, doi: 10.1038/nature03067
10.1038/nature03067...
, 2006WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., ITO, E. & SOLHEID, M. 2006. Interhemispheric anti-phasing of rainfall during the last glacial period. Quaternary Sci. Rev. 25:3391-3403, doi: 10.1016/j.quascirev.2006.02.009
10.1016/j.quascirev.2006.02.009...
, Kanner et al. 2012KANNER, L.C., BURNS, S.J., CHENG, H. & EDWARDS, R.L. 2012. High-latitude forcing of the South American summer monsoon during the Last Glacial. Science 335:570-573, doi: 10.1126/science.1213397
10.1126/science.1213397...
, Mosblech et al. 2012MOSBLECH, N.A.S., BUSH, M.B., GOSLING, W.D., HODELL, D., THOMAS, L., VAN CALSTEREN, P., CORREA-METRIO, A., VALENCIA, B.G., CURTIS, J. & VAN WOESIK, R. 2012. North Atlantic forcing of Amazonian precipitation during the last ice age. Nat. Geosci. 5:817-820, doi: 10.1038/ngeo1588
10.1038/ngeo1588...
) analyses, further support for these ideas. These results suggest a stepping-stone-like series of dispersal events across a heterogeneous topography dictated by effects of glacial-interglacial cycles (Vegas-Vilarrúbia et al. 2012VEGAS-VILARRÚBIA, T., NOGUÉ, S. & RULL, V. 2012. Global warming, habitat shifts and potential refugia for biodiversity conservation in the neotropical Guayana Highlands. Biol. Conserv. 152:159-168, doi: 10.1016/j.biocon.2012.03.036
10.1016/j.biocon.2012.03.036...
) and strongly influenced by the North Atlantic climate (Fritz et al. 2010FRITZ, S.C., BAKER, P.A., EKDAHL, E., SELTZER, G.O. & STEVENS, L.R. 2010. Millennial-scale climate variability during the last glacial period in the tropical Andes. Quaternary Sci. Rev. 29:1017-1024, doi: 10.1016/j.quascirev.2010.01.001
10.1016/j.quascirev.2010.01.001...
).

Though still not completely clear, overall understanding of late Pleistocene climatic events and biotic responses in the Amazon Basin has improved significantly in recent years. The vast majority of data feeding this understanding of South America’s climate during the Pleistocene derive from sites along the Atlantic seaboard and in the central Andes (Wang et al. 2004WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART, P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740-743, doi: 10.1038/nature03067
10.1038/nature03067...
, Whitney et al. 2011WHITNEY, B.S., MAYLE, F.E., PUNYASENA, S.W., FITZPATRICK, K.A., BURN, M.J., GUILLEN, R., CHAVEZ, E., MANN, D., PENNINGTON, R.T. & METCALFE, S.E.2011. A 45 kyr palaeoclimate record from the lowland interior of tropical South America. Palaeogeogr. Palaeocl. 307:177-192, doi: 10.1016/j.palaeo.2011.05.012
10.1016/j.palaeo.2011.05.012...
); however, limited data also now exist for South America’s continental interior (Whitney et al. 2011WHITNEY, B.S., MAYLE, F.E., PUNYASENA, S.W., FITZPATRICK, K.A., BURN, M.J., GUILLEN, R., CHAVEZ, E., MANN, D., PENNINGTON, R.T. & METCALFE, S.E.2011. A 45 kyr palaeoclimate record from the lowland interior of tropical South America. Palaeogeogr. Palaeocl. 307:177-192, doi: 10.1016/j.palaeo.2011.05.012
10.1016/j.palaeo.2011.05.012...
). While paleoclimatic reconstructions from the coastal and Central Andean regions suggest an overall increase in summer monsoon activity during the LGM, Whitney et al. (2011)WHITNEY, B.S., MAYLE, F.E., PUNYASENA, S.W., FITZPATRICK, K.A., BURN, M.J., GUILLEN, R., CHAVEZ, E., MANN, D., PENNINGTON, R.T. & METCALFE, S.E.2011. A 45 kyr palaeoclimate record from the lowland interior of tropical South America. Palaeogeogr. Palaeocl. 307:177-192, doi: 10.1016/j.palaeo.2011.05.012
10.1016/j.palaeo.2011.05.012...
concluded that South America’s continental interior and lowlands regions experienced significantly drier conditions. Generally, the Last Glacial period (10-110 Ky BP) was characterized by abrupt, millennial-scale climatic fluctuations correlating with northern glacial-interglacial cycles (Wang et al. 2004WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART, P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740-743, doi: 10.1038/nature03067
10.1038/nature03067...
, 2006WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., ITO, E. & SOLHEID, M. 2006. Interhemispheric anti-phasing of rainfall during the last glacial period. Quaternary Sci. Rev. 25:3391-3403, doi: 10.1016/j.quascirev.2006.02.009
10.1016/j.quascirev.2006.02.009...
, Kanner et al. 2012KANNER, L.C., BURNS, S.J., CHENG, H. & EDWARDS, R.L. 2012. High-latitude forcing of the South American summer monsoon during the Last Glacial. Science 335:570-573, doi: 10.1126/science.1213397
10.1126/science.1213397...
, Mosblech et al. 2012MOSBLECH, N.A.S., BUSH, M.B., GOSLING, W.D., HODELL, D., THOMAS, L., VAN CALSTEREN, P., CORREA-METRIO, A., VALENCIA, B.G., CURTIS, J. & VAN WOESIK, R. 2012. North Atlantic forcing of Amazonian precipitation during the last ice age. Nat. Geosci. 5:817-820, doi: 10.1038/ngeo1588
10.1038/ngeo1588...
). Varying in duration from a few hundred years to several thousand, episodes of high precipitation during active summer monsoons appear to have been associated with northern stadials (LGM, 20-25 Ky BP; Heinrich event 1, 15-17 Ky BP; and Younger Dryas, 11-13 Ky BP), while drier periods were associated with reduced monsoonal activity and interglacial events in the Northern Hemisphere (Wang et al. 2004WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART, P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740-743, doi: 10.1038/nature03067
10.1038/nature03067...
, 2006WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., ITO, E. & SOLHEID, M. 2006. Interhemispheric anti-phasing of rainfall during the last glacial period. Quaternary Sci. Rev. 25:3391-3403, doi: 10.1016/j.quascirev.2006.02.009
10.1016/j.quascirev.2006.02.009...
, Zech et al. 2008ZECH, R., MAY, J.H., KULL, C., ILGNER, J., KUBIK, P.W. & VEIT, H. 2008. Timing of the late Quaternary glaciation in the Andes from ∼15 to 40° S. J. Quaternary Sci. 23:635-647, doi: 10.1002/jqs.v23:6/7
10.1002/jqs.v23:6/7...
, Kanner at al. 2012KANNER, L.C., BURNS, S.J., CHENG, H. & EDWARDS, R.L. 2012. High-latitude forcing of the South American summer monsoon during the Last Glacial. Science 335:570-573, doi: 10.1126/science.1213397
10.1126/science.1213397...
).

The frequency and variable durations of these events may have presented opportunities for periodic dispersal events by C. durissus southward across the Amazon Basin as variable climatic conditions expanded and contracted suitable habitat patches (Vegas-Vilarrúbia et al. 2012VEGAS-VILARRÚBIA, T., NOGUÉ, S. & RULL, V. 2012. Global warming, habitat shifts and potential refugia for biodiversity conservation in the neotropical Guayana Highlands. Biol. Conserv. 152:159-168, doi: 10.1016/j.biocon.2012.03.036
10.1016/j.biocon.2012.03.036...
). Indeed, paleovegetation projections indicated expansion of cerrado and other grassland habitats across the eastern edge of the Amazon Basin (Anhuf et al. 2006ANHUF, D., LEDRU, M.P., BEHLING, H., DA CRUZ JR, F.W., CORDEIRO, R.C., VAN DER HAMMEN, T., KARMANN, I., MARENGO, J.A., DE OLIVEIRA, P.E., PESSENDA, L., SIFFEDINE, A., ALBUQUERQUE, A.L. & DA SILVA DIAS, P.L. 2006. Paleo-environmental change in Amazonian and African rainforest during the LGM. Palaeogeogr. Palaeocl. 239:510-527, doi: 10.1016/j.palaeo.2006.01.017
10.1016/j.palaeo.2006.01.017...
), as well as seasonally dry tropical forest (Whitney et al. 2011WHITNEY, B.S., MAYLE, F.E., PUNYASENA, S.W., FITZPATRICK, K.A., BURN, M.J., GUILLEN, R., CHAVEZ, E., MANN, D., PENNINGTON, R.T. & METCALFE, S.E.2011. A 45 kyr palaeoclimate record from the lowland interior of tropical South America. Palaeogeogr. Palaeocl. 307:177-192, doi: 10.1016/j.palaeo.2011.05.012
10.1016/j.palaeo.2011.05.012...
). Of course, caution must be exercised in stating explicitly where particular vegetation types expanded or contracted, particularly for cerrado versus seasonally dry forest (Pennington et al. 2000PENNINGTON, R.T., PRADO, D.E. & PENDRY, C.A. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27:261-273, doi: 10.1046/j.1365-2699.2000.00397.x
10.1046/j.1365-2699.2000.00397.x...
, Mayle et al. 2004MAYLE, F.E., BEERLING, D.J., GOSLING, W.D. & BUSH, M.B. 2004. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos. T. R. Soc. Lon. B 359:499-514, doi: 10.1098/rstb.2003.1434
10.1098/rstb.2003.1434...
, Pennington 2004), as modern distributions of seasonally dry tropical forest tend to be discontinuous and adjacent to cerrado (Mayle et al. 2004MAYLE, F.E., BEERLING, D.J., GOSLING, W.D. & BUSH, M.B. 2004. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos. T. R. Soc. Lon. B 359:499-514, doi: 10.1098/rstb.2003.1434
10.1098/rstb.2003.1434...
). However, given the broad climatic overlap of these two biomes at present, the general pattern of expansion and contraction in response to glacial cycles likely occurred in concert (Prado and Gibbs 1993PRADO, D.E. & GIBBS, P.E. 1993. Patterns of species distributions in the dry seasonal forests of South America. Ann. Mo. Bot. Gard. 80:902-927, doi: 10.2307/2399937
10.2307/2399937...
, Pennington et al. 2000PENNINGTON, R.T., PRADO, D.E. & PENDRY, C.A. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27:261-273, doi: 10.1046/j.1365-2699.2000.00397.x
10.1046/j.1365-2699.2000.00397.x...
).

Our modeling exercise indicated two possible routes of dispersal for C. durissus during the LGM: an Atlantic corridor and a western corridor along the foothills of the Andes. The Atlantic corridor, as reconstructed by both Maxent and GARP, falls in line with current understanding of overall dynamics of the coastal region of northeastern South America during the late Pleistocene. Determining the exact proportions of savannah versus seasonally dry forest will require more palynological and geomorphological data than are presently available (Prado and Gibbs 1993PRADO, D.E. & GIBBS, P.E. 1993. Patterns of species distributions in the dry seasonal forests of South America. Ann. Mo. Bot. Gard. 80:902-927, doi: 10.2307/2399937
10.2307/2399937...
, Colinvaux and de Oliveira 2001, Anhuf et al. 2006ANHUF, D., LEDRU, M.P., BEHLING, H., DA CRUZ JR, F.W., CORDEIRO, R.C., VAN DER HAMMEN, T., KARMANN, I., MARENGO, J.A., DE OLIVEIRA, P.E., PESSENDA, L., SIFFEDINE, A., ALBUQUERQUE, A.L. & DA SILVA DIAS, P.L. 2006. Paleo-environmental change in Amazonian and African rainforest during the LGM. Palaeogeogr. Palaeocl. 239:510-527, doi: 10.1016/j.palaeo.2006.01.017
10.1016/j.palaeo.2006.01.017...
, Quijada-Mascareãas et al. 2007QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
10.1111/j.1365-2699.2007.01707.x...
, Cowling 2011COWLING, S.A. 2011. Ecophysiological response of lowland tropical plants to Pleistocene climate, p. 359- 380. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York., Hannah et al. 2011HANNAH, L., BETTS, R.A. & SHUGART, H.H. 2011. Modeling future effects of climate change on tropical forests, p. 411-429. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.). However, the overarching pattern of change is consistent with periodic establishment of suitable habitat in lieu of favorable climatic conditions as suggested by our models.

The interior (western) corridor along the eastern base of the Andes identified in some of our models was not as well supported as the Atlantic corridor. The extent to which millennial-scale climate events of the Last Glacial cycle were manifested in interior South America remains unclear (Fritz et al. 2010FRITZ, S.C., BAKER, P.A., EKDAHL, E., SELTZER, G.O. & STEVENS, L.R. 2010. Millennial-scale climate variability during the last glacial period in the tropical Andes. Quaternary Sci. Rev. 29:1017-1024, doi: 10.1016/j.quascirev.2010.01.001
10.1016/j.quascirev.2010.01.001...
); however, a recent study by Mosblech et al. (2012)MOSBLECH, N.A.S., BUSH, M.B., GOSLING, W.D., HODELL, D., THOMAS, L., VAN CALSTEREN, P., CORREA-METRIO, A., VALENCIA, B.G., CURTIS, J. & VAN WOESIK, R. 2012. North Atlantic forcing of Amazonian precipitation during the last ice age. Nat. Geosci. 5:817-820, doi: 10.1038/ngeo1588
10.1038/ngeo1588...
found no evidence of significant drying of the western Amazon Basin in the last 94,000 years. While this result does not instill much confidence, lack of evidence of drying does not necessarily mean that vegetative communities in the region were not impacted by overall drier LGM conditions. In fact, the notion of an Andean dispersal corridor for savannah species during the LIG is not new (da Silva and Bates 2002DA SILVA, J.M.C. & BATES, J.M. 2002. Biogeographic patterns and conservation in the South American cerrado: a tropical savanna hotspot. BioScience. 52:225-234, doi: 10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2
10.1641/0006-3568(2002)052[0225:BPACIT]2...
), so until a better picture of paleoclimates of the South American interior emerges, the potential of an Andean route should not be discarded entirely.

Finally, phylogeographic investigations by Wüster et al. (2005aWÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005a. Tracing an invasion: landbridges, refugia and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol. Ecol. 14:1095-1108, doi: 10.1111/j.1365-294X.2005.02471.x
10.1111/j.1365-294X.2005.02471.x...
,b) and Quijada-Mascareãas et al. (2007)QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
10.1111/j.1365-2699.2007.01707.x...
found low sequence divergence between C. durissus populations north and south of the Amazon Basin, indicating a fairly recent (∼1.08 My BP, if molecular clock estimates are to be believed) vicariant event most probably via interruption of a corridor of suitable habitat. Assuming accuracy of this estimation, vicariance of C. durissus perhaps coincided with the Mid-Pleistocene Transition (MPT; 1.5 My - 650 Ky BP), a period exhibiting pseudo-periodic moderate climate shifts approximately every 100 Ky (Sepulcre et al. 2011SEPULCRE, S., VIDAL, L., TACHIKAWA, K., ROSTEK, F. & BARD, E. 2011. Sea-surface salinity variations in the northern Caribbean Sea across the Mid-Pleistocene Transition. Clim. Past 7:75-90, doi: 10.5194/cp-7-75-2011
10.5194/cp-7-75-2011...
). Despite on-going debate regarding the pattern and extent of vegetation shifts during the Pleistocene, at present no adequate climate data resources exist from which niche models can anticipate mid-Pleistocene distributional responses with any confidence. However, extrapolating from evidence for the more chaotic and extreme Late Pleistocene, MPT climate shifts could have provided windows of optimal conditions stable for long enough to facilitate dispersal from north to south across the Amazon Basin.

The issue of model transferability more generally in ENM studies is an ongoing challenge (Peterson et al. 2007PETERSON, A.T., PAPEŞ, M. & EATON, M. 2007. Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550-560., Owens et al. 2013OWENS, H.L., CAMPBELL, L.P., DORNAK, L.L., SAUPE, E.E., BARVE, N., SOBER=N, J., INGENLOFF, K., LIRA-NORIEGA, A., HENSZ, C.M., MEYERS, C.E. & PETERSON, A.T. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263:10-18, doi: 10.1016/j.ecolmodel.2013.04.011
10.1016/j.ecolmodel.2013.04.011...
), and some degree of uncertainty should be expected when projecting spatial and temporal responses of vegetation across time owing to the coarse spatio-temporal resolution (∼5 km resolution after downscaling) of paleoclimate reconstructions. A single grid cell at this resolution may often encompass diverse situations (Marchant and Lovett 2011MARCHANT, R. & LOVETT, J. 2011. Tropical environmental dynamics: a modeling perspective, p. 381-409. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.), leading to generalization of conditions. This generalization reduces ability to identify climatically suitable patches at finer extents, thus preventing detection of narrow barriers (Peterson and Nyári 2008PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183.). Further, because data available for the LGM and LIG encompass only climatic variables, our models are indicators of climatic suitability only, and do not distinguish directly among vegetation types or other landscape attributes (Nogués-Bravo 2009NOGUÉS-BRAVO, D. 2009. Predicting the past distribution of species climatic niches. Global Ecol. Biogeogr. 18:521-531, doi: 10.1111/geb.2009.18.issue-5
10.1111/geb.2009.18.issue-5...
).

Climate change is a significant factor in the future shifting of plant community structure subsequently impacting the distribution and survivability of most organisms on Earth. Knowledge of the spatiotemporal distribution of species is a major underpinning in understanding the evolution of biodiversity (Svenning et al. 2011SVENNING, J.S., FLØJGAARD, C., MARSKE, K.A., N=GUES-BRAVO, D. & NORMAND, S. 2011. Applications of species distribution modeling to paleobiology. Quaternary Sci. Rev. 30:2930-2947, doi: 10.1016/j.quascirev.2011.06.012
10.1016/j.quascirev.2011.06.012...
). Paleoreconstruction exercises such as the one we present here strengthen understanding of the biogeographic patterns of a given region, enhancing ability to assess “critical” areas more adequately and ultimately playing a significant role in management and preservation of regions such as the cerrado and other centers of endemism (da Silva and Bates 2002, Varela et al. 2011VARELA, S., LOBO, J.M. & HORTAL, J. 2011. Using species distribution models in paleobiogeography: a matter of data, predictors and concepts. Palaeogeogr. Palaeocl. 310:451-463, doi: 10.1016/j.palaeo.2011.07.021
10.1016/j.palaeo.2011.07.021...
). Exploration of model-based scenarios for many taxa in relation to critically, non-model-based studies (genetic, paleo-environmental studies, etc.), provide a form of “ground-truthing” for the model-based results. By identifying most parsimonious scenario(s) of species’ and community responses to past climate changes, we improve ability to develop and implement more effective, long-term management strategies in the face of projected future climate scenarios.

Acknowledgments

Robert Hijmans kindly carried out plaeoclimate downscaling. Adrian Quijada-Mascareãas initially suggested these analyses and provided occurrence data. Juan Manuel Ortega Rodríguez provided helpful comment and discussion. Translations were kindly provided by Enrique Martínez Meyer.

References

  • ANDERSON, R.P., LEW, D. & PETERSON, A.T. 2003. Evaluating predictive models of species’ distributions: criteria for selecting optimal models. Ecol. Model. 162:211-232, doi: 10.1016/S0304-3800(02)00349-6
    » 10.1016/S0304-3800(02)00349-6
  • ANHUF, D., LEDRU, M.P., BEHLING, H., DA CRUZ JR, F.W., CORDEIRO, R.C., VAN DER HAMMEN, T., KARMANN, I., MARENGO, J.A., DE OLIVEIRA, P.E., PESSENDA, L., SIFFEDINE, A., ALBUQUERQUE, A.L. & DA SILVA DIAS, P.L. 2006. Paleo-environmental change in Amazonian and African rainforest during the LGM. Palaeogeogr. Palaeocl. 239:510-527, doi: 10.1016/j.palaeo.2006.01.017
    » 10.1016/j.palaeo.2006.01.017
  • BARVE, N., BARVE, V., JIMÉNEZ-VALVERDE, A., LIRA-NORIEGA, A., MAHER, S.P., PETERSON, A.T., SOBER=N, J. & VILLALOBOS, F. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol. Model. 222:1810-1819, doi: 10.1016/j.ecolmodel.2011.02.011
    » 10.1016/j.ecolmodel.2011.02.011
  • BASTOS, E.G.M., DE ARAÚJO, A.F.B. & DA SILVA, H.R. 2005. Records of the rattlesnakes Crotalus durissus terrificus (Laurenti) (Serpentes, Viperidae) in the state of Rio de Janeiro, Brazil: a possible case of invasion facilitated by deforestation. Rev. Bras. Zool. 22:812-815, doi: 10.1590/S0101-81752005000300047
    » 10.1590/S0101-81752005000300047
  • BONACCORSO, E., KOCH, I. & PETERSON, A.T. 2006. Pleistocene fragmentation of Amazon species’ ranges. Divers. Distrib. 12:157-1164, doi: 10.1111/ddi.2006.12.issue-2
    » 10.1111/ddi.2006.12.issue-2
  • BONATELLI, I.A.S., PEREZ, M.F., PETERSON, A.T., TAYLOR, N.P., ZAPPI, D.C., MACHADO, M.C., KOCH, I., PIRES, A.H.C. & MORAES, E.M. 2014. Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Mol. Ecol. 23:3044-3063, doi: 10.1111/mec.12780
    » 10.1111/mec.12780
  • BRACONNOT, P., OTTO-BLIESNER, B., HARRISON, S., JOUSSAUME, S., PETERCHMITT, J.Y., ABE-OUCHI, A., CRUCIFIX, M., DRIESSCHAERT, E., FICHEFET, T., HEWITT, C.D., KAGEYAMA, M., KITOH, A., LAÎNÉ, A., LOUTRE, M.F., MARTI, O., MERKEL, U., RAMSTEIN, G., VALDES, P., WEBER, S.L., YU, Y. & ZHAO, Y. 2007. Results of PMIP2 coupled simulations of the mid-Holocene and Last Glacial Maximum - part 1: experiments and large-scale features. Clim. Past 3:261-277, doi: 10.5194/cp-3-261-2007
    » 10.5194/cp-3-261-2007
  • BUSH, M.B. 1994. Amazonian speciation: a necessarily complex model. J. Biogeog. 21:5-17, doi: 10.2307/2845600
    » 10.2307/2845600
  • BUSH, M.B. & DE OLIVEIRA, P.E. 2006. The rise and fall of the refugial hypothesis of Biota Neotrop. 6, doi: http://dx.doi.org/10.1590/S1676-06032006000100002
    » http://dx.doi.org/10.1590/S1676-06032006000100002
  • BUSH, M.B., GOSLING, W.D. & COLINVAUX, P.A. 2011. Climate and vegetation change in the lowlands of the Amazon Basin, p. 61-84. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.
  • COLINVAUX, P.A. & DE OLIVEIRA, P.E. 2001. Amazon plant diversity and climate through the Cenozoic. Palaeogeogr. Palaeocl. 166:51-63, doi: 10.1016/S0031-0182(00)00201-7
    » 10.1016/S0031-0182(00)00201-7
  • COLLEVATTI, R.G., TERRIBILE, L.C., LIMA-RIBEIRO, M.S., NABOUT, J.C., DE OLIVEIRA, G., RANGEL, T.F., RABELO, S.G. & DINIZ-FILHO, J.A.F. 2012. A coupled phylogeographical and species distribution modelling approach recovers the demographical history of a Neotropical seasonally dry forest tree species. Mol. Ecol. 21:5845-5863, doi: 10.1111/mec.12071
    » 10.1111/mec.12071
  • COWLING, S.A. 2011. Ecophysiological response of lowland tropical plants to Pleistocene climate, p. 359- 380. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.
  • DA SILVA, J.M.C. & BATES, J.M. 2002. Biogeographic patterns and conservation in the South American cerrado: a tropical savanna hotspot. BioScience. 52:225-234, doi: 10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2
    » 10.1641/0006-3568(2002)052[0225:BPACIT]2.0.CO;2
  • EHLERS, J. & GIBBARD, P. 2007. The extent and chronology of Cenozoic global glaciation. Quatern. Int. 164-165:6-20, doi: 10.1016/j.quaint.2006.10.008
    » 10.1016/j.quaint.2006.10.008
  • ELITH, J., FERRIER, S., HUETTMANN, F. & LEATHWICK, J. 2005. The evaluation strip: a new and robust method for plotting predicted responses from species distribution models. Ecol. Model. 186:280-289, doi: 10.1016/j.ecolmodel.2004.12.007
    » 10.1016/j.ecolmodel.2004.12.007
  • FISCHER, A.G. 1960. Latitudinal variations in organic diversity. Evolution 14:64-81.
  • FRITZ, S.C., BAKER, P.A., EKDAHL, E., SELTZER, G.O. & STEVENS, L.R. 2010. Millennial-scale climate variability during the last glacial period in the tropical Andes. Quaternary Sci. Rev. 29:1017-1024, doi: 10.1016/j.quascirev.2010.01.001
    » 10.1016/j.quascirev.2010.01.001
  • HAFFER, J. 1969. Speciation in Amazon forest birds. Science 165:131-137.
  • HANNAH, L., BETTS, R.A. & SHUGART, H.H. 2011. Modeling future effects of climate change on tropical forests, p. 411-429. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.
  • HIJMANS, R.J., CAMERON, S. & PARRA, J. 2005. WorldClim v.1.3. http://biogeo.berkely.edu/worldclim/worldclim.htm University of California. Berkeley, CA.
    » http://biogeo.berkely.edu/worldclim/worldclim.htm
  • KANNER, L.C., BURNS, S.J., CHENG, H. & EDWARDS, R.L. 2012. High-latitude forcing of the South American summer monsoon during the Last Glacial. Science 335:570-573, doi: 10.1126/science.1213397
    » 10.1126/science.1213397
  • LAWING, A.M. & POLLY, P.D. 2011. Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species’ response to climate change. PLoS ONE 6:e28554, doi: 10.1371/journal.pone.0028554
    » 10.1371/journal.pone.0028554
  • MARCHANT, R. & LOVETT, J. 2011. Tropical environmental dynamics: a modeling perspective, p. 381-409. In: Tropical Rainforest Responses to Climatic Change, 2nd Edition. Bush, M., Flenley, J., Gosling, W. (eds.). Springer-Praxis Books, New York, New York.
  • MAYLE, F.E., BEERLING, D.J., GOSLING, W.D. & BUSH, M.B. 2004. Responses of Amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos. T. R. Soc. Lon. B 359:499-514, doi: 10.1098/rstb.2003.1434
    » 10.1098/rstb.2003.1434
  • MAYR, E. & O’HARA, R.J. 1986. The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution 40:55-67, doi: 10.2307/2408603
    » 10.2307/2408603
  • MOSBLECH, N.A.S., BUSH, M.B., GOSLING, W.D., HODELL, D., THOMAS, L., VAN CALSTEREN, P., CORREA-METRIO, A., VALENCIA, B.G., CURTIS, J. & VAN WOESIK, R. 2012. North Atlantic forcing of Amazonian precipitation during the last ice age. Nat. Geosci. 5:817-820, doi: 10.1038/ngeo1588
    » 10.1038/ngeo1588
  • MUÑOZ, M.E.S., GIOVANNI, R., SIQUEIRA, M.F., SUTTON, T., BREWER, P., PEREIRA, R.S., CANHOS, D.A.L. & CANHOS, V.P. 2011. OpenModeller: a generic approach to species' potential distribution modelling. Geoinformatica 15:111-135, doi: 10.1007/s10707-009-0090-7
    » 10.1007/s10707-009-0090-7
  • NOGUÉS-BRAVO, D. 2009. Predicting the past distribution of species climatic niches. Global Ecol. Biogeogr. 18:521-531, doi: 10.1111/geb.2009.18.issue-5
    » 10.1111/geb.2009.18.issue-5
  • NORES, M. 1999. An alternative hypothesis for the origin of Amazonian bird diversity. J. Biogeogr. 26:475-485, doi: 10.1046/j.1365-2699.1999.t01-1-00311.x
    » 10.1046/j.1365-2699.1999.t01-1-00311.x
  • OLSON, D.M., DINERSTEIN, E., WIKRAMANAYAKE, E.D., BURGESS, N.D., POWELL, G.V.N., UNDERWOOD, E.C., D’AMICO, J.A., ITOUA, I., STRAND, H.E., MORRISON, J.C., LOUCKS, C.J., ALLNUTT, T.F., RICKETTS, T.H., KURA, Y., LAMOREAUX, J.F., WETTENGEL, W.W., HEDAO, P. & KASSEM, K.R. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51:933- 938.
  • OTTO-BLIESNER, B.L., MARSHALL, S.J., OVERPECK, J.T., MILLER, G.H., HU, A. & CAPE LAST INTERGLACIAL PROJECT MEMBERS. 2006. Simulating arctic warmth and icefield retreat in the Last Interglacial. Science 311:1751-1753, doi: 10.1126/science.1120808
    » 10.1126/science.1120808
  • OWENS, H.L., CAMPBELL, L.P., DORNAK, L.L., SAUPE, E.E., BARVE, N., SOBER=N, J., INGENLOFF, K., LIRA-NORIEGA, A., HENSZ, C.M., MEYERS, C.E. & PETERSON, A.T. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol. Model. 263:10-18, doi: 10.1016/j.ecolmodel.2013.04.011
    » 10.1016/j.ecolmodel.2013.04.011
  • PEARSON, R.G., THUILLER, W., ARAÚJO, M.B., MARTINEZ-MEYER, E., BROTONS, L., MCCLEAN, C., MILES, L., SEGURADO, P., DAWSON, T.P. & LEES, D.C. 2006. Model-based uncertainty in species range prediction. J. Biogeogr. 33:1704-1711, doi: 10.1111/jbi.2006.33.issue-10
    » 10.1111/jbi.2006.33.issue-10
  • PEARSON, R.G., RAXWORTHY, C.J., NAKAMURA, M. & PETERSON, A.T. 2007. Predicting species’ distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34:102-117, doi: 10.1111/j.1365-2699.2006.01594.x
    » 10.1111/j.1365-2699.2006.01594.x
  • PENNINGTON, R.T., PRADO, D.E. & PENDRY, C.A. 2000. Neotropical seasonally dry forests and Quaternary vegetation changes. J. Biogeogr. 27:261-273, doi: 10.1046/j.1365-2699.2000.00397.x
    » 10.1046/j.1365-2699.2000.00397.x
  • PENNINGTON, R.T., LAVIN, M., PRADO, D.E., PENDRY, C.A., PELL, S.K. & BUTTERWORTH, C.A. 2004. Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Philos. T. R. Soc. Lon. 359:515-537, doi: 10.1098/rstb.2003.1435
    » 10.1098/rstb.2003.1435
  • PETERSON, A.T., PAPEŞ, M. & EATON, M. 2007. Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550-560.
  • PETERSON, A.T. & NYÁRI, Á.S. 2008. Ecological niche conservatism and Pleistocene refugia in the Thrush-like mourner, Schiffornis sp., in the Neotropics. Evolution 62:173-183.
  • PETERSON, A.T. & NAKAZAWA, Y. 2008. Environmental data sets matter in ecological niche modeling: an example with Solenopsis invicta and Solenopsis richteri Global Ecol. Biogeogr. 17:135-144.
  • PETERSON, A.T., SOBER=N, J., PEARSON, R.G., ANDERSON, R.P., MARTINEZ-MEYER, E., NAKAMURA, M. & ARÚJO, M.B. 2011. Ecological Niches and Geographic Distributions. Princeton University Press, Princeton.
  • PHILLIPS, S.J., ANDERSON, R.P. & SCHAPIRE, R.E. 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190:231-259, doi: 10.1016/j.ecolmodel.2005.03.026
    » 10.1016/j.ecolmodel.2005.03.026
  • PRADO, D.E. & GIBBS, P.E. 1993. Patterns of species distributions in the dry seasonal forests of South America. Ann. Mo. Bot. Gard. 80:902-927, doi: 10.2307/2399937
    » 10.2307/2399937
  • QUIJADA-MASCAREÑAS, J.A., FERGUSON, J.E., POOK, C.E., DA GRAÇA SALOMÃO, M., THORPE, R.S. & WÜSTER, W. 2007. Phylogeographic patterns of trans-Amazonian vicariants and Amazonian biogeography: the Neotropical rattlesnake (Crotalus durissus complex) as an example. J. Biogeogr. 34:1296-1312, doi: 10.1111/j.1365-2699.2007.01707.x
    » 10.1111/j.1365-2699.2007.01707.x
  • SEPULCRE, S., VIDAL, L., TACHIKAWA, K., ROSTEK, F. & BARD, E. 2011. Sea-surface salinity variations in the northern Caribbean Sea across the Mid-Pleistocene Transition. Clim. Past 7:75-90, doi: 10.5194/cp-7-75-2011
    » 10.5194/cp-7-75-2011
  • STOCKWELL, D. 1999. The GARP modelling system: problems and solutions to automated spatial prediction. Int. J. Geogr. Inf. Sci. 13:143-158, doi: 10.1080/136588199241391
    » 10.1080/136588199241391
  • SVENNING, J.S., FLØJGAARD, C., MARSKE, K.A., N=GUES-BRAVO, D. & NORMAND, S. 2011. Applications of species distribution modeling to paleobiology. Quaternary Sci. Rev. 30:2930-2947, doi: 10.1016/j.quascirev.2011.06.012
    » 10.1016/j.quascirev.2011.06.012
  • TOZETTI, A.M. & MARTINS, M. 2008. Habitat use by the South-American rattlesnake (Crotalus durissus) in south-eastern Brazil. J. Nat. Hist. 42:1435-1444, doi: 10.1080/00222930802007823
    » 10.1080/00222930802007823
  • TOZETTI, A.M., VETTORAZZO, V. & MARTINS, M. 2009. Short-term movement of the South American rattlesnake (Crotalus durissus) in southeastern Brazil. Herpetol. J. 19:201-206.
  • VAN DER HAMMEN, T. & HOOGHIEMSTRA, H. 2000. Neogene and Quaternary history of vegetation, climate, and plant diversity in Amazonia. Quaternary. Sci. Rev. 19:725-742, doi: 10.1016/S0277-3791(99)00024-4
    » 10.1016/S0277-3791(99)00024-4
  • VARELA, S., LOBO, J.M. & HORTAL, J. 2011. Using species distribution models in paleobiogeography: a matter of data, predictors and concepts. Palaeogeogr. Palaeocl. 310:451-463, doi: 10.1016/j.palaeo.2011.07.021
    » 10.1016/j.palaeo.2011.07.021
  • VEGAS-VILARRÚBIA, T., NOGUÉ, S. & RULL, V. 2012. Global warming, habitat shifts and potential refugia for biodiversity conservation in the neotropical Guayana Highlands. Biol. Conserv. 152:159-168, doi: 10.1016/j.biocon.2012.03.036
    » 10.1016/j.biocon.2012.03.036
  • WALTARI, E., HIJMANS, R.J., PETERSON, A.T., NYÁRI, Á.S., PERKINS, S.L. & GURALNICK, R.P. 2007. Locating Pleistocene refugia: comparing phylogeographic and ecological niche model predictions. PLoS One 2:e563, doi: 10.1371/journal.pone.0000563
    » 10.1371/journal.pone.0000563
  • WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., CRISTALLI, P.S., SMART, P.L., RICHARDS, D.A. & SHEN, C.C. 2004. Wet periods in northeastern Brazil over the past 210 kyr linked to distant climate anomalies. Nature 432:740-743, doi: 10.1038/nature03067
    » 10.1038/nature03067
  • WANG, X., AULER, A.S., EDWARDS, R.L., CHENG, H., ITO, E. & SOLHEID, M. 2006. Interhemispheric anti-phasing of rainfall during the last glacial period. Quaternary Sci. Rev. 25:3391-3403, doi: 10.1016/j.quascirev.2006.02.009
    » 10.1016/j.quascirev.2006.02.009
  • WARREN, D.L., GLOR, R.E. & TURELLI, M. 2010. ENMTools: a toolbox for comparative studies of environmental niche models. Ecography 33:607-611, doi: 10.1111/eco.2010.33.issue-1
    » 10.1111/eco.2010.33.issue-1
  • WHITNEY, B.S., MAYLE, F.E., PUNYASENA, S.W., FITZPATRICK, K.A., BURN, M.J., GUILLEN, R., CHAVEZ, E., MANN, D., PENNINGTON, R.T. & METCALFE, S.E.2011. A 45 kyr palaeoclimate record from the lowland interior of tropical South America. Palaeogeogr. Palaeocl. 307:177-192, doi: 10.1016/j.palaeo.2011.05.012
    » 10.1016/j.palaeo.2011.05.012
  • WÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005a. Tracing an invasion: landbridges, refugia and the phylogeography of the Neotropical rattlesnake (Serpentes: Viperidae: Crotalus durissus). Mol. Ecol. 14:1095-1108, doi: 10.1111/j.1365-294X.2005.02471.x
    » 10.1111/j.1365-294X.2005.02471.x
  • WÜSTER, W., FERGUSON, J.E., QUIJADA-MASCAREÑAS, J.A., POOK, C.E., DA GRAÇA SALOMÃO, M. & THORPE, R.S. 2005b. No rattlesnakes in the rainforests: reply to Gosling and Bush. Mol. Ecol. 14:3619-3621, doi: 10.1111/mec.2005.14.issue-11
    » 10.1111/mec.2005.14.issue-11
  • ZECH, R., MAY, J.H., KULL, C., ILGNER, J., KUBIK, P.W. & VEIT, H. 2008. Timing of the late Quaternary glaciation in the Andes from ∼15 to 40° S. J. Quaternary Sci. 23:635-647, doi: 10.1002/jqs.v23:6/7
    » 10.1002/jqs.v23:6/7

Publication Dates

  • Publication in this collection
    June 2015

History

  • Received
    7 Dec 2013
  • Reviewed
    5 Feb 2015
  • Accepted
    31 Mar 2015
Instituto Virtual da Biodiversidade | BIOTA - FAPESP Departamento de Biologia Vegetal - Instituto de Biologia, UNICAMP CP 6109, 13083-970 - Campinas/SP, Tel.: (+55 19) 3521-6166, Fax: (+55 19) 3521-6168 - Campinas - SP - Brazil
E-mail: contato@biotaneotropica.org.br