UNIVERSIDADE FEDERAL DE GOIÁS INSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS GRADUAÇÃO EM ECOLOGIA E EVOLUÇÃO
Cleber Ten Caten
Padrões de variação de tamanho corporal e de distribuição geográfica são métodos-dependente em serpentes viperídeas
do Novo Mundo
Orientadora: Levi Carina Terribile
Co-orientador: Matheus de Souza Lima-Ribeiro
Goiânia Março de 2018
ii UNIVERSIDADE FEDERAL DE GOIÁS
INSTITUTO DE CIÊNCIAS BIOLÓGICAS
PROGRAMA DE PÓS GRADUAÇÃO EM ECOLOGIA E EVOLUÇÃO
Cleber Ten Caten
Padrões de variação de tamanho corporal e de distribuição geográfica são métodos-dependente em serpentes viperídeas do
Novo Mundo
Orientadora: Levi Carina Terribile
Co-orientador: Matheus de Souza Lima-Ribeiro
Dissertação apresentada ao Programa de Pós-graduação em Ecologia e Evolução, do Instituto de Ciências Biológicas da Universidade Federal de Goiás, como parte dos requisitos para a obtenção do título de Mestre.
Goiânia, Março de 2018
ii
iii
iv Agradecimentos
À Universidade Federal de Goiás e ao CNPq pela disponibilidade de um local e auxílio financeiro que tornou possível que eu pudesse desenvolver essa dissertação de mestrado.
Aos orientadores e amigos, Levi Carina e Matheus, que desde a época da graduação me acolheram como orientado e que desde então tem me auxiliado durante essa jornada acadêmica.
Pela paciência, pelos ensinamentos compartilhados e pelas diversas conversas, tanto acadêmicas quanto relacionadas ao cotidiano, que foram essenciais durante esse processo.
Aos meus pais, Protásio e Maria Helena, que sempre me incentivaram e apoiaram durante essa caminhada e ao meu irmão, Helder, que me ajudou diversas vezes nesse período aqui em Goiânia, principalmente arrumando meu notebook sempre que ele dava “pau”.
Aos diversos amigos de Mineiros e Jataí, especialmente ao Táric, Bruno, Igor, Tracy, Bruninho, Jean, James, Álvaro, Juninho e Emerson, que tornaram os períodos de descanso ainda mais prazerosos.
Ao pessoal do LETS, principalmente ao Danilo, Lucas Jardim, Leila, Elisa, Alice, Marco Túlio, Luciano, Lorena, Hauanny e Júlio, tanto pela ajuda em questões práticas quanto pelas conversas jogadas fora durante os cafés.
Por fim, ao Lucas Martins, Karlo, Anderson, Paola e Daniel, membros da Equipe Chorume, que tornaram essa jornada muito mais animada e agradável, seja pelas ajudas com as análises, ou principalmente, tomando uma de “leve” no Gurupi e contando uma “história engraçada da sua vida”. Valeu de mais galera!
v RESUMO
Tradicionalmente, ecólogos e biogeógrafos tem demonstrado grande interesse por padrões ecogeográficos, especialmente durante as ultimas décadas. As regras de Bergmann e de Rapoport são dois dos padrões ecogeográficos mais debatidos, os quais propõe um aumento no tamanho corporal e na área de distribuição geográfica das espécies, respectivamente, com aumento na latitude. No entanto, ainda é incerto se repteis seguiriam essas regras. Além disso, ainda há duvida se o método utilizado para obter a área de distribuição geográfica das espécies pode afetar nossa percepção de tais padrões. No presente trabalho, testamos diferentes hipóteses em relação as regras de Bergmann e Rapoport usando os viperídeos do Novo Mundo (Viperidae: Crotalinae) como modelo biológico, além de analisarmos a robustez de diferentes métodos de obter a distribuição geográfica das espécies e avaliamos os dois padrões ecogeográficos usando diferentes abordagens. Nós reunimos dados de ocorrência para as 136 espécies de Crotalineos e geramos suas distribuições geográficas construindo polígonos utilizando o método Alpha Hull e através de modelos de nicho ecológico. Nós avaliamos ambas as regras utilizando uma abordagem interespecífica e uma de assembleia. A primeira considera cada espécie como um dado independente enquanto a segunda considera cada assembleia (i.e. célula de grid) como um dado independente. Nós utilizamos Quadrados mínimos generalizados filogenéticos (PGLS) e Quadrados mínimos generalizados (GLS) para avaliar os padrões interespecíficos e de assembleias, respectivamente. O primeiro considera a independência filogenética do dado enquanto o segundo a autocorrelação espacial e ambos fornecem coeficientes e níveis de significância não enviesados. Nossos resultados demonstram que a regra de Bergmann não ocorre a nível interespecífico, ao passo que é estatisticamente significativa em nível de assembleia e independente de como foi obtido a distribuição geográfica das espécies. Nós
vi encontramos suporte para regra de Rapoport a nível interespecífico independente de como geramos a distribuição geográfica das espécies. Por outro lado, a analise de assembleia não foi robusta metodologicamente, revelando diferentes padrões ecogeográficos dependendo do método usado para gerar a distribuição geográfica das espécies. Nossos resultados demonstram inconsistência entre os padrões observados nas análises interespecíficas e de assembleia.
Finalmente, nossos resultados ressaltam que essa sensibilidade é especialmente evidente na análise de assembleia da regra de Rapoport e que ao avaliar esse padrão em nível de assembleia o método que será usado para obter a distribuição geográfica das espécies deveria ser escolhido cuidadosamente.
Palavras-Chave: Regra de Bergmann, Regra de Rapoport, Viperideos do Novo Mundo, Crotalinae, Distribuição geográfica.
ABSTRACT
Traditionally, ecologists and biogeographers have been interested in ecogeographical patterns with increasing demand over the last years. Bergmann´s and Rapoport´s rules are two of the most debated ecogeographical patterns, which propose increasing in species body size and range size, respectively, with latitudes. However, whether such rules widely apply to reptiles remains unclear. Moreover, there might be uncertainty regarding the method used to obtain species geographical range that might change our perception of such patterns. Here we tested different hypotheses regarding Bergmann‟s and Rapoport‟s rules using the New World Pit vipers (Viperidae: Crotalinae) as biological model, as well as analyzed the robustness of different methods to obtain species geographical range and evaluated both ecogeographical patterns using
vii different approaches. We gathered occurrence data for the 136 Crotalinae species and generated geographical ranges by building polygons from Alpha Hull method and Ecological Niche Modelling. We assessed both rules using a „cross-species‟ and an „assemblage‟ approach. The former considers each species as an independent data, whereas the latter consider each assemblage (i.e. a grid cell) to be an independent data. We used Phylogenetic Least Squares (PGLS) and Generalized Least Squares (GLS) to evaluate the cross-species and the assemblage pattern, respectively. The former considers the phylogenetic independence of the data as the latter the geographic autocorrelation and both provide unbiased coefficients and significance levels. Our results show that Bergmann‟s rule did not occur in the cross-species level, whereas it was statistically significant in the assemblage level regardless of the method used to obtain range size. We found support for Rapoport‟s rule in the cross-species level regardless of the method used to generate range size. Meanwhile, the assemblage analysis was not robust methodologically, revealing different ecogeographical patterns depending on the method used to generate species geographical range. Our findings point that there are inconsistences between the patterns observed in the cross-species and the assemblage analysis, which could indicate that different processes producing these patterns in the cross-species and assemblage levels. Finally, our results highlight that this sensibility is especially evident in Rapoport‟s rule assemblage analysis and that when evaluating this pattern in assemblage level the method that will be used to obtain species geographical range should be carefully chosen.
KeyWords: Bergmann‟s rule, Rapoport‟s rule, New World Pit vipers, Crotalinae, Geographic range.
viii SUMÁRIO
INTRODUÇÃO GERAL... 1
REFERÊNCIAS ... 4
INTRODUCTION ... 7
METHODS ... 10
Data ... 10
Building range maps ... 13
Statistical analysis ... 14
RESULTS ... 16
Testing Bergmann’s rule ... 16
Testing Rapoport’s rule ... 17
Phylogenetic uncertainty ... 18
DISCUSSION ... 19
CONCLUSION ... 25
CONCLUSÃO GERAL ... 25
REFERENCES ... 26
MATERIAL SUPLEMENTAR ... 39
1 INTRODUÇÃO GERAL
Durante os últimos séculos, um dos grandes objetivos dos biogeógrafos e ecólogos tem sido a tentativa de compreender padrões macroecologicos que descrevessem generalizações entre características biológicas e ecológicas das espécies e o ambiente em que elas se encontram.
Dentre essas generalizações, que são conhecidas como regras ecogeográficas, estão as regras da ilha (animais que são grandes em continente ficariam menores em ilhas e vice-versa), de Jordan (espécies de peixe desenvolvem mais vertebras em ambientes frios do que em ambientes
quentes) e de Rensh (populações de mamíferos e pássaros geram proles maiores em locais mais frios) (Gaston et al. 2008). Dois desses padrões mais bem estudados são as regras de Bergmann e de Rapoport. A regra de Bergmann afirma que espécies que ocorrem em locais mais frios teriam um tamanho corporal maior do que aquelas que ocorrem em locais mais quentes (James 1970), enquanto que a regra de Rapoport diz que quanto mais distante uma espécie se encontra da linha do equador, maior tenderá a ser a sua área de ocorrência (Stevens 1989). De forma geral, a regra de Bergmann tem sido demonstrada principalmente para mamíferos e aves (Meiri & Dayan 2003) com suporte controverso para o padrão em animais ectotérmicos (Ashon & Feldman 2003, Pincheira-Donoso & Meiri 2013). Enquanto isso, a regra de Rapoport tem sido descrita
principalmente para o hemisfério norte (e.g. Whitton et al. 2012, Ruggiero & Werekraunt 2007), o que tem gerado questionamentos quanto a generalização desse padrão e tem sido sugerido que seja descrito como um fenômeno regional ao invés de global (Gaston et al. 1998).
Recentemente, tem sido muito debatido sobre qual a forma correta de avaliar esses padrões, principalmente em relação à regra de Bergmann (Blackburn et al. 1999), com falta de consenso quanto a qual abordagem correta em descrever tal padrão (Blackburn et al. 1999, Meiri 2011). Dentre os tipos de abordagens utilizados para avaliar esses padrões se encontram a
2 abordagem intraespecífica (em que se avalia um determinado padrão dentro de populações de uma única espécie, o indivíduo é a unidade de análise), a interespecífica (em que o padrão é avaliado entre um grupo próximo de espécies, a espécie é a unidade de análise) e a de assembleia (em que o padrão é avaliado considerando as espécies que são preditas para ocorrer em
diferentes assembleias, a assembleia é a unidade de análise) (Gaston et al. 2008). Cada tipo de abordagem captura um tipo de variação que corresponde a fenômenos diferentes. Por exemplo, variação de tamanho corporal a nível intraespecífico pode surgir como meio de os indivíduos de uma espécie sobreviver em locais com menos recursos, enquanto uma variação interespecífica poderia surgir quando grande parte dos recursos disponíveis para as espécies é diferente em regiões com climas diferentes (Blackburn et al. 1999). Além disso, os padrões interespecíficos capturam como ocorre a variação do tamanho corporal das espécies ao longo dos ambientes que elas se encontram, enquanto a análise de assembleia avalia como o tamanho corporal das
espécies preditas em uma assembleia varia ao longo dos ambientes (Chown & Gaston 2010).
Assim, parte das controvérsias quanto à ocorrência desses padrões pode ser devido ao fato de que diferentes estudos podem ter usados diferentes abordagens para avaliar tais padrões, e
consequentemente estarem avaliando níveis diferentes de variação de determinado padrão.
Além disso, uma das principais variáveis utilizadas para avaliar as regras ecogeográficas é a área de distribuição geográfica das espécies. É a partir dela que se obtêm os dados climáticos associados a cada espécie para se utilizar na análise interespecífica e ela é essencial na análise de assembleia, pois é a partir dela que se delimita em quais assembleias uma espécie se encontrará.
A área de distribuição geográfica de uma espécie pode ser obtida por diversos métodos (Boitani
& Fuller 2000), sendo que o mais apropriado depende dos objetivos específicos de cada trabalho (Fortin et al. 2005). Recentemente tem sido demonstrado que os mapas usados em grande parte
3 das análises macroecológicas (i.e. obtidos através de métodos de polígonos e opinião de experts) não são ideais para esse tipo de análise (Herkt et al. 2017). Desse modo, além de diferentes abordagens poderem levar a conclusões diferentes em relação à ocorrência de um padrão em um grupo de espécies, os diferentes métodos utilizados para obter a área distribuição geográfica das espécies pode potencialmente contribuir ainda mais para o fornecimento de falta de robustez quanto à ocorrência dos padrões ecogeográficos em determinados grupos de organismos.
As serpentes viperídeas do Novo Mundo compreendem um grupo monofilético de 136 espécies que ocorrem da Argentina até a região norte dos Estados Unidos, e que possuem uma grande variação quanto ao seu tamanho corporal e tamanho de área de distribuição (Campbell &
Lamar 2004). Isso torna esse grupo um modelo ideal para a avaliação de regras ecogeográficas.
Durante a ultima década, trabalhos sugerindo conformação às regras de Bergmann e Rapoport em serpentes do Novo Mundo (e.g. Ollala-Tarraga et al. 2006, Böhm et al. 2017) assim como trabalhos não suportando a ocorrência de tais padrões (e.g. Reed 2003) tem enfatizado a falta de robustez quanto a descrição de tais padrões nesse grupo de organismos. Isso demonstra a
necessidade de trabalhos que avaliem como diferentes abordagens usadas para avaliar os padrões e como diferentes métodos de obter a área de ocorrência das espécies podem potencialmente levar a diferentes conclusões quanto à ocorrência das regras ecogeográficas nos grupos estudados.
Assim, no presente trabalho, avaliamos como o uso de duas abordagens (i.e.
interespecífica e de assembleia) e o uso de diferentes métodos para obter a área de distribuição das espécies (Métodos de Polígonos e Modelos de Nicho Ecológico) podem levar a diferentes conclusões quanto à ocorrência das regras de Bergmann e Rapoport nas serpentes viperídeas do Novo Mundo. Para a regra de Bergmann, especificamente, nós avaliamos a hipótese de
4 conservação de calor, em que as espécies teriam tamanho corporal maior em locais mais frios como um mecanismo de diminuir a perda de calor para o ambiente (James 1970); a hipótese de produtividade primária, em que animais atingiriam um tamanho corporal maior em zonas mais produtivas devido ao maior suprimento de alimento (Rosenzweig 1968) e a hipótese de
resistência à inanição, que afirma que em locais com mais sazonalidade climática os animais seriam maiores (Lindstedt & Boyce 1985). Em relação à regra de Rapoport, nós avaliamos a hipótese de variabilidade climática, que prediz que espécies teriam uma distribuição geográfica maior em locais com clima mais variável (Stevens 1989) e a hipótese dos extremos climáticos, que afirma que a área de distribuição das espécies é delimitada pelos extremos climáticos que elas enfrentam (Pither 2003). Nós avaliamos essa hipótese considerando tanto a temperatura mínima como a temperatura máxima enfrentada pelas espécies.
REFERÊNCIAS
Ashton, K.G. & Feldman, C.R. (2003) BERGMANN‟s RULE IN NONAVIAN REPTILES:
TURTLES FOLLOW IT, LIZARDS AND SNAKES REVERSE IT. Evolution, 57, 1151–
1163.
Blackburn, T.M., Gaston, K.J., & Loder, N. (1999) Geographic gradients in body size: a clarification of Bergmann‟s rule. Diversity and Distributions, 5, 165–174.
Boitani, L. & Fuller, T.K. (2000) Research Techniques in Animal Ecology Methods and Cases in Conservation Science. Columbia University Press, New York.
Böhm, M., Kemp, R., Williams, R., Davidson, A.D., Garcia, A., McMillan, K.M., Bramhall, H.R., & Collen, B. (2017) Rapoport‟s rule and determinants of species range size in snakes.
Diversity and Distributions, 23, 1472–1481.
5 Campbell, J.A. & Lamar, W.W. (2004) The venomous reptiles of the Western Hemisphere.
Cornell University Press, New York.
Chown, S.L. & Gaston, K.J. (2010) Body size variation in insects: A macroecological perspective. Biological Reviews, 85, 139–169.
Fortin, M.-J., Keitt, T.H., Maurer, B.A., Taper, M.L., Kaufman, D.M., & Blackburn, T.M. (2005) Species‟ geographic ranges and distributional limits: pattern analysis and statistical issues.
Oikos, 108, 7–17.
Gaston, K.J., Blackburn, T.M., & Spicer, J.I. (1998) Rapoport‟s rule : time for an epitaph ? Trends in Ecology and Evolution, 13, 70–74.
Gaston, K.J., Chown, S.L., & Evans, K.L. (2008) Ecogeographical rules: Elements of a synthesis. Journal of Biogeography, 35, 483–500.
Herkt, K.M.B., Skidmore, A.K., & Fahr, J. (2017) Macroecological conclusions based on IUCN expert maps: A call for caution. Global Ecology and Biogeography, 26, 930–941.
James, F.C. (1970) Geographic Size Variation in Birds and Its Relationship to Climate. Ecology, 51, 365–390.
Lindstedt, S.L. & Boyce, M.S. (1985) Seasonality, Fasting Endurance, and Body Size in Mammals. The American Naturalist, 125, 873–878.
Meiri, S. (2011) Bergmann‟s Rule - what‟s in a name? Global Ecology and Biogeography, 20, 203–207.
Meiri, S. & Dayan, T. (2003) On the validity of Bergmann‟ s rule. Journal of Biogeography, 30,
6 331–351.
Olalla-Tárraga, M.Á., Rodríguez, M.Á., & Hawkins, B.A. (2006) Broad-scale patterns of body size in squamate reptiles of Europe and North America. Journal of Biogeography, 33, 781–
793.
Pincheira-Donoso, D. & Meiri, S. (2013) An Intercontinental Analysis of Climate-Driven Body Size Clines in Reptiles: No Support for Patterns, No Signals of Processes. Evolutionary Biology, 40, 562–578.
Pither, J. (2003) Climate tolerance and interspecific variation in geographic range size.
Proceedings of the Royal Society B: Biological Sciences, 270, 475–481.
Reed, R.N. (2003) Interspecific patterns of species richness, geographic range size, and body size among New World venomous snakes. Ecography, 26, 107–117.
Rosenzweig, M.L. (1968) The Strategy of Body Size in Mammalian Carnivores. American Midland Naturalist, 80, 299–315.
Ruggiero, A. & Werenkraut, V. (2007) One-dimensional analyses of Rapoport‟s rule reviewed through meta-analysis. Global Ecology and Biogeography, 16, 401–414.
Stevens, G.C. (1989) The Latitudinal Gradient in Geographical Range: How so Many Species Coexist in the Tropics. The American Naturalist, 133, 240–256.
Whitton, F.J.S., Purvis, A., Orme, C.D.L., & Olalla-Tárraga, M.Á. (2012) Understanding global patterns in amphibian geographic range size: does Rapoport rule? Global Ecology and Biogeography, 21, 179–190.
7 INTRODUCTION
Over the last two hundred years several generalizations known as „ecogeographical rules‟
have been proposed in macroecology and biogeography. These rules usually summarize biological patterns occurring on space at different levels of organization (i.e. intraspecific, interspecific and assemblage) (Gaston et al., 2008). Bergmann´s and Rapoport´s rules are two ecogeographical patterns that have been widely studied over a broad range of organisms (Gaston et al., 1998; Blackburn et al., 1999; Ruggiero & Werenkraut, 2007; Meiri, 2011). Briefly, Bergmann´s rule states that animals occurring in cold areas would have a larger body size than those inhabiting warmer areas (James, 1970). Likewise, Rapoport´s rule states that the geographic range size of species would increase with latitude (Stevens, 1989). Mammals and birds apparently follow Bergmann´s rule (e.g. Meiri & Dayan, 2003; Olson et al., 2009; Clauss et al., 2013; Torres-Romero et al., 2016), but its application to reptiles remains controversial. Some studies found no relationship between body size and environmental variables (e.g. Pincheira- Donoso & Meiri, 2013; Feldman & Meiri, 2014; Angielczyk et al., 2015) whereas others found contrasting results, even with a converse pattern (e.g. Ashton & Feldman, 2003; Olalla-Tárraga et al., 2006; Terribile et al., 2009; Muñoz et al., 2014). Contrasting results have also been found for Rapoport´s rule, with the pattern being mainly described across the northern hemisphere (Ruggiero & Werenkraut, 2007; Whitton et al., 2012).
Interestingly, a possible cause for these contrasting results in ecogeographical patterns might be the specific approach used to assess them. For instance, when evaluating Bergmann‟s rule in amphibians, Adams & Church (2008) found no support for the occurrence of the pattern using an interspecific approach, whereas Olalla-Tárraga et al.(2010) found evidence for the occurrence of such pattern when carrying an assemblage analysis. This suggests that, at least to
8 some extent, these contrasting results might be arising simply because we are comparing results obtained from different approaches used to assess these ecogeographical patterns, when in fact they are actually evaluating different kinds of variation (Chown & Gaston, 2010). In addition, a key variable used to assess these patterns is the species geographic range size. Range size is often obtained by accumulating the locations where a species could occur and it is delimited by diverse factors such as biotic and abiotic conditions, as well as dispersal and evolutionary dynamics (Gaston, 1991; Brown et al., 1996). Moreover, several methods can be employed to determine species geographic range depending on the available data and the questions being asked (Fortin et al., 2005). Therefore, the use of different techniques to obtain species range size might also affect ecogeographical analysis (Graham & Hijmans, 2006; Herkt et al., 2017). For example, the polygon maps provided by International Union for the Conservation of Nature (IUCN) are not appropriated to test macroecological questions because they were built for conservation purposes and other methods for generating species geographic range, such as ecological niche modeling, should be preferred (Herkt et al., 2017) to avoid biased results in macroecological analyses.
Here we explored whether and how the use of distinct approaches and methods for generating species geographic range would lead us to different interpretations as for Bergmann´s and Rapoport´s rules in New World Pit vipers (Viperidae: Crotalinae). The Crotalinae‟s clade comprises about 230 species in both Old and New World (Campbell & Lamar, 2004; Uetz et al., 2016), and distinguishes from other snakes due to the occurrence of “loreal pits”, a heat-sensing structure usually associated with the radiation of the clade through space (Rosenzweig et al., 1987; Alencar et al., 2016). The New World Pit vipers are a monophyletic clade comprising about 136 species (Alencar et al., 2016) that shows a striking variation regarding body size and
9 geographic range size, making it an ideal biological model to evaluate robustness in detecting ecogeographical rules.
We used two approaches („cross-species‟ and „assemblage‟) to assess these ecogeographical patterns, and species geographic range size estimated from two methods (polygon Alpha Hull and Ecological Niche Modelling). Regarding Bergmann‟s rule, we specifically addressed: i) if species body size purely responds to the latitudinal gradient of temperature variation, once larger body sizes would dissipate less body heat in cold areas (heat conservation hypothesis – HCH), and ii) distinguishing possible effects arising from other factors such as primary productive and environmental seasonality. Primary productive is thought to regulate body size once places with larger food supply would support larger animals (Primary productive hypothesis – PPH) (Rosenzweig, 1968a; McNab, 2010). Furthermore, we also assessed the starvation endurance hypothesis (SEH), which states that variation regarding body size is better predicted by environmental seasonality (Lindstedt & Boyce, 1985; Millar &
Hickling, 1992). This hypothesis was first suggested for mammals and it could also occur in ectotherm animals due to the linking between growth season length and physiological time available for development (Mousseau, 1997). Regarding Rapoport´s rule, we tested the: i) climatic variability hypothesis (CVH), which states that species inhabiting more variable environments developed a higher physiological tolerance to the environment, enabling them to occur in a larger range of environments and consequently having a larger geographic range size (Stevens, 1989) and ii) the climatic extremes hypothesis (CEH), which predicts that the climatic extremes a species experience may explain its range size (Pither, 2003). Because extreme temperatures directly affect reptiles‟ locomotion (Spellerberg, 1972), we expect that CEH may also be useful to explain the Rapoport‟s rule in New World Pit vipers.
10 METHODS
Data
Occurrence data for the 136 Viperidae species that inhabit the New World were thoroughly gathered from online repositories such as GBIF (https://www.gbif.org/), VertNet (http://vertnet.org/), SpeciesLink (http://splink.cria.org.br/) and scientific literature (e.g. scientific articles, books and published theses). We eliminated duplicate records and those that were located in regions that were clearly inaccessible to the species (e.g. records that fell into the sea or on other continents where the species is not distributed naturally). We call the occurrences that resulted from this first cleaning: 'original database'. Also, we used the “spThin” R package (Aiello-Lammens et al., 2015) to reduce spatial autocorrelation and model overfitting. We used a nearest-neighbor distance of 20 km based on the clustering nature and density of occurrences; we would have lost many data for some species if we had used a greater distance. We called 'filtered database' to the occurrences that were obtained from the 'spThin' analysis. We also excluded 9 island endemic species due to the fact that different processes might be acting on body and range size evolution of those species (Boback & Guyer, 2003; Meik et al., 2010). We used the log- transformed maximum snout-vent length (SVL) (in mm) as a measure of body size, which is a commonly used and available index for snakes. In addition this measure provides similar results as when using mean or minimum SVL (Ashton, 2001). Body size estimates were mainly gathered from Campbell & Lamar (2004) and, occasionally, updated from complementary herpetological literature. Even though Rapoport´s rule was first proposed to be assessed in terms of latitudinal extent (Stevens, 1989), here we used the log-transformed occurrence area as a response variable, which has been recently chosen over the classical approach (e.g. Hawkins &
Felizola Diniz-filho, 2006; Whitton et al., 2012), although both range estimates provide similar results (Ruggiero & Werenkraut, 2007).
11 Despite a great number of phylogenetic hypothesis proposed for the New World Pit vipers (e.g. Fenwick et al., 2009; Carrasco et al., 2012; Pyron et al., 2013) we used the most complete molecular phylogeny proposed by Alencar et al. (2016) for New World Pit vipers to date, with >80% of species and which is in agreement with previously proposed phylogenies.
Next, we used the phylogenetically uncertain taxon (PUT) procedure proposed by Rangel et al.
(2015) to complete the Alencar et al.`s (2016) phylogeny. We first gathered our phylogenetically uncertain taxon (PUT), which in our case are the lacking species in the phylogenetic tree, and then added the PUTs in the most derived consensus clade (MDCC), which is the most basal node from which contains the living relatives of our PUTs (for a more detailed explanation on PUT and MDCC, see Rangel et al.(2015). Because the PUTs can be added at any level into the MDCC, we explored uncertainties by randomly obtaining 1000 complete phylogenies. We defined the MDCCs based on taxonomy, specifically in the node at which the genera belonging to the PUT was originated. To generate the 1000 trees, we used the software SUNPLIN (Martins et al., 2013, http://wsmartins.net/sunplin/).
Environmental data were gathered with 1º x 1º resolution of both latitude and longitude covering the entire New World. Regarding Bergmann´s rule, we used the mean annual temperature to test the HCH. Despite potential evapotranspiration (PET) being commonly used to assess this hypothesis, it is highly correlated with mean annual temperature in the western hemisphere (Rodríguez et al., 2008), making it inappropriate for the analysis. We then used annual evapotranspiration (AET) to test the hypothesis of primary production. AET measures water and energy balance which leads plants growth, and due to its correlation with plants production it has been used as a measure of primary productivity (Rosenzweig, 1968b; Hawkins et al., 2003). To test the SHE we used a variable of seasonality. Regarding Rapoport´s rule, we
12 used the annual temperature range associated with the specific species range to test the CVH. To test CEH we used values of maximum and minimum temperature associated with the species range. Temperature data were obtained from ecoClimate database (http://ecoclimate.org/, Lima- Ribeiro et al., 2015) at a resolution of 0.5º and then re-escalated to 1 º using aggregate function from raster package (Hijmans, 2017). We obtained AET from United Nations Environment Programme (2014, available at http://www.unep.org/). To calculate seasonality we first obtained the Gaussian xerothermic index by following Olalla-Tárraga et al. (2006) in which for each month of the year we calculated when two times the mean monthly temperature was bigger than the mean monthly precipitation to account for seasonality due to limitation in precipitation. For seasonality regarding low temperatures limiting plant growth we first realized a split-line regression between mean temperature and NDVI to find a threshold below which plant growth would not occur. Then we calculated for each month when mean monthly temperature lower than our threshold. Thus, we obtained our Gaussian xerothermic index for each grid cell by summing how many months plant growth was limited either by precipitation or by lower temperatures. NDVI data was obtained from (Sietse et al., 2010, https://daac.ornl.gov/cgi- bin/dsviewer.pl?ds_id=972).
We collected environmental predictors (spatial resolution of 10') used for ecological niche modelling from the CliMond database (Kriticos et al., 2012; https://www.climond.org/).
We decided to use this set of variables instead of those of WorldClim (Hijmans et al., 2005) sacrificing resolution for a greater number of niche dimensions. CliMond has the same 19 variables derived from precipitation and temperature that can be downloaded from WorldClim plus 16 derived from humidity and radiation. The latter is particularly important for reptiles because of their physiology (Dubois et al., 2009; Norris & Kunz, 2012). We performed a
13 principal component analysis (PCA) to reduce multicollinearity and dimensions in the
environmental predictors. To do so, we employed the PCARaster function of the ENMGadgets package in R (Barve & Barve, 2013). Then, we retained only the first eight components that accounted for more than 95% of the overall variance.
Building range maps
Range maps for the New World Pit vipers were constructed using two distinct approaches: i) from polygons, using the Alpha Hull Method, and ii) from Ecological Niche Modelling (ENM).
The use of different methods to generate species range has been widely debated over the past decade (Graham & Hijmans, 2006) mainly due to the fact that different frameworks used to generate the species range may lead to different results regarding the extent of the species occurrence area (Burgman et al., 2005). Here we generated polygons distribution maps using Alpha Hull approach. To do so, we used the rangeBuilder (Rabosky et al., 2016) package in R.
We chose to construct the polygons through Alpha Hull Method instead of Minimum Convex Polygon (MCP) because it is not sensitive to irregular distribution of occurrence points, which usually has an effect of overestimating the geographic area when using other methods such as MCP (Burgman & Fox, 2003), and may consequently be less likely to jeopardize the results of the analysis that will be carried. Even though when building polygons it is usually considered a fraction of 95% of occurrence data in order to avoid the use of occurrence points originated from
“non-normal activities pattern” from organisms, such as exploratory behavior, here we decided to use 100% of occurrence data to build ours polygons, because we also used 100% of the data to build our ENM.
To generate range maps through ecological niche modeling we used the MaxEnt algorithm (Phillips et al., 2006) implemented in the ENMeval package (Muscarella et al., 2014)
14 in R (R Development Core Team). Specifically we applied the ENMevaluate function to „tune‟
our models and thus find an optimal combination between occurrence datasets, feature combinations and regularization multipliers that had the best balance between complexity and overfitting. Thus, for each species we obtained 96 models (2 occurrence datasets * 6 feature combinations * 8 regularization multipliers) that were ranked according to their performance.
We based the evaluation of the performance of each combination of settings on the AICc which was calculated with a set of independent occurrences obtained via the checkerboard cross- validation method (Muscarella et al., 2014). We retained for each species only the model with the lowest AICc. Then we thresholded this model based on the 10th percentile training presence criterion (to avoid including in the prediction records of sink populations and taxonomic or georreferencing errors) to obtain the potential distribution models.
Statistical analysis
We evaluated Bergmann´s and Rapoport´s rules using two distinct interspecific approaches, one denominated „cross-species‟ and the other „assemblage‟ (Ruggiero & Werenkraut, 2007; Gaston et al., 2008). In the cross-species approach, each species is treated as an independent data, being the response variable the maximum body size attained by the species and its range size to Bergmann´s and Rapoport´s rules, respectively. We obtained species climatic data from their geographic range latitudinal midpoint (Rohde et al., 1993). Regarding the assemblage approach, we also used a unique measure of body size and range size for the species, however, here the unit of analysis is the grid cells; we estimated the median body size and range size of all species predicted to occur inside a given grid cell (Meiri & Thomas, 2007). Thus, each grid cell is considered to be an independent data, for which we obtained the climatic values associated with each hypothesis.
15 Since species are not phylogenetically independent (Felsenstein, 1985), nor the grid cells are spatially independent, it is necessary to use methods that consider their dependence when running statistical analysis to decrease the chance for committing a type I error. Thus, to consider the effects of the phylogenetic relationships on our response variable of body size and range size, we carried a Phylogenetic Least Squares (PGLS) regression, which deals with the co-variation between the species and provides appropriate regression coefficients and significance levels (Freckleton et al., 2002). The amount of phylogenetic dependence in our data was obtained using maximum-likelihood of the lamba parameter (Pagel, 1999) through the use of the package
„caper‟ in R software (Orme et al., 2013). To account for the spatial autocorrelation, we used a Generalized Least Square (GLS) regression. This was accomplished by adding five different spatial correlation structures using gls function from nlme package (Pinheiro et al., 2018) in the software R (R Core Team, 2017). The best model was then chosen through the use of AIC. To ensure that we really accounted for the spatial autocorrelation, we generated Moran´s I correlogram (Diniz-Filho et al., 2003) for each one of the hypothesis we tested for Bergmann´s and Rapoport´s rule.
To assess the robustness of the rule regarding the method used to generate species occurrence area we contrasted how the coefficients and significance levels varied between the models when analyzing the same hypothesis using the two different methods of obtaining occurrence area. Thus, we were able to tell whether the use of different methods may lead to different conclusions regarding our perception of ecogeographical rules. In addition to that, we also run a PGLS on the 1000 random phylogenies generated in order to evaluate whether the use of different phylogenetic hypothesis in the cross-species approach might lead to uncertainty regarding the interpretation of these rules. We used the method proposed by Nakagawa & de
16 Villemereuil (2015) to evaluate phylogenetic uncertainty. This method uses the Rubin‟s rule to evaluate how regression coefficients (i.e. slopes in our case) vary among different phylogenies.
First, we obtained the total variation in our slopes, that is the variation associated with the standard error of our regressions (i.e., from each one of the 1000 phylogenies) plus the variation associated with the use of different phylogenies. Then we divided the variation associated with the phylogenies by the total variation of the coefficients. This value is the amount of variation in our coefficients arising due to the use of different phylogenies to run the analyses and is the phylogenetic uncertainty value we used to address how different phylogenies could affect our final results.
RESULTS
Testing Bergmann’s rule
Regardless of the method (i.e. Polygons or ENMs) used to obtain species geographical range when evaluating the occurrence of Bergmann´s rule in the New World Pit vipers, we found no support for the HCH, PPH and the SEH considering the cross-species approach. Contrasting, both the HCH and the primary productivity hypotheses were supported in the assemblage approach regardless of the method whereas the SHE was supported when using Polygons but not when using ENMs (Table 1).
17 Table 1 Coefficient values for Bergmann‟s rule considering the occurrence area from polygons for both cross-species and assemblage analysis
Method Approach Hypothesis Slope t-value p-value DFs
Polygons
Cross-species
HCH 0.00392 0.4478 >0.65 134 PPH 0.00076 1.2851 >0.20 134 SHE -0.00841 -0.6491 >0.51 134 Assemblage
HCH 0.01145 3.3271 <0.01** 2597 PPH 0.00045 4.2568 <0.01** 2597 SHE 0.00509 2.2820 <0.05* 2410
ENMs
Cross-species
HCH -0.00249 -0.3152 >0.75 134 PPH 0.00058 0.9630 >0.33 134 SHE -0.02351 -1.6299 >0.10 134 Assemblage
HCH 0.00460 2.6810 <0.01** 2761 PPH 0.00020 4.2359 <0.01** 2761 SHE 0.00107 0.8102 >0.41 2546
Testing Rapoport’s rule
We found support for Rapoport´s rule regarding the CVH and the CEH considering both maximum and minimum temperature at the cross-species regardless of the method used to obtain species geographical range. In the assemblage level we found mixed support for Rapoport‟s rule, with support to the CVH and to the CEH when considering minimum temperature, but the maximum temperature was not supported as an extreme climatic predictor (CEH) of Pit Vipers range sizes estimated by polygons (Table 2). We also found mixed support by using ENMs to obtain species ranges, contradicting most of the results from polygons. The CVH and CEH considering maximum temperature were not supported whereas CEH considering minimum temperature was supported (Table 2).
18 Table 2 Coefficient values for Rapoport‟s rule considering the occurrence area from polygons for both cross-species and assemblage analysis.
Method Approach Hypothesis Slope t-value p-value DFs
Polygons
Cross-species
CVH 0.14000 6.3290 <0.01** 134 CEH (Tmin) -0.08908 -3.4188 <0.01** 134 CEH (Tmax) 0.16822 4.3648 <0.01** 134 Assemblage
CVH -0.02723 -4.0038 <0.01** 2597 CEH (Tmin) 0.03364 4.5651 <0.01** 2597 CEH (Tmax) 0.00275 0.3494 >0.72 2597 ENMs
Cross-species
CVH 0.16119 5.6513 <0.01** 134 CEH (Tmin) -0.09942 -2.9870 <0.01** 134 CEH (Tmax) 0.19616 4.1705 <0.01** 134 Assemblage
CVH 0.00396 1.4210 >0.15 2761 CEH (Tmin) -0.00710 -2.4491 <0.05* 2761 CEH (Tmax) -0.00342 -1.0506 >0.29 2761
Phylogenetic uncertainty
Table 3 Mean coefficient values (slope) for the cross-species analyses and their respective phylogenetic uncertainty (Uncertainty). Uncertainty is measured as the percentage of the variation in slope values that emerged due to the use of different phylogenies.
Rule Method Hypothesis Mean slope Uncertainty
Bergmann
Polygons
HCH 0.00392 0.266
PPH 0.00076 0.178
SEH -0.00841 0.243
ENMs
HCH -0.00249 0.205
PPH 0.00058 0.200
SEH -0.02351 0.236
Rapoport
Polygons
CVH 0.14000 0.015
CEH (Tmin) -0.08908 0.013
CEH (Tmax) 0.16822 0.012
ENMs
CVH 0.16119 0.037
CEH (Tmin) -0.09942 0.035
CEH (Tmax) 0.19616 0.030
19 Bergmann‟s rule showed more phylogenetic uncertainty regarding the use of different phylogenies than Rapoport‟s rule. However, even for Bergmann‟s rule, the use of different phylogenies produced on average only 20% of the variation in slope values, showing that the use of different phylogenies has a small effect on the difference in slope values regarding this rule.
For Rapoport‟s rule the different phylogenies produced an even smaller uncertainty, which is on average 2% of the total variation in the slope values obtained from different phylogenies.
Overall, our results show that there is no phylogenetic uncertainty in our cross-species analyses, both for Bergmann‟s and Rapoport‟s rule.
DISCUSSION
We found a lack of robustness in our results when considering the different means of evaluating Bergmann‟s and Rapoport‟s rule, showing that both, methods for obtaining range size and approaches to evaluate these patterns, are important in defining whether or not Pit Vipers follow these rules. First, the method used to obtain species geographic range size only affected assemblage analysis, mainly Rapoport‟s rule. Secondly, the approach used to evaluate the ecogeographical patterns influence whether or not a pattern is statistically significant, mainly regarding Bergmann‟s rule. Cross-species analysis does not support Bergmann‟s rule in Pit Vipers, whereas the assemblage analysis supports, although the acceptance of one specific hypothesis depended on how geographic range was obtained. Rapoport‟s rule cross species analysis showed support for the patterns whereas in the assemblage approach, both acceptance and effect direction of a hypothesis were dependent on the method used to obtain species geographic range. Finally, we found that there is no phylogenetic uncertainty in our cross-species analyses, which was expected due to the fact that our phylogeny is almost entirely complete.
20 Here we found support for the recent suggestion that macroecological analyses results might depend on how species geographic range is obtained (Herkt et al., 2017). However, this was only true when considering the assemblage analyses, and particularly for Rapoport‟s rule.
This is not surprising since the different methods employed to generate species geographic range usually produce different species richness maps (Graham & Hijmans, 2006), which would directly affect assemblage analysis (Gaston, 1990; Rahbek, 2005). These differences likely reflect how each method defines the species geographic range. Species geographic range generated by polygons frequently encompass large areas that are meaningless for the species (Worton, 1987), as it simply connects the outmost occurrence points of a species to generate its geographic range in space. Alternatively, ENMs generate geographic range based on how the species occurrence data are related to environmental variables (Zimmermann et al., 2010;
Peterson et al., 2011). As a consequence, geographic range obtained from ecological niche modeling reflects how climatic factors shape species ranges (Searcy & Shaffer, 2016), which in turn leads to the prediction of species occurrence where the suitable environment for their occurrence are (Rebelo & Jones, 2010; Verovnik et al., 2014; Fois et al., 2015). Thus, these two methods potentially provide different species geographic range maps that likely document different pattern of variation of traits across the assemblages, which could explain the different patterns we found. On the other hand, it is unlikely that these kinds of changes would affect cross-species analyses. As the mid-point method considers only the central point of a species range for the analysis (Rohde et al., 1993), unless there are really considerable differences between the maps provided by the distinct methods for obtaining species range, the species mid- point will roughly be the same. For example, polygons and ENMs might even generate maps that have different arrangements, which would lead to different richness maps and potentially affect
21 the assemblage analyses. However, these maps could still have approximately the same extent, which would result basically in the same species mid-point regardless of how their geographic range was obtained. This would explain why the different methods for obtaining species geographic range affected the assemblage analyses but not the cross-species analyses.
Over the past decades there has been an increasing interest on how the use of distinct approaches (e.g. „assemblage‟ and „cross-species‟) to assess ecogeographic patterns are associated with each other. Even though the two approaches we used here to describe patterns are documenting different levels of variation of our traits (Chown & Gaston, 2010), they are expected, at least to some extent, to lead to the same conclusion regarding the occurrence of a pattern in a group of organisms (Gaston et al., 2008). Our results partially fail to support this expectation, mainly with regards to Bergmann‟s rule. It is likely that caveats associated with each approach are playing a role in it. For instance, the use of the cross-species approach usually causes undesirable information loss because it summarizes geographic and environmental data of a species into a single point, which ignores how the data may be structured in the geographic space (Blackburn & Hawkins, 2004; Ruggiero & Hawkins, 2006; Olalla-Tárraga et al., 2010).
On the other hand, in the assemblage approach, a pattern observed may be only evident due to geographic outliers (i.e. a handful widespread species) or factors not considered during the analysis, such as species richness of the assemblages, that could also affect the perception of the pattern (Meiri & Thomas, 2007; Gaston et al., 2008; Adams & Church, 2011). This might have led to the inconsistences we found in Bergmann‟s rule. However, Bergmann‟s rule has been found using both approaches elsewhere (Torres-Romero et al., 2016) suggesting that when the pattern is solid in a group it would be observed regardless of the analysis scale. As a matter of fact, we believe the occurrence of Bergmann‟s rule in the assemblage approach has no biological
22 meaning, because the increase in body size as a response to our predictors is minimal. However, failing in accepting the occurrence of patterns such as Bergmann‟s rule in interspecific analyses (i.e. cross-species and assemblage) could occur if each species was affected differently by the environment (Yom-Tov & Geffen, 2011; Berke et al., 2013). Here we do not believe this be the case, because our analysis only encompassed closely related species belonging to a subfamily.
In addition, we found robustness in the acceptance of Rapoport‟s rule, with congruent results achieved by both approaches. This suggests that some patterns may be more approach-sensible than others and that a thoughtful evaluation about which one should be used to answer a specific question should be carefully done.
We did not find support for Bergmann‟s rule in the cross-species analyses but it became statistically significant in the assemblage analyses. Our assemblage analyses showed a positive relationship (converse Bergmann‟s rule) between body size and mean temperature, AET and seasonality when using polygons. However, our trends only explain a minimal fraction of variation in snakes‟ body size and whether they are biologically relevant remain an open question. For example, Slavenko & Meiri (2015) evaluated Bergmann‟s rule in amphibians and found slope values similar to ours, but in a cross-species context, and concluded that Bergmann‟s rule does not occur in the group. If we also assume that, then our findings confirm those from previous studies that found no relationship between body size and climatic variables in snakes (e.g. Reed, 2003; Terribile et al., 2012; Pincheira-Donoso & Meiri, 2013), enhancing the
proposition that Bergmann‟s rule does not occur in this group. However, one caveat in our study is that we did not consider species ecological traits, such as diel activity patterns, when
evaluating this pattern and Bergmann‟s rule occurrence in snakes might be dependent on their ecological traits (Feldman & Meiri, 2014). Due to these constant failing in support Bergmann‟s
23 rule occurrence in some ectotherms, it has been suggested that its evaluation should be restricted to endotherms only as originally proposed (Pincheira-Donoso et al., 2008). On the other hand, this lack of support to Bergmann‟s rule in ectotherms might occur because different variables might be important in regulating body size in different groups of ectotherms, such as
macronutrients balance are important in caterpillars, oxygen in aquatic ectotherms and
temperature for snails (Arendt, 2015; Hoefnagel & Verberk, 2015; Lee et al., 2015). Hence, it is unlikely that single theories would explain body size variation across all ectotherms (Angilletta et al., 2004). Here, even when testing for correlations of body size and different environmental variables representing competing hypotheses we still failed to obtain support for Bergmann‟s rule, indicating that other variables might be more important to explain variation in New World Pit vipers body size.
Our findings on Rapoport‟s rule support the pattern both in the cross-species and
assemblage analysis. Although this pattern is expected to be more evident in assemblage analysis (Ruggiero & Hawkins, 2006), we found the opposite. In addition, the acceptance and effect direction of our hypotheses in the assemblage level depended on how we obtained our species geographic range. For example, the CVH was associated with decreasing range size when using polygons but this decrease was not significant when using ENMs. Even when one hypothesis was significant using both species geographic range, its effect direction was different. For instance, CEH provided a positive relationship between geographic range size and minimum temperature when using polygons and an opposite negative relationship from niche models. In the light of that, our discussion on Rapoport‟s rule was focused in the cross-species results.
Overall, we found a positive support for the CVH, with species having larger occurrence areas in places with more variable temperatures. Temperature variation selects for broader thermal
24 tolerances in species (Bozinovic et al., 2011; Sunday et al., 2011; Quintero & Wiens, 2013), which increases their physiological flexibility and consequently their performance and capability to adapt to changing biotic and abiotic conditions (Chown et al., 2004; Bozinovic et al., 2011), which would potentially enable snakes to expand their occurrence area. Interestingly, we also found support for the CEH. We found a positive relationship between maximum temperature and geographic range size. This is unexpected since most ectotherms show almost no capacity to change their upper thermal limits (Araújo et al., 2013; Hoffmann et al., 2013), which would result in high temperatures preventing them to expand their geographical range. However, two main factors might explain this finding. First, the highest temperature recorded in our analysis is 41.3ºC, which is slightly below the critical maximum temperature of 42.2 ºC for reptiles (Araújo et al., 2013), showing that there is no major restriction of temperature on snakes occurrence in our studied area. Secondly, even when facing temperatures as high as or higher than their critical maximum, snakes can handle these temperatures through their thermoregulatory behavior (Huey et al., 1989; Grant, 1990; Sunday et al., 2014), which potentially enable them to expand their geographic distribution even though temperatures are not favorable. Thus, high temperatures in our studied area are not likely to restrict snakes range size in the present. On the other hand, we found a negative relationship between minimum temperature and geographic range size. Low temperatures are thought to be important in limiting snakes distribution (Spellerberg, 1972) and empirical evidence suggests that it acts as a range barrier in some ectotherms (Lee et al., 2009).
However, the increasing geographic range size with lower minimum temperatures as we
obtained here could be explained due to the high lability of lower thermal limits of ectotherms, in which species inhabiting colder locations can usually adapt their lower thermal limits (Sunday et al., 2011; Araújo et al., 2013). Thus, lower temperatures might not be as restrictive to ectotherms
25 as usually suggested, and even when inhabiting colder places, they could still potentially expand their range size.
CONCLUSION
Overall, the cross-species approach was more robust whereas the assemblage approach was more sensible to the method for obtaining species geographic range, especially for detecting Rapoport‟s rule. Moreover, the approach used to assess ecogeographical rules was also important to define whether a pattern is statistically significant, mostly for Bergmann‟s rule. Thus, we suggest that the method used to obtain species range size needs to be thoroughly evaluated when testing ecogeographical rules, with special attention for Rapoport‟s rule in an assemblage
context. In addition, we also recommend using more than one approach to assess these patterns whenever possible so that it can be shown at what level environment is important in acting on specific species traits.
CONCLUSÃO GERAL
Nosso trabalho demonstrou que tanto o método utilizado para obter a área de ocorrência das espécies quanto a abordagem utilizada para avaliar os padrões ecogeográficos podem afetar nossas conclusões em relação ocorrência das regras ecogeográficas. Especificamente, o método utilizado para obter a área de ocorrência das espécies afeta se um padrão é significativo ou não, especificamente nas análises de assembleia e principalmente em relação ao padrão proposto pela regra de Rapoport. Além disso, as diferentes abordagens utilizadas para avaliar um padrão levam
26 a diferentes conclusões quanto à ocorrência do padrão, principalmente em relação à regra de Bergmann. Assim, nós recomendamos que o método a ser utilizado para gerar a área de ocorrência das espécies deve ser considerado de forma cuidadosa, especialmente quando avaliando os padrões de Rapoport em um contexto de assembleia. Além disso, nós também recomendamos, sempre que possível, o uso de mais de uma abordagem para avaliar a ocorrência de tais padrões, pois assim pode ser demonstrado em qual nível de organização o ambiente está influenciando o tamanho corporal e de área de distribuição das espécies.
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