Mastozoología Neotropical ISSN: 0327-9383 ISSN: 1666-0536 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina

Maestri, Renan A MACROECOLOGICAL PERSPECTIVE ON NEOTROPICAL Mastozoología Neotropical, vol. 27, núm. 0, 2020, -Julio, pp. 27-36 Sociedad Argentina para el Estudio de los Mamíferos Tucumán, Argentina

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Número Aniversario

A MACROECOLOGICAL PERSPECTIVE ON NEOTROPICAL RODENTS

Renan Maestri

Departamento de Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre Brazil [Correspondence: ].

ABSTRACT. The last 25 years have seen the growth of Mastozoología Neotropical and the rise of macroecology. Neotropical rodents offer ideal groups to understand broad-scale ecological processes, and at the same time, macroecological approaches applied to these rodents help us achieve understanding about their biogeography and evolution. Some patterns resulting from the radiations in the Neotropics are now adequately understood, but we are still far from understanding the underlying ecological processes. Paths to advance macroecological research include fully integrating biogeographical and evolutionary accounts into large scale ecological studies, and improving macroecological models using process-based models and proper null predictions. In order to do that, it is essential to have more reliable information about the biology of Neotropical rodents, which depend on basic natural history research and data storage in museum collections.

RESUMO. Uma perspectiva macroecológica dos roedores neotropicais. Os últimos 25 anos viram o crescimento da Mastozoología Neotropical e a ascensão da macroecologia. Roedores neotropicais oferecem grupos ideais para entender processos ecológicos de larga escala, e, ao mesmo tempo, abordagens macroecológicas aplicadas a estes roedores nos ajudam a aumentar o entendimento sobre sua biogeografia e evolução. Alguns padrões resultantes das radiações de roedores nos Neotrópicos são adequadamente entendidos, mas ainda estamos longe de entender os processos ecológicos subjacentes. Alguns caminhos para avançar a pesquisa em macroecologia incluem integrar melhor fenômenos biogeográficos e evolutivos em estudos de larga escala, e melhorar os modelos macroecológicos usando modelos baseados em processos e modelos nulos adequados. Para este fim, é essencial obter informações confiáveis sobre a biologia de roedores neotropicais, o que depende de pesquisa básica em história natural e armazenamento de dados em coleções de museus.

RESUMEN. Una perspectiva macroecológica de los roedores neotropicales. Los últimos 25 años han sido testigos del crecimiento de Mastozoología Neotropical y del surgimiento de la macroecología. Los roedores neo- tropicales son un grupo ideal para estudiar procesos ecológicos a gran escala, y, al mismo tiempo, los enfoques macroecológicos aplicados a estos roedores contribuyen a nuestra comprensión de su biogeografía y evolución. Algunos patrones resultantes de las radiaciones de roedores en el Neotrópico se comprenden adecuadamente en la actualidad, pero estamos todavía lejos de entender los procesos ecológicos subyacentes. Los caminos para avanzar en la investigación macroecológica incluyen tanto una integración plena de los fenómenos biogeográficos y ecológicos en estudios ecológicos de gran escala como mejorar los modelos macroecológicos usando modelos basados en procesos y predicciones nulas apropiadas. A estos efectos, es esencial contar con más información

Recibido 28 diciembre 2018. Aceptado 20 mayo 2019. Editor invitado: E. Lessa 28 Mastozoología Neotropical, 27(SI):27-36, Mendoza, 2020 R. Maestri http://www.sarem.org.ar - https://sbmz.org confiable de la biología de los roedores neotropicales, en base a investigación de su historia natural- ydelde pósito de datos en colecciones de museo.

Key words: clades, diversification, evolutionary history, macroecology, macroevolution.

Palavras chave: clados, diversificação, história evolutiva, macroecologia, macroevolução.

Palabras clave: clados, diversificación, historia evolutiva, macroecología, macroevolución.

INTRODUCTION (Smith et al. 2008; Smith & Lyons 2011; Weber 2018), studies considering only Neotropical The middle ’90s saw the beginning of Masto- rodents are scarce. In order to contextualize the zoología Neotropical (Ojeda 1994), now the current state of macroecological/biogeographi- leading journal for Neotropical mammalogy, cal research for this group, I conducted a search and also the rise of a new field called macro- for studies of macroecology specifically focused ecology (Brown & Maurer 1989; Brown 1995). on Neotropical rodents. This search returned The macroecological approach focuses on large only 10 articles in the last 25 years (searched spatial and temporal scales to find and explain in the database of Web of Science using the recurrent patterns that emerge consistently terms: [macroecol* AND (neotrop* OR South enough to suggest that general mechanism are America OR Central America) AND (rodent* in operation (Brown & Maurer 1989; Brown OR sigmodont* OR caviomorp* OR hystrico*)], 1995). Such mechanisms can take place at the including mentions in the title, abstract and assemblage and ecosystem levels, as well as at key words). Replacing macroecology with the individual and population levels (Brown biogeography (term: [biogeogr*], other terms 1995; Brown et al. 2004; Smith & Lyons 2011), unchanged) returned 258 articles for the same helping to distinguish macroecology from time window. While some of the biogeography biogeography (the latter usually centered on articles may have used an ecological approach -level processes such as speciation, considering a relationship between organisms extinction and range expansion). and environment, still a macroecological em- Nevertheless, macroecology and biogeography phasis on these rodents seems to be scarce. are not always easily distinguished, and with the In the search for general regularities, macro- omnipresence of molecular phylogenetics, both ecology has focused on patterns characterizing are now closely connected to macroevolution. broad taxonomic groups, such as Common questions in these fields involve the (Safi et al. 2011) and birds (Jetz et al. 2012), search for processes behind patterns of species which explains the small number of articles richness (e.g., Pereira & Palmeirim 2013), phy- mentioned previously. Indeed, such a broad fo- logenetic lineage distribution (e.g., Duarte et al. cus can help uncover patterns sustained by deep 2014), body size variation (e.g., Martinez et al. biological functioning (e.g., a pattern repeatedly 2013), and range size distribution (e.g., Arita et found, regardless of the taxonomic group anal- al. 2005), among others. The merger of macro- ysed), such as metabolic scaling theory (Brown ecology and biogeography should be encouraged et al. 2004; West & Brown 2005). However, and embraced, since using a common language this approach can also mask some interesting and concepts can only help us to understand patterns that occur in particular clades. For patterns and processes at regional and larger example, bats have an unusual biology, and scales (Jenkins & Ricklefs 2011). Neotropical clades of bats have been targets of While the overall number of macroecological interesting discoveries using macroecological studies have been rising fast in the last decades investigations (Stevens 2005; López-Aguirre et MACROECOLOGY OF NEOTROPICAL RODENTS 29 al. 2018). Monophyletic clades with singular in tropical montane regions. Concatenating histories of colonization in a given region can data on biogeographical ranges for each major illuminate particular macroecological patterns, clade separately reveals that sigmodontines and which are obscured when more comprehensive caviomorphs share similar patterns of richness, groups with multiple independent histories are although sigmodontine richness is largely asso- mixed. Focusing on monophyletic groups as the ciated with mountainous regions in the Andes hierarchical level of analyses (Eldredge 1985) and in the Atlantic forest, while caviomorphs offers interesting perspectives into ecological better reflect a latitudinal gradient with richness patterns and processes. positively associated with temperature (Maestri Neotropical rodents comprise the largest & Patterson 2016) and peaks in richness even component of mammalian diversity in the at low elevations in Amazonia (Upham & Pat- Neotropics, including more than half of all terson 2012). The Andes harbor/support regions species in this region (Patterson 2000). of high richness for both groups, as well as Two major radiations contain most of the ~650 regions of endemism (Ferro 2013; Upham et rodent species in the New World (Patton et al. al. 2013; Prado et al. 2015), and are crucial to 2015): the sigmodontines and the caviomorph sustaining rodent diversity in South America rodents. Caviomorphs have a ~50 million-year (Patterson et al. 2012; Novillo & Ojeda 2014). history in the Neotropics, which began after Unsurprisingly, spatial patterns of species beta- transoceanic dispersal from Africa, and the diversity uncover the highest values of rodent group has about 250 living species today (Rowe turnover along the Andes chain (Maestri & et al. 2010; Upham & Patterson 2015; Vucetich Patterson 2016), a pattern shared by both et al. 2015). Sigmodontines have a shorter his- caviomorphs and sigmodontines. tory of diversification, dating back ~10 million Patterns of species richness and diversifi- years (Steppan et al. 2004; Leite et al. 2014), cation dynamics can vary according to the and the colonization of South America was phylogenetic scale used (Morlon et al. 2011; performed via dispersal from North America Graham et al. 2018), making it important to (Parada et al. 2013; Vilela et al. 2014). Neverthe- evaluate clade-specific patterns. For example, less, sigmodontines underwent a rapid radiation variation in species richness by elevation varies resulting in over 400 living species (D’Elía & by family of anurans (Hutter et al. 2017), which Pardiñas 2015). The contrasting histories of is similar to the strong effect of elevation found colonization of caviomorphs and sigmodontines on sigmodontine richness than on caviomorph in the Neotropics pose a number of questions richness (Maestri & Patterson 2016). There- that call for a macroecological perspective; few fore, by pulling contrasting clades together in of these questions have been answered. In this a single analysis, dominant groups can mask Perspective, I offer a brief standpoint on the richness patterns occurring in less species rich current research on the most basic subjects groups, and interesting patterns can vanish. of macroecological research—patterns and Given the different histories of diversification processes of species and lineage diversity, body of sigmodontines and caviomorphs—as is size, and range size distribution—focusing on also true for many other large groups—it is Neotropical rodents. important that both rodent clades are treated separately in macroecological studies. The re- PATTERNS sulting distinct patterns/processes can then be compared to achieve synthesis on the factors Advances in and field studies have affecting biodiversity. led to refined data on the distribution of rodent The uneven distribution of lineages inside big species over the years (Wilson & Reeder 2005; clades (e.g., sigmodontines and caviomorphs) Patton et al. 2015). This effort allowed the can also generate distinct patterns of lineage depiction of patterns of rodent richness over diversity and distribution (Heard & Cox 2007), the Neotropics (Amori et al. 2013), revealing calling for a phylogenetic perspective. A num- a latitudinal gradient with peaks of richness ber of articles on biogeography of Neotropical 30 Mastozoología Neotropical, 27(SI):27-36, Mendoza, 2020 R. Maestri http://www.sarem.org.ar - https://sbmz.org rodents confirm that a historical approach is and its association with elevation (Stevens important to understand current patterns (Leite 1992). Body size patterns have been explored et al. 2014; Upham & Patterson 2015; Prado & for a few rodent groups (e.g., Medina et al. Percequillo 2018; Gonçalves et al. 2018; Mach- 2007; Maestri et al. 2016). Body size variation ado et al. 2018). Moreover, using phylogenetic in caviomorphs is very heterogeneous in its metrics of diversity can be a way to approximate rates of evolution (Álvarez et al. 2017) and historical biogeography and macroecology seems to be associated with variation in life (Davies & Buckley 2011; Cisneros et al. 2014; mode (Upham 2014), although we still lack a Stevens & Gavilanez 2015). Few studies have clear picture of how size is spatially distributed. considered phylogenetic metrics of diversity for For sigmodontines, assemblages of species with Neotropical rodents at a continental scale. At larger body sizes seem to be associated with least one study with caviomorphs has shown re- open and warm areas in South America (Mae- gions of high phylogenetic diversity (controlled stri et al. 2016), but more studies are needed for richness effects) associated with open areas to refine body size estimates and investigate in the Neotropics (Fergnani & Ruggiero 2015), within-species and cross-species patterns. and one study with sigmodontines revealed Skewness of body size and other traits are also lower average phylogenetic relatedness for relevant and its patterns are still to be explored. assemblages in the Amazon basin and higher Patterns in the distribution of other phe- values for assemblages in Central America and notypic traits are still poorly understood at a northern South America (Maestri et al. 2019). macroecological scale, although efforts have Patterns of phylogenetic diversity and phyloge- been made to understand the evolution of such netic turnover are still to be entirely explored traits as appendicular morphology, tail and feet for Neotropical rodents and its sub-clades at length, and molar morphology across species a macroecological scale. (Morgan & Álvarez 2013; Carrizo et al. 2014; It is important to stress that well-resolved Parada et al. 2015; Tulli et al. 2016; Tavares et phylogenetic trees are essential to reliably in- al. 2018a). Attempts to depict spatial patterns of terpret phylogenetic metrics in macroecology. shape variation are promising and have shown, Despite the existence of many phylogenetic for example, an association between relatively hypotheses for Neotropical rodents (e.g., Up- larger and rounded tympanic bullas with arid ham & Patterson 2015; Maestri et al. 2017), areas in the Neotropics at an assemblage level better phylogenies are still needed to resolve (Maestri et al. 2018), a pattern recurring gen- the relationships among species and subclades erally among rodents (Alhajeri et al. 2015). within caviomorphs and sigmodontines. For Evidently, phenotypic traits carry a relation- example, tribal-level relationships among sig- ship with overall body size, and allometry is modontine rodents are still poorly resolved an important factor in trait evolution (Marroig (Steppan et al. 2004; Parada et al. 2013; Leite 2007; Tavares et al. 2018b), which must also et al. 2014). Moreover, the scarcity of fossils be accounted for in future macroecological for sigmodontines cast doubts on the chronol- studies of traits. Another pattern frequently ogy of diversification (Barbière et al. 2019). A overlooked for these rodents, but little studied, broader taxonomic and gene coverage is needed is the frequency of sexual dimorphism across to increase support for phylogenetic patterns species, which can generate a macroecological in macroecology. pattern for sexual selection (Macías-Ordóñez Other patterns such as the distribution of et al. 2014). range sizes (Ruggiero & Werenkraut 2007; A voluminous number of recent investiga- Novillo & Ojeda 2012) and traits like body size tions have studied body size and other traits (Medina et al. 2007) are still little known for at the macroevolutionary level (Alhajeri et al. Neotropical rodents. Despite the all-importance 2016; Álvarez et al. 2017; Maestri et al. 2017; of Andes to determine rodent richness in the Tavares et al. 2018a), in large part enabled by Neotropics, we lack an understanding of pat- the availability of data in museums and the terns of range-size distribution (Rapoport 1982) ability to access DNA sequences from reposi- MACROECOLOGY OF NEOTROPICAL RODENTS 31 tories (Lessa et al. 2014; Dunnum et al. 2018). be occupied during the group’s biogeographi- General macroecological patterns for traits can cal history (Maestri et al. 2019), suggesting be expected to emerge from spatially explicit that processes of diversification depend on approaches to trait evolution (e.g., Polly et al. the sequence of biogeographical occupation. 2017), and integrating concepts and analysis Studies that integrate estimates of diversifica- from related disciplines, such as metacom- tion and dispersal (e.g., using new promising munity and phylogenetic ecology (Duarte et approaches as the geographical state-dependent al. 2018), which can be achieved by mapping diversification—Goldberg et al. 2011) with ex- the trait’s averages and disparities among point plicitly spatial and environmental contexts are localities or grid cells and associating their spa- still lacking, and may offer novel perspectives tiotemporal variation with major environmental on the processes behind the observed patterns and geological events. of species richness and phylogenetic diversity for Neotropical rodents. PROCESSES The relationship between richness and abun- dance across space has been the subject of Understanding the processes that generate few Neotropical studies (e.g., Novillo & Ojeda broad-scale patterns of diversity is a long- 2014). Insights into macroecological patterns term goal of macroecology. The task is not of abundance can be gained by exploring new straightforward and involves the adoption of refined data, such as those recently compiled mechanistic and process-based models that for the Atlantic forest (Figueiredo et al. 2017). consist of explicit expectations derived from Another potentially interesting approach to biological reasoning (Keith et al. 2012; Connolly understand processes is to investigate the role et al. 2017). A recent advance incorporated of large-scale biotic interactions on species estimates for parameters as dispersal, evolution- richness. Caviomorphs had more than 30 mil- ary rate, time for speciation, and competition lion years to colonize the Neotropics (Lessa et into a macroecological model (Rangel et al. al. 2014; Upham & Patterson 2015), and still, 2018), offering a promising approach to the incumbency effects seem to be unimportant study of processes in macroecology. Simple given the astonishing radiation of sigmodon- macroecological models could be improved by tines (although caviomorphs have an extensive incorporating biotic interactions and historical record of extinctions). Yet, a proper assessment factors, which would allow the development of of the influence of biotic interactions on rich- proper null predictions. To date, progress in ness patterns has not been conducted. A per- the understanding of processes for Neotropical spective focused on interactions among species rodents has been large gained through infer- may help to elucidate the causes of richness ences from statistical associations between differences among clades (Fig. 1). biodiversity variables and environmental and Elucidating the processes behind range size biogeographical predictors. distribution depends first on documenting the How the processes of speciation, extinc- patterns. The general relationship between el- tion, and dispersal unfolded to generate the evation and range size (Stevens 1992; McCain current diversity patterns are still poorly 2009) may hide interesting explanations con- understood. Integrating information from sidering the particular association of rodents studies on phylogenetics and biogeography with elevation and the peculiarities of the Andes of Neotropical rodents (e.g., Leite et al. 2014; Mountains. For instance, Steven’s rule (Stevens Upham & Patterson 2015) with a spatially ex- 1992) predicts larger elevational ranges with plicit macroecological standpoint offers a new increasing elevation, following an increased perspective on how diversification occurred climatic variability at high elevations (McCain across space. For example, regions of faster & Knight 2013). However, Andes Mountains in diversification for sigmodontines have been South America have extensive Puna regions, found in southern and northeastern South which may have homogeneous climatic condi- America, which were among the last regions to tions, possibly disrupting the expected linear 32 Mastozoología Neotropical, 27(SI):27-36, Mendoza, 2020 R. Maestri http://www.sarem.org.ar - https://sbmz.org

Fig. 1. A) Difference in richness between sigmodontines and caviomorphs. For each cell, sigmodontine minus caviomorph richness was calculated. Blue cells indicate more species of caviomorphs than sigmodontines, and the inverse for red cells. B) The 25% richest assemblages in terms of number of species for caviomorphs (red), and sigmodontines (blue), with black cells indicating overlap. relationship at the highest elevations (Patterson and also illuminate patterns of diversity for et al. 1998). these rodents. We still know little about rates Patterns of body size can have a number of energy intake and consumption for Neo- of ramifications still to be explored. Body tropical rodent species, as well as the effect of size is positively related with total metabolic ambient temperature on body size (Naya et costs (Kleiber 1932; Brown et al. 2004) and al. 2018), and such knowledge is essential to negatively with population density (Damuth understand the basics of metabolic demands 1981), such that an ‘energetic equivalency’ ex- and its differences among rodents. This may ists where energy use is independent of body be fundamental to understand processes in size (Nee et al. 1991), but see Marquet et al. macroecology (Brown et al. 2004). (1995). Large species are also thought to utilize Finally, we do not understand how traits are larger geographic areas because of energetic associated with diversification rates for Neo- necessities (Diniz-Filho & Balestra 1998; Olifi- tropical rodents. Body size, appendicular and ers et al. 2004) and have increased extinction molar morphology, and skull shape and size are rates (Cardillo et al. 2005) compared to small a few of the phenotypic characteristics that have . If so, small rodents can be expected been studied (Morgan & Álvarez 2013; Parada to have smaller range sizes than large rodents et al. 2015; Maestri et al. 2017). Any could (still to be properly investigated) and that can have acted to trigger niche occupation and contribute to higher speciation rates (greater species diversification. Yet, few attempts have opportunity for reproductive isolation due to been made to connect traits to diversification range fragmentation) and less extinction in rates (Parada et al. 2015; Álvarez et al. 2017), such clades owing to higher population density. which promises to reveal the links among rates Therefore, understanding the forces behind of diversity, disparity, and its uneven spatial body size evolution can explain size variation distribution. MACROECOLOGY OF NEOTROPICAL RODENTS 33

FINAL CONSIDERATIONS ACKNOWLEDGMENTS

Recent decades have seen a rise in the field I thank Enrique Lessa, Gabriel Marroig, and Eileen Lacey for inviting me to contribute this perspective. Most of of macroecology, which could be attributed to my understanding and perspectives about the subjects both the development of spatial statistics and presented here were heavily influenced by conversations the availability of data (Smith et al. 2008). A with Thales Freitas, Leandro D. S. Duarte, Nathan S. Up- macroecological perspective is highly depen- ham, and especially Bruce D. Patterson over the years. I dent on studies that collect biodiversity data also thank Bruce Patterson, André L. Luza, Enrique Lessa, and one anonymous reviewer for helpful comments on and/or document the distribution, phenotypic, this manuscript. and genetic characteristics of organisms (Beck et al. 2012). Improvements in macroecological LITERATURE CITED research will thus depend on basic biological research and the availability of specimens in Alhajeri, B. H., J. J. Schenk, & S. J. Steppan. 2016. Ecomorphological diversification following continental scientific collections and information on their colonization in muroid rodents (Rodentia: Muroidea). spatial distribution (De la Sancha et al. 2017). Biological Journal of the Linnean Society 117:463-481. Macroecological models would be greatly im- Alhajeri, B. H., O. J. Hunt, & S. J. Steppan. 2015. proved with enhanced biological knowledge, Molecular systematics of gerbils and deomyines (Rodentia: Gerbillinae, Deomyinae) and a test of desert including stronger data on density and dispersal adaptation in the tympanic bulla. Journal of Zoological abilities, biotic interactions, as well as diet, Systematics and Evolutionary Research 53:312-330. habitat, and behavior. Álvarez, A., R. L. M. Arévalo, & D. H. Verzi. 2017. Remaining questions include intensive inves- Diversification patterns and size evolution in caviomorph rodents. Biological Journal of the Linnean tigations of the most basic aspects of species Society 121:907-922. diversity, body size and range size distribution, Amori, G., F. Chiozza, B. D. Patterson, C. Rondinini, some presented in this perspective. Certainly, J. Schipper, & L. Luiselli. 2013. Species richness and the distinctive histories of Neotropical rodent distribution of Neotropical rodents, with conservation implications. Mammalia 77:1-19. clades must be considered explicitly, since, for Arita, H. T., P. Rodríguez, & E. Vázquez-Domínguez. example, regions functioning as ‘cradles’ and 2005. Continental and regional ranges of North ‘museums’ of biodiversity are likely to be clade- American mammals: Rapoport’s rule in real and null specific. By comparing processes responsible worlds. Journal of Biogeography 32:961-971. Barbière, F., P. E. Ortiz, & U. F. J. Pardiñas. 2019. for biodiversity distribution in those clades, The oldest sigmodontine rodent revisited and the general regularities may emerge, and knowledge age of the first South American cricetids. Journal of about the evolution and biogeography of these Paleontology 93:268-384. rodents can be achieved. Beck, J., L. et al. 2012. What’s on the horizon for macroecology? Ecography 35:673-683. Decades of efforts by taxonomists, pale- Brown, J. H. 1995. Macroecology. University of Chicago ontologists, ecologists, phylogeneticists and Press, Chicago. many others working on Neotropical rodents Brown, J. H., & B. A. Maurer. 1989. Macroecology: the (Reig 1986; Pardiñas et al. 2002; D’Elía 2003; division of food and space among species. Science 243:1145-1150. Weksler et al. 2006; Voss et al. 2013; Luza Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage, et al. 2015) have created the foundation to & G. B. West. 2004. Toward a metabolic theory of document patterns and understand processes ecology. Ecology 85:1771-1789. in macroecology. In turn, a macroecological Cardillo, M. et al. 2005. Multiple causes of high extinction risk in large mammal species. Science perspective can help to integrate ecology, 309:1239-1241. evolution, and biogeography of Neotropical Carrizo, L. V., M. J. M. J. Tulli, D. A. Dos Santos, rodents, and elucidate the biological mecha- & V. Abdala. 2014. Interplay between postcranial nisms behind large-scale ecological patterns. morphology and locomotor types in Neotropical sigmodontine rodents. Journal of Anatomy 224:469- Much work remains to be done, both to docu- 481. ment patterns, and especially to understand Cisneros, L. M. et al. 2014. Multiple dimensions of bat underlying processes—this task is still in its biodiversity along an extensive tropical elevational infancy for Neotropical rodents. gradient. Journal of Ecology 83:1124-1136. 34 Mastozoología Neotropical, 27(SI):27-36, Mendoza, 2020 R. Maestri http://www.sarem.org.ar - https://sbmz.org

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