Sociobiology of Caviomorph Rodents ebook

Table of Contents

Cover

Title Page

Copyright

Dedication

Acknowledgments

Notes on contributors

Introduction

I.1 Social behavior of caviomorph rodents and book aims

I.2 Research approaches to social behavior

I.3 Terminology

I.4 Structure of the book

Acknowledgments

References

Chapter 1: The caviomorph rodents: distribution and ecological diversification

1.1 The caviomorph radiation

1.2 The families

1.3 General social behavior

1.4 Synthesis and future directions

Acknowledgments

References

Chapter 2: Diversity of social behavior in caviomorph rodents

2.1 Introduction

2.2 The comparative approach in sociobiology

2.3 Intraspecific variation in social systems of caviomorphs

2.4 Future directions

2.5 Conclusion

Acknowledgments

References

Chapter 3: Comparative neurobiology and genetics of mammalian social behavior

3.1 Introduction

3.2 Molecular and circuit bases of social behavior

3.3 Genes and social behavior

3.4 Mechanisms of sociality in caviomorphs

3.5 Future directions

Acknowledgments

References

Chapter 4: Developmental underpinnings of social behavior

4.1 Introduction

4.2 Prenatal epigenetic factors: intrauterine position and prenatal stress

4.3 Formation, strength and persistence of attachment bonds in early infancy

4.4 Social deprivation during infancy and consequences of breaking social bonds

4.5 Discussion and future research directions

Acknowledgments

References

Chapter 5: Dispersal in caviomorph rodents

5.1 Introduction

5.2 What is dispersal?

5.3 Studying dispersal: logistic challenges

5.4 Dispersal in caviomorph rodents

5.5 Understanding dispersal: adaptive explanations

5.6 Understanding dispersal: proximate explanations

5.7 Consequences of dispersal: social behavior

5.8 Consequences of dispersal: genetic structure

5.9 Toward an integrated understanding of dispersal

5.10 Future directions

Acknowledgments

References

Chapter 6: Mechanisms of social communication in caviomorph rodents

6.1 Introduction

6.2 Social species

6.3 Solitary species

6.4 General trends and future directions

Acknowledgments

References

Chapter 7: Causes and evolution of group-living

7.1 Introduction

7.2 Reasons for group-living

7.3 Evolutionary trends

7.4 Future directions and conclusion

Acknowledgments

References

Chapter 8: Rodent sociality: a comparison between caviomorphs and other rodent model systems

8.1 Introduction

8.2 Defining and assessing sociality

8.3 Overview of hypotheses concerning sociality

8.4 Sociality in non-caviomorph rodents

8.5 Sociality in caviomorphs

8.6 What do we still need to know about sociality in caviomorphs?

Acknowledgments

References

Chapter 9: Cooperation in caviomorphs

9.1 Introduction

9.2 Mechanisms explaining cooperative behaviors

9.3 Disentangling cooperative behaviors and group size effects

9.4 Cooperative behavior in caviomorphs

9.5 Final outlook and future directions

Acknowledgments

References

Chapter 10: Caviomorphs as models for the evolution of mating systems in mammals

10.1 Introduction

10.2 “Solitary,” pair-bonding caviomorphs

10.3 Social caviomorphs

10.4 Other caviomorphs and future directions

Acknowledgments

References

Chapter 11: Parent-offspring and sibling-sibling interactions in caviomorph rodents: a search for elusive patterns

11.1 Introduction and theoretical background

11.2 Caviomorph life history and family interactions

11.3 Phylogenetic synthesis

11.4 Future directions

11.5 Conclusion

Acknowledgments

References

Chapter 12: Fitness consequences of social systems

12.1 Theoretical framework

12.2 Fitness consequences in caviomorph rodents

12.3 Future directions

Acknowledgments

References

Chapter 13: An integrative view of caviomorph social behavior

13.1 Introduction

13.2 Mechanistic underpinnings of sociality

13.3 An integrative model of caviomorph sociality

13.4 Future directions

13.5 Concluding remarks

Acknowledgments

References

Glossary

References

Index

End User License Agreement

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Guide

Cover

Table of Contents

Introduction

Begin Reading

List of Illustrations

Chapter 1: The caviomorph rodents: distribution and ecological diversification

Figure 1.1 Representative genera of major caviomorph macroniches combining modes of life, such as substrate use, and feeding habits. Original drawings by Benjamín Bender.

Figure 1.2 Geographic distribution of caviomorph families and species density.

Figure 1.3 Illustrative graphic which summarizes the general behavior (solitary and social) in major caviomorph lineages (superfamilies and families). Phylogeny after Upham & Patterson (2012).

Chapter 2: Diversity of social behavior in caviomorph rodents

Figure 2.1 The distribution of social systems for 117 species of caviomorphs over the range of log10 body sizes.

Chapter 3: Comparative neurobiology and genetics of mammalian social behavior

Figure 3.1 Overview of oxytocin receptor distribution in the degu forebrain. Olf = olfactory bulbs, PFC = infralimbic prefrontal cortex, NAc = nucleus accumbens, IG = indusium grisium, Pir = piriform cortex, ICj = islands of Calleja, LS = lateral septum, BNST = bed nucleus of the stria terminalis, MPOA = medial preoptic area of the hypothalamus, VMH = ventromedial nucleus of the hypothalamus, BLA = basolateral amygdala (shown later than scored region), MeA = medial amygdala, CA1 = cornu ammonis 1 of the hippocampus, CA3 = cornu ammonis 3 of the hippocampus. Not all subregions scored are illustrated.

Chapter 4: Developmental underpinnings of social behavior

Figure 4.1 Attachment theory process.

Chapter 5: Dispersal in caviomorph rodents

Figure 5.1 Schematic of the balance of adaptive costs and benefits that influence individual dispersal decisions. The costs of dispersal are determined by multiple factors (e.g. risk of predation) that vary in magnitude across taxa, environments, and individuals. Here, these costs are depicted as a slider bar; the location of the bar represents the total costs of dispersal for a given individual in a given environment. The total benefits of dispersing (e.g. outbreeding) are depicted similarly. The balance of these costs and benefits determines the net adaptive consequences of dispersal from the natal or breeding area. Collectively, these individual-level dispersal decisions have significant impacts on social and genetic structure.

Figure 5.2 Schematic of the dispersal process. For individuals that leave their natal or breeding area, the process of dispersal typically consists of three stages: initiation, transit, and settlement. A detailed explanation of each stage is provided in the text. Because each of these stages may be subject to different net cost-benefit outcomes and may be influenced by different combinations of proximate mechanisms, distinguishing between these distinct components of dispersal may be critical to understanding variation in this fundamental aspect of behavior.

Figure 5.3 Integrative framework for studies of natal dispersal. At the individual level (light gray rectangle), extrinsic (e.g. ecological) and intrinsic (e.g. physiological) factors interact to determine the net costs-benefits of dispersal; because both types of factors are variable, individual dispersal decisions may vary. In general, individuals that fail to disperse tend to remain in their natal group and to live with closely related conspecifics; in contrast, individuals that disperse from the natal area tend to live alone or, if they immigrate to an existing social group, to live with conspecifics that are not close kin. These dispersal-mediated differences in social environment have significant implications for the fitness benefits (direct, indirect) achieved by individuals. These individual-level decisions, in turn, determine population-level patterns of behavior, including the typical frequency of dispersal and the mean distance moved by dispersing individuals. These population-level patterns (medium gray rectangle) have critical implications for social and genetic structure. Because environmental conditions likely vary among populations (hatched rectangle), the frequency and extent of dispersal may also vary; these inter-population differences in dispersal (dark rectangle) have potentially important implications for patterns of gene flow and drift and, ultimately, evolutionary change. These distinct scales of dispersal behavior (individual, population, species) have typically been studied independently; this schema offers a clear framework for assessing the causes and consequences of variation in dispersal at all of these levels of biological organization.

Chapter 7: Causes and evolution of group-living

Figure 7.1 Relative importance of distribution and abundance of resources, and predation in predicting median group size of well-studied caviomorphs. Data on group size follow different authorities reported in Table 7.1. The relative role of resources and predation has been inferred from the extent of evidence supporting each, and from the overall assessments made by some of the authorities.

Chapter 9: Cooperation in caviomorphs

Figure 9.1 Different cases for hypothetical group foraging animals, showing total group vigilance (i.e. individual vigilance times the number of members in the group) as a function of group size (see text for details).

Chapter 10: Caviomorphs as models for the evolution of mating systems in mammals

Figure 10.1 A conceptual model of the effect of ecology on mating systems in mammals, starting with the main factor affecting the mating system, which is reproductive investment (Bateman 1948). Altriciality (low development at birth), another factor affecting the mating system, is also shown.

Chapter 11: Parent-offspring and sibling-sibling interactions in caviomorph rodents: a search for elusive patterns

Figure 11.1 Phylogeny showing distribution of group living and other relevant traits. Adapted from Sobrero et al. (2014).

Chapter 13: An integrative view of caviomorph social behavior

Figure 13.1 An integrative model of caviomorph sociality. The model highlights the ways in which proximate mechanisms interact with social and habitat conditions to cause sociality, its potential variation, its current adaptive value, and evolution. Shaded boxes represent the main components of the model (social group, habitat conditions, developmental conditions, adult individual), which in turn are connected to or have effects through different processes and mechanisms (

italics

). In the case of social groups, we further distinguish between group attributes (composition and size; within the shaded box) and emergent characteristics (stability, cooperation/conflict; white boxes). A behavioral type is an emergent attribute of the individual. This profile is central to an individual's predisposition to associate with conspecifics, form groups, and cooperate or compete with group members. Life history, separated by a black box, includes organismal and population traits, and is crucial to phenotypic trade-offs and developmental conditions. Arrows indicate the direction of the predicted influence. Further details and justification for different components and connections are given in the text (Section 13.3).

List of Tables

Chapter 1: The caviomorph rodents: distribution and ecological diversification

Table 1.1 Ecoregions (see Fig. 1.2), macroniches, body mass (g), and general social behavior of caviomorph genera

Chapter 2: Diversity of social behavior in caviomorph rodents

Table 2.1 Interspecific variation in caviomorph species for which there is sufficient information

Table 2.2 Intraspecific variation in social systems and ecological correlates associated with changes in caviomorph social organization

Chapter 3: Comparative neurobiology and genetics of mammalian social behavior

Table 3.1 Select “non-classic” species used for comparative neurobiological studies of vertebrate social behavior

Table 3.2 Oxytocin receptor binding densities in the degu forebrain

Chapter 4: Developmental underpinnings of social behavior

Table 4.1 Synopsis of developmental milestones in degus, guinea pigs, rats, and mice

Table 4.2 Synopsis of the main separation and isolation procedures in degus

Table 4.3 Mean ± SE % of time spent close to the mother

vs

an unfamiliar female during a social choice test of degus after rearing from postnatal day 21 to 31 in a family group with the mother and littermates, complete isolation, or isolation combined with daily 30-min restricted reunions with the family group through a grid

Chapter 5: Dispersal in caviomorph rodents

Table 5.1 Summary of dispersal patterns in caviomorph rodents

Chapter 6: Mechanisms of social communication in caviomorph rodents

Table 6.1 Communicative characteristics presented by social caviomorph species, classified by communication channel

Table 2 Communicative characteristics presented by solitary caviomorph species, classified by communication channel

Chapter 7: Causes and evolution of group-living

Table 7.1 Species of caviomorph rodents with available information on sociality

Chapter 8: Rodent sociality: a comparison between caviomorphs and other rodent model systems

Table 8.1 Rodent species thought to be social (more than two adults interacting or showing overlapping use of space, nests or burrows) at least during one season or under certain conditions. Species listed as social include animals living in colonies or social groups

Chapter 11: Parent-offspring and sibling-sibling interactions in caviomorph rodents: a search for elusive patterns

Table 11.1 Life history traits of Caviomorph rodents, including levels of precociality as defined in the text: fully, moderately, and least precocial

Chapter 12: Fitness consequences of social systems

Table 12.1 Summary of fitness trends observed in six species of caviomorph rodents

Sociobiology of Caviomorph Rodents

An Integrative Approach

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To Marcela and Erika

Acknowledgments

The editors of this book are highly indebted to former Wiley editor Suzanne Albrecht for her immediate and unconditional support in materializing this editorial project. We also appreciate the positive reception and suggestions to the original project from three anonymous reviewers. Subsequently, all chapters of this book have benefited from the constructive and useful suggestions made by the following colleagues: Sabine Begall, Daniel Blumstein, Robbie Burger, Patrick Gouat, James Hare, Melissa Holmes, Barbara König, John Koprowski, Karen Mabry, Lisa McGraw, Betty McGuire, Peter Meserve, Daniel Olazabal, Steve Phelps, Neville Pillay, Janet Randall, Carsten Schradin, Jane Waterman, and one anonymous reviewer.

Notes on contributors

Annaliese K. Beery (Ph.D., University of California-Berkeley, USA).

Dr. Beery is a neuroendocrinologist with interests in social behavior, stress, and comparative approaches to understanding the brain and behavior.

Joseph R. Burger (Ph.D., University of New Mexico, USA).

Dr. Burger is an evolutionary ecologist with an interest in field and macroecological approaches to studying social behavior and life history in mammals.

Valentina Colonnello (Ph.D., Sapienza University of Rome, Italy).

Dr. Colonnello is a developmental psychobiologist and clinical psychologist. Her research focuses on the formation of social bonds and developmental trajectories, within a cross-species affective neuroscience perspective.

Elizabeth R. Congdon (Ph.D., University of Missouri-St. Louis, USA).

Dr. Congdon is a science educator and behavioral ecologist specializing in natal dispersal and conservation of Neotropical mammals. She has most recently focused her research on capybaras, both in their native range and as a potential invasive species in the southern United States.

Luis A. Ebensperger (Ph.D., Boston University, USA).

Since 1997, Professor Ebensperger's research has focused on the current function and evolution of group-living and cooperation of caviomorph rodents and other mammals.

Gabriel Francescoli (Ph.D., Universidad de la República, Uruguay).

Dr. Francescoli is head of the Ethology Section at the Sciences College, Montevideo, Uruguay. His research interests are related to the evolution of animal communication systems, and to subterranean rodent communication strategies.

Loren D. Hayes (Ph.D., Miami University, USA).

Professor Hayes is a behavioral ecologist with an interest in caviomorph rodent sociality. Since 2005, his primary research focus has been on

Octodon degus

sociality in Chile.

Emilio Herrera (Ph.D., Oxford University, UK).

Dr. Herrera gained his B.Sc. in Biology at Universidad Simón Bolívar in Venezuela in 1980 and then went on to get a D.Phil. in Zoology at Oxford with a thesis on capybara social behavior (1986). After a one-year post doc at the Smithsonian in Panama, he returned to Universidad Simón Bolívar where he is a professor.

Yasmin Kamal (M.D./Ph.D. student, Dartmouth Medical School, USA).

Yasmin is a student at Dartmouth Medical School with an interest in neuroendocrinology and genetics.

Brian Keane (Ph.D., Purdue University, USA).

Dr. Keane is a behavioral ecologist who combines field studies with molecular genetics methods to assess questions regarding social behavior.

Eileen A. Lacey (Ph.D., University of Michigan-Ann Arbor, USA).

Dr. Lacey is a behavioral ecologist specializing in studies of rodent social behavior. Currently, her research focuses on the ecological, evolutionary, and neuroendocrine bases for variation in social structure among tuco-tucos (genus

Ctenomys

) and closely related caviomorph taxa.

Christine R. Maher (Ph.D., University of California-Davis, USA).

Dr. Maher is a behavioral ecologist with a long-term interest in intraspecific variation in social behavior in mammals.

Ruth C. Newberry (Ph.D., University of Edinburgh, UK).

Dr. Newberry is an applied ethologist at the Norwegian University of Life Sciences, specializing in environmental enrichment, social behavior, and animal welfare.

Selene Nogueira (Ph.D., University of São Paulo, Brazil).

Dr. Nogueira is Full Professor in the Department of Biological Science, the coordinator of the Applied Ethology Laboratory at Universidade Estadual de Santa Cruz, Ilhéus–Bahia, Brazil. Her research is dedicated to studying social behavior, animal communication, and animal welfare.

Agustina Novillo (Ph.D., Instituto Argentino de Investigaciones de Zonas Áridas, IADIZA, Mendoza, Argentina).

Dr. Novillo is Assistant Researcher of the National Council for Science & Technology of Argentina (CONICET). Her research has been oriented towards the biogeography and ecology of Andean rodents, with a particular focus on patterns of biodiversity along elevation gradients.

Agustina Ojeda (Ph.D., Instituto Argentino de Investigaciones de Zonas Áridas, IADIZA, Mendoza, Argentina).

Dr. Ojeda is Assistant Researcher of the National Council for Science & Technology of Argentina (CONICET). Her research centers on the study of the patterns and processes that shape the distribution of genetic variation in small desert mammals, particularly in geographically isolated systems, and she uses different approaches, from phylogeography and molecular systematic to genetics landscape.

Ricardo A. Ojeda (Ph.D., Instituto Argentino de Investigaciones de Zonas Áridas, IADIZA, Mendoza, Argentina).

Dr. Ojeda is Principal Researcher of the National Council for Science & Technology of Argentina (CONICET) and his research has been oriented towards the biogeography and ecology of desert mammals, patterns of biodiversity, and the ecological diversification of rodents.

Jaak Panksepp (Ph.D., University of Massachusetts, USA).

Dr. Panksepp is a psychobiologist/neuroscientist whose research during the first half of his career was at Bowling Green State University, OH, and devoted heavily to brain social-emotional systems. He is currently Professor of Neuroscience at Washington State University. He is the author of

Affective Neuroscience

(Oxford, 1998) and

Archaeology of Mind

with Lucy Biven (Norton, 2012).

Cristian E. Schleich (Ph.D., Universidad de Mar del Plata, Argentina).

Dr Schleich is a behavioral researcher whose interests are focused on the behavioral ecology and sensory biology of solitary subterranean rodents, particularly

Ctenomys

.

Raúl Sobrero (Ph.D., P. Universidad Católica de Chile, Chile).

Dr. Sobrero combines ecological and evolutionary perspectives, integrating behavioral, brain anatomy, ecological and phylogenetic studies on wild caviomorph rodents to understand the causes and consequences of animals' responses to physical and social conditions.

Nancy G. Solomon (Ph.D., University of Illinois at Champaign-Urbana, USA).

Dr. Solomon is a behavioral ecologist who has studied small mammal social behavior and reproduction. She has primarily worked with voles in studies conducted in natural populations, semi-natural populations, and laboratory settings.

Zuleyma Tang-Martínez (Ph.D., University of California-Berkeley, USA).

Dr. Tang-Martínez has worked on chemical communication, kin and individual discrimination, dispersal, and social behavior of rodents for approximately 44 years. She supervised E.R. Congdon's research on capybaras (with E. Herrera as field advisor) in her native Venezuela.

Rodrigo A. Vásquez (Ph.D., Oxford University, UK).

The research carried out by Dr. Vásquez is focused on behavioral intra-specific variability at different levels, and the integrative study of behavior, including energetics, endocrinology, and genetics, using small mammals (mainly

Octodon degus

) and birds.

Introduction

Luis A. Ebensperger1 & Loren D. Hayes2

1Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago, Chile

2Department of Biology, Geology, and Environmental Sciences, University of Tennessee at Chattanooga, Chattanooga, TN, USA

I.1 Social behavior of caviomorph rodents and book aims

Social behaviorinvolves the actions directed toward, or in response to conspecifics and the fitness consequences for all individuals involved (Wersinger 2009; Székely et al. 2011). Given that social interactions are diverse in nature and extent, social behavior is similarly diverse. Thus, social behavior encompasses a variety of agonistic (including aggressive) behaviors that result in the establishment of dominance hierarchies and territoriality, but also a similarly diverse array of affiliative interactions. Affiliative interactions takes place in different contexts, including courtship and other sexual interactions that result in mating systems, parent–offspring interactions that result in parental care patterns, or the relatively permanent association of adult conspecifics that result in sociality (or group-living) and different forms of cooperation.

In the late 1990s and early 2000s, some researchers began to argue that generalizations about rodent social behavior were premature due to the lack of information coming from the caviomorph or New World hystricognath rodents, a socially diverse group of South American rodents (Ebensperger 1998; Tang-Martínez 2003). We propose that a greater focus on caviomorph rodents as subject models of social behavior would contribute greatly to collaborative and integrative research on this area. Caviomorph rodents exhibit a diverse range of social behaviors and life history attributes, and are found in a wide range of habitats. Caviomorphs span from solitary living (Adler 2011) to highly social (Herrera et al. 2011), and live in kin-biased (Lacey & Wieczorek 2004) or non-kin biased (Quirici et al. 2011) groups. Some species provide communal care to offspring (Ebensperger et al. 2007) while others attempt to avoid contact with non-descendant offspring held in communal crèches (Taber & Mcdonald 1992; Campos et al. 2001). Mating systems are equally diverse, with some species exhibitingmonogamy and territoriality, while others exhibit polygyny, or promiscuity (Adrian & Sachser 2011). In terms of life history, caviomorph rodents exhibit a mixture of “fast” and “slow” traits; many have long gestation periods and produce small litters of precocial offspring, yet reach sexual maturity at a young age and exhibit low survival (Kraus et al. 2005). High mortality rates effectively make some species (Ebensperger et al. 2013). Finally, caviomorph rodents are ecologically diverse, occurring in habitats such as high and low altitude shrublands, tropical and temperate forests, and coastal areas. Habitats range from arboreal to semiaquatic to subterranean. Numerous species have wide geographical ranges, increasing the potential for social and life history flexibility.

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