Intraspecific variation in space use, group size, and mating systems of caviomorph rodents

Abstract

Intraspecific variation in social systems is widely recognized across many taxa, and specific models, including polygamy potential, resource defense, and resource dispersion, have been developed to explain the relationship between ecological variation and social organization. Although mammals from temperate North America and Eurasia have provided many insights into this relationship, rodents from the Neotropics and temperate South America have largely been ignored. In this review we focus on reports documenting intraspecific variation in spacing systems, group size, and mating systems of caviomorphs. This large group of New World hystricognath rodents occupies a diverse array of habitats; thus, members of the same species potentially exhibit different social systems in response to different ecological conditions. Spatial patterns vary in response to a diverse array of factors, including predation, food availability, population density, and soil characteristics. Changes in group size typically correlate with changes in resource availability, particularly food. Mating systems generally reflect the ability of males to control access to females, which may depend on population density or food distribution. In general, social organization in caviomorphs fits predictions of resource-based models; however, most studies have been purely observational, involving small numbers of animals over short time periods and reporting qualitative rather than quantitative levels of ecological correlates. In future studies the use of molecular techniques and controlled, experimental manipulations can increase our understanding of intraspecific variation in caviomorph social systems. This understudied group of rodents offers excellent opportunities to provide insights into the influence of ecological conditions on behavior such as social systems.

Within a species different populations, and even the same populations at different times, can exhibit variability in social systems, including changes in spatial patterns (Brashares and Arcese 2002; Schradin and Pillay 2005), group sizes (Cochran and Solomon 2000; Lenihan and Van Vuren 1996), and mating systems (Travis et al. 1995). Researchers have attributed this behavioral plasticity to underlying patterns of ecological resources (Emlen and Oring 1977; Lott 1991), and several models have been developed to explain the influence of ecological conditions on social organization (Brown 1964; Clutton-Brock 1989; Emlen and Oring 1977; Jarvis et al. 1994; Johnson et al. 2002; Macdonald 1983; Orians 1969; Slobodchikoff 1984; Verner and Willson 1966; Wittenberger and Tilson 1980). Although many models explain variation in social systems, we focused on those models pertaining to resources that would appear to apply most widely to the New World hystricognath rodents. Some models make similar predictions, making it difficult to distinguish among them. However, these models often focus on different ecological factors producing those outcomes or consider alternative mechanisms. The literature contains numerous examples of empirical tests of these models (Foster and Endler 1999; Lott 1991). To determine the generalities of proposed models we must 1st examine the literature on understudied taxa, including New World hystricognaths.

The classic model of polygamy potential proposed by Emlen and Oring (1977) links ecology to mating systems, positing that ecological constraints limit the degree to which sexual selection can operate. The hypothesis asserts that when critical resources are distributed homogeneously in the environment, few opportunities exist for resource monopolization. Thus, individuals within a population tend to be dispersed evenly and rarely encounter multiple mates. Conversely, heterogeneously distributed resources should lead to some individuals (in mammals, typically males) having the ability to defend resource patches economically (Brown 1964) and ultimately to monopolize female groups (Orians 1969; Verner and Willson 1966). Thus, the model predicts that uniform resource distribution leads to solitary living and monogamy, whereas patchily distributed resources lead to group formation and polygamy (Emlen and Oring 1977; Table 1).

Table 1.

Summary of resource-based models and predicted effects of changes in resources on group size, mating systems, and spatial organization.

Model	Ecological variable to increase	Change in group size	Change in mating system	Change in home-range features	Advantage to sociality	References
Polygamy potential	Spatial distribution of resources	Increase	Monogamy → polygamy	Group defends 1 high-quality patch	Increase access to additional mates or resources	Emlen and Oring (1977)
Habitat-variability mating system model = resource defense	Patchiness and quality of resources	Increase	Monogamy → polygyny	Home-range size increases and group defends multiple high-quality patches	Increase access to high-quality resources	Slobodchikoff (1984); Travis et al. (1995)
Female dispersion– male behavior	Abundance and quality of food	Increase	Monogamy → polygyny	Home-range size decreases	Increase access to mates (for males)	Brashares and Arcese (2002)
Resource dispersion	Temporal and spatial heterogeneity, richness, and dispersion of resources	Increase	Not applicable	Home-range size increases	Neutral	Johnson et al. (2002); Macdonald (1983)

Similarly, the habitat-variability mating system model (also referred to as resource defense—Slobodchikoff 1984) suggests that in some species individuals must form groups to defend patches of high-quality resources. Thus, the habitat-variability mating system model distinguishes differences in how resource distribution and quality influence mating systems. It predicts that low-quality, uniformly distributed resources lead to monogamy; high-quality resources distributed in patches result in polygyny. The primary difference between the habitat-variability mating system model and the model of Emlen and Oring (1977) is territory size in relation to high-quality resource patches. The habitat-variability mating system model predicts that polygynous groups form to defend several resource patches that solitary individuals could not defend; the model of Emlen and Oring predicts that a single social group occupies a single, high-quality resource patch in a heterogeneous environment (Table 1). Therefore, the habitat-variability mating system model predicts that a territory in heterogeneous habitats will be large enough to defend multiple resource patches; the model of Emlen and Oring suggests that the territory of a group encompasses only 1 high-quality patch.

The basic premise provided in resource-based models of social organization is that when resources are distributed heterogeneously through space and time, opportunities arise to monopolize those resources (Emlen and Oring 1977). Brashares and Arcese (2002) followed this logic in their female dispersion–male behavior hypothesis, suggesting that food resources are linked to female dispersion and subsequently to male space use (Table 1). Their model assumes that females range the minimum distance necessary to meet nutritional requirements. Male behavior is determined not by food availability but by the dispersion of potential mates (Emlen and Oring 1977; Ostfeld 1985). As food abundance and quality increase, home-range sizes decrease and female group sizes increase. Males then can monopolize stable female groups by defending territories that encompass the ranges of multiple females (resource defense polygyny—Clutton-Brock 1989) or by defending female groups themselves (female defense polygyny—Clutton-Brock 1989). In contrast, scarce and low-quality food leads to smaller female group size and larger home ranges for females to meet energetic needs, ultimately resulting in solitary females occupying large areas. However, when the distribution of critical resources is sparse and patchy, females are hyperdispersed on small territories, resulting in the defense of single females by solitary males (Komers and Brotherton 1997; Ostfeld 1985). Regardless of resource heterogeneity, when critical resources are scarce, opportunities rarely arise for males to encounter and defend multiple females effectively, leading to solitary males guarding single females (female defense monogamy—Clutton-Brock 1989).

A final model, the resource dispersion hypothesis, distinguishes differences in how resource patchiness and richness (quality) influence sociality and spacing systems (Johnson et al. 2002; Macdonald 1983; but see Revilla 2003). Social group size is not necessarily correlated with territory size but is influenced by resource heterogeneity and richness, whereas territory size is influenced primarily by the dispersion of resources (i.e., distance between resource patches). The resource dispersion hypothesis predicts that as resources become temporally or spatially clumped, or as patch richness or variability increases, social group size increases. As the dispersion of resources increases spatially or temporally, territory size also should increase (Table 1).

Rodents have served as model organisms in furthering our understanding of how ecological conditions can influence social organization (Armitage 1999; Ebensperger 2001; Hare and Murie 2007; Lacey and Sherman 2007; Solomon 2003; Waterman and Fenton 2000). However, such studies have focused primarily on a relatively small subset of taxa, particularly North American or Holarctic species. The New World hystricognath rodents, also known as caviomorphs, include capybaras (Hydrochoerus), cavies (family Caviidae), pacas (Dasyprocta), and agoutis (Cuniculus). This group offers additional insights into ways in which ecological conditions affect social organization. Several previous reports on this group have used interspecific comparisons to investigate links between ecological variables and social systems (Asher et al. 2008; Ebensperger and Blumstein 2006; Ebensperger and Cofré 2001; Trillmich et al. 2004). However, our understanding of these effects can be hampered by phylogeny. Recently, systematists have published caviomorph phylogenies that will facilitate interspecific comparisons of social organization (Honeycutt et al. 2003; Huchon and Douzery 2001; Rowe and Honeycutt 2002). By studying intraspecific variation we can reduce problems associated with phylogenetic inertia (Harvey and Pagel 1991; Lott 1991).

In this review we surveyed the literature for reports of intraspecific variation in social organization within cavio-morph rodents. Specifically, we included papers in which authors discuss specific ecological conditions that might affect such variation. Social organization results from relationships produced from social interactions among conspecifics (Hinde 1976, 1983). Thus, such organization includes several facets of the lives of animals, including space use, the size of the group to which they belong, and form of mating relationships. First, we describe variation in spacing systems; that is, the temporal and spatial pattern of distribution of members of a species, because spatial distribution of individuals forms the basis for social interactions within a population (Emlen and Oring 1977; Lacey 2000). We did not find cases of change in spacing systems, although we do not know if the absence of studies is due to the lack of an effect or simply to a lack of data in this area. However, several authors describe changes in home-range size that correlate with differences in ecological variables, and thus we include them here. Next, we examine group size and mating systems, which result from particular spatial distributions of males and females (Brashares and Arcese 2002; Emlen and Oring 1977; Slobodchikoff 1984). Finally, we offer some recommendations for future work regarding the links between resources and intraspecific variation in social organization in this relatively understudied taxon (Ebensperger 1998; Hayes et al. 2011 [this issue]; Tang-Martínez 2003).

Spacing Systems

In general, predation risk and distribution or availability of food resources are the most commonly reported correlates of variation in space use in caviomorphs (Table 2). However, few studies report actual changes in spatial organization; that is, shifts from 1 spacing system to another, either within the same population or across different populations. Only 1 author describes such a transition, which involved domesticated guinea pigs (Cavia porcellus—Sachser 1986). At low density (4 males and 4 females housed in a 7.8-m² enclosure) males organize themselves into a linear dominance hierarchy. However, at high density (12 males and 12 females in the same enclosure) males change spatial organization, with 2 or 3 males establishing nonoverlapping territories that they defend against other males, some of which defend females rather than space. Furthermore, some territorial males tolerate other males in the area as long as they do not court females (Sachser 1986). Based on previous work, such a shift at higher density was surprising because higher intruder pressure can increase the costs of maintaining exclusive access to resources relative to the benefits (Brown 1964). However, the artificial nature of the study could have affected results. Alternatively, perhaps the higher density still represents an overall intermediate density such that territorial males accrued sufficient benefits that outweighed costs of defense.

Table 2.

Intraspecific variation in home-range characteristics and ecological correlates associated with changes in caviomorph space use.

Species	Home-range characteristic	Ecological correlate	Habitat	References
Cavia porcellus	Shift from dominance hierarchy to territoriality	Population density	Captivity	Sachser (1986)
C. aperea	Shift in usage	Predation risk	University of São Paulo campus	Asher et al. (2004)
C. magna	Overlap, size, shift in core area	Water level (direct), population density (indirect)	Wetland surrounded by grassland	Kraus et al. (2003)
Proechimys semispinosus	Overlap, size	Population density	Tropical moist forest	Endries and Adler (2005)
Cuniculus paca	Size, shift in core area	Food availability	Tropical lowland wet forest	Beck-King et al. (1999)
Dasyprocta leporina	Size, shift in core area	Food availability	Stands of Brazil nuts; transitional forest between rain forest and savannah	Jorge and Peres (2005); Silvius and Fragoso (2003)
D. punctata	Size	Food availability	Tropical moist and semideciduous forest	Aliaga-Rossel et al. (2008)
Ctenomys talarum	Distribution	Population density, environmental heterogeneity	Grassland coastal dunes	Busch et al. (1989); Malizia (1998); Pearson et al. (1968)
	Size	Soil characteristics		Cutrera et al. (2006)
Octodon degus	Size	Predation or population density	Mediterranean thorn scrub	Lagos et al. (1995)
		Predation, food availability	Scrubland	Hayes et al. (2007)
		Food abundance, quality	Scrubland	Quirici et al. (2010)

Two studies report changes in home-range characteristics in cavids living under more-natural conditions, although they do not describe shifts from 1 type of spacing system to another. In the wild (or Brazilian) guinea pig (Cavia aperea), animals respond to increased vegetation height by shifting their core home ranges to these areas of greater cover, resulting in decreased exposure to predators (Asher et al. 2004). Such changes last only 1–2 weeks or <2 months and involve either individuals (n = 5) or small groups of 2 or 3 animals (total of 7 animals). Once these areas were mowed, resulting in reduced cover, animals returned to their original ranges. Such a shift in space use also occurs in response to flooding, with animals moving to dry ground (Asher et al. 2004).

A related cavid, the greater guinea pig (Cavia magna), also responds to changes in water level by altering home-range size (Kraus et al. 2003). High water effectively increases population density by forcing animals into smaller areas. Like Brazilian guinea pigs, greater guinea pigs move home ranges and also exhibit greater amounts of home-range overlap as water levels rise and thus population density increases. Results vary, however, depending on how the authors measure home-range area. Nonetheless, regardless of environmental conditions, these animals never exhibit stable home ranges, as evidenced by cumulative area curves never reaching a plateau (Kraus et al. 2003). Even at low density and low water levels greater guinea pigs exhibit large amounts of home-range overlap and no signs of territoriality.

Total home-range size differs between wet and dry seasons in Tome’s spiny rats (Proechimys semispinosus). Animals use larger home ranges during the wet season when resources are abundant and breeding occurs, with animals covering larger areas to locate mates; however, core home-range size does not change with season (Endries and Adler 2005). Furthermore, Tome’s spiny rats increase the amount of home-range overlap during the wet season, which correlates with reproductive activity (Endries and Adler 2005). To explain this unusual pattern of home-range sizes increasing with increased food abundance the authors suggest that population density instead of food abundance drives changes in total home-range size. During the dry season population density increases, leading to smaller home ranges (Endries and Adler 2005).

Among paca and agouti species researchers report that food availability correlates with changes in home ranges, but sample size was small and study duration short. Beck-King et al. (1999) radiotracked 1 female lowland paca (Cuniculus paca) over a total of 26 nights and found that she shifted her home range and decreased home-range size as trees stopped fruiting in 1 area and other fruits became available elsewhere.

Similarly, red-rumped agoutis (Dasyprocta leporina) reduce home-range size as fruit availability increases and shift their ranges to overlap fruiting trees (Jorge and Peres 2005; Silvius and Fragoso 2003). Sample sizes were small, however; 1 study followed 3 females, and the other sampled 5 animals. Finally, another study of red-rumped agoutis reports high amounts of home-range overlap for 9 radiocollared males and females and describes smaller home ranges at Barro Colorado Island, Panama, than in other areas, perhaps in response to greater food availability (Aliaga-Rossel et al. 2008).

Different ecological correlates can affect spatial patterns in tucotucos (Ctenomys talarum). Tucotucos living in a heterogeneous environment and at low density (13–65 individuals/ha) show a clumped distribution (Busch et al. 1989; Malizia 1998), whereas a higher density of 207 individuals/ha correlates with evenly spaced individuals (Pearson et al. 1968). Another study suggests that soil characteristics are responsible for differences in home-range size, with softer, less-humid soils correlating with larger ranges because of lower energetic costs associated with digging (Cutrera et al. 2006).

Three studies report on changes in home-range characteristics associated with ecological conditions in degus (Octodon degus). One report represents the only project to manipulate environmental conditions and compare space use experimentally. Using predator exclusions and fluorescent tracking powder, Lagos et al. (1995) document smaller daily home ranges in predator-free areas compared to areas with predator access. The authors surmise that without the risk of predation degus concentrate foraging activity in smaller patches with more-abundant food. However, population density is a confounding factor, because predator-excluded areas also experience higher population density, which can restrict home ranges (Lagos et al. 1995).

In another study of degus home-range size increases and animals use more burrows as distance from cover and amounts of shrub cover increase, presumably reflecting greater predation risk (Hayes et al. 2007). However, food is more abundant farther from cover, perhaps because animals prefer to feed near cover, which reduces food availability there, forcing them to move greater distances to secure adequate resources (Hayes et al. 2007).

Finally, food availability correlated with home-range size of degus in one year but not another (Quirici et al. 2010), probably due to differences between years in sample size (n = 7 and 19), although ecological factors also might have changed between years. During the austral summer food abundance and quality, measured as amount of insoluble fiber, decline. Home-range sizes then increase compared to winter, despite an increase in population density related to the influx of juveniles born into the population (Quirici et al. 2010). The authors suggest that lower abundance of food resources and higher density increase competition, forcing animals to expand ranges to obtain adequate food (Quirici et al. 2010).

Reports of changes in home-range characteristics indicate that ecological conditions impact space use. However, many published studies either present limited data from a small number of animals, took place over a short time period, or both. Furthermore, researchers often use different techniques to obtain spatial data (e.g., radiotelemetry, direct observations, and fluorescent tracking) and estimate home-range sizes with different methods (e.g., minimum convex polygons, grid cells, fixed kernels, and excavated burrows). Such variation clearly hampers comparison across populations.

Nevertheless, similarities emerge across studies. As expected, predation levels, population density, and food availability correlate with spatial patterns of caviomorphs. Increased predation risk is related to larger home ranges, and increased food resources and population density usually are associated with smaller home ranges. Given the secretive nature of these animals, logistical difficulties associated with trapping and tracking, and small sample sizes, we still know relatively little about spacing systems of these species. However, ecological conditions often vary spatially and temporally, thus providing opportunities to examine shifts in spacing patterns of individuals seasonally and across geographic distances that exhibit variable resource availability. Although authors report changes in home-range characteristics, many of them do not describe spatial organization as such; that is, positions of these populations along the continuum between undefended home ranges and territoriality (Asher et al. 2004; Endries and Adler 2005; Quirici et al. 2010). Such characterization requires longer-term studies of neighboring animals to record amounts of home-range overlap and, ideally, to observe behavioral interactions.

Group Size

Researchers have described changes in group size in 6 species of caviomorphs: pacas, plains vizcachas (Lagostomus maximus), maras (Dolichotis patagonum), capybaras (Hydrochoerus hydrochaeris), lesser cavies (Microcavia australis), and degus. In the majority of these cases resource availability or distribution correlates with varying group size (Table 3). Generally, the authors relate changes in group size to direct or indirect changes in food abundance, except in capybaras where the important resource is water availability. Additionally, changes in social group size of degus appear to reflect variation in predation risk due to differences in habitat structure.

Table 3.

Ecological correlates of intraspecific variation in group size in caviomorph species.

Species	Ecological correlate	Habitat	References
Cuniculus paca	Food abundance	Lowland wet tropical forest	Beck-King et al. (1999)
Lagostomus maximus	Food abundance, predation	Semiarid scrub	Branch et al. (1993)
Dolichotis patagonum	Food abundance, distribution	Semiarid thorn scrub	Taber and Macdonald (1992)
Hydrochoerus hydrochaeris	Water availability, population density	Tropical floodplain savanna; seasonally flooded grassland	Herrera and Macdonald (1987, 1989); Herrera et al. (2011 [this issue]); Schaller and Crawshaw (1981)
Microcavia australis	Climate severity, food abundance, quality	Desert	Taraborelli and Moreno (2009)
Octodon degus	Habitat structure, predation	Scrubland	Ebensperger and Wallem (2002)

In pacas the authors anecdotally report seeing as many as 5 unmarked animals feeding in a localized area, and they attribute such grouping to high food abundance occurring in a tropical lowland wet forest reserve in Costa Rica (Beck-King et al. 1999). Unfortunately, information about kinship, age, or sex is unknown because animals were not marked.

Alternatively, during times of food scarcity animals may also congregate. One study of plains vizcachas in Argentina reports that adult females and subadults transfer to other social groups, perhaps to accrue antipredator benefits associated with larger group size. During this study population size declined due, in part, to a drought, and small groups fused to form larger groups (Branch et al. 1993). Similarly, maras studied in a semiarid habitat in Argentina increase group size during the dry season as they concentrate on lagoons or sheep stations; that is, areas distributed in patches that contain water and more-abundant, nutritious food (Macdonald et al. 2007). However, groups consisting of >2 animals do not persist, dispersing after a few hours (Taber and Macdonald 1992).

Capybaras also form larger groups in seasonal habitats and at higher population density. In Venezuela group size is related to the area of bancos, habitats characterized by tall grasses and shrubs that rarely flood and thus provide refuges of dry ground during the rainy season (Herrera and Macdonald 1989). Capybaras living in the Pantanal of Argentina and in Venezuela form larger groups during the dry season, as ponds shrink and become more patchily distributed, leading to increased population density (Herrera and Macdonald 1987; Herrera et al. 2011 [this issue]; Schaller and Crawshaw 1981). Like maras, however, these groups are not cohesive. In the Pantanal animals minimize contact by spacing themselves apart in the smaller area where they have good visibility across pastures (Schaller and Crawshaw 1981). Similarly, capybara groups in the Pantanal could be considered short-term aggregations because smaller subunits retain their identities. When the dry season ends, the original groups, with their original members, form again (Herrera and Macdonald 1987).

Lesser cavies form larger groups in an area experiencing harsher climate; that is, wide temperature fluctuations and arid and cold conditions (Taraborelli and Moreno 2009). However, climate also affects food resources, and animals thus encounter lower-quality, less-abundant food under more-severe climatic conditions. Although larger groups might increase competition for scarce resources, the authors propose that larger groups facilitate social thermoregulation (Taraborelli and Moreno 2009).

Finally, factors other than resources can impact group size. Degus living in exposed habitats form larger foraging groups than those living in covered microhabitats (Ebensperger et al. 2006; Ebensperger and Wallem 2002). Additionally, degus in larger groups increase collective vigilance and detect a human predator at farther distances, and they escape to refugia at a greater distance from predators than do individuals of smaller groups (Ebensperger and Wallem 2002). Thus, predation risk may favor larger groups.

Studies of capybaras and lesser cavies involved at least some marked individuals, which allowed researchers to notice that animals did not mix in their larger groups. However, studies on other species often involved unmarked individuals or a small number of animals. Nonetheless, in most cases, increased group size was associated with decreased resources—either food or water—and animals came together as food or water decreased or became more patchily distributed. These results support several hypotheses that predict larger groups as resource distribution becomes more spatially and temporally clumped (Emlen and Oring 1977; Johnson et al. 2002; Slobodchikoff 1984). On the contrary, at the opposite end of the continuum pacas encountered abundant food that enabled them to feed in larger groups, presumably because of reduced competition for resources. Results from pacas support the resource defense and the female dispersion–male behavior hypotheses, which both predict that abundant resources lead to increased group size (Brashares and Arcese 2002; Slobodchikoff 1984); however, the authors do not provide information about resource distribution, precluding evaluation of the resource dispersion hypothesis in this species.

Many caviomorph rodents experience seasonal or annual variation in ecological conditions, and such changes should predictably alter the costs and benefits of group living. Thus, this taxon can provide insights not only into these potential costs and benefits but also the mechanisms by which they result in changes in group size.

Mating Systems

Variation in mating systems has been reported within 3 species of caviomorphs, guinea pigs, southern bamboo rats (Kannabateomys amblyonyx), and Tome’s spiny rats (Table 4). Such variation is linked to differences in population density or food distribution.

Table 4.

Ecological correlates of variable mating systems in caviomorphs.

Species	Mating systems	Ecological correlate	References
Proechimys semispinosus	Monogamy, promiscuity	Population density	Endries and Adler (2005)
Cavia aperea	Monogamy, polygyny	Population density, food distribution	Asher et al. (2004)
Kannabateomys amblyonyx	Social monogamy, polygyny	Food distribution	Silva et al. (2008); Stallings et al. (1994)

Domestic guinea pigs, studied in captivity, display polygyny. However, males respond to an increase in housing density by changing strategies and switch from female defense to resource defense polygyny (Sachser 1986). At low density (4 males and 4 females) the dominant male can monopolize access to females (female defense polygyny) and secure most copulations by displacing other males. However, at higher densities (12 males and 12 females) more males can defend females, and more males copulate (Sachser 1986). In addition, males may maintain territories (as described above under “Spacing Systems”), thus displaying resource defense polygyny (Sachser 1986).

Population density also can affect the mating system of spiny rats, which appears to vary from promiscuity to social monogamy (Endries and Adler 2005). High density and larger home ranges in males can correlate with promiscuity (Endries and Adler 2005); however, the authors base conclusions about mating systems using indirect spatial patterns compiled from radiotelemetry data and not direct behavioral observations or molecular evidence. Given the need to distinguish between social and genetic mating systems, spatial data alone are no longer sufficient to describe mating systems.

Another study focused on a population of wild guinea pigs located on the campus of the University of São Paolo, Brazil (Asher et al. 2004). The authors reported both socially monogamous pairs and polygynous groups of 1 male with 2 females. They attributed monogamy to low population density (12.5 individuals/ha) and inability of males to monopolize >1 female. In turn, they proposed that uniform distribution of food precludes group formation in females. Because females are more dispersed, males cannot monopolize them. The authors also observed shifts between social monogamy and polygyny but did not describe the circumstances associated with those changes.

Southern bamboo rats vary between polygyny and social monogamy, and such variation correlates with food distribution (Silva et al. 2008; Stallings et al. 1994). As obligate bamboo specialists, bamboo rats feed exclusively on bamboo stems and leaves (Stallings et al. 1994). Homogeneously distributed bamboo (Bambusa tuldoides) stands are associated with high population densities and polygyny among bamboo rats (Stallings et al. 1994), presumably because males can secure access to >1 female. When bamboo stands are sparse and distributed in patches, females occur at low densities and occupy small, hyperdispersed territories (Silva et al. 2008). Thus, single males defend solitary females (Komers and Brotherton 1997; Ostfeld 1985), resulting in social monogamy (Silva et al. 2008).

As noted in other species (Davies 1986; Iossa et al. 2009), variation in mating systems of caviomorphs reflects the ability to monopolize access to mates. Furthermore, access to mates depends on resource distribution, which supports the resource-based models (Brashares and Arcese 2002; Emlen and Oring 1977; Johnson et al. 2002; Slobodchikoff 1984; Table 1). However, different patterns of distribution can lead to the same mating system in different species. In guinea pigs uniform distribution leads to social monogamy (Asher et al. 2004), whereas in southern bamboo rats it leads to polygyny (Silva et al. 2008; Stallings et al. 1994). One difference lies in population density. Uniform distribution of abundant food results in high densities among southern bamboo rats, which specialize on that food source. Yet, uniform distribution of food leads to a low population density in a more generalist species such as the guinea pig. Thus, population density, rather than food distribution, might influence mating system more strongly. The resource defense hypothesis considers both resource distribution and population density, and it predicts that distribution plays a larger role than population density (Travis et al. 1995). Thus, experimental manipulations of species experiencing different patterns of resource distribution and population density, while holding the other variable constant, could provide critical tests of these models.

Finally, although authors describe shifts between monogamy and either promiscuity or polygyny, they usually do not distinguish between genetic and social monogamy. Molecular techniques can verify whether animals produce offspring with multiple partners, but only 1 study examined paternity, and only for 2 juveniles from 2 groups (Asher et al. 2004). Such techniques can help to document variation in the genetic mating systems of caviomorphs.

Recommendations for Future Studies

A morphologically and physiologically diverse taxon (Mares and Ojeda 1982; Redford and Eisenberg 1992), caviomorphs also exhibit behavioral diversity. They occupy a range of habitats and ecological conditions across Central and South America, resulting in behavioral plasticity and extensive variation in social organization (Ebensperger and Cofré 2001; Lacey and Ebensperger 2007; Lacher 1981; Redford and Eisenberg 1992; Trillmich et al. 2004). Thus, caviomorph rodents present opportunities to increase our understanding of the evolutionary and ecological mechanisms that influence intraspecific variation in social organization. Populations within species experience different ecological conditions, often seasonally. Some species occupy narrow ranges, whereas other species are more broadly distributed. Thus, the potential for behavioral flexibility is high, particularly in species with broad distributions. From the reports briefly summarized here, several species display behavioral plasticity in spatial organization, group size, and mating system. Such variation correlates with variation in ecological conditions, particularly food abundance and distribution but also predation and population density. In addition to environmental variables, factors intrinsic to the organism, such as kinship (Travis et al. 1995), influence social systems; however, to our knowledge, factors such as kinship have not been examined in caviomorphs. For these reasons caviomorphs represent excellent model systems. We conclude by proposing some future directions for research.

Use of molecular techniques

Just 4 studies have reported intraspecific variation in mating systems in caviomorphs (Table 4), and only 1 (Asher et al. 2004) used molecular techniques. These studies correlated ecological changes with variation in mating systems ranging from monogamy to multimate systems. However, because it is estimated that <10% of mammals are monogamous (Kleiman 1977), these studies should be viewed with caution. Whenever possible, molecular markers such as microsatellite primers (e.g., tucotucos [Lacey et al. 1999], degus [Quan et al. 2009], and corurus [Spalacopus cyanus—Schroeder et al. 2000]) should be used to determine maternity and paternity and measure direct and inclusive fitness, increasing our understanding of the links between environmental variation and social and mating systems in caviomorph rodents (Hayes et al. 2011 [this issue]).

Additionally, a key element in intraspecific studies involves distinguishing between genotypic variation as a result of adaptation to local environments and behavioral plasticity where changes in phenotype (rather than genotype) occur in response to varying local conditions. Molecular techniques can provide population-level phylogenies to determine candidate species that occur across environmental gradients for comparative studies. Spatially, this issue can be overcome by identifying variation in social organization among contiguous subpopulations of the same species occurring across an environmental gradient (Brashares and Arcese 2002) or by comparing populations of the same species inhabiting quite different environments (L. A. Ebensperger, Pontificia Universidad Católica de Chile, pers. comm.; L. D. Hayes, University of Louisiana at Monroe, pers. comm.; E. A. Lacey, University of California, Berkeley, pers. comm.; Schradin and Pillay 2005; Travis and Slobodchikoff 1993; Travis et al. 1995).

Experimental manipulation

Through the use of controlled experiments we can discriminate between causal and correlative effects of ecological conditions on social systems. Replicated experimental manipulations can provide insight into links between habitat variability and social organization within the same population (Ims 1987; Slobodchikoff 1984). Additionally, many caviomorphs live in dynamic environments with seasonal rainfall leading to variation in resource availability, quality, and abundance, which provide additional opportunities to test the temporal links between resources, habitat, and sociality.

Testing the predation risk hypothesis

Although we focused primarily on resource-based models to explain plasticity in social behavior, an alternative, non–resource-based hypothesis is predation risk (Ebensperger 2001). Previous interspecific comparisons have failed to demonstrate that social group size is related to predation risk across caviomorphs (Ebensperger and Blumstein 2006; Ebensperger and Cofré 2001). However, we found several examples of this relationship within species such as degus, plains vizcachas, and guinea pigs, which suggests that intraspecific variation in predation risk leads to plasticity in social group size and space use (Asher et al. 2004; Branch et al. 1993; Ebensperger and Wallem 2002; Hayes et al. 2007). Therefore, the predation risk hypothesis may be worthy of study as a primary driver of group formation and intraspecific variation in space use in caviomorphs.

The predation risk hypothesis suggests that sociality enhances predator detection (Hoogland 1981; Kenward 1978; Uetz et al. 2002) or group defense (Alexander 1974; Duffy et al. 2002; Pulliam 1973; van Schaik 1983). Additionally, simple dilution of per capita predation risk can drive social group formation (Krause and Godin 1995; Watt and Chapman 1998; Watt et al. 1997). Although predation risk likely has little effect on plasticity in mating systems, several predictions stem from predation-related hypotheses that address changes in group size and space use. The habitat structure hypothesis suggests that open habitats lead to increased predation pressure, resulting in increased group sizes and home ranges (Brashares and Arcese 2002). Conversely, more-structured habitats should drive solitary living on small home ranges because of the advantages of protective cover and familiarity with refuges. Predation risk likely varies temporally and spatially and thus may influence social organization more strongly at the intraspecific than interspecific level.

The resource, habitat, and predation model of sociality (Brashares and Arcese 2002) incorporates components of resource-based and predation risk models. However, connections between the effects of predation risk and resource distribution on social organization remain unclear, and hypotheses contradict each other. Thus, future studies should test the influence of resources and predation risk on social organization simultaneously to tease out these discrepancies. Interspecific comparisons of caviomorph species did not support some predation risk models (Ebensperger and Cofré 2001); therefore, further research may determine if this group differs in important ways from temperate zone species and provides independent tests of hypotheses formulated for temperate zone species (Ebensperger 1998, 2001).

Testing the habitat saturation hypothesis

Several studies suggest that population density can influence variation in social organization (Asher et al. 2004; Busch et al. 1989; Cutrera et al. 2006; Endries and Adler 2005; Kraus et al. 2003; Lagos et al. 1995; Sachser 1986). The habitat saturation hypothesis suggests that population density in relation to ecological limitations can affect social organization and space use (Koenig and Pitelka 1981; Komdeur 1992). For example, social group formation increases and territory size decreases as population density increases in prairie voles (Microtus ochrogaster—Lucia et al. 2008). High-density populations of southern bamboo rats correlate with polygynous mating (Stallings et al. 1994), whereas social monogamy is related to low population densities (Silva et al. 2008). In degus population density appears to have no effect on social group size (Ebensperger et al. 2011 [this issue]). However, areas of degu home ranges increase at higher population density, although it is unclear whether this change is related directly to population density or to food availability (Quirici et al. 2010). Thus, population density may interact with other ecological variables, and future studies should carefully control for effects of density or other ecological factors.

Future studies could systematically examine populations living in different areas and follow known individuals over extended time periods, such as 1 year or more. Researchers also should attempt to quantify ecological variables rather than relying on qualitative terms such as “high” and “low.” Moreover, experimental manipulation of ecological resources (Slobodchikoff 1984) and population density (Lucia et al. 2008) can clarify effects of different variables and demonstrate causation. Although caviomorph social behavior is challenging to study, given that many species are nocturnal, semifossorial, or occupy densely vegetated habitats, modern technologies can facilitate efforts of researchers to learn more about this topic. These animals represent a vast resource that can provide insights into the role of ecological conditions in shaping social organization and tests of ideas formulated in other taxa.