Spacing patterns and social mating systems of echimyid rodents

Author(s) :Gregory H. Adler Source: Journal of Mammalogy, 92(1):31-38. 2011. Published By: American Society of Mammalogists DOI: URL: http://www.bioone.org/doi/full/10.1644/09-MAMM-S-395.1

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Journal of Mammalogy, 92(1):3138, 2011

Spacing patterns and social mating systems of echimyid rodents

GREGORY H. ADLER*
Department of Biology and Microbiology, University of WisconsinOshkosh, Oshkosh, WI 54901, USA * Correspondent: adler@uwosh.edu Echimyid rodents are widely distributed and abundant throughout most of the Neotropics. I review the available information on spacing patterns and mating systems and develop a general framework for understanding variation among populations and species. In most studied species males have larger home ranges than do females, and overlap with either sex can range from 0% to nearly 100%. Males typically display more overlap with both other males and females than do females. Although lack of overlap has been interpreted as territoriality, most such cases have been from populations at low densities. Individuals of those same species show considerable overlap at higher densities. I suggest that individuals typically are not territorial but instead merely space themselves out when vacant space is abundant. Individuals are then facultatively monogamous because multiple mates are not available. As densities increase male home ranges overlap more simply because their home ranges are larger than those of females. Males then can acquire multiple mates, and polygyny becomes evident. At the highest densities multiple mates are available for both males and females, and promiscuity results. The mating system within a given population of many echimyids therefore depends upon density, which in turn is determined primarily by resource availability.
Key words: Echimyidae, home range, mating systems, social systems, spacing patterns

E 2011 American Society of Mammalogists

DOI: 10.1644/09-MAMM-S-395.1

Spacing patterns of individuals and the mechanisms that maintain them have important implications for populationlevel processes (Mares et al. 1982). If individuals (whether males, females, or both sexes) actively maintain territories, other individuals will be excluded from territories. Because only a certain number of territories will fit into a given area, the entire population will be limited and most likely regulated by density-dependent processes (Wolff 1985). Social spacing mitigates intraspecific competition and increases fitness by decreasing the costs incurred from encounters with conspecifics (Wilson 1975). Determining the mating system of cryptic mammals such as many rodents can be difficult, but spacing patterns also directly influence the mating system of individuals within a population (Ostfeld 1985). Because of the relationship between spacing patterns and mating systems, such patterns therefore frequently are used to infer the mating system of individuals within a given population. However, genetic mating systems of mammals frequently differ from social mating systems (Lin et al. 2009), and spacing patterns typically reveal only social mating systems. A substantial body of theory is available for formulating testable predictions of mating systems. Many factors can influence space use by individuals, including predation, food resources, moisture regimes, habitat heterogeneity, and
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population density (Brashares and Arcese 2002; Ostfeld 1990). Of critical importance are the spatial and temporal distributions of resources that are necessary for adult males and females, sex-specific differential use of such resources, and the temporal distribution of potential mates (Emlen and Oring 1977; Ostfeld 1985, 1990). These factors presumably determine the spacing patterns of males and females, which then influence mating systems. For rodents Ostfeld (1990) suggested that resource abundance, distribution, and renewal rate influence the spacing patterns of females. Females of species that rely on slowly renewing food resources distributed in patches, such as fruits and seeds, most likely will be territorial (Ostfeld 1990). Under this scenario spacing patterns of males will be determined directly by spacing of females rather than by resource distribution. In the case of territorial females relying on resources distributed in patches, males are hypothesized to be nonterritorial, resulting in polygyny (Ostfeld 1990). Because rodents live under various environmental conditions and use different resources, they display a remarkable diversity of

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mating systems, ranging from monogamy to promiscuity (Lott 1991). Mating systems can vary even among populations of a given species, depending upon environmental conditions, population density, and mate availability (Lott 1991). Although spacing patterns and both social and genetic mating systems of many temperate rodents have been studied, those of tropical rodents remain poorly known. In this paper I summarize the available information on spacing patterns and social mating systems of the echimyids, which are widely distributed in the Neotropics and whose general ecology, at least for some species, is well known. I also make some general predictions concerning social mating systems of species that have not been studied sufficiently and develop a simple conceptual model to facilitate such predictions. However, the purported mating systems discussed in this review are merely inferences based largely upon spacing patterns. Genetic data are sorely needed to determine actual mating systems of echimyid rodents by identifying paternity. Furthermore, mating pattern rather than mating system may be a more appropriate designation for a particular population at a given time because of the spatial and temporal flexibility in social spacing apparently demonstrated by many echimyids.

ECHIMYIDS AND THEIR ENVIRONMENTS

Genera and distributions.The family Echimyidae (the Neotropical spiny rats) is distributed from northern Central America to southern Argentina. Hoplomys includes a single terrestrial species, H. gymnurus (the armored rat), confined to the northern Neotropics. Proechimys (the spiny rats) includes at least 25 named terrestrial species distributed widely from Honduras to northern Argentina (Woods and Kilpatrick 2005). Trinomys (the Atlantic spiny rats) includes 11 terrestrial species restricted to eastern Brazil (Lara et al. 1996; Lara and Patton 2000). The taxonomy of these rodents has long been confused, and all 3 genera have been placed variously within Proechimys. The 3 recognized terrestrial species of Thrichomys are found in southern Brazil and Paraguay (Freitas et al. 2008). Other terrestrial echimyids have not been studied with respect to spacing patterns and mating systems (e.g., Carterodon and Clyomys) or are extinct (e.g., Boromys, Brotomys, and Heteropsomys) and will not be included here. Among arboreal echimyids only Kannabateomys amblyonyx (the southern bamboo rat) has been studied with respect to its spacing patterns and mating system (Silva et al. 2008; Stallings et al. 1994). This rodent is found in southern Brazil, Paraguay, and northeastern Argentina (Stallings et al. 1994). Arboreal forms in other genera (e.g., Dactylomys, Diplomys, Echimys, Isothrix, Makalata, and Mesomys) are sometimes common and widely distributed (Emmons and Feer 1990), but information on spacing patterns and mating systems is lacking. Accordingly, among the arboreal echimyids I include in this discussion only K. amblyonyx. Myocastor coypus (the coypu or nutria) recently has been moved to Echimyidae (Galewski et al. 2005; Leite and Patton 2002). Coypus are the largest members of the family and are

distributed widely in southern South America. I also include this species in my discussion of echimyid mating systems. Habitats and diets.Echimyids occupy a variety of habitats, including lowland forests, grasslands, drier habitats such as caatinga and semiarid sand dunes, and marshes and other aquatic systems (Emmons and Feer 1990). The terrestrial forest echimyids include the genera Hoplomys and Proechimys and several species of Trinomys. These rodents are often the most abundant rodents within lowland forests throughout their geographic range (Eisenberg 1989). Accordingly, they are generally the most thoroughly studied echimyids and will be the main focus of this review. At least 1 species of terrestrial echimyid occurs in most forested lowlands throughout the geographic distribution of the family, and some forests host multiple syntopic species (Emmons 1982; Lambert et al. 2006; Voss et al. 2001). At least 1 species of arboreal echimyid also typically occurs syntopically (Lambert et al. 2005; Voss et al. 2001). Forests that harbor echimyids range from tropical dry to pluvial and from young 2nd growth to old growth. Many terrestrial echimyids appear to be habitat generalists, ranging across forests of different moisture regimes and ages (Adler 2000; Adler et al. 2000; Gonzalez-M. and Alberico 1993; Lambert and Adler 2000), although some species (e.g., Proechimys guyannensis) apparently are restricted mostly to old-growth forests (Lambert et al. 2003; Voss et al. 2001). These rats are primarily frugivorous and granivorous (Adler 1995; Guillotin 1982; Henry 1997) but also consume mycorrhizal fungi (Janos and Sahley 1995; Mangan and Adler 1999), and some species occasionally include insects in their diets (Guillotin 1982). The arboreal K. amblyonyx is much more specialized with respect to habitat and diet. Individuals are restricted to patches of native and introduced bamboo and are largely folivorous (Stallings et al. 1994). Most forest-dwelling echimyids occur in areas with pronounced rainfall seasonality, although those living within the aseasonal pluvial forests on the Pacific slope of Colombia and northern Ecuador (Proechimys semispinosus and H. gymnurus) experience abundant year-round rainfall (Gonzalez-M. and Alberico 1993). Seasonal areas also are subjected to periodic irregular climatic fluctuations such as El Nino events, which superimpose additional constraints on organisms within their influence (Wright et al. 1999). Because of the pronounced environmental fluctuations experienced by forest echimyids, the availability of food resources (primarily fruits, seeds, and mycorrhizal fungi) also varies seasonally and across years (Adler 1998; Mangan and Adler 2002). Populations of terrestrial echimyids at least sometimes are limited by resource abundance (Adler 1998). Food resources are typically overdispersed or distributed in patches within tropical forests, and resource availability consequently also varies spatially (Adler 1994). Thus, most forest-dwelling echimyids live in environments with temporally ephemeral, spatially patchy, and occasionally limiting resources, all of which are likely to influence spacing patterns and mating systems. However, for species such as K. amblyonyx, which is

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TABLE 1.Spacing patterns and reported mating systems of 9 species of echimyid rodents. Density is on a relative basis, with low being 5 individuals/ha, medium approximately 6 to 15 individuals/ha, and high .15 individuals/ha. NA 5 not available.
Species Proechimys semispinosus Density Low Medium to high High High Medium Low NA Low Low Medium Medium NA Myocastor coypus NA Relative home-range size Males . females Males . females Males . females Males . females NA Males . females Males . females Males . females Males . females Similar to high Males . females NA NA None Little to extensive Extensive Extensive Moderate Females exclusive, Females exclusive, Females exclusive, Females exclusive, Extensive males males males males unknown extensive extensive extensive Home-range overlap Reported mating system NA Polygynous to promiscuous Polygynous to promiscuous Promiscuous NA Polygynous? Polygynous Polygynous or promiscuous Polygynous Promiscuous Polygynous Monogamous Polygynous Source Fleming (1971) Adler et al. (1997) Seamon and Adler (1999) Endries and Adler (2005) Everard and Tikasingh (1973) Emmons (1982) Guillotin (1982) Aguilera M. (1999) Bergallo (1995) Santos and Lacey (2011 [this issue]) Stallings et al. (1994) Silva et al. (2008) Guichon et al. (2003a, 2003b)

P. trinitatus P. brevicauda P. cuvieri P. guairae Trinomys iheringi T. yonenagae Kannabateomys amblyonyx

Consexually exclusive; males overlap with females Consexually exclusive; males overlap with females Extensive

highly specialized and feeds only on the leaves and stems of native and introduced bamboo within lowland forests (Silva et al. 2008; Stallings et al. 1994), resources are distributed in patches but spatially more abundant and temporally more persistent than fruit. Bamboo rats typically do not use other habitats except when moving from 1 patch of bamboo to another (Stallings et al. 1994). Echimyids, such as all 3 species of Thrichomys, some species of Trinomys, and M. coypus, experience dramatically different environmental conditions. Members of the genus Thrichomys and nonforest species of Trinomys (e.g., Trinomys yonenagae) inhabit drier caatinga habitats, dune areas, and open highland habitats (Freitas et al. 2008; Marcomini and de Oliveira 2003) and are granivorous, frugivorous, and herbivorous (Manaf et al. 2003). M. coypus is mostly aquatic and subsists primarily on a diet of aquatic vegetation that is supplemented with terrestrial plants (Borgnia et al. 2000). Based upon current theory on the spacing patterns of rodents, we could expect females in forested habitats to be territorial but males to be nonterritorial (Ostfeld 1990). Species of Trinomys and Thrichomys that live in drier, nonforested habitats and M. coypus, which lives in a wet and more constant environment, likely use resources that are distributed differently both spatially and temporally. Consequently, such species would be expected to have different spacing patterns (including greater sociality and group living) and social mating systems. Thus, echimyid rodents likely vary in their social and mating systems, and any family-wide treatment must take into account their respective environments.

SPACING PATTERNS AND SOCIAL MATING SYSTEMS

Several species within the genus Proechimys are the best studied of the echimyids. Spacing patterns of at least 5 species

have been examined using livetrapping data, tracking with fluorescent powder, or radiotelemetry (Table 1). Because different methods and home-range estimators (e.g., minimum convex polygons and fixed kernel methods) have been used to describe home ranges, quantitative estimates of home-range size and degree of overlap are likely to vary depending upon methodology, but descriptions of spacing patterns are not expected to vary as much. Therefore, I will not address quantitative estimates but will compare only qualitative assessments of home-range descriptors. Reviewed studies, albeit lacking concomitant behavioral and molecular data that would allow more refined descriptions of social and genetic mating systems, nonetheless reveal different spacing patterns and suggest several different social mating systems. The earliest study on spacing patterns of Proechimys spp. was based on livetrapping of P. semispinosus in low-density (,5-individuals/ha) populations in central Panama (Fleming 1971). Home ranges of both adult males and females were largely exclusive and showed no overlap with neighbors, thereby suggesting territoriality. Home ranges of males were larger than those of females. Although the mating system of individuals within those populations was not addressed, the exclusive home ranges and larger male home ranges suggested that males and females were either facultatively monogamous if multiple mates were not available or polygynous if multiple females could be found by males. Spacing patterns of P. semispinosus within mid- to highdensity populations on 5 small (1.8- to 2.7-ha) islands in Gatun Lake in central Panama were examined also using livetrapping data (Adler et al. 1997). Males again had larger home ranges than did females, but home ranges overlapped extensively; individuals generally did not exhibit any evidence of territoriality or exclusive use of space. On islands that harbored the lowest densities, however, home ranges did not

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overlap as extensively and in 1 case were nearly exclusive of other home ranges. Home-range size was related negatively to density, indicating that home ranges could be compressed if resources were abundant. Differences in spacing patterns from mid- to high-density islands further suggested that social mating patterns of individuals varied among populations, depending upon density, and could range from polygyny to promiscuity (Adler et al. 1997). In a radiotelemetric study of adults on 1 of those highdensity islands (Seamon and Adler 1999) males had marginally larger home ranges than did females, and home ranges overlapped extensively, showing no evidence of territoriality of adult males or females in that population. Adults also shared diurnal resting sites (subterranean cavities or burrows) with other adults and demonstrated low fidelity to those burrows. A single male frequently co-occupied a burrow with a single female, and on 1 occasion 2 males shared a burrow. Seamon and Adler (1999) suggested that the mating system of P. semispinosus varied with density, ranging from monogamy in low-density populations to promiscuity in highdensity populations. A more intensive radiotelemetric study of 16 P. semispinosus on another small (0.28-ha), high-density island in Gatun Lake showed similar patterns and also revealed seasonal changes in home-range size and overlap (Endries and Adler 2005). Males again had larger home ranges than did females, and home ranges were larger and overlapped more during the rainy season when fruit abundance and reproductive output were greater than during the dry season. No evidence of attraction, avoidance, or territoriality was found on either a short-term (within a single night) or long-term (within a season) basis. Overlap was so extensive that individual home ranges were not readily distinguishable when all home ranges were mapped together. All individuals used diurnal resting sites in subterranean cavities. Co-occupancy of burrows was extensive and greater during the rainy season; all radiotracked adults shared a burrow on at least 1 occasion. Burrows variously were shared by 2 females, by a male and a female, and by 2 males and 1 female. Endries and Adler (2005) suggested that individuals within this population were promiscuous. In Trinidad Everard and Tikasingh (1973) used livetrapping data to estimate that home ranges of Proechimys trinitatus overlapped an estimated 46.8%, based on a maximum density of 13.8 individuals/ha. Overlap by sex and age classes was not given, and the putative mating system was not addressed. However, relative to other studied populations of Proechimys spp. included in this review, both density and overlap were moderate, suggesting a polygynous stystem. In southeastern Peru Emmons (1982) studied spacing patterns of Proechimys brevicauda using radiotelemetry in a low-density population (3 or 4 individuals/ha). Although sample sizes were small, putative patterns were reported. Home ranges of adult female P. brevicauda were mutually exclusive and were overlapped by those of an adult male. The single adult male included in the study had a much larger home range than did the adult females. All individuals

included in the study used multiple burrows. If such spacing relationships prevailed with larger sample sizes, a polygynous mating system could be expected. Spacing patterns of Proechimys cuvieri in French Guiana were studied using radiotelemetry and tracking with fluorescent powder (Guillotin 1982). Males had home ranges that were more than twice the surface area of those of females, and the smallest male home range was nearly twice as large as that of the largest female home range. Females maintained exclusive home ranges, but those of males overlapped extensively with both males and females. Results from a study (Guillotin 1982) on spacing patterns of other species of Proechimys suggest a polygynous mating system. Adult male Proechimys guairae in Venezuela had home ranges, based on livetrapping data, that were nearly 3 times larger than those of adult females in a population with a density of ,4 individuals/ha (Aguilera M. 1999). Male home ranges overlapped extensively, but females showed no such overlap, thereby suggesting female territoriality. Aguilera (1999) suggested a polygynous or promiscuous mating system within this population. No comparable studies have been conducted on the spacing patterns of H. gymnurus. However, using nearest-neighbor analysis of livetrapping data from central Panama, adult males and females were distributed more closely to each other than were those of syntopic P. semispinosus (Adler et al. 1998). Based on those results, Adler et al. (1998) suggested that the more specialized H. gymnurus might have been monogamous or polygynous in the study area, where it was restricted to narrow corridors of moist riparian areas within contiguous forest (Tomblin and Adler 1998). However, in larger expanses of wet habitats, such as on the Pacific slope of Colombia, this species might reach higher densities and be polygynous or even promiscuous (Adler et al. 1998). Few studies have been conducted on spacing patterns of Trinomys spp. In a study of Trinomys iheringi based on trapping within a population with a mean density of 5.32 individuals/ha, Bergallo (1995) found that males had larger home ranges than females. Females showed little overlap of home ranges with other females, but male home ranges overlapped extensively with those of other males and females. These spacing patterns suggested a polygynous mating system (Bergallo 1995). Stallings et al. (1994) used radiotelemetry to study spacing patterns of the arboreal K. amblyonyx in stands of an introduced Asian bamboo in southeastern Brazil. Density of bamboo rats was 14.7 individuals/ha. Male home ranges were larger than those of females and typically overlapped 1 or 2 female home ranges. However, home ranges generally were exclusive of consexuals and expanded following the abandonment of an adjacent home range. Together with frequent vocalizations, such spatial patterns suggested that individuals were territorial in this population and were likely polygynous (Silva et al. 2008). Silva et al. (2008) also used radiotelemetry to study spacing patterns of K. amblyonyx in stands of introduced bamboo in

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southern Brazil and provided compelling evidence for a socially monogamous mating system. Adults occurred as mated pairs, in which home-range overlap between the male and female was sometimes 100%, and occupied patches of bamboo that were exclusive of other mated pairs. Mutual grooming behavior was observed for all mated pairs. Individuals constructed nests of leaves, and pairs co-occupied nests an average of 16% of total nest-use observations. Males also provided parental care. Silva et al. (2008) attributed the difference in mating systems between their study population and that of Stallings et al. (1994) to a difference in the distribution of bamboo patches (and therefore food resources). Bamboo patches were more segregated in their study site, and it was not energetically profitable to search for and attempt to monopolize .1 female. Thus, even this highly specialized species displayed variation in spacing patterns and apparent social mating systems. Behavioral methods also have been used to infer social structure of echimyid rodents. Freitas et al. (2008, 2010) studied sociality of 3 species of Trinomys (T. yonenagae and T. albispinus from semiarid caatinga and T. iheringi from Atlantic Forest) and Thrichomys apereoides from semiarid caatinga by observing dyadic encounters. An affiliation index was calculated for each species to quantify the degree of sociality. T. yonenagae was the most affiliative, as indicated by its lower levels of aggressive behaviors and higher degree of sociality. T. albispinus and Th. apereoides were the least affiliative and showed high levels of aggression toward conspecifics, and T. iheringi displayed intermediate levels of aggressive interactions with conspecifics. Trinomys yonenagae forms colonies within its desert-like sand-dune caatinga habitat, and individuals even cooperate in digging burrows. Such social behavior apparently is adaptive within its habitat (Freitas et al. 2008) and represents an evolutionary trend from more aggressive behaviors in species such as T. albispinus and T. iheringi to completely affiliative behaviors in T. yonenagae (Freitas et al. 2010). Freitas et al. (2010) further argued that the evolution of sociality in T. yonenagae was influenced more by predation pressures than by resource distribution. Although Freitas et al. (2008, 2010) did not specifically address the mating systems of the 4 study species, the dramatic differences in sociality strongly suggest different mating systems, particularly for the highly social T. yonenagae. T. yonenagae apparently displays a promiscuous mating system across a range of densities (1020 individuals/haJ. W. A. Santos, University of California, Berkeley, pers. comm.). In contrast to other studied species of echimyids, male and female homerange sizes are similar, overlap is extensive across a range of densities, and burrows commonly are shared (Santos and Lacey 2011 [this issue]). Guichon et al. (2003a, 2003b) observed groups of M. coypus in northeastern Argentina. Mean group size was 11 individuals, and each group contained 1 dominant adult male, socially subordinate adult and subadult males, adult and subadult females, and juveniles (Guichon et al. 2003a). Subgroups,

containing mostly juveniles and young adult males, were found within the larger groups. Interactions among individuals were largely amicable and even cooperative, and agonistic interactions were rare. Guichon et al. (2003a, 2003b) suggested that individuals within the study groups were polygynous, with only the dominant male mating with multiple adult females within a social group.

GENERAL MODEL OF ECHIMYID MATING SYSTEMS

Any attempt to develop a general model to explain the mating systems of echimyid rodents must account for both similarities and differences that have been observed among populations and species. All of the above-mentioned studies of terrestrial echimyids, with the exception of T. yonenagae, show that adult males have larger home ranges than do adult females, and several studies suggest that adults are territorial, particularly females (Bergallo 1995). However, the evidence for territoriality is mostly circumstantial and is based upon nonoverlapping home ranges. Most of the studies in which overlap was minimal were conducted within populations at low densities (typically 5 individuals/ha). In such studies no concurrent behavioral studies were conducted to demonstrate that individuals were actively maintaining territories. By contrast, no evidence of territoriality has been found in higherdensity populations, either over the course of several months or even within a single night around a food source (Endries and Adler 2005). I suggest that in most cases where home ranges overlap little in low-density populations, individuals merely occupy the abundant available space without actively defending a territory. The energetic and temporal costs of vigilance against potential intruders would exceed the benefits of such vigilance. Consequently, at very low densities individuals could be monogamous simply because multiple mates might not be available. As densities increase home ranges begin to overlap more. Because male home ranges are typically larger than those of females, male ranges are likely to overlap more with both sexes, but females still might show little evidence of home-range overlap because of their much smaller areas rather than because of active territorial defense. Thus, multiple females could become available to males, and a polygynous mating system, as suggested by several of the abovementioned studies, is most likely. At very high densities, such as on small islands or in large contiguous patches of forest following an El Nino event (which dramatically increases plant reproduction and consequently resource abundance throughout large parts of the NeotropicsWright et al. 1999), home ranges of both males and females are compressed and overlap extensively. A promiscuous mating system then becomes apparent (Endries and Adler 2005; Seamon and Adler 1999). I suggest that many of the more-specialized arboreal echimyids will show a similar pattern, although it is likely that their densities rarely will reach the level at which individuals would become promiscuous because they might be limited more by availability of suitable nest sites.

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FIG. 1.Schematic diagram showing the ultimate influence of resources on the social mating system of typical (i.e., terrestrial, frugivorous, and forest) echimyid rodents (after Ostfeld 1990). The model also applies to arboreal frugivorous and folivorous species, but resource patchiness and patch size can be more important than renewability and abundance. The model does not apply to highly social or colonial species.

Individuals of many species of echimyids thus might be highly flexible with respect to mating systems, and such systems will depend upon environmental conditions (Silva et al. 2008). Thus, a given species generally cannot be denoted by a single mating system, but rather individuals within populations will demonstrate a particular mating pattern. The type of mating pattern likely will be dictated by density, which ultimately depends upon availability and spatial distribution of resources (including both food and nest sites). Density and consequent mate availability therefore appear to be crucial determinants of the mating pattern of individuals within a given population of echimyids (Fig. 1). Such patterns can range from facultative monogamy, when a lack of multiple mates precludes a male from monopolizing multiple females, to polygyny when a male can gain access to multiple females, to promiscuity when both males and females can readily gain access to multiple mates simultaneously (for males) or in succession (for females). Cases of apparent monogamy and polygyny could also include cuckoldry, whereby litters could be sired by more than 1 male. Thus, social and genetic mating systems could differ within echimyids. Flexibility in mating systems of many species of echimyids is not surprising. Populations of P. semispinosus show tremendous variation in demography, both spatially and temporally. This demographic flexibility, resulting from reaction norms in life-history traits of individuals within populations, apparently allows individuals to respond quickly to unpredictable environmental changes, such as El Nino events and forest disturbance (Adler 1996, 2000). Therefore, it is almost inevitable that spacing patterns and social mating systems are also variable among populations of this generalized species. If P. semispinosus is typical of other species of generalized echimyids, which I suggest, it is likely that other such species will show variability in life-history traits,

demography, and mating systems along a continuum of environmental conditions and population densities. Even individuals within different populations of the more highly specialized and arboreal K. amblyonyx display evidence of different mating systems, including both social monogamy and polygyny, depending upon local environmental conditions. Studies of this species provide the most compelling evidence for territoriality, yet the mating system is nonetheless flexible. It is likely that other arboreal echimyids, such as those in the genera Dactylomys, Diplomys, Echimys, Makalata, and Mesomys, because of their ecological similarity, are also territorial but have flexible mating systems. Such flexibility in spacing patterns and social mating systems therefore might be common within the family Echimyidae. Furthermore, this flexibility could be adaptive, allowing individuals to maximize fitness in spatially heterogeneous and constantly fluctuating environments. I suggest that few exceptions to this putative general trend of mating-system flexibility among echimyids exist. The most likely exceptions would be in species that have unique social systems, such as the highly social T. yonenagae and M. coypus. Because of their cooperative behaviors, they are not likely to display such flexibility in their mating systems. Because of the diversity of species and life styles within the family Echimyidae, this family offers an excellent opportunity to study the evolution and phylogeny of social systems. It would be particularly interesting to find additional species of echimyids with unusual or inflexible social systems. The most likely habitats to harbor such species are not tropical forests but rather drier or highland habitats, and a potential candidate would be Clyomys bishopi, a colonial and fossorial echimyid in Brazil (Manaf et al. 2003). Behavioral and phylogenetic approaches used by Freitas et al. (2008, 2010) provide an excellent template for developing future studies. Experimental

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studies that manipulate resource abundance and predation also would help to explain the importance of those factors in affecting mating systems and their relationships to density. Perhaps most crucial of all is to conduct molecular studies to reveal genetic mating systems and to compare those systems with social mating systems that are inferred from spatial patterns.

RESUMEN
Los roedores de la familia Echimyidae son abundantes y tienen una amplia distribucion en la mayora del Neotropico. En este artculo reviso la informacion disponible acerca de sus patrones de distribucion y sistemas de apareamiento, y desarrollo un marco general para entender la variacion entre poblaciones y especies. En la mayora de las especies el tamano del rango de hogar de los machos es mayor que el de las hembras, y la superposicion de este con el de otros individuos del mismo sexo o el sexo opuesto puede variar entre el 0% y el 100%. Los machos usualmente presentan una mayor superposicion con cualquiera de los sexos lo que ha sido interpretado como territorialidad. Sin embargo, la mayora de estos casos han ocurrido en poblaciones con densidades poblacionales bajas. Individuos de las mismas especies exhiben una superposicion territorial considerable cuando las densidades son poblacionales mayores. Aqu propongo que los individuos usualmente no son territoriales sino que se distribuyen ampliamente cuando hay disponibilidad de espacio. De esta forma, los individuos son monogamos facultativos porque no hay multiples parejas disponibles. A medida que aumentan las densidades, los machos pueden acceder a multiples parejas y se hace evidente la poliginia. La superposicion en los territorios de los machos es debida simplemente a que sus territorios son mas grandes que los de las hembras. Con un incremento en las densidades, hay multiples parejas disponibles tanto para machos como para hembras, lo cual resulta en un sistema promiscuo. El sistema de apareamiento dentro de una poblacion de muchos echimyidos depende entonces de la densidad poblacional, que a su vez es determinada principalmente por la disponibilidad de recursos.

ACKNOWLEDGMENTS
I thank T. D. Lambert, J. W. A. Santos, and 2 anonymous reviewers for helpful comments on an earlier draft of the manuscript and A. Carvajal for providing the Spanish abstract.

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Special Feature Editor was Barbara H. Blake.