Journal of Mammalogy, 92(1):39–53, 2011

Diversity of social and mating systems in cavies: a review

OLIVER ADRIAN* AND NORBERT SACHSER Department of Behavioural Biology, University of Mu¨nster, Badestrasse 13, 48149 Mu¨nster, Germany (OA, NS) Museum of Natural History, Mu¨nsterstrasse 271, 44145 Dortmund, Germany (OA) * Correspondent: [email protected] Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 Cavies (family Caviidae) are a group of rodents distributed over much of South America. The high diversity of habitats inhabited by different species is paralleled by a high diversity of social organizations. Comparisons of behavioral and reproductive strategies between species can provide valuable insights into mammalian social evolution. In this review we 1st summarize the literature to give an idea of the diversity of social and mating systems within the genera Cavia, Galea, Microcavia, and Kerodon. Social systems range from solitary animals through pairs and harems to multimale–multifemale groups. Mating systems of cavies include monogamy and promiscuity and different forms of polygyny. We then review behavioral strategies of females and males that account for this social diversity. Particularly, the role of females and the potential of males to monopolize mates are examined. In some species, for example, estrous females actively solicit copulations with several males and thereby prevent their monopolization by single males. We also discuss adaptations of reproductive physiology to different mating systems. Finally, environmental factors influencing aspects of the social and mating systems of cavies are considered. Particularly, differences in resource distribution, predation risk, and climatic conditions might explain the great variation in species social organization.

Key words: behavioral strategies, cavies, Caviidae, communal burrowing, mating system, paternities, predation risk, sexual size dimorphism, social system, spacing behavior E 2011 American Society of Mammalogists DOI: 10.1644/09-MAMM-S-405.1

Cavies or guinea pigs (Caviidae) are a small group of The capybara traditionally has been placed in a family of its caviomorph (New World hystricognath) rodents distributed own (Hydrochoeridae) but now is included in the family over much of South America. The domestic guinea pig, 1 of Caviidae (Woods and Kilpatrick 2005), forming a subfamily only 3 ancient New World domesticated mammals (Lavalle´e with Kerodon (Hydrochoerinae). The remaining 3 genera of 1990), has experienced an extraordinary worldwide distribu- cavies constitute the subfamily Caviinae. A 3rd subfamily tion as a laboratory animal and a pet. In pre-Columbian times (Dolichotinae) contains 2 species of maras (Dolichotis guinea pigs were sacrificed in religious ceremonies to the gods patagonum and D. salinicola), which resemble small ungu- of the ancient cultures of the central andes. They also lates or short-eared lagomorphs more than other cavies. represented an important source of food for humans, as they Within the genera Cavia and Galea several species have been do today (Sandweiss and Wing 1997). described that later were synonymized with other species. The guinea pig was domesticated from a wild form still Knowledge of the number of and relationships between abundant in Peru (Hu¨ckinghaus 1961; Spotorno et al. 2004, different species and subspecies and their geographic 2007), but more than a dozen wild species exist on the distribution remains limited. An overview of cavy species continent. Four genera of cavies—Cavia (common or wild and subspecies currently accepted is given by Woods and cavies), Galea (yellow-toothed cavies), Microcavia (mountain Kilpatrick (2005). The species G. monasteriensis (Solmsdorff or desert cavies), and Kerodon (rock cavies or mokos)—can et al. 2004) has not yet been included there. According to a be distinguished easily. All have a similar appearance on 1st recent phylogenetic study G. monasteriensis might be a junior view and will be identified as guinea pigs even by a layperson. synonym of G. musteloides boliviensis, whereas the lowland Upon closer look, Kerodon represents the genus whose forms of G. musteloides would not be conspecific to the morphology differs the most. Recent molecular phylogenetic studies revealed that Kerodon is related more closely to the capybara (Hydrochoerus hydrochaeris) than to the other cavies (Rowe and Honeycutt 2002; Trillmich et al. 2004). www.mammalogy.org 39 40 JOURNAL OF MAMMALOGY Vol. 92, No. 1 highland forms and should be named G. leucoblephara conditions, or costs of burrow construction and maintenance, (Dunnum and Salazar-Bravo 2010). All field studies on G. among other factors, must be considered when assessing musteloides cited in this review (with the exception of Mares determinants of social and mating systems. et al. 1981) and the laboratory studies for which the origin of Beginning with Rood (1969, 1970, 1972), multiple detailed the study animals is reported are based on the lowland forms. studies on the social organization in the natural habitat of Caviids inhabit almost all of South America with the different cavy species have been conducted, complemented by exception of western Chile and Tierra del Fuego. The investigations of captive colonies in seminatural enclosures northwestern edge of the continent and parts of the Amazon and laboratory studies, to answer specific questions on the Basin are occupied only by the capybara but not the cavies. social and mating system through experimental research under Distribution maps of the different species are given by Mares controlled and standardized conditions. In this review we 1st and Ojeda (1982), Eisenberg (1989), Redford and Eisenberg summarize the available literature to note the remarkable Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 (1992), and Eisenberg and Redford (1999). The wide distri- diversity of social and mating systems within this group of bution of the family results in 1 or several species present in South American rodents and present data on spacing behavior, all major habitat types of South America (Mares and Ojeda social interactions, sexual size dimorphism, mating, and 1982). Capybaras live in the tropical rain forests of the paternity. Where it seemed relevant to us, we also included Amazon Basin and surrounding savannas and swamps. Maras unpublished field data from our group. We focus here on the inhabit the deserts, grasslands, scrubs, and dry forests of the cavies (Fig. 1). The maras and capybaras are excluded from southern part of South America. Habitats of cavies include this review. Information on their social and mating systems grasslands, savannas, marshes, moist and dry forests, scrubs, can be found in Herrera et al. (2011 [this issue]), Lord (2009), deserts, montane regions, and cultivated areas. A variety of Macdonald et al. (2007), Taber and Macdonald (1992a, different ecotypes has been recognized in this group and 1992b), and references therein. Because it represents a special include semiaquatic forms with webbed feet (H. hydrochaeris case due to artificial selection during the long process of and C. magna) and semiscansorial (M. australis and K. domestication (Ku¨nzl et al. 2003; Ku¨nzl and Sachser 1999), rupestris), burrowing (Dolichotis spp. and Microcavia spp.), we also do not consider the domestic guinea pig. Its social cursorial (Dolichotis spp.), and ground-dwelling forms (Cavia organization is the central theme of papers by Fuchs (1980), spp. and Galea spp.). Sachser (1986), Sachser et al. (2004), and references therein. This diversity of habitats and ecotypes is reflected in a high Subsequently, we review behavioral strategies of females diversity of social and mating systems. The male(s) of an and males responsible for the diversity of social and mating established social unit (e.g., a monogamous pair, a harem, or a systems. Particularly, the role of females and the potential of multimale–multifemale group) is (are) often not the exclusive males to monopolize mates are examined. After this we mating partner(s) of the female(s) of that unit. Extrapair or describe adaptations of reproductive physiology in cavies with extragroup copulations and paternities occur in many species, different mating systems. Finally, environmental factors particularly in birds (Birkhead and Møller 1992, 1995), but influencing certain aspects of the social and mating systems also in mammals (Digby 1999; Martin et al. 2007; Munshi- of cavies are discussed. South 2007). Thus, both the mating behavior (social mating system) and the genetic outcome of matings (genetic mating system) are not necessarily determined by the composition of SOCIAL AND MATING SYSTEMS:SPACING BEHAVIOR, a social group. SOCIAL INTERACTIONS,SEXUAL SIZE DIMORPHISM, A classical view of social organization of animals is that MATING, AND PATERNITY resource distribution determines the distribution of females in Cavia aperea.—Distribution of C. aperea is associated with space and time. Female distribution then explains male areas of dense ground vegetation and surrounding zones of distribution, and these patterns together with male–male short grass where the animals forage (Asher et al. 2004, 2008; competition for mates effect different forms of social Bonaventura et al. 2003; Cassini and Galante 1992). Male and organization (including mating systems—Clutton-Brock and female cavies have stable home ranges (Asher et al. 2004, Harvey 1978; Emlen and Oring 1977). However, the role of 2008; Rood 1969, 1970, 1972), those of males being larger females is much more active than expressed in this view. than those of females (Table 1). Male home ranges overlap Female, just as well as male, behavioral strategies for survival those of 1–3 females almost completely, whereas little or no and successful reproduction represent the proximate factors overlap is found among neighboring males; neighboring generating the diversity of social and mating systems in females overlap about 40% on average (Asher et al. 2004, different species. Behavioral strategies find their expression 2008). Although little home-range overlap exists among also in morphological (e.g., sexual size dimorphism) and males, they do not behave territorially; home-range borders reproductive (e.g., sperm characteristics and estrous type) are neither scent-marked nor defended against intruding adaptations and have consequences for male and female males. However, females are scent-marked, and other males reproductive success. Ultimately, behavioral strategies evolve are chased by a resident male when they approach a resident as adaptations to specific environmental conditions. Thus, female (Asher et al. 2004, 2008). Distribution and overlap of the distribution of food resources, predation risk, climatic home ranges allows the differentiation of distinct spatial units: February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 41 Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021

FIG.1.—Taxonomy of Caviidae (following Woods and Kilpatrick 2005) at the generic level and above, genera of the cavies (light gray background color), and species described in this review. pairs (1 adult male and 1 adult female) and harems (1 adult ranges but moved across areas much larger than the home- male and 2 or 3 adult females). In harems home-range overlap range areas of resident males, and were found for 1 or a few is greater between the male and his females than between the days within each resident male’s home range. The following females, and females are found at greater distances from each scenario might explain the relationship between male size and other than from the male. The number of females belonging to home ranges (Asher et al. 2008). Young males disperse from a male unit can depend on the home-range sizes of the their natal area and become satellite males at neighboring females. At a site in Uruguay (Asher et al. 2008) with a 2.4- sites. They assume the dominant position if the resident male fold greater population density than at a site in Brazil, female dies. When they grow too large, the resident male perceives home ranges were smaller (Asher et al. 2004; Table 1), and in them as potential rivals and evicts them. The young males then Uruguay harem groups dominated, whereas in Brazil the start a roaming life searching for a vacant resident male predominant type of social unit was the pair. position. In Uruguay all harem males were large, with a body mass . Cavia aperea is crepuscular, leaving the dense vegetation in 500 g (Asher et al. 2008). Within 2 of the spatial units a small the morning and late afternoon for short foraging bouts on but sexually mature male of ,350-g body mass (satellite more open sites. The animals forage alone or with a male) was present whose home range was much smaller than conspecific (Asher et al. 2004, 2008; Rood 1972). In most those of the large resident male and the females. A 3rd cases 2 animals foraging together are the male and a female of category of mature males was termed roaming males. These a harem unit; joint foraging of 2 females from the same harem were of intermediate size (350–500 g), had no stable home is much rarer (Asher et al. 2008). Aggression is rare in these

2 TABLE 1.—Male and female individual home-range sizes (m ) in cavies. Note that absolute home-range sizes must be compared with caution among studies because of different estimation methods and sample sizes. D signif. 5 difference between males and females statistically significant (P , 0.05). MCP 5 minimum convex polygon.

Home-range size (mean 6 SD) Males (n) Females (n) D signif. Method Source Cavia aperea 1,387 6 657 (9) 1,173 6 464 (8) Exclusive boundary strip Rood (1972) 880 6 217 (5) 549 6 218 (7) Yes MCP 100% Asher et al. (2004) 604 6 324 (4) 320 6 249 (12) Yes MCP 100% Asher et al. (2008)a 165 6 22 (2) — MCP 100% Asher et al. (2008)b 543 6 503 (7) 302 6 368 (15) Yes MCP 100% Asher et al. (2008)a Cavia magna 11,830 6 6,210 (24) 7,670 6 3,970 (25) Yes MCP 100% Kraus et al. (2003)c Cavia intermedia 1,700 6 1,000 (7) 1,700 6 1,300 (5) No MCP 100% Salvador and Fernandez (2008a) Galea musteloides 4,275 (1) — Exclusive boundary strip Rood (1972) 12,083 6 5,416 (6) 2,250 6 1,041 (4) Yes MCP 100% M. Asher, University of Mu¨nster, pers. comm. Galea spixii 872 6 497d 632 6 978d No Intertrap distances Lacher (1981) Microcavia australis 3,942 6 2,420 (22) 2,187 6 940 (16) Exclusive boundary strip Rood (1972)e 7,720 6 1,160 (5) 3,525 6 382 (3) Exclusive boundary strip Rood (1970, 1972)e 6,737 6 4,443 (6) 3,517 6 2,449 (12) No MCP 95% Ebensperger et al. (2006) 3,738 6 1,322 (9) 1,963 6 1,143 (14) Yes MCP 100% Lu¨ttmann (2006); Ranft (2005)

a Data of the same population during early summer and late summer, respectively. b Small satellite males in contrast to large resident males above. c Drifting home ranges. d Sample size not reported in original source. e Data of the same population including all animals with 6 records and animals with 50 records, respectively. 42 JOURNAL OF MAMMALOGY Vol. 92, No. 1 feeding groups as are social interactions in general (Rood and his female(s) exists, no such relationship exists among 1972). Males maintain proximity to females, whereas the latter females of the same harem. seem to ignore them. In captive colonies with several males usually only the Social interactions are difficult to observe in C. aperea alpha male (and sometimes the beta male) exhibits frequent because most occur in dense vegetation. Hence, most courtship behavior toward the adult females (Rood 1972). information on social interactions stems from observations Courtship behavior of other males seems to be inhibited by the of captive groups. C. aperea is characterized by a low alpha male. However, the other males show courtship behavior threshold for aggression and possesses a greater variety of to subadults and juveniles. When pregnant females near term, aggressive behavioral patterns compared to the cavies G. the alpha male starts to guard them, maintaining close musteloides and M. australis (Rood 1972). Aggressive proximity and chasing other approaching males away. The interactions usually occur between 2 males or 2 females or alpha male is usually the 1st to copulate, but subordinate Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 between females and subadults. In the captive groups of males also can copulate successfully with the female in the Sachser et al. (1999) and Stahnke (1987) adult males were course of a mating chase. The alpha male is highly aggressive incompatible; not more than 1 adult male could be kept in an toward rivals but can prevent other males from copulating enclosure because fighting between 2 males always escalated, only in about one-half of all cases (Rood 1972). The other leading to severe injury. In the groups of C. aperea of Rood males usually ejaculate rapidly on the 1st intromission in (1972) the males formed linear dominance hierarchies. contrast to alpha males, which mount the female several times Dominance depended on body mass and former residency. before ejaculation. When a new male was introduced into a group he was attacked In the field courtship and sexual behavior were observed severely by the resident male, which often caused the death of exclusively between members of the same social group of C. the intruder. Loss of dominance also resulted in the death of aperea (Asher et al. 2004). Microsatellite analyses of 15 litters former alpha males within a month after they withdrew from with .2 pups born to females captured in the field while any social interactions. Frequent alpha male aggression toward gravid revealed that multiple paternity occurred in 13–27% of subordinate males was a primary cause of high male mortality litters, a value much lower than in G. musteloides, the only in the captive colonies. other cavy species in which paternity has been examined Among females intrasexual aggression is much less (Asher et al. 2008). All individual males identified as sires of pronounced, but it also occurs frequently (Rood 1972; Sachser the offspring had a body mass of .500 g, thus belonging to et al. 1999; Stahnke 1987). In the field females seem to avoid the category of large resident, harem males. No multiple each other (Asher et al. 2008). In captive groups they establish paternities were observed in litters from mate-choice tests in linear dominance hierarchies (Rood 1972) that are age- which females could mate with 2 or 4 different males, dependent (Sachser et al. 1999). Only high-ranking females although several females had copulated with .1 male (6 litters successfully breed in such colonies. An adult male might each—Adrian et al. 2008a; Hohoff 2002). intervene in a fight between 2 females by placing himself As is common when males compete for access to females, between the adversaries and starting courtshiplike behavior males of C. aperea are significantly heavier than nongravid (Stahnke 1987). Unfamiliar adult males and females frequent- females (Asher et al. 2004, 2008; Bonaventura et al. 2003; ly exhibit heightened aggression (Rood 1972; Stahnke 1987). Sachser et al. 1999). In the study population of Asher et al. Between males and females familiar with each other, (2008) males were, on average, 17% heavier. Large resident interactions are predominantly amicable, but rare. Social males were about 32% heavier than females, whereas no grooming and close bodily contact almost never occur (Asher significant difference in body mass was found between et al. 2004; Rood 1972; Sachser et al. 1999). In mate-choice roaming or satellite males and adult females. The exclusivity experiments, where females had access to 4 (Hohoff 2002) or of reproductive success of large males, strong sexual size 2 (Adrian et al. 2008a) different males, each female had a dimorphism, and rarity of multiple paternities point to male clear social preference for 1 of the males, measured as the contest competition for females. The mating system can be relative time spent with each male. described as female-defense polygyny with limited promiscu- Because females seem to avoid each other and interact only ous mating (Table 2). aggressively, it is not surprising that nursing of other females’ Cavia magna.—The social organization of C. magna is very pups is extremely rare (Rood 1972; Stahnke 1987). Females different from that of C. aperea. C. magna lives in wetlands seem to distinguish between their own and alien young and that periodically are flooded. Adaptations of this species to may aggressively repel the latter (Rood 1972). Males of C. these environmental conditions are webbed feet and good aperea show paternal behaviors in the form of social play and swimming ability. Individuals of both sexes of C. magna were grooming and only rarely are aggressive toward their pups distributed randomly at a site in Uruguay (Kraus et al. 2003). (Adrian et al. 2005). Home ranges (Table 1) were significantly larger in males than In conclusion, although large mixed-sex groups were in females and depended on water levels. When water levels described (Rood 1972), the social system of C. aperea seems were high, male home-range size increased, whereas female better characterized by 1-male units (Table 2). Although a home-range size decreased. Home ranges were not stable but stable social relationship between the male of a pair or harem shifted from month to month across the study area indepen- February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 43

TABLE 2.—Social and mating systems and associated traits in the cavies. For references to the data see the main text. Note that different terms have been used here for the description of social and mating systems to emphasize their different character. In the literature the term monogamy, for example, is used for both pair-living and exclusive mating with 1 partner by both male and female.

Sexual size Multiple Paternal Social system Mating system dimorphism Relative testes size paternity behavior Cavia aperea Pair/harem Female-defense Males . females Low compared to Infrequent Moderate polygyny G. musteloides Cavia magna Solitary Promiscuity? Males . females ? ? ? Cavia intermedia ? ? Males 5 females ? ? ? Galea musteloides Solitary/multimale– Promiscuity Females . males High Frequent No multifemale groups Galea spixii ? Lek-type of male-domi ?? ?NoDownloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 nance polygyny (?) Galea monasteriensis Pair Monogamy Females . males Low compared to Absent Frequent G. musteloides Microcavia australis Female-centered Promiscuity Males 5 females High ? ? multimale– multifemale groups Microcavia niata ?????? Kerodon rupestris Harem Resource-defense Males 5 females ? ? Frequent polygyny dently of the water level. Male home-range fidelity was lower of contest competition, and an estrous female might be than that of females. Home ranges overlapped strongly within monopolized by a guarding male. and between sexes. At high water levels overlap was higher Cavia intermedia.—This species was described recently because the animals congregated in the drier areas. Male–male (Cherem et al. 1999). C. intermedia is restricted to Moleques and male–female overlap tended to be higher than female– do Sul Island off southern Brazil. Information relating to its female overlap. Male home ranges did not completely social and mating system is largely lacking. C. intermedia has encompass single female home ranges, as is the case in C. a high and stable population density and a balanced sex ratio aperea (Asher et al. 2004, 2008). (Salvador and Fernandez 2008a). In contrast to C. aperea and Analysis of static and dynamic interactions of animals C. magna, home-range size does not differ between males and within the overlap zones suggested that use of these zones was females (Table 1), and sexual size dimorphism is absent random. Group memberships were not apparent, and no stable (Salvador and Fernandez 2008b). These findings clearly point social relationships between males and females or among to differences from the other Cavia species in both social females existed (Kraus et al. 2003). Intersexual interactions organization and mating system. were more frequent than intrasexual ones. Animals neither Galea musteloides.—This species is a habitat generalist. In avoided nor were attracted by conspecifics sharing parts of Salta Province, Argentina, it occurs in 4 of the 5 major habitat their home ranges. During foraging several animals sometimes types. It is most common in moist microhabitats (Mares aggregated. Territorial behavior was not observed. In et al. 1981). In a capture–mark–recapture study on a wild accordance with this, an increasing population density did population in N˜ acun˜a´n, Argentina (M. Asher, University of not lead to smaller home ranges, as would be expected in Mu¨nster, pers. comm.), the sex ratio was biased in favor of territorial species, but rather to an increase in home-range males. Telemetry data revealed that home ranges of males overlap. Nonstationary use of space is unusual for rodents. In were .5 times as large as those of females (Table 1). Female this species it might have evolved as an adaptation to the home ranges usually did not overlap, whereas the large male regular flooding and varying distribution of food resources. home ranges overlapped strongly with those of several females The social system can be described as solitary (Table 2). and several other males. This situation differs from that in C. The larger male home ranges suggest that males might aperea but is similar to that in C. magna, although intersexual exhibit a roaming strategy and mate with every estrous female home-range size differences are not as large in the latter they encounter. The unpredictable location of females and species. The large aggregation of about 25 animals found at a their solitary lifestyle makes the monopolization of several 48-m-long stone wall in Buenos Aires Province, Argentina, females impossible. Rather, temporary consortships between a also points to extensive home-range overlap (Rood 1969, male and an estrous female might occur. Because reproduction 1972). is not strongly synchronized among females, a male also might In captive colonies males and females form dominance form consortships with different females in succession. The hierarchies (Rood 1972; Schwarz-Weig and Sachser 1996). mating system is described as overlap promiscuity (Kraus et Male–male aggressive interactions are frequent despite stable al. 2003); however, no data exist on multiple mating by linear hierarchies. Some authors could keep only 1 adult male females. The sexual size dimorphism found with males in a cage due to high intermale aggression (Rood and Weir heavier than females (Ximenez 1980) points to some degree 1970; Weir 1970). Male–male aggressive interactions occur 44 JOURNAL OF MAMMALOGY Vol. 92, No. 1 more than twice as often as those among females (Schwarz- 7 female G. musteloides that could mate freely, multiple Weig and Sachser 1996). Females frequently direct socio- paternities were detected in 83% of litters with .1 pup (Keil positive behaviors toward each other. Dominance hierarchies et al. 1999). In contrast to C. aperea and C. magna, a reversed among them are less stable and not strictly linear (Rood 1972). sexual size dimorphism is present in G. musteloides, which Reproductive status and age are factors affecting female points to little effect of body size in male–male competition. dominance relationships. Lactating females occasionally can In a captive population nongravid females were, on average, improve their dominance status temporarily, and older animals 15% heavier than males (Sachser et al. 1999). In a feral are usually dominant over younger ones. Adult females are population in Argentina females were about 8% heavier dominant over low-ranking (in the male hierarchy) males but than males (M. Asher, University of Mu¨nster, pers. comm.). subordinate to the alpha male. Intersexual aggression is rare G. musteloides clearly has a promiscuous mating system compared to intrasexual aggression. All individuals of a (Table 2). Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 mixed-sex group can be observed regularly sitting together in Galea spixii.—Like G. musteloides, G. spixii is a habitat close bodily contact in rest periods that alternate with activity generalist that occurs in a wide variety of open habitats. Male periods throughout the day (Schwarz-Weig and Sachser 1996). and female home ranges overlap strongly (Lacher 1981). The Social tolerance is higher in G. musteloides than in C. aperea. home ranges of G. spixii are strikingly smaller than those of G. However, subadult animals experience much aggression from musteloides (Table 1). Males scent-mark at certain locations adults, mainly from those of the same sex. Adult males are of their home ranges, and tolerance between males is very low. aggressive toward young males but less so toward young In captive groups both sexes form linear dominance females (Rood 1972). Males of G. musteloides never engage in hierarchies. Agonistic behavior varies, depending on whether direct parental activities. They treat even their own offspring a dominance hierarchy is already established (Lacher 1981). rather aggressively, beginning at birth (Adrian et al. 2005). Unfamiliar animals, both males and females, are overtly Allonursing is common in captive groups of G. musteloides aggressive toward each other. Even in established groups (Ku¨nkele and Hoeck 1995) and also was observed in the field social grooming is rare. The general aggressiveness of adults (Rood 1972). All lactating females in a group nursed offspring toward juveniles, even toward their own progeny, is of other females, and the majority of pups received milk from remarkable in this species. Paternal care has never been females other than their mother (Ku¨nkele and Hoeck 1995). observed. The social system, although not fully described, However, females can discriminate between their own and might be similar to that of G. musteloides. alien pups and favor the former. Alien pups older than 8 days Aggression increases as a female approaches estrus. Males are treated aggressively (Ku¨nkele and Hoeck 1989). try to deter competing males from mating through overt In conclusion, field data are ambiguous, some pointing to a aggression. According to Lacher (1981), however, females solitary social system (M. Asher, University of Mu¨nster, pers. ultimately choose with which males to copulate. He states that comm.) and others to multimale–multifemale groups (Rood the mating system of G. spixii can be described best as a lek- 1972), which is possibly due to intraspecific variation in the type male dominance polygyny (Table 2). It would be social organization of G. musteloides (Table 2). Examination interesting to gather genetic data on the mating system to of laboratory data argues against a solitary life of this species, specify differences from G. musteloides. because communal huddling and frequent allonursing point to Galea monasteriensis.—This species was described in closer relationships, at least among females. recent years (Solmsdorff et al. 2004—but named Galea sp. Female estrus is the only situation where the position of the by Hohoff et al. [2002] and Galea sp. nov. by Trillmich et al. dominant male is challenged (Rood 1972). Increased male [2004]). All data stem from captive animals, and virtually interest in females begins 1 or a few days before parturition nothing is known from field studies. Unfamiliar individuals of and thus just before the next estrus (all cavies exhibit a G. monasteriensis are extremely aggressive toward each other, postpartum estrus). Often, several males gather near the much more than are individuals of G. musteloides. When 2 female. The alpha male shows mate-guarding behavior and males or 2 females confronted each other, fighting escalated in occasionally attempts to chase other males away. As soon as all encounters without exception and thus had to be terminated the female leaves the birth site after parturition all males by the experimenters to prevent serious injury to the animals usually follow her in a mating chase. (Hohoff et al. 2002). As well, 60% of male–female encounters Although often mate-guarding the receptive female and led to escalated aggression. Aggression was initiated more attacking his rivals, the alpha male does not successfully often by the female than by the male. prevent other males from copulating (Rood 1972; Schwarz- In a series of mate-choice tests where a female had Weig and Sachser 1996). Moreover, Rood (1972) found that unrestricted access to 2 males housed singly, she usually the alpha male was seldom the 1st male to copulate. The exhibited a clear social preference for one of the males, occurrence of multiple paternities in litters from females measured as the relative time spent with the males in their caught gravid in the field was determined using microsatellites respective enclosures (Adrian et al. 2008b). In mate-choice (M. Asher, University of Mu¨nster, pers. comm.). The experiments where a female could choose between 4 different percentage of multiple paternities amounted to at least 50– males, females not only spent more time with a single male 80% of litters. In captive groups consisting of 4 male and 6 or but also directed more contact and sociopositive behaviors February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 45 toward this preferred male (Hohoff 2002). Adrian et al. Females of M. australis can be found most of the time in the (2008b) measured the effects of separation and subsequent vicinity of a bush or a group of bushes, whereas males wander reunion in established pairs of G. monasteriensis on stress around visiting different female sites (Rood 1970, 1972). A hormones and behavior of males. If the female was removed particular plant structure, weeping branches of certain plant from the home enclosure, blood cortisol levels of the male species almost reaching the ground, are used preferentially by increased significantly. Upon reunion, a decline in cortisol M. australis (Tognelli et al. 1995). Underneath these bushes levels was noticeable. Reunion also led to increased socio- burrow systems are located in which the animals spend the positive and courtship and sexual behaviors of the male night. Several cavies share such a burrow system with a toward the female and to more spatial proximity. Agonistic number of entrance holes and nests and form a social unit, also behaviors never were observed during reunion. These effects called nesting association (Contreras and Roig 1978; Eben- of separation from and reunion with a partner point to a social sperger et al. 2006; Lu¨ttmann 2006; Ranft 2005). No switching Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 bond between the male and the female of a pair of G. of females between nesting associations over a study period of monasteriensis. about 1–2 weeks suggested some stability of associations In contrast to G. musteloides and G. spixii, where males (Ebensperger et al. 2006). Newly established social units never engage in direct paternal activities and treat even their consist exclusively of young animals, which indicates own offspring rather aggressively, males of G. monasteriensis dispersal from the native unit at adolescence (Contreras and exhibit social play and grooming behavior with their offspring Roig 1978). Social units can comprise between 2 and 38 (Adrian et al. 2005). Offspring-directed aggression is rare. members with various sex ratios (Contreras and Roig 1978; When transferred with her pups to an unfamiliar environment, Ebensperger et al. 2006). Adult males do not associate with a a mother of G. monasteriensis has an attenuating influence on specific nesting association but spend successive nights in her pups’ increased blood cortisol levels, and mother– nests of different social units (Lu¨ttmann 2006; Ranft 2005). offspring interactions are characterized by physical closeness Some animals of both sexes do not share nests with and sociopositive behavior (Hennessy et al. 2006). Such an conspecifics (Ebensperger et al. 2006). influence is not found when the pups are transferred to an Animals show high fidelity to their burrow systems, fleeing unfamiliar female. In contrast, interactions between pups of C. to the nearest entrance of their system in the event of danger, aperea and their mother and interactions between the pups and even when many entrance holes to burrow systems of other an unfamiliar female do not differ markedly. groups are closer. Members of a social unit defend their The high incompatibility between adults, the existence of a burrow system against nonmembers (Contreras and Roig social bond with physiological correlates, and the frequency 1978). Above the ground no territorial behavior is obvious, of paternal behaviors are strong evidence for a pair-based and space is shared among members of different social units social system in G. monasteriensis (Table 2). Other data also that interact during aboveground activities (Contreras and argue for a monogamous mating system. In 4-male choice Roig 1978). However, home ranges of both males and females tests conducted by Hohoff (2002) the socially preferred male of the same social unit overlap extensively (.60% on was always a copulation partner of the female—although average—Ebensperger et al. 2006; Lu¨ttmann 2006; Ranft several females copulated with 2 males—and he gained a 2005), whereas overlap of animals from different social units higher number of copulations than the 2nd male. In contrast is much lower, usually ,10%. Male home ranges are about to females of G. musteloides tested in identical experiments, twice the size of those of females (Table 1; Ebensperger et al. copulations with 3 or all 4 males never occurred. In the 2- 2006; Lu¨ttmann 2006; Ranft 2005; Rood 1970, 1972). male choice tests multiple paternities did not occur in litters Social tolerance is higher in M. australis than in C. aperea resulting from these tests, and in 7 of 8 litters the socially or G. musteloides (Rood 1972). Among males relationships preferred male sired the offspring (Adrian et al. 2008b). are hostile, but aggressive interactions are avoided and Multiple paternities also did not occur in other choice tests physical injuries are rare. Data on dominance relationships (Hohoff 2002; Hohoff et al. 2002). All of 15 litters of 2 are ambiguous. Both a stable, linear hierarchy (Rood 1970, pups resulting from these experiments were sired by a single 1972) among males with overlapping home ranges and a lack male. A reversed sexual size dimorphism in G. monaster- of a rigid linear hierarchy (Contreras and Roig 1978) have iensis,withfemalesbeing9% heavier than males (Hohoff et been reported. The character of female–female interactions al. 2002), points to little direct male competition for access to varies. Aggressive and amicable interactions can be observed females. (Rood 1970, 1972). This variation might depend on the Microcavia australis.—This species occurs throughout most membership of females in social units. In a discrete social unit of western and southern Argentina and some parts of southern of 4 females and 4 males, female–female interactions were Chile in arid and semiarid habitats (Tognelli et al. 2001). It is predominantly sociopositive, and agonistic interactions oc- sympatric with G. musteloides at some locations but has much curred rarely. Females initiated social interactions with other higher population densities (Contreras 1966; Rood 1969, females much more often than they did with males (Lu¨ttmann 1970). Relationships between the 2 species are amicable; 2006). Such amicable social interactions among females animals use the same runways and burrow systems, and contrast strikingly with female–female relationships in other interspecific grooming occurs (Rood 1970). cavy species, particularly with those of G. monasteriensis, 46 JOURNAL OF MAMMALOGY Vol. 92, No. 1 which exhibits complete intrasexual incompatibility. Male– Brazil. It is associated with rock piles, where it takes refuge female interactions are almost always amicable (Rood 1970, from predators and unpleasant weather conditions. K. rupestris 1972) and usually initiated by the males. Individuals of M. climbs in trees and shrubs to feed on leaves (Lacher 1981). australis can be seen regularly resting together in bodily Males defend a rock pile and aggressively exclude other contact. These groups contain several females and juveniles males from this resource, and several females inhabit the rock but usually only 1 adult male. Huddling during severe weather pile of a dominant male. Thus, a 1-male–multifemale (harem) conditions could serve to conserve body heat (Rood 1970). group is formed (Table 2). In captive groups dominance Allonursing is common (Contreras and Roig 1978; Rood hierarchies among females are linear, whereas male hierar- 1970, 1972), particularly when females inhabit the same bush; chies are not (Lacher 1981). Male–male behavior is usually however, females can discriminate between their own pups aggressive, but sociopositive behavior can occur in groups and those of other females. They occasionally are aggressive with an established dominance hierarchy. In the captive Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 toward other pups attempting to suckle (Rood 1970). colony studied by Lacher (1981) the alpha male was groomed Originally, social groups of M. australis were described as frequently by subordinate males. The beta male also was noncohesive, mere aggregations at resources (Rood 1970). groomed but never groomed other males. Social grooming Subsequent studies emphasized that the animals do not merely never was observed among females, and it was infrequent aggregate but form stable social units (Contreras and Roig between males and females. Other social behaviors (crawl- 1978; Ebensperger et al. 2006; Lu¨ttmann 2006; Ranft 2005) over and huddling) did occur between females. However, that are female-centered, with males associating more loosely aggression among females is pronounced in this species. High with female units (Table 2). Contradictory results possibly can stress levels of females, due to female–female aggression and be ascribed to intraspecific variation of the social organiza- female aggression toward juveniles other than their own, tion. might be responsible for the high juvenile mortality (Lacher During the reproductive season Contreras and Roig (1978) 1981). Females seem to belong to the same harem due to their observed an increased tendency of males of M. australis to reliance on the shelter site only. The harem is an internally move to the areas of neighboring social units. Males competitive group; frequent aggression toward offspring of sometimes form temporary associations with gravid and other females of the same harem points to competition among lactating females and spend several hours each day with them females (Lacher 1981). (Rood 1970, 1972). At the time of female estrus, intermale Males are very tolerant toward their offspring. In captive aggression is enhanced. Several males congregate in the pairs of K. rupestris males spent much time with the young vicinity of the female’s home bush, and the dominant male and exhibited paternal behaviors such as grooming them and frequently attacks and chases away his rivals when they huddling with them (Tasse 1986). approach the female. However, this mate-guarding is not very In the captive colony observed by Lacher (1981) the alpha successful. As in G. musteloides, mating chases involving male and some subadult males, but not the beta male, were several males occur, and a female usually mates with several involved in mating chases with a female in estrus. The mating males. In contrast to G. musteloides, copulation by a male system of K. rupestris has been named resource-defense during mating chases often is impeded by frequent attacks by polygyny (Lacher 1981); however, no genetic data on the other males. Successful copulations occur more often when a mating system are available. Contrary to the pattern observed single male encounters a receptive female (Rood 1970). in other polygynous mammals, sexual size dimorphism is not Although body size in this species varies according to found in K. rupestris. climatic differences within the total distribution area (Tar- aborelli et al. 2007), no sexual dimorphism in body mass exists in M. australis (Lu¨ttmann 2006; Ranft 2005; Taraborelli ROLE OF FEMALES AND MALE POTENTIAL TO and Moreno 2009). All available data point to a promiscuous MONOPOLIZE THEM mating system in this species (Table 2); however, no genetic The active role of females in shaping the social and mating data exist on the incidence of multiple paternity. system of a species has long been underestimated, particularly Microcavia niata.—Two field colonies studied in northern in mammals (Clutton-Brock and McAuliffe 2009). In G. Chile consisted of 15 and 17 individuals, respectively, living musteloides, however, female behavior is obviously a decisive in small areas of 100 m2 each (Marquet et al. 1993). The factor that prevents monopolization by males. Receptive smaller colony consisted of 2 adult males, 5 adult females, and females suddenly start racing around, often changing direction 8 juveniles. Neither sexual nor agonistic behaviors were and then stopping abruptly. The females thus attract the observed, but sociopositive interactions, mainly grooming, attention of all nearby males, which then participate in a occurred among colony members. Cavies reacted highly mating chase (Rood 1972; Schwarz-Weig and Sachser 1996). aggressively toward intrusions of noncolony members. They The male closest to the female tries to position its chin on the retreated into their burrow system when a colony member rump of the female while both animals are moving. Other emitted alarm calls (Marquet et al. 1993). males follow in a row. The alpha male shows this courtship Kerodon rupestris.—This species is a habitat specialist behavior of chin–rump-follows with the highest frequency. restricted to the Caatinga, a semiarid region in northeastern When the female stops, the male behind her mounts to February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 47 copulate. Although a copulating male is sometimes pushed of the offspring operates via sperm competition rather than away by another male, in most cases the queuing males wait directly (see below). Detailed studies on paternities and until copulation has finished. They then resume the mating possible fitness benefits of female polyandrous mating, as chase until the female stops again and another male mounts to demonstrated in G. musteloides, are needed for M. australis. copulate. A female often does not terminate her soliciting The promiscuous behavior of G. musteloides and M. behavior until all males present have copulated with her australis contrasts sharply with that of G. monasteriensis.In (Schwarz-Weig and Sachser 1996). the latter species females mate with 1 or 2 males, even when In choice tests with G. musteloides, in which a female had they could mate with up to 4 males in a mate-choice apparatus access to 4 males while direct male–male competition and (Adrian 2001; Hohoff 2002). Mate switching is rare and so is harassment of the female by the males were prevented, 7 of 10 extensive sperm mixing. Females of G. monasteriensis females copulated with 2 males and 1 each with 3 and all 4 obviously exhibit a different behavioral strategy than females Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 males, respectively (Hohoff et al. 2003). Males gained a of G. musteloides. G. monasteriensis is the only cavy species median number of 12 copulations. These were not in direct where the existence of a pair-bond has been demonstrated succession, however; females switched partners several times, experimentally (Adrian et al. 2008b). In addition, paternal thus mixing up sperm extensively. First-mating males did not behaviors (grooming and playing with the young) are gain significantly higher numbers of copulations than 2nd- performed frequently compared to other species (Adrian et mating males. However, males with higher within-trial body- al. 2005). Because G. monasteriensis lives in high-altitude mass rank gained a higher number of copulations. A habitats in the Bolivian Andes where climatic conditions can significant correlation was found between the number of male be harsh, a female might need a male partner to raise offspring courtship behavior acts elicited and the number of copulations successfully. For a male it might pay to stay, where the gained. Females thus exercised mate choice by favoring probability of paternity is high, rather than roaming in search heavier, more-courting males, and simultaneously enabled of polygynous matings. In the cavies a general link between sperm competition by switching between multiple partners. probability of paternity and paternal behavior exists. Males of Because reproductive monopolization of a female by a male is G. monasteriensis and C. aperea, both with 1-male systems circumvented by the behavior of the female, no selective and no or a low frequency of multiple paternities, frequently pressure for the evolution of a large male body mass (as a show paternal behaviors, whereas no paternal behavior is proxy of fighting strength) acted upon males. The high observed in G. musteloides, which mates promiscuously and percentage of multiple paternities found both in captive groups has a high frequency of litters with multiple paternity (Adrian and in the field (M. Asher, University of Mu¨nster, pers. et al. 2005). comm.; Keil et al. 1999) reflects female promiscuity and In C. aperea the tendency of females to copulate inability of males to monopolize females. polyandrously is much lower than in G. musteloides. However, Females gain fitness benefits through their polyandrous in a 4-male mate choice experiment, half of the 12 females mating behavior (Keil and Sachser 1998). Proportions of tested copulated with .1 male (Hohoff 2002). Polyandrously females of G. musteloides that became gravid, litter sizes, and mating females had significantly more stillborn offspring than birth mass of offspring did not differ between females paired did monandrously mating females (Hohoff 2002). This with either 4 males or a single male; however, females paired analysis, however, was based on the total number of pups. If with a single male had significantly more stillborn offspring the number of females with and without stillborn offspring and offspring that died before weaning. Thus, females paired was compared, the difference between polyandrously and with 4 males weaned significantly more young. Although we monandrously mating females was not significant. In contrast can only speculate about the mechanisms responsible for this to G. musteloides, in the choice tests with C. aperea 1 male difference, this is a rare example of direct fitness benefits of was clearly preferred as social partner, and this male gained polyandrous mating in a mammal (Alcock 2005). the highest number of copulations. Mate switching was much Males of G. musteloides, however, do not lack counter- rarer; 4 of the 6 females mating with several males changed strategies to gain fitness benefits. Keil et al. (1999) determined their copulation partner only once, and the other 2 females male dominance ranks in mixed-sex groups and subsequently changed them twice and 5 times, respectively. DNA analysed paternities. Males of all ranks sired offspring. Yet, fingerprinting of litters resulting from the mate-choice tests higher ranking males sired significantly more offspring than revealed that all pups were sired by preferred partners of lower ranking individuals. The authors suggest that the high females (Hohoff 2002). Mating order did not seem to affect level of aggression among males of G. musteloides might probability of successful fertilization. suppress the gonadal activity in lower ranking males, giving In females of C. aperea mate choice is much more dominant males an advantage in sperm competition (see also pronounced than in G. musteloides. Adrian et al. (2008a) Kruczek and Styrna 2009). found that male body mass predicted female preferences. In In M. australis mating behavior also is promiscuous. From contrast, male body mass was not a significant factor in what is known from the field, females likely play the same determining copulation success in another study (Hohoff role in the mating system as in G. musteloides. Males cannot 2002). In the natural habitat the significance of female mate successfully monopolize females. Competition for parentage choice in C. aperea is difficult to evaluate. This species 48 JOURNAL OF MAMMALOGY Vol. 92, No. 1 usually lives in habitats with abundant food resources throughout the year (Asher et al. 2004), leading to stable and relatively small home ranges (Table 1); thus several females are found close to each other in small areas. Such a situation generally generates a high environmental potential for male polygamy (Emlen and Oring 1977), because defense of several females against other males becomes feasible and females can be monopolized by powerful males. However, because female home ranges overlap only partially due to the uniform distribution of abundant food plants, males can establish only small harems (Asher et al. 2004). Selection Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 pressure of direct male–male competition has led to the FIG.2.—Males of Microcavia australis, Cavia aperea, and Galea evolution of a sexual size dimorphism in C. aperea. Because musteloides (left to right) during the breeding season. Whereas the polygynous C. aperea has relatively small testes, those of the 2 the females of the same harem avoid each other, harem males promiscuous species are extremely large (photographs by K. cannot guard and defend all of their females simultaneously, Lu¨ttmann, S. Ranft, and M. Asher). creating opportunities for female mate choice and extragroup copulations. Gonad size is not the only adaptation of male reproductive For K. rupestris, the rock piles where animals take shelter physiology. Sperm characteristics also differ significantly are critical, highly clumped resources. Females rely on these among cavy species with different mating systems (Cooper et resources for reproduction. Thus, several females gather at al. 2000). Sperm of C. aperea are larger than those of G. single rock piles and create the potential for males to musteloides, swim faster, and are more prone to acrosome monopolize them. However, in contrast to C. aperea, where damage. Smaller size of sperm of G. musteloides allows the female-defense polygyny is present, K. rupestris exhibits production of even higher sperm numbers (see also Holt resource-defense polygyny. A female can mate outside the 1977). In the monogamous G. monasteriensis the percentages rock piles, and whether females frequently perform extragroup of motile sperm and sperm with intact acrosomes in the cauda copulations is not known. epididymidis are distinctly lower than in G. musteloides. Different sperm characteristics likely also evolved as adaptations to female estrous types. As all cavies, female G. ADAPTATIONS OF REPRODUCTIVE PHYSIOLOGY musteloides exhibit postpartum estrus (Weir 1974). If they are Both male and female cavies exhibit adaptations in isolated at this time or fail to conceive after mating, the next reproductive physiology to the mating system of their species. estrus is induced by the presence of a male (Touma et al. In promiscuous mating systems sperm competition can replace 2001). Although Weir (1971, 1973) argued that direct physical contest competition in males. Hence, males are selected for the contact was necessary to induce estrus, Touma et al. (2001) number and quality of their sperm and—because sperm found that contact through a wire mesh was sufficient to number depends on gonad size—for high testes and epidid- induce vaginal estrus within 2–3 days. Ovulation then ymides mass. In single-male mating systems (monogamy and occurred spontaneously without stimuli from copulation. polygyny with female monandrous mating) gonad size is Because ovulation takes place several hours after sperm comparatively small (Kenagy and Trombulak 1986; Munshi- deposition (Weir 1971), sperm of G. musteloides will have South 2007; Ramm et al. 2005) because few sperm suffice to been selected for longevity rather than velocity. fertilize the females. The induction of estrus is atypical for caviomorph rodents The relationship described above is obvious in the cavies (Weir 1974). It is an advantage if population density is very (Fig. 2; Table 2). Male relative testes mass in the promiscuous low and males are not constantly present at a female’s living G. musteloides is among the highest recorded for mammals site, which might be the case in some populations of G. (Cooper et al. 2000; Sachser et al. 1999). Relative testes mass musteloides. This species is a habitat generalist and also is almost 3 times higher than in the polygynous C. aperea, and dwells in deserts and other areas not supporting large groups relative epididymides mass is more than twice as high (Cooper of animals. Population densities of G. musteloides generally et al. 2000). Relative testes and epididymides masses of males have been reported to be lower than those of M. australis of G. musteloides also are significantly higher than those of (Contreras and Roig 1978; Rood 1969, 1970, 1972). Induced males of the monogamous G. monasteriensis (Hohoff et al. estrus allows a solitary nongravid female to resume reproduc- 2002). During the reproductive season males of the promis- tion immediately when she encounters a fertile male. cuous M. australis show very large scrotal testes (K. Microcavia australis has an estrous cycle of approximately Lu¨ttmann, University of Mu¨nster, pers. comm.), similar to 15 days (Rood 1972). Because males are always present in this those of G. musteloides. Gonad size is not maintained group-living species, no advantage for induced estrus exists. throughout the year. In G. musteloides (Gutie´rrez et al. The same is true for C. aperea. Estrus occurs spontaneously 1995) and C. aperea (Barlow 1969) gonads regress in winter and is followed by spontaneous ovulation and corpus luteum when reproduction is minimal. activity. Touma et al. (2001) found a median cycle length of February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 49

15 days, whereas other authors reported a mean cycle length of In addition to resource distribution, other ecological factors 20.6 days (Rood and Weir 1970; Weir 1970). The cyclicity of such as predation pressure, climatic conditions, and, in female estrus, in combination with a short receptive phase burrowing species, soil characteristics might be important to around ovulation and a polygynous–monandrous (1-male) the development of a given social system. Predation pressure mating system, might have favored the evolution of larger, is high in both C. aperea and M. australis (Asher et al. 2004, faster sperm in lower numbers in C. aperea than in G. 2008; Taraborelli et al. 2008). Comparing both species, we can musteloides. see that different strategies might have arisen to solve the same problem. M. australis was studied at 2 sites in Argentina that differed in predation risk (Taraborelli et al. 2008). At El ENVIRONMENTAL FACTORS Leoncito, where plant cover is lower, cavies responded earlier

The social organization of animals is dependent in part on when predator models were presented than at N˜ acun˜a´n. Group Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 the environment. For only some cavy species are data size of cavies affected vigilance behavior. Although cavies did available concerning both the social and mating systems and not forage farther from their burrow when a higher number of the ecological conditions under which they live. These will be individuals was present, individual vigilance decreased with exemplified here. larger group size while total group vigilance increased Resource distribution is an important factor affecting social (Taraborelli 2008). Increased group vigilance can enhance organization. K. rupestris, for example, relies on rock piles. survival in the presence of multiple predators. Vigilance These are clumped, and hence females aggregate at this behavior of M. australis is thus in accordance with the resource, providing the basis for the harem–resource-defense hypothesis that the degree of sociality is related to predation polygyny system of the species (Lacher 1981). In C. magna risk in caviomorph rodents (Ebensperger 1998; Ebensperger frequent flooding of the habitat leads to frequent changes of and Blumstein 2006—but compare the situation for C. aperea the distribution of areas with food and shelter prompting the described below). In M. niata enhanced vigilance for predator cavies to shift their home ranges regularly (Kraus et al. 2003). detection appears to represent a benefit of group living as well. The unpredictable location of females prevents males from Marquet et al. (1993) observed cavies to flee into their burrow monopolizing them and is a definitive factor for the solitary– system upon alarm calling from group members. promiscuous system. Cavia aperea uses a very different antipredator strategy The distribution of food resources is a codetermining factor compared to M. australis. This species has no burrows in for differences in the social organization of C. aperea and G. which to seek shelter from predators. When threatened the musteloides. Although both species might be sympatric at some animals freeze or dash into dense vegetation where they freeze locations (Contreras 1966), the typical habitat of C. aperea is and allow a predator or a human to approach within a few more humid, with abundant food that supports high numbers of meters (Asher et al. 2008; Rood 1972). Such a cryptic cavies with small home ranges. The even distribution of food predator-avoidance strategy precludes the evolution of large does not lead to a clumping of females as in K. rupestris, and groups, because the presence of many active animals in a males of C. aperea can monopolize only 1 or a few females, small area increases the risk of detection by a predator. thus forming pairs or small harems (Asher et al. 2004, 2008). In Foraging groups of C. aperea are small and often only contrast, the typical habitat of G. musteloides is dryer, and comprise 2 animals (Asher et al. 2004, 2008). Cassini (1991) vegetation might be sparse. Under such conditions competition suggested that foraging in groups is an antipredator strategy of for food is high, and the cavies use larger areas to find enough C. aperea similar to that of M. australis. Cavies had longer food leading to the solitary lifestyle of this species and to foraging bouts and scanned the environment marginally less nonoverlapping home ranges of the females (M. Asher, frequently when foraging in a group. However, the observa- University of Mu¨nster, pers. comm.). Males, in turn, roam tion that usually a harem male and 1 of his females form such even more widely in search of receptive females (Table 1). foraging groups, whereas 2 females very rarely do so (Asher et Because G. musteloides is a habitat generalist, the species might al. 2008), might indicate that in addition to increased vigilance exhibit a different social organization in habitats with more mate-guarding is another cause of group foraging in C. aperea. abundant food. Observations by Rood (1972) hint at such a Potential benefits of group living, other than group conclusion, because he described multimale–multifemale vigilance, were tested in M. australis by comparing popula- groups rather than solitary animals. M. australis also occurs tions from the 2 sites in Argentina differing in climatic sympatrically with G. musteloides at some locations (Contreras conditions and food resource availability (Taraborelli 2009; 1966; Lu¨ttmann 2006; Rood 1969, 1972). Whereas the latter Taraborelli and Moreno 2009). At El Leoncito population primarily feeds on grasses, M. australis has exploited another density was almost 4 times higher than at N˜ acun˜a´n food resource by climbing into shrubs and trees to feed on (Taraborelli and Moreno 2009). Social groups were formed leaves and fruits (Campos et al. 2001; Monge et al. 1994). This of 5 individuals on average at El Leoncito and of 3.3 habit of 3-dimensional foraging supports higher population individuals at N˜ acun˜a´n. At El Leoncito the index of densities compared to those found in G. musteloides, which association among individuals was significantly higher and might have influenced the evolution of a higher social tolerance the rate and proportion of agonistic behavior were lower than in M. australis. at N˜ acun˜a´n. El Leoncito is the site with stronger climatic 50 JOURNAL OF MAMMALOGY Vol. 92, No. 1 harshness and lower winter temperatures (down to 24uC— RESUMEN Taraborelli 2009); having larger groups here could serve for Los cuyes o conejillos de Indias y sus aliados (familia more effective social thermoregulation. Stronger association Caviidae) son un grupo de roedores distribuidos sobre casi en and less agonistic behavior among members of a social group toda Sud Ame´rica. La alta diversidad de los ha´bitats ocupados point to higher social tolerance, which might be an adaptation por especies diferentes va acompan˜ado por una alta diversidad to reduce water and energy loss in this harsh environment. de las organizaciones sociales. Por consiguiente, las compar- Sharing costs of burrow construction and maintenance also aciones de estrategias del comportamiento y de la reproduc- is often quoted as an advantage of group living in burrowing cio´n entre las especies pueden proporcionar un mejor species. Communal burrowing was identified as a general entendimiento de la evolucio´n social de estos mamı´feros. En factor in the evolution of group living in caviomorph rodents este trabajo, se resume primero la literatura con respecto a la

(Ebensperger and Blumstein 2006; Ebensperger and Cofre´ diversidad de los sistemas sociales y del apareamiento de los Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 2001). Comparison of burrow systems of M. australis at El ge´neros Cavia, Galea, Microcavia y Kerodon. Los sistemas Leoncito and N˜ acun˜a´n showed that they were significantly sociales se extienden de animales solitarios a parejas, harenes smaller and less complex at El Leoncito (Taraborelli 2009) y grupos de varios machos y varios hembras. Los sistemas de where soils are softer and hence energetic costs of burrow apareamiento de los cuyes incluyen monogamia y promiscu- digging should be lower. At El Leoncito social groups idad ası´ como diversas formas de poliginia. Luego evaluamos contained a higher number of animals than at N˜ acun˜a´n. No las estrategias del comportamiento de hembras y machos que linear relationship was found between group size and areas causan esta diversidad social. Se examino´ particularmente el encompassed by burrow systems. Thus, in contrast to benefits papel de las hembras y el potencial de los machos para from group vigilance and more effective thermoregulation, the monopolizar parejas. En algunas especies, por ejemplo, las hypothesis that larger groups form to share costs of burrow hembras en estro solicitan activamente copulaciones con construction and maintenance is not supported in M. australis. varios machos y de tal modo previenen su monopolizacio´n por un u´nico macho. Adema´s discutimos las adaptaciones de la fisiologı´a reproductiva de diversos sistemas de apareamiento. CONCLUDING REMARKS Finalmente, se consideranon los factores ambientales que A high diversity of social and mating systems exists within influencian aspectos en los sistemas sociales y de aparea- the cavies, a group with relatively few species. Earlier miento de los cuyes. En particular, las diferencias en la generalizations that they would exhibit promiscuous mating distribucio´n de los recursos, el riesgo de la depredacio´n y las systems, form no permanent social bonds, and live in condiciones clima´ticas pudieron explicar la gran variacio´n en noncohesive groups that are nothing more than aggregations la organizacio´n social de las especies. associated with natural resources (Rood 1972) have turned out to be inadequate. Phylogenetic constraints, although suggested ACKNOWLEDGMENTS by Rowe and Honeycutt (2002), appear not to play a We thank M. Asher for providing unpublished field data on G. fundamental role in the evolution of social organizations in musteloides.K.Lu¨ttmann, S. Ranft, and M. Asher took the cavies. Consider the remarkable differences that can be found photographs of the cavies. We are grateful to the guest editors of even within the same genus as, for example, between G. this special issue, L. Hayes and L. Ebensperger, for inviting us to musteloides and G. monasteriensis or C. aperea and C. magna contribute a paper. Comments by E. Herrera, J. Koprowski, and 2 (Trillmich et al. 2004). These differences provide strong anonymous reviewers were very helpful in improving earlier drafts of evidence that ecological factors are more important (Lacher the manuscript. Our studies on cavies have been supported 1982) and have shaped the morphology, physiology, and continuously by grants of the German Research Foundation behavior of individuals. Male and female reproductive and (Deutsche Forschungsgemeinschaft) to NS. Current funding: behavioral strategies under given environmental conditions FOR1232; Sa389/11-1. bring about the different social and mating systems whereby females are significantly involved in this process. LITERATURE CITED Studies on the social life of cavies already have provided ADRIAN, O. 2001. Das Partnerwahlverhalten der Weibchen einer neu valuable insights into the social evolution of this group and of entdeckten su¨damerikanischen Nagetierart. M.S. thesis, University mammals in general. However, further studies could increase of Mu¨nster, Mu¨nster, Germany. our understanding of the mechanisms and functions underly- ADRIAN, O., I. BROCKMANN,C.HOHOFF, AND N. SACHSER. 2005. ing the formation of different social and mating systems. Paternal behaviour in wild guinea pigs: a comparative study in Research on intraspecific variation in social organization three closely related species with different social and mating systems. Journal of Zoology (London) 265:97–105. deserves more attention. The wide distribution of some cavy ADRIAN, O., G. DEKOMIEN,J.T.EPPLEN, AND N. SACHSER. 2008a. Body species and their occurrence in various habitats are promising weight and rearing conditions of males, female choice and paternities prerequisites. Also, genetic studies on paternities and degrees in a small mammal, Cavia aperea. Ethology 114:897–906. of kinship within groups could reveal fitness benefits of ADRIAN, O., ET AL. 2008b. Female influences on pair formation, different behavioral and reproductive strategies that determine reproduction and male stress responses in a monogamous cavy what we observe as social and mating systems. (Galea monasteriensis). Hormones and Behavior 53:403–412. February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 51

ALCOCK, J. 2005. Animal behavior: an evolutionary approach. 8th ed. EBENSPERGER, L. A., P. TARABORELLI,S.M.GIANNONI,M.J.HURTADO, Sinauer Associates, Inc., Publishers, Sunderland, Massachusetts. C. LEO´ N, AND F. BOZINOVIC. 2006. Nest and space use in a highland ASHER, M., T. LIPPMANN,J.T.EPPLEN,C.KRAUS,F.TRILLMICH, AND N. population of the southern mountain cavy (Microcavia australis). SACHSER. 2008. Large males dominate: ecology, social organization, Journal of Mammalogy 87:834–840. and mating system of wild cavies, the ancestors of the domestic EISENBERG, J. F. 1989. Mammals of the Neotropics. Vol. 1. The guinea pig. Behavioral Ecology and Sociobiology 62:1509–1521. northern Neotropics: Panama, Colombia, Venezuela, Guyana, ASHER, M., E. SPINELLI DE OLIVEIRA, AND N. SACHSER. 2004. Social Suriname, French Guiana. University of Chicago Press, Chicago, system and spatial organization of wild guinea pigs (Cavia aperea) Illinois. in a natural population. Journal of Mammalogy 85:788–796. EISENBERG, J. F., AND K. H. REDFORD. 1999. Mammals of the BARLOW, J. C. 1969. Observations on the biology of rodents in Uruguay. Neotropics. Vol. 3. The central Neotropics: Ecuador, Peru, Bolivia, Life Sciences Contributions, Royal Ontario Museum 75:1–59. Brazil. University of Chicago Press, Chicago, Illinois.

BIRKHEAD, T. R., AND A. P. MØLLER. 1992. Sperm competition in EMLEN, S. T., AND L. W. ORING. 1977. Ecology, sexual selection, and Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 birds: evolutionary causes and consequences. Academic Press, the evolution of mating systems. Science 197:215–223. Orlando, Florida. FUCHS, S. 1980. Spacing patterns in a colony of guinea pigs: BIRKHEAD, T. R., AND A. P. MØLLER. 1995. Extra-pair copulation and predictability from environmental and social factors. Behavioral extra-pair paternity in birds. Animal Behaviour 49:843–848. Ecology and Sociobiology 6:265–276. BONAVENTURA, S. M., V. PANCOTTO,R.L.VICARI,N.MADANES, AND GUTIE´ RREZ, L. S., M. H. BURGOS, AND S. D. BRENGIO. 1995. Cauda M. I. BELLOCQ. 2003. Demography and microhabitat use of the wild epididymis of Galea musteloides in periods of reproduction and guinea pig (Cavia aperea) in freshwater Spartina densiflora gonadal regression. I. Ultrastructural and cytochemical studies. marshes in Argentina. Acta Zoologica Sinica 49:20–31. Biocell 19:141–151. CAMPOS, C., R. OJEDA,S.MONGE, AND M. DACAR. 2001. Utilization of HENNESSY, M. B., G. NEISEN,K.L.BULLINGER,S.KAISER, AND N. food resources by small and medium-sized mammals in the Monte SACHSER. 2006. Social organization predicts nature of infant–adult Desert biome, Argentina. Austral Ecology 26:142–149. interactions in two species of wild guinea pigs (Cavia aperea and CASSINI, M. H. 1991. Foraging under predation risk in the wild guinea Galea monasteriensis). Journal of Comparative Psychology 120: pig Cavia aperea. Oikos 62:20–24. 12–18. CASSINI, M. H., AND M. L. GALANTE. 1992. Foraging under predation HERRERA, E. A., V. SALAS,E.R.CONGDON,M.J.CORRIALE, AND risk in the wild guinea pig: the effect of vegetation height on Z. TANG-MARTI´NEZ. 2011. Capybara social structure and dis- habitat utilization. Annales Zoologici Fennici 29:285–290. persal patterns: variations on a theme. Journal of Mammalogy CHEREM, J. J., J. OLIMPIO, AND A. XIMENEZ. 1999. Descric¸ao de uma 92:12–20. nova especie do geˆnero Cavia Pallas, 1766 (Mammalia—Caviidae) HOHOFF, C. 2002. Female choice in three species of wild guinea pigs. das Ilhas dos Moleques do Sul, Santa Catarina, Sul do Brasil. Ph.D. dissertation, University of Mu¨nster, Mu¨nster, Germany. Biotemas 12:95–117. HOHOFF, C., K. FRANZEN, AND N. SACHSER. 2003. Female choice in a CLUTTON-BROCK, T. H., AND P. H. HARVEY. 1978. Mammals, resources promiscuous wild guinea pig, the yellow-toothed cavy (Galea and reproductive strategies. Nature 273:191–195. musteloides). Behavioral Ecology and Sociobiology 53:341–349. CLUTTON-BROCK, T., AND K. MCAULIFFE. 2009. Female mate choice in HOHOFF, C., ET AL. 2002. Monogamy in a new species of wild guinea mammals. Quarterly Review of Biology 84:3–27. pigs (Galea sp.). Naturwissenschaften 89:462–465. CONTRERAS, J. R. 1966. Un caso de simpatrı´a entre tres generos de la HOLT, W. V. 1977. Postnatal development of the testes in the cuis, subfamilia Caviinae (Mammalia, Rodentia). Physis 26:111–112. Galea musteloides. Laboratory Animals 11:87–91. CONTRERAS, J. R., AND V. G. ROIG. 1978. Observaciones sobre la HU¨ CKINGHAUS, F. 1961. Zur Nomenklatur und Abstammung des organizacio´n social, la ecologı´a y la estructura de los habita´culos Hausmeerschweinchens. Zeitschrift fu¨rSa¨ugetierkunde 26:108–111. de Microcavia australis australis en N˜ acun˜a´n, provincia de KEIL, A., J. T. EPPLEN, AND N. SACHSER. 1999. Reproductive success of Mendoza. Ecosur 5:191–199. males in the promiscuous-mating yellow-toothed cavy (Galea COOPER, T. G., S. WEYDERT, C.-H. YEUNG,C.KU¨ NZL, AND N. SACHSER. musteloides). Journal of Mammalogy 80:1257–1263. 2000. Maturation of epididymal spermatozoa in the nondomesti- KEIL, A., AND N. SACHSER. 1998. Reproductive benefits from female cated guinea pigs Cavia aperea and Galea musteloides. Journal of promiscuous mating in a small mammal. Ethology 104:897–903. Andrology 21:154–163. KENAGY, G. J., AND C. TROMBULAK. 1986. Size and function of DIGBY, L. J. 1999. Sexual behavior and extragroup copulations in a mammalian testes in relation to body size. Journal of Mammalogy wild population of common marmosets (Callithrix jacchus). Folia 67:1–22. Primatologica 70:136–145. KRAUS, C., J. KU¨ NKELE, AND F. TRILLMICH. 2003. Spacing behaviour DUNNUM, J. L., AND J. SALAZAR-BRAVO. 2010. Phylogeny, evolution, and its implications for the mating system of a precocial small and systematics of the Galea musteloides complex (Rodentia: mammal: an almost asocial cavy Cavia magna? Animal Behaviour Caviidae). Journal of Mammalogy 91:243–259. 66:225–238. EBENSPERGER, L. A. 1998. Sociality in rodents: the New World KRUCZEK, M., AND J. STYRNA. 2009. Semen quantity and quality fossorial hystricognaths as study models. Revista Chilena de correlate with bank vole males’ social status. Behavioural Processes Historia Natural 71:65–77. 82:279–285. EBENSPERGER, L. A., AND D. T. BLUMSTEIN. 2006. Sociality in New KU¨ NKELE, J., AND H. N. HOECK. 1989. Age-dependent discrimination World hystricognath rodents is linked to predators and burrow of unfamiliar pups in Galea musteloides (Mammalia, Caviidae). digging. Behavioral Ecology 17:410–418. Ethology 83:316–319. EBENSPERGER, L. A., AND H. COFRE´ . 2001. On the evolution of group- KU¨ NKELE, J., AND H. N. HOECK. 1995. Communal suckling in the cavy living in the New World cursorial hystricognath rodents. Galea musteloides. Behavioral Ecology and Sociobiology 37:385– Behavioral Ecology 12:227–236. 391. 52 JOURNAL OF MAMMALOGY Vol. 92, No. 1

KU¨ NZL, C., S. KAISER,E.MEIER, AND N. SACHSER. 2003. Is a wild ROOD, J. P. 1970. Ecology and social behavior of the desert cavy mammal kept and reared in captivity still a wild animal? Hormones (Microcavia australis). American Midland Naturalist 83:415–454. and Behavior 43:187–196. ROOD, J. P. 1972. Ecological and behavioural comparisons of three KU¨ NZL, C., AND N. SACHSER. 1999. The behavioral endocrinology of genera of Argentine cavies. Animal Behaviour Monographs 5: domestication: a comparison between the domestic guinea pig 1–83. (Cavia aperea f. porcellus) and its wild ancestor, the cavy (Cavia ROOD, J. P., AND B. J. WEIR. 1970. Reproduction in female wild aperea). Hormones and Behavior 35:28–37. guinea-pigs. Journal of Reproduction and Fertility 23:393–409. LACHER, T. E., JR. 1981. The comparative social behavior of Kerodon ROWE, D. L., AND R. L. HONEYCUTT. 2002. Phylogenetic relationships, rupestris and Galea spixii and the evolution of behavior in the ecological correlates, and molecular evolution within the Cavioi- Caviidae. Bulletin of Carnegie Museum of Natural History 17:1–71. dea (Mammalia, Rodentia). Molecular Biology and Evolution LACHER, T. E., JR. 1982. Behavioral research in South America. Pp. 19:263–277.

209–230 in Mammalian biology in South America (M. A. Mares SACHSER, N. 1986. Different forms of social organization at high and Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 and H. H. Genoways, eds.). Special Publication Series 6, low population densities in guinea pigs. Behaviour 97:253–272. Pymatuning Laboratory of Ecology, University of Pittsburgh. SACHSER, N., C. KU¨ NZL, AND S. KAISER. 2004. The welfare of LAVALLE´ E, D. 1990. La domestication animale en Ame´rique du Sud— laboratory guinea pigs. Pp. 181–209 in The welfare of laboratory le point des connaissances. Bulletin de l’Institut Franc¸ais d’E´ tudes animals (E. Kaliste, ed.). Kluwer Academic Publishers, Dordrecht, Andines 19:25–44. The Netherlands. LORD, R. D. 2009. Capybaras: a natural history of the world’s largest SACHSER, N., E. SCHWARZ-WEIG,A.KEIL, AND J. T. EPPLEN. 1999. rodent. Johns Hopkins University Press, Baltimore, Maryland. Behavioural strategies, testis size, and reproductive success in two LU¨ TTMANN, K. 2006. The behavioural ecology of the southern desert caviomorph rodents with different mating systems. Behaviour cavy—the female perspective. M.S. thesis, University of Mu¨nster, 136:1203–1217. Mu¨nster, Germany. SALVADOR, C. H., AND F. A. S. FERNANDEZ. 2008a. Population MACDONALD, D. W., E. A. HERRERA,A.B.TABER, AND J. R. MOREIRA. dynamics and conservation status of the insular cavy Cavia 2007. Social organization and resource use in capybaras and maras. intermedia (Rodentia: Caviidae). Journal of Mammalogy 89:721– Pp. 393–402 in Rodent societies: an ecological and evolutionary 729. perspective (J. O. Wolff and P. W. Sherman, eds.). University of SALVADOR, C. H., AND F. A. S. FERNANDEZ. 2008b. Reproduction and Chicago Press, Chicago, Illinois. growth of a rare, island-endemic cavy (Cavia intermedia) from MARES, M. A., AND R. A. OJEDA. 1982. Patterns of diversity and southern Brazil. Journal of Mammalogy 89:909–915. adaptation in South American hystricognath rodents. Pp. 393–432 SANDWEISS, D. H., AND E. S. WING. 1997. Ritual rodents: the guinea in Mammalian biology in South America (M. A. Mares and H. H. pigs of Chincha, Peru. Journal of Field Archaeology 24:47–58. Genoways, eds.). Special Publication Series 6, Pymatuning SCHWARZ-WEIG, E., AND N. SACHSER. 1996. Social behaviour, mating Laboratory of Ecology, University of Pittsburgh. system and testes size in cuis (Galea musteloides). Zeitschrift fu¨r MARES, M. A., R. A. OJEDA, AND M. P. KOSCO. 1981. Observations on Sa¨ugetierkunde 61:25–38. the distribution and ecology of the mammals of Salta Province, SOLMSDORFF, K., D. KOCK,C.HOHOFF, AND N. SACHSER. 2004. Argentina. Annals of Carnegie Museum 50:151–206. Comments on the genus Galea Meyen 1833 with description of MARQUET, P. A., L. C. CONTRERAS,S.SILVA,J.C.TORRES-MURA, AND Galea monasteriensis n. sp. from Bolivia (Mammalia, Rodentia, F. BOZINOVIC. 1993. Natural history of Microcavia niata in the high Caviidae). Senckenbergiana Biologica 84:137–156. Andean zone of northern Chile. Journal of Mammalogy 74:136– SPOTORNO, A. E., G. MANRI´QUEZ,L.A.FERNA´ NDEZ,J.C.MARI´N,F. 140. GONZA´ LEZ, AND J. WHEELER. 2007. Domestication of guinea pigs MARTIN, J. K., K. A. HANDASYDE,A.C.TAYLOR, AND G. COULSON. from a southern Peru–northern Chile wild species and their middle 2007. Long-term pair-bonds without mating fidelity in a mammal. pre-Columbian mummies. Pp. 367–388 in The quintessential Behaviour 144:1419–1445. naturalist: honoring the life and legacy of Oliver P. Pearson MONGE, S., M. DACAR, AND V. G. ROIG. 1994. Comparacio´n de dietas (D. A. Kelt, E. P. Lessa, J. Salazar-Bravo, and J. L. Patton, eds.). de cuises en la reserva de la biosfera de N˜ acun˜a´n (Santa Rosa, University of California Publications in Zoology 134:1–981. Mendoza, Argentina). Vida Silvestre Neotropical 3:115–117. SPOTORNO, A. E., J. P. VALLADARES,J.C.MARI´N, AND H. ZEBALLOS. MUNSHI-SOUTH, J. 2007. Extra-pair paternity and the evolution of 2004. Molecular diversity among domestic guinea-pigs (Cavia testis size in a behaviorally monogamous tropical mammal, the porcellus) and their close phylogenetic relationship with the large treeshrew (Tupaia tana). Behavioral Ecology and Sociobi- Andean wild species Cavia tschudii. Revista Chilena de Historia ology 62:201–212. Natural 77:243–250. RAMM, S. A., G. A. PARKER, AND P. STOCKLEY. 2005. Sperm STAHNKE, A. 1987. Verhaltensunterschiede zwischen Wild- und competition and the evolution of male reproductive anatomy in Hausmeerschweinchen. Zeitschrift fu¨r Sa¨ugetierkunde 52:294– rodents. Proceedings of the Royal Society of London, B. Biological 307. Sciences 272:949–955. TABER, A. B., AND D. W. MACDONALD. 1992a. Spatial organization and RANFT, S. 2005. Behavioural ecology of the desert cavy—the male monogamy in the mara Dolichotis patagonum. Journal of Zoology perspective. M.S. thesis, University of Mu¨nster, Mu¨nster, Germany. (London) 227:417–438. REDFORD, K. H., AND J. F. EISENBERG. 1992. Mammals of the TABER, A. B., AND D. W. MACDONALD. 1992b. Communal breeding in Neotropics. Vol. 2. The Southern Cone: Chile, Argentina, the mara, Dolichotis patagonum. Journal of Zoology (London) Uruguay, Paraguay. University of Chicago Press, Chicago, Illinois. 227:439–452. ROOD, J. 1969. Observations on the ecology and behavior of TARABORELLI, P. 2008. Vigilance and foraging behaviour in a social Microcavia, Galea and Cavia. Acta Zoologica Lilloana 24:111– desert rodent, Microcavia australis (Rodentia, Caviidae). Ethology 114. Ecology and Evolution 20:245–256. February 2011 SPECIAL FEATURE—SOCIAL AND MATING SYSTEMS IN CAVIES 53

TARABORELLI, P. 2009. Is communal burrowing or burrow sharing a TRILLMICH, F., ET AL. 2004. Species-level differentiation of two cryptic benefit of group living in the lesser cavy Microcavia australis? species pairs of wild cavies, genera Cavia and Galea, with a Acta Theriologica 54:249–258. discussion of the relationship between social systems and TARABORELLI, P., AND P. MORENO. 2009. Comparing composition of phylogeny in the Caviinae. Canadian Journal of Zoology 82:516– social groups, mating system and social behaviour in two 524. populations of Microcavia australis. Mammalian Biology 74:15–24. WEIR, B. J. 1970. The management and breeding of some more TARABORELLI, P. A., P. MORENO,A.SRUR,A.J.SANDOBAL,M.G. hystricomorph rodents. Laboratory Animals 4:83–97. MARTI´NEZ, AND S. M. GIANNONI. 2008. Different antipredator WEIR, B. J. 1971. The evocation of oestrus in the cuis, Galea responses by Microcavia australis (Rodentia, Hystricognate, musteloides. Journal of Reproduction and Fertility 26:405– Caviidae) under predation risk. Behaviour 145:829–842. 408. TARABORELLI, P., P. SASSI, AND S. M. GIANNONI. 2007. Registro morfo- WEIR, B. J. 1973. The roˆle of the male in the evocation of oestrus in

ecolo´gico de Microcavia australis (Caviidae, Rodentia) en la puna the cuis, Galea musteloides (Rodentia: Hystricomorpha). Journal Downloaded from https://academic.oup.com/jmammal/article/92/1/39/944612 by guest on 27 September 2021 de la provincia de San Juan, Argentina. Mastozoologı´a Neotropical of Reproduction and Fertility, Supplement 19:421–432. 14:107–112. WEIR, B. J. 1974. Reproductive characteristics of hystricomorph TASSE, J. 1986. Maternal and paternal care in the rock cavy, Kerodon rodents. Symposia of the Zoological Society of London 34:265– rupestris, a South American hystricomorph rodent. Zoo Biology 301. 5:27–43. WOODS, C. A., AND C. W. KILPATRICK. 2005. Infraorder Hystricognathi TOGNELLI, M. F., C. M. CAMPOS, AND R. A. OJEDA. 2001. Microcavia Brandt, 1855. Pp. 1538–1600 in Mammal species of the world: a australis. Mammalian Species 648:1–4. taxonomic and geographic reference (D. E. Wilson and D. M. TOGNELLI, M. F., C. M. CAMPOS,R.A.OJEDA, AND V. G. ROIG. 1995. Is Reeder, eds.). 3rd ed. Johns Hopkins University Press, Baltimore, Microcavia australis (Rodentia: Caviidae) associated with a Maryland. particular plant structure in the Monte Desert of Argentina? XIMENEZ, A. 1980. Notas sobre el ge´nero Cavia Pallas con la Mammalia 59:327–333. descripcio´n de Cavia magna sp. n. (Mammalia—Caviidae). TOUMA, C., R. PALME, AND N. SACHSER. 2001. Different types of Revista Nordestina de Biologia 3, especial:145–179. oestrus cycle in two closely related South American rodents (Cavia aperea and Galea musteloides) with different social and mating systems. Reproduction 121:791–801. Special Feature Editor was Barbara H. Blake.