Genetic relatedness and space use in a behaviorally flexible species of marmot, the woodchuck (Marmota monax)

Solitary species show several patterns of space use and relatedness. Individuals may associate randomly or may live near female or male kin, often as a result of natal philopatry or dispersal patterns. Although usually described as solitary or asocial, woodchucks (Marmota monax) are behaviorally flexible marmots that exhibit greater sociality in some populations than others. I examined relationships between kinship, geographic distance, and home range overlap, as well as dispersal and philopatry, to determine the extent to which kin associated spatially. I used a combination of microsatellite DNA analysis, long-term behavioral observations, and radiotelemetry to test predictions that females, but not males, would associate with kin. Indeed, woodchucks lived closer and shared a greater proportion of their home range with more closely related animals. Overlap of females' and males' home ranges was positively correlated with kinship, and male–female dyads shared more area with closer kin. Most juveniles delayed dispersal beyond their first summer. Females often remained philopatric and settled near their natal range. Although males often dispersed as yearlings, some males also established territories within or immediately adjacent to their natal home ranges. A combination of factors can explain these spatial patterns, including high population density associated with the study site's location within a suburban environment, high dispersal costs, and abundant food. Thus, despite their asocial and solitary reputation, woodchucks displayed spatial patterns seen in other, more social species of ground-dwelling sciurids.     

Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling

Living with relatives can be beneficial to individuals via the evolution of kin-directed altruism, but this is tempered by the increased risk of inbreeding. Therefore, in social species, the ability to recognise relatives can be highly advantageous. This study focuses on kin discrimination in the Lake Eacham rainbowfish, Melanotaenia eachamensis, an endangered freshwater species from north-east Queensland, Australia. First, I examined kin recognition abilities when a combination of both chemical and visual recognition cues was available. When given a choice of shoaling with same-sex groups, females spent significantly longer with full-sibs rather than half-sibs, full-sibs rather than non-relatives and half-sibs rather than non-relatives. Males spent significantly longer shoaling with full-brothers versus half-brothers, but showed no other shoalmate preferences. Second, in the presence of only chemical cues, females did not discriminate among groups of different levels of relatedness, but males showed a non-significant tendency to associate with full-sibs rather than non-relatives. Male shoaling behaviour seemed to be more influenced by factors other than relatedness, e.g. intra-sexual competition. Finally, I found that the shoaling preferences of females changed when exposed to groups of males. Females preferred to associate with non-relatives rather than half-brothers and non-relatives rather than full-brothers. There was no significant difference in the time spent with half-brothers versus full-brothers. Taken together, my results suggest that females have very good kin recognition abilities. They prefer to shoal with female relatives but avoid male relatives, and so are able to balance the benefits of nepotism and the costs of incest. Received: 2 May 2000 / Revised: 26 July 2000 / Accepted: 30 July 2000     

Social organization of woodchucks (Marmota monax)

Summary The social organization of woodchucks (Marmota monax) in southeast Ohio was studied at two sites, at one for two 2 years (1979–1980) and the other for 3 years (1981–1983). Spatial organization was determined by trapping and radio tracking. The home ranges of adult females did not overlap in the early spring but during late spring and summer there was some overlap (<10%) as females expanded their home ranges. Adult females tended to occupy the same home range in consecutive years. Some adult males occupied well-defined home ranges that did not overlap the home ranges of other males but did overlap extensively the home range of one to three adult females. These males tended to occupy the same home range in consecutive years. Infants used the same home range of their dam until about 2–3 months of age when most males and females apparently dispersed. About 35% of the juvenile females did not disperse until their second spring, just before their mother's new litter first emerged from their burrow. The average social group consisted of an adult male with two female kin groups comprising an adult female, an offspring (usually female) of the previous year, and the young of the year. Interactions within the kin group and with the adult male were relatively frequent and generally amicable. Interactions between kin groups both within and between different social groups were relatively rare and agonistic. The social organization of woodchucks in Ohio differs from that described in previous studies of woodchucks elsewhere and from that predicted by current models proposed by others on the evolution of social organization of marmots.     

Alarm calling behavior of the thirteen-lined ground squirrel,Spermophilus tridecemlineatus

Summary Alarm calling in a population of thirteenlined ground squirrels, Spermophilus tridecemlineatus, was studied over a three-year period. Data on ground squirrel reactions to human and canine approaches and to the approach or presence of avian predators were used to quantify alarm calling behavior.The results support the hypothesis that alarm calling in this species functions to warn genetic relatives. Human and canine approach-elicited calls were most frequently given by mothers and their recently emerged young; adult males and nonparous females rarely called. The onset of maternal calling coincided with the aboveground appearance of a mother's own litter, and both juvenile and maternal calling were terminated at approximately three weeks post-emergence. Alarm calls were rarely emitted during encounters with avian predators.Alarm calling behavior in S. tridecemlineatus thus appeared to be dependent upon the presence of newly emerged juvenile relatives. To investigate whether the population structure of S. tridecemlineatus was perhaps incompatible with the evolution of alarm calling directed toward adult relatives, the distance between the home ranges of adult relatives and the distance over which the alarm vocalization is audible to ground squirrels were measured. The results revealed that females were likely to have adult relatives relatives residing within audible range of the call.     

Kin-related spatial structure in brown bears Ursus arctos

Kin-related social structure may influence reproductive success and survival and, hence, the dynamics of populations. It has been documented in many gregarious animal populations, but few solitary species. Using molecular methods and field data we tested: (1) whether kin-related spatial structure exists in the brown bear (Ursus arctos), which is a solitary carnivore, (2) whether home ranges of adult female kin overlap more than those of nonkin, and (3) whether multigenerational matrilinear assemblages, i.e., aggregated related females, are formed. Pairwise genetic relatedness between adult (5 years and older) female dyads declined significantly with geographic distance, whereas this was not the case for male–male dyads or opposite sex dyads. The amount of overlap of multiannual home ranges was positively associated with relatedness among adult females. This structure within matrilines is probably due to kin recognition. Plotting of multiannual home-range centers of adult females revealed formation of two types of matrilines, matrilinear assemblages exclusively using an area and dispersed matrilines spread over larger geographic areas. The variation in matrilinear structure might be due to differences in competitive abilities among females and habitat limitations. The influence of kin-related spatial structure on inclusive fitness needs to be clarified in solitary mammals.     

Temporal overlap of female kin in Columbian ground squirrels (Spermophilus columbianus)

Summary Columbian ground squirrels (Spermophilus columbianus) were live-trapped from 5 to 7 years at three sites in southwestern Alberta, Canada. The two most common adult matrilineal relatives for 2-year-old females were the mother and a 1 year older non-littermate sister. Co-occurrence of female kin depended firstly on size and sexual composition of litters and secondly on age-specific survival and recruitment rates. Adult matrilineal kin frequently coexisted among breeding females of this species, leading us to predict a social system strorgly influenced by nepotism. However, the life history traits of S. columbianus suggest an adult female kin cluster unlike that found for other species of Spermophilus in which littermate sisters are common. If availability of adult female kin influences kin-differential behaviour, then female S. columbianus should favour mothers, daughters and non-ittermate sisters.     

Interspecific competition between native Eurasian red squirrels and alien grey squirrels: does resource partitioning occur?

In heterogeneous environments, differential niche selection by two competing species will result in niche partitioning so that individuals of each species can maximise their fitness under different sets of environmental variables. Thus, niche partitioning is considered essential to allow co-existence of ecologically related species. To assess whether niche partitioning was occurring between native red squirrels and alien grey squirrels living together in a 13-ha high-quality mixed deciduous woodland in north Italy, we investigated temporal and spatial patterns in their activity and foraging behaviour between 1996 and 1998. We used live trapping and radio-tracking to study numbers, distribution and behaviour of squirrels. Daily and seasonal temporal activity patterns, and activity on the ground and in the trees, were similar in the two species. However, grey squirrels were more tree specialists and had a narrower tree-species niche width than red squirrels, in particular making greater use of oak. Other studies of red and grey squirrels in allopatry show that the two species differ in the extent they utilise oak. Overall, tree-species niche overlap was about 70%. Grey squirrels had larger home ranges than red squirrels. Home ranges and core areas of both species were larger in males than females. Also, intraspecific home range and core-area overlap patterns were similar to those found in allopatric populations of these species. Overall, there was no evidence that the use of space of one species was affected by the other. Our results show that there was no niche partitioning of activity or foraging behaviour in time or space during the study. This suggests that, at moderate grey-squirrel densities, red squirrels are unable to avoid competition with grey squirrels, and that competition for food and/or space will occur when these resources become limiting.     

Inheritance of nest sites in female Columbian ground squirrels

Summary Home ranges, areas of intensive use, and locations of nest sites were determined for female Columbian ground squirrels and their daughters over seven years from a low-density population in southwestern Alberta. Adult females usually retained similar home ranges from year to year. However, they moved their nest sites more often than expected in years when a yearling daughter was present. Core areas and centres of activity also changed when the nest site was moved. Most daughters settled on their natal areas. The relinquishing of nest sites by females to their daughters is seen as a form of parental investment.     

Simultaneous GPS tracking reveals male associations in a solitary carnivore

In hypercarnivorous species, females have large spatial requirements to meet their nutritional needs, and food competition among females is intense. As a result, females are typically solitary and territorial, and solitary males compete for access to dispersed females. Yet, largely anecdotal reports indicate that facultative male sociality may be more common in solitary carnivores than previously thought. We studied spatial interactions among fossas (Cryptoprocta ferox), Madagascar's largest carnivore, using simultaneous GPS tracking of 13 adult individuals to determine patterns of sex-specific spatial distribution and sociality. Male home ranges were larger than those of females, male home ranges overlapped more with those of other males than those of females with other females. Whereas some males were solitary, a subset of adult males was found to have very high home range overlap, high rates of co-location within <50 m, low minimum inter-individual distances, and significantly positive “dynamic interaction”. These associated dyads sometimes, but not always, were close relatives. The fact that solitary and associated males coexist in this population raises interesting questions concerning constraints and flexibility of social tolerance. This study yielded preliminary indications that female distribution appears to be primarily structured by resource competition, whereas male sociality seems to depend on demographic chance events, yet unknown proximate determinants of social tolerance, and it is associated with somatic and reproductive advantages. Male associations among carnivores are therefore more widespread and appear to be based on a wider range of factors than previously thought.     

Communal nesting in an ‘asocial’ mammal: social thermoregulation among spatially dispersed kin

Communal nesting can help defray the high cost of endothermic heat production in cold environments, but such social behavior is generally thought to be incompatible with the persistent defense of exclusive territories in typically ‘asocial’ animals. We examined the propensity for communal nesting in female red squirrels (Tamiasciurus hudsonicus), which maintain individual year-round territories, through intensive monitoring of litters over 22 years and by radio-tracking females during 3 years in late winter/early spring. Communal nesting was exceptionally rare during lactation: of 1,381 litters tracked to emergence, we observed a single instance in which two closely related (r?=?0.5) females pooled their litters into a single nest. In contrast, nest sharing between 2–3 females was relatively common in the late winter/early spring, prior to mating; at least 12 of 63 females (19 %) engaged in communal nesting during a year of systematic tracking of radio-collared females from late February to April. Communal nesting occurred more frequently when temperatures were colder, suggesting that such aggregations might function to reduce thermoregulatory costs. These social associations were typically, though not exclusively, between closely related individuals (r?≥?0.25 for seven of eight cases; mother–daughter dyads: four of eight), suggesting this cooperative behavior might evolve through kin selection and/or may reflect extended parental care. Our results demonstrate that female red squirrels engage in communal nesting, typically with closely related kin, despite a dispersed population structure that stems from the persistent defense of individual territories.     

Determinants of male spacing behavior in microtines: an experimental manipulation of female spatial distribution and density

Theory on microtine mating systems predicts that male spacing behavior will be related to female spatial and temporal distribution. However, data from a natural population of field voles, Microtus agrestis, indicated a potential influence of female density on the spacing behavior of males. Therefore, I experimentally investigated the relative importance of female density and female spatial distribution for the spacing behavior of males in M. agrestis. Males were radio-tracked in enclosed natural habitats in which females at different densities were placed in two different spatial arrangements: clumped versus even distribution. Female density was the main factor determining male spacing behavior. At the high female density males had smaller home ranges and moved shorter distances between radio-tracking recordings. Also, home ranges were more exclusive at high female density. However, since there was a significant positive correlation between home range size and range overlap, range exclusiveness seemed to be influenced by female density indirectly through the effect of range size. Female spatial distribution, on the other hand, had no influence on male home range exclusiveness.     

Pregnancy failure and suppression by female-female interaction in enclosed populations of the red-backed vole,Clethrionomys rufocanus bedfordiae

Summary Experimental populations of the redbacked vole,Clethrionomys rufocanus bedfordiae (Thomas), were introduced into field enclosures and then subsequently checked for home range overlap and reproductive condition. The times to parturition of females that did not have exclusive home ranges were significantly delayed compared with those of females whose ranges did not overlap (Table 4). The delays in parturition were not significantly related to the age of the females or to the number and ages of males that overlapped with a female. Copulatory plugs observed in the females that did not have exclusive ranges indicated that they often failed to become pregnant, regardless of having copulated. After the acquisition of exclusive ranges, these same females came into estrus and became pregnant (Figs. 2, 3).     

Snake-directed mobbing by the Formosan squirrel Callosciurus erythraeus thaiwanensis

Summary The Formosan squirrel Callosciurus erythraeus thaiwanensis was often observed mobbing the snake Elaphe climacophora. A total of 36 natural and 21 experimentally induced mobbings were observed and analyzed. The number of attending squirrels per mobbing event varied from one to seven, and 84% of observed mobbings were performed by more than one individual. The duration of a mobbing bout increased directly with the number of assembled mobbers. In 68% of cases, one adult female was one of the mobbers; there was never more than one female per mob. The number of assembled males per mob varied from 0 to 5; 40% of the mobbings involved two or more males. This difference is correlated to a difference in spacing patterns of both sexes; female home ranges were distributed exclusively, whereas male home ranges overlapped each other. Females mated with multiple males whose home ranges overlapped theirs. Female's reproductive status (conception, lactation, and weaning) affected their intensity of response to the playback of mobbing calls, females in pup-rearing period being the most sensitive. One function of the mobbing appears to be defense of the young against snake predation. Females mobbed more intensively and longer than males. Males that had resided at the study site for at least 1 year tended to mob more frequently than intruders.     

Discrimination between related and unrelated individuals in the Australian lizard Egernia striolata

We examined evidence for kin-related signal discrimination in the Australian scincid lizard Egernia striolata, using 41 juvenile lizards from 14 litters from a population in the Mount Lofty Ranges, South Australia. We characterised each juvenile at four polymorphic microsatellite DNA loci, determined genetic relatedness among pairs of juveniles, and assigned for each litter one other litter that was genetically closest and one other litter that was genetically most distant. Lizards responded significantly more strongly, with tongue flicks and time in contact, to skin secretion stimuli from more distant than genetically close, unfamiliar conspecific juveniles. When presented with an intruder, juvenile lizards basked for shorter periods when the intruder was more distantly related, and aggressive lizards directed more aggressive acts towards more distantly related than closely related conspecific intruders. We deduce from these results that there is kin recognition in juvenile E. striolata, and that they are able to discriminate related from unrelated individuals among unfamiliar conspecifics.     

Vocal alliances in Chacma baboons (<Emphasis Type="Italic">Papio hamadryas ursinus</Emphasis>)

Theory predicts that females in species with matrilineal dominance hierarchies should use nepotistic support systems to maintain their family’s rank. Female Old World monkeys, however, form alliances against other females at surprisingly low rates. Nonetheless, in many species, females utter threat vocalizations when observing others’ disputes, suggesting that these vocalizations may function as ‘vocal alliances’. We describe a playback experiment testing the efficacy of vocal alliances in free-ranging female baboons. Subjects were played the same female’s threat-grunts under three separate conditions: after being threatened by the signaller’s close relative to mimic kin support, after being threatened by a female maternally unrelated to the signaller to mimic non-kin support, and after a friendly interaction with the signaller’s close relative as a control. Subjects responded more strongly to the playback and avoided the signaller and her matrilineal relatives for a longer period of time in kin support trials than in either non-kin support or no aggression trials. In contrast, there was no difference in subjects’ behaviour between non-kin support and no aggression trials. These results corroborate observational data showing that vocal support occurs at a higher rate than physical support in female baboons, and that kin are more likely to provide vocal support than non-kin. We conclude that vocal support plays a similar role as physical support in the alliances of female baboons.     

Dynamics of space use and male vigour amongst wood mice,Apodemus sylvaticus,in the cereal ecosystem

The spatial organisation of male and female wood mice,Apodemus sylvaticus, was investigated in a large-scale radio-tracking study on arable farmland near Oxford, United Kingdom, during the breeding season. Both sexes had significantly larger home ranges in the breeding season than at other times, and the breeding season home ranges of male (X = 1.44 ha) were significantly larger than those of females (X = 0.49 ha). Home range overlap was significantly greater between males, and between males and females, than it was between females. Overlap between males tended to be greatest in heavily utilised areas. Except during sexual consortship, there was minimal evidence of dynamic interaction among individuals. Home range sizes of breeding males varied widely, as did their body weights. There was no relationship between male body weight and home range size or any other movement parameter. However, males with the largest home ranges had the highest scores on all other movement parameters, indicating that they expended more energy in movement. These more vigorous males had access to the home ranges of more females than did males with small home ranges.     

Kin associations and direct vs indirect fitness benefits in colonial cooperatively breeding sociable weavers Philetairus socius

Indirect fitness benefits are believed to be an important force behind the evolution of cooperative breeding. However, helpers may associate with their relatives as a result of delayed dispersal, hence, kin associations might be a consequence of demographic viscosity rather than active choice. In addition, recent studies showed that helpers may have access to reproduction therefore direct benefits might also play an important role. Here, we investigate the possible roles of direct genetic benefits and kin associations on helping behavior in the sociable weaver Philetairus socius, a colonial and cooperatively breeding passerine. We used a microsatellite-based genotyping method to describe the genetic structure within nests and colonies. Within a colony, we found considerable genetic structure between males but not females. Sociable weaver colonies have several nests that are simultaneously active, giving individuals a choice of associating with a range of first-order kin to unrelated individuals. Helpers were significantly more related to the young in the helped nests than in other nests of the colony, suggesting an active choice for associating with kin. The helpers were generally offspring or first-order relatives of one (50%) or both (43%) breeders, although more infrequently, seemingly unrelated individuals also helped (7%). We found no supporting evidence of extrapair parentage and hence no direct genetic gains from helping in our population. This strong reproductive skew is contrary to theoretical models predicting conflicts over reproduction in stepfamilies. We discuss whether female decisions and/or other direct benefits of remaining in kin associations or helping might explain the high skew observed.     

Sociogenetic structure in a free-living nocturnal primate population: sex-specific differences in the grey mouse lemur (Microcebus murinus)

The grey mouse lemur (Microcebus murinus) has a dispersed social structure, within which female sleeping associations are common. These sleeping associations have been hypothesised to confer anti-predatory and thermoregulatory benefits, especially when rearing offspring. The genetic composition of these associations was determined using microsatellite markers to test predictions derived from kin selection theory. 161 (99 males, 62 females) individual M. murinus belonging to a free-living population in Ampijoroa, north-western Madagascar, were genotyped and observed over a total of 13 months distributed over the dry seasons of 3 successive years (1995-1997). Kin selection theory predicts that these female associations should consist of closely related members, and that female philopatry and male natal dispersal should characterise the dispersal pattern within this species. These predictions were confirmed by the data. Five out of six female sleeping groups consisted of one or more closely related dyads. Females that slept alone did not have close female kin in the vicinity or within the population at all. Closely related female dyads lived in significantly closer proximity than closely related male dyads and closely related male-female dyads showed intermediate proximity. In combination with the result that females possessed significantly more relatives within the population than males, these findings support the behavioural hypotheses of female philopatry and male natal dispersal. Matrilinear grouping patterns and sex-biased dispersal are therefore genetically established in a dispersed primate social organisation for the first time. The results further indicate that several generations of mouse lemurs live together within a given area, implying both an effective mechanism of kin recognition to avoid father-daughter incest and the potential for social learning to ensure individual recognition.     

Spatial organization and mating system of Microtus townsendii

Summary Space use by individual Townsend's voles, Microtus townsendii, was investigated in spring and summer by means of radiotelemetry and intensive live trapping in undisturbed grasslands near Vancouver, British Columbia. Home ranges of males were larger than those of females; females had significantly larger ranges in spring than in summer. Most males and females maintained territories free of individuals of the same sex in spring. Male-female pairs had their exclusive territories closely overlapping each other. The 1:1 operational sex ratio and the spatial association of pairs of males and females suggest that the voles were monogamous in the spring of 1988 and that 50% of the males were monogamous in the spring of 1989. In summer, there was more intrasexual overlap between home ranges of males and females and female ranges were considerably smaller than those of males. Females were more philopatric than males and females thought to be members of the same family group lived adjacent to each other or had overlapping home ranges. Males overlapped with more than one female in summer, but most females still overlapped with only one male, which suggests that the mating system is polygynous in summer. Thirty-five percent of the philopatric females became pregnant for the first time when the male spatially associated with their mother in the spring was still alive and thus could potentially have mated with their fathers. Male and female territoriality in spring is the proximate mechanism for the limitation of breeding density by spacing behaviour.[/p] Offprint requests to: C.J. Krebs     

The reproductive consequences of male cooperation in the red howler monkey: paternity exclusion in multi-male and single-male troops using genetic markers

Summary Variance in male reproductive success in single and multi-male red howler (Alouatta seniculus) troops was examined through paternity exclusion using genetic markers. Coalitions of relatives were compared to coalitions of non-relatives with regard to duration, stability, and number of offspring expected for each participant based on paternity exclusion results. No evidence of paternity by males living outside of the troop was found. In multi-male troops, only the dominant male was found to father offspring conceived during his tenure. This was the only male observed to mount females. In both troops examined genetically wherein a status change had occurred, paternity changed with status. Coalitions of relatives and potential relatives lasted significantly longer than coalitions of non-relatives, and experienced fewer status changes between males. A direct advantage of forming a coalition for both dominant and subordinate red howler males resulted from the superior competitive ability of coalitions over single males in establishing and maintaining tenure in the limited number of female troops in the population. Although the mating success of a subordinate male in a coalition appears to be extremely low, his chances of achieving membership in a bisexual troop as a single male may be even lower. Since the majority of troops in the population during any given year were multi-male or age-graded male (85%–96%), the number of troops that a single male would be able to invade unaided was very small. A subordinate male may be able to assume dominance, particularly if he is a subadult. In coalitions in which males are related, the subordinate male will further benefit from inclusive fitness. A dominant male that forms a coalition with a relative can expect to have longer reproductive tenure than in a troop with a non-relative, thereby producing more offspring and directly enhancing his fitness. Anecdotal evidence suggests that males choose relatives over non-relatives as coalition partners when possible.