Female territoriality and the function of scent-marking in a monogamous antelope (Oreotragus oreotragus)

In monogamous species, females often choose between males according to the quality of the territories they defend, but the extent to which females themselves contribute to territory defence is frequently underestimated. Here we test for differences in male and female roles during paired scent-marking bouts, a key component of territorial defence, in a monogamous antelope. In two populations (Kenya, Zimbabwe) of klipspringer, Oreotragus oreotragus, both males and females usually scent-marked at the same site, but there were significant differences between sexes in terms of investment within bouts. Females initiated most bouts, thus dictating the marking strategy of the pair. Males initiated relatively few bouts, but deposited more scent marks per bout than females and were usually the last to scent-mark before leaving the site; they marked on the same branches as the female and thus overmarked her scent. Both sexes deposited more marks during paired than solo visits. Immediately preceding and following scent-marking bouts, males approached females and females left males more often than expected. Female scent-marking rates were higher when they were receptive than at other times, and this increase was matched by elevated marking rates of males. Females may increase marking rates when they are receptive in order to test the quality of their mate or to incite male competition. However, these ideas are unlikely to explain female scent-marking behaviour outside the mating season, which appears to be related primarily to territorial defence. We suggest that these differences in investment in scent-marking bouts are consistent with predictions that females may be autonomously territorial and that overmarking of female scent by males is a form of mate-guarding. Received: 17 November 1999 / Received in revised form: 24 February 2000 / Accepted: 13 March 2000     

Scent-marking behavior in wild groups of common marmosets (Callithrix jacchus)

Scent-marking in mammals has been frequently related to within-group social and reproductive dominance and to defense of territory and resources. We studied the scent-marking behavior of five wild groups of common marmosets, Callithrix jacchus, during 5 months of the fruiting season in northeastern Brazil. Circumgenital marking was the most common type of marking. Marks were distributed throughout the home range and were deposited mainly during travel and intergroup encounters. Although marks were commonly deposited at gum trees, there was no evidence that the animals used scent marks to label fruiting trees or sleeping sites. Contrary to expectations, reproductively dominant females did not mark more than reproductively subordinate females. Moreover, during intergroup encounters, reproductively subordinate females displayed higher frequencies of scent-marking than the reproductively dominant females of their group. Our results suggest that scent-marking is not strictly tied to reproductive dominance or territorial (or resource) defense in common marmosets. Because marks provide information about individual identity and reproductive condition, scent marks could serve different functions when used by different individuals. The high frequency of marking by reproductively subordinate females during intergroup encounters suggests that scent-marking might be used to signal to individuals of neighboring groups. Our data highlight the importance of social and ecological variables in scent-marking behavior. Received: 26 October 1998 / Received in revised form: 20 May 1999 / Accepted: 30 May 1999     

Sex differences in olfactory communication in a primate, the moustached tamarin, Saguinus mystax (Callitrichinae)

This study examines the hypothesis that sexual selection has shaped patterns of olfactory communication in wild moustached tamarins, Saguinus mystax. Do sex differences exist in frequencies and in the intensity of scent marking, in the use of different scent-marking types, and in behavioural responses to scent marks? Scent marking (anogenital, suprapubic, sternal) and behavioural responses (sniffing and overmarking) were recorded in four groups (ten adult and subadult males, seven adult and subadult females in all groups combined) in north-eastern Peru. Frequencies and intensity of scent marking were significantly higher in female tamarins. Males and females did not differ in the use of anogenital marking, but suprapubic marking was employed significantly more often by females. Only 10% of scent marks were monitored by another group member, and only 5% were overmarked by another group member. Most sniffing of scent marks was done by males, and males sniffed at marks produced by females significantly more often than at marks produced by males. Both sexes overmarked scent marks with similar frequency, but females overmarked scent marks produced by males significantly more often than those produced by females. An increase in frequencies of scent marking was observed in two females of one group after the death of the reproducing female, but frequencies of scent marking remained the same in the males of this group. The female-biased rates of scent marking are consistent with predictions made by sexual selection theory for species with substantial male care for offspring and strong reproductive competition between females. However, a decisive test of the proposed role of sexual selection will only be possible with more field data on patterns of olfactory communication in other callitrichine species.     

The association of female kin in the arctic ground squirrel Spermophilus parryii

Summary The association of kin in arctic ground squirrels (Spermophilus parryii) was studied near Haines Junction, Yukon Territory, during the summers of 1977, 1978, and 1979. Males dispersed in this population, thus only females were likely to live near relatives.Close female kin (sisters, mothers/daughters) had greater overlap of home ranges and interacted more amicably and less agonistically than did less closely related females. Closely related females clumped their young at emergence, whereas more distantly related females did not; there was little indication of clumping of pre-emerged young. The overlap of home ranges of distant relatives (known genetic relatives that had not associated in a natal burrow) was intermediate to that of close relatives and non-relatives. The types of interactions between distant relatives were more similar to those between non-relatives than between close relatives.I conclude that female arctic ground squirrels exhibit nepotism. Females may benefit from associations with relatives by sharing watching for predators once juveniles become conspicuous. Male arctic ground squirrels commit infanticide and several females may be more effective at protecting their young from infanticidal males than females living alone. I suggest that clumping of young by close relatives may provide a mechanism allowing distantly related females to identify each other.Address for offprint requests     

Vigilance in wild Thomas's langurs (Presbytis thomasi ): the importance of infanticide risk

This study examines vigilance as a behavioural indicator of the importance of infanticide risk by comparing the infanticide avoidance hypothesis with the predation avoidance and mate defence hypotheses for wild Thomas's langurs (Presbytis thomasi) in Sumatra. We found that all individuals were more vigilant in situations of high predation risk, i.e. lower in the trees and in the absence of neighbours. Females were also more vigilant on the periphery of the group. However, there were variations in vigilance levels that could not be accounted for by the predation avoidance hypothesis. Males without infants showed higher levels of vigilance in areas of home range overlap than in non-overlap areas during the early phase of their tenure, strongly suggesting mate defence. In these areas of home range overlap where Thomas's langur groups can interact, males may attack females and infants, and so the infanticide risk for males and females with infants is likely to be high in these areas. Only females with infants, but not males with infants or females without infants, showed higher vigilance levels in overlap areas than in non-overlap areas; in addition, in overlap areas, females with an infant were more vigilant than females without an infant, while this was not the case in non-overlap areas. Both females and males with infants were more vigilant high in the trees than at medium heights in overlap areas but not elsewhere. These findings can only be explained by the infanticide avoidance hypothesis. In contrast to predator attacks, infanticidal male attacks come from high in the canopy, and only occur in overlap areas. There was a significant sex difference in vigilance, but males were only more vigilant than females without an infant, and not more vigilant than females with an infant. We conclude that vigilance varied mainly in relation to the risk of predation and infanticide. Mate competition only played a role for males during the early phase of their tenure. Predation risk seems to offer the best explanation for vigilance for all individuals in the absence of infants. Both predation risk and infanticide risk played a role for females and males with infants. Received: 4 April 1998 / Accepted after revision: 6 September 1998     

Competitor assessment by scent matching: an experimental test

Summary If males assess potential opponents by comparing their odour with that of scent marks in the vicinity (the so called scent matching hypothesis) they should be more reluctant to fight when these odours are the same. Under these circumstances the potential opponent is thus identified as a resource holder (a male monopolising a territory or group of females) that would escalate encounters to defend its resources. We tested this prediction by comparing the fighting behaviour of male house mice, Mus domesticus, when on a scent-marked substrate that matched the odour of an opponent with their behaviour on a substrate that did not match. As predicted, the delay before the first fight was longer and the rate of subsequent fighting lower when the scents matched. This result is consistent with the interpretation that resource holders scent mark to provide opponents with a means of competitor assessment and that they thus reduce the costs of resource defence. Offprint requests to: L.M. Gosling     

Sex differences in the ontogeny of social behavior in pikas: possible relationships to dispersal and territoriality

Summary A laboratory study on the ontogeny of social behavior in pikas (Ochotona princeps), an alpine lagomorph, was conducted to determine the role of early relationships between adult females and young and among siblings in the development of territorial and dispersal behaviors. Sex differences during development were examined because field studies have reported greater dispersal distances in young females than young males. At birth, females were significantly heavier than males. There were no sex differences in nursing frequency until after the 2nd week of age, when males initiated more nursing attempts than females. By the end of the weaning period (weeks 5 and 6), adult females became non-interactive with young, but aggression of young toward littermates and the mother increased until the eighth week. At this time, young males outweighed their sibling females. Young were dominant over their mothers by the age of 5 weeks, and young males were dominant over their sibling females.Sex differences were observed in aggression, scent-marking, exploratory activity, and submissive vocalizations, with higher rates in young males, except for submissive vocalizations, which were higher in females (Table 2). Vocalizations and scent-marking behavior increased over time, and were positively correlated with interaction rates.These data support the hypothesis that female young disperse farther than male young largely as the result of unsuccessful competition with male siblings for available territories close to the birthplance. A dispersal strategy for pkkas is proposed.     

The functional significance of infanticide in a population of California ground squirrels (Spermophilus beecheyi)

Naturally-occurring infanticide was observed in a population of California ground squirrels (Spermophilus beecheyi). In four seasons, 40 infanticides were observed. All victims were post-emergent pups. Of 37 killings in which the killer was sexed 36 were by females. All infanticidal females were mothers at the time they killed, but in no case was a mother seen to kill or harm her own young. The victim was cannibalized in 22 cases and taken immediately into the killer’s burrow in 16 others. In no case did killers gain access to the victimized mother’s burrow or territory and female pups were not killed preferentially over males. In light of evolutionary explanations, infanticide in this population may best fit the resource exploitation hypothesis, in which killers commit infanticide to gain a nutritional benefit. Resource competition is a possible auxiliary explanation, since any time a female kills unrelated young she is eliminating possible competitors to her own offspring. This behavior could confer a fitness advantage on killers or it could be an adaptively neutral, alternative feeding strategy. More data are necessary to distinguish between these hypotheses. Received: 26 January 1995/Accepted after revision: 9 September 1995     

Sex allocation and paternity in a cooperatively breeding passerine: evidence for the male attractiveness hypothesis?

Sex allocation theory predicts that female birds with high-quality mates will benefit from producing more sons, since sons will inherit their father’s superior traits and enjoy a great reproductive success, whereas females with low-quality mates will benefit from producing more daughters, since the variance in reproductive success among daughters is typically lower. The male attractiveness hypothesis may apply to extra-pair paternity (EPP) because socially monogamous females routinely mate with higher quality males outside the pair bond. We test these predictions using the Tibetan ground tit (Pseudopodoces humilis), a sexually monomorphic, socially monogamous, facultatively cooperative breeder. There was greater variation in actual reproductive success among males than females due to EPP. An excess of sons was detected for bi-parental (i.e., non-cooperative) broods wherein EPP was mainly sired by bi-parental males. The pattern was attributed to male-biased sex ratios produced for both EPP and within-pair offspring within the same broods. The reason for the latter case might be a random allocation of more offspring to sons by the potentially EPP-exposed females that have an inability to control fertilization by specific males. In cooperative broods where EPP mostly resulted from within-group helpers of presumed low-quality, as indicated by their failure in acquiring a social mate, there was a non-significant tendency for EPP offspring to be daughters and for within-pair offspring in the same broods to be unbiased. These results support the EPP-related male attractiveness hypothesis especially in terms of the overproduction of sons. Offspring produced through quasi-parasitism was unbiased towards either sex, suggesting a weak female choiceness with respect to the quality of host males.     

Why do female mice mate with multiple males?

Females often show multi-male mating (MMM), but the adaptive functions are unclear. We tested whether female house mice (Mus musculus musculus) show MMM when they can choose their mates without male coercion. We released 32 females into separate enclosures where they could choose to mate with two neighboring males that were restricted to their own territories. We also tested whether females increase MMM when the available males appeared unable to exclude intruders from their territories. To manipulate territorial intrusion, we introduced scent-marked tiles from the neighboring males into males' territories, or we rearranged tiles within males' own territories as a control. Each female was tested in treatment and control conditions and we conducted paternity analyses on the 57 litters produced. We found that 46 % of litters were multiply sired, indicating that multiple paternity is common when females can choose their mates. Intrusion did not increase multiple paternity, though multiple paternity was significantly greater in the first trial when the males were virgins compared to the second trial. Since virgin male mice are highly infanticidal, this finding is consistent with the infanticide avoidance hypothesis. We also found that multiple paternity was higher when competing males showed small differences in their amount of scent marking, suggesting that females reduce MMM when they can detect differences in males' quality. Finally, multiple paternity was associated with increased litter size but only in the intrusion treatment, which suggests that the effect of multiple paternity on offspring number is dependent on male–male interactions.     

Female sensory bias may allow honest chemical signaling by male Iberian rock lizards

Some mate choice theories propose that only male signals that are honest and condition-dependent can be stable, while another hypothesis states that males evolve signals that exploit the sensory system of females. However, sensory traps might evolve into honest signals if they are differentially costly for males. We tested whether a pre-existing sensory bias for food chemicals explained chemosensory preferences of female Iberian rock lizards for male scents. We manipulated hunger levels of females and found that food-deprived females had increased chemosensory responses to chemical stimuli from both invertebrate prey and femoral secretions of males, but not to control water. Further tests suggested that cholesta-5,7-dien-3-ol (provitamin D₃), a lipid found in both prey and males’ scent, may be one of the chemicals eliciting these responses. Moreover, hungry females spent more time on scent marks of males that had experimentally increased cholesta-5,7-dien-3-ol than on scent marks of males alone, whereas for control females this effect was not significant. We suggest that preexisting sensory bias for essential nutrients (i.e., provitamin D) may be the origin of similar female responses to male chemicals. However, previous studies have suggested that the allocation of these chemicals to ornaments is costly and only high quality males can afford it. Therefore, preexisting sensory bias for essential nutrients may further allow the evolution and maintenance of honest sexual displays.     

Levels of social behaviors and genetic structure in a population of round-tailed ground squirrels (Xerospermophilus tereticaudus)

Ground-dwelling sciurids exhibit a continuum of sociality and several models predict levels of sociality within this taxon. Models of ground squirrel sociality predict round-tailed ground squirrels (Xerospermophilus tereticaudus) to be solitary; however, previous behavioral studies suggest round-tailed ground squirrels have a matrilineal social structure. To resolve this discrepancy, we combined behavioral observations with genetic analyses of population structure. We assessed levels of agonistic and amicable behaviors combined with fine-scale population genetic structure of round-tailed ground squirrels in a multi-year study in AZ. Only 45 agonistic and 40 amicable interactions were observed between adults in over 137 h of observations. Overall rates of agonistic or amicable interactions between adults were low (≤0.69/h), with no relationship between relatedness of individuals and rates of either amicable or agonistic interactions. Interactions between juvenile littermates were predominantly amicable. Population substructure was not evident with Bayesian analyses, global or pairwise F _ST values; average relatedness among females was not different from males. However, in 2006, the year after a population reduction through targeted animal elimination, a population bottleneck was detected within at least five of seven loci. Contrary to previous behavioral studies, this population of round-tailed ground squirrels, although aggregated spatially, did not exhibit high levels of social behavior nor subpopulation genetic structure. Analyses of the genetic relationships and sociality along a continuum, particularly within aggregates of individuals, may lead to insights into the origin and maintenance of social behaviors by elucidating the mechanisms by which aggregates with intermediate social levels are formed and maintained.     

Possible causes and consequences of philopatry and breeding dispersal in red-backed shrikes <Emphasis Type="BoldItalic">Lanius collurio</Emphasis>

Studies of animal breeding dispersal have often focused on possible causes, whereas its adaptive significance has received less attention. Using an information-theoretic approach, we assessed predictions of four hypotheses relating to causes and consequences of breeding dispersal in a migratory passerine, the red-backed shrike Lanius collurio. As predicted by the reproductive performance hypothesis, probability of breeding dispersal in females (though not in males) decreased with increasing annual average number of fledglings produced in the past year, but there was no association with conspecific reproductive performance in either sex. The site choice hypothesis, stating that individuals disperse to improve breeding site quality, received support in males only, as dispersal probability was positively associated to a measure indicating low territory quality. The social constraints hypothesis, referring to dispersal in relation to intraspecific interactions, received little support in either sex. The predation risk hypothesis was hardly supported either. Consequences of dispersal were marginal in both sexes because neither fledgling production in females, nor territory quality in males improved after dispersal. In addition, males settled on territories closer to the forest edge than those occupied predispersal, which is opposite to the prediction of the predation risk hypothesis. We conclude that own reproductive success was the major factor determining dispersal behavior in females, whereas territory quality and possibly predation risk were most important in males. Overall, breeding dispersal appeared not to be adaptive in this dense population inhabiting an optimal habitat.     

Natal dispersal in Belding's ground squirrels (Spermophilus beldingi)

Summary Dispersal from the natal site was documented in two populations of Belding's ground squirrels (Spermophilus beldingi) living at different altitudes in the Sierra Nevada of North America. Distance dispersed and age at dispersal were monitored by a combination of observation, trapping, radio telemetry, and examination of road kills. Dispersal was sexually dimorphic in both populations (Tables 1 and 2). All surviving males emigrated before they were 55 weeks of age, with most dispersing midway through the juvenile summer (Fig. 1). By contrast, most females remained within the boundaries of their mothers' home range (Fig. 2 and 3). Those very few females that did emigrate moved distances from their natal burrows similar to those travelled by dispersing males (200–450 m; Table 2), but females tended to disperse at a slightly older age. Significant differences between the study populations were found in distances moved by juveniles of both sexes (Fig. 2). Body weights of juvenile male dispersers were significantly greater than were those of juvenile males of equivilent ages that had not yet dispersed (Fig. 4). The results were considered in light of Shields' (1982) discussion of dispersal and inbreeding. I concluded that if dispersal is related to reproductive success, then dispersal distances selected for use in tests of evolutionary hypotheses should be measured just prior to the subject animals' first reproduction. Finally, although not tested in the present study, the evolutionary hypothesis most consistent with my data suggests that dispersal in S. beldingi may function to minimize nuclear family incest.     

Tail loss reduces mating success in the Iberian rock-lizard,Lacerta monticola

Summary Many lizards autotomize their tails to escape when grasped by a predator. It is hypothesized that tail loss causes a reduction in social status, thereby potentially lowering their reproductive success. We experimentally induced tail loss in Lacerta monticola in a semi-natural enclosure, and show that tail loss reduced social status and mating access in males. Tailless males increased body mass more rapidly than tailed dominant males, probably due to lower aggression costs. Also, tailless females were courted less and copulated less than tailed females, supporting the hypothesis that tail loss decreases reproduction potential.Correspondence to: J. Martin     

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (<Emphasis Type="Italic">Urocitellus columbianus</Emphasis>)

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.     

Does reproductive state affect a lizard's behavior toward predator chemical cues?

We examined how reproductive state affected shifts in behavior of adult female Podarcis sicula toward chemical cues from a natural snake predator (Coronella austriaca). The oviparous P. sicula lizards do not experience a major physical burden during reproduction, but gravid females substantially increase duration of basking. Therefore, gravid lizards are likely to experience a greater risk of mortality because they are exposed to predators for longer periods. Both gravid and non-gravid females shifted patterns of locomotion when confronted with snake chemical cues, but the change was notably larger when females were non-gravid. When non-gravid, lizards responded to predator scent by increasing the number of stand-ups and starts, while such a response was not observed when females were gravid. By contrast, gravid lizards clearly reduced the time spent basking in the presence of predator scent, whereas no change in basking behavior was observed when females were non-gravid. Thus, females exhibit differential behavioral responses to predator scents that is dependent on reproductive state.     

Manipulation of Olfactory Signaling and Mate Choice for Conservation Breeding: a Case Study of Harvest Mice

Abstract:  Mate choice by females can introduce difficulties to captive breeding programs because there may be a conflict between the conservation manager's choice of mate (based on random allocation or maximizing heterogeneity) and the females' own preferences, often resulting in incompatibility and aggression. Similar effects are caused by inappropriate social contexts at the time of pairing. We manipulated the social experience of male and female harvest mice ( Micromys minutus ) to investigate whether we could enhance compatibility between randomly allocated mates by altering female preferences. In one experiment, we used a choice test to identify female preferences between two males and then varied the competitive context of unpreferred males by transferring competitor's scent marks into their cages. The manipulation caused them to increase their investment in a form of olfactory signaling (scent marking), which female rodents use as an indicator of male quality when choosing mates. The manipulation increased their attractiveness relative to the initially preferred male when the choice test was repeated. In a second experiment, we tested the effect of females' familiarity with the odor of males by transfer of male scent marks to female cages. Females preferred familiar males in choice tests and were less aggressive toward them when pairs were introduced than females paired with unfamiliar males. This kind of approach can influence mate choice, and transferring scent marks between cages or collections is an effective and practical behavioral means of improving success in conservation breeding programs.     

The scent of dominance: female field crickets use odour to predict the outcome of male competition

Pheromones may convey information about mate quality and social status. In the field cricket Gryllus integer, females mount the males for copulation, such that males cannot coerce females to mate. We examined whether virgin G. integer females preferred the scent of potentially dominant males to that of subordinate males. First, we collected pheromones by confining males on filter paper. Next, we offered filter paper from each of two size-matched males and control paper to females that had never been exposed to males, and measured the time spent by the female on each kind of paper. Finally, dominance status of the males in each size-matched pair was determined by pitting the two males against one another in agonistic contests. When offered filter paper from subsequently dominant versus subsequently subordinate males, females spent more time on the paper from the dominant male than the subordinate male, and much less time on control paper. Thus, pheromones may inform female G. integer about a male's potential to achieve dominant social status. Male pheromones were also associated with the female's tendency to mount a male. In contrast to cockroaches, where females prefer the scent of subordinate males (presumably to avoid risk of injury), female crickets prefer the scent of potentially dominant males and are more likely than males to wound their mating partners.     

Differential reproduction among female Richardson's ground squirrels and its relation to sex ratio

Summary The reproductive success of ten female Richardson's ground squirrels resident on a grassland pasture in southern Alberta in 1975 was determined by noting the number of their descendants present in 1976, 1977, and 1978.The two most successful females were the progenitors of 67% of the females resident in 1977 and of 57% of the females resident in 1978. None of the other eight females had descendants in the population in 1978. The two most successful females produced more daughters than did the other females and they did so, not by rearing larger litters, but by producing female-biased litters. The daughters of the two most successful females lived slightly longer than did the daughters of other females.Although the adult sex ratio was strongly female biased each breeding season, ranging between 0.26 and 0.42 males per female, typically all females became pregnant.Adult female offspring inherited their mother's home range and, if the mother or any female sibs were present, shared this area with them. Sons rarely remained resident in or near the natal area and adult males rarely remained resident in the same area for two consecutive years. Thus, post-weaning investments were greater in daughters than in sons.There were no conclusive correlations between sex ratio of litters and size of litters, age of the mother, previous reproductive success of the mother, population density, or the length of the overwinter period. More studies spanning several generations are required to elucidate the effects of the sex ratio of litters on the likelihood of an animal being represented by descendants in subsequent generations.