Scent communication by female Columbian ground squirrels, Urocitellus columbianus

Scent-marking is a frequent behaviour of highly social ground squirrels and might play an important role in their social dynamics. Female Columbian ground squirrels exhibit considerable scent-marking during the reproductive period. We examined how gestating and lactating females responded to jugal gland scent-marks of same-sexed and opposite-sexed conspecifics with attention to genetic relatedness and the geographical location of the territory of individuals. We tested the dear-enemy, threat-level and kin-discrimination hypotheses to explain patterns of scent-marking. Females sniffed the scent of non-neighbouring males significantly longer than other types of scent categories and tended to over mark the scent of females more than the scent of males. Furthermore, females sniffed significantly longer at scents during gestation than during lactation. We concluded that scent-marking mainly functioned in the defence of female territories and for protection of pups against infanticidal females (threat-level hypothesis). Our results were also in accordance with the kin-discrimination hypothesis, because greater attention was paid to the marks of non-kin females. Kin females might not pose an infanticidal threat, perhaps explaining greater tolerance among related reproductive females. We concluded that scent-marking may be a relatively low-cost means of territorial defence, as well as a means of communication of aspects of individual identity.     

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.     

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     

The scent of sun worship: basking experience alters scent mark composition in male lizards

Signals used in female choice should honestly advertise the benefits that males can provide, with direct benefits often argued as being more important than indirect benefits. However, the nature of direct benefits in species without paternal care or nuptial gifts is poorly understood. Previous studies on lizards suggest that females decide where to settle and assumedly who to mate with based on information contained in scent marks from territorial males. Access to high-quality thermal resources is crucial for female reproductive success. Females may therefore be able to detect and exploit thermal-induced variation in the chemical composition of male scent marks when assessing the quality of his territory. We show that the amount of time male wall lizards (Podarcis muralis) are allowed to bask significantly alters the chemical composition of their femoral secretions used in scent marking. The direction of the change is consistent with adaptive plasticity to maintain signalling efficacy under warm conditions that increase evaporation of femoral secretions. The compounds affected by basking experience included those previously associated with male quality or shown to mediate male–male competition in lizards. However, whilst female lizards could discriminate between scent marks of males that had experienced different basking conditions, they did not preferentially associate with the scent from males from high-quality thermal conditions. These results highlight the potential importance of a previously neglected environmental effect on chemical signalling. We suggest thermal effects may have significant consequences for scent-mark composition in variable environments, with potential repercussions on olfactory communication in lizards.     

Seasonal variation in male-female competition,cooperation and selfish hoarding in a monogamous songbird

Both cooperation and conflict between the sexes are commonplace in monogamous mating systems. However, little is known about how cooperation and competition varies seasonally in monogamous species that maintain permanent territories. We presented territorial pairs of male and female New Zealand robins (Petroica australis) with a large supply of insect prey at monthly intervals for 2 years. Behavioural observations after food presentation were then made to quantify seasonal and sexual differences in aggressive interactions over prey, prey acquisition rates, mate provisioning, offspring provisioning, selfish food hoarding and cache retrieval. Data were used to evaluate sex-specific behavioural strategies of mediating competition for food. Results showed that males aggressively excluded females from experimental food sources year-round. Females only accessed food sources when males left them unattended. Consequently, females acquired fewer prey than males. After controlling for differences in prey acquisition, both sexes consumed similar amounts of prey in the non-breeding season. Even though males aggressively excluded females from accessing food sources directly, males fed large amounts of prey to females during the breeding season. Both sexes provisioned young at similar rates. Males cached less prey than females in the breeding season but more prey than females in the non-breeding season. Females showed similar caching intensities year-round. Although males tried to defend their hoards, females frequently retrieved male-made caches. Overall, results showed that although New Zealand robins cooperate to raise offspring during the breeding season, conflict between the sexes occurs year-round. Males and females display different behavioural strategies to gain access to experimental food sources, which appear to lessen male–female competition for food and evenly distribute food resources between the sexes.     

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.     

Female foraging and male vigilance in white-tailed ptarmigan (Lagopus leucurus): opportunism or behavioural coordination?

For several species of birds, high rates of male vigilance are correlated with high rates of female foraging. This relationship is thought to ultimately result in higher reproductive success for females paired with highly vigilant males. However, previous research has not examined the behavioural mechanism that produces the correlation between male vigilance and rates of female foraging. Foraging females may take advantage of vigilance that males are using for other purposes. Alternatively, the purpose of male vigilance may be to increase females' ability to forage. We examined these alternatives by testing whether vigilance preceded or followed bouts of female foraging more often than would occur by chance alone, using simultaneous behaviour observations of pre-incubation pairs of white-tailed ptarmigan (Lagopus leucurus). Our results indicate that each member of a pair may influence the behaviour of the other. Females were more likely to initiate foraging bouts after males became vigilant than if their mate remained non-vigilant. Moreover, non-vigilant males were more likely to become vigilant if their mate was foraging than if she was engaged in some other activity. Despite the possibility that a sexual conflict exists as each member of a pair attempts to maximize its fitness, both sexes behave as though a major role of male vigilance is to enhance female foraging opportunities. Received: 3 May 1999 / Received in revised form: 14 June 1999 / Accepted: 16 June 1999     

Land or lover? Territorial defence and mutual mate guarding in the crimson-breasted shrike

Crimson-breasted shrikes produce duets which are used in interactions with neighbours and intruders. We examined two major hypotheses explaining duetting, the territorial defence and mate guarding hypotheses, using playback experiments. The responses of 12 pairs towards solo male, solo female and stereo duet playback were analysed using principal component analysis and ANOVA. The measures of response intensity revealed in most cases highly coordinated responses of the pair partners. Although these joint responses could suggest cooperative territorial defence or mutual mate defence, responses to the treatments differed between males and females in terms of three variables. Females increased their answer rates significantly in response to unpaired female intruders, compared to unpaired male intruders. During duet playback, females directed their responses equally at both intruding pair members. In contrast, males were equally responsive towards unpaired male intruders and intruding pairs, but in the latter case directed their responses at the male pair member. In the presence of unpaired female intruders, males increased their solo song rates, but in the presence of intruding pairs, they increased overlapping rates and duetted with their mates. These divergent responses suggest that females use duets for mate guarding against unpaired females, whereas males use solo songs for mate guarding and both solos and duets in territorial defence.     

Female-coerced monogamy in burying beetles

The reproductive interests of the sexes often do not coincide, and this fundamental conflict is believed to underlie a variety of sex-specific behavioral adaptations. Sexual conflict in burying beetles arises when a male and female secure a carcass that can support more offspring than a single female can produce. In such a situation, any male attracting a second female sires more surviving offspring than he would by remaining monogamous, whereas the female's reproductive success decreases if a rival female is attracted to the carcass. Monogamously paired males on large carcasses do in fact attempt to attract additional females by means of pheromone emission, whereas males on small carcasses do not. Females physically interfere with male polygynous signaling using various behavioral tactics. We demonstrate that such interference leads to a significant decrease in the amount of time that males spend signaling, according females a means by which to impose monogamy on their mates.     

Testing function of fiddler crab claw waving by manipulating social context

Many territorial advertisement signals are thought to be dual-function signals, directed to both rival male and receptive female conspecifics. However, few studies have tested this assumption by examining whether in fact both sexes are likely to elicit signaling behavior from territorial males. In this study, I experimentally manipulated the social context of male sand fiddler crabs (Uca pugilator) to investigate the effect of different audiences on the performance of the claw-waving display, a territorial signal that is often presumed to be directed to both males and females. To test whether males perform this signal to both audiences, I measured the frequency of waving behavior by focal males when housed in field enclosures alone, with only males, with only females, or with both males and females. Focal males waved at a low frequency when alone, and the presence of males had no effect on their level of waving. However, in the presence of females, focal males showed a significantly higher level of waving, whether or not males were also present. In addition, there was no association between fighting and waving behavior. This experiment provides evidence that from the perspective of the signaling male, the claw-waving display of U. pugilator is not a dual-function signal but rather is primarily directed to receptive females. Received: 16 December 1999 / Received in revised form: 1 February 2000 / Accepted: 19 February 2000     

Effect of pair-bonding with adults on the ontogenetic manifestation of aggressive behavior in a primate,Saguinus fuscicollis

Summary Injurious aggression, scent marking and some visual displays shown in situations analogous to territorial defense were studied in young saddleback tamarins who had lived with nonrelated adult and juvenile social partners from 6 months of age under the experimental conditions outlined below. Twenty male and 20 female tamarins were removed from their natal families when 6 months old, and were used to form pairs and trios of the following composition: (1) one juvenile female and one juvenile male (10 pairs); (2) one juvenile female and one adult male (4 pairs); (3) one juvenile female, one juvenile male, and one adult male (6 trios); (4) one adult female and one juvenile male (4 pairs). These groups cohabited permanently and when the subjects were between 10 and 12 months old, their social interactions with adult conspecific strangers were studied, using series of 10-min social encounter tests. During these tests injurious aggression (attacks, fights, chases), a number of visual hostile displays (threat face, ruffle, arch) and scent marking were recorded.Young males and females living with adults of the opposite sex showed more injurious aggression against strangers and scent marked more frequently than young subjects living with partners of their own age. Males living with adult females also showed more facial threat than males living with young females (Figs. 1 and 2). Young males living in trios with adult males and young females scent marked less frequently than males living only with a young female. Aggression, scent marking and facial threat shown by subjects living with adult sex partners were at the level of socially and sexually experienced, pair-bonded adults (Fig. 3). No differences in ruffling and arching scores were found. The injurious aggression scores of the subjects were correlated with those of their mates. These results show that tamarins can fulfill the behavioral roles of pair bonded adults and also breed (Epple and Katz 1980) at an unexpectedly early age, when they live under the influence of an adult sex partner. Young animals cohabiting with an adult of the same sex, on the other hand, show a trend toward inhibition of adult-like behaviors.     

Pairing patterns in relation to body size,genetic similarity and multilocus heterozygosity in a tropical monogamous bird species

The relative influence of genetic and phenotypic quality on pairing status and mating patterns in socially monogamous species remains poorly documented. We studied social status and pairing patterns in relation to genetic similarity and multilocus heterozygosity (MLH) estimates from 11 microsatellite markers, and both tarsus length and wing chord (as a measure of competitive ability in territorial defence) in a socially monogamous tropical bird species where individuals defend territories year-round, alone or in pairs, the Zenaida dove, Zenaida aurita. Tarsus length and wing chord did not differ between unpaired territorial birds and paired ones in either sex, whereas paired females, but not paired males, tended to be more heterozygous than unpaired ones. Among 84 pairs, we found no evidence for assortative mating for tarsus length, wing chord, MLH or genetic similarity. However, within pairs, male wing chord was positively related to female MLH and female tarsus length was positively related to male MLH, with no evidence for local effects, suggesting assortative mating by individual quality. Although the observed pattern of mating in Zenaida doves may be the product of mutual mate choice, further assessment of this hypothesis requires direct investigation of both mating preference in each sex and lifetime reproductive success in relation to body size and MLH.     

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 mate choice in the Pied Flycatcher Ficedula hypoleuca

Summary We have examined male and territorial factors which might influence female mate choice in the Pied Flycatcher (Ficedula hypoleuca). Mating success of males was largely determined by the order of arrival on the breeding grounds. Females actively selected those males that had been longest in the area. This is likely to be due to territorial cues, early males having the best territories. About 15% of the males become polygynous, and these are the males that arrived earliest.Male age was relatively unimportant for breeding success, but because old males tend to arrive earlier than yearlings, most polygynous males were old. On average, old males are somewhat darker than young males, but male colour also varies within males of the same age. Polygynous and monogamous males did not differ significantly in colour, and female breeding success was not correlated with the colour of their mates. We show theoretically that it does not pay for females to select young males to avoid polygyny unless polygyny frequency or the number of reliable monogamous males almost double. Hence our hypothesis of polygyny-by-deceit in the Pied Flycatcher remains realistic. Because of male polyterritoriality, females are unaware of the males' status when mating.     

Effects of male removal on female foraging behavior in the Eurasian treecreeper

In old, spruce-dominated forests of central Finland, Eurasian treecreepers Certhia familiaris divide their territories spatially during the breeding season. Females forage primarily on the upper parts of the tree trunks, while males use the lower parts of the tree trunks. In this study we removed males from eight territories in the early nestling period to see if the mate's absence would change the foraging patterns of the resident female. Widowed females foraged at lower heights, thus behaving more like paired males. These females also spent less time on each tree and on each foraging bout than did paired females. We conclude that male removal facilitated the change in a female's foraging niche and foraging time at the trees. Females may re-optimize their foraging site selection owing to the absence of dominant males and a consequent need to increase their parental care. Behavioral plasticity may be the mechanism of niche partitioning between the sexes in this species. Received: 28 June 1996 / Accepted after revision: 27 March 1997     

Reproductive success of monogamous and polygynous pied flycatchers (Ficedula hypoleuca)

One of the most interesting aspects of the mating system of pied flycatchers is the regular occurrence of polygyny. Here we present data on the reproductive success of polygynously paired pied flycatcher males compared to monogamous males based on paternity analyses through DNA fingerprinting. Males paired with two females suffered a higher loss in reproductive output per female compared to monogamous males due to (1) a greater proportion of unhatched eggs in their broods, (2) greater nestling mortality and (3) a greater probability of being cuckolded. Nevertheless, the number of fledglings was significantly greater for polygynous males. Based on the number of nestlings that returned for subsequent breeding seasons, however, the reproductive success of monogamous and polygynous males did not differ significantly. These data raise the question as to why males attempt polygyny. Received: 16 August 1999 / Received in revised form: 15 March 2000 / Accepted: 18 March 2000     

Sex-role reversal in willow tit nest defence

Summary The roles of sexes in the nest defence behavior of monogamous willow tit (Parus montanus) were studied near Oulu, northern Finland, in 1988–1990. The relative roles of the sexes changed during the breeding cycle: females defended their nests more vigorously before hatching and males defended more after hatching. This sexual asymmetry was studied by means of the cost/benefit model of optimal parental investment (PI). Because of the monogamous breeding system, sexual differences in future benefits were not a likely explanation for the asymmetry. This was also supported by preliminary results of DNA-fingerprinting analyses. Behavioral observations — sex-role reversal, high correlation between the mates, and equal variations in male and female behavior — indicated the same. In the beginning of the breeding cycle, higher female defence was related to renesting potential. The extra costs of renesting are considerably higher for females than for males, and therefore, females appeared to benefit more than males in keeping the first clutch alive while renesting was still possible. Such a female strategy was possible in this northern population, since the time for renesting was rather short and never lasted beyond the hatching of the first nests. After this point, the male can only invest in the present clutch. By the end of the breeding cycle, increased defence of the nest by males may be a consequence of males being larger and/or in better condition than females. Therefore, in the latter half of the breeding cycle, the sexual differences in nest defence did not indicate any sexual difference in PI. The asynchronous arrival of the parents at the nest also affected individual responses, indicating that defending the nest is a dynamic process.     

Do male plumage and song characteristics influence female off-territory forays and paternity in the hooded warbler?

Extra-pair fertilizations are common in many socially monogamous species, and paternity studies have indicated that females may use male vocal performance and plumage ornaments as cues to assess male quality. Female off-territory forays may represent a key component of female choice and male extra-pair mating success, and female foray behaviour is expected to be strongly influenced by indictors of male quality. In this study, we examined how male song and ornamentation affect how often females left their territories, which males they visited and extra-pair paternity in a socially monogamous passerine, the hooded warbler (Wilsonia citrina). We radiotracked 17 females during the fertile period and quantified male vocal performance (song output and rate) and plumage characteristics (size of the black melanin hood and colour of the black hood, yellow cheeks and breast areas). We obtained blood samples and determined paternity at 35 nests including those of 14 females that we radiotracked. Eleven (65%) of the 17 females forayed off-territory, whilst fertile and female foray rate was positively correlated with the number of extra-pair young in the nest. Females that left their territories more frequently were paired with males that sang at a low rate. In addition, extra-pair mates had higher song rates than the social mates they cuckolded (5.3 songs/min vs. 4.4 songs/min). Female off-territory forays or extra-pair paternity were not significantly related to male plumage characteristics. Our results indicate that a high song rate influences both the foray behaviour of a male’s social mate and the likelihood that he will sire extra-pair offspring with neighbouring females.     

Plasticity in spawning visits of female damselfish, Stegastes nigricans : effect of distance to mates

Both sexes of the damselfish Stegastes nigricans hold individual territories in which they feed on filamentous algae. At dawn, females visit males' territories to spawn, and the males guard the eggs until hatching. We examined how females' spawning behavior varied according to the distances to their mates. Females usually mated with a single male per morning. The distance to the territory of a mate (0.7–12.8 m) did not affect a female's total spawning time per morning, but affected the number of her spawning visits with that male. Females made many repeated spawning visits when spawning with males at short distances, while they spawned the entire clutch in one visit when spawning with males at long distances. This plasticity in female behavior appears to be related to two costs during the spawning visits: (1) intrusions by other fish to feed on algae in the female's territory during her absence, which may cause the female to return repeatedly to her territory for defense, and (2) attacks on the female by other territorial fish, which increased with the distance to their mates' territories. To minimize the sum of both costs, females should change the number of spawning visits depending on the distance to the males' territories. Received: 30 September 1996 / Accepted after revision: 17 March 1997     

Multiple sexual pigments,assortative social pairing,and genetic paternity in the yellow warbler (Setophaga petechia)

In socially monogamous species, extra-pair paternity may increase the reproductive success of highly ornamented males, mediating the evolution of sexual ornaments. However, ornaments may also attract social mates, and a tradeoff between extra-pair paternity (EPP) and within-pair paternity (WPP) may complicate mating strategies. Further, in many socially monogamous species, females are also ornamented, and the relationship between female ornamentation and patterns of EPP has been neglected. We investigated the patterns of genetic paternity with respect to carotenoid- and melanin-based pigmentation in yellow warblers (Setophaga petechia) of both sexes. We asked whether males face tradeoffs between EPP and WPP, how paternity patterns relate to carotenoid- versus melanin-based pigmentation, and whether less EPP occurs in broods when males and females are assortatively paired. Males faced a tradeoff between EPP and WPP. Moreover, non-additive relationships existed between paternity patterns and the two pigment types in both sexes. Males with high melanin coverage but dull carotenoid pigmentation achieved EPP but lost WPP, whereas males with high levels of both pigment types had high WPP but gained little EPP. A parallel pattern occurred in females. Warblers paired assortatively by pigmentation and EPP was less common in broods when the sexes were assortatively paired by carotenoid pigmentation. Results suggest that the most colorful birds obtain high quality social mates and advance reproductive success through WPP, show that correlations can arise between female ornamentation and patterns of EPP, and also uniquely suggest that social pairing patterns may influence extra-pair mating strategies.