Scent marking by male dwarf hamsters (Phodopus sungorus campbelli) in response to conspecific odors

Male hamsters (Phodopus sungorus campbelli) scent marked at greater frequencies in the presence of conspecific odor, either male or female, than in clean areas. Marking rates were not different between male and female odor conditions. In contrast, the pattern of investigation in response to conspecific odor did differ between the male and the female odor conditions. When male odors were used as stimuli, investigative sniffing increased at the scent marking sites but when female odors were used as stimuli investigative sniffing increased throughout the arena. Thus, male dwarf hamsters direct their scent marks at both male and female conspecifics, discriminate between male and female odor, and investigate in a different manner areas scent marked by males and females.     

Vaginal scent marking: effects on ultrasonic calling and attraction of male golden hamsters

Male hamsters were tested for their responses to areas that had been scent marked by intact or vaginectomized females to determine the effects of naturally deposited vaginal secretions on male behavior. In the first experiment males produced more ultrasonic courtship calls when investigating areas marked by intact females than areas scented by vaginectomized females, demonstrating that vaginal marks facilitate such calling. In a wind-tunnel preference test situation in which scent-marked alleys and clean alleys served as sources of odor, males approached the scented alley first if it had been freshly marked by intact females but not if it had been scented by vaginectomized females or other males. Thus, the odors of vaginal marks are sufficient to attract males over short distances. After males entered these alleys they showed a preference for odors of both intact and vaginectomized females over no odors, but still spent significantly more time investigating the odors of intact females than those of vaginectomized females. These experiments indicate that vaginal secretions are one of the primary cues that elicit male courtship calling, and the small quantities of vaginal secretions deposited by females in vaginal marks are sufficient to elicit ultrasonic calling and attract males over short distances. Thus it is likely that vaginal scent marking and ultrasonic calling by females interact to facilitate attraction and location of mates during courtship.     

Female meadow voles,Microtus pennsylvanicus,respond differently to the scent marks of multiple male conspecifics

Many nonhuman animals are capable of discriminating a group or entity containing more objects from one containing less of the same objects. The capacity for making judgments of numerousness may also allow individuals to discriminate between potential mates. Female meadow voles (Microtus pennsylvanicus) may use judgments of relative numerousness to distinguish between potential suitors by selecting males that signal their interest by depositing more scent marks relative to other males. We used a familiarization–discrimination paradigm in the absence of training to test the hypothesis that female voles will discriminate between the different numerosities of scent marks of two male conspecifics that are similar in features of their phenotype and quality. During the exposure phase, we presented female voles with different ratios of feces scent marks from two males. During the test phase, we presented females with a single, fresh fecal scent mark from each of the two male donors, whose marks they had previously encountered during the exposure phase. In both phases, females spent more time investigating the scent mark(s) of the male that deposited more scent marks than that of the male that deposited fewer scent marks provided the difference in the ratio of scent marks provided by the male donors in the exposure phase was ≥2. Our results are consistent with studies on a variety of taxa, suggesting that numerosity discriminations are evolutionarily ancient and spontaneously available to nonhuman animals and humans.     

Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus)

Prairie voles (Microtus ochrogaster) and montane voles (M. montanus) display marked differences in social organization in the field. Trios of 1 male and 2 females were studied in a large enclosure for a 10-day period. Prairie voles spent 59% of the observation time in side-by-side contact, whereas montane voles spent only 7% of the time in contact. Vaginal smears indicated female-female suppression of estrus in prairie voles; female montane voles appeared to cycle in the presence of males. Male prairie voles preferentially paired and nested with 1 of the females, and vaginal estrus generally followed pair formation by 2 days. Male montane voles did not spend time preferentially with either female, even after mating. These results suggest that the contrasting mating systems of these species result from differences in the propensity for affiliative behavior and social bonding rather than from mate availability or female receptivity.     

Pheromone‐mediated intrasexual aggression in male lizards,Podarcis hispanicus

Sex recognition is based on color signals in many species of lizards. However, olfactory stimuli are also clearly involved, and many species might rely primarily on chemoreception. We aimed to examine whether color pattern or odors, or a combination of both factors, induce the aggressive response of males of the lizard P. hispanicus. We experimentally manipulated the coloration and odor of male P. hispanicus, thereby creating groups with all combinations between coloration and odor of males or females. Using data from staged encounters, we compared the responses of resident males to the experimental groups of manipulated males and their response to unmanipulated individuals (males and females). Responding males reacted significantly more aggressively to intruders with male odors independent of their coloration, whereas intruders with female odors did not elicit aggressive responses but were preferentially courted, irrespective of their actual sex and body coloration. In addition, intruders with female odors elicited a higher number of tongue‐flick explorations than male odor ones. Comparisons with unmanipulated male and female intruders agreed with these expectations. Therefore, at least at close range, odoriferous cues seem to be more important than color patterns in sex recognition and intrasexual aggression by male P. hispanicus. We suggest that this might be a pattern commoner than expected in many species of reptiles.Aggr. Behav. 28:154–163, 2002. © 2002 Wiley‐Liss, Inc.     

Agonistic behaviour and bite wound patterns in wild water voles (Arvicola terrestris L.)

Intra‐specific aggression was investigated in a wild colony of Water voles between 1999 and 2004 in South Wales, UK. The occurrence and location (i.e. on the head, neck, body or tail) of bite wounds were recorded for adult and juvenile male and female voles. The greatest (33%) incidence of bite wounds were recorded on juvenile females and the lowest (18%) in adult females. Seasonal analysis of wound data in adults revealed that females were more likely to be bitten during the breeding season whereas bite patterns in males did not vary seasonally. Analysis of bite pattern topography revealed that most Water voles seemingly attempt to bite vulnerable target areas of the body (namely the head and tail). This is in contrast with studies on rats and mice where competitive forms of attack (particularly involving males) largely avoid these areas of the attacked animal's body. Targeting vulnerable areas is normally a characteristic of defensive modes of attack. Patterns of bite topography and agonistic behaviour in this species seem to reflect competitive interactions between individuals, particularly between territorial females and their female offspring, over access to essential resources. Aggr. Behav. 32:599–603. 2006. © 2006 Wiley‐Liss, Inc.     

Role of neonatal androgens in sexual differentiation of brain structure, scent marking, and gonadotropin secretion in gerbils

Gerbils display a sexually dimorphic scent marking behavior that responds to testosterone (T) in adulthood and develops under the influence of testosterone perinatally. A complex of cell groups between the preoptic area and anterior hypothalamus of the gerbil brain is also sexually dimorphic and responsive to testosterone. One of these cell groups, the sexually dimorphic area pars compacta (SDApc), usually exists only in males. Even when given testosterone, adult female gerbils rarely have an SDApc. To determine if the SDApc develops under the influence of testosterone, male gerbils were castrated or given sham operations on the day they were born or 1 day later, or were not manipulated. Female gerbils were injected subcutaneously with 0, 50, or 100 micrograms testosterone propionate (TP) on the day after birth. When given ovarian transplants as adults, neonatally castrated males scent marked at low levels typical of females. Neonatally androgenized females given testosterone as adults scent marked at high levels typical of males. Neonatal castration did not affect the probability that the SDApc would develop, but neonatal androgenization did. Half the females given either dose of TP as neonates had SDApcs bilaterally. The sizes of the SDApcs present in females depended on the dose of testosterone given neonatally. The larger dose produced larger SDApcs. The 100-micrograms dose of TP also defeminized gonadotropin secretion, but the 50-micrograms dose did not. The castration of males neonatally prevented the defeminization normally caused by endogenous testosterone. Both groups of neonatally castrated males formed corpora lutea in their ovarian transplants, but control males did not.     

Female behavior in populations of mice in the presence and absence of male hierarchy

Female aggression may be the regulator of population size in small mammals. Freely growing populations of house mice showed several differences in aggressive female behavior in the presence and the absence of a male hierarchy. Territoriality in females and not in males appeared to maintain social order and regulate population density. Certain females were seen patrolling and guarding the territory and chasing and fighting with both male and female intruders. These females did not fight amongst themselves, suggesting that they were not fighting for rank (as do the males) but for territory. Although these aggressive females produced young, the pups were neglected, and few were weaned. The non-aggressive females were the successful breeders. Aggression by the females only occurred when there was reproduction and increased densities. Assembled females with no males present never show this aggression. The occurrence of “male-type” behavior became most apparent when the males were removed at peak population densities. The removed males were then castrated and injected with testosterone cyprionate. Doses were increased by population cage, and therefore all males returned to each freely growing population were given the same dose. The males given oil placebo injections showed no return of a male hierarchy and the females showed high levels of aggression toward them. Males injected with testosterone cyprionate showed return of male aggression and fighting and mounting of females. But the new “dominant” females continued their patrols and chased males away from their territories and did not permit these males to mount. Male-male fighting consisted primarily of frontal attacks to the face and roll and tumble fights. Female-male aggression consisted primarily of attacks to the posterior region targeted at the base of the tail and the genitals of the male. The males were rarely seen attacking females and then only during mating. Females only attacked each other in defense of their territories.     

Meadow voles, Microtus pennsylvanicus, can distinguish more over-marks from fewer over-marks

Is it possible that voles have a sense of number? To address this question, we determined whether voles discriminate between two different scent-marking individuals and identify the individual whose scent marks was on top more often than the other individual. We tested whether voles show a preference for the individual whose scent marks was on top most often. If so, the simplest explanation was that voles can make a relative size judgement—such as distinguishing an area containing more of one individual’s over-marks as compared to less of another individual’s over-marks. We found that voles respond preferentially to the donor that provided a greater number of over-marks as compared to the donor that provided a lesser number of over-marks. Thus, we concluded that voles might display the capacity for relative numerousness. Interestingly, female voles were better able than male voles to distinguish between small differences in the relative number of over-marks by the two scent donors.     

Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): II. Discrimination of conspecific scent

Scent marking in spotted hyenas (Crocuta crocuta) includes the deposition of anal sac secretions, or "paste," and presumably advertises territorial ownership. To test whether captive hyenas classify and discriminate individuals using odor cues in paste, the authors conducted behavioral discrimination bioassays and recorded hyena investigation of paste extracted from various conspecific donors. In Experiment 1, subjects directed most investigative behavior toward scents from unfamiliar hyenas and members of the opposite sex. In Experiment 2, male hyenas discriminated between concurrent presentations of paste from various unfamiliar females in similar reproductive states. Thus, pasted scent marks convey information about the sex, familiarity, and even identity of conspecifics. Aside from territory maintenance, scent marking may also communicate information about individual sexual status.     

Olfactory discrimination of estrous condition by the male golden hamster (Mesocricetus auratus)

After repeated exposure to receptive and nonreceptive females, male golden hamsters were tested for olfactory preferences in a four-choice olfactometer. Males discriminated between the odor of anesthetized females in different stages of their estrous cycle when the airstreams carrying the stimulus odors were diluted. Previous failures to demonstrate such an ability were probably due to ceiling effects resulting from laboratory testing. Males preferred the odor of females on the day before receptivity (a day coincident with maximal scent marking by the female) and least preferred the odor of females on diestrus-1 (the day on which females attacked and chased males during pretesting encounters). Detection and quick response to an impending estrus would be especially important for males of a solitary and promiscuous species in which there is a first male mating advantage.     

Role of female behavior in controlling population growth in mice

Sex ratio does not appear to be a factor in generating the characteristic population growth curve. Freely growing populations of house mice, consisting of all females and one male, stopped their growth at approximately the same densities as normal sexratio populations used as references. The mechanism(s) of female control of population dynamics may be related to female aggressive behavior. As the all-female/one-male populations approached their maximum size, the females began to show wounding patterns and social hierarchies in much the same manner as males in populations with normal sex ratios. The male in each of the populations was severely wounded in the posterior region, and each lost its tail as a result of injuries which could have been inflicted only by the females. The female social hierarchy can be seen only when there has been reproduction and population growth. Assembled populations of all females rarely exhibit aggressive behavior. Female aggression becomes apparent only when the population approaches its maximum size and thereafter. These data are consistent with the hypothesis that males are competitive among themselves for territory and social rank, and ultimately to mate with the females. Other investigators have indicated that females respond to population size, which may reflect increased competition between the females with the establishment of territories. Thus female agression may control population growth, a role previously ascribed to male aggression.     

Effects of female odors on the sexual behavior of male hamsters

A series of experiments was undertaken to investigate the effects of removal of several scent glands and scent-producing organs of female hamsters on the copulatory performance of male hamsters. In the first experiment it was shown that males engage in less copulatory activity toward females lacking vaginal secretions than toward females with these odors. Eliminating visual cues by observing pairs under infrared illumination did not change the performance of males toward these two kinds of females. The results of Experiment 2 indicated the importance of flank, ear, and Harderian glands as well as vaginal secretions--males showed the highest levels of copulatory behavior toward females with a full complement of odors and the lowest levels toward those lacking three of four sources of scent. Similar results were obtained in the third experiment in which anesthetized females were used as stimulus animals to increase the importance of chemical cues and to reduce variability due to the behavior of females. The sexual behavior of males was greatest toward females with all sources of scent present, lower toward those lacking vaginal secretions, and still lower toward those lacking vaginal secretions and other sources of odors. In the fourth experiment we asked whether any one of the nonvaginal scent glands was particularly important in stimulating male sexual behavior, but we found no differences in male performance toward females that lacked vaginal secretions or that in addition lacked one of the other scent glands. In the fifth experiment males displayed higher levels of sexual behavior toward vaginectomized females than toward vaginectomized females that had been deodorized by a cleaning procedure, again indicating the importance of nonvaginal odors in stimulating copulatory performance. Thus these experiments demonstrate the importance of vaginal secretions in the sexual arousal of male hamsters, a role for nonvaginal odors in sexual arousal of males, and the lack of necessity of these odors for male copulatory behavior. These results have implications for theories of olfactory communication in mammals and for interpretations of experiments in which lesions of the olfactory system lead to deficits in male copulatory performance.     

Sex and species recognition by wild male southern white rhinoceros using contact pant calls

Recognition of information from acoustic signals is crucial in many animals, and individuals are under selection pressure to discriminate between the signals of conspecifics and heterospecifics or males and females. Here, we first report that rhinos use information encoded in their calls to assess conspecifics and individuals of closely related species. The southern (Ceratotherium simum) and critically endangered northern (C. cottoni) white rhinos are the most social out of all the rhinoceros species and use a contact call pant. We found that southern white rhino pant calls provide reliable information about the caller’s sex, age class and social situation. Playback experiments on wild territorial southern white rhinoceros males revealed that they responded more strongly to the pant calls of conspecific females compared to the calls of other territorial males. This suggests that pant calls are more important form of communication between males and females than between territorial males. Territorial southern males also discriminated between female and territorial male calls of northern species and reacted more intensively to the calls of northern than southern males. This might be caused by a novelty effect since both species naturally live in allopatry. We conclude that white rhinos can directly benefit from assessing individuals at long distances using vocal cues especially because their eyesight is poor. Pant calls thus likely play a significant role in their social relationships and spatial organization. In addition, better understanding of vocal communication in white rhinos might be helpful in conservation management particularly because of their low reproduction in captivity.     

Significance of visual cues in choice behavior in the female zebra finch (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis><Emphasis Type="Italic">castanotis</Emphasis>)

Female zebra finches show a preference for male zebra finches over heterospecific males based solely on the auditory cues of males, such as songs. The present study was designed to investigate whether females show a similar preference for male zebra finches based solely on visual cues. Using a Y-maze apparatus, social preference of female zebra finches was studied between male zebra finches and male Bengalese finches in three experiments. In experiment 1, where female zebra finches could see and hear live male zebra finches and male Bengalese finches, the females preferred to associate with the male zebra finches. In experiment 2, using a sound-attenuated experimental apparatus, subjects could see, but not hear, male zebra finches and male Bengalese finches. The subjects did not show a significant preference for associating with zebra finches. In experiment 3, as in experiment 2, females could see live male zebra finches and male Bengalese finches in the sound-attenuated chambers. However, in experiment 3, the subjects also heard prerecorded auditory cues (i.e., songs and calls) of male zebra finches, which were presented simultaneously in both arms of the maze. Although the females could not use the auditory cues to identify the location of the male zebra finches, they preferred to associate with the male zebra finches rather than the male Bengalese finches. These results suggest that visual cues alone were effective in initiating choice behaviors by females and that auditory cues facilitate such visually based choice behaviors. Electronic Publication     

Endocrine Mediators of Masculinization in Female Mammals

ABSTRACT— Most mammal species show traditional patterns of sexual dimorphism (e.g., greater male size and aggression), the proximal mechanism of which involves the male's greater pre- and postnatal exposure to circulating androgens. But in several species, females diverge from the traditional pattern, converging on the male form or even reversing sexual dimorphisms. Such "masculinized" females might show elongation of the clitoris, enhanced body size, and aggressively mediated social dominance over males, and they are interesting case studies for examining the role of androgens in females. This review addresses our understanding of the mediating mechanisms of morphological and behavioral development in both traditional and exceptional mammal species. Although certain lines of evidence implicate testosterone in female masculinization, the role for sex steroids in female development remains unclear. The results call for continued study of both hormonal and nonhormonal mechanisms of sexual differentiation, particularly focused on active processes of feminine development.     

Variation in aggressive behavior and anatomo-physiological correlates generated by crowding without physical contact in the house mouse

Behavioral, physiological (i.e., endocrine), and anatomical consequences of crowding in mice were studied in a situation where animals were in auditory, visual, olfactory, and tactile contact but restrained from full physical interactions, to prevent overt aggression. Males that cohabited with females undisturbed by neighboring conspecifics showed greater propensity to attack same-sex intruders and had higher plasma testosterone levels than did their “crowded” counterparts, that is, males cohabiting with females and housed adjacent to other male/female pairs. In this respect, the latter animals resembled submissive males. However, a significant increase in weight of androgen-dependent target organs (i.e., seminal vesicles and preputial glands) was found in crowded males. These data indicate that despite the observed inhibition of social aggression these males are not physiologically comparable (homologous) to male mice that experienced defeat and the stress of submission during fighting. The intriguing possibility that different conversion pathway of testosterone are accelerated, as a result of social communication, in males living in these two environments and the behavioral implications of these possibilities are discussed. Finally, the parental behavior of crowded animals, although not freely interacting with each other, was disrupted, causing a marked decrease in reproductive success. In this situation a high incidence of infanticide of their offspring by both parents was observed, whereas this behavior was virtually absent in non-crowded male/female pairs.     

Sex categorization of conspecific pictures in Japanese monkeys (Macaca fuscata)

We investigated whether monkeys discriminate the sex of individuals from their pictures. Whole-body pictures of adult and nonadult monkeys were used as stimuli. Two male Japanese monkeys were trained for a two-choice sex categorization task in which each of two choice pictures were assigned to male and female, respectively. Following the training, the monkeys were presented with novel monkey pictures, and whether they had acquired the categorization task was tested. The results suggested that while monkeys discriminate between the pictures of adult males and females, discrimination of nonadult pictures was difficult. Partial presentations of the pictures showed that conspicuous and sexually characteristic parts (i.e., underbellies including male scrotums or breasts including female nipples) played an important role in the sex categorization.     

Male-female interactions across the female estrous cycle: a comparison of two species of dwarf hamster (Phodopus campbelli and Phodopus sungorus)

Recent studies in our laboratory have suggested that monogamy may be the preferred mating system in the Djungarian hamster (Phodopus campbelli), whereas the available evidence for the closely related Siberian hamster (P. sungorus) does not show the same pattern. Here we examine the behavior of male-female dyads of both species interacting during 1-hr tests in large, familiar habitats containing defensible nest boxes, food, and water. Levels of aggression within pairs were low, compared with those seen during brief intrasexual encounters, whereas affiliative behaviors, such as sniffs, were high. P. campbelli scent marked more than twice as frequently as P. sungorus. Females of both species scent marked at a constant rate irrespective of their location in the habitat, whereas males scent marked at a higher rate in the female's home area. Two major features of the copulatory pattern differed between the two species: (a) The duration of the ejaculatory lock was five times longer in P. sungorus than in P. campbelli. (b) Both species had approximately the same number of mounts in each ejaculatory series, but the intromission/mount ratio was significantly higher in P. sungorus.     

Steroidal modulation of scent investigation and marking behaviors in male and female ferrets (Mustela putorius furo)

Gonadectomized male and female ferrets (Mustela putorius furo) given either testosterone propionate (TP) or oil vehicle preferred to investigate the side of a test cage previously soiled by a breeding male or female as opposed to a clean side. Male and female ferrets receiving TP showed more urogenital wiping than oil-treated animals in either side of the test cage. In a 2nd experiment, ferrets treated sequentially with TP, oil, and estradiol benzoate (EB) were given simultaneous access to sides of a test cage previously soiled by either a breeding female or male. Either EB or TP treatment of females and TP treatment of males facilitated the investigation of odors of opposite-sex ferrets. Females given TP and males given either TP or EB showed increased urogenital wiping in both sides of the test cage. Sex steroids modulate scent investigation and marking in adult ferrets in a sexually differentiated fashion.