Richard E. Brown

Mammalian Social Odors: A Critical Review

Publisher Summary This chapter discusses the information contained in the odorous secretions of mammals and provides a classification system based on the behavioral and chemical analyses. This classification divides social odors into two groups: identifier and emotive. Identifier odors are defined as those produced through the regular metabolic processes of the animal, without specific stimulation. The emotive odors are those produced as the result of some transient emotional state or external stimulus. The chapter categorizes nine different types of information contained in mammalian social odors: species, age, sex, colony membership, individuality, social status, reproductive state, maternal state, and stress odors. Social odors are modified by diet and hormone levels and by bacterial action. When the chemicals and bacteria responsible for producing the social odors have been identified, the responses of test animals show large individual differences. Responses to olfactory stimuli depend on hormonal and experiential factors. Theoretical models in the study of population regulation, sexual selection, kinship recognition, altruism, parental care, and territoriality infer that animals recognize particular individuals and specific relationships, and such recognition may depend to some extent on the information contained in olfactory signals.

The Major Histocompatibility Complex and the chemosensory recognition of individuality in rats

The present experiments provide the first evidence that congenic strains of rats, which differ only in the MHC, produce discriminably different urinary chemosignals. Urine from adult male PVG and PVG.R1 rats, which differ only in the A region (class 1) of the MHC, was used in a habituation-dishabituation task, with male PVG-RTlu, Wistar albino, and Lister hooded rats as subjects. Urine from PVG males was easily distinguished from that of PVG.R1 males by all three strains. Individual PVG males were not distinguished by their urine odours, but individual PVG.R1 males appeared to have discriminably different odours. A repetition of this experiment indicated that this discrimination may have been due to impurities in the urine. Odours from serum were not sufficient for discrimination between the two strains, nor was the class 1 molecule purified from the urine. Urine with the class 1 molecule removed (remainder fraction) could, however, be used to distinguish between the strains. The chemicals in the urine which give this distinctive odour may be fragments of the class 1 molecule or small molecules associated with the class 1 molecule. The MHC appears to control the odour cues which are used by mammals for individual recognition and may provide an olfactory basis for kin recognition but the mechanism by which the MHC controls these olfactory signals is unknown.

Social and hormonal factors influencing infanticide and its suppression in adult male Long-Evans rats (Rattus norvegicus).

In a series of six experiments, the experiential and hormonal factors influencing infanticide in Long-Evans hooded rats were examined. Males, but not females, purchased from a breeder as adults exhibited infanticide at high rates, whereas males reared in the laboratory until adulthood were less likely to be infanticidal. Sexual experience reduced the rate of infanticide in laboratory-reared males, and cohabitation with a female through pregnancy and lactation (including exposure to pups) inhibited infanticide in previously infanticidal males. Fourteen days of cohabitation with a pregnant female following copulation inhibited infanticide in males purchased from a breeder, but copulation without cohabitation and copulation followed by cohabitation with a nonpregnant (ovariectomized) female did not inhibit infanticide. Castration of laboratory-reared males in adulthood did not reduce their rate of infanticide, whereas testosterone implants increased the number of males exhibiting infanticide. The importance of hormonal and experiential factors for controlling infanticide in male rats is discussed.

Class I and class II regions of the major histocompatibility complex both contribute to individual odors in congenic inbred strains of rats

The major histocompatibility complex (MHC) of the rat has three regions—A (class I), B/D (class II), and C/E (class I)—and congenic strains are available which differ in each of these regions. We used the habituation-dishabituation procedure to examine the ability of PVG-RT1u male rats to discriminate between the urinary odors of congenic rat strains which differ genetically only at certain individual regions of the MHC. The results of five experiments indicate that discrimination can be made between urine from rats which differ in all three regions of the MHC (PVG vs. PVG-RT1av1 donors), only in the class I A region (PVG vs. PVG.R1 donors), only in the class I C/E region (PVG.R19 vs. PVG-RT1av1 donors), only in the class II B/D region (PVG.R1 vs. PVG.R19 donors), and in all regions except the classical class IA locus (PVG-RT1av1 vs. PVG.R1 donors). These results indicate that all of the MHC regions may contribute to the individual odors of rats.

Hormonal control of odor preferences and urine-marking in male and female rats.

Abstract Gonadectomized male and female rats show no preferences for the odors of conspecifics of the opposite sex and no urine-marking. Castrated males given testosterone propionate (TP) injections showed preferences for female odors over no odor as did males given estradiol benzoate (EB). Males given EB plus progesterone (P), P only, or oil (controls) showed no preferences for female odors. No group of ovariectomized females (TP, EB, EB+P, or oil injected) showed a preference for male odors over no odor. Males given TP, EB, or EB+P injections showed an increase in urine-marking while males given P or oil showed no marking. Females given TP injections showed an increase in marking but those given EB, EB+P or oil showed no marking. These results are discussed in relation to studies on the hormonal control of scent-marking in gerbils and sexual behaviour in rats.

Object-directed urine-marking by male rats (Rattus norvegicus)

Male rats use anogenital drag and leg-lift positions to direct urine toward objects in their environment. Paired-comparison tests indicated that objects which were previously odorized with urine from male or female rats were investigated and urinated upon more than nonodorized objects. Objects odorized with the males own urine were investigated more, but not urinated upon more than nonodorized objects. These results indicate that conspecific urine odors function both to attract other rats and to stimulate scent marking.

Individual odors of rats are discriminable independently of changes in gonadal hormone levels

Male Long-Evans hooded rats were tested for their ability to discriminate between the urine odors from individual outbred Long-Evans rats using the habituation-dishabituation method. There were discriminable differences between the urine odors of two individual intact males, castrated males, estrous/proestrous females, diestrous/metestrous females and ovariectomized females. Thus, individual outbred rats of both sexes can be discriminated on the basis of their urine odors using this technique and discrimination between individuals occurs despite changes in gonadal hormone levels. This suggests that individual recognition is independent of reproductive state and social status although these may influence the production of body odors used for individual discrimination in rats. Individual odors most likely reflect genetic differences between individuals within the outbred strain.

Interaction of hunger and sexual motivation in the male rat: A time-sharing approach

Abstract To examine the interaction of hunger and sexual motivation, male rats were given sexual behaviour tests under 0, 24, and 48 h of food deprivation. Each male was placed with an oestrous-induced female and allowed to copulate until sexual exhaustion. Food was freely available throughout the test period. Mount and intromission latencies increased under both levels of food deprivation, but neither ejaculation frequency nor any of the other fourteen measures of sexual behaviour were altered under deprivation conditions. There was a decreased latency to start eating, an increase in time spent eating, and an increase in the amount of food eaten with increased food deprivation. The frequency of feeding bouts increased, but the duration of feeding bouts was constant over deprivation conditions. Under food deprivation, animals shifted from sexual behaviour to feeding more frequently than when they were non-deprived. These shifts occurred primarily during periods of low sexual arousal. The majority of feeding occurred during the post-ejaculatory intervals. Bouts of sexual behaviour were not usually interrupted by bouts of feeding. This pattern suggests that feeding and sexual activity occur on a time-sharing basis with sexual behaviour as the dominant activity.

Preferences of pre- and post-weanling long-evans rats for nest odors

Three experiments were conducted on the preferences of infant rats for nest odors. Pre-weanling rats preferred their own nest odor to nests of strange litters and showed low preferences for the nest odors of virgin females. Nest odors of unmated males were investigated less than the pups own nest odor but more than the odors of virgin females. Male and female rats did not differ in odor preferences. Rats reared with both their dam and sire did not differ in their odor preferences from rats reared with their dam alone when tested at 16-20 days of age, but when tested at 33-38 days of age they showed a greater preference for male odors. Post-weanling rats did not show a preference for the nest odors of lactating females and began to show sex differences in their preferences.

The 22-kHz pre-ejaculatory vocalizations of the male rat☆

Abstract Male rats were found to emit 22-kHz pre-ejaculatory vocalizations when approaching females after they had achieved 4 or more ejaculations. The onset of these vocalizations was associated with increases in mounts without intromissions and decreases in intromission rate. On those ejaculatory series with 22-kHz pre-ejaculatory vocalizations, the females showed a lower lordosis intensity and a higher number of agonistic responses than on series with no vocalizations. It is suggested that the pre-ejaculatory vocalizations may serve to inhibit female agonistic behavior and stimulate sexual responsiveness.