Do Pine Voles (Microtus pinetorum) Use Numerous Types of Olfactory Cues to Discriminate Gender?

Olfactory cues can contain information for discrimination of gender that can affect subsequent social interactions. Social rodents are hypothesized to use more olfactory cues than nonsocial rodents to distinguish males from females. The generality of this hypothesis was tested using the pine vole (Microtus pinetorum), a social vole. We examined nine possible sources of odors. A slide containing an odor from a male and a female was presented to each test subject for 3 min. We recorded the amount of time each test subject spent investigating each odor. Females spent significantly more time investigating male urine and male anogenital odors; however, they did not use any other odor sources to discriminate gender. In contrast, males did not use any odor sources to discriminate gender. Our results do not support the hypothesis that all social rodents use numerous odor sources to discriminate gender. Instead, our results are consistent with the alternative hypothesis that use of odor sources to convey information about gender may differ in rodents that live in different microhabitats.     

Olfactory Responses of Neotropical Short-Tailed Singing Mice, <Emphasis Type="Italic">Scotinomys teguina</Emphasis>, to Odors of the Mid-Ventral Sebaceous Gland: Discrimination of Conspecifics,Gender, and Female Reproductive Condition

We examined the olfactory communication of the Neotropical short-tailed singing mouse, Scotinomys teguina, by investigating whether S. teguina responded to odors produced by the mid-ventral sebaceous gland of conspecifics. Females spent significantly more time investigating male odor than an odorless stimulus or a female odor. Males spent significantly more time investigating female odor than an odorless stimulus, but not that of a male odor. This latter result does not seem to be explained by differences in age or sexual experience of test subjects, but may be influenced by reproductive condition of the female odor donor. Male S. teguina spent significantly more time (1) investigating and (2) in total proximity to odors of estrous than non-estrous females. Males spent more time (1) investigating and (2) in total proximity to odors of males than non-estrous females. Finally, given the choice between odor of males vs proestrous females, males showed no preference. Thus, the mid-ventral gland in S. teguina seems to convey information about conspecifics, sex, and female reproductive condition. Male odor, compared with proestrous female odor, is equally interesting to males, suggesting that the gland also plays an important role in male–male communication. Sexual dimorphism in the size of the gland and in the amount of secretion produced by the gland may be related to either male–male competition or female choice.     

Chemo-Orientation Using Conspecific Chemical Cues in the Stripe-Necked Terrapin (Mauremys leprosa)

Although chemical communication has been studied intensively in may reptilian species, little attention has been paid to the role that chemical signals play in aquatic reptiles, such as freshwater turtles. Here, I tested the hypothesis that the stripe-necked terrapin (Mauremys leprosa), an abundant freshwater turtle that inhabits the Iberian peninsula, is able to recognize chemical cues from conspecifics in the water and to modify its behavior in response to such cues. I compared the time spent by adult males and adult females in clean water to the time spent in water that presumably contained their own odor, odor from other males, and odor from other females, both during and outside the mating season. Results show that outside the mating season, both males and females avoid water that contains chemical cues from conspecifics of the opposite sex. During the mating season, male turtles clearly select water with chemical cues from females. Moreover, males prefer to occupy water from their home containers over clean water, and avoid water with chemical cues from other conspecific males. Conversely, during the mating season, females prefer to occupy water with chemical cues from other females, but do not select water from their home containers or water from males. The evolution of chemical communication in turtles, its relation to sexual selection processes, and the implications for turtle behavior are discussed.     

Use of odor baits in traps to test reactions to intra- and interspecific chemical cues in house mice living in outdoor enclosures

House mice (Mus musculus) living in outdoor enclosures were tested for urinary chemical cue preferences using odor-baited traps. In the first experiment, with only volatile cues available, odors from conspecific males and females of various age classes and reproductive conditions were tested; no preferences were exhibited. In the second experiment mice had both nonvolatile and volatile cues available from the same sources as in experiment I. All age and sex class and female reproductive condition groups exhibited odor cue preferences except juvenile females. There were no specific odor cue preferences exhibited by any of the responder types with regard to odors from juvenile females. In the third and fifth experiments, mice were presented with nonvolatile plus volatile or only volatile urine odor cues, respectively, from four genera,Mus, Peromyscus, Microtus, andHomo. Mice of all age classes and both sexes preferredMus musculus odor, were neutral towardMicrotus ochrogaster odor, and avoided odors fromPeromyscus leucopus andHomo sapiens; these patterns were the same regardless of whether only volatile or both volatile and nonvolatile cues were presented. The fourth and sixth experiments involved testing volatile cues only and volatile cues plus nonvolatile cues from human sweat or feces from dogs, cats, or shrews. Mice avoided the human sweat and feces from cats and shrews, but were neutral toward the odor of dog feces. There were effects on whether mice were trapped in the interior of the enclosure or on the perimeter for some odors tested in these six experiments. The findings provide insights regarding possible functions of odor cues in the behavioral ecology of house mice. Odor-baiting traps can be an effective tool with respect to testing some, but not all questions pertaining to olfactory cues and house mouse social biology.     

Patterns of deposition of urine containing chemosignals that affect puberty and reproduction by wild stock male and female house mice (Mus domesticus)

House mice release chemosignals in their urine that influence the timing of puberty and reproductive condition in conspecific females. These experiments tested the possibility that mice depositing urine containing chemosignals that affect puberty and reproduction do so differentially with respect to urine cues from conspecifics. Mice were tested in cages containing samples of urine or water on cotton in wire mesh capsules protruding from the cage floor. Their urine deposition patterns were recorded on squares of filter paper positioned below the cages. Males deposited more urine than females housed in groups, estrous females, diestrous females, or prepubertal females. All groups of mice deposited urine in a nonrandom fashion with regard to urine cues from conspecifics. Male mice deposited more urine near locations previously soiled by females than near water or other males. Grouped females deposited more urine near male urine cues and avoided depositing urine near urine from other group-housed females. Both estrous and diestrous female mice deposited more urine near males than near other urine cues or water, possibly to attract mates. Prepubertal females avoided depositing their urine near male urine and urinated more near urine from grouped females than near other urine types or water. Young females may be avoiding possible male mates until they have attained puberty. This avoidance behavior may enhance the long-term reproductive success of the females that otherwise might mature and mate at too young an age.     

Attractiveness of Opposite-Sex Odor and Responses to It Vary with Age and Sex in Meadow Voles (Microtus pennsylvanicus)

Current models suggest that among short-lived mammals, such as rodents, older adults are less attractive to the opposite sex and spend less time associated with the opposite sex than do younger adults. The objective of this study was to test two hypotheses in three different age groups of meadow voles. The first hypothesis is that 3- to 5 month old voles produce scents that are more attractive to opposite sex conspecifics than those of 7- to 12 month old and 14- to 18 month old voles. The second hypothesis is that 3- to 5 month old voles spend more time than either 7- to 12 month old or 14- to 18 month old voles investigating the scents of an opposite sex conspecific. The first experiment shows that when choosing between two conspecifics, females prefer the odor of the older male within each pair and that males prefer the odor of the 7- to 12 month old females to those of either 3- to 5 month old or 14- to 18 month old females. Thus, the data did not support the first hypothesis. The second experiment shows that the 14- to 18 month old males spent more time investigating female odors than did either the 3- to 5 month old or 7- to 12 month old males and that 7- to 12 month old females spent more time investigating male odors than did the 3- to 5 month old and 12- to 18 month old females. These data did not support the second hypothesis. Overall, older adult male meadow voles are more interested in and attractive to females than are younger adult males. The present data raise questions as to whether current models predict the age-related effects on the behavior of short-lived mammals.     

Odor preferences of wild stock female house mice (Mus domesticus) tested at three ages using urine and other cues from conspecific males and females

Urinary chemosignals from conspecific males and females can influence the physiological processes of sexual development in female house mice. The experiments reported here involved testing the odor and whole animal preferences of female mice presented with stimuli from male mice and grouped female mice. Mice were tested at three different ages. Five types of tests were performed: an olfactometer test using whole animals as stimuli, a second olfactometer test using urine stimuli, a soiled bedding substrate preference test, an animal association test, and a stick-chewing test. The results from all tests indicate that prepubertal females avoided male odors and prefer odors associated with grouped females. By about the age of puberty, the females exhibited a preference for male cues and generally avoided cues from grouped females. As adults, the females strongly preferred cues associated with males and avoided cues from grouped females. Thus, female mice appear to be exhibiting some control over their own physiological development and their reproductive condition by the nature of the stimuli with which they associate. Their stimulus preferences may have consequences for their fitness.     

Recognition of Dominance Status By Chemoreception in the Red Swamp Crayfish, Procambarus clarkii

We tested the hypothesis that chemical signals play a role in the recognition of dominance status in the red swamp crayfish, Procambarus clarkii. Dominance was judged on the outcome of dyadic interactions in all male or female groups of three individuals. This resulted in a dominant, intermediate, and subordinate individual within each population. A choice paradigm in a flow-through Y maze was used to judge whether crayfish were able to recognize dominance through chemical cues alone. Both individuals that interacted with the animal producing the odor and naive individuals were tested. Irrespective of sex and previous experience, individuals increased their rates of locomotion in the presence of conspecific odor. Naive males investigated the dominant arm first, spent more time at the dominant nozzle, and responded more aggressively (as measured by meral spread) to dominant male odor and subordinate female odor. Intermediate males spent more time at the dominant male nozzle and responded more aggressively to dominant male odor. Naive females spent more time at the dominant nozzle. These results show that males recognize dominant animals. Since both naive and experienced males respond to water from dominant animals, we concluded that this is recognition of dominance and not just individual recognition. This signal may be important for the formation or reinforcement of dominance relationships. Based on the change in behavior between odors, we suggest that crayfish can use chemical cues to recognize the dominance status of conspecifics.     

Chemically Mediated Species Recognition in Closely Related Podarcis Wall Lizards

In many animals, chemical signals play an important role in species recognition and may contribute to reproductive isolation and speciation. The Iberian lizards of the genus Podarcis, with up to nine currently recognized lineages that are often sympatric, are highly chemosensory and provide an excellent model for the study of chemically mediated species recognition in closely related taxa. In this study, we tested the ability of male and female lizards of two sister species with widely overlapping distribution ranges (Podarcis bocagei and P. hispanica type 1) to discriminate between conspecific and heterospecific mates by using only substrate-borne chemical cues. We scored the number of tongue flicks directed at the paper substrate by each individual in a terrarium previously occupied by a conspecific or a heterospecific lizard of the opposite sex. Results show that males of P. bocagei and P. hispanica type 1 are capable of discriminating chemically between conspecifics and heterospecifics of the opposite sex, but females are not. These results suggest that differences in female, but not male, chemical cues may underlie species recognition and contribute to reproductive isolation in these species. The apparent inability of females to discriminate conspecific from heterospecific males, which is not because of reduced baseline exploration rates, is discussed in the context of sexual selection theory and species discrimination.     

Odor Preferences of Weanling and Mature Male and Female Pine Voles

Olfactory cues from conspecifics have strong influences on behavior. Both female and male juveniles are attracted to familiar odors while adults show preferences for odors of opposite-sex conspecifics. Females show an increased preference for male odors as they mature, but no study has examined whether change with age is seen in males. In this experiment, responses of weanling and mature male and female pine voles (Microtus pinetorum) to familiar odor cues from their family versus those of an unfamiliar, opposite-sex conspecific were examined. Voles were tested in a three-chambered cage with end chambers containing the stimuli. There was a significant difference in odor preference between weanling and mature females. Weanling females preferred odor cues from their families, and mature females preferred the odors of unfamiliar mature males. The pattern was similar in males but the effect was not as strong. The results support the hypothesis that responses to odor cues change with age in pine voles. At least for females, the change in response to odor cues may be involved in the timing of reproduction and thus dispersal.     

Chemically Mediated Mate Location and Evaluation in the Lobster, Homarus americanus

Many aspects of lobster (Homarus americanus) social behavior have been shown to be regulated by chemical signals. Female lobsters can determine the sex of sheltered conspecifics from a distance, and will approach and attempt to enter male-occupied shelters. We investigated (1) if female attraction to male-occupied shelters and entering decisions are based upon chemical signals, particularly male urine signals, and (2) if male dominance status and female molt stage influence these female behaviors. Sheltered dominant males were fitted with urine catheters, which collect urine and prevent its release into the environment. We found that males increased urine output in response to female entering attempts. Blocking male urine release significantly reduced the incidence of female shelter approach and the time spent attempting to enter. Artificial release of male urine in the presence of a catheterized male restored female approach but not time spent attempting to enter, while artificial urine release alone did not induce either behavior. Females approached any single male, but seemed to prefer to enter shelters occupied by more dominant males. Premolt and intermolt females differed in their behaviors: premolts showed more interest in approaching dominant male shelters without much effort to enter, while intermolts appeared less likely to approach but more motivated to attempt to enter shelters. This study suggests that both intermolt and premolt female lobsters use one or more chemical signals from sheltered males for location and evaluation of potential mates. Male urine appears to carry compound(s) important for both location and entering decisions, although nonurine chemical or other sensory signals are also implicated during close-up mate evaluation.     

The Chemical Basis of Species,Sex, and Individual Recognition Using Feces in the Domestic Cat

Scents emitted from excretions provide important information about the owner. Volatile compounds with higher levels in a species and/or sex, or that vary among individuals could be odor cues for species and/or sex, or individual recognition. However, such compounds have been identified in only a few vertebrate species. In domestic cats (Felis silvestris catus), it is known that unburied cat feces are territorial markers asserting the border of their home range, but little was known which fecal compounds are scent cues for species, sex, and individual recognition in cats. In the present study, we demonstrated the chemical basis for species, sex, and individual recognition using feces of cats. For males, major contents were fatty acids and 3-mercapto-3-methyl-1-butanol (MMB), a derivative of the unusual amino acid, felinine. MMB emission levels from feces had sex-based differences (male > female) and dynamic temporal changes during aging. Cats distinguished fecal odors with and without MMB, and different fatty acid compositions among individuals. No cat-specific compound, such as MMB, was detectable from their anal odor emitting fatty acids. We concluded that fecal MMB is a male sex recognition pheromone in cats and also provides a temporal trace of the owner. After sensing MMB, they may distinguish individual differences of conspecific feces with variable subsets of fatty acids. In contrast to scent marks, since cats can obtain species information from visual cues before sniffing conspecific anal odors, they may use their efforts to distinguish individual differences of anal odors during sniffing.     

Chemical Ecology of the host searching behavior in an Egg Parasitoid: are Common Chemical Cues exploited to locate hosts in Taxonomically Distant Plant Species?

Parasitoids are known to exploit volatile cues emitted by plants after herbivore attack to locate their hosts. Feeding and oviposition of a polyphagous herbivore can induce the emission of odor blends that differ among distant plant species, and parasitoids have evolved an incredible ability to discriminate them and locate their hosts relying on olfactive cues. We evaluated the host searching behavior of the egg parasitoid Cosmocomoidea annulicornis (Ogloblin) (Hymenoptera: Mymaridae) in response to odors emitted by two taxonomically distant host plants, citrus and Johnson grass, after infestation by the sharpshooter Tapajosa rubromarginata (Signoret) (Hemiptera: Cicadellidae), vector of Citrus Variegated Chlorosis. Olfactory response of female parasitoids toward plants with no herbivore damage and plants with feeding damage, oviposition damage, and parasitized eggs was tested in a Y-tube olfactometer. In addition, volatiles released by the two host plant species constitutively and under herbivore attack were characterized. Females of C. annulicornis were able to detect and significantly preferred plants with host eggs, irrespectively of plant species. However, wasps were unable to discriminate between plants with healthy eggs and those with eggs previously parasitized by conspecifics. Analysis of plant volatiles induced after sharpshooter attack showed only two common volatiles between the two plant species, indole and β-caryophyllene. Our results suggest that this parasitoid wasp uses common chemical cues released by many different plants after herbivory at long range and, once on the plant, other more specific chemical cues could trigger the final decision to oviposit.

     

Searching for Major Urinary Proteins (MUPs) as Chemosignals in Urine of Subterranean Rodents

Chemosensory information mediates behavior in many rodent genera. Major Urinary Proteins (MUPs) facilitate chemical communication in some species of mice. We sought to demonstrate the importance of MUPs in chemosignaling across a range of rodent genera that live in different habitats and social structures. We analyzed urine from three subterranean rodent genera from different continents, and with diverse social systems: eusocial Zambian mole-rats (Fukomys), solitary Israeli blind mole rats (Spalax), and social Chilean coruros (Spalacopus). 2D gel electrophoresis revealed low levels of protein, with sequences similar to aphrodisin, in Fukomys mole-rat urine, but no MUPs in urine of any of the studied species. Previous research demonstrated that subjects from the tested genera responded differentially to odors indicating transmission of individuality, family/colony or population, species, and reproductive state in secretions and excretions of conspecifics. This extends, to subterranean rodents, the evidence that rodent species can successfully transmit and receive chemosignals without the necessity of MUPs.     

Demonstration of an odorous intramale primer effect in short-tailed vole,Microtus agrestis L.

Anal (proctodeal) glands of maleMicrotus agrestis housed in social isolation undergo severe atrophy. Their weight and volume is significantly lower than those of the stock control males. The atrophied glands can be revived by subjecting deprived voles to various social odors. Atrophied glands of isolated males do not respond to the odors of male and female urine, voided feces of females, and unvoided feces of males. Atrophied anal glands of males exposed to voided male feces (which have passed the orifice of the anal gland) and soiled bedding from adult males show strong recrudescence. The mean weight and volume of the glands and plasma testosterone level are significantly higher than of males maintained in complete social isolation, although they are significantly less than those of stock control males. Atrophied glands of socially deprived males strongly respond to the odor of ethereal extract of gland secretion. In males exposed daily to anal gland secretion extract, the weight and volume of the gland and plasma testosterone level increase and are not significantly different from those of stock controls. They enjoy higher plasma testosterone levels and consequently larger and more active anal glands than complete isolates.     

Odors in traps: Does most recent occupant influence capture rates for house mice?

Responses of house mice (Mus domesticus) to odors in live traps were studied in a series of eight 0.1-ha outdoor field enclosures. It was assumed that the most recent mouse capture would provide the predominant odor in a trap for at least one week. Three different populations were tested, one in 1989 and two in 1992, involving over 800 different mice. Similar response patterns were recorded from all three groups. Two types of questions were tested: (1) Were there any biases contingent upon what had been previously caught? (2) Were there consistent responses of mice of particular age, sex, or reproductive classes to trap odors? Traps soiled by juvenile females caught adult females significantly less often than expected, but there were no consistent relationships in terms of the effects of specific residual odors on the subsequent capture at a particular trap. For various age, sex, and reproductive classes, (1) adult males preferred odors from juvenile and estrous females and avoided odors of other males significantly more than expected, (2) juvenile females selected traps with odors of other juvenile females and avoided all other types of female odors significantly more than expected, (3) nonestrous females exhibited a significant preference for adult male odor, and (4) estrous females selected traps containing odors from adult males but avoided those that had previously contained either nonestrous or pregnant/lactating females significantly more than expected. These findings have potential implications with regard to both the methods used for trapping small rodents and the social biology of house mice.     

Olfactory recognition of individuals by male cavies (Cavia aperea)

In one study, using a habituation procedure, male South American cavies,Cavia aperea, distinguished individual differences in odors collected from three sources: perineal gland secretions, urine, and supracaudal gland secretions. In a second study, male cavies spent more noninvestigatory time and rested more on the side of a cage containing the odor of a familiar subordinate male as compared to the cage side containing the odor of a familiar dominant male. Since the odor source was a glass plate which had been left in the home cage of the donor males for three days, the actual odorous cue to which the test males responded is not known. These studies demonstrate that male cavies distinguish odors of individuals, that individual differences in odors are found in at least three different sources, and that cavies use chemical cues to distinguish between known individuals.     

Effect of Male House Mouse Pheromone Components on Behavioral Responses of Mice in Laboratory and Field Experiments

Urine of male house mice, Mus musculus, is known to have primer pheromone effects on the reproductive physiology of female mice. Urine-mediated releaser pheromone effects that trigger certain behavioral responses are much less understood, and no field studies have investigated whether urine deposits by male or female mice, or synthetic mouse pheromone, increase trap captures of mice. In field experiments, we baited traps with bedding soiled with urine and feces of caged female or male mice, and recorded captures of mice in these and in control traps containing clean bedding. Traps baited with female bedding preferentially captured adult males, whereas traps baited with male bedding preferentially captured juvenile and adult females, indicating the presence of male- and female-specific sex pheromones in soiled bedding. Analyses of headspace volatiles emanating from soiled bedding by gas chromatography/mass spectrometry revealed that 3,4-dehydro-exo-brevicomin (DEB) was seven times more prevalent in male bedding and that 2-sec-butyl-4,5-dihydrothiazole (DHT) was male-specific. In a follow-up field experiment, traps baited with DEB and DHT captured 4 times more female mice than corresponding control traps, thus indicating that DEB and DHT are sex attractant pheromone components of house mouse males. Our study provides impetus to identify the sex attractant pheromone of female mice, and to develop synthetic mouse pheromone as a lure to enhance the efficacy of trapping programs for mouse control.     

Particular Levels of Odors Released by Virgin Females Attract Conspecific Males of the Funnel-Web Spider <Emphasis Type="Italic">Allagelena difficilis</Emphasis>

Female-released chemical signals are crucial clues for mate-searching males to locate and gain sexual receptivity of conspecific females. Abundant behavioral evidence indicates that female spiders release sex pheromones to guide mate-searching behavior of conspecific mature males. However, the chemical nature of spider pheromones is poorly understood. Females of the funnel-web spider, Allagelena difficilis, employ sit-and-wait tactics for mating. Field observations indicate that males leave their retreats to search for potential mates during the breeding season. Therefore, we investigated whether virgin females release a sex attractant to conspecific males and then explored the chemical nature of the female pheromone. Four fatty acids extracted from the female bodies (palmitic acid, linoleic acid, cis-vaccenic acid and stearic acid) constitute a multiple-component sex attractant to conspecific males in A. difficilis. Unexpectedly, mated females also produce the same fatty acids, but at trace levels. Two-choice experiments showed that males were significantly attracted by the blend of the four fatty acids in appropriate concentrations while avoiding the blend consisting of the same acids at very low concentrations, suggesting that mate-searching males are able to discriminate virgin females from mated females by the quantities of female-specific fatty acids in the funnel-web spider A. difficilis.     

Studies on the nature of chemical signals in scent marks and urine ofSaguinus fuscicollis (Callitricidae,primates)

The circumgenital scent marks ofSaguinus fuscicollis are mixtures of skin gland secretions, urine, and perhaps vaginal discharge. One of their ingredients, urine, is readily investigated by conspecifics. Female tamarins are able to utilize urine to discriminate between the sexes, but it appears that urine, unlike the scent marks, offers no clues for individual discrimination. Moreover, urine is less attractive to conspecifics than complete scent marks, which signal sex and individuality. The sexual identity of marks is recognized even if the tamarins are prevented from contacting the material directly and seems to be retained in a mixture of scent from both sexes.