Roles of the Olfactory and Vomeronasal Systems in Behavior

Farm Animal Behavior

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Roles of the Olfactory and Vomeronasal Systems in Behavior

Benjamin L. Hart, D.V.M., Ph.D.*

Social interactions require identification not only of individuals but of sexual status, social position, physiologic state, and group membership. Of course, animals can recognize each other and discriminate different states on the basis of auditory or visual cues, but chemosensory stimuli interpreted by the olfactory system appear to be most important in individual and subgroup recognition. Because our human chemosensory abilities are very limited compared with that of farm animals, the chemical signals used by animals are inconspicuous to us. An animal's olfactory world is completely different from ours, so it is difficult to imagine the types of chemical cues an animal might be utilizing, what they mean, or how prominent they are. Advancements in this area are based on painstaking experimental work rather than recognizing with our own senses the stimuli that animals are reacting to, as we might in interpreting an animal's response to visual or auditory stimuli. In terms of using chemical cues for identifYing individuals, detecting changes in the environment, or discriminating social or physiologic status, animals may utilize five chemosensory systems associated with the nose:1 4 (1) olfactory system, (2) vomeronasal or accessory olfactory system, (3) septal organ, (4) nervus terminalis, and (5) trigeminal nerve. The gustatory (taste) system is also a chemosensory system, but it appears not to be used in social interactions. In contrast to chemosensory systems associated with the nose, taste in domestic animals is, if anything, inferior to that of humans in terms of acuity or range of stimuli perceived. The two chemosensory systems about which we know the most and that appear to be the most important in understanding animal behavior are the olfactory and vomeronasal systems. In this article, the role of the olfactory system in some general aspects of the behavior of domestic ruminants will be discussed. The vomeronasal system also will be considered, especially with regard to *Professor, Department of Physiological Sciences, University of California School of Veterinary Medicine, Davis, California

Veterinary Clinics of North America: Food Animal Practice-Vol. 3, No.2, July 1987

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recent inforn1ation on the role of flehmen behavior in vomeronasal organ function. Both of these systems are important to ungulates, and knowledge about them is critical to understanding farm animal behavior.

OLFACTION AND SOCIAL INTERACTIONS The functional role of different types of social odors, as outlined by Brown5 in his comprehensive review, appears to apply quite well to farm animals. Identifier odors are those presumably produced by metabolic processes and are constant over long periods of time. These include those that are sex-specific, age-specific, and species-specific. Identifier odors also include those that are group-specific among members of animals housed together as well as those that are individual-specific. A few studies on farm animals have indicated that in probably all species olfactory cues can be used for individual recognition. For example, pigs that were temporarily blinded with contact lenses could still form a dominance hierarchy when mixed with previously unacquainted blind pigs. When the olfactory sense was blocked, the formation of a dominance hierarchy was prevented. 13 Animals of every species tested so far (goats,3 calves,3 sheep,4 and pigs 36) have shown an ability to recognize different individuals on the basis of urine odors. Probably all animal handlers have suspected that farm animals are able to identify different persons on the basis of chemical cues. Curiously, this phenomenon has not been investigated specifically with regard to farm animals. However, Kalmus found that dogs could discriminate between odors of unrelated people and members of the same family but had trouble distinguishing between identical twins. 25 It is probably safe to assume that farm animals have the same olfactory capacity as dogs and are able to recognize the odors of human handlers that they frequently encounter at close ranges. Sex Attractants and Sex Pheromones Social odors that serve as a medium for chemical communication between conspecifics are referred to as pheromones. An important characteristic of a pheromone is its effectiveness over distance and the persistence of the signal over time, allowing for communication in the absence of the signaling animal. Some of the best examples of the functions of pheromones actually come from studies on invertebrates. A classic example is the chemical substance liberated into the air by the female sphinx moth, which can be detected in minute concentrations by male moths 2 or 3 miles down wind. Simply by following the wind in response to the chemical signal, the male is able to come sufficiently close to the female to be able to locate her visually. With some insects, the chemical substances identified with pheromones have been biochemically isolated and identified. Pheromones are assumed to exist in mammals, particularly in association with the occurrence of estrus in females. They function presumably to communicate the occurrence of estrus or impending estrus to conspecific males. Thus, we interpret the olfactory investigation of female urine or

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genitalia by males as a reflection of the male's attempt to utilize the information carried by the sex pheromones of females. To date, no pheromone from females of any species of farm animal has been completely chemically identified or isolated. Because we do not know the chemical structure of such pheromones or the type of information conveyed, some behaviorists prefer to talk about sex attractants of urine or genital secretions rather than sex pheromones. Because females presumably secrete sex pheromones or attractants, it is logical to ask if males might produce a chemical cue of interest to females. An instance in which this is clear has been recognized in boars. In fact, boars produce two sexual attractants or pheromones-one in secretions of the preputial pouch and the other in the saliva produced by the submaxillary salivary glands. The boar pheromones have been identified and are known to be androgens with musk-like odors.2 Both chemicals are responsible for the flavor taint in boar meat. The chemical isolation of a boar pheromone has stimulated some work on the reaction of neurons along the olfactory pathway to this substance and, indeed, certain neurons in the olfactory bulb seem to be selectively activated by this pheromone. 33 One of the boar pheromones, androsterone, has an effect on the display of the immobility response by female pigs when a herdsman places pressure on their backs. Normally only about half of the gilts in estrus pass this back pressure test for estrus in the absence of a boar. However, when the sex pheromone from boars is sprayed towards the nose of gilts in estrus, about 80 per cent respond to the back pressure test. 38,44 An interesting issue with regard to pheromones of females relates to detectability versus attractiveness. The chemical composition of sex pheromones of urine and vaginal secretions must be quite different for different species. Males are sexually excited by chemicals from estrous females of only their own species. If males were attracted to the sex pheromones of many other species, they would spend all their time investigating urine spots and perhaps even making sexual responses to females of different species. Although not necessarily attracted to such substances, animals can detect pheromones from different species. For example, rats can be trained to press a lever in response to air bubbled through urine from estrous cows and to refrain from pressing the lever when the air is from nonestrous cows. 31 This work is a quantitative confirmation of the old herdsman's claim that some dogs can reliably pick out estrous cows in a herd of cows without being instructed as to which cows to choose. This ability of dogs to detect cows in estrus has been demonstrated recently in the laboratory.27 The experience with training rats and dogs to detect chemical cues associated with estrus suggests that chemical identification of such cues is theoretically possible. Undetected estrus is a major problem in farm animal reproduction, so the identification of sex pheromones, such that one could develop practical field tests for chemical markers of estrus, would be a major innovation in reproduction. Another type of behavior that swine pheromones seem to influence is aggression. Androsterone, when applied to the skin of young pigs, suppresses aggressive interactions, suggesting that this is one means by which

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the presence of adult boars reduces fighting in juvenile pigs. 35 It has been found that urine from young pigs that are stressed by moving or fighting can either decrease or increase agression when applied to the skin of other young pigs. ,35 Apparently there are two pheromones produced by fighting pigs, one that inhibits and one that increases aggression.

Scent Marking The marking of environmental objects or the animal's own body with urine, feces, saliva, or secretions from specialized scent glands is referred to as scent marking. Although scent marking of the environment with urine is common in dogs and cats, only one domestic ruminant commonly engages in a type of scent marking. Male goats, especially when they are sexually stimulated, urinate on their chests, necks, front legs, and beards. This behavior, referred to as self-enurination, is seen in some wild ungulates related to goats such as Barbary sheep, mountain goats, and bighorn sheep. Self-en urination is most likely to occur when a male is sexually aroused but restrained from interacting with the female or in the post-ejaculatory refractory period. 41 The function of this behavior has not been established experimentally, but it is suggested that the behavior may hasten the onset of synchronized estrus in females through olfactory stimulation. 7 The behavior may also reveal the male's physiologic condition as indicated by metabolic by-products. Thus, for a dominant male, his urine documents his superior state of nutrition and well-being to both other male competitors and to breeding females. There is a flip side to such chemical advertisement in that subordinate males may recognize a decline in condition of the dominant animal due to aging or declining food intake and utilize this information in timing an appropriate opportunity to challenge his dominance.

THE VOMERONASAL SYSTEM AND SOCIAL INTERACTIONS As remarkable as the olfactory system is for dealing with a complex chemosensory world, investigators are rapidly learning more about the equally complex functioning of the vomeronasal system. The more we investigate chemosensory function in animals, the more functions we come to attribute to the vomeronasal system rather than the olfactory system. Although most of the advances have been made in laboratory rodents, the findings can be applied to explain behavior of ruminants and point to new important areas for future research. The vomeronasal and olfactory systems appear to have separate and distinct functions. This is perhaps most apparent in terms of peripheral receptor location and central nervous system projections. The olfactory system receives input from receptor cells located in the olfactory mucosa of the nasal cavity. The central projection is from olfactory nerves terminating in the olfactory bulbs and projecting from there to the anterior olfactory nuclei, olfactory tubercles, prepyriform cortex, and parts of the amygdala. 9, 43 The vomeronasal organs are paired mucus-filled tubes lying inside the

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base of the nasal septum. In domestic ruminants, stimuli reach the vomeronasal organ openings from both the nasal cavity and the oral cavity. The sensory epithelium lining the lumen of this organ in ruminants is quite similar to that of the main olfactory system,l, 29 but there could easily be biochemical differences in the receptors, as have been found in mice. 8 Vomeronasal nerves that arise from receptor cells in the epithelium project to the accessory olfactory bulbs, which in turn project to the parts of the amygdala and hypothalamus that are specifically involved in the mediation of sexual behavior and reproductive cycles. 43 The vomeronasal organ is absent in human beings as well as in Old World monkeys and apes. 48 Behavioral Functions of the Vomeronasal System Because the vomeronasal system projects to parts of the brain concerned with regulation of sexual behavior and reproductive cycles, it is not surprising to find that virtually all studies in mammals have pointed to the system as having influences on reproductive behavior and physiology.39, 47, 48 Basically, there are two types of functions. One is that of priming or modulation of neuroendocrine regulatory systems from long-term exposure (several hours or days) to chemical stimuli. Typical of effects relating to this function are findings that soiled bedding of adult male mice contains an androgen-dependent chemosignal that accelerates puberty in female mice 46 and that removal of vomeronasal organs in females blocks this acceleration effect. 26 Another finding is that housing female mice together generally results in prolonged estrous cycles and even elimination of cycles in some females. This effect, caused by a chemosignal produced by females housed in groups, is also attenuated by removal of the vomeronasal organ. 42 A similar finding in male mice is that exposure to females results in acute elevations of circulating testosterone concentration and that removal of the vomeronasal organ in males blocks such an effect. 49 A second type of function assigned to the vomeronasal organ and explored to a more limited degree in rodents is that of detection of chemical cues associated with females. This type of function is more like that of olfactory identification of particular odors and requires exposure to the stimulus for only a few minutes or less. Male mice, for example, emit ultrasonic vocalizations in the presence of female mice or female-produced chemical cues. Male mice or male-produced chemical cues do not evoke such ultrasonic vocalizations. Removal of the vomeronasal organ greatly impairs a male mouse's ability to discriminate between chemical cues of male and female mice, as indicated by vocalization responses. 50 Male hamsters that can normally match vaginal scent marks they have sniffed and licked with a female they subsequently encounter lose this chemosensory matching ability after removal of the vomeronasal organ. 45 The stimuli for such short-term detection functions are believe to be fluid-borne, and males typically make physical contact with the stimulus material before making a discrimination. Flehmen Behavior It is primarily chemical detection of information about a female or her state of estrus that has been ascribed to the vomeronasal organ in- ungulates;

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this detection is accomplished through the performance of flehmen. In ungulates such as goats, cattle, and sheep, it has been argued for several years that the lip curl, or flehmen, response of males, which frequently occurs when they contact females or their recently voided urine, is involved in the transfer of substances from the oral cavity to the vomeronasal organ through the naso-palatine duct. 12, 28 It is debatable whether swine exhibit flehmen. There is one report, complete with photograph, that describes such behavior.34 If flehmen does occur in swine, the behavior undoubtedly would be more or less like the gape, or flehmen, response of cats rather than the lip curl of ruminants; therefore, it has possibly escaped observers as being a form of flehmen. The display of flehmen behavior during sexual encounters is sexually dimorphic in that it is seen virtually only in males. Characteristically, the male, after making contact with recently voided urine or the genitalia of a female, elevates his head and curls or lifts his upper lip (Fig. 1). He remains motionless for as short a time as a couple of seconds to as long as 30 seconds or more. Recent experimental evidence from my laboratory has confirmed earlier speculations that flehmen is in fact involved in the transport of samples of urine and vaginal secretions from the oral cavity to the vomeronasal organ. The first direct evidence was from a study on male goats in which a fluorescent dye was placed in the oral cavity just prior to inducing the goats to perform flehmen. The goats were then sacrificed for microscopic examination of the vomeronasal organ, and the dye was found in heavier concentrations in the vomeronasal organ than in control subjects that did not flehmen but had equivalent oral exposure to the dye. 30 A much clearer picture of the relationship between flehmen and vomeronasal organ function was obtained by cannulation of the lumen of the organ, which allowed for repeated sampling of contents in freely moving, conscious animals. 37 Flehmen was evoked after placing urine mixed with a tracer dye in the oral cavity. Contents of the vomeronasal organ were sampled during flehmen as well as after non-flehmen. The concentration of dye was measured by means of a spectrofluorophotometer and was found to be much higher after the occurrence of flehmen than non-flehmen (Fig. 2). The incisive papillae and incisive ducts located just behind the dental pad playa role in the initial movement of fluid from the oral cavity into the nasopalatine ducts. Bulls stroke their tongues against the incisive papilla just prior to flehmen, and these tongue compressions are considered effective in forcing fluid along grooves of the incisive papilla and into the nasopalatine ducts. 23 ,24 At the present time, it is not possible to ascribe a particular role to the lip curl or head elevation during flehmen. Extrapolating from research on other animals, it would appear there is a vascular pumping apparatus surrounding the vomeronasal organ lumen that causes emptying and refilling of the lumen, much as squeezing on a rubber bulb empties and fills a tube. Such a vascular pump, regulated by the autonomic nervous system, has been described for hamsters40 and cats. 10 The vascular morphology surrounding the vomeronasal organ lumen of ruminants is as

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Figure 1. Characteristic head elevation and lip curl posture of Hehmen behavior seen in domestic ruminants. The posture is usually held for 10 to 30 seconds.

extensive as that of rodents and cats, strongly suggesting that a similar pumping mechanism operates during flehmen. It is clear that the stimuli that evoke flehmen are sexually significant odors detected initially by the olfactory system. Olfactory bulbectomy virtually eliminates the display of flehmen behavior in goats. 32 Surgically blocking the naso-palatine ducts and thereby eliminating the oral access to the vomeronasal organ has no effect on the occurrence offlehmen in goats. 32 Persistence of the behavior probably represents a continuation of a species-

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typical behavior in the absence of sensory input, just as olfactory bulbectomized animals continue to sniff and perform close investigation. With regard to oral cavity sampling during flehmen, the question about what is detected and how the information is perceived is problematical because the vomeronasal organ is apparently not required for olfactory discrimination of estrus. Female ungulates communicate to males that they are in estrus by several means, such as holding the tail up, approaching the male, or standing in response to a male's sexual advances. Furthermore, it appears as though virtually all mammalian species, including the farm ungulates, can discriminate estrous from anestrous urine or vaginal secretions by olfaction alone. A major clue in determining the function of flehmen behavior is that males seem to pay more attention to urine from females in diestrus than to urine from females in estrus. In one experiment, for example, goats were exposed in a two-choice test to urine from female goats in diestrus and estrus. Usually subjects approached and sniffed each sample of urine once but returned to perform flehmen preferentially to diestrous urine. 32 Flehmen was also performed for a longer duration toward diestrous urine. These and other observations (reviewed by Hart 16) of preferential investigation and flehmen towards diestrous urine in ruminants suggest that flehmen is involved in a type of chemosensory analysis that is beyond the capability of olfaction. Thus, through the use of the vomeronasal organ, a male may be able to detect small quantities of sex pheromones associated with proestrus when the olfactory system may not be able to distinguish proestrus from diestrus. In terms of guarding or tending a female that will soon come

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into estrus, such detection may be highly advantageous in a situation in which two males are competing. Flehmen performed after copulation may tell a male how much longer a female will remain in estrus on the basis of falling sex pheromone concentration. This information would determine whether or not he continued to tend a female.

Ruminants that Do Not Display Flehmen Given the rather universal occurrence of flehmen behavior among ruminants, it is interesting that there are some antelope species belonging to the tribe alcelaphini that do not display flehmen. These species, which include topi, Coke's hartebeest, the common wildebeest, blesbok, and Hunter's hartebeest, lack the incisive papillae and incisive ducts that constitute the oral access to the vomeronasal organ. Individuals of this unique group of ruminants not only fail to display flehmen behavior in sexual encounters with females but show an overall deemphasis on chemosensory investigation of females. 20 Presumably the vomeronasal system is still functional and is possibly used to monitor sexually relevant or environmental cues dissolved in nasal cavity fluid for regulation of some neuroendocrine processes. Our work on alcelaphine antelopes brings up the point that consideration of vomeronasal organ function in ruminants has largely excluded any vomeronasal organ stimulation aside from that involving flehmen. The nasal connection to the vomeronasal organ orifice is located rostrally in a fashion in which gravity would funnel fluid from the nasal cavity to the organ when the head is lowered. Thus, fluid from the nasal cavity could be sampled through diffusion on a tonic basis during resting or grazing and may not even involve use of the vascular pump. With the background of rodent experiments on the alteration of neuroendocrine events by long-term vomeronasal organ stimulation, one might look for comparable influences in domestic ruminants. One experiment on cattle indicates the kind of neuroregulatory function that would be naturally attributable to the vomeronasal organ. The onset of ovarian activity in heifers can be accelerated by spraying daily a quantity of bull urine into the nasal cavity.22 This is a virtual duplication of the same effect that is described in mice in which odors produced by male mice accelerate female sexual maturation46 and that is eliminated by vomeronasal organ removal. 26 The two types of proposed vomeronasal organ function-that of longterm modulating or priming influences from nasal cavity stimuli and that of short-term proestrus or estrus detection from analysis from oral cavity stimuli during flehmen-are illustrated in Figure 3. As emphasized elsewhere, 16 flehmen can be viewed as a behavioral marker that the vomeronasal system is being utilized much as pronounced sniffing is taken as a marker that an animal is using the olfactory system. However, just as the olfactory system is still used as an environmental monitoring system when sniffing does not occur, the vomeronasal system is probably monitoring certain environmental chemical cues when flehmen is not occurring. Because the latter function may relate to regulation of important neuroendocrine activities, we need to learn more about this function.

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B Figure 3 . Two types of vomeronasal organ stimulation by chemical cues. In A , the vomeronasal organ is proVided long-term exposure to chemostimuli that are dissolved in nasal cavity fluid and that gravitate to the rostral part of nasal cavity for access to vomeronasal organ opening. In 8 , the vomeronasal organ is proVided short-term exposure to fluid-borne chemostimuli from the oral cavity that reach the vomeronasal organ during flehmen . The long-term exposure to chemostimuli may regulate neuroendocrine functions, whereas shortterm exposure to chemostimuli during performance of flehmen is presumably involved in detection of sex phe romones signaling impending estrus of females.

Stimulus, Hormonal and Neural Control of Flehmen Behavior Although female ruminants virtually never display flehmen in heterosexual encounters with males, there are occasions in which they do. For example, female ruminants display flehmen after snifling the urine or genitalia of other cows that are in estrus or proestrus. H . 21 Also, female as well as male goats may be induced to perform flehmen by spraying urine from either male or female goats toward the nasal cavity (Hart, unpublished observations). Thus, the behavior may reflect a dimorphism in the tendency to approach stimuli that evoke flehmen rather than to elicitation of flehmen by stimuli. This notion is supported by observations on domestic cats, which are the other main group of mammals that display flehmen behavior. As in ungulates, only male cats display flehmen during heterosexual encounters. However, the sexual dimorphism is situation-specific. When exploring a urine-marked room without a male cat present, females were found to perform flehmen more than half the time; when urine was applied to the naso-oral surface, flehmen was evoked as reliably in male cats as in female cats. 19 Interestingly, administration of testosterone propionate to

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spayed female cats that were paired with estrogen-treated females markedly increased their tendency to inspect the genitals of a female partner and subsequently perform flehmen. I9 In adult male goats, flehmen behavior is under hormonal control because the behavior is reduced by castration. I8 Female sheep that are artificially androgenized by prenatal injections of testosterone into their dams 6 or female cattle that are naturally androgenized, as in freemartins,I5 have a greater tendency to show flehmen behavior than normal females when injected with testosterone in adulthood. Although flehmen behavior is altered by hormonal manipulation much as male sexual behavior is altered by hormonal manipulation, the neural mediation of flehmen would appear to be quite different. In male goats, flehmen is not reduced by lesions of the medial preoptic-anterior hypothalamic area of the brain, although such lesions produce marked decrements in sexual responses. 17

SUMMARY The chemosensory experiences of farm animals involve a stimulus world that we are incapable of appreciating through our own limited olfactory system and nonexistent vomeronasal system. It is obvious that to domestic ruminants as well as their wild counterparts these systems are an important element in day-to-day activities and in social encounters. As we come to learn more about the role of chemosensory analysis by both the olfactory system and the vomeronasal system, we will eventually have the opportunity to utilize such information more effectively to manage the reproduction, growth, and welfare of our domestic livestock species.

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11. Esslemont RJ, Glencross RG, Bryant MJ, et al: A quantitative study of preovulatory behavior in cattle (British Friesian heifers). Appl Anim Ethol 6:1-17, 1980 12. Estes RD: The role of the vomeronasal organ in mammalian reproduction. Mammalia 36:315-341, 1972 13. Ewbank R, Meese GB: Individual recognition and dominance hierarchy in the domesticated pig. The role of sight. Anim Behav 22:473-480, 1974 14. Graziadei PPC: Functional anatomy of the mammalian chemoreceptor system. In MullerSchwarze D, Mozell MM (eds): Chemical Signals in Vertebrates. New York, Plenum Press, 1977, pp 435-454 15. Greene WA, Mogil L, Foote RH: Behavioral characteristics of freemartins administered estradiol, esterone, testosterone and dihydrotestosterone. Horm Behav 10:71-84, 1978 16. Hart BL: Flehmen behavior and vomeronasal organ function. In Silverstein RM, MullerSchwarze D (eds): Chemical Signals in Vertebrates III. New York, Plenum Press, 1978, pp 87-103 17. Hart BL: Medial preoptic-anterior hypothalamic lesions and sociosexual behavior of male goats. Physiol Behav 36:301-305, 1986 18. Hart BL, Jones TOAC: Effects of castration on sexual behavior of tropical male goats. Horm Behav 6:247-258, 1975 19. Hart BL, Leedy MG: Stimulus and hormonal determinants of £lehman behavior in cats. Horm Behav 21:44-52, 1987 20. Hart BL, Hart LA, Maina IN: Alteration of vomeronasal system anatomy in alcelaphine antelopes (submitted to Nature) 21. Hurnik JF, King GJ, Robertson HA: Estrus and related behaviour in postparturient Holstein cows. Appl Anim Ethol 2:55-68, 1975 22. Izard MK, Vandenbergh JG: The effects of bull urine on puberty and calving dates in crossbred heifers. J Anim Sci 55: 1160-1168, 1982 23. Jacobs VL, Sis RF, Chenoweth pJ, et al: Tongue manipulation of the palate assists estrus detection in the bovine. Theriogenology 13:353-356, 1980 24. Jacobs VL, Sis RF, Chenoweth pJ, et al: Structures of the bovine vomeronasal complex and its relationship to the palate: Tongue manipulation. Acta Anat 110:48-58, 1987 25. Kalmus H: The discrimination by the nose of the dog of individual human odors and in particular the odors of twins. Br J Anim Behav 3:25-31, 1955 26. Kaneko N, Debski EA, Wilson MC, et al: Puberty acceleration in mice. II. Evidence that the vomeronasal organ is a receptor for the primer pheromone in male mouse urine. BioI Reprod 22:873-877, 1980 27. Kiddy CA, Mitchell DS, Bolt DJ, et al: Detection of estrus-related odors in cows by trained dogs. BioI Reprod 19:389-395, 1978 28. Knappe H: Zur Funktion des Jacobsonschen Organs (organon vomeronasale Jacobsoni). Der Zoologische Garten 28:188-194, 1964 29. Kratzing J: The structure of the vomeronasal organ in the sheep. J Anat 108:247-260, 1971 30. Ladewig J, Hart BL: Flehmen and vomeronasal organ function in male goats. Physiol Behav 24:1067-1071, 1980 31. Ladewig J, Hart BL: Demonstration of estrus-related odors in cow urine by operant conditioning of rats. BioI Reprod 24:1165-1169, 1987 32. Ladewig J, Price EO, Hart BL: Flehmen in male goats: Role in sexual behavior. Behav Neurol BioI 30:312-322, 1980 33. MacLeod N, Reinhardt W, Ellendorf F: Olfactory bulb neurons of the pig respond to an identified steroidal pheromone and testosterone. Brain Res 164:323-327, 1979 34. Martys M: Das flehmen der schweine, suidae. (The flehmen behavior of pigs.) Zoo I Anz 199:433-440, 1977 35. McGlone JJ, Curtis SE, Banks EM: Evidence for aggression-modulating pheromones in prepuberal pigs. Behav Neural BioI 47:27-39, 1987 36. Meese GB, Conner DJ, Baldwin BA: Ability of the pig to distinguish between con specific urine samples using olfaction. Physiol Behav 15:121-125, 1975 37. Melese d'Hospital PY, Hart BL: Vomeronasal organ cannulation in male goats: Evidence for transport of fluid from oral cavity to vomeronasal organ during flehmen. Physiol Behav 35:941-944, 1985 38. Melrose DR, Reed HCB, Patterson LS: Androgen steroids associated with boar odour as

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Department of Physiological Sciences School of Veterinary Medicine University of California Davis, California 95616