Social interactions and scent marking in the Mongolian gerbil (Meriones unguiculatus)

Social interactions and scent marking in the Mongolian gerbil (Meriones unguiculatus)

Anim. Behav.,1970, 19, 505-513 SOCIAL INTERACTIONS AND SCENT MARKING IN THE MONGOLIAN GERBIL (MERIONES UNGUICULATUS) BY D. D. THIESSEN, G. LINDZEY, S...

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Anim. Behav.,1970, 19, 505-513

SOCIAL INTERACTIONS AND SCENT MARKING IN THE MONGOLIAN GERBIL (MERIONES UNGUICULATUS) BY D. D. THIESSEN, G. LINDZEY, S. L. BLUM* & P. WALLACE Department of Psychology, University of Texas, Austin, Texas 78712, U.S.A. Abstract. Scent marking is common for many species, and affords olfactory cues for a variety of social reactions. The Mongolian gerbil (Meriones unguiculatus) marks objects with a ventral sebaceous scent gland. In both paired and triplet male encounters, animals marking most frequently generally become dominant. Grouping, however, can have the additional effect of depressing marking and morphological indices of androgen activity. In related studies it was demonstrated that males are attracted to the sebum coming from the scent glands of other males but not to sebum from females. Females show no obvious reference. These studies add support to the notion that gerbil marking has territorial significance and serves recognition functions. The widespread use of chemical communication is suggested by the frequent appearance of scent glands in many species. According to MiillerSchwarze (1967) scent glands have been described in fifteen of the nineteen mammalian orders, and on the basis of location on the body as many as forty different types of glands can be classified. Most species have not been studied sufficiently to conclude that the presence of scent glands automatically indicates that they have behavioural significance. In fact, the early study of scent glands was concerned with the commercial use of civet, musk and castoreum in perfumes. In view of the paucity of experimental data (Ralls 1971) our group has turned toward the gerbil for study. Mongolian gerbils (Meriones unguiculatus) mark objects in their environment with a midventral scent gland. The response is sexually dimorphic, with the male marking about twice as frequently as the female (Thiessen, Blum & Lindsey 1970). Although much is known about the control of the scent gland and the marking response by gonadal hormones (Glenn & Gray 1965; Lindzey, Thiessen & Tucker 1968; Thiessen 1968; Blum 1970; Thiessen & Yahr 1970; Whitsett 1970), there is little information concerning the social significance of the behaviour, or its control by environmental factors. Field studies on other related species, however, suggest that gerbils may be territorial (Kirschshofer 1958). In the Mongolian gerbil, if high marking males are exposed to aggressive interaction in *Present address: Stanford University Medical Center, Stanford, California 94305, U.S.A.

the territory of animals raised there since birth the intruder's marking is significantly inhibited (Nyby, Thiessen & Wallace 1970). The decrement in marking is associated with olfactory cues of the territory and cannot be attributed to visual or auditory cues, stress, or other emotional disturbances. More recently, in a compartmentalized seminatural living situation, we have found that aggressive males will force other males from the field and mark foreign areas much more frequently than their own (Thiessen, Owen & Lindzey 1971). This information strongly suggests that gerbil marking has territorial significance; however, the evidence is not decisive. Scent gland excretions also could be used to aggregate conspecifics, to disperse members of a population, to alarm or arouse groups or individuals, to attract members of the opposite sex, to afford cues for individual and species recognition or to reflect social status. In all probability multiple functions are served depending on the social and environmental context. In this paper we report five studies on social interaction and marking in the Mongolian gerbil. Two studies deal with the relationship between various measures (including marking) and social dominance in males. A third study concerns the effects of laboratory controlled population density on marking and other variables in males. The two final studies investigate the preference of males and females for the gland secretions of other gerbils. In general, the studies indicate that aggression and dominance are related to marking behaviour and that male gerbils, at least, are sensitive to the glandular secretions of other males. The results increase our confidence that scent marking has territorial 505

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significance, and may be related to sexual recognition in the male.

period each gerbil was again assessed for mark, ing behaviour during a 5-min period.

Experiment 1: The Relation Between Dominance and Marking in Paired Encounters Methods Animals and apparatus. Sixty-four male gerbils, raised in all mate groups after weaning, were isolated in cages measuring 10 cm high by 13 cm wide by 25 cm long at the start of the experiment. Marking and other responses were assessed in a grey wooden field 1 m 2 in area, and marked off into sixteen squares of equal size. A 0.16-cm thick sheet of clear Plexiglas covered the floor, and a roughened Plexiglas peg 2-6 cm inlength, 1.2 cm in width, and 0.7 cm in height was positioned at each of the nine lined intersections. Marking was confined almost entirely to the pegs. A 15-W fluorescent tube, positioned 152 cm above the floor of the apparatus, provided the only illumination in the testing room. Encounters between pairs of gerbils occurred in a grey wooden box 61 cm 2 with 20-cm high walls. Eight of these structures were used so that the experimenter could observe eight paired encounters at one time. Hardware cloth covered the compartments during the bouts, and observations were made under fluorescent ceiling lights. Procedure. Following six weeks of isolation gerbils were tested for marking during a 5-min period. A mark consisted of lowering the belly over the peg as it moved in a forward direction. The total number of marks, the number of line crossings, faecal boluses and urine pools were recorded during the 5-min test. The apparatus was cleaned with a 70 per cent ethyl alcohol solution and wiped clean prior to each test. On the day following the marking test, the animals were weighed to the nearest 0.1 g; and the ventral scent glands were exposed by clipping the hair and measured to the nearest millimetre (length • width). Five days later animals were assigned to pairs on a random basis and allowed t o fight for 30 min in the fighting compartments. The animals were identified by clipping a small amount of hair from the back of one of each pair. The pairs were tested for ten consecutive days and were placed back in isolation following each bout. The experimenter assessed the dominance order of each pair without knowledge of the previous behaviour. On the last day of the 10-day

Dominance was determined by a composite score from the ten bouts. As fighting was not always intense or even observable, the criterion for dominance relied on most heavily was the order of chasing. A gerbil that won fights invariably chased the other gerbil. Or, if no fighting was evident, the animal to give chase exhibited threat reactions while the other assumed a submissive posture, such as huddling and closing of the eyes. A gerbil's dominance score was the number of bouts in which it was judged to be dominant and ranged from 0 to 10. For data analysis, the difference in dominance score between pairs was correlated with the difference in marking between the same pair. Thus, pairs of animals that were highly disparate in dominance scores were expected to show equally disparate scores in marking. One or 2 days following the last bout and marking test the animals were killed and the following measures were obtained: body weight, ventral scent gland size, and testis, adrenal, seminal vesicle and spleen weights. Body weight was determined to the nearest 0.1 g and organ weights to the nearest 0-1 mg. Pearsonian coefficients of correlation were used to assess variations between measures.

Results The results can be easily summarized. Initial and terminal marking scores correlated significantly (r=0.77, d f = 2 9 ; P < 0 . 0 1 ) indicating behavioural stability regardless of the intervening fights. The difference in dominance scores between pairs correlated significantly with the difference in initial marking scores between pairs ( r = 3 8 ; P<0.05), but not with the difference in terminal marking scores between pairs (r=0.28). Last, seminal vesicle weight correlated significantly with both initial marking and dominance scores (r=0.43 and 0.38; P<0.05). All other relationships were insignificant. It ~ppears that animals that are frequent markei:s and have high androgen titres, as evidenced by seminal vesicle weight, are also the ones most likely to win bouts. There was no evidence of physiological stress (e.g. changes in body and spleen weight, adrenal weight, and urination) and no significant wounding was evident.

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Experiment 2: The Relation Between Dominance and Marking in Triplet Encounters Methods Animals and apparatus. Eighty male gerbils raised in all male groups from weaning, were isolated in metal cages measuring 10 cm high by 13 cm wide by 25 cm long at 90 days of age. Marking and related measures were recorded in the same apparatus as described in experiment 1, except that the pegs were painted black and were 1.9 cm high. There is no evidence that peg size or colour within limits of these studies affect marking in any major way. Procedure. Following 2 months of isolation twenty matched groups of four gerbils each were formed on the basis of scent gland size (length x width in mm) and body weight (to the nearest 0.1 g). Three of each quartet were placed together in plastic cages measuring 16 x 30 x 38 cm and the fourth placed in a plastic cage measuring 13 x 18 x 30 cm. Unit space per animal was therefore approximately equal. Small patches of hair were clipped from the back of grouped gerbils for the purpose of identification. Triplet and isolated gerbils lived in their respective conditions for 2 weeks. Immediately following the grouping procedure fighting bouts were observed for 30 min, and periodic daily observations were made thereafter. Criteria for dominance were the same as those described for experiment 1. At the end of 2 weeks each animal was tested for 10 min in the marking apparatus and scored for frequency of marking, general activity (line crossings), number of faecal boluses and urine pools. The procedure of testing followed that described earlier. Immediately following the test the animal was killed and the following measures recorded: body weight, sebaceous gland size and spleen, adrenal testis and seminal vesicle weights. Body weight was determined to the nearest 0.1 g and organ weights to the nearest 0.1 mg.

one in four others. Fighting and dominance variations were therefore available for seven groups; however scores from isolated versus grouped conditions were available for all twenty groups. For each variable the scores of the seven dominant animals were compared to submissive animals by means of t-tests for matched samples, after the individual scores of the submissive members of each group had been averaged together. The comparison of groups and isolated animals was handled in a similar way; i.e. individual scores of twenty isolated gerbils were compared with average scores of the grouped animals remaining in each quartet at the end of the study. The comparative results for dominant versus submissive animals and for isolated versus grouped animals are given in Table I. Only significant values are indicated. The use of a one-tailed test of significance on the difference between marking scores for dominant versus submissive animals is justified on the basis of the results of experiment 1. The major associations with dominance were a high marking frequency, a decrease in ventral gland length, and an increase in ventral gland width and a decrease in testis weight. Total gland area, body weight, organ measurements related to stress, and other behavioural indices did not relate to dominance. The most pronounced and significant effects of grouping were decreases in general activity and relative testis weight, and an increase in body weight. Absolute measures of spleen and adrenal weights were significantly elevated i n grouped animals, but these organs did not vary between conditions when corrected for body weight differences. In short, dominance was related to high marking, and grouping was related to low activity, testis weight, and to high body weight. Morphological indices of stress were not evident; however, reduced testis weight suggests a depressed secretion of pituitary gonadotropins.

Results Severe fighting was initially observed in only eight of the twenty group cages. One dominant animal invariably emerged in each cage and no distinction could be made between the remaining submissive animals. Aggression normally continued for several days, and in only two cases did the dominance order appear to reverse itself. In the eight cages in which fighting occurred six deaths were recorded, two in one cage and

Experiment 3: The Effects of Laboratory Controlled Population Density on Marking and Related Variables Methods Animals and apparatus. Sixty male gerbils, raised in all male groups from weaning, and 120 days of age at the beginning of the experiment, were isolated in plastic cages measuring 13 cm high by 16 cm wide by 30 cm long. Marking and associated behaviours were assessed in the

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Table I. Effects of Dominance and Grouping on Marking and Related Measures

Measure

Social condition

~ -t- SE

Marking

Dominant

39.0 •

8.34

frequency (10 rain)

Submissive

17.5 •

5.82

Submissive

Change in

Dominant

--5-00 ~: 1.51

(N=7 Groups dr=6)

gland length (mm)

Submissive

--1-93 ~ 0.70

Change in

Dominant

0.71 q- 0.18

gland width(mm)

Submissive

0.04 ~ 0.20

General

Isolated

317-00 ~ 11-84

activity (10 min)

Grouped

270-30 :t: 8.34

Terminal

Isolated

73.00 -4- 2.93

body weight (g)

Grouped

77.60 -t- 1.45

Testis weight (g

Isolated

1727-70 • 43.65

per 100 g B.W.)

Grouped

1593.30 ~ 17-24

Dominant

t

P

1.94

0.05*

2"67

<0-05

versus

Isolated versus Grouped (N=20 Groups dr= 19)

3.36

0.02

2-88

<0.01

2.21

<0-05

3.23

<0.01

*One-tailed test. same apparatus as described in experiment 1 except that the marking pegs were dome-shaped and painted black. Procedure. Seven days following isolation, the sixty gerbils were randomly assigned to three living conditions and housed in cages measuring 16 x 30 • 38 cm; twenty remained isolated; twenty were placed in four groups of five each; and twenty were placed in two groups of ten each. Immediately following this procedure, groups were observed for fighting for 30 min. Daily observations were made thereafter. Eight days after differential housing each animal was tested for marking, general activity faecal boluses, and number of urine pools during a 5-min period. On the following day the animals were sacrificed and the following measures recorded: body weight, number of wounds, sebaceous gland size in millimetres (length x width) and spleen, adrenal, seminal vesicle and testis weights. Body weight was determined to the nearest 0.1 g and organ weights to the nearest 0.1 mg. Results were evaluated using analyses of variance and t-tests for independent samples. Results

While some fighting was observed in grouped cages immediately following formation of the

groups, it was neither prolonged nor severe enough to cause wounding. Groups 5 and 10 did not differ in fighting activity. Table II summarizes the significant variations due to the grouping procedure. When compared to isolated animals, grouped animals showed decreases in marking, deposition o f urine pools, and relative seminal vesicle weight. General activity was elevated. Body weight, defecation, ventral gland size, spleen weight and adrenal weight were not altered by density. Absolute testis weight was significantly depressed by grouping (not shown in Table II) but showed little variation when a correction for body weight differences was made. Experiment 4: Olfactory Responsiveness of Males and Females to Glandular Sebum Methods Animals and apparatus. Thirty males and thirty

females served as subjects for this experiment. They were raised in bisexual groups until 55 days of age and isolated thereafter in plastic cage~ measuring 13 cm high by 18 cm wide by 30 cm long. Testing began at 114 days of age. The same subjects were used to obtain ventral gland sebum during the course of the experiment. The oestrous state of the female subjects and the female stimulus animals was allowed to vary randomly for this experiment.

THIESSEN ET AL. : SOCIAL INTERACTIONS IN GERBILS

PLATE

XIV

Fig. 1. Olfactory test apparatus

Thiessen et al., Anim. Behav., 19, 3

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509

Table H. Effects of Population Density on Marking and Related Measures

Measure

Social conditions

R 4- sE

F (df=2 and 57)

Results of t-tests (df=38)

Marking frequency (5 min)

Isolated (1) Group (5) Group (10)

16-95 4- 3.53 9.90 4- 1.63 6"55 4- 1"74

4.66*

1>10"

General activity (5 min)

Isolated (1) Group (5) Group (10)

139.00 • 5.69 158.45 -4- 5.64 162.70 4- 6.49

4.51"

1
No. of urine pools (5 min)

Isolated (1) Group (5) Group (10)

1.00 4- 0.16 0.40 4- 0.11 0.50 4- 0.11

5"95t

1>5" 1>10"

Seminal vesicle weight (g per 100 g body weight)

Isolated (1) Group (5) Group (10)

529.60 4- 12-22 496.15 4- 16-85 464.95 4- 15.35

4.69*

I >0"

*P<0.05;

tP<0.01.

The apparatus is shown in Plate XIV, Fig. 1. It consists of a Plexiglas Y-tube with equal length arms of 39 cm and an inside diameter of 7 cm. The start box and goal boxes (indicated as A and B) measure 13 cm high by 16 cm wide by 27 cm long. Behind each goal box is a retaining box for stimulus animals, and in front of the start box is a variable speed fan. The fan can be used to draw air through the retaining and goal boxes back to the choice point and start box. For this experiment and experiment 3 the fan unit and the restraining boxes were removed. Filter paper strips impregnated with sebum or control material from skin areas adjacent to the ventral gland were attached outside a double-screen barrier at the end of each goal box. The fan was not used as it seemed to disturb the gerbils. Procedure. The thirty males and thirty females were individually given choices in the Y-tube. Both sexes were presented with choices between (1) male and female sebum, (2) male sebum and no sebum (skin smear), and (3) female sebum and no sebum. Every gerbil was used in each condition in a counter-balanced design. Several days were required to complete the schedule, but no animal received more than one trial a day. Smears were obtained by clipping the hair around the ventral gland and rubbing a piece o f filter paper, measuring approximately 1.5 • 2.5 cm, ten to fifteen times across the length o f the gland, or in the case of tile control smears, rubbing an adjacent skin area. Each animal was employed as a stimulus animal four times during the study, with the restriction that no animal

was used within 2 days of being tested for odour preference. Each subject was adapted for 30 min to the apparatus with free access to every area. At the end of this period the appropriate smears were taped on the ends of the goal boxes and a 15rain preference test begun. Tests were begun within 5 min of sebum being removed from the stimulus animal. The amount of time spent in each of the two goal boxes was recorded. At the end of the 15-rain period the animal was trapped in the start box by means of a guillotine door. The adaptation and test periods were conducted under red light (25 W) to which the gerbil is apparently insensitive and during the middle light part of a 12-hr light-dark cycle. The smears were positioned on the two sides in a random order, and the apparatus was dismantled, cleaned with a 95 per cent ethanol-alcohol solution, rinsed and dried, after each animal was tested. Results Table III indicates that only male gerbils show a preferential reaction to sebum and then only to sebum coming from other males. It is perhaps important however, that the preference for male sebum disappears when the alternative is female sebum. Apparently the male does react to the remale odour to some degree. Experiment 5: Olfactory Responsiveness of Males to Male Glandular Sebum Methods Animals and apparatus. Twenty-two males, raised in all male groups from weaning, were used as subjects for this experiment: A t l 2 0 days

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Table HI. Olfactory Responsiveness of Males and Females to Glandular Sebum

Mean time spent investigating olfactory stimuli (rain)

Subject Male

Female

Male sebum

2.73 4- 0.39

Blank smear

1.25 4- 0.14

Female sebum

2-63 4- 0.28

Blank smear

2.29 4- 0-22

Male sebum

2.30 4- 0.26

Female sebum

2.53 4- 0.32

Male sebum

2.00 4- 0.18

Blank smear

1-89 4- 0-19

Female sebum

2-12 4- 0.31

Black smear

1.67 4- 0-19

Male sebum

2.02 4- 0.20

Female sebum

2-45 4- 0-31

of age they were isolated in plastic cages measuring 13 x 18 • 30 cm, Separate adult male donors were used to obtain sebum or control skin smears. The Y-tube apparatus was the one described in experiment 4. P r o c e d u r e . Initial tests were begun at 190 days of age with a fan drawing the air through the Y-tube. However the fan disturbed the animals enough so that it was discontinued; and the animals were run for a second time as described in the previous experiment. Smears were obtained either from the ventral gland of adult males or from the same area of animals whose gland had been previously excised (Blum 1970). Otherwise the procedure was identical to that described in experiment 4. Results

Males spent significantly more time in the goal box adjacent to the sebum smear than in the goal box associated with the skin smear (t=3.87; d f = 2 1 ; P<0.001).. The respective means and standard errors m minutes are 2-16-+-0.23 and 1.26 4-0.18. Clearly, the male preference for male sebum seen in the previous experiment is also evident here. Discussion

The five studies strengthen the view that the ventral gland and the associated marking be-

t (dr=29)

P

3-44

<0.01

1.26

NS

0-48

NS

0-44

NS

1-28

NS

1.69

NS

haviour of the male Mongolian gerbil both affect and are affected by the social life of these animals. Experiment 1 indicated a significant and positive correlation between marking frequency and subsequent dominance order in pairs. No stress effects of fighting or dominance position were evident, as measured by body weight or spleen and adrenal weights. Seminal vesicle weight did correlate significantly with marking and with dominance. Thus our results support earlier evidence that androgen titer and marking are positively correlated (Blum 1970; Lindzey et al. 1968; Thiessen, Friend & Lindzey 1968), and they moreover suggest a positive correlation between androgen titre and aggression, also reported by Saylor (1970). Experiment 2, conducted on triplet groups and comparing their responses to isolated animals, verified the association of dominance with high marking and indicated that grouping was associated with higher body weight, and lower activity and testis weight. There was a suggestion in this experiment that gland length and width are associated with dominance (Table I), although the overall size (length • width) showed no consistent variation. The traditional organ measures o f stress did not show a dominance or grouping effect. Experiment 3 showed that density, particularly that of ten per cage, lowered marking, the deposition of urine pools,

THIESSEN ET AL.: SOCIAL INTERACTIONS IN GERBILS and seminal vesicle weight. In contrast to the grouping effects of experiment 2, general activity was elevated. Number of animals per cage, density per unit volume or unknown variables could have contributed to this discrepancy. Once more high markers had the higher seminal vesicle weight and no indices of stress emerged. The control of both aggression and marking by a single hormonal system is consistent with the view that marking has territorial significance, since both types of behaviour could obviously be important in territorial defence. Presumably, animals are high in marking and aggression because of elevated levels of circulating androgen, and it is this that leads to dominance, not the reverse. On the other hand, increasing population density appears to reduce androgen secretion, as evidenced by reduced testis weight in experiment 2 and depressed seminal vesicle weight in experiment 3. Marking is accordingly depressed. As no obvious stress effects existed under any social condition, it would appear that the link between marking, aggression and androgen status is direct and not mediated by indirect hormone influences from the adrenals. Experiments 4 and 5 established that the male gravitates toward scent gland secretions of other males but not those of females in a Y-tube choice situation. The secretions of the females may differ from the males both qualitatively and quantitatively. In most cases the scent gland of the female is only about half as big as that of the male. The absence of a preference does not, of course, signify that there is no ability to discriminate between the odours in the two arms of the apparatus. It is probably quite significant that males are most responsive to male sebum odours, as it may be that males carry the greatest burden for territorial defence and acquisition. The task of assessing territorial behaviour in the laboratory is difficult. Our general procedure is to observe marking frequency during a 5 or 10-rain exposure to an open field studded withplastic pegs. It is debatable if this brief exposure to a novel area should be considered territorial. However, we do note relations expected of territorial expression (see above), and, in any case, there are obvious advantages in simplifying our initial social studies. We are extending the diversity and times of observations (Nyby et al. 1970) and find little to contradict our original findings. At most, the newer findings give greater emphasis to the social stimulation of marking and more clearly implicate the importance of social status. The open-field tech-

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nique, nevertheless, has proved to be quite adequate in establishing individual and sex differences and in assessing hormonal and neurological correlates. Each type of situation has its unique advantages. Most recently our group is assessing the social behaviour of the Mongolian gerbil in plots of land provided to us by Dr Frank Blair of the Department of Zoology. It is hoped that the combined laboratory and field investigations will give a realistic picture of the mechanisms and functions of territorial marking in this fascinating species. Ultimately several criteria must be met before it can be definitively said that a scent gland has evolutionary, behavioural and social significance. In ascending order of significance it would seem that the following criteria must be established: (1) First the gland should appear well organized and interfaced with the substratum that the animal usually contacts. Thus, glands on the sides, flanks and dorsal surface occur in a number of small rodents that either inhabit burrows or use runways through thick vegetation (Ewer 1968). Among species that commonly sunbathe (e.g. Heteromyid) or depress their anal-genital area against the substrate because of any irritation (e.g. Carnivora and many rodents) anal gland smearing, vaginal secretions or cloaca rubbing are common (Gleason & Reynierse 1969). In aboreal marsupials (e.g. koala and phalangers) and New World Primates (e.g. marmosets and tree shrews) that contact tree branches while climb, ing, sternal scent glands are often evident. (2) For proficient use a scent gland must be innervated in such a way that secretion is readily available and can be easily applied. This means that reservoirs of sebum should be present or that synthesis is rapid. Moreover, the external ducts must allow openings to the environment that match the manner in which the substratum is approached. For example, the hairs protruding from the ventral gland of the Mongolian gerbil are grooved and orient toward the rear to provide the best possible deposition of sebum as the animal moves forward over an object. (3) Sexual dimorphism and seasonal variation should be evident in scent glands related to reproduction, implying that hormone innervation is essential. (4) To be most effective a scent gland should be stimulated by internal or external events most closely related to significant social behaviours. Evidence here is almost entirely lacking, with

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the obvious exception that the hormone status is of critical importance. (5) A scent gland is likely to have signalling function if a correspondence exists between the chemical nature of the secretion and the development of the receptor system. This criterion is one of the most difficult to establish. At the most basic level it is expected that only macrosmatie animals would possess scent glands, and that the olfactory material would be volatile and easily captured by the olfactory epithelium. (6) Scent glands will generally have signalling qualities when other sensory systems are depressed or otherwise nonfunctional. Similarly, chemical communication will be enhanced when it is integrated with other modes of communication. Thus it is expected that olfactory signaling will predominate in: (a) nocturnal species that cannot rely on visual displays, (b) species that live in thick foliage where visual displays are likely to be obscured, (c) species that are terrestrial and whose vision or audition are obscured by terrain features, (d) species with short home ranges where olfactory material can provide reliable signposts, and (e) desert species that must conserve body water and hence cannot rely on desiccating responses of urination, defecation or salivation for object marking. In short, scent glands a n d marking must show ecological adaptiveness. (7) Last, and most significant, scent marking is generally more evident in gregarious species and has obvious relations to sexual fitness and gene transmission. Pfeiffer (1962), for instance, finds that the most extensive use of pheromones occurs in fish with complex social behaviours. Young (1950) points out a similar distinction between the social frogs, Bufo, and t h e semisocial groups, Rana. Likewise, scent marking by chinning in the swamp rabbit, Sylvilagus aquaticus, is much more evident than in the cotton-tail rabbit, Sylvilagus floridanus (Marsden & Holler 1964). The former species is highly territorial and possesses a large chin gland, while the latter species is never observed to defend a territory and has a small chin gland. Obviously no single criterion or set of criteria can predict the appearance and use of scent glands for communication. Both dirurnal and nocturnal species have marking glands as do aboreal, semi-aboreal and terrestrial mammals. Glands are neither restricted to desert forms nor are they absolutely linked to burrowing animals. Finally, phylogenetic status is not, i n and of itself, a criterion for scent gland use. The effee-

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tive use of glands can occur in any species, genus, family or order. More important is the type of ecology faced by the organism and how well scent marking acts as a signalling system relative to other systems that might have developed. Acknowledgments This investigation was supported by Grant M H 14076-04, and Research Scientist Development Award M H 11, 174-04 to D. D. Thiessen from the National Institutes of Mental Health, and by Biomedical Sciences Support Grant FR, 07091-05 from the General Research Support Branch, Division of Research Resources, Bureau of Health Professions Education and Manpower Training, National Institutes of Health. REFERENCES Blum, S. L. (1970). The androgen coptrol of scent marking in the Mongolian gerbil (Meriones unguiculatus). Doctoral dissertation, University of Texas, Austin, Texas, University Microfilms. Ewer, R. F. (1968). Ethology of Mammals. New York: Plenum Press. Gleason, K. K. & Reynierse, J. H. (1969). The behavioural significance of pheromones in vertebrates. PsychoL Bull., 71, 58-73. Glenn, E. M. & Gray, J. (1965). Efect of various hormones on the growth and histology of the gerbil (Meriones unguiculatus) abdominal sebaceous gland pad. Endrocrinology, 76, 1115-1123. Kirchshofer, R. (1958). Freiland-und Gefangenschaftsbeobachtungen an der nordafrikanischen Rennmaus Gerbillus nanus garamantis. Siiugetierkunde, 23, 33-39. Lindzey, G., Thiessen, D. D. & Tucker, A. (1968). Development and hormonal control of territorial marking in the male Mongolian gerbil (Meriones unguiculatus). Develop. PsychobioL, 1, 97-99. Marsden, H. M. & Holler, N. R. (1964). Social behaviour in confined populations of the cottontail and the swamp rabbit. Wildlife Monogr., 13. Mtil!er-Schwarze,D. (1967). Social odors in young mule deer. Am. ZooL, 7, 430. Nyby, J., Thiessen, D. D. & Wallace, P. (1970). Social inhibition of territorial marking in the Mongolian gerbil (Meriones unguiculatus). Psychon. Sci., 21r 310-312. Pfeiffer, W. (1962). The fright reaction of fish. Biol. Rev., 37, 495-511. Rails, K. (1971). Mammalian scent marking. Science, N.Y., 171, 443--449. Saylor, A: (1970). The effect of anti-androgens on aggressive behavior in the gergil. Physiol. Behav., 5, 667-671. Thiessen, D. D. (1968). The roots of territorial marking in the Mongolian gerbil: A problem of speciescommon topography. Behav., Res. Meth. & Instrum., 1, 70-76. Thiessen, D, D., Blum, S. L. & Lindzey, G. (1970). A scent marking response associated with the ventral sebaceous gland of the Mongolian gerbil (Meriones unguiculatus). Anim. Behav., 18, 26-30.

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(Received 15 April 1970; revised 15 December 1970; second revision 23 March 1971 ; MS. number: A983).