- Email: [email protected]
A mechanism for individual recognition by odour in Herpestes auropunctatus (Carnivora: Viverridae)
Anita. Behav., 1976, 24, 141-145 A M E C H A N I S M F O R I N D I V I D U A L R E C O G N I T I O N BY O D O U R I N HERPESTES A UROPUNCTATUS (CARNIVORA: VIVERRIDAE) BY MARTYN L. G O R M A N Department of Zoology, University of Aberdeen, Aberdeen. Abstract. The anal pockets of Herpestes auropunctatus are used in marking and give a distinctive odour to the animal. The contents of the pocket include six, short-chain, odorous carboxylic acids; these are produced from sebum and apocrine secretions by bacterial action. The relative concentrations of the six acids vary from one individual to another, giving each a different odour. Mongooses can discriminate between the anal pocket contents of conspecifics and also between synthetic odours made from pure acids. on a vortex mixer. The resultant mixture was centrifuged and the ether layer withdrawn. The extracted secretion was then acidified with dilute hydrochloric acid to pH 1 and re-extracted with ether as above. The ether extracts were examined by gasliquid chromatography using a dual glass column Pye-Unicam 104 chromatograph with flame ionization detectors. Analyses were made at 140~ with nitrogen as carrier gas at 30 ml per minute, on a 1.8 m • 6 mm O.D. (outside diameter) column packed with Carbowax 20Mterphthalic acid on AW-DCMS chromosorb G 80-100 mesh (5:95).
In common with a wide variety of carnivores, the small Indian mongoose Herpestes auropunetatus has a pair of anal pockets (Pocock 1916) which open one to each side of the anus. The material within the pockets imparts a powerful odour to the animal and is also deposited on prominent objects, such as stones and trees, within the animal's home range. An analysis of the contents of the pockets (Gorman, Nedwell & Smith 1974) has shown that they include a series of volatile, shortchain, carboxytic acids; namely acetic, propionic, n-butyric, iso-butyric, n-valeric and iso-valeric acids, all of which are the products of bacterial breakdown of sebum and apocrine secretion deposited within the pocket. The six acids, each of which has a unique odour, occur at different relative concentrations in individual mongooses, thus imparting a distinctive and probably unique odour to each. It has been suggested (Gorman et al. 1974) that such a situation could allow for individual recognition by scent, each mongoose having a different odour based on a unique combination of these six carboxylic acids. The present paper verifies that individuals have different carboxylic acid profiles and demonstrates that mongooses can indeed recognize each other, as individuals, on the basis of the odour of their anal pockets.
Behavioural In order to demonstrate that mongooses could recognize each other as individuals, on the basis of anal pocket odours, four, hand-reared animals were used in choice experiments similar to those described by Rasa (1973), and to those employed in domestic-dog obedience trials. Anal pocket contents from seven different mongooses were applied to a series of glass slides; the tame mongooses were trained to select from this series that slide which had the same odour as a glass slide which they were allowed to sniff. During training, sniffing of the correct slide, by the tame mongoose, was rewarded by saying 'Yes' and the offering of an earthworm, for which the mongoose had to return to the observer. After about 100 trials the tame mongooses would consistently choose the correct slide and return to the trainer for reward before 'Yes' was uttered, or the earthworm offered. At this point they were considered to be fully trained. During the experimental trials, which were carried out with the observer unaware of the identity of the samples, the anal pocket contents
Methods Chemical The anal pocket contents of twenty-four individuals, caught on the island of Viti Levu (18 ~ S. 180 ~ W.), were subjected to chemical analysis. The secretion was expressed by external pressure on the anal pocket, and collected in a Teflon-capped vial. The secretion was extracted with Analar diethyl ether by means of agitation 141
ANIMAL
142
BEHAVIOUR,
of seven new individuals ( A - G ) were used; fresh secretion was obtained from each at the beginning of each set of trials. N o vocal cue of correctness was given a n d the a n i m a l ' s choice of slide was t a k e n as the last one to be sniffed before r e t u r n i n g to the observer for reward. Correct choices were rewarded, incorrect ones were not. I n a subsequent set of trials, anal pocket secretions were replaced by synthetic odours, p r o d u c e d by mixing pure acids in water. These mixtures were designed to simulate the relative a n d absolute concentrations of acids f o u n d in real secretions (Table I). The ability of mongooses to differentiate between these mixtures was tested in the way described above. Results Composition
The Chemical of Anal Pocket Secretions The analyses confirmed the presence of acetic, propionic, n-butyric, iso-butyric, n-valeric a n d iso-valeric acids in the anal pockets. The relative concentrations of these, i n the twentyfour animals studied, are shown i n Table II. It is clear that different individuals have different acid profiles a n d thus that they have different odours. T h e length of time for which a n individual's profile remains c o n s t a n t is, as yet, unclear. The Ability to Discriminate Anal Pocket Secretions and Synthetic Odours The results from the choice experiments using the four trained mongooses, a n d the anal pocket contents of animals A - G , are shown in Tables I I I to VI.
Table I. The Chemical Composition of the Synthetic Odours Used in Choice Experiments Concentration (mM) of carboxylic acids Synthetic Pro.pio- isonisonmixture Acetic mc Butyric Butyric Valeric Valeric
24,
1
T h e results show clearly that mongooses are able to distinguish between the anal pocket secretions of different individuals; i n the great majority of cases the trained animals were able to choose f r o m the series presented, the odour which they had been allowed to sniff. Table H. The Carboxylic Acid Profiles of Twenty-Four Mongooses. The Concentrations are in Relative Molarities with the Most Concentrated Acid Equal to 100 Relative concentration of carboxylic acids: No. Sex Acetic
Propio- isonisonnic Butyric Butyric Valeric Valeric
1
M
100
25
9
8
15
1
2
M
100
38
21
15
17
5
3
M
95
100
15
i1
7
9
4
M
100
20
16
30
35
8
5
M
70
100
6
28
25
2
6
M
100
21
17
38
4
16
7
M
100
16
28
11
7
1
8
M
100
18
13
10
18
16
9
M
100
98
4
6
15
4
10
M
100
15
41
4
13
9
11
M
100
46
4
18
9
18
12
M
51
100
68
15
4
10
13
M
75
100
14
100
18
4
14
M
100
15
17
63
4
8
15
M
100
28
10
7
3
1
16
F
100
31
15
1
4
1
17
F
100
15
19
0
16
0
18
F
100
14
28
16
38
4
19
F
I00
80
14
11
0
10
20
F
100
30
14
21
0
18
21
F
100
60
1
30
1
I
22
F
100
30
41
15
11
10
23
F
100
6
4
13
21
3
24
F
100
68
40
0
4
10
rio. :
1
30
20
10
10
5
5
2
30
0
10
5
30
10
3
30
10
30
20
5
10
4
10
30
10
20
10
5
G O R M A N : MECHANISM FOR I N D I V I D U A L RECOGNITION BY O D O U R
143
Table III. The Performance of tile Trained Mongoose Laisa in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Table V. The Performance of the Trained Mongoose Sid in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Sample presented
A
Sample presented
A
A
48
1
A
23
0
Sample chosen (no. of occasions) B
C
0
D
0
E
F
G
1
7
0
Sample chosen (No. of occasions) B
C
D
E
F
G
0
0
1
1
1
B
0
6
0
0
0
0
0
B
0
7
0
0
0
0
0
C
7
0
24
0
1
1
0
C
0
1
19
6
7
1
1
D
0
0
0
19
1
0
3
D
0
0
0
18
0
0
0
E
0
0
0
3
16
0
1
E
0
0
7
4
28
0
0
F
0
1
3
I
2
17
0
F
0
0
1
4
0
20
0
G
0
0
1
4
0
1
15
G
0
0
0
0
0
0
11
Table IV. The Performance of the Trained Mongoose Fred in Discriminating Between the Anal Pocket Contents of Mongooses A - G Sample presented
A
A
16
0
0
0
0
0
B
0
11
0
0
0
C
0
0
17
0
D
0
0
0
E
0
0
F
0
G
0
Table VI. The Performance of the Trained Mongoose Tavita in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Sample chosen (no. of occasions)
1
Sample presented
A
0
0
A
11
1
0
0
0
1
1
0
1
3
B
0
17
0
1
3
4
1
28
0
1
4
C
0
1
9
0
0
0
1
4
0
16
0
0
D
0
0
0
14
0
0
0
0
0
0
1
28
0
E
0
1
5
4
17
0
0
1
1
3
0
0
17
F
0
0
0
0
1
6
0
G
0
0
0
0
1
1
19
B
C
D
E
F
G
T h e results f r o m t h e c h o i c e e x p e r i m e n t s i n v o l v i n g s y n t h e t i c o d o u r s are s h o w n in T a b l e VII. Since t h e p r e v i o u s e x p e r i m e n t s h o w e d t h a t all f o u r m o n g o o s e s c o u l d effectively d i s c r i m i n a t e b e t w e e n different o d o u r s , the d a t a f r o m t h e f o u r a n i m a l s are c o m b i n e d in T a b l e V I I . T h e results i n d i c a t e t h a t m o n g o o s e s c a n distinguish b e t w e e n s y n t h e t i c m i x t u r e s o f c a r b o x ylic acids j u s t as effectively as they c a n b e t w e e n a n a l p o c k e t secretions. Discussion It is well e s t a b l i s h e d t h a t a v a r i e t y o f m a m m a l species c a n r e c o g n i z e conspecifics, as i n d i v i d u a l s , o n t h e basis o f their o d o u r ; f o r e x a m p l e b l a c k tailed d e e r Odocoileus hemionus (MtillerS c h w a r z e 1971), m i c e Mus musculus ( B o w e r s &
Sample chosen (No. of occasions) B
C
D
E
F
G
Table VII. The Performances of the Four Mongooses Discriminating Between Synthetic Mixtures of Carboxylic Acids
Mixture chosen: total No. of choices by all four trained mongooses Mixture presented
1
2
3
4
1
25
2
2
0
2
2
12
0
0
3
1
0
41
1
4
3
0
0
19
144
ANIMAL
BEHAVIOUR,
Alexander 1967), rats Rattus norvegicus (Krames 1970), gerbils Meriones unguiculatus (Halpin 1974) and the African dwarf mongoose Helogale undulata (Rasa 1973). This final species is of interest in that marks made by the anal glands can be distinguished by conspecifics. The present paper shows that H. auropunctatus also, cart recognize conspecifics as individuals using olfactory cues from the secretions of the anal pockets. It is suggested that this ability is based upon the fact that each animal has a different, and probably unique, combination of concentrations of six odorous organic acids within its anal pockets. It has previously been established that these acids are the products of bacterial metabolism of sebum and apocrine secretions (Gorman et al. 1974). The behavioural work reported here shows that this mongoose can also effectively discriminate between synthetic mixtures of pure acids, suggesting that these acid profiles form the basis for olfactory discrimination of anal pocket secretions from different individuals. The question still remains as to why each individual has a different odour. Gorman et al. (1974) have shown that the substrate presented to the bacteria in the anal pocket is a complex mixture of sebum and apocrine secretions. It is possible that each animal produces a chemically unique substrate, which when metabolized by bacteria produces a unique combination of carboxylic acids. It is more likely, however, that all individuals produce chemically similar substrates and that differences in carboxylic acid profiles are due to differences in the symbiotic microfloras. Gorman et al. (1974) identified at least four species of bacteria within the anal pocket, each producing different combinations of carboxylic acids. Clearly, if individual mongooses have different bacterial populations they will also have different acid profiles and consequently different odours. Rasa (1973) found that her dwarf mongooses could distinguish between anal secretions of different ages, as well as between secretions from different individuals. She suggested that a chemical change must take place when the secretion was exposed to air. The present findings suggest what changes may occur. The six acids found in the anal pocket of 1t. auropunctatus vary greatly in volatility, from n-valeric acid with a boiling point of 186 ~ C to acetic acid with a boiling point of 118~ Clearly, as a deposited secretion ages, its chemical composition will change as the more volatile constituents evaporate
24,
1
at a proportionally higher rate than the less volatile ones. Consequently, a mark may contain not only the information as to which mongoose deposited it, but also its age. Problems will dearly arise if the ageing mark, during its chemical changes, comes to resemble the mark of some other individual. Prehaps this is not a serious problem in a species such as H. auropunctatus which is largely sedentary and in contact with relatively few conspecifics and their marks. Finally, it is of interest to speculate on the evolution of such a system. Sebum, and to a much lesser extent apocrine secretion, is generally deposited on the pelage of mammals where it is thought to have a water-proofing function. The normal skin microflora will metabolize these materials producing small quantities of short-chain carboxylic acids, and imparting a faint smell to the animal, In a variety of species this smell appears to have become involved in a communicating function; under selection the sebaceous and apocrine glands have become concentrated into discrete organs producing quantities of secretion containing, amongst other substances, carboxylic acids. Thus we find that carboxylic acids form a part of the scents of many mammals; they have been detected in the anal pockets of the red fox Vulpes vulpes (Albone & Fox 1971), of the lion Panthera leo (Albone et al. 1974) and of the weasel Mustela nivalis (Gorman unpublished data); they occur in the vagina of the rhesus monkey Macaca mulatta (Curtis et al. 1971) where they serve to attract the male; in the human vagina, particularly around the time of ovulation (Michael, Bonsall & Warner 1974); in the human axilla (Shelley, Harley & Nicholls 1953); in the guineapig Cavia porcellus perineaI gland (Beriiter, Beauchamp & Muetterties 1974); in the subauricular gland of the male prong-horn Antilocapra americana (Miiller-Schwarze et al1974). The involvement of bacteria in the production of these acids has been implicated for the red fox (Albone et al. 1974), for the rhesus monkey (Michael et al. 1972), for the human axilla (Shelley et al. 1953) and for the guinea-pig (Gorman unpublished observations). It is likely that future work will show their involvement in other species also.
Acknowledgments I am grateful to the Leverhulme Trust for financial support, to Waisake Volau for his
GORMAN: MECHANISM FOR INDIVIDUAL RECOGNITION BY ODOUR assistance i n Fiji, and to D r P. Boyle a n d D r C. H. F r y for their criticisms of this manuscript. REFERENCES
Albone, E. S. & Fox, M. W. (1971). Anal gland secretion of the red fox. Nature, Lond., 233, 569-570. Albone, E. S., Eglinton, G., Walker, G. M. & Ware, G. C. (1974). The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sciences, 14, 387-400. Bertiter, J., Beauchamp, G. K. & Muetterties, E. L. (1974). Mammalian chemical communication: perineal gland secretion of the guinea pig. PhysioL Zool., 47, 130-136. Bowers, J. M. & Alexander, B. K. (1967). Mice: individual recognition by olfactory cues. Science, 158, 1208-1210. Curtis, R. F., BaUantine, J. A., Keverne, E. B., Bonsall, R. W. & Michael, R. P. (t971). Identification of primate sex pheromones and the properties of synthetic attractants. Nature, Lond., 232, 396-398. Gorman, M. L., Nedwell, D. B. & Smith, R. M. (1974). An analysis of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J. Zool. Lond., 172, 389-399. Halpin, Z. T. (1974). Individual differences in the biological odours of the mongolian gerbil (Meriones unguiculatus). Behav. Biol., 11, 253-259.
145
Krames, L. (1970). Responses of female rats to the individual body odours of male rats. Psychon. Sci. Sect. Anim. Physiol. Psychol., 20,274--275. Michael, R. D., Zumpe, D., Keverne, E. B. & Bonsall, R. W. (1972). Neuro-endocrine factors in the control of primate behaviour. Recent Progr. Horm. Res., 28, 665-706. Michael, R. D., Bonsall, R. W., & Warner, D. (1974). Human vaginal secretions: Volatile fatty acid content. Science, 186, 1217-1219. Mtiller-Schwarze, D. (1971). Pheromones in black-tailed deer (Odocoiles hemionus columbianus). Anim. Behav., 19, 141-152. Mtiller-Schwarze, D., Mtiller-Schwarze, C., Singer, A. G. & Silverstein, R. M. (1974). Mammalian pheromone: identification of active component in sub-auricular scent of the male pronghorn. Science, 183, 860-862. Pocock, R. I. (1916). On the external characters of the mongoose (Mungotidae). Proc. zool. soc., Lond., 1916, 349-374. Rasa, A. E. (1973). Marking behaviour and its social significance i n the African dwarf mongoose Helogale undulata rufula. Z. Tierpsychol., 32, 293-318. Shelley, W. B., Harley, H. J. & Nicholls, A. C. (1953). Axillary odour: an experimental study of the role of bacteria, apocrine sweat and deodorants. Arch. DermatoL Syph. N.Y., 68, 430--446.
(Received 28 April 1975; MS. number: 1423)
In common with a wide variety of carnivores, the small Indian mongoose Herpestes auropunetatus has a pair of anal pockets (Pocock 1916) which open one to each side of the anus. The material within the pockets imparts a powerful odour to the animal and is also deposited on prominent objects, such as stones and trees, within the animal's home range. An analysis of the contents of the pockets (Gorman, Nedwell & Smith 1974) has shown that they include a series of volatile, shortchain, carboxytic acids; namely acetic, propionic, n-butyric, iso-butyric, n-valeric and iso-valeric acids, all of which are the products of bacterial breakdown of sebum and apocrine secretion deposited within the pocket. The six acids, each of which has a unique odour, occur at different relative concentrations in individual mongooses, thus imparting a distinctive and probably unique odour to each. It has been suggested (Gorman et al. 1974) that such a situation could allow for individual recognition by scent, each mongoose having a different odour based on a unique combination of these six carboxylic acids. The present paper verifies that individuals have different carboxylic acid profiles and demonstrates that mongooses can indeed recognize each other, as individuals, on the basis of the odour of their anal pockets.
Behavioural In order to demonstrate that mongooses could recognize each other as individuals, on the basis of anal pocket odours, four, hand-reared animals were used in choice experiments similar to those described by Rasa (1973), and to those employed in domestic-dog obedience trials. Anal pocket contents from seven different mongooses were applied to a series of glass slides; the tame mongooses were trained to select from this series that slide which had the same odour as a glass slide which they were allowed to sniff. During training, sniffing of the correct slide, by the tame mongoose, was rewarded by saying 'Yes' and the offering of an earthworm, for which the mongoose had to return to the observer. After about 100 trials the tame mongooses would consistently choose the correct slide and return to the trainer for reward before 'Yes' was uttered, or the earthworm offered. At this point they were considered to be fully trained. During the experimental trials, which were carried out with the observer unaware of the identity of the samples, the anal pocket contents
Methods Chemical The anal pocket contents of twenty-four individuals, caught on the island of Viti Levu (18 ~ S. 180 ~ W.), were subjected to chemical analysis. The secretion was expressed by external pressure on the anal pocket, and collected in a Teflon-capped vial. The secretion was extracted with Analar diethyl ether by means of agitation 141
ANIMAL
142
BEHAVIOUR,
of seven new individuals ( A - G ) were used; fresh secretion was obtained from each at the beginning of each set of trials. N o vocal cue of correctness was given a n d the a n i m a l ' s choice of slide was t a k e n as the last one to be sniffed before r e t u r n i n g to the observer for reward. Correct choices were rewarded, incorrect ones were not. I n a subsequent set of trials, anal pocket secretions were replaced by synthetic odours, p r o d u c e d by mixing pure acids in water. These mixtures were designed to simulate the relative a n d absolute concentrations of acids f o u n d in real secretions (Table I). The ability of mongooses to differentiate between these mixtures was tested in the way described above. Results Composition
The Chemical of Anal Pocket Secretions The analyses confirmed the presence of acetic, propionic, n-butyric, iso-butyric, n-valeric a n d iso-valeric acids in the anal pockets. The relative concentrations of these, i n the twentyfour animals studied, are shown i n Table II. It is clear that different individuals have different acid profiles a n d thus that they have different odours. T h e length of time for which a n individual's profile remains c o n s t a n t is, as yet, unclear. The Ability to Discriminate Anal Pocket Secretions and Synthetic Odours The results from the choice experiments using the four trained mongooses, a n d the anal pocket contents of animals A - G , are shown in Tables I I I to VI.
Table I. The Chemical Composition of the Synthetic Odours Used in Choice Experiments Concentration (mM) of carboxylic acids Synthetic Pro.pio- isonisonmixture Acetic mc Butyric Butyric Valeric Valeric
24,
1
T h e results show clearly that mongooses are able to distinguish between the anal pocket secretions of different individuals; i n the great majority of cases the trained animals were able to choose f r o m the series presented, the odour which they had been allowed to sniff. Table H. The Carboxylic Acid Profiles of Twenty-Four Mongooses. The Concentrations are in Relative Molarities with the Most Concentrated Acid Equal to 100 Relative concentration of carboxylic acids: No. Sex Acetic
Propio- isonisonnic Butyric Butyric Valeric Valeric
1
M
100
25
9
8
15
1
2
M
100
38
21
15
17
5
3
M
95
100
15
i1
7
9
4
M
100
20
16
30
35
8
5
M
70
100
6
28
25
2
6
M
100
21
17
38
4
16
7
M
100
16
28
11
7
1
8
M
100
18
13
10
18
16
9
M
100
98
4
6
15
4
10
M
100
15
41
4
13
9
11
M
100
46
4
18
9
18
12
M
51
100
68
15
4
10
13
M
75
100
14
100
18
4
14
M
100
15
17
63
4
8
15
M
100
28
10
7
3
1
16
F
100
31
15
1
4
1
17
F
100
15
19
0
16
0
18
F
100
14
28
16
38
4
19
F
I00
80
14
11
0
10
20
F
100
30
14
21
0
18
21
F
100
60
1
30
1
I
22
F
100
30
41
15
11
10
23
F
100
6
4
13
21
3
24
F
100
68
40
0
4
10
rio. :
1
30
20
10
10
5
5
2
30
0
10
5
30
10
3
30
10
30
20
5
10
4
10
30
10
20
10
5
G O R M A N : MECHANISM FOR I N D I V I D U A L RECOGNITION BY O D O U R
143
Table III. The Performance of tile Trained Mongoose Laisa in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Table V. The Performance of the Trained Mongoose Sid in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Sample presented
A
Sample presented
A
A
48
1
A
23
0
Sample chosen (no. of occasions) B
C
0
D
0
E
F
G
1
7
0
Sample chosen (No. of occasions) B
C
D
E
F
G
0
0
1
1
1
B
0
6
0
0
0
0
0
B
0
7
0
0
0
0
0
C
7
0
24
0
1
1
0
C
0
1
19
6
7
1
1
D
0
0
0
19
1
0
3
D
0
0
0
18
0
0
0
E
0
0
0
3
16
0
1
E
0
0
7
4
28
0
0
F
0
1
3
I
2
17
0
F
0
0
1
4
0
20
0
G
0
0
1
4
0
1
15
G
0
0
0
0
0
0
11
Table IV. The Performance of the Trained Mongoose Fred in Discriminating Between the Anal Pocket Contents of Mongooses A - G Sample presented
A
A
16
0
0
0
0
0
B
0
11
0
0
0
C
0
0
17
0
D
0
0
0
E
0
0
F
0
G
0
Table VI. The Performance of the Trained Mongoose Tavita in Discriminating Between the Anal Pocket Contents of Mongooses A - G
Sample chosen (no. of occasions)
1
Sample presented
A
0
0
A
11
1
0
0
0
1
1
0
1
3
B
0
17
0
1
3
4
1
28
0
1
4
C
0
1
9
0
0
0
1
4
0
16
0
0
D
0
0
0
14
0
0
0
0
0
0
1
28
0
E
0
1
5
4
17
0
0
1
1
3
0
0
17
F
0
0
0
0
1
6
0
G
0
0
0
0
1
1
19
B
C
D
E
F
G
T h e results f r o m t h e c h o i c e e x p e r i m e n t s i n v o l v i n g s y n t h e t i c o d o u r s are s h o w n in T a b l e VII. Since t h e p r e v i o u s e x p e r i m e n t s h o w e d t h a t all f o u r m o n g o o s e s c o u l d effectively d i s c r i m i n a t e b e t w e e n different o d o u r s , the d a t a f r o m t h e f o u r a n i m a l s are c o m b i n e d in T a b l e V I I . T h e results i n d i c a t e t h a t m o n g o o s e s c a n distinguish b e t w e e n s y n t h e t i c m i x t u r e s o f c a r b o x ylic acids j u s t as effectively as they c a n b e t w e e n a n a l p o c k e t secretions. Discussion It is well e s t a b l i s h e d t h a t a v a r i e t y o f m a m m a l species c a n r e c o g n i z e conspecifics, as i n d i v i d u a l s , o n t h e basis o f their o d o u r ; f o r e x a m p l e b l a c k tailed d e e r Odocoileus hemionus (MtillerS c h w a r z e 1971), m i c e Mus musculus ( B o w e r s &
Sample chosen (No. of occasions) B
C
D
E
F
G
Table VII. The Performances of the Four Mongooses Discriminating Between Synthetic Mixtures of Carboxylic Acids
Mixture chosen: total No. of choices by all four trained mongooses Mixture presented
1
2
3
4
1
25
2
2
0
2
2
12
0
0
3
1
0
41
1
4
3
0
0
19
144
ANIMAL
BEHAVIOUR,
Alexander 1967), rats Rattus norvegicus (Krames 1970), gerbils Meriones unguiculatus (Halpin 1974) and the African dwarf mongoose Helogale undulata (Rasa 1973). This final species is of interest in that marks made by the anal glands can be distinguished by conspecifics. The present paper shows that H. auropunctatus also, cart recognize conspecifics as individuals using olfactory cues from the secretions of the anal pockets. It is suggested that this ability is based upon the fact that each animal has a different, and probably unique, combination of concentrations of six odorous organic acids within its anal pockets. It has previously been established that these acids are the products of bacterial metabolism of sebum and apocrine secretions (Gorman et al. 1974). The behavioural work reported here shows that this mongoose can also effectively discriminate between synthetic mixtures of pure acids, suggesting that these acid profiles form the basis for olfactory discrimination of anal pocket secretions from different individuals. The question still remains as to why each individual has a different odour. Gorman et al. (1974) have shown that the substrate presented to the bacteria in the anal pocket is a complex mixture of sebum and apocrine secretions. It is possible that each animal produces a chemically unique substrate, which when metabolized by bacteria produces a unique combination of carboxylic acids. It is more likely, however, that all individuals produce chemically similar substrates and that differences in carboxylic acid profiles are due to differences in the symbiotic microfloras. Gorman et al. (1974) identified at least four species of bacteria within the anal pocket, each producing different combinations of carboxylic acids. Clearly, if individual mongooses have different bacterial populations they will also have different acid profiles and consequently different odours. Rasa (1973) found that her dwarf mongooses could distinguish between anal secretions of different ages, as well as between secretions from different individuals. She suggested that a chemical change must take place when the secretion was exposed to air. The present findings suggest what changes may occur. The six acids found in the anal pocket of 1t. auropunctatus vary greatly in volatility, from n-valeric acid with a boiling point of 186 ~ C to acetic acid with a boiling point of 118~ Clearly, as a deposited secretion ages, its chemical composition will change as the more volatile constituents evaporate
24,
1
at a proportionally higher rate than the less volatile ones. Consequently, a mark may contain not only the information as to which mongoose deposited it, but also its age. Problems will dearly arise if the ageing mark, during its chemical changes, comes to resemble the mark of some other individual. Prehaps this is not a serious problem in a species such as H. auropunctatus which is largely sedentary and in contact with relatively few conspecifics and their marks. Finally, it is of interest to speculate on the evolution of such a system. Sebum, and to a much lesser extent apocrine secretion, is generally deposited on the pelage of mammals where it is thought to have a water-proofing function. The normal skin microflora will metabolize these materials producing small quantities of short-chain carboxylic acids, and imparting a faint smell to the animal, In a variety of species this smell appears to have become involved in a communicating function; under selection the sebaceous and apocrine glands have become concentrated into discrete organs producing quantities of secretion containing, amongst other substances, carboxylic acids. Thus we find that carboxylic acids form a part of the scents of many mammals; they have been detected in the anal pockets of the red fox Vulpes vulpes (Albone & Fox 1971), of the lion Panthera leo (Albone et al. 1974) and of the weasel Mustela nivalis (Gorman unpublished data); they occur in the vagina of the rhesus monkey Macaca mulatta (Curtis et al. 1971) where they serve to attract the male; in the human vagina, particularly around the time of ovulation (Michael, Bonsall & Warner 1974); in the human axilla (Shelley, Harley & Nicholls 1953); in the guineapig Cavia porcellus perineaI gland (Beriiter, Beauchamp & Muetterties 1974); in the subauricular gland of the male prong-horn Antilocapra americana (Miiller-Schwarze et al1974). The involvement of bacteria in the production of these acids has been implicated for the red fox (Albone et al. 1974), for the rhesus monkey (Michael et al. 1972), for the human axilla (Shelley et al. 1953) and for the guinea-pig (Gorman unpublished observations). It is likely that future work will show their involvement in other species also.
Acknowledgments I am grateful to the Leverhulme Trust for financial support, to Waisake Volau for his
GORMAN: MECHANISM FOR INDIVIDUAL RECOGNITION BY ODOUR assistance i n Fiji, and to D r P. Boyle a n d D r C. H. F r y for their criticisms of this manuscript. REFERENCES
Albone, E. S. & Fox, M. W. (1971). Anal gland secretion of the red fox. Nature, Lond., 233, 569-570. Albone, E. S., Eglinton, G., Walker, G. M. & Ware, G. C. (1974). The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sciences, 14, 387-400. Bertiter, J., Beauchamp, G. K. & Muetterties, E. L. (1974). Mammalian chemical communication: perineal gland secretion of the guinea pig. PhysioL Zool., 47, 130-136. Bowers, J. M. & Alexander, B. K. (1967). Mice: individual recognition by olfactory cues. Science, 158, 1208-1210. Curtis, R. F., BaUantine, J. A., Keverne, E. B., Bonsall, R. W. & Michael, R. P. (t971). Identification of primate sex pheromones and the properties of synthetic attractants. Nature, Lond., 232, 396-398. Gorman, M. L., Nedwell, D. B. & Smith, R. M. (1974). An analysis of the anal scent pockets of Herpestes auropunctatus (Carnivora: Viverridae). J. Zool. Lond., 172, 389-399. Halpin, Z. T. (1974). Individual differences in the biological odours of the mongolian gerbil (Meriones unguiculatus). Behav. Biol., 11, 253-259.
145
Krames, L. (1970). Responses of female rats to the individual body odours of male rats. Psychon. Sci. Sect. Anim. Physiol. Psychol., 20,274--275. Michael, R. D., Zumpe, D., Keverne, E. B. & Bonsall, R. W. (1972). Neuro-endocrine factors in the control of primate behaviour. Recent Progr. Horm. Res., 28, 665-706. Michael, R. D., Bonsall, R. W., & Warner, D. (1974). Human vaginal secretions: Volatile fatty acid content. Science, 186, 1217-1219. Mtiller-Schwarze, D. (1971). Pheromones in black-tailed deer (Odocoiles hemionus columbianus). Anim. Behav., 19, 141-152. Mtiller-Schwarze, D., Mtiller-Schwarze, C., Singer, A. G. & Silverstein, R. M. (1974). Mammalian pheromone: identification of active component in sub-auricular scent of the male pronghorn. Science, 183, 860-862. Pocock, R. I. (1916). On the external characters of the mongoose (Mungotidae). Proc. zool. soc., Lond., 1916, 349-374. Rasa, A. E. (1973). Marking behaviour and its social significance i n the African dwarf mongoose Helogale undulata rufula. Z. Tierpsychol., 32, 293-318. Shelley, W. B., Harley, H. J. & Nicholls, A. C. (1953). Axillary odour: an experimental study of the role of bacteria, apocrine sweat and deodorants. Arch. DermatoL Syph. N.Y., 68, 430--446.
(Received 28 April 1975; MS. number: 1423)