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Display of penile erection in squirrel monkey (Sainuri sciureus)
DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY (Suiniri .sciureus) By DETLEV W . PLOOG, M .D .,* AND PAUL D . MACLEAN, M .D . Laboratory of Neurophysiology, National Institute of Mental Health, National Institutes of Health, Public Health Service, Department of Health, Education, and Welfare, Bethesda, Maryland
In this laboratory
the
squirrel monkey
perches . A water trough was at the bottom rear of the cage. Food was delivered through a hinged door in the front panel . Because of restrictions of space it was not feasible to isolate the viewing cage from the rest of the animal quarters which generally houses about 20 monkeys in 16 cages placed on 4 moveable double-decked frames . The animal room was lighted by a large window and fluorescent lights. It was darkened at night . The staple diet consisted of soft pellets of purina chow. Ten pellets appeared to satisfy an animal's food requirements for 1 day . An average pellet weighed 3 . 5 g . Favoured foods, such as bananas, peanuts and grapes, were fed for special purposes . Each week all animals were routinely weighed and examined in order to check on their general condition . Vitamins, vermifuges and antibiotics were given when necessary .
(Saimiri sciureus) has been extensively used for
brain stimulation and electro-encephalographic studies on the cerebral representation of sexual functions (MacLean, 1959 ; MacLean & Ploog, 1962). Because of its small body and large brain this New World primate has many advantages for investigations on neurophysiological and neuro-anatomical correlates of behaviour . Representative measurements of its body and brain were given in a previous communication (Carmichael & MacLean, 1961) . In order to obtain background information for interpreting the results of electrical stimulation we have made studies of the individual and social behaviour of the squirrel monkey . Of particular interest has been the finding that the male displays penile erection under a variety of conditions . The first part of this paper will describe the various types of penile display that have been observed . The second part will deal with special studies that suggest that under certain conditions a male displays to another male as a means of exerting and establishing dominance . Some phylogenetic and other implications of these findings will be discussed .
Observational Procedures In order to avoid heating effects fluorescent lighting was used for making observations and taking motion pictures . Observers (usually 2 to 3 in number) sat quietly in chairs about 6 feet from the viewing cage . Control observations behind a one-way mirror showed that screening of the observers was unnecessary . In each hourly session an observer focused on one animal and its activities in relation to itself and the group . Special protocol sheets were used for descriptive comments and to score the occurrence of particular behaviours for the purpose of obtaining quantifiable data that could be subjected to statistical analysis . Further details will be given in connection with the special studies to be described . Sample sessions indicated that the total activity of a group showed little variation during the daylight hours . For the sake of laboratory routine observational sessions in any one study were scheduled at the same time each day .
METHODS General observations have been made on over 100 squirrel monkeys admitted to the Laboratory . Special studies have been conducted on individual and small groups of animals . The present paper is based largely on the findings on (i) one group of 4 males and 2 females that was intensively studied for 1 year and on (ii) another group of 6 monkeys with the inverse ratio of males to females that was observed for 3 months. The small groups of animals were observed in a home cage 3 feet x 3 feet x 4 feet with transparent panels of lucite for the sides and ceiling . The cage and the first group of animals studied are shown in Fig. 1 . In the middle of the cage is seen a plastic tree providing a number of
Statistical Analysis For our purposes, it was desired to rank the animals with respect to their performance of
*Now at : Deutsche Forschungsanstalt fur Psychiatrie Max-Planck-Institut, Munich, Germany . 32
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY PLATE
V
Fig. 1 . Group of six squirrel monkeys used in the majority of the social studies described in text . Throughout the year of observation they lived in the viewing cage shown here . On the plexiglass tree from left to right : Gertrude ; the two immature animals, Dwight and Frances ; and Bert, the second ranking male . Caspar, the dominant male, is on floor at the right, and Edgar, the lowest ranking male, is in the left hand corner .
Anim . Behav ., 11, 1
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY various behaviours . To this end, chi-square analysis was used to ascertain whether or not the animals were performing alike . For example, the hypothesis tested in the feeding experiments was that animals could obtain the same number of pellets and the observed scores differed by chance . If the null hypothesis was rejected by the chi-square analysis, the animals were then ranked on a relative basis. The animals with the highest score for a particular behavioural pattern received a rank of 10 . Ranks (to the nearest integer) for the remaining animals were obtained by multiplying the ratio of an animal's score to the maximum by 10 . It was considered that this method of ranking was more informative than a score of 1 to 6 based on the number of animals in the group . Thus in the feeding experiments to be described the animal Edgar ranked third from the highest on the first three pellets won and received a relative rank of 3 ; whereas, on the second three pellets won, he again was third from the highest, but his relative rank was 6 . RESULTS I. Types of Penile Display The types of display of penile erection will be described under the headings of (1) distant display, (2) mirror display and (3) display in the communal situation . (1) Distant Display It is frequently observed that the introduction of a new monkey into the animal room may precipitate the display of penile erection by some of the males in separate cages . They usually climb up on the wire mesh of their cages in an attempt to approach the new animal and then display. Display also occurs from time to time among old inhabitants in separate cages . It is commonly precipitated by the transfer of an animal from one cage to another. During the display the monkey inclines the head to one side and abducts one thigh while the penis gradually reaches partial or full erection concurrently with a few spurts of urine . At the same time there is typically scratching of the body with a hand or foot, together with highpitched, soft vocalization during which the corners of the mouth are retracted . With each vocalization there may be a thrusting forward of the fully erect penis . This combined behavioural pattern may occur intermittently during the better part of 1 minute .
33
(2) Mirror Display A behavioural pattern practically identical to that just described may be elicited by holding a mirror before a male . Here again there, is usually an attempt to approach the observed animal . In this case, however, full erection may be achieved more rapidly as the simultaneous erection seen in the reflection appears to facilitate the response . The response can be obtained a number of times each day and on successive days over a period of-several weeks . A study on the role of temporal factors in its reproducibility is now in progress . (3) Display in the Communal Situation In the communal situation the male may display penile erection to another male or to a female . Such displays are performed in (i) the open position and (ii) the closed position . (i) Open position . In the open position the male approaches within the visual field of the other animal and displays from a distance of several inches . It looks towards the animal receiving the display and abducts the thigh on the same side while erection develops . Sometimes the thigh spreading occurs without the development of erection . Display in the open position occurs from time to time among animals in an established group, and it is commonly seen when a new animal is introduced into a group . (ii) Closed position . An illustration of display in the closed position is shown in Fig . 2 . In this display the male approaches a female or another male head on, places one or both hands on its back and thrusts the erect penis towards the face . In doing so it "thigh-spreads" as in the open display, but in this instance the gaze is directed away from the recipient . The entire act usually takes place in less than 10 seconds . The animal receiving the display sits in a cowering position while ducking its head as though dodging a blow . It sometimes responds with an erection afterwards, but never spreads the thighs . If it does not remain quiet during the display, it may be viciously attacked . The display of the male towards the female in the closed pattern has been observed to precede attempts at copulation . Display in the Female In the first group of 4 males and 2 females that was observed, there was no behaviour of the
34
ANIMAL BEHAVIOUR, XI, I
similar impression . The display in the closed position, however, appears to have aggressive implications because in the case of two males, it may be followed by vicious assault by the displaying male if the recipient does not remain passive and quiet during the act . Such behaviour has been observed to occur repeatedly in circumstances in which the displaying, pugnacious animal finally seemed to establish himself as the dominant animal . Studies supporting the inference that penile display towards another male is used as a means of exerting and establishing dominance will be described in the following section . In the case of the male and female, display in the closed position has not been observed to be followed by fighting . As it may precede attempts at copulation, it presumably has some communicative significance in courtship behaviour.
Fig. 2 . In the communal situation the male squirrel monkey may display penile erection in courtship, or, as illustrated above, it may display to another male as a means of exerting and establishing dominance . In each case the (display is performed with the thighs spread and the erect penis thrust almost into the face of the other animal.
female suggesting the thigh spreading and display of the male . In the second group comprising 2 males and 4 females, however, the animal judged to be the dominant female sometimes responded to the open display of the dominant male by similar assumption of posture. On several such occasions her clitoris appeared to be enlarged . In this same group two of the females sometimes displayed to one another in the open position, a mutual display that was never observed to occur between two males . Rarely a female would "thigh-spread" towards another female or male in the closed position . One female has been observed to display to animals in other cages (distant display) . Comment The circumstances in which distant display takes place, and the fact that it occurs in response to an animal's own reflection, suggest that it represents a form of greeting to a strange animal. The display in the open position that happens in the communal situation gives a
II. Penile Display in Relation to Dominance Indications of the aggressive nature of penile display in a communal situation became evident in the first colony that was studied . This colony consisted of 4 males and 2 females that were named Bert, Caspar, Dwight, Edgar, Frances and Gertrude. In the figures they will be referred to by their initials . Skeletal x-rays and other evidence showed that Dwight and Frances were not fully mature . The chronological order of the various studies carried out on this group is shown in Fig . 3, which also gives a graph of the respective weights of the animals during the year of observation . Only those aspects of the feeding, grooming and distance studies that pertain to display behaviour will be considered here . From the beginning the impression was gained that Caspar was the dominant animal in this group . In January of 1959 he pursued the immature animal, Dwight, constantly and fought with him many times . In February he continued to fight with Dwight and also began to fight with Bert . Dwight sometimes retaliated, but Bert never did . In March, Caspar began to show aggressive behaviour toward Edgar . The latter was observed from the beginning to stay apart from the group and was often seen circling the floor of the cage. During the 3 months of preliminary observations it also became evident that Caspar displayed penile erection to all the other animals, but none displayed to him (see chart of General Observations in Fig. 5) . In contrast, Edgar, the animal which appeared to be a kind of outcast,
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
Iu 3
850
700
W
u
Q
W
550
400 I FEEDING
II
STUDIES
DISPLAY STUDIES
R.
I
35
Preliminary to other studie s on the colony that were planned, it was desirable to obtain an accepted behavioural measure of dominance among animals . As the outcome of rivalry among animals for food is generally considered to be a reliable indicator of dominance, a series of such studies was undertaken . These will be referred to as feeding studies. Their temporal relationship to the other studies is given in Fig. 3 .
A. Feeding Studies Methods Four series of feeding tests GENERAL OBSERVATIONS were conducted between March and October . Each Fig. 3 . Weight curves of the group of animals shown in Fig. 1 during the year series consisted of the presenof various studies chronologically indicated below the graph . The letters B, C, tation of 10 food pellets on 10 different days . It was anD, etc., in this and following figures are the inititals of the names of animals ticipated that the presentation in the group . of 10 pellets which satisfies the daily food requirement of an animal (see displayed to none of the other males, but all Methods) might reveal behavioural differences displayed to him . attributable to the factor of satiation . The last The impression that Caspar was the dominfeeding before a test was at 3 p .m . on the preant animal was also supported by the fact that ceding day . Series 1 to 3 were conducted behe was the only animal in the group that tried tween 10.00 and 12 .00 a.m. and series 4 between to attack monkeys that were placed close to 1 .00 and 3 .00 p .m. Pellets were put one at a time the colony cage. He vocalized and rattled the into the front of the cage . As soon as one pellet . sides of the plastic cage in trying to attack them was eaten, it was followed by another . It usually On a number of occasions single males were required 5 to 10 minutes for an animal to conintroduced into the colony for short periods . sume one pellet . It was recorded in the protocol Caspar was the only male of the established which animal obtained the pellet, which stole a group that persisted in trailing the new animal pellet from another and what animals fought and displaying in the closed position . If the newover pellets . The tests in the first series were comer did not remain passive and quiet during scattered over a period of 10 weeks, whereas the the display, it was viciously attacked . This is second, third and fourth series were completed illustrated by what happened to a large, strong respectively within 3 weeks, 10 days, and 3 weeks . monkey, Napoleon, which was introduced under Results the supposition that, unlike his predecessors, The results of the 4 series of feeding tests are he would be able to overpower Caspar. Napoleon summarized in Table I, together with the findings fulfilled expectations by refusing to remain on statistical significance . In order to assess quiet during Caspar's display, but as a result possible differences owing to the factor of suffered such severe lacerations of the back of the satiation, the winnings were analysed in terms head and neck during the violent scuffles that of the first, the first 3, first 5, second 3 and second followed that humane considerations required 5 pellets won . Only the figures for the first, the his removal after a short time . The same pattern first 3, and second 3 pellets are given in the table, of behaviour shown by Caspar-penile display because the scores on the first 5 and second 5 followed by vicious attack-has been observed added no essential information, in other aggressive males . GROOMING DISTANCE
STUDIES
STUDIES
EJ
36
ANIMAL BEHAVIOUR, XI, I
Although Caspar, the animal judged to be dominant on the basis of general observations, won more pellets than each of the other animals,
his winnings were not significantly different from those of Bert, the second animal . Statistical analysis showed that this lack of distinction
Table I. Feeding Studies-Series I-IV . First Pellet won I
II
III
IV
Total
Rank
Bert
2
4
4
3
13
7
Caspar
5
4
5
4
18
10
Dwight
2
1
0
0
3
2
(b) p< .01
Edgar
1
1
0
3
5
3
(c) not sign .
Frances
0
0
0
0
0
0
(d) not sign .
Gertrude
0
0
1
0
1
0
1
(a) p< -001
l First three pellets won I Bert
II
6-
f I
III
IV
Total
Rank
9
16
15
46
10
Caspar
18 .
11
12
7
48
10
(a) p < -001
Dwight
4
3
0
1
8
1
(b) p< •0 01
Edgar
2
6
1
7
16
3
(c) not sign .
Frances
0
0
0
0
0
0
(d) not sign .
Gertrude
0
1
1
0
2
0
j
120 Second three pellets won I
II
III
IV
Total
Rank
9
13
8
8
38
9
Caspar
16
10
9
7
42
10
(a) p<-001
Dwight
3
2
2
1
8
2
(b) p< . 001
1
4
8
14
27
6
(c) not sign .
Frances
1
0
1
0
2
0
(d) p< . 01
Gertrude
0
1
2
0
3
1
Bert
Edgar
!
120 (a) Difference among all animals (b) Difference among males (c) Difference between Bert and Caspar (d) Difference between Dwight and Edgar
PLOOG & MAcLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
between the first two animals was not owing to the factor of satiation . On the contrary, there was a highly significant difference between the winnings of the first two animals and the rest of the group . Caspar and Bert were incontestably the dominant animals in obtaining food . It is possible that satiety on the part of these two animals might have favoured Edgar's increase in score in the second 3 pellets won in the third and fourth series of tests . With respect to the first three and second three pellets won, his ranking score increased from 3 to 6 . The analysis of the data on pellet stealing will be dealt with elsewhere when the total group structure is considered in the light of other studies listed in Fig . 3 . At this time it is significant only to point out that Caspar stole from all the animals except Gertrude, but none of the animals except the immature monkey, Dwight, stole from him . Bert, the other animal dominant in the feeding situation, stole from none of the other animals, but all except Gertrude stole from him . B. Display Studies The studies collectively referred to as display studies had two primary purposes . One was to learn whether or not in the communal situation display showed any correlation with the findings on dominance in the feeding studies, and the other was to ascertain in the case of male and female whether it was a part of courtship behaviour . An ancillary purpose was to obtain information on masturbatory activity . Only the observations pertaining to the first purpose will be considered here . Methods There were two series of observations . Their temporal relationship to the other studies is shown in Fig. 3 . In both series each of the 4 males was observed 6 times for a period of 1 hour . Consequently there were 24 hours of observation for each series and a total observation time of 48 hours . Each display was recorded with respect to the active and passive participants and the circumstances under which it occurred . The size and duration of the erections during display and the incidence of masturbation were noted . As described in a previous communication, the size of erection is graded on a 6 point scale, varying from ± to 5 + (Maclean & Ploog, 1962) . Data on display were also obtained in the grooming and distance studies which respectively involved 30 and 15
37
hours of observation . Although focusing on grooming behaviour, the grooming studies were also concerned with obtaining information in regard to possibly related patterns of behaviour ; hence, it was significant to record findings with respect to display. The same was true in regard to the so-called "distance studies" in which observations on the physical closeness or distance maintained between various animals were made in order to gain added information about the social organization of the group . Results Fig . 4 gives the incidence of penile display by the various animals in the two series of observations . Caspar proved to be by far the most active animal in displaying. It is to be emphasized that all but two of his displays were directed to the other males . In contrast, the immature male, Dwight, made most of his displays to the
DISPLAY STUDIES NUMBER OF DISPLAYS PASSIVE PARTICIPANTS
B C D E F 9 G9 B
0
C 58 D
6
0
E
0
0
TOTAL
2
4
4
12
7 33
I
I
100
3 32 4
45
0
0
0
0
Fig . 4 . Incidence of display of penile erection in the two display studies described in the text .
immature female, Frances . It is also to be emphasized that Edgar, the animal that remained peripheral to the group, displayed to none of the other males, whereas all displayed to him. Edgar displayed only to the observers or to other persons who entered the animal room . If displays to females were subtracted, the ranking order for displays would be Caspar,
38
ANIMAL BEHAVIOUR, XI,
Dwight, Bert and Edgar, and their respective ranking scores would be 10, 1, 0, 0 . Fig. 5 shows for comparison the incidence of display in the display, grooming, and distance studies. The fewer number of displays observed in the grooming and distance studies correlates with the shorter time of observation in these
where that would shed light on the findings pertaining to the feeding and display studies described here . In the wild they are said to feed in large aggregations (Sanderson 1957) . The failure of the feeding studies to show a clear distinction in dominance between the two high scoring animals possibly reflects some natural propensity for pairs or small numbers of animals within INCIDENCE OF DISPLAY IN VARIOU S STUDIES large groups to co-operate in getting food . In a subsequent communication the feeding PASSIVE PPARTICIPANTS PASSIVE PARTICIPANTS and display studies will be considered in the light of other E F G B C D B D E F G studies on grooming behaviour and propinquity factors B 0 2 t within groups . On the basis U B Iof the combined evidence, it 7 33 I I C 58 C may be concluded that obser32 4 D 6 0 vations on penile display give vations D w a better indication of hier0 0 E 0 0 E archy in the social structure archy IU of squirrel monkeys in capQ DISPLAY STUDIES GENERAL OBSERVATIONS tivity than does the outcome of rivalry for food . The bodily orientation of PASSIVE PA RTICIPANTS two squirrel monkeys during PASSIVE PARTICIPANTS 1penile display in the closed z Z D E F G G B C B C D E F position is somewhat suggestive of two dogs mutually 0 2 4 0 4 1 1 B 0 2 U B U smelling the genitalia, with I1= I 5 0 0 the important difference that8 X C 13 5 14 1 ir C -; in the monkey the emphasis 0 0 0 D 0 0 appears to be on visual rather 9 10 D 3 0 0 W W '~ than olfactory cues . In this 0 0 0 0 0 0 0 E E 0 0 0 1regard it is to be recalled I. . : •: U that the dog is guided to a Q Q DISTANC E STUDIES GROOMING STUDIES large extent by its olfactory sense whereas the monkey is dominated by its visual sense . Fig. 5 . Comparison of incidence of display noted in the display studies with The inference that vision plays that observed in the grooming and distance studies and duri ng the course of general observations . Consideration should be given only to th e relative values a key role in penile display ies . because the periods of observation varied in the different stud is supported by the fact that in mirror display olfactory cues are autostudies . In each case there was the like finding matically excluded . In brain stimulation studies that Caspar was unquestionably the most active on the representation of penile erection, animal in displaying to other males . The groomnodal points for erection have been found in ing and distance studies also confirmed the the medial septopreoptic region and in the original findings that none of the animals medial part of the medial dorsal nucleus displayed to Caspar, and that Edgar, the (MacLean & Ploog, 1962) . In ascending the apparent outcast, displayed to none of the other phylogenetic scale one finds in higher primates males . that the septum shows regressive changes whereDISCUSSION as the systems associated with the anterior and We know of no observations on squirrel medial thalamic nuclei increase in size and monkeys in their natural environment or elsereach their maximum development in man .
rz
a
a
a
a
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
We have speculated that these changes may reflect a shifting emphasis from olfactory to visual influence in sociosexual behaviour (MacLean, 1962 ; MacLean & Ploog, 1962) . The pattern assumed by two monkeys during display, combined with the apparent emphasis on visual factors, would suggest that the squirrel monkey is a primate form representing an evolutionary "link" between the macrosmatic animal and the visually dominant animal. The finding that the squirrel monkey assumes the same posture for penile display in courtship and in aggression is of special phylogenetic interest in view of the fact that the courtship display of some male fishes and birds is indistinguishable from their aggressive posturing . The similarity between sexual and aggressive display becomes more understandable in the light of recent physiological studies which have shown that mechanisms for sexual and combative behaviour lie in close proximity in the brain stem and that excitation in one may spill over into the other (MacLean, 1959 ; 1962) . This is illustrated by brain stimulation studies on the cerebral representation of sexual functions in the squirrel monkey (MacLean & Ploog, 1962) . When stimulating in the hypothalamus one may pass within a millimetre from a point at which stimulation results in penile erection and an apparent state of placidity, to a point at which stimulation elicits erection in conjunction with angry or fearful vocalization and the showing of fangs . When the electrode is advanced a fraction of a millimetre further, only the signs of fear or anger appear during stimulation, but erection may occur as a rebound phenomenon after the termination of stimulation . There is also evidence that feeding mechanisms are closely allied to those underlying sexual and combative behaviour (MacLean, 1959 ; 1960) . This is not an unexpected finding inasmuch as fighting is frequently seen as a preliminary to both feeding and mating. Some evolutionary implications of the studies on penile display in regard to neuropsychiatric observations and to man's adoption of the loin cloth have been discussed elsewhere (MacLean, 1960) . SUMMARY In studies on the social behaviour of the squirrel monkey (Saimiri sciureus), it has been found that the male displays penile erection
39
under a variety of conditions. The types of display are described under the headings of (1) distant display, (2) mirror display, and (3) display in the communal situation . Distant display refers to the display that occurs between animals separated in cages . The same pattern of display occurs when a mirror is held up before a monkey (mirror display) . In the communal situation, the male may display penile erection to another male or to a female . Such displays are performed in what is described as the (i) open position and (ii) closed position . General observations suggested that a male may display to another male in the closed position as a means of exerting and establishing dominance. Special studies were undertaken to obtain measurements of dominance based on the outcome of rivalry for food and on display . The findings indicated that the observations based on penile display give a clearer indication of hierarchy in the social structure of squirrel monkeys in captivity than does the outcome of rivalry for food . Acknowledgments We wish to express our great appreciation to Dr . Samuel W . Greenhouse of the Biometrics Branch of the National Institute of Mental Health for his invaluable consultations in regard to statistical aspects of this study and for his statistical analysis of the results . We are much indebted to Mrs . Jean Cobb Blitz and Dr . Frauke Ploog for their help in making behavioural observations and analysing data . REFERENCES Carmichael, M . & MacLean, P. D. (1961) . Use of squirrel monkey for brain research, with description of restraining chair . EEG Clin. Neurophysiol., 13, 128-129 . MacLean, P . D . (1959) . The limbic system with respect to two basic life principles . In conference on the Central Nervous System and Behaviour, 2nd, 1959 . Transactions, New York Josiah Macy, Jr. Foundation, 1959, pp. 31-118 . MacLean, P . D . (1962) . New findings relevant to the evolution of psychosexual functions of the brain . J. nerv. ment . Dis ., 135, 289-301 . MacLean, P . D . & Ploog, D . W. (1962). Cerebral representation of penile erection . J. Neurophysiol., 25, 29-55 . Sanderson, 1 . T . (1957) . The monkey kingdom . Garden City, Hanover House, 200 pp . (Accepted for publication 7th May, 1962 Ms. number : 275) .
In this laboratory
the
squirrel monkey
perches . A water trough was at the bottom rear of the cage. Food was delivered through a hinged door in the front panel . Because of restrictions of space it was not feasible to isolate the viewing cage from the rest of the animal quarters which generally houses about 20 monkeys in 16 cages placed on 4 moveable double-decked frames . The animal room was lighted by a large window and fluorescent lights. It was darkened at night . The staple diet consisted of soft pellets of purina chow. Ten pellets appeared to satisfy an animal's food requirements for 1 day . An average pellet weighed 3 . 5 g . Favoured foods, such as bananas, peanuts and grapes, were fed for special purposes . Each week all animals were routinely weighed and examined in order to check on their general condition . Vitamins, vermifuges and antibiotics were given when necessary .
(Saimiri sciureus) has been extensively used for
brain stimulation and electro-encephalographic studies on the cerebral representation of sexual functions (MacLean, 1959 ; MacLean & Ploog, 1962). Because of its small body and large brain this New World primate has many advantages for investigations on neurophysiological and neuro-anatomical correlates of behaviour . Representative measurements of its body and brain were given in a previous communication (Carmichael & MacLean, 1961) . In order to obtain background information for interpreting the results of electrical stimulation we have made studies of the individual and social behaviour of the squirrel monkey . Of particular interest has been the finding that the male displays penile erection under a variety of conditions . The first part of this paper will describe the various types of penile display that have been observed . The second part will deal with special studies that suggest that under certain conditions a male displays to another male as a means of exerting and establishing dominance . Some phylogenetic and other implications of these findings will be discussed .
Observational Procedures In order to avoid heating effects fluorescent lighting was used for making observations and taking motion pictures . Observers (usually 2 to 3 in number) sat quietly in chairs about 6 feet from the viewing cage . Control observations behind a one-way mirror showed that screening of the observers was unnecessary . In each hourly session an observer focused on one animal and its activities in relation to itself and the group . Special protocol sheets were used for descriptive comments and to score the occurrence of particular behaviours for the purpose of obtaining quantifiable data that could be subjected to statistical analysis . Further details will be given in connection with the special studies to be described . Sample sessions indicated that the total activity of a group showed little variation during the daylight hours . For the sake of laboratory routine observational sessions in any one study were scheduled at the same time each day .
METHODS General observations have been made on over 100 squirrel monkeys admitted to the Laboratory . Special studies have been conducted on individual and small groups of animals . The present paper is based largely on the findings on (i) one group of 4 males and 2 females that was intensively studied for 1 year and on (ii) another group of 6 monkeys with the inverse ratio of males to females that was observed for 3 months. The small groups of animals were observed in a home cage 3 feet x 3 feet x 4 feet with transparent panels of lucite for the sides and ceiling . The cage and the first group of animals studied are shown in Fig. 1 . In the middle of the cage is seen a plastic tree providing a number of
Statistical Analysis For our purposes, it was desired to rank the animals with respect to their performance of
*Now at : Deutsche Forschungsanstalt fur Psychiatrie Max-Planck-Institut, Munich, Germany . 32
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY PLATE
V
Fig. 1 . Group of six squirrel monkeys used in the majority of the social studies described in text . Throughout the year of observation they lived in the viewing cage shown here . On the plexiglass tree from left to right : Gertrude ; the two immature animals, Dwight and Frances ; and Bert, the second ranking male . Caspar, the dominant male, is on floor at the right, and Edgar, the lowest ranking male, is in the left hand corner .
Anim . Behav ., 11, 1
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY various behaviours . To this end, chi-square analysis was used to ascertain whether or not the animals were performing alike . For example, the hypothesis tested in the feeding experiments was that animals could obtain the same number of pellets and the observed scores differed by chance . If the null hypothesis was rejected by the chi-square analysis, the animals were then ranked on a relative basis. The animals with the highest score for a particular behavioural pattern received a rank of 10 . Ranks (to the nearest integer) for the remaining animals were obtained by multiplying the ratio of an animal's score to the maximum by 10 . It was considered that this method of ranking was more informative than a score of 1 to 6 based on the number of animals in the group . Thus in the feeding experiments to be described the animal Edgar ranked third from the highest on the first three pellets won and received a relative rank of 3 ; whereas, on the second three pellets won, he again was third from the highest, but his relative rank was 6 . RESULTS I. Types of Penile Display The types of display of penile erection will be described under the headings of (1) distant display, (2) mirror display and (3) display in the communal situation . (1) Distant Display It is frequently observed that the introduction of a new monkey into the animal room may precipitate the display of penile erection by some of the males in separate cages . They usually climb up on the wire mesh of their cages in an attempt to approach the new animal and then display. Display also occurs from time to time among old inhabitants in separate cages . It is commonly precipitated by the transfer of an animal from one cage to another. During the display the monkey inclines the head to one side and abducts one thigh while the penis gradually reaches partial or full erection concurrently with a few spurts of urine . At the same time there is typically scratching of the body with a hand or foot, together with highpitched, soft vocalization during which the corners of the mouth are retracted . With each vocalization there may be a thrusting forward of the fully erect penis . This combined behavioural pattern may occur intermittently during the better part of 1 minute .
33
(2) Mirror Display A behavioural pattern practically identical to that just described may be elicited by holding a mirror before a male . Here again there, is usually an attempt to approach the observed animal . In this case, however, full erection may be achieved more rapidly as the simultaneous erection seen in the reflection appears to facilitate the response . The response can be obtained a number of times each day and on successive days over a period of-several weeks . A study on the role of temporal factors in its reproducibility is now in progress . (3) Display in the Communal Situation In the communal situation the male may display penile erection to another male or to a female . Such displays are performed in (i) the open position and (ii) the closed position . (i) Open position . In the open position the male approaches within the visual field of the other animal and displays from a distance of several inches . It looks towards the animal receiving the display and abducts the thigh on the same side while erection develops . Sometimes the thigh spreading occurs without the development of erection . Display in the open position occurs from time to time among animals in an established group, and it is commonly seen when a new animal is introduced into a group . (ii) Closed position . An illustration of display in the closed position is shown in Fig . 2 . In this display the male approaches a female or another male head on, places one or both hands on its back and thrusts the erect penis towards the face . In doing so it "thigh-spreads" as in the open display, but in this instance the gaze is directed away from the recipient . The entire act usually takes place in less than 10 seconds . The animal receiving the display sits in a cowering position while ducking its head as though dodging a blow . It sometimes responds with an erection afterwards, but never spreads the thighs . If it does not remain quiet during the display, it may be viciously attacked . The display of the male towards the female in the closed pattern has been observed to precede attempts at copulation . Display in the Female In the first group of 4 males and 2 females that was observed, there was no behaviour of the
34
ANIMAL BEHAVIOUR, XI, I
similar impression . The display in the closed position, however, appears to have aggressive implications because in the case of two males, it may be followed by vicious assault by the displaying male if the recipient does not remain passive and quiet during the act . Such behaviour has been observed to occur repeatedly in circumstances in which the displaying, pugnacious animal finally seemed to establish himself as the dominant animal . Studies supporting the inference that penile display towards another male is used as a means of exerting and establishing dominance will be described in the following section . In the case of the male and female, display in the closed position has not been observed to be followed by fighting . As it may precede attempts at copulation, it presumably has some communicative significance in courtship behaviour.
Fig. 2 . In the communal situation the male squirrel monkey may display penile erection in courtship, or, as illustrated above, it may display to another male as a means of exerting and establishing dominance . In each case the (display is performed with the thighs spread and the erect penis thrust almost into the face of the other animal.
female suggesting the thigh spreading and display of the male . In the second group comprising 2 males and 4 females, however, the animal judged to be the dominant female sometimes responded to the open display of the dominant male by similar assumption of posture. On several such occasions her clitoris appeared to be enlarged . In this same group two of the females sometimes displayed to one another in the open position, a mutual display that was never observed to occur between two males . Rarely a female would "thigh-spread" towards another female or male in the closed position . One female has been observed to display to animals in other cages (distant display) . Comment The circumstances in which distant display takes place, and the fact that it occurs in response to an animal's own reflection, suggest that it represents a form of greeting to a strange animal. The display in the open position that happens in the communal situation gives a
II. Penile Display in Relation to Dominance Indications of the aggressive nature of penile display in a communal situation became evident in the first colony that was studied . This colony consisted of 4 males and 2 females that were named Bert, Caspar, Dwight, Edgar, Frances and Gertrude. In the figures they will be referred to by their initials . Skeletal x-rays and other evidence showed that Dwight and Frances were not fully mature . The chronological order of the various studies carried out on this group is shown in Fig . 3, which also gives a graph of the respective weights of the animals during the year of observation . Only those aspects of the feeding, grooming and distance studies that pertain to display behaviour will be considered here . From the beginning the impression was gained that Caspar was the dominant animal in this group . In January of 1959 he pursued the immature animal, Dwight, constantly and fought with him many times . In February he continued to fight with Dwight and also began to fight with Bert . Dwight sometimes retaliated, but Bert never did . In March, Caspar began to show aggressive behaviour toward Edgar . The latter was observed from the beginning to stay apart from the group and was often seen circling the floor of the cage. During the 3 months of preliminary observations it also became evident that Caspar displayed penile erection to all the other animals, but none displayed to him (see chart of General Observations in Fig. 5) . In contrast, Edgar, the animal which appeared to be a kind of outcast,
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
Iu 3
850
700
W
u
Q
W
550
400 I FEEDING
II
STUDIES
DISPLAY STUDIES
R.
I
35
Preliminary to other studie s on the colony that were planned, it was desirable to obtain an accepted behavioural measure of dominance among animals . As the outcome of rivalry among animals for food is generally considered to be a reliable indicator of dominance, a series of such studies was undertaken . These will be referred to as feeding studies. Their temporal relationship to the other studies is given in Fig. 3 .
A. Feeding Studies Methods Four series of feeding tests GENERAL OBSERVATIONS were conducted between March and October . Each Fig. 3 . Weight curves of the group of animals shown in Fig. 1 during the year series consisted of the presenof various studies chronologically indicated below the graph . The letters B, C, tation of 10 food pellets on 10 different days . It was anD, etc., in this and following figures are the inititals of the names of animals ticipated that the presentation in the group . of 10 pellets which satisfies the daily food requirement of an animal (see displayed to none of the other males, but all Methods) might reveal behavioural differences displayed to him . attributable to the factor of satiation . The last The impression that Caspar was the dominfeeding before a test was at 3 p .m . on the preant animal was also supported by the fact that ceding day . Series 1 to 3 were conducted behe was the only animal in the group that tried tween 10.00 and 12 .00 a.m. and series 4 between to attack monkeys that were placed close to 1 .00 and 3 .00 p .m. Pellets were put one at a time the colony cage. He vocalized and rattled the into the front of the cage . As soon as one pellet . sides of the plastic cage in trying to attack them was eaten, it was followed by another . It usually On a number of occasions single males were required 5 to 10 minutes for an animal to conintroduced into the colony for short periods . sume one pellet . It was recorded in the protocol Caspar was the only male of the established which animal obtained the pellet, which stole a group that persisted in trailing the new animal pellet from another and what animals fought and displaying in the closed position . If the newover pellets . The tests in the first series were comer did not remain passive and quiet during scattered over a period of 10 weeks, whereas the the display, it was viciously attacked . This is second, third and fourth series were completed illustrated by what happened to a large, strong respectively within 3 weeks, 10 days, and 3 weeks . monkey, Napoleon, which was introduced under Results the supposition that, unlike his predecessors, The results of the 4 series of feeding tests are he would be able to overpower Caspar. Napoleon summarized in Table I, together with the findings fulfilled expectations by refusing to remain on statistical significance . In order to assess quiet during Caspar's display, but as a result possible differences owing to the factor of suffered such severe lacerations of the back of the satiation, the winnings were analysed in terms head and neck during the violent scuffles that of the first, the first 3, first 5, second 3 and second followed that humane considerations required 5 pellets won . Only the figures for the first, the his removal after a short time . The same pattern first 3, and second 3 pellets are given in the table, of behaviour shown by Caspar-penile display because the scores on the first 5 and second 5 followed by vicious attack-has been observed added no essential information, in other aggressive males . GROOMING DISTANCE
STUDIES
STUDIES
EJ
36
ANIMAL BEHAVIOUR, XI, I
Although Caspar, the animal judged to be dominant on the basis of general observations, won more pellets than each of the other animals,
his winnings were not significantly different from those of Bert, the second animal . Statistical analysis showed that this lack of distinction
Table I. Feeding Studies-Series I-IV . First Pellet won I
II
III
IV
Total
Rank
Bert
2
4
4
3
13
7
Caspar
5
4
5
4
18
10
Dwight
2
1
0
0
3
2
(b) p< .01
Edgar
1
1
0
3
5
3
(c) not sign .
Frances
0
0
0
0
0
0
(d) not sign .
Gertrude
0
0
1
0
1
0
1
(a) p< -001
l First three pellets won I Bert
II
6-
f I
III
IV
Total
Rank
9
16
15
46
10
Caspar
18 .
11
12
7
48
10
(a) p < -001
Dwight
4
3
0
1
8
1
(b) p< •0 01
Edgar
2
6
1
7
16
3
(c) not sign .
Frances
0
0
0
0
0
0
(d) not sign .
Gertrude
0
1
1
0
2
0
j
120 Second three pellets won I
II
III
IV
Total
Rank
9
13
8
8
38
9
Caspar
16
10
9
7
42
10
(a) p<-001
Dwight
3
2
2
1
8
2
(b) p< . 001
1
4
8
14
27
6
(c) not sign .
Frances
1
0
1
0
2
0
(d) p< . 01
Gertrude
0
1
2
0
3
1
Bert
Edgar
!
120 (a) Difference among all animals (b) Difference among males (c) Difference between Bert and Caspar (d) Difference between Dwight and Edgar
PLOOG & MAcLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
between the first two animals was not owing to the factor of satiation . On the contrary, there was a highly significant difference between the winnings of the first two animals and the rest of the group . Caspar and Bert were incontestably the dominant animals in obtaining food . It is possible that satiety on the part of these two animals might have favoured Edgar's increase in score in the second 3 pellets won in the third and fourth series of tests . With respect to the first three and second three pellets won, his ranking score increased from 3 to 6 . The analysis of the data on pellet stealing will be dealt with elsewhere when the total group structure is considered in the light of other studies listed in Fig . 3 . At this time it is significant only to point out that Caspar stole from all the animals except Gertrude, but none of the animals except the immature monkey, Dwight, stole from him . Bert, the other animal dominant in the feeding situation, stole from none of the other animals, but all except Gertrude stole from him . B. Display Studies The studies collectively referred to as display studies had two primary purposes . One was to learn whether or not in the communal situation display showed any correlation with the findings on dominance in the feeding studies, and the other was to ascertain in the case of male and female whether it was a part of courtship behaviour . An ancillary purpose was to obtain information on masturbatory activity . Only the observations pertaining to the first purpose will be considered here . Methods There were two series of observations . Their temporal relationship to the other studies is shown in Fig. 3 . In both series each of the 4 males was observed 6 times for a period of 1 hour . Consequently there were 24 hours of observation for each series and a total observation time of 48 hours . Each display was recorded with respect to the active and passive participants and the circumstances under which it occurred . The size and duration of the erections during display and the incidence of masturbation were noted . As described in a previous communication, the size of erection is graded on a 6 point scale, varying from ± to 5 + (Maclean & Ploog, 1962) . Data on display were also obtained in the grooming and distance studies which respectively involved 30 and 15
37
hours of observation . Although focusing on grooming behaviour, the grooming studies were also concerned with obtaining information in regard to possibly related patterns of behaviour ; hence, it was significant to record findings with respect to display. The same was true in regard to the so-called "distance studies" in which observations on the physical closeness or distance maintained between various animals were made in order to gain added information about the social organization of the group . Results Fig . 4 gives the incidence of penile display by the various animals in the two series of observations . Caspar proved to be by far the most active animal in displaying. It is to be emphasized that all but two of his displays were directed to the other males . In contrast, the immature male, Dwight, made most of his displays to the
DISPLAY STUDIES NUMBER OF DISPLAYS PASSIVE PARTICIPANTS
B C D E F 9 G9 B
0
C 58 D
6
0
E
0
0
TOTAL
2
4
4
12
7 33
I
I
100
3 32 4
45
0
0
0
0
Fig . 4 . Incidence of display of penile erection in the two display studies described in the text .
immature female, Frances . It is also to be emphasized that Edgar, the animal that remained peripheral to the group, displayed to none of the other males, whereas all displayed to him. Edgar displayed only to the observers or to other persons who entered the animal room . If displays to females were subtracted, the ranking order for displays would be Caspar,
38
ANIMAL BEHAVIOUR, XI,
Dwight, Bert and Edgar, and their respective ranking scores would be 10, 1, 0, 0 . Fig. 5 shows for comparison the incidence of display in the display, grooming, and distance studies. The fewer number of displays observed in the grooming and distance studies correlates with the shorter time of observation in these
where that would shed light on the findings pertaining to the feeding and display studies described here . In the wild they are said to feed in large aggregations (Sanderson 1957) . The failure of the feeding studies to show a clear distinction in dominance between the two high scoring animals possibly reflects some natural propensity for pairs or small numbers of animals within INCIDENCE OF DISPLAY IN VARIOU S STUDIES large groups to co-operate in getting food . In a subsequent communication the feeding PASSIVE PPARTICIPANTS PASSIVE PARTICIPANTS and display studies will be considered in the light of other E F G B C D B D E F G studies on grooming behaviour and propinquity factors B 0 2 t within groups . On the basis U B Iof the combined evidence, it 7 33 I I C 58 C may be concluded that obser32 4 D 6 0 vations on penile display give vations D w a better indication of hier0 0 E 0 0 E archy in the social structure archy IU of squirrel monkeys in capQ DISPLAY STUDIES GENERAL OBSERVATIONS tivity than does the outcome of rivalry for food . The bodily orientation of PASSIVE PA RTICIPANTS two squirrel monkeys during PASSIVE PARTICIPANTS 1penile display in the closed z Z D E F G G B C B C D E F position is somewhat suggestive of two dogs mutually 0 2 4 0 4 1 1 B 0 2 U B U smelling the genitalia, with I1= I 5 0 0 the important difference that8 X C 13 5 14 1 ir C -; in the monkey the emphasis 0 0 0 D 0 0 appears to be on visual rather 9 10 D 3 0 0 W W '~ than olfactory cues . In this 0 0 0 0 0 0 0 E E 0 0 0 1regard it is to be recalled I. . : •: U that the dog is guided to a Q Q DISTANC E STUDIES GROOMING STUDIES large extent by its olfactory sense whereas the monkey is dominated by its visual sense . Fig. 5 . Comparison of incidence of display noted in the display studies with The inference that vision plays that observed in the grooming and distance studies and duri ng the course of general observations . Consideration should be given only to th e relative values a key role in penile display ies . because the periods of observation varied in the different stud is supported by the fact that in mirror display olfactory cues are autostudies . In each case there was the like finding matically excluded . In brain stimulation studies that Caspar was unquestionably the most active on the representation of penile erection, animal in displaying to other males . The groomnodal points for erection have been found in ing and distance studies also confirmed the the medial septopreoptic region and in the original findings that none of the animals medial part of the medial dorsal nucleus displayed to Caspar, and that Edgar, the (MacLean & Ploog, 1962) . In ascending the apparent outcast, displayed to none of the other phylogenetic scale one finds in higher primates males . that the septum shows regressive changes whereDISCUSSION as the systems associated with the anterior and We know of no observations on squirrel medial thalamic nuclei increase in size and monkeys in their natural environment or elsereach their maximum development in man .
rz
a
a
a
a
PLOOG & MACLEAN : DISPLAY OF PENILE ERECTION IN SQUIRREL MONKEY
We have speculated that these changes may reflect a shifting emphasis from olfactory to visual influence in sociosexual behaviour (MacLean, 1962 ; MacLean & Ploog, 1962) . The pattern assumed by two monkeys during display, combined with the apparent emphasis on visual factors, would suggest that the squirrel monkey is a primate form representing an evolutionary "link" between the macrosmatic animal and the visually dominant animal. The finding that the squirrel monkey assumes the same posture for penile display in courtship and in aggression is of special phylogenetic interest in view of the fact that the courtship display of some male fishes and birds is indistinguishable from their aggressive posturing . The similarity between sexual and aggressive display becomes more understandable in the light of recent physiological studies which have shown that mechanisms for sexual and combative behaviour lie in close proximity in the brain stem and that excitation in one may spill over into the other (MacLean, 1959 ; 1962) . This is illustrated by brain stimulation studies on the cerebral representation of sexual functions in the squirrel monkey (MacLean & Ploog, 1962) . When stimulating in the hypothalamus one may pass within a millimetre from a point at which stimulation results in penile erection and an apparent state of placidity, to a point at which stimulation elicits erection in conjunction with angry or fearful vocalization and the showing of fangs . When the electrode is advanced a fraction of a millimetre further, only the signs of fear or anger appear during stimulation, but erection may occur as a rebound phenomenon after the termination of stimulation . There is also evidence that feeding mechanisms are closely allied to those underlying sexual and combative behaviour (MacLean, 1959 ; 1960) . This is not an unexpected finding inasmuch as fighting is frequently seen as a preliminary to both feeding and mating. Some evolutionary implications of the studies on penile display in regard to neuropsychiatric observations and to man's adoption of the loin cloth have been discussed elsewhere (MacLean, 1960) . SUMMARY In studies on the social behaviour of the squirrel monkey (Saimiri sciureus), it has been found that the male displays penile erection
39
under a variety of conditions. The types of display are described under the headings of (1) distant display, (2) mirror display, and (3) display in the communal situation . Distant display refers to the display that occurs between animals separated in cages . The same pattern of display occurs when a mirror is held up before a monkey (mirror display) . In the communal situation, the male may display penile erection to another male or to a female . Such displays are performed in what is described as the (i) open position and (ii) closed position . General observations suggested that a male may display to another male in the closed position as a means of exerting and establishing dominance. Special studies were undertaken to obtain measurements of dominance based on the outcome of rivalry for food and on display . The findings indicated that the observations based on penile display give a clearer indication of hierarchy in the social structure of squirrel monkeys in captivity than does the outcome of rivalry for food . Acknowledgments We wish to express our great appreciation to Dr . Samuel W . Greenhouse of the Biometrics Branch of the National Institute of Mental Health for his invaluable consultations in regard to statistical aspects of this study and for his statistical analysis of the results . We are much indebted to Mrs . Jean Cobb Blitz and Dr . Frauke Ploog for their help in making behavioural observations and analysing data . REFERENCES Carmichael, M . & MacLean, P. D. (1961) . Use of squirrel monkey for brain research, with description of restraining chair . EEG Clin. Neurophysiol., 13, 128-129 . MacLean, P . D . (1959) . The limbic system with respect to two basic life principles . In conference on the Central Nervous System and Behaviour, 2nd, 1959 . Transactions, New York Josiah Macy, Jr. Foundation, 1959, pp. 31-118 . MacLean, P . D . (1962) . New findings relevant to the evolution of psychosexual functions of the brain . J. nerv. ment . Dis ., 135, 289-301 . MacLean, P . D . & Ploog, D . W. (1962). Cerebral representation of penile erection . J. Neurophysiol., 25, 29-55 . Sanderson, 1 . T . (1957) . The monkey kingdom . Garden City, Hanover House, 200 pp . (Accepted for publication 7th May, 1962 Ms. number : 275) .