- Email: [email protected]
Evidence for seasonal variation in aggressive behaviour by Macaca mulatta
Anim. Behav ., 1970, 18, 719-724
EVIDENCE FOR SEASONAL VARIATION IN AGGRESSIVE BEHAVIOUR BY MACACA MULATTA BY
ANDREW P . WILSON & R . CHARLES BOELKINS*
Department of Psychiatry, Stanford University School of Medicine, Stanford, California 94305
There is widespread evidence for reproductive seasonality among diverse mammalian species . Although it was at one time postulated that certain nonhuman primates were acyclic (Zuckerman 1932), field studies have demonstrated the occurrence of breeding seasonality in many species . The early data showing reproductive seasonality in monkeys have been excellently reviewed by Lancaster & Lee (1965) . Since their article appeared there have been additional investigations whose results substantiate Lancaster & Lee's conclusions . Annual reproductive cycles have been reported by MacRoberts & MacRoberts (1966) for Macaca sylvana (the Barbary `ape') ; by Kawai, Azuma & Yoshiba (1967) for M. fuscata ; and for M. mulatta by Conaway & Koford (1965), Kaufmann (1965), Koford (1966), Lindburg (1967) and Vandenbergh & Vessey (1968) . Reports that the frequency of aggressive behaviours may also fluctuate seasonally have been made for rhesus monkeys by Kaufmann (1967), Lindburg (1967), Neville (1966), Sade (1966), Southwick, Beg & Siddiqi (1965) and Vandenbergh & Vessey (1968) . However, only Vandenbergh & Vessey (1968) report the percentages of males and females that were observed to be wounded during the mating season and the birth season . The Oregon troop of Japanese macaques (Alexander & Bowers 1968) appears also to display seasonally different patterns of aggressive behaviour, although generalisations from this troop must be made with caution since it is confined, natural troop fission is impossible, and population density is relatively high . The present paper reports distinct variations in the frequency of observed wounds and deaths for free-ranging, albeit captive, rhesus monkeys living on Cayo Santiago . Based on the best available evidence for the Cayo Santiago rhesus population, we have defined the mating season as that 5-month period beginning on 1 August and terminating 31 December . Correspondingly, the birth season
is defined as that 5-month period beginning 1 January and continuing through 30 May (Koford 1966) . The months of June and July form an interim period during which neither copulation nor parturition is likely to occur . These two 5-month `seasons' encompass about 90 per cent of the known births and an equivalent proportion of reproductively fertile matings . Clearly, any individual mating season may be precisely defined only retrospectively from the inclusive dates of the following birth season . Methods Cayo Santiago is a hilly, wooded 16-ha island located 1 km offshore from Playa de Humacao, Puerto Rico at latitude 18°09'N and longitude 65°44'W . The rhesus living there are all descendents of an original colony of about 400 animals imported from India and studied by Carpenter (1942) . In addition to the limited amounts of indigeneous foodstuffs, the monkeys had continuous access to six large food hoppers which were distributed about the island . The hoppers were filled to capacity three times a week with monkey chow so that food was available ad libitum. In addition to two rainwater catchment basins, water was piped to outlets at all of the feeders . During the dry season water was brought from the mainland, if necessary, to continue ad libitum availability. The island colony is now maintained under the auspices of the National Institutes of Health (Public Health Service, United States Department of Health, Education, and Welfare) . The data presented here were collected by the first author during over 1400 hr of direct observation made between July 1965 and August 1967 . Supplementary data were provided by Mr Angelo Figueroa who had primary responsibility for maintenance of the colony. Because of the size of the colony and difficulty in making perfectly accurate counts, a complete census of the population could be made only about once a month. In many cases an animal was not noticed as missing until as much as a month had elapsed from the probable time of death . It is likely that the recorded frequencies of wounds and
*Please address all reprint requests to R . C. Boelkins, Department of Psychiatry, Stanford University School of Medicine, Stanford, California, 94305, U .S .A . 719
720
ANIMAL BEHAVIOUR, 18,
4
Table I. Distribution by Age-Sex Class of all Animals Recorded during the Censuses of August 1965 and August 1967 on Cayo Santiago Females
Unsexed < 12 months
1-3 years
Males
4+ years
1-3 years
4+ years
Total
August 1965
122
123
153
96
85
579
August 1967
136
144
179
150
109
718
Median
129
133 .5
166
123
97
deaths for the months of July and August are slightly lower than the actual frequencies as a consequence of numerous interruptions and observational difficulties during those months . Table I gives the distribution of animals by age-sex classes for the censuses of August 1965 and August 1967, and shows the median number of individuals in each class for the 24-month period (Wilson 1968). Results Frequency of Wounding A wound was arbitrarily defined as any visible cut of approximately 4 cm length or
648 .5
longer. Such a definition is clearly restrictive in that the most serious wounds inflicted by adult males are those deep punctures, produced by the canine teeth, which are undetectable except by minute investigation . Similarly, the small cuts less than 4 cm in length, but equally likely to result in disabling infections, went unrecorded. Table II indicates the distribution of wounds and deaths on a month by month basis for both males and females . September proved to be the peak month for wounding of both sexes ; however, unlike the males, the females received many wounds during the birth season in February and March .
Table II. Distribution of Wounds and Deaths by Month in which First Observed Deaths
Wounds Females
Males
Females
Males
Birth 6
4
1
0
February
12
2
2
1
March
11
7
2
0
April
5
6
5
0
May
9
5
0
0
June
8
4
1
0
July
4
9
1
1
August
6
15
1
2
September
16
27
1
1
October
10
15
2
6
November
6
10
0
3
December
0
5
0
1
93
109
16
15
January
Interim
Mating
Total
WILSON & BOELKINS : SEASONAL VARIATION IN AGGRESSION
Significantly more wounds were incurred by males during the mating season than during the birth season or the interim period (x2 = 27 . 13, df = 2, P<0 . 001). While the monthly distribution of wounds incurred by females seems clearly related to reproductive seasonality, the difference in the frequency of wounding in the mating and birth seasons was not statistically significant (x2 = 1 . 27) . While slightly more females were wounded in the birth season than in the mating season, those wounds may have been caused by males protecting mother-infant pairs from over-zealous attention . Alternatively, the wounds may have been made by other females who, during late pregnancy, usually become irascible and short-tempered .
while no males died during the months of January, March, April, May and June . Comparison of observed frequencies of deaths as a function of the reproductive season (Table III) clearly reveals that deaths were seasonal. Even though 62 . 5 per cent of the female deaths occurred during the birth season, a chi-square test was not statistically significant . However, the 86 . 6 per cent of the male deaths that occurred during the mating season was significantly greater than would be expected if deaths were distributed equally throughout the 12 months of the year (x 2 = 12 . 60, df = 2, P<0 .01) . The high percentage of birth-season deaths for females can perhaps be attributed to complications developing during labour and the postpartum period, though this is admittedly conjectural . More precise data collection methods will be required to determine if there is a significant correlation between the incidence of wounds and deaths for females during the breeding season. It does seem clear that wounds and deaths are directly related for males : both categories peak during the mating season . Wilson (1968) tables the month in which the dead monkeys were assumed to have died . Using these data in conjunction with known birth year, one can calculate the age in months at death . (All individuals were assumed to have been born in the third month of their year of birth.) Males and females were not significantly
Frequency of Deaths An individual was assumed to have died when it did not appear in the monthly census records . Continued absence from the records was assumed to confirm the death even though the carcase may not have been located . Death was recorded only for animals bearing tatoos or those recognizable infants older than 3 months whose mother had been positively identified . That deaths did not occur on a random basis throughout the year is clearly revealed by the monthly distribution (Table II) . During the 24month study period, no females died during the months of May, November, or December ;
Table III. Observed and Expected (Italics) Freguendes of Womb and Deaths as a Function of Reproductive Season Females Obs.
721
Males
Exp. •
Obs.
Exp. •
Wounds Mating season
38
38 . 75
72
45.42
Birth season
43
38.75
24
45 .42
Interim
12
15 .50
13
18 . 17
Total
93
109
Deaths Mating season
4
6 . 67
13
6 . 25
Birth season
10
6.67
1
6 .25
Interim
2
2 . 67
1
2 . 50
Total
16
15
'Expected frequencies were calculated as equal to 5/12, 5/12, and 2/12 of the grand total for each sex, on the assumption that the probability of occurrence was the same for every month of the year.
722
ANIMAL BEHAVIOUR, 18, 4 Table IV. Observed and Expected (Italics) Frequencies of Deaths for Successive 3-year Age Classes within Each Sex Females Age (years)
Obs.
Exp . *
Males Obs .
Exp . *
Total
0-3
3
3 .09
3
2 . 90
6
4-6
6
5 . 67
5
5 . 32
11
7-9
1
1 . 55
2
1 . 45
3
10-12
4
3 .09
2
2. 90
6
13+
2
2 . 58
3
2.42
5
Total
16
15
*Expected frequencies in each cell were calculated as equal to
different in age at death (t = 0 . 23) . Of the sixteen females dying, the youngest was 6 months old and the oldest 185 months old with a mean age of 89 . 81 months (7 .48 years) . Of the fifteen males that died, the youngest was 4 months old and the oldest 188 months old ; mean age at death was 94 . 27 months (7 . 85 years) . Since deaths of untatooed infants and infants less than 3 months old were not included in the sample, the calculated mean ages at death are higher than would be found if infant mortality were included . While eleven of the thirty-one animals were between 4 and 6 years old (Table IV) there was no statistically significant relationship (x2=1 .26) between sex and age-class at death . It should be noted that animals more than 4 years old did suffer differential mortality as a function of sex . Of the median number of reproductively mature females (N=166), thirteen died, a mortality rate of 7 . 83 per cent . Of the median number of mature males (N=97), twelve animals died, a mortality rate of 12 . 37 per cent. These figures are reasonably consistent with Koford's (1966) calculations of 5 . 1 per cent and 8 . 8 per cent mortality for females and males, respectively, at least 4 years old . Discussion These data are clearly strong evidence for seasonally varying levels of aggressive behaviour in the male rhesus monkeys living in Cayo Santiago . The finding that wounds of at least 4 cm length occur most frequently during the mating season supports earlier reports of high levels of aggression and social instability during the fall reproductive period . While approximately equal numbers of each sex died during the
31
(row total) x (column total). grand total
period of study, males were most likely to die during the mating season while females were more likely to die during the birth season . In 1962 an island colony of free-ranging rhesus was established on LaCueva, off the south-west coast of Puerto Rico near La Parguera. During the 5-year period from 1962 through 1966 the colony was studied by Vandenbergh & Vessey (1968) . They found that the animals displayed both a well-defined birth season (74 per cent of the births occurred in May and June of each year), and a mating season extending from October through February (with a peak in November and December) . There too the incidence of visible wounds (dimensions were not reported) was significantly related to the reproductive cycle . For each of four (excluding the first year because of the social instability) mating-gestation-birth-interim cycles, males were wounded significantly more frequently (P<0 .05, chi-square test) during the mating season than during the birth season . During two of the yearly cycles, females also were wounded significantly more frequently (P<0 . 05) during the mating season . Those two cycles occurred in 1962 to 1963 and 1965 to 1966 which were the cycles having the highest percentage of males wounded. Over the four reproductive cycles the percentage of males wounded during the mating season was consistently twice as great as the percentage of females wounded . However, during the birth season the percentage of males bearing wounds was virtually the same as the females, never greater than 2 per cent more and in one case 1 . 6 per cent less . The highest relative frequencies of aggression
WILSON & BOELKINS : SEASONAL VARIATION IN AGGRESSION
(due to lower frequencies of nonagonistic behaviours) were reported (Kaufmann 1967) to occur during the interim period for male members of Group A on Cayo Santiago, while the absolute frequency of aggression was highest during the mating season . Thus, the data reported here support the earlier evidence given by Kaufmann (1967) and Vandenbergh & Vessey (1968) . At the present time the most plausible interpretation of the elevated frequencies of aggressive interactions during mating seasons is that they result indirectly from hormonal changes in sexually mature male monkeys . It has been assumed that mating seasonality in non-human primates is determined by the reproductive state of the sexually mature females within the group (Lancaster & Lee 1965) . There is now initial evidence, however, which suggests that sexually mature males also display reproductive seasonality. Sade (1964) reported seasonal variations in testis size of adult males on Cayo Santiago testes were larger during the fall breeding season than during the spring birth season . As a result of testis biopsies conducted on fifty-five adult males at different periods of the year, Conaway & Sade (1965) were able to report relative aspermatogenesis during the spring birth season and maximum spermatogenesis during the mating season . Changes in male reproductive physiology are not independent of female reproductive state, however . Vandenbergh (1969) has recently reported that ovariectomized female rhesus brought into oestrus (by treatment with oestradiol benzoate) during the interim period were able to stimulate sexually quiescent males. The males showed increases in testis size, seminiferous tubule diameter, and scrotal colouration . Sexual mounts and ejaculations were observed (with increasing day-to-day frequency) after but not before exogenous oestrogen was administered to the females . That some pheromone may be produced by sexually receptive females was evidenced by the altered frequency with which males came voluntarily to sit near the females' cages . Prior to administration of oestrodiol benzoate (25 gg per day for 8 days) free-ranging males spent 92 min near the cages, while after hormone treatment males spent 414 min adjacent to the cages within an equivalent time period. Michael (1968) has also offered evidence that pheromones may play a part in the sexual activity of rhesus monkeys . Knowing that there are significant increases
723
in the levels of circulating male hormones during the breeding season, one can postulate that the observed significant increases in frequency of aggressive behaviours are a consequence of the altered hormonal state . That androgens, and especially testosterone, are strongly implicated in the ontogenesis, the expression, and the control of aggressive behaviours in many mammalian species is no longer a debatable statement (Beach 1965) . However, the process by which altered hormonal states effect the observed behavioural changes is still undetermined . The most plausible hypothesis seems to be that there are changes in threshold levels for those stimuli which evoke aggressive responses . Unfortunately, there are no data comparable to those presented here for seasonality of aggression among species which are not notably seasonal in their reproductive activity (e .g. Papio spp.) . While the evidence is clear that for males more intra-specific aggression occurs during the mating than during the birth season among rhesus monkeys, it may also be true that rhesus males are especially sensitive to and respond aggressively to extra-specific threats during the birth season, thus providing greater protection for parturient females and newborn infants . Summary Observations were made on the Macaca mulatta colony on the island of Cayo Santiago over a period that included two reproductive cycles . The frequency of aggressive behaviour was found to fluctuate cyclically as a function of the colony's reproductive state . Males were wounded and died significantly more frequently during the mating season than at any other time of year . Females were wounded about as often during the mating season as during the birth season, and more died during the birth season than during the mating season, although not significantly so . There was no significant difference between sexes in age at death, nor was there a significant departure from expectation of number of deaths per age class. However, mortality among the reproductively mature males was greater than among mature females . It was suggested that differential injury and mortality rates among adult males might be an indirect result of high levels of androgens which could conceivably alter threshold levels for stimuli initiating severe aggressive interactions . Acknowledgments The research reported here was supported by
724
ANIMAL BEHAVIOUR, 18, 4
Public Health Service grants MH-08623, GM1224 and MH-8304. The Cayo Santiago primate colony is administered by the Laboratory of Perinatal Physiology, National Institute of Neurological Diseases and Blindness, National Institutes of Health, Public Health Service, United States Department of Health, Education, and Welfare ; San Juan, Puerto Rico . The authors wish to acknowledge the assistance of Mr Angelo Figueroa, Dr Ronald E . Myers, Dr John A . Morrison and Dr. Chester Swett of the Laboratory of Perinatal Physiology . We are indebted to Dr John H . Crook, Dr David A. Hamburg, Dr Thelma E . Rowell and Dr Sherwood L . Washburn for their critical readings of the manuscript. REFERENCES Alexander, B . K. & Bowers, J. M . (1968) . The social behavior of Japanese macaques in the corral . Primate News, 6, 3-10. Beach, F. A . (Ed.) (1965) . Sex and Behavior . New York : Wiley & Sons. Carpenter, C. R . (1942) . Sexual behavior in free-ranging rhesus monkeys. J. comp. Psychol., 33, 113-142 . Conaway, C. H . & Koford, C. B . (1965). Estrous cycles and mating behavior in a free-ranging band of rhesus monkeys. J. Mammal., 45, 577-588 . Conaway, C. H . & Sade, D. S. (1965) . The seasonal spermatogenic cycle in free ranging rhesus monkeys. Folia Primat., 3, 1-12. Kaufmann, J . H . (1965) . A three-year study of mating behavior in a free ranging band of rhesus monkeys . Ecology, 46, 500-512 . Kaufmann, J. H. (1967) . Social relations of adult males in a free-ranging band of rhesus monkeys . In : Social Communication among Primates (Ed . by S. A . Altmann), pp . 73-98 . Chicago : University of Chicago Press. Kawai, M., Azuma, S. & Yoshiba, K . (1967) . Ecological studies of reproduction in Japanese monkeys (Macaca fuscata) . I . Problems of the birth season . Primates, 8, 35-74 .
Koford, C . B . (1966). Population changes in rhesus monkeys : Cayo Santiago, 1960-1964. Tulane Stud. in Zool., 13, 1-7. Lancaster, J. B. & Lee, R . B . (1965) . The annual reproductive cycle in monkeys and apes . In : Primate Behavior : Field Studies of Monkeys and Apes (Ed. by I . DeVore), pp . 486-513 . New York, Holt, Rinehart & Winston. Lindburg, D . G . (1967). Patterns of reproduction in wild rhesus monkeys. Paper presented at A.A .A.S., New York. MacRoberts, M. H . & MacRoberts, B . R . (1966). The annual reproductive cycle of the Barbary ape (Macaca sylvana) in Gibralter. Am . J. phys . Anthrop ., 25, 299-304 . Michael, R. P . (1968) . Pheromones in the communication of sexual status in primates . Nature, Lond., 218, 746-749 . Neville, M . K. (1966) . A study of the free-ranging behavior of rhesus monkeys . Harvard University Ph .D . thesis, unpublished . Sade, D . S . (1964) . Seasonal cycle in size of testes of freeranging Macaca mulatta. Folia Primat., 2, 171180 . Sade, D. S. (1966) . Ontogeny of social relations in a freeranging group of rhesus monkeys . University of California (Berkeley) Ph .D . thesis, unpublished . Southwick, C. H., Beg, M . A . & Siddiqi, M . R. (1965). Rhesus monkeys in north India. In : Primate Behavior : Field Studies of Monkeys and Apes (Ed . by I . DeVore), pp . 111-159. New York : Holt, Rinehart & Winston . Vandenbergh, J . G. (1969). Endocrine coordination in monkeys : Male sexual response to the female . Physiol. & Behav., 4, 261-264 . Vandenbergh, J. G . & Vessey, S . (1968) . Seasonal breeding of free-ranging rhesus monkeys and related ecological factors . J. reprod. Fert ., 15, 71-79. Wilson, A . P . (1968). Behavior of free-ranging rhesus monkeys with an emphasis on aggression . University of California (Berkeley) Ph .D . thesis, unpublished . Zuckerman, S . (1932) . The Social Life of Monkeys and Apes. London : Kegan Paul. (Received 22 October 1969 ; revised 22 April 1970 ; MS. number : A904)
EVIDENCE FOR SEASONAL VARIATION IN AGGRESSIVE BEHAVIOUR BY MACACA MULATTA BY
ANDREW P . WILSON & R . CHARLES BOELKINS*
Department of Psychiatry, Stanford University School of Medicine, Stanford, California 94305
There is widespread evidence for reproductive seasonality among diverse mammalian species . Although it was at one time postulated that certain nonhuman primates were acyclic (Zuckerman 1932), field studies have demonstrated the occurrence of breeding seasonality in many species . The early data showing reproductive seasonality in monkeys have been excellently reviewed by Lancaster & Lee (1965) . Since their article appeared there have been additional investigations whose results substantiate Lancaster & Lee's conclusions . Annual reproductive cycles have been reported by MacRoberts & MacRoberts (1966) for Macaca sylvana (the Barbary `ape') ; by Kawai, Azuma & Yoshiba (1967) for M. fuscata ; and for M. mulatta by Conaway & Koford (1965), Kaufmann (1965), Koford (1966), Lindburg (1967) and Vandenbergh & Vessey (1968) . Reports that the frequency of aggressive behaviours may also fluctuate seasonally have been made for rhesus monkeys by Kaufmann (1967), Lindburg (1967), Neville (1966), Sade (1966), Southwick, Beg & Siddiqi (1965) and Vandenbergh & Vessey (1968) . However, only Vandenbergh & Vessey (1968) report the percentages of males and females that were observed to be wounded during the mating season and the birth season . The Oregon troop of Japanese macaques (Alexander & Bowers 1968) appears also to display seasonally different patterns of aggressive behaviour, although generalisations from this troop must be made with caution since it is confined, natural troop fission is impossible, and population density is relatively high . The present paper reports distinct variations in the frequency of observed wounds and deaths for free-ranging, albeit captive, rhesus monkeys living on Cayo Santiago . Based on the best available evidence for the Cayo Santiago rhesus population, we have defined the mating season as that 5-month period beginning on 1 August and terminating 31 December . Correspondingly, the birth season
is defined as that 5-month period beginning 1 January and continuing through 30 May (Koford 1966) . The months of June and July form an interim period during which neither copulation nor parturition is likely to occur . These two 5-month `seasons' encompass about 90 per cent of the known births and an equivalent proportion of reproductively fertile matings . Clearly, any individual mating season may be precisely defined only retrospectively from the inclusive dates of the following birth season . Methods Cayo Santiago is a hilly, wooded 16-ha island located 1 km offshore from Playa de Humacao, Puerto Rico at latitude 18°09'N and longitude 65°44'W . The rhesus living there are all descendents of an original colony of about 400 animals imported from India and studied by Carpenter (1942) . In addition to the limited amounts of indigeneous foodstuffs, the monkeys had continuous access to six large food hoppers which were distributed about the island . The hoppers were filled to capacity three times a week with monkey chow so that food was available ad libitum. In addition to two rainwater catchment basins, water was piped to outlets at all of the feeders . During the dry season water was brought from the mainland, if necessary, to continue ad libitum availability. The island colony is now maintained under the auspices of the National Institutes of Health (Public Health Service, United States Department of Health, Education, and Welfare) . The data presented here were collected by the first author during over 1400 hr of direct observation made between July 1965 and August 1967 . Supplementary data were provided by Mr Angelo Figueroa who had primary responsibility for maintenance of the colony. Because of the size of the colony and difficulty in making perfectly accurate counts, a complete census of the population could be made only about once a month. In many cases an animal was not noticed as missing until as much as a month had elapsed from the probable time of death . It is likely that the recorded frequencies of wounds and
*Please address all reprint requests to R . C. Boelkins, Department of Psychiatry, Stanford University School of Medicine, Stanford, California, 94305, U .S .A . 719
720
ANIMAL BEHAVIOUR, 18,
4
Table I. Distribution by Age-Sex Class of all Animals Recorded during the Censuses of August 1965 and August 1967 on Cayo Santiago Females
Unsexed < 12 months
1-3 years
Males
4+ years
1-3 years
4+ years
Total
August 1965
122
123
153
96
85
579
August 1967
136
144
179
150
109
718
Median
129
133 .5
166
123
97
deaths for the months of July and August are slightly lower than the actual frequencies as a consequence of numerous interruptions and observational difficulties during those months . Table I gives the distribution of animals by age-sex classes for the censuses of August 1965 and August 1967, and shows the median number of individuals in each class for the 24-month period (Wilson 1968). Results Frequency of Wounding A wound was arbitrarily defined as any visible cut of approximately 4 cm length or
648 .5
longer. Such a definition is clearly restrictive in that the most serious wounds inflicted by adult males are those deep punctures, produced by the canine teeth, which are undetectable except by minute investigation . Similarly, the small cuts less than 4 cm in length, but equally likely to result in disabling infections, went unrecorded. Table II indicates the distribution of wounds and deaths on a month by month basis for both males and females . September proved to be the peak month for wounding of both sexes ; however, unlike the males, the females received many wounds during the birth season in February and March .
Table II. Distribution of Wounds and Deaths by Month in which First Observed Deaths
Wounds Females
Males
Females
Males
Birth 6
4
1
0
February
12
2
2
1
March
11
7
2
0
April
5
6
5
0
May
9
5
0
0
June
8
4
1
0
July
4
9
1
1
August
6
15
1
2
September
16
27
1
1
October
10
15
2
6
November
6
10
0
3
December
0
5
0
1
93
109
16
15
January
Interim
Mating
Total
WILSON & BOELKINS : SEASONAL VARIATION IN AGGRESSION
Significantly more wounds were incurred by males during the mating season than during the birth season or the interim period (x2 = 27 . 13, df = 2, P<0 . 001). While the monthly distribution of wounds incurred by females seems clearly related to reproductive seasonality, the difference in the frequency of wounding in the mating and birth seasons was not statistically significant (x2 = 1 . 27) . While slightly more females were wounded in the birth season than in the mating season, those wounds may have been caused by males protecting mother-infant pairs from over-zealous attention . Alternatively, the wounds may have been made by other females who, during late pregnancy, usually become irascible and short-tempered .
while no males died during the months of January, March, April, May and June . Comparison of observed frequencies of deaths as a function of the reproductive season (Table III) clearly reveals that deaths were seasonal. Even though 62 . 5 per cent of the female deaths occurred during the birth season, a chi-square test was not statistically significant . However, the 86 . 6 per cent of the male deaths that occurred during the mating season was significantly greater than would be expected if deaths were distributed equally throughout the 12 months of the year (x 2 = 12 . 60, df = 2, P<0 .01) . The high percentage of birth-season deaths for females can perhaps be attributed to complications developing during labour and the postpartum period, though this is admittedly conjectural . More precise data collection methods will be required to determine if there is a significant correlation between the incidence of wounds and deaths for females during the breeding season. It does seem clear that wounds and deaths are directly related for males : both categories peak during the mating season . Wilson (1968) tables the month in which the dead monkeys were assumed to have died . Using these data in conjunction with known birth year, one can calculate the age in months at death . (All individuals were assumed to have been born in the third month of their year of birth.) Males and females were not significantly
Frequency of Deaths An individual was assumed to have died when it did not appear in the monthly census records . Continued absence from the records was assumed to confirm the death even though the carcase may not have been located . Death was recorded only for animals bearing tatoos or those recognizable infants older than 3 months whose mother had been positively identified . That deaths did not occur on a random basis throughout the year is clearly revealed by the monthly distribution (Table II) . During the 24month study period, no females died during the months of May, November, or December ;
Table III. Observed and Expected (Italics) Freguendes of Womb and Deaths as a Function of Reproductive Season Females Obs.
721
Males
Exp. •
Obs.
Exp. •
Wounds Mating season
38
38 . 75
72
45.42
Birth season
43
38.75
24
45 .42
Interim
12
15 .50
13
18 . 17
Total
93
109
Deaths Mating season
4
6 . 67
13
6 . 25
Birth season
10
6.67
1
6 .25
Interim
2
2 . 67
1
2 . 50
Total
16
15
'Expected frequencies were calculated as equal to 5/12, 5/12, and 2/12 of the grand total for each sex, on the assumption that the probability of occurrence was the same for every month of the year.
722
ANIMAL BEHAVIOUR, 18, 4 Table IV. Observed and Expected (Italics) Frequencies of Deaths for Successive 3-year Age Classes within Each Sex Females Age (years)
Obs.
Exp . *
Males Obs .
Exp . *
Total
0-3
3
3 .09
3
2 . 90
6
4-6
6
5 . 67
5
5 . 32
11
7-9
1
1 . 55
2
1 . 45
3
10-12
4
3 .09
2
2. 90
6
13+
2
2 . 58
3
2.42
5
Total
16
15
*Expected frequencies in each cell were calculated as equal to
different in age at death (t = 0 . 23) . Of the sixteen females dying, the youngest was 6 months old and the oldest 185 months old with a mean age of 89 . 81 months (7 .48 years) . Of the fifteen males that died, the youngest was 4 months old and the oldest 188 months old ; mean age at death was 94 . 27 months (7 . 85 years) . Since deaths of untatooed infants and infants less than 3 months old were not included in the sample, the calculated mean ages at death are higher than would be found if infant mortality were included . While eleven of the thirty-one animals were between 4 and 6 years old (Table IV) there was no statistically significant relationship (x2=1 .26) between sex and age-class at death . It should be noted that animals more than 4 years old did suffer differential mortality as a function of sex . Of the median number of reproductively mature females (N=166), thirteen died, a mortality rate of 7 . 83 per cent . Of the median number of mature males (N=97), twelve animals died, a mortality rate of 12 . 37 per cent. These figures are reasonably consistent with Koford's (1966) calculations of 5 . 1 per cent and 8 . 8 per cent mortality for females and males, respectively, at least 4 years old . Discussion These data are clearly strong evidence for seasonally varying levels of aggressive behaviour in the male rhesus monkeys living in Cayo Santiago . The finding that wounds of at least 4 cm length occur most frequently during the mating season supports earlier reports of high levels of aggression and social instability during the fall reproductive period . While approximately equal numbers of each sex died during the
31
(row total) x (column total). grand total
period of study, males were most likely to die during the mating season while females were more likely to die during the birth season . In 1962 an island colony of free-ranging rhesus was established on LaCueva, off the south-west coast of Puerto Rico near La Parguera. During the 5-year period from 1962 through 1966 the colony was studied by Vandenbergh & Vessey (1968) . They found that the animals displayed both a well-defined birth season (74 per cent of the births occurred in May and June of each year), and a mating season extending from October through February (with a peak in November and December) . There too the incidence of visible wounds (dimensions were not reported) was significantly related to the reproductive cycle . For each of four (excluding the first year because of the social instability) mating-gestation-birth-interim cycles, males were wounded significantly more frequently (P<0 .05, chi-square test) during the mating season than during the birth season . During two of the yearly cycles, females also were wounded significantly more frequently (P<0 . 05) during the mating season . Those two cycles occurred in 1962 to 1963 and 1965 to 1966 which were the cycles having the highest percentage of males wounded. Over the four reproductive cycles the percentage of males wounded during the mating season was consistently twice as great as the percentage of females wounded . However, during the birth season the percentage of males bearing wounds was virtually the same as the females, never greater than 2 per cent more and in one case 1 . 6 per cent less . The highest relative frequencies of aggression
WILSON & BOELKINS : SEASONAL VARIATION IN AGGRESSION
(due to lower frequencies of nonagonistic behaviours) were reported (Kaufmann 1967) to occur during the interim period for male members of Group A on Cayo Santiago, while the absolute frequency of aggression was highest during the mating season . Thus, the data reported here support the earlier evidence given by Kaufmann (1967) and Vandenbergh & Vessey (1968) . At the present time the most plausible interpretation of the elevated frequencies of aggressive interactions during mating seasons is that they result indirectly from hormonal changes in sexually mature male monkeys . It has been assumed that mating seasonality in non-human primates is determined by the reproductive state of the sexually mature females within the group (Lancaster & Lee 1965) . There is now initial evidence, however, which suggests that sexually mature males also display reproductive seasonality. Sade (1964) reported seasonal variations in testis size of adult males on Cayo Santiago testes were larger during the fall breeding season than during the spring birth season . As a result of testis biopsies conducted on fifty-five adult males at different periods of the year, Conaway & Sade (1965) were able to report relative aspermatogenesis during the spring birth season and maximum spermatogenesis during the mating season . Changes in male reproductive physiology are not independent of female reproductive state, however . Vandenbergh (1969) has recently reported that ovariectomized female rhesus brought into oestrus (by treatment with oestradiol benzoate) during the interim period were able to stimulate sexually quiescent males. The males showed increases in testis size, seminiferous tubule diameter, and scrotal colouration . Sexual mounts and ejaculations were observed (with increasing day-to-day frequency) after but not before exogenous oestrogen was administered to the females . That some pheromone may be produced by sexually receptive females was evidenced by the altered frequency with which males came voluntarily to sit near the females' cages . Prior to administration of oestrodiol benzoate (25 gg per day for 8 days) free-ranging males spent 92 min near the cages, while after hormone treatment males spent 414 min adjacent to the cages within an equivalent time period. Michael (1968) has also offered evidence that pheromones may play a part in the sexual activity of rhesus monkeys . Knowing that there are significant increases
723
in the levels of circulating male hormones during the breeding season, one can postulate that the observed significant increases in frequency of aggressive behaviours are a consequence of the altered hormonal state . That androgens, and especially testosterone, are strongly implicated in the ontogenesis, the expression, and the control of aggressive behaviours in many mammalian species is no longer a debatable statement (Beach 1965) . However, the process by which altered hormonal states effect the observed behavioural changes is still undetermined . The most plausible hypothesis seems to be that there are changes in threshold levels for those stimuli which evoke aggressive responses . Unfortunately, there are no data comparable to those presented here for seasonality of aggression among species which are not notably seasonal in their reproductive activity (e .g. Papio spp.) . While the evidence is clear that for males more intra-specific aggression occurs during the mating than during the birth season among rhesus monkeys, it may also be true that rhesus males are especially sensitive to and respond aggressively to extra-specific threats during the birth season, thus providing greater protection for parturient females and newborn infants . Summary Observations were made on the Macaca mulatta colony on the island of Cayo Santiago over a period that included two reproductive cycles . The frequency of aggressive behaviour was found to fluctuate cyclically as a function of the colony's reproductive state . Males were wounded and died significantly more frequently during the mating season than at any other time of year . Females were wounded about as often during the mating season as during the birth season, and more died during the birth season than during the mating season, although not significantly so . There was no significant difference between sexes in age at death, nor was there a significant departure from expectation of number of deaths per age class. However, mortality among the reproductively mature males was greater than among mature females . It was suggested that differential injury and mortality rates among adult males might be an indirect result of high levels of androgens which could conceivably alter threshold levels for stimuli initiating severe aggressive interactions . Acknowledgments The research reported here was supported by
724
ANIMAL BEHAVIOUR, 18, 4
Public Health Service grants MH-08623, GM1224 and MH-8304. The Cayo Santiago primate colony is administered by the Laboratory of Perinatal Physiology, National Institute of Neurological Diseases and Blindness, National Institutes of Health, Public Health Service, United States Department of Health, Education, and Welfare ; San Juan, Puerto Rico . The authors wish to acknowledge the assistance of Mr Angelo Figueroa, Dr Ronald E . Myers, Dr John A . Morrison and Dr. Chester Swett of the Laboratory of Perinatal Physiology . We are indebted to Dr John H . Crook, Dr David A. Hamburg, Dr Thelma E . Rowell and Dr Sherwood L . Washburn for their critical readings of the manuscript. REFERENCES Alexander, B . K. & Bowers, J. M . (1968) . The social behavior of Japanese macaques in the corral . Primate News, 6, 3-10. Beach, F. A . (Ed.) (1965) . Sex and Behavior . New York : Wiley & Sons. Carpenter, C. R . (1942) . Sexual behavior in free-ranging rhesus monkeys. J. comp. Psychol., 33, 113-142 . Conaway, C. H . & Koford, C. B . (1965). Estrous cycles and mating behavior in a free-ranging band of rhesus monkeys. J. Mammal., 45, 577-588 . Conaway, C. H . & Sade, D. S. (1965) . The seasonal spermatogenic cycle in free ranging rhesus monkeys. Folia Primat., 3, 1-12. Kaufmann, J . H . (1965) . A three-year study of mating behavior in a free ranging band of rhesus monkeys . Ecology, 46, 500-512 . Kaufmann, J. H. (1967) . Social relations of adult males in a free-ranging band of rhesus monkeys . In : Social Communication among Primates (Ed . by S. A . Altmann), pp . 73-98 . Chicago : University of Chicago Press. Kawai, M., Azuma, S. & Yoshiba, K . (1967) . Ecological studies of reproduction in Japanese monkeys (Macaca fuscata) . I . Problems of the birth season . Primates, 8, 35-74 .
Koford, C . B . (1966). Population changes in rhesus monkeys : Cayo Santiago, 1960-1964. Tulane Stud. in Zool., 13, 1-7. Lancaster, J. B. & Lee, R . B . (1965) . The annual reproductive cycle in monkeys and apes . In : Primate Behavior : Field Studies of Monkeys and Apes (Ed. by I . DeVore), pp . 486-513 . New York, Holt, Rinehart & Winston. Lindburg, D . G . (1967). Patterns of reproduction in wild rhesus monkeys. Paper presented at A.A .A.S., New York. MacRoberts, M. H . & MacRoberts, B . R . (1966). The annual reproductive cycle of the Barbary ape (Macaca sylvana) in Gibralter. Am . J. phys . Anthrop ., 25, 299-304 . Michael, R. P . (1968) . Pheromones in the communication of sexual status in primates . Nature, Lond., 218, 746-749 . Neville, M . K. (1966) . A study of the free-ranging behavior of rhesus monkeys . Harvard University Ph .D . thesis, unpublished . Sade, D . S . (1964) . Seasonal cycle in size of testes of freeranging Macaca mulatta. Folia Primat., 2, 171180 . Sade, D. S. (1966) . Ontogeny of social relations in a freeranging group of rhesus monkeys . University of California (Berkeley) Ph .D . thesis, unpublished . Southwick, C. H., Beg, M . A . & Siddiqi, M . R. (1965). Rhesus monkeys in north India. In : Primate Behavior : Field Studies of Monkeys and Apes (Ed . by I . DeVore), pp . 111-159. New York : Holt, Rinehart & Winston . Vandenbergh, J . G. (1969). Endocrine coordination in monkeys : Male sexual response to the female . Physiol. & Behav., 4, 261-264 . Vandenbergh, J. G . & Vessey, S . (1968) . Seasonal breeding of free-ranging rhesus monkeys and related ecological factors . J. reprod. Fert ., 15, 71-79. Wilson, A . P . (1968). Behavior of free-ranging rhesus monkeys with an emphasis on aggression . University of California (Berkeley) Ph .D . thesis, unpublished . Zuckerman, S . (1932) . The Social Life of Monkeys and Apes. London : Kegan Paul. (Received 22 October 1969 ; revised 22 April 1970 ; MS. number : A904)