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Male-male and female-female courtship and copulation behaviour in a communally breeding bird
Short Communications Department o f Zoology, Tel-Aviv University, Ramat Aviv 69978, Israel. * Department of Psychology, University o f Pennsylvania, Philadelphia, PA 19104, U.S.A. References Hartline, P. H. 1971. Physiological basis for detection of sound and vibration in snakes. J. exp. Biol., 54, 349 371. Lewis, E. R. & Marins, P. M. 1985. Do frogs communicate with seismic signals? Science, N. }1., 227, 187 189. Liu, H. P., Anderson, D. L. & Kanamori, H. 1976. Velocity dispersion due to inelasticity; implication for seismology and mantle composition. Geophys..L R. Astronom. Soc., 47, 41 58. MacDonald, D. (Ed.) 1985. The Encyclopedia (~f Mammals. Vol. 2. London: George Allen & Unwin. Nevo, E. 1961. Observation on Israeli populations of the mole rat. Mammalia, 25, 127-144, Randall, J. A. 1984. Territorial defence and advertisement by footdrumming in bannertail kangaroo rats (Dipodomys spectabilis) at high and low population densities. Behav. Ecol. Sociobiol., 16, 11-20. Swanson, H. H. 1974. Sex differences in behaviour of the Mongolian gerbil (Meriones unguiculatus) in encounters between pairs of the same or opposite sex. Anita. Behav., 22, 638-644. (Received 13 November 1986,"revised5 January 1987; MS. number." sc-345)
Male-Male and Female-Female Courtship and Copulation Behaviour in a Communally Breeding Bird Interpreting sexual behaviour between males and females in group-living organisms seems relatively straightforward compared to interpreting that seen during encounters between individuals of the same sex. The latter interactions immediately raise a number of questions including what are the causes and consequences of such behaviour. However, interpreting the function of behaviour should not be done without regard for the context in which it occurred. Courtship or mounting behaviour is just one behavioural link in a series of events that precede and follow it (Hanby 1974). In a recent study of the communally breeding pukeko, Porphyrio porphyrio, we recorded several instances of male male and female-female courtship and copulations. The purpose of this paper is to document and analyse these interactions in relation to the behavioural context in which they
1251
occurred in an attempt to gain a better understanding of this unusual behaviour. The pukeko is a gallinule which lives in groups of two seven breeding males, two breeding females, who lay their eggs in a single nest, and as many as seven non-breeding birds who are offspring from previous matings. The study was carried out in Shakespear Regional Park approximately 25 km north of Auckland, New Zealand. Birds were colour-banded for individual recognition, and dominance status was determined independently of mounting behaviour. There was no relation between differences in the number of mountings observed between groups and observation time. Before analysing observations on interactions between pukeko of the same sex, we must give a brief description of mating behaviour between males and females (for a more detailed account plus illustrations see Craig 1977). Mating behaviour can be divided into three sequential components. First, a male approaches a female in a 'sexual upright' posture and follows behind her, giving a loud 'humming' call. As many as five other males may join in and pursue the female at this time. Second, if the female responds to the male's initial courting behaviour, she will stop and assume a precopulatory 'hunched' position after which the male will step onto the female's back. Third, the female raises her tail as the male attains cloacal contact and ejaculation. What we term as male-male or femalefemale 'sexual' interactions is behavioural activity that is indistinguishable to that described above except that the participants are of the same sex. It can include all three components or any part of the behavioural sequence. During 174 h of observation over a period of 3 years, 555 heterosexual interactions were recorded, compared to 41 homosexual interactions (12 male-male, 29 female-female). D o m i n a n t males clearly initiated the 12 m a l e male interactions. In two of these, dominant males approached subordinates in a 'sexual upright' posture and attempted to mount them. However, in the other 10 interactions which occurred during male female courtship activity, the alpha male ran in front of the other courting males and assumed a 'hunched' position. The subordinate males immediately stopped pursuing the female and mounted the alpha male; three of these resulted in birds making cloacal contact in the same manner as in male-female copulations. However, these interactions were confined to only a few individuals. Three of the nine alpha males initiated nine (five, two, two) of the 10 interactions. Male male sexual interactions occurred only in groups with four or more breeding males: groups in which mating interactions were most intense (Jamieson & Craig, in press). The alpha male
1252
Animal Behaviour, 35, 4
behaving functionally like a female results in a and females commenced almost 2 months beforeredirection of sexual activity of the other breeding hand. Could female-female interactions be somemales in a group during a male-female mating how related to alpha females regulating the number of eggs laid in the communal nest? attempt. Although this type of behaviour appears to be linked to sexual competition, other research Egg-tossing behaviour, which has the effect of has shown that dominant males are just as likely to biasing the total number of eggs that each female ignore totally a mating involving a subordinate as contributes to the final clutch, has been described in they are to interrupt it (Jamieson & Craig, in press). other polygynandrously breeding birds (e.g. This was true for both the prelaying and laying Mumme et al. 1983; Vehrencamp et al. 1986), but periods. These observations, added to the fact that does not occur in pukeko. In addition, aggressive only a few alpha males initiated male rnale mount- interactions between breeding females within pukings, suggest that attaching any adaptive signifi- eko groups are rare. Nevertheless, the alpha female cance to the behaviour would be difficult and usually lays at least one more egg and contributes unwarranted. The 'hunched' posture is more com- to more clutches than the beta female (Craig 1980). monly exhibited by males during territorial dis- However, we have been unable to tease apart the putes (see Craig 1977), and appears to be involved effects that age, experience and dominance have on in reducing aggression between territorial males an individual's egg production. It should also be after they have interacted. It may be that a few remembered that although the difference in the individuals have developed a tendency to display number of eggs laid by alpha and beta females is this stereotyped posture during courtship interac- found among most breeding groups, female tions which involve other males from within their female courtship and copulations were relatively group. rare and confined to only a few individuals. Most of the instances of female-female courtship Therefore, homosexual behaviour by alpha females and copulations (26 of 29) also involved only a few does not appear to be necessary to produce the bias individuals (I0, 9, 4, 3). As with alpha males, it was . in egg production and by itself is of doubtful the alpha female who initiated the homosexual adaptive significance. However, the lack of overt interactions. Unlike alpha males (10 of 12), the aggression among breeding females as well as males alpha female behaved functionally like a male, during reproductive competition is in keeping with approaching in a 'sexual upright' posture, mount- the pukeko's highly developed social system and ing and copulating with another female in her appears to be essential for the maintenance of a group. In addition, all interactions involved only breeding territory (Craig 1984). alpha and beta females even though most groups We would like to thank Ed Minot and two had one or two additional non-breeding females. anonymous referees for their comments on the Female-female interactions occurred in three manuscript. Finance for the research was provided types of situations. On three occasions all involving by New Zealand University Grants Committee and the same individual, a female apparently tried to the University of Auckland. evade several courting males who were chasing her by running towards the other breeding female in 1AN G. JAM1ESON the group and assuming a 'sexual upright' posture. JOHN L. CRAIG The effect of this behaviour was that the males Department of Zoology, stopped pursuing her and began courting the other University of Auckland, female. Auckland, New Zealand. The remaining 26 interactions were of a different nature. On 17 occasions an alpha female approached a beta female, who was alone at the References time, assumed a 'sexual upright' posture, gave a Craig, J. L. 1977. The behaviour of the pukeko. N.Z.J. precopulatory call, and proceeded to mount the Zool., 4, 413~33. beta. In nine other instances, the alpha female ran Craig, J. L. 1980. Breeding success of a communal gallinule. Behav. Ecol. Sociobiol., 6, 289-295. towards the beta and assumed a 'sexual upright' posture after one or more males had initiated Craig, J. L. 1984. Are pukeko caught in a prisoner's dilemma? Behav. Ecol. SociobioL, 14, 147-150. courtship behaviour with the beta female. In the Hanby, J. P. 1974. Male-male mounting in Japancse latter cases the alpha female ran in fi'ont of the monkeys, Macaca fizscata. Anim. Behav., 22, 836~849, males and mounted the beta female. In total, six of Jamieson, 1. G. & Craig, J. L. In press. Dominance and the mountings resulted in cloacal contact. mating in a communal polygynandrous bird: cooperAll 26 interactions of the type described above ation or indifference towards mating competitors? occurred just prior to or during egg laying even Ethology. though courtship and copulations between males Mumme, R. L., Koenig, W. D. & Pitelka, F. A. 1983.
Short Communications
Reproductive competition in the communal acorn woodpecker: sisters destroy each other's eggs. Nature, Lond., 306, 583-584. Vehrencamp, S., Bowen, B. S. & Koford, R. R. 1986. Breeding roles and pairing patterns within communal groups of groove-billed anis. Anim. Behav., 34, 347367. (Received 18 August 1986; revised 27 October 1986," MS. number." sc-331)
Partial Mortality in Nestling Meadow Voles, Microtus pennsylvanicus
Nestling mortality is important in theories concerning population regulation and life history, but is poorly measured in small mammal populations. Nestling mortality in microtine rodents has been divided into two types: whole and partial loss of the litter (Hoffmann 1958). Whole litter loss was thought to result from predation or the death of the mother prior to weaning of the litter. Partial litter loss was described as the result of the inherent physiological weaknesses of some pups. Infanticide by neighbouring adults (Mallory & Brooks 1978) and maternal manipulation of litters (McClure 1981) should also be considered as possible sources of litter loss. These causative factors can be investigated by studying the survivorship of nestlings. The purpose of this study was to look for nestling mortality, and possible patterns of selective mortality, in a natural population. A 0.63 ha trapping grid was set up within a 100 ha field in Brackney, Pennsylvania, 25 km south of Binghamton, New York. Live-trapping was conducted 1 day a week over four periods during 1983 and 1984 (3 M a r c h - 6 July and 26 A u g u s t 8 November in 1983; 23 March-10 July and 18 August-25 October in 1984). For the remainder of both years, trapping was conducted monthly. We will refer to the period of weekly trapping as 'spring' and 'autumn'. Trap stations were placed at 10-m intervals, and two live-traps were placed at each station. All stations were pre-baited 1 day before being checked every 2 h over a 10-h period. Captured animals were weighed, sexed, uniquely marked (toe-clipped), and checked for reproductive condition. The maternal weight of the female, for each litter located, was considered the weight at first capture after parturition. Weekly, during the spring and autumn period, 15-20 females were radiotracked for 10 h (for implant and tracking techniques, see Madison et al. 1985). The located nests of lactating females were opened and the pups removed for examination. The pups were uniquely marked (toe-clipped), weighed, counted and their anal-genital length
1253
recorded. Pups were returned to the nest within 5 min of removal. The process of locating the natal nest did not appear to disturb the care-giving behaviour of the females, as mothers with undisturbed nests, in other studies, exhibited similar patterns of nest visitation (Madison 1981). However, entering the nest did cause some temporary stress, as every nest examined resulted in the mother transferring the pups to a new nest. We maintain that the level of disturbance was not extreme, since (1) no litters were abandoned after nest examination; (2) females often moved nests after natural disturbances (i.e. heavy rainfalls); (3) field-captured females that gave birth in the laboratory (N= 14) exhibited no infanticide in response to having their pups handled in a similar fashion. For 36 litters, we were able to relocate and examine the pups 4-9 days following their initial examination. All re-examined litters were of pups prior to eye-opening, and therefore under complete care by the mother. Pup growth is linear over this period, with no significant sexual dimorphism in the pups (Innes & Millar 1979). For those litters in which some mortality occurred between nest checks (N= 16), the following traits were recorded: two measures of population density at the time of parturition (a global estimate based on the total number of animals captured and a local estimate based on the number of animals captured within a radius of two home ranges (approximately 30 m) of the animal), the mass of pups and the mother, the number of pups in the litter, the period of time between checks, and, based on the pup's weight, a relative rank within the litter. Fluctuations in recruitment over the study period did not appear to be due to changes in dispersal, as the minimum trappability of the juveniles (N=484) did not change significantly from spring to autumn (54 and 55%, respectively; calculated according to Hilborn et al. 1976), and the mean weight for marked juveniles at first capture did not differ from spring to autumn (J? = 17.8 g and 17.6 g respectively, t = 0.9, P > 0.1). Of the 635 pups marked over the course of the study, 153 (24%) later entered the trappable population. Entry of an entire litter into the trappable population occurred in only eight of 131 (6%) litters, but the litters contributing at least a single pup varied seasonally from 40 to 78% (Table I). Partial recruitment of a litter may be due to partial dispersal of the litter, or partial survival of the litter prior to dispersal. If mortality plays a role in the partial recruitment observed (and the mortality occurs prior to weaning), then the size of the located litters should be negatively correlated with
Male-Male and Female-Female Courtship and Copulation Behaviour in a Communally Breeding Bird Interpreting sexual behaviour between males and females in group-living organisms seems relatively straightforward compared to interpreting that seen during encounters between individuals of the same sex. The latter interactions immediately raise a number of questions including what are the causes and consequences of such behaviour. However, interpreting the function of behaviour should not be done without regard for the context in which it occurred. Courtship or mounting behaviour is just one behavioural link in a series of events that precede and follow it (Hanby 1974). In a recent study of the communally breeding pukeko, Porphyrio porphyrio, we recorded several instances of male male and female-female courtship and copulations. The purpose of this paper is to document and analyse these interactions in relation to the behavioural context in which they
1251
occurred in an attempt to gain a better understanding of this unusual behaviour. The pukeko is a gallinule which lives in groups of two seven breeding males, two breeding females, who lay their eggs in a single nest, and as many as seven non-breeding birds who are offspring from previous matings. The study was carried out in Shakespear Regional Park approximately 25 km north of Auckland, New Zealand. Birds were colour-banded for individual recognition, and dominance status was determined independently of mounting behaviour. There was no relation between differences in the number of mountings observed between groups and observation time. Before analysing observations on interactions between pukeko of the same sex, we must give a brief description of mating behaviour between males and females (for a more detailed account plus illustrations see Craig 1977). Mating behaviour can be divided into three sequential components. First, a male approaches a female in a 'sexual upright' posture and follows behind her, giving a loud 'humming' call. As many as five other males may join in and pursue the female at this time. Second, if the female responds to the male's initial courting behaviour, she will stop and assume a precopulatory 'hunched' position after which the male will step onto the female's back. Third, the female raises her tail as the male attains cloacal contact and ejaculation. What we term as male-male or femalefemale 'sexual' interactions is behavioural activity that is indistinguishable to that described above except that the participants are of the same sex. It can include all three components or any part of the behavioural sequence. During 174 h of observation over a period of 3 years, 555 heterosexual interactions were recorded, compared to 41 homosexual interactions (12 male-male, 29 female-female). D o m i n a n t males clearly initiated the 12 m a l e male interactions. In two of these, dominant males approached subordinates in a 'sexual upright' posture and attempted to mount them. However, in the other 10 interactions which occurred during male female courtship activity, the alpha male ran in front of the other courting males and assumed a 'hunched' position. The subordinate males immediately stopped pursuing the female and mounted the alpha male; three of these resulted in birds making cloacal contact in the same manner as in male-female copulations. However, these interactions were confined to only a few individuals. Three of the nine alpha males initiated nine (five, two, two) of the 10 interactions. Male male sexual interactions occurred only in groups with four or more breeding males: groups in which mating interactions were most intense (Jamieson & Craig, in press). The alpha male
1252
Animal Behaviour, 35, 4
behaving functionally like a female results in a and females commenced almost 2 months beforeredirection of sexual activity of the other breeding hand. Could female-female interactions be somemales in a group during a male-female mating how related to alpha females regulating the number of eggs laid in the communal nest? attempt. Although this type of behaviour appears to be linked to sexual competition, other research Egg-tossing behaviour, which has the effect of has shown that dominant males are just as likely to biasing the total number of eggs that each female ignore totally a mating involving a subordinate as contributes to the final clutch, has been described in they are to interrupt it (Jamieson & Craig, in press). other polygynandrously breeding birds (e.g. This was true for both the prelaying and laying Mumme et al. 1983; Vehrencamp et al. 1986), but periods. These observations, added to the fact that does not occur in pukeko. In addition, aggressive only a few alpha males initiated male rnale mount- interactions between breeding females within pukings, suggest that attaching any adaptive signifi- eko groups are rare. Nevertheless, the alpha female cance to the behaviour would be difficult and usually lays at least one more egg and contributes unwarranted. The 'hunched' posture is more com- to more clutches than the beta female (Craig 1980). monly exhibited by males during territorial dis- However, we have been unable to tease apart the putes (see Craig 1977), and appears to be involved effects that age, experience and dominance have on in reducing aggression between territorial males an individual's egg production. It should also be after they have interacted. It may be that a few remembered that although the difference in the individuals have developed a tendency to display number of eggs laid by alpha and beta females is this stereotyped posture during courtship interac- found among most breeding groups, female tions which involve other males from within their female courtship and copulations were relatively group. rare and confined to only a few individuals. Most of the instances of female-female courtship Therefore, homosexual behaviour by alpha females and copulations (26 of 29) also involved only a few does not appear to be necessary to produce the bias individuals (I0, 9, 4, 3). As with alpha males, it was . in egg production and by itself is of doubtful the alpha female who initiated the homosexual adaptive significance. However, the lack of overt interactions. Unlike alpha males (10 of 12), the aggression among breeding females as well as males alpha female behaved functionally like a male, during reproductive competition is in keeping with approaching in a 'sexual upright' posture, mount- the pukeko's highly developed social system and ing and copulating with another female in her appears to be essential for the maintenance of a group. In addition, all interactions involved only breeding territory (Craig 1984). alpha and beta females even though most groups We would like to thank Ed Minot and two had one or two additional non-breeding females. anonymous referees for their comments on the Female-female interactions occurred in three manuscript. Finance for the research was provided types of situations. On three occasions all involving by New Zealand University Grants Committee and the same individual, a female apparently tried to the University of Auckland. evade several courting males who were chasing her by running towards the other breeding female in 1AN G. JAM1ESON the group and assuming a 'sexual upright' posture. JOHN L. CRAIG The effect of this behaviour was that the males Department of Zoology, stopped pursuing her and began courting the other University of Auckland, female. Auckland, New Zealand. The remaining 26 interactions were of a different nature. On 17 occasions an alpha female approached a beta female, who was alone at the References time, assumed a 'sexual upright' posture, gave a Craig, J. L. 1977. The behaviour of the pukeko. N.Z.J. precopulatory call, and proceeded to mount the Zool., 4, 413~33. beta. In nine other instances, the alpha female ran Craig, J. L. 1980. Breeding success of a communal gallinule. Behav. Ecol. Sociobiol., 6, 289-295. towards the beta and assumed a 'sexual upright' posture after one or more males had initiated Craig, J. L. 1984. Are pukeko caught in a prisoner's dilemma? Behav. Ecol. SociobioL, 14, 147-150. courtship behaviour with the beta female. In the Hanby, J. P. 1974. Male-male mounting in Japancse latter cases the alpha female ran in fi'ont of the monkeys, Macaca fizscata. Anim. Behav., 22, 836~849, males and mounted the beta female. In total, six of Jamieson, 1. G. & Craig, J. L. In press. Dominance and the mountings resulted in cloacal contact. mating in a communal polygynandrous bird: cooperAll 26 interactions of the type described above ation or indifference towards mating competitors? occurred just prior to or during egg laying even Ethology. though courtship and copulations between males Mumme, R. L., Koenig, W. D. & Pitelka, F. A. 1983.
Short Communications
Reproductive competition in the communal acorn woodpecker: sisters destroy each other's eggs. Nature, Lond., 306, 583-584. Vehrencamp, S., Bowen, B. S. & Koford, R. R. 1986. Breeding roles and pairing patterns within communal groups of groove-billed anis. Anim. Behav., 34, 347367. (Received 18 August 1986; revised 27 October 1986," MS. number." sc-331)
Partial Mortality in Nestling Meadow Voles, Microtus pennsylvanicus
Nestling mortality is important in theories concerning population regulation and life history, but is poorly measured in small mammal populations. Nestling mortality in microtine rodents has been divided into two types: whole and partial loss of the litter (Hoffmann 1958). Whole litter loss was thought to result from predation or the death of the mother prior to weaning of the litter. Partial litter loss was described as the result of the inherent physiological weaknesses of some pups. Infanticide by neighbouring adults (Mallory & Brooks 1978) and maternal manipulation of litters (McClure 1981) should also be considered as possible sources of litter loss. These causative factors can be investigated by studying the survivorship of nestlings. The purpose of this study was to look for nestling mortality, and possible patterns of selective mortality, in a natural population. A 0.63 ha trapping grid was set up within a 100 ha field in Brackney, Pennsylvania, 25 km south of Binghamton, New York. Live-trapping was conducted 1 day a week over four periods during 1983 and 1984 (3 M a r c h - 6 July and 26 A u g u s t 8 November in 1983; 23 March-10 July and 18 August-25 October in 1984). For the remainder of both years, trapping was conducted monthly. We will refer to the period of weekly trapping as 'spring' and 'autumn'. Trap stations were placed at 10-m intervals, and two live-traps were placed at each station. All stations were pre-baited 1 day before being checked every 2 h over a 10-h period. Captured animals were weighed, sexed, uniquely marked (toe-clipped), and checked for reproductive condition. The maternal weight of the female, for each litter located, was considered the weight at first capture after parturition. Weekly, during the spring and autumn period, 15-20 females were radiotracked for 10 h (for implant and tracking techniques, see Madison et al. 1985). The located nests of lactating females were opened and the pups removed for examination. The pups were uniquely marked (toe-clipped), weighed, counted and their anal-genital length
1253
recorded. Pups were returned to the nest within 5 min of removal. The process of locating the natal nest did not appear to disturb the care-giving behaviour of the females, as mothers with undisturbed nests, in other studies, exhibited similar patterns of nest visitation (Madison 1981). However, entering the nest did cause some temporary stress, as every nest examined resulted in the mother transferring the pups to a new nest. We maintain that the level of disturbance was not extreme, since (1) no litters were abandoned after nest examination; (2) females often moved nests after natural disturbances (i.e. heavy rainfalls); (3) field-captured females that gave birth in the laboratory (N= 14) exhibited no infanticide in response to having their pups handled in a similar fashion. For 36 litters, we were able to relocate and examine the pups 4-9 days following their initial examination. All re-examined litters were of pups prior to eye-opening, and therefore under complete care by the mother. Pup growth is linear over this period, with no significant sexual dimorphism in the pups (Innes & Millar 1979). For those litters in which some mortality occurred between nest checks (N= 16), the following traits were recorded: two measures of population density at the time of parturition (a global estimate based on the total number of animals captured and a local estimate based on the number of animals captured within a radius of two home ranges (approximately 30 m) of the animal), the mass of pups and the mother, the number of pups in the litter, the period of time between checks, and, based on the pup's weight, a relative rank within the litter. Fluctuations in recruitment over the study period did not appear to be due to changes in dispersal, as the minimum trappability of the juveniles (N=484) did not change significantly from spring to autumn (54 and 55%, respectively; calculated according to Hilborn et al. 1976), and the mean weight for marked juveniles at first capture did not differ from spring to autumn (J? = 17.8 g and 17.6 g respectively, t = 0.9, P > 0.1). Of the 635 pups marked over the course of the study, 153 (24%) later entered the trappable population. Entry of an entire litter into the trappable population occurred in only eight of 131 (6%) litters, but the litters contributing at least a single pup varied seasonally from 40 to 78% (Table I). Partial recruitment of a litter may be due to partial dispersal of the litter, or partial survival of the litter prior to dispersal. If mortality plays a role in the partial recruitment observed (and the mortality occurs prior to weaning), then the size of the located litters should be negatively correlated with