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Allofeeding and dominance interactions in the cooperatively breeding pied starling
Short Communications In species where mating investment is high, behaviour that ensures paternity is reproductively advantageous (Trivers 1972). In surface mating, a male's energy and time investment is relatively low and little is lost when courting unripe females, Both ripe and unripe females often mate at the surface. Thus, males that copulate with many females increase their chances for reproductive success with relatively little energy and time cost. With underground mating males expend energy enlarging burrows, forgo surface feeding for several days, and abandon their burrows to incubating mates. By keeping the female in his burrow until spawning, the male ensures no other male will mate with her. Uca pugilator shows similar behaviour, both sexes remaining in the male's burrow until spawning is over (Christy 1982). The sperm of the last male to mate with a female occupies the position closest in the spermatheca to the oviduct (Murai et al. 1987). Therefore, though not proven, it is reasonable to assume this sperm will be used first in clutch fertilization. Mate guarding (Ridley 1983) minimizes the potential risk of uselessly abandoning burrows to females, otherwise the male's sperm could be displaced by that of another male. Examples of alternative male mating strategies are common in the literature (see e.g. Davies 1982). A population may be genetically monomorphic with individuals adopting both strategies. According to Murai et al. (1987) surface matings were 4.5 times more frequent than underground matings, but only 31% of surface-mated females laid eggs. Thus males may not gain equally from surface and underground mating. More exact information on the relative fitness payoffs of the alternative strategies is required before we can see whether or not they are maintained as a mixed evolutionarily stable strategy. We thank T. Yamaguchi, N. Yamamura, A. Fuji, S. Nakao, Y. Ono and A. J. Paul for their critical reading of the manuscript. This research was partially supported by Grants-in-Aid from the Ministry of Education, Science and Culture.
SEIJI GOSHIMA* MINORU MURAlt * Department o f Biology and Aquaculture, Faculty o f Fisheries, Hokkaido University, Hakodate 041, Japan. t Department o f Biology, Faculty o f Science, Kyushu University, Fukuoka 812, Japan.
References Christy, J. H. 1982. Burrow structure and use in the sand
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fiddler crab, Uca pugilator (Bosc). Anita. Behav., 30, 687-694. Davies, N. B. 1982. Behaviourand competition for scarce resources. In: Current Problems in Sociobiology (Ed. by King's College Sociobiology Group), pp. 363-380. Cambridge: Cambridge University Press. Murai, M., Goshima, S. & Henmi, Y. 1987. Analysis of the mating system of the fiddlercrab, Uea lactea. Anita. Behav., 35, 1334-1342. Ridley, M. 1983. The Explanation of Organic Diversity. Oxford: Clarendon Press. Robertson, J. R. & Newell, S. Y. 1982. Experimental studies of particle ingestion by the sand fiddler crab Ucapugilator (Bose). J. Exp. Mar. Biol. Ecol., 59,1 21. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine. Yamaguehi, T. 1971. Courtship behavior of a fiddler crab, Uca lactea. Kumamoto J. Sci., BioL, 10, 13-37.
(Received 27 May 1987; revised 22 October 1987; MS. number: sc-377)
Ailofeeding and Dominance Interactions in the Cooperatively Breeding Pied Starling Avian cooperative and communal breeding systems have been a focus of interest in recent years (Emlen & Vehrencamp 1983). Allofeeding may occur (1) at the nest when helpers feed the young and sometimes the incubating or brooding female; (2) as courtship feeding between breeding adults; (3) between group members in a non-breeding context. Most studies have concentrated on breeding behaviour, but this paper focuses on interactions away from the nest. Allofeeding in a non-sexual context may be governed by dominance relationships. In green woodhoopoes, Phoeniculus purpureus, dominant birds feed subordinates (Ligon & Ligon 1983), and in the northwestern crow, Corvus caurinus, helpers are fed regularly by the male breeder (Verbeek & Butler 1981). Dominant female pukekos, Porphyrio porphyrio, sometimes feed subordinate females (Craig 1980). Kemp & Kemp (1980) proposed that food transfers between adult ground hornbills, Bucorvus leadbeateri, of the same sex served to define social status. Breeding male pied kingfishers, Ceryle rudis, sometimes accept food from male helpers, and this inhibits the aggression often displayed towards other males by the male breeder (Reyer 1986). However, Hardy (1974) reported that in three neotropical jays (Cyanocorax) allofeeding could occur between any members of the flock, without reference to sex or age. The pied starling, Spreo bicolor, is a dull-
Animal Behaviour, 36, 3
1252
coloured, monomorphic species which is endemic to South Africa. The birds occur in flocks throughout the year, and are colonial breeders, nesting in holes in river banks and in other sites. Helpers feed young in the nest, and for a few weeks afterwards (Craig 1983, 1987). Pied starlings were observed at Table Farm 10 km north of Grahamstown, South Africa, between February 1981 and February 1985. Observations were made on foot or from a vehicle, using 10 x 40 binoculars and a 20 x telescope. Four age classes can be distinguished in the field on the basis of iris colour and plumage: (1) birds of the year (0-3 months old); (2)juveniles (4-12 months); (3) subadults (1-2 years); (4) adults (more than 2 years). On each visit every colour-ringed bird seen was recorded, and the numbers of each age class present were counted. Sexes were distinguished only for birds of known breeding history. All observations at the nest or involving a bird of the year are excluded here. Allofeeding occurs throughout the year. It was most frequently observed when the flock was spread out, foraging on the ground. The behaviour sequence is quite stereotyped: a bird finds a food item and walks rapidly towards another flock member, which may be several metres away. The donor approaches with slow deliberate steps, the neck stretched upwards, the bill pointed slightly downwards. The recipient crouches, drawing in the neck, and gapes. The food item is then placed in its open bill. The donor appears to select a particular individual, and will ignore birds which may beg from it en route. If the recipient does not gape and turns away repeatedly, the food is swallowed by the donor (15 refusals seen). A bird may approach another individual which has found food, and
solicit feeding by crouching and gaping. It was fed in 27 cases, but disregarded on 28 occasions. 'Symbolic' allofeeding was also noted (23 cases), in which a 'donor' placed its empty bill within the open gape of another bird. Pied starlings have a bright yellow base to the lower mandible, and a yellow wattle at the corner of the gape. At all ages the lining of the mouth is bright yellow, but in nestlings the gape wattles are white. Most passerine nestlings have fleshy wattles on the gape which disappear soon after fledging. These juvenile features on thebill of pied starlings may be signals functioning in the context of allofeeding. Overt aggression between flock members was rare, and most frequently took the form of one bird supplanting another on a perch. Dominance appears to be related to age class (Table I) and sex; males initiated 33 aggressive interactions, females only seven. Four cases in which a subadult displaced an adult involved a subadult male and an adult female, and females were apparently always subordinate to males. In both allofeeding and aggressive interactions, subadults participated as often as expected from the numbers present in the flock (Table I). Adults were 'donors' much more often than recipients, while the reverse was true of juveniles (Table I). However, the dominance hierarchy indicated by the data on aggression is not a good indicator of the roles played in allofeeding. Juveniles did feed both adults and subadults, and females fed males as often as they received food from them. Allofeeding in the pied starling cannot be classified as courtship feeding. It was observed once only between members of a known pair, when a female fed her mate. Subadults do not normally breed (Craig, 1987), but they participated actively in
Table I. Allofeeding and aggression by different age classes of pied starlings
Recipient
Donor
Food Aggression Food Aggression Age class (average number) Observed Expected Observed Expected Observed Expected Observed Expected Adults (8.4) Subadults (10"3) Juveniles (4.5) Total (23-2)
69
99-6
15
33.7
133
99-6
49
33.7
127
122.1
40
41.3
131
122.1
34
41.3
79
53.4
38
18.0
11
53-4
10
18.0
275
93
275
93
Short Communications allofeeding. I suspect that allofeeding serves to establish or reinforce social bonds between individuals. In 58 instances both participants were identified, and in 28 cases they had been members o f the same breeding group in a previous year. Foodsharing in the vampire bat Desmodus rotundus depends both on relatedness and on reciprocity between unrelated animals (Wilkinson 1984). This question cannot be resolved for the pied starling yet, since the relatedness of members of the Table F a r m flock is unknown. Further long-term studies are needed to clarify the functions of bonds between related and unrelated birds. At present I have only two records o f reciprocal allofeeding. This suggests that if the system depends on reciprocity, 'repayment' may be made in some other form, such as helping at the nest. M r F. White has allowed me free access to Table F a r m at all times, for which I am most grateful. The study was supported by a research grant from Rhodes University. The paper was greatly improved by the suggestions of two referees. A. J. F. K. CRAIG Department o f Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa.
1253
References Craig, A. J. F. K. 1983. Co-operative breeding in two African starlings, Sturnidae. Ibis, 125, 114- 115. Craig, A. J. F. K. 1987. Cooperative breeding in the pied starling. Ostrich. 58, 176-180. Craig, J. L. 1980. Pair and group breeding behaviour of a communal gallinule, and pukcko, Porphyrio p. melanotus. Anim. Behav., 28, 593-603. Emlen, S. T. & Vehrencamp, S. L. 1983. Cooperative breeding strategies among birds. In: Perspectives in Ornithology (Ed. by A. H. Brush & G. A. Clarke), pp. 93-120. Cambridge: Cambridge University Press. Hardy, J. W. 1974. Behavior and its evolution in neotropical jays (Cissilopha). Bird-Banding, 45, 253-268. Kemp, A. C. & Kemp, M. I. 1980. The biology of the southern ground hornbill Bucorvus leadbeateri (Vigors) (Aves: Bucerotidae). Ann. Transv. Mus., 32, 65-100. Ligon, J. D. & Ligon, S. D. 1983. Reciprocity in the green woodhoopoe Phoeniculus purpureus. Anim. Behav., 31, 480~-89. Reyer, H.-U. 1986. Breeder-helper interactions in the pied kingfisher reflect the costs and benefits of cooperative breeding. Behaviour, 96, 277 303. Verbeek, N. A. M. & Butler, R. W. 1981. Cooperative breeding of the northwestern crow Corvus caurinus in British Columbia. Ibis, 123, 183-189. Wilkinson, G. S. 1984. Reciprocal food sharing in the vampire bat. Nature, Lond., 308, 181-184. (Received 30 June 1987; revised 11 October 1987; MS. number." sc 384)
SEIJI GOSHIMA* MINORU MURAlt * Department o f Biology and Aquaculture, Faculty o f Fisheries, Hokkaido University, Hakodate 041, Japan. t Department o f Biology, Faculty o f Science, Kyushu University, Fukuoka 812, Japan.
References Christy, J. H. 1982. Burrow structure and use in the sand
1251
fiddler crab, Uca pugilator (Bosc). Anita. Behav., 30, 687-694. Davies, N. B. 1982. Behaviourand competition for scarce resources. In: Current Problems in Sociobiology (Ed. by King's College Sociobiology Group), pp. 363-380. Cambridge: Cambridge University Press. Murai, M., Goshima, S. & Henmi, Y. 1987. Analysis of the mating system of the fiddlercrab, Uea lactea. Anita. Behav., 35, 1334-1342. Ridley, M. 1983. The Explanation of Organic Diversity. Oxford: Clarendon Press. Robertson, J. R. & Newell, S. Y. 1982. Experimental studies of particle ingestion by the sand fiddler crab Ucapugilator (Bose). J. Exp. Mar. Biol. Ecol., 59,1 21. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871-1971 (Ed. by B. Campbell), pp. 136-179. Chicago: Aldine. Yamaguehi, T. 1971. Courtship behavior of a fiddler crab, Uca lactea. Kumamoto J. Sci., BioL, 10, 13-37.
(Received 27 May 1987; revised 22 October 1987; MS. number: sc-377)
Ailofeeding and Dominance Interactions in the Cooperatively Breeding Pied Starling Avian cooperative and communal breeding systems have been a focus of interest in recent years (Emlen & Vehrencamp 1983). Allofeeding may occur (1) at the nest when helpers feed the young and sometimes the incubating or brooding female; (2) as courtship feeding between breeding adults; (3) between group members in a non-breeding context. Most studies have concentrated on breeding behaviour, but this paper focuses on interactions away from the nest. Allofeeding in a non-sexual context may be governed by dominance relationships. In green woodhoopoes, Phoeniculus purpureus, dominant birds feed subordinates (Ligon & Ligon 1983), and in the northwestern crow, Corvus caurinus, helpers are fed regularly by the male breeder (Verbeek & Butler 1981). Dominant female pukekos, Porphyrio porphyrio, sometimes feed subordinate females (Craig 1980). Kemp & Kemp (1980) proposed that food transfers between adult ground hornbills, Bucorvus leadbeateri, of the same sex served to define social status. Breeding male pied kingfishers, Ceryle rudis, sometimes accept food from male helpers, and this inhibits the aggression often displayed towards other males by the male breeder (Reyer 1986). However, Hardy (1974) reported that in three neotropical jays (Cyanocorax) allofeeding could occur between any members of the flock, without reference to sex or age. The pied starling, Spreo bicolor, is a dull-
Animal Behaviour, 36, 3
1252
coloured, monomorphic species which is endemic to South Africa. The birds occur in flocks throughout the year, and are colonial breeders, nesting in holes in river banks and in other sites. Helpers feed young in the nest, and for a few weeks afterwards (Craig 1983, 1987). Pied starlings were observed at Table Farm 10 km north of Grahamstown, South Africa, between February 1981 and February 1985. Observations were made on foot or from a vehicle, using 10 x 40 binoculars and a 20 x telescope. Four age classes can be distinguished in the field on the basis of iris colour and plumage: (1) birds of the year (0-3 months old); (2)juveniles (4-12 months); (3) subadults (1-2 years); (4) adults (more than 2 years). On each visit every colour-ringed bird seen was recorded, and the numbers of each age class present were counted. Sexes were distinguished only for birds of known breeding history. All observations at the nest or involving a bird of the year are excluded here. Allofeeding occurs throughout the year. It was most frequently observed when the flock was spread out, foraging on the ground. The behaviour sequence is quite stereotyped: a bird finds a food item and walks rapidly towards another flock member, which may be several metres away. The donor approaches with slow deliberate steps, the neck stretched upwards, the bill pointed slightly downwards. The recipient crouches, drawing in the neck, and gapes. The food item is then placed in its open bill. The donor appears to select a particular individual, and will ignore birds which may beg from it en route. If the recipient does not gape and turns away repeatedly, the food is swallowed by the donor (15 refusals seen). A bird may approach another individual which has found food, and
solicit feeding by crouching and gaping. It was fed in 27 cases, but disregarded on 28 occasions. 'Symbolic' allofeeding was also noted (23 cases), in which a 'donor' placed its empty bill within the open gape of another bird. Pied starlings have a bright yellow base to the lower mandible, and a yellow wattle at the corner of the gape. At all ages the lining of the mouth is bright yellow, but in nestlings the gape wattles are white. Most passerine nestlings have fleshy wattles on the gape which disappear soon after fledging. These juvenile features on thebill of pied starlings may be signals functioning in the context of allofeeding. Overt aggression between flock members was rare, and most frequently took the form of one bird supplanting another on a perch. Dominance appears to be related to age class (Table I) and sex; males initiated 33 aggressive interactions, females only seven. Four cases in which a subadult displaced an adult involved a subadult male and an adult female, and females were apparently always subordinate to males. In both allofeeding and aggressive interactions, subadults participated as often as expected from the numbers present in the flock (Table I). Adults were 'donors' much more often than recipients, while the reverse was true of juveniles (Table I). However, the dominance hierarchy indicated by the data on aggression is not a good indicator of the roles played in allofeeding. Juveniles did feed both adults and subadults, and females fed males as often as they received food from them. Allofeeding in the pied starling cannot be classified as courtship feeding. It was observed once only between members of a known pair, when a female fed her mate. Subadults do not normally breed (Craig, 1987), but they participated actively in
Table I. Allofeeding and aggression by different age classes of pied starlings
Recipient
Donor
Food Aggression Food Aggression Age class (average number) Observed Expected Observed Expected Observed Expected Observed Expected Adults (8.4) Subadults (10"3) Juveniles (4.5) Total (23-2)
69
99-6
15
33.7
133
99-6
49
33.7
127
122.1
40
41.3
131
122.1
34
41.3
79
53.4
38
18.0
11
53-4
10
18.0
275
93
275
93
Short Communications allofeeding. I suspect that allofeeding serves to establish or reinforce social bonds between individuals. In 58 instances both participants were identified, and in 28 cases they had been members o f the same breeding group in a previous year. Foodsharing in the vampire bat Desmodus rotundus depends both on relatedness and on reciprocity between unrelated animals (Wilkinson 1984). This question cannot be resolved for the pied starling yet, since the relatedness of members of the Table F a r m flock is unknown. Further long-term studies are needed to clarify the functions of bonds between related and unrelated birds. At present I have only two records o f reciprocal allofeeding. This suggests that if the system depends on reciprocity, 'repayment' may be made in some other form, such as helping at the nest. M r F. White has allowed me free access to Table F a r m at all times, for which I am most grateful. The study was supported by a research grant from Rhodes University. The paper was greatly improved by the suggestions of two referees. A. J. F. K. CRAIG Department o f Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa.
1253
References Craig, A. J. F. K. 1983. Co-operative breeding in two African starlings, Sturnidae. Ibis, 125, 114- 115. Craig, A. J. F. K. 1987. Cooperative breeding in the pied starling. Ostrich. 58, 176-180. Craig, J. L. 1980. Pair and group breeding behaviour of a communal gallinule, and pukcko, Porphyrio p. melanotus. Anim. Behav., 28, 593-603. Emlen, S. T. & Vehrencamp, S. L. 1983. Cooperative breeding strategies among birds. In: Perspectives in Ornithology (Ed. by A. H. Brush & G. A. Clarke), pp. 93-120. Cambridge: Cambridge University Press. Hardy, J. W. 1974. Behavior and its evolution in neotropical jays (Cissilopha). Bird-Banding, 45, 253-268. Kemp, A. C. & Kemp, M. I. 1980. The biology of the southern ground hornbill Bucorvus leadbeateri (Vigors) (Aves: Bucerotidae). Ann. Transv. Mus., 32, 65-100. Ligon, J. D. & Ligon, S. D. 1983. Reciprocity in the green woodhoopoe Phoeniculus purpureus. Anim. Behav., 31, 480~-89. Reyer, H.-U. 1986. Breeder-helper interactions in the pied kingfisher reflect the costs and benefits of cooperative breeding. Behaviour, 96, 277 303. Verbeek, N. A. M. & Butler, R. W. 1981. Cooperative breeding of the northwestern crow Corvus caurinus in British Columbia. Ibis, 123, 183-189. Wilkinson, G. S. 1984. Reciprocal food sharing in the vampire bat. Nature, Lond., 308, 181-184. (Received 30 June 1987; revised 11 October 1987; MS. number." sc 384)