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Inter-nest distance and sneaking in the three-spined stickleback
Anita. Behav., 1992,44, 793-795
Inter-nest distance and sneaking in the three-spined stickleback T I J S G O L D S C H M I D T * , S U S A N A. FOSTER]" & P I E T S E V E N S T E R *
*Ethology Research Group, Zoological Laboratory, University of Leiden, P.O. Box 9516, 2300 RA Leiden, The Netherlands' tDepartment of Biological Sciences, University of Arkansas, Fayetteville, A R 72701, U.S.A. (Received30 September 1991; initial acceptance 12 November 1991; final acceptance 21 April 1992; MS. number: sc-747)
During the first three-quarters of this century, ethologists tended to view species as having single, species-specific tactics for obtaining mates (e.g. Tinbergen 1951). It is now known, however, that in species in which variance in male mating success is high, males often exhibit two or more kinds of mating behaviour that result in fertilization of eggs. Often, the expression of alternative mating tactics is condition-dependent and individual males can shift between them (e.g. Austad 1984; Dominey 1984). Here, we describe the first field observations of a classical example of an alternative male mating tactic: sneaking by male three-spined sticklebacks, Gasterosteus aeuleatus. We describe the context in which it occurred and evaluate possible causes of variation in sneaking between and within populations. We observed reproductive male sticklebacks in eight populations, two in the Netherlands and six in British Columbia, Canada. In the Netherlands, observations were made in small ponds at trout cultivation stations, one at 't Smallert, Ernst and the other at de Zwaanspreng, Apeldoorn. Observations were made at 't Smallert from 26 April to 20 July 1978 and at de Zwaanspreng from 29 July to 6 September 1978, from 26 July to 8 September 1981, and from 10 to 15 June and 17 to 21 July 1985. All observations were made from the shoreline. Observations were made on 21 courting males at 't Smallert and on 89 at de Zwaanspreng. In British Columbia, daily 10-min observations were made on 103 males in Crystal Lake between 15 May and t August 1985 and on 83 males, in Garden Bay Lake between 15 May and 8 July 1986. We observed, respectively, 72 and 25 courtship interactions in which the female reached the nest entrance. Descriptions of courtship interactions in which the female reached the nest were recorded for 27 females in Hotel Lake, 19 in North Lake, and 20 0003-3472/92/100793 + 03 $08.00/0
in Cowichan Lake between 14 May and 26 June 1988. During this period and between 14 May and 26 June 1988, 161 such courtships were recorded at Sproat Lake. Observations were made while snorkelling. In the Dutch populations, the distances between the nests of males were measured with a tape measure. In Crystal and Garden Bay Lakes, maps were made of the nests on study grids and inter-nest distances were calculated from these. Mean internest distance refers to the mean distance between a male's nest and those of his three nearest neighbours, provided one of the three fell on the opposite side of a straight line drawn through the nest. If all three were within 180~ only the two nearest were used and the closest male on the other side of the line was used instead. I f a male had no near neighbour on one side of his nest, a value of 1-5 m was substituted. Sneaking was never observed in five of the six Canadian populations, and was common only in the Dutch populations. At 't Smallert sneaking occurred in 22 (10%) of 223 courtships and sneakers fertilized eggs in the nests of courting males in seven (35%) of 20 spawnings. At de Zwaanspreng, sneaking occurred nearly as often during courtship (9% of 172 courtships), but sneakers never entered the nests to fertilize the eggs during recorded observations. A chance observation demonstrated, however, that sneakers do sometimes enter nests at de Zwaanspreng. The sneaking behaviour of males in the Dutch populations was virtually identical to that described in the laboratory by Van den Assem (1967). The sneakers would freeze, sink to the bottom, and swim slowly to the nest of a courting male. If undetected, the sneaker often dashed forward near the nest and attempted to enter. If successful, he usually followed the resident male through,
9 1992The Association for the Study of Animal Behaviour 793
794
Animal Behaviour, 44, 4
although occasionally the order was reversed. Once the sneaker had passed through a nest, he always returned to the entrance and stole a mouthful of eggs, which he attempted to return to his nest. Egg stealing was often repeated several times. Sneaking was condition-dependent in the Dutch populations, and the sneakers always appeared to be neighbouring males that had constructed nests. They typically had less well-developed nuptial coloration than did males that courted females. Following successful sneaking and egg theft, these males usually became brighter, stopped sneaking, and began to court females. Although sneaking in three-spined sticklebacks has been considered characteristic of males with small territories or low dominance ranks (Van den Assem 1967; Li & Owings 1978), our own observations, and those of Jamieson & Colgan (1989), suggest that sneaking behaviour also reflects the order of territory and nest establishment among close neighbours. This did not appear to be the case at Sproat Lake, however, where only three males were ever observed sneaking, and none entered a nest. All three had lost nests in the previous 3 days, suggesting that sneaking in this population, is performed only by males that have experienced a disruption of the normal reproductive cycle. Males with new nests may benefit from sneaking in at least three ways. First, when sneaking is successful, males may fertilize some of the eggs in the nest of their neighbour (Van den Assam 1967). Second, a sneaker could cause a courtship interaction to fail and then court the female himself. At 't Smallert females never entered a nest when a sneaker interfered first ( N = 16) but did enter in 35 of 188 courtships in which there was no interference by a sneaker (G=5.260, df=l, P<0.025). However, none of the sneakers was ever observed to court the female subsequently, suggesting that this is not a primary benefit of sneaking. Third, sneakers may enhance their future courtship success by acquiring eggs and placing them in their own nests, because females prefer to spawn in nests that already contain eggs (Rohwer 1978; Ridley & Rechten 1981). This has recently been tested (Goldschmidt et al., in press) at de Zwaanspreng: there, females preferred nests with eggs. This preference was partly a direct consequence of the eggs themselves, suggesting that egg theft may be adaptive in this context. In polygynous species, the advantage of adopting an alternative mating tactic may be higher when
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Figure 1. The incidence of sneaking versus mean internest distance at 't Smallert (Spearman rank correlation coefficient, r=-0.836, two-tailed P=0-0003). The incidence of sneaking was defined as the probability that sneaking would occur during courtship or the ensuing 5 min. The number of courtships used to calculate the probability is given for each point. the operational sex ratio is low (number of receptive females/receptive males). However, our data do not support the hypothesis that sneaking is more common where the operational sex ratio is low. The encounter rate between courting males and females (which presumably reflect the operational sex ratio reasonably well) was lowest in Garden Bay Lake (0.94/h; 29 in 31 h), intermediate in 't Smallert (2.9/h; 420 in 145 h) and de Zwaanspreng (2.7/h; 84 in 31 h) and highest at Crystal Lake (11.9/h; 98 in 16.3 h). At 't Smallert, however, the incidence of sneaking (during courtship or within the 5 min following courtship) and inter-nest distance were negatively correlated (Fig. 1). Also, the mean inter-nest distances of courting males were shortest (.,~-I-SD = 76_+22 cm, N = 17) at 't Smallert, intermediate (118 _52cm, N = 2 6 ) at Crystal Lake, and longest (213___66 cm, N = 21) at Garden Bay Lake (non-parametric Student-Newman-Keuls test, P<0-05 for each between-row comparison; Zar 1984). These results indicate that at 't Smallert, sneaking is most likely to occur when courting males are relatively close to one another. They also suggest that sneaking may be absent in the Canadian populations because of the longer internest distances. Why longer inter-nest distances should have had this effect is unclear, as males in the Canadian populations are typically in visual contact with one another and interact frequently. Because the Dutch and Canadian populations have
Short Communications very similar behavioral repertoires in other respects (unpublished data), it seems surprising that sneaking is observed only in the Dutch populations. We thank J. A. Baker, V. B. Garcia, S. A. Ploch, M. Sadagursky, M. Y. T o w n and C. Vestuto for assistance in the field. T.G. would like to dedicate this paper to his friend and companion during the field observations, the late Jeroen Kroese. We thank J. A. Baker, I. G. Jamieson and two anonymous referees for useful comments on the manuscript. T.G. gratefully acknowledges M. M. Soeting for moral support and the Albach family for shelter. S.F. thanks J. M c O u a t for both. The research was partially supported by a Research Service Award from N I M H to S.F.
REFERENCES Van den Assem, J. 1967. Territoriality in the three-spined stickleback Gasterosteus aculeatus L. An experimental
795
study in intra-specific competition. Behaviour, Suppl., 16, 1 164. Austad, S. N. 1984. A classification of alternative reproductive behaviors and methods for field-testing ESS models. Am. Zool., 24, 309-319. Dominey, W. J. 1984. Alternative mating tactics and evolutionary stable strategies. Am. Zool., 24, 385 396. Goldschmidt, T., Bakker, Th. C. M. & Feuth-de Bruijn, E. In press. Selective copying in mate choice of female stickleback? Anita. Behav. Jamieson, I. G. & Colgan, P. W. 1989. Eggs in the nests of males and their effect on mate choice in the three-spined stickleback. Anita. Behav., 38, 859 865. Li, S. K. & Owings, D. H. 1978. Sexual selection in the three-spined stickleback, II. Nest raiding during the courtship phase. Behaviour, 64, 298-304. Ridley, M. & Rechten, C. 1981. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour, 76, 152-161. Rohwer, S. 1978. Parent cannibalism of offspring and egg raiding as a courtship strategy. Am. Nat., 112, 429~440. Tinbergen, N. 1951. The Study of Instinct. London: Clarendon Press. Zar, J. H. 1984. Biostatistical Analysis. Englewood Cliffs, New Jersey: Prentice-Hall.
Inter-nest distance and sneaking in the three-spined stickleback T I J S G O L D S C H M I D T * , S U S A N A. FOSTER]" & P I E T S E V E N S T E R *
*Ethology Research Group, Zoological Laboratory, University of Leiden, P.O. Box 9516, 2300 RA Leiden, The Netherlands' tDepartment of Biological Sciences, University of Arkansas, Fayetteville, A R 72701, U.S.A. (Received30 September 1991; initial acceptance 12 November 1991; final acceptance 21 April 1992; MS. number: sc-747)
During the first three-quarters of this century, ethologists tended to view species as having single, species-specific tactics for obtaining mates (e.g. Tinbergen 1951). It is now known, however, that in species in which variance in male mating success is high, males often exhibit two or more kinds of mating behaviour that result in fertilization of eggs. Often, the expression of alternative mating tactics is condition-dependent and individual males can shift between them (e.g. Austad 1984; Dominey 1984). Here, we describe the first field observations of a classical example of an alternative male mating tactic: sneaking by male three-spined sticklebacks, Gasterosteus aeuleatus. We describe the context in which it occurred and evaluate possible causes of variation in sneaking between and within populations. We observed reproductive male sticklebacks in eight populations, two in the Netherlands and six in British Columbia, Canada. In the Netherlands, observations were made in small ponds at trout cultivation stations, one at 't Smallert, Ernst and the other at de Zwaanspreng, Apeldoorn. Observations were made at 't Smallert from 26 April to 20 July 1978 and at de Zwaanspreng from 29 July to 6 September 1978, from 26 July to 8 September 1981, and from 10 to 15 June and 17 to 21 July 1985. All observations were made from the shoreline. Observations were made on 21 courting males at 't Smallert and on 89 at de Zwaanspreng. In British Columbia, daily 10-min observations were made on 103 males in Crystal Lake between 15 May and t August 1985 and on 83 males, in Garden Bay Lake between 15 May and 8 July 1986. We observed, respectively, 72 and 25 courtship interactions in which the female reached the nest entrance. Descriptions of courtship interactions in which the female reached the nest were recorded for 27 females in Hotel Lake, 19 in North Lake, and 20 0003-3472/92/100793 + 03 $08.00/0
in Cowichan Lake between 14 May and 26 June 1988. During this period and between 14 May and 26 June 1988, 161 such courtships were recorded at Sproat Lake. Observations were made while snorkelling. In the Dutch populations, the distances between the nests of males were measured with a tape measure. In Crystal and Garden Bay Lakes, maps were made of the nests on study grids and inter-nest distances were calculated from these. Mean internest distance refers to the mean distance between a male's nest and those of his three nearest neighbours, provided one of the three fell on the opposite side of a straight line drawn through the nest. If all three were within 180~ only the two nearest were used and the closest male on the other side of the line was used instead. I f a male had no near neighbour on one side of his nest, a value of 1-5 m was substituted. Sneaking was never observed in five of the six Canadian populations, and was common only in the Dutch populations. At 't Smallert sneaking occurred in 22 (10%) of 223 courtships and sneakers fertilized eggs in the nests of courting males in seven (35%) of 20 spawnings. At de Zwaanspreng, sneaking occurred nearly as often during courtship (9% of 172 courtships), but sneakers never entered the nests to fertilize the eggs during recorded observations. A chance observation demonstrated, however, that sneakers do sometimes enter nests at de Zwaanspreng. The sneaking behaviour of males in the Dutch populations was virtually identical to that described in the laboratory by Van den Assem (1967). The sneakers would freeze, sink to the bottom, and swim slowly to the nest of a courting male. If undetected, the sneaker often dashed forward near the nest and attempted to enter. If successful, he usually followed the resident male through,
9 1992The Association for the Study of Animal Behaviour 793
794
Animal Behaviour, 44, 4
although occasionally the order was reversed. Once the sneaker had passed through a nest, he always returned to the entrance and stole a mouthful of eggs, which he attempted to return to his nest. Egg stealing was often repeated several times. Sneaking was condition-dependent in the Dutch populations, and the sneakers always appeared to be neighbouring males that had constructed nests. They typically had less well-developed nuptial coloration than did males that courted females. Following successful sneaking and egg theft, these males usually became brighter, stopped sneaking, and began to court females. Although sneaking in three-spined sticklebacks has been considered characteristic of males with small territories or low dominance ranks (Van den Assem 1967; Li & Owings 1978), our own observations, and those of Jamieson & Colgan (1989), suggest that sneaking behaviour also reflects the order of territory and nest establishment among close neighbours. This did not appear to be the case at Sproat Lake, however, where only three males were ever observed sneaking, and none entered a nest. All three had lost nests in the previous 3 days, suggesting that sneaking in this population, is performed only by males that have experienced a disruption of the normal reproductive cycle. Males with new nests may benefit from sneaking in at least three ways. First, when sneaking is successful, males may fertilize some of the eggs in the nest of their neighbour (Van den Assam 1967). Second, a sneaker could cause a courtship interaction to fail and then court the female himself. At 't Smallert females never entered a nest when a sneaker interfered first ( N = 16) but did enter in 35 of 188 courtships in which there was no interference by a sneaker (G=5.260, df=l, P<0.025). However, none of the sneakers was ever observed to court the female subsequently, suggesting that this is not a primary benefit of sneaking. Third, sneakers may enhance their future courtship success by acquiring eggs and placing them in their own nests, because females prefer to spawn in nests that already contain eggs (Rohwer 1978; Ridley & Rechten 1981). This has recently been tested (Goldschmidt et al., in press) at de Zwaanspreng: there, females preferred nests with eggs. This preference was partly a direct consequence of the eggs themselves, suggesting that egg theft may be adaptive in this context. In polygynous species, the advantage of adopting an alternative mating tactic may be higher when
i.o
,6
0.8 ,I0 "6 ,5
-
0.6
0.4 ,10 4 , , .4 13 ,5
0.2 0"0
I
40
I
60
I
I
"921 i
I
~
I
80 I00 120 Inter-nest distance
I
I
140
Figure 1. The incidence of sneaking versus mean internest distance at 't Smallert (Spearman rank correlation coefficient, r=-0.836, two-tailed P=0-0003). The incidence of sneaking was defined as the probability that sneaking would occur during courtship or the ensuing 5 min. The number of courtships used to calculate the probability is given for each point. the operational sex ratio is low (number of receptive females/receptive males). However, our data do not support the hypothesis that sneaking is more common where the operational sex ratio is low. The encounter rate between courting males and females (which presumably reflect the operational sex ratio reasonably well) was lowest in Garden Bay Lake (0.94/h; 29 in 31 h), intermediate in 't Smallert (2.9/h; 420 in 145 h) and de Zwaanspreng (2.7/h; 84 in 31 h) and highest at Crystal Lake (11.9/h; 98 in 16.3 h). At 't Smallert, however, the incidence of sneaking (during courtship or within the 5 min following courtship) and inter-nest distance were negatively correlated (Fig. 1). Also, the mean inter-nest distances of courting males were shortest (.,~-I-SD = 76_+22 cm, N = 17) at 't Smallert, intermediate (118 _52cm, N = 2 6 ) at Crystal Lake, and longest (213___66 cm, N = 21) at Garden Bay Lake (non-parametric Student-Newman-Keuls test, P<0-05 for each between-row comparison; Zar 1984). These results indicate that at 't Smallert, sneaking is most likely to occur when courting males are relatively close to one another. They also suggest that sneaking may be absent in the Canadian populations because of the longer internest distances. Why longer inter-nest distances should have had this effect is unclear, as males in the Canadian populations are typically in visual contact with one another and interact frequently. Because the Dutch and Canadian populations have
Short Communications very similar behavioral repertoires in other respects (unpublished data), it seems surprising that sneaking is observed only in the Dutch populations. We thank J. A. Baker, V. B. Garcia, S. A. Ploch, M. Sadagursky, M. Y. T o w n and C. Vestuto for assistance in the field. T.G. would like to dedicate this paper to his friend and companion during the field observations, the late Jeroen Kroese. We thank J. A. Baker, I. G. Jamieson and two anonymous referees for useful comments on the manuscript. T.G. gratefully acknowledges M. M. Soeting for moral support and the Albach family for shelter. S.F. thanks J. M c O u a t for both. The research was partially supported by a Research Service Award from N I M H to S.F.
REFERENCES Van den Assem, J. 1967. Territoriality in the three-spined stickleback Gasterosteus aculeatus L. An experimental
795
study in intra-specific competition. Behaviour, Suppl., 16, 1 164. Austad, S. N. 1984. A classification of alternative reproductive behaviors and methods for field-testing ESS models. Am. Zool., 24, 309-319. Dominey, W. J. 1984. Alternative mating tactics and evolutionary stable strategies. Am. Zool., 24, 385 396. Goldschmidt, T., Bakker, Th. C. M. & Feuth-de Bruijn, E. In press. Selective copying in mate choice of female stickleback? Anita. Behav. Jamieson, I. G. & Colgan, P. W. 1989. Eggs in the nests of males and their effect on mate choice in the three-spined stickleback. Anita. Behav., 38, 859 865. Li, S. K. & Owings, D. H. 1978. Sexual selection in the three-spined stickleback, II. Nest raiding during the courtship phase. Behaviour, 64, 298-304. Ridley, M. & Rechten, C. 1981. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour, 76, 152-161. Rohwer, S. 1978. Parent cannibalism of offspring and egg raiding as a courtship strategy. Am. Nat., 112, 429~440. Tinbergen, N. 1951. The Study of Instinct. London: Clarendon Press. Zar, J. H. 1984. Biostatistical Analysis. Englewood Cliffs, New Jersey: Prentice-Hall.