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Visual assessment of fighting ability in the cichlid fish Nannacara anomala
Animal Behaviour, 35, 4
1262
M. Vallieres, J. Kimmel and A. Shah for collecting data and maintaining the birds; and P. Colgan, R. Beninger, S. I. Rothstein and M. J. West for useful comments on the manuscript. LAURENE RATCLIFFE* RON WEISMAN'~
* Department o f Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada. t Department o f Psychology, Queen's" University, Kingston, Ontario K7L 3??6, Canada. References Becker, P. H. 1982. The coding of species-specific characteristics in bird sounds. In: Acoustic Communication in Birds, Vol. 1 (Ed. by D. E. Kroodsma & E. H. Miller), pp. 213-252. New York: Academic Press. King, A. P. & West, M. J. 1986. The experience of experience: an exogenetic program for social competence. In: Perspectives in Ethology, Vol. 7 (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 153-182, New York: Plenum Press. Rothstein, S. I., Yokel, D. A. & Fleischer, R. C. 1986. Social dominance, mating and spacing systems, female fecundity, and vocal dialects in captive and freeranging brown-headed cowbirds. Curr. Ornithol., 3, 127 185. Searcy, W. A. & Marler, P. 1981. A test for responsiveness to song structure and programming in female sparrows. Science, N. Y., 213, 92(~928. West, M. J., King, A. P., Eastzer, D. H. & Staddon, J. E. R. 1979. A bioassay of isolate cowbird song. J. comp. physiol. Psychol., 93, 124 133. (Received 12 September 1986; revised 7 January 1987," MS. number." AS-423)
Visual Assessment of Fighting Ability in the Cichlid Fish Nannacara anomala Recent theorizing about the evolution of fighting strategies in animals has strongly emphasized the importance of traits that allow assessment of fighting ability (Parker 1974; Maynard Smith & Parker 1976; Enquist & Leimar 1983). Empirical studies also show that assessment of fighting ability occurs during fights. Relative fighting ability can be defined as the opponents' relative ability to injure each other. Assessment of fighting ability may, however, be based not only on the result of attempts to injure each other but also on variables correlated with fighting ability. Such indirect assessment of fighting ability seems to be a nearly universal phenomenon and may be based on trials of strength, the ability to perform activities such as calling, and on size assessment (e.g. Parker 1974; Davies & Halliday 1978; Clutton-Brock & Albon 1979; Krebs & Dawkins 1984). In this paper we consider visual assessment of size by male cichlid fish Nannacara anomala. We used the traditional ethological technique of letting individuals interact through a glass partition to determine the extent to which the fish visually assess their opponent's size during fighting. Details of fighting behaviour of N. anomala have been described by Jakobsson et al. (1979) and Enquist & Jakobsson (1986). The origin of the fish, housing conditions and experimental routine are described in Enquist & Jakobsson (1986) and will only be summarized here. The fish used weighed 1-6 g. In all, 24 pairs of males were studied, with weight ratios (weight of lighter fish/weight of heavier fish) equally distributed in the range 0.20-0.70. The test aquarium
Table I. Correlations between various ratios and the outcome of interactions and between various size variables and weight
Size variable Weight Dorsal fin area Caudal fin area Body area Total area?
Rank correlation between ratio* Correlation between size variable and outcome and weight N=24 N=50 0.81 0.73 0.61 0.82 0.77
1.00 0.93 0-85 0.98 0.94
All rank correlations are significant at P < 0.001. * Each ratio is the weight of the smaller fish divided by the size variable of the larger fish (see text for details). t The area of the dorsal fin, the caudal fin and the body.
Short Communications was divided down the middle by an opaque partition. On the day before a test two male fish were chosen and one placed in each part. The aquarium contained two metal boxes which were used to close in the fish before the test. The opaque partition was then exchanged for a glass one. Both boxes were opened slowly and simultaneously and the interaction between the fish was filmed on video for half an hour or until one fish gave up. Giving up is associated with clear changes in behaviour and coloration. By removing the glass partition, we allowed the fish to fight after each test. For analysis, the outcomes of the interactions were divided into three categories: the smaller fish (1) gave up without showing any agonistic behaviour, (2) gave up after some interaction (0-5 rain) including lateral display and tail beating, and (3) did not give up. The results show that when the weight of the smaller fish was more than 50% of the weight of the larger one, it never gave up ( N = 7). When the smaller fish was 40 50% of the weight of the larger one, it gave up immediately in two cases, after some interaction in three cases, and did not give up in two cases. When the smaller fish was less than 40% of the weight of the larger fish, it always gave up. In eight of these cases it gave up immediately and in two cases after some interaction. The outcomes of the interactions show a highly significant correlation with relative difference in weight (see Table I). The result agrees with previous studies of the fighting behaviour of N. anomala. For example, Enquist et al. (unpublished data) staged 20 fights between fish with weight ratios of 0.45, and 40% of these ended without any tailbeating, biting, or mouth-wrestling. Although the fishes seem to estimate fighting ability by visual assessment of size the precision appears to be quite low. With a weight difference of only 10% a human observer can usually detect a size difference. In contrast, when the weight of the smaller fish is only half that of the heavier one, fights normally continue beyond the visual assessment stage. The discrepancy may arise because the fish have poor information about their own size. It might also be that in nature, variation in physical condition, as well as variation in weight, affects fighting ability. To see what variables the fish use when visually assessing fighting ability we calculated the rank correlation between the outcome (ranked I-3 as above) and various size measures of the larger fish divided by the weight of the smaller fish. We assumed that experience of own size is most related to weight. To obtain the various size measures, the fish were photographed after the test with erected fins in a thin glass chamber with transparent graphpaper attached to one of the walls. The different
1263
areas of a fish were then measured by counting the number of ram-squares covered on the photographs. The analysis (Table I) shows that weight and body area of the opponent gave the highest rank correlations with the outcome of the interaction, 0.81 and 0-82 respectively, whereas total area (body plus fins), area of the caudal fin only and dorsal fin only were less well correlated with the result of the interaction. In N. anomala the best predictor of the outcome of a fight is the weight relationship of the opponents. When the smaller fish is 90% of the weight of the heavier one, it wins less than 10% of the fights. Differences in other size parameters are less reliable predictors of the outcome (Enquist, unpublished data). With respect to this information, it is of some interest to see how well different size measures correlate with weight. We would expect the fish to be most sensitive to size measures highly correlated with weight during assessment. Correlations calculated from an independent sample of 50 fish are given in Table I. The strongest relationship is between weight and body area, whereas area of fins and total area were less well correlated with weight. In conclusion, N. anomala are able to estimate relative fighting ability by visual assessment alone. However, the precision is quite low. Furthermore, the fish were most sensitive to the area of the body which is better correlated with fighting ability than the area of fins. This will decrease the adaptive value of enlarging the fins in order to bluff the opponent. We thank Anthony Arak and Bj6rn Forkman for comments on the manuscript. The study had financial support from the Swedish Natural Science Research Council.
MAGNUS ENQUIST TOMASLJUNGBERG ANNALENAZANDOR
Department o f Zoology, Division of Ethology, University of Stockholm, Stockholm, S-106 91 Sweden. References Clutton-Brock, T. H. & Albon, S. D. 1979. The roaring of the red deer and the evolution of honest advertisement. Behaviour, 69, 145-169. Davies, N. B. & Halliday, T. R. 1978. Deep croaks and fighting assessment in toads Bulb bufo. Nature, Lond., 274, 683-685. Enquist, M. & Jakobsson, S. 1986. Assessment of fighting ability in the cichlid fish Nannacara anomala. Ethology, 72, 143 153. Enquist, M. & Leimar, O. 1983. Evolution of fighting
1264
Animal Behaviour, 35, 4
behaviour: decision rules and assessment of relative strength. J. theor. Biol., 102, 387-410. Jakobsson, S., Rades~ter, T. & J/irvi, T. t979. On the fighting behaviour of Nannacara anomala (Pisces, Cichlidae) males. Z. Tierpsychol., 49, 210220. Krebs, J. R. & Dawkins, R. 1984. Animals signals: mindreading and manipulation. In: Behavioural Ecology. 2nd edn (Ed. by J. R. Krebs & N. B. Davies), pp. 380402. Oxford: Blackwei1 Scientific Publications. Maynard Smith, J. & Parker, G. A. 1976. The logic of asymmetric contests. Anim. Behav., 24, 159-175. Parker, G. A. 1974. Assessment strategy and the evolution of fighting behaviour. J. theor. Biol., 47, 223243. (Received 21 October 1986; revised 29 December 1986," MS. number." s~-343) Effects of Deafening on the Contact Call of the Budgerigar, Melopsittaeus undulatus Vocal development is rigid and inflexible in some species of birds (i.e. the domestic chicken, Gallus domesticus, ring dove, Streptopelia risoria, and turkey, Meleagris gallopavo) while in others, notably songbirds, vocal development is guided by learning and is often critically dependent on the influence of the auditory environment (Konishi 1978, 1985). Many psittacines, including the budgerigar, Melopsittacus undulatus, are known for their ability to mimic a variety of sounds including human speech. Yet, so far as we know, the classic experiments of deafening, isolation-rearing and song tutoring aimed at delineating the roles of auditory feedback and external acoustic models have not been conducted with psittacines. One tutoring experiment has shown that budgerigars can imitate tonal patterns and song segments from other avian species (Gramza 1970), so it would not be too surprising if this mimetic capacity is also involved in the development of species-specific vocalizations. As a first step in comparing vocal development in budgerigars with that of songbirds, we sought to determine whether hearing is required for the development of normal vocalizations. Two 3-week-old male budgerigars from different broods were taken fi'om their nest boxes and deafened bilaterally by extirpation of the cochlea. The procedure for deafening the birds was similar to that described in detail by Konishi (1964). Briefly, the birds were anaesthetized with chloropent and mounted on a homemade operating table. An incision was made behind the ear exposing the neck muscles. The neck muscles were displaced, allowing access to the underlying skull. A window was cut in the skull near the crossing point of the external semicircular canals. The budgerigars were slightly different from other birds described by Konishi (1964) in that large blood sinuses in the
vicinity of the semicircular canals hampered direct access to the cochlea. All minor bleeding complications which occurred were resolved during the surgery and no post-operative complications were noted. Cochlear removals were confirmed by examination and identification of basilar papilla material under the dissecting microscope. At the conclusion of surgery, the birds were watched continuously for 1 h while they recovered from the effects of anaesthesia and then returned to their respective nest boxes. Each bird was monitored closely for the next few days to ensure that it was being fed by its parents. Each bird was allowed to develop without further experimental interference. As further evidence that the surgery was not unduly traumatic, the deafened birds fledged on schedule with their respective siblings at about 5 weeks of age (2 weeks following surgery). They were then placed in a large flight cage of about 25 budgerigars of mixed sexes, but similar ages. At the time of fledging, neither deafened bird showed any evidence of vestibular or behavioural disorders. Calls were recorded with a Tandberg Model 15 tape-recorder at a tape speed of 7-5 ips with a Uher Model M-139 microphone using Scotch Brand number 206 recording tape. A bird was placed in a small holding cage within view but several metres away from a larger cage containing several other budgerigars. Both hearing and deafened budgerigars would readily utter contact calls under these conditions, though deafened birds tended to vocalize less frequently than birds with normal hearing. Seven contact calls were recorded from each of the two deafened birds. Recording sessions for deafened birds were spaced over a period of several weeks as a check on the stability of these calls. A typical contact call from each deafened budgerigar (RD85-15 and RD85-16) is shown in Fig. 1. Contact calls were analysed with a Kay Elemetrics Digital Sonagraph using a 300 Hz analysis bandwidth and the print-expanded mode. Measurements were taken of the highest frequency, lowest frequency, bandwidth (highest frequency minus lowest frequency), duration and the number of tonal elements in the call. Tonal elements were defined as continuous traces on an expanded sonagram where the instantaneous bandwidth (and a first harmonic if present) never exceeded 500 Hz. For example, the number of tonal elements for the calls (from left to right) in Fig. 1A are five, zero and four. For the sonagrams in Fig. 1B, the number of tonal elements are four, one and five. The average rating of the three scorers served as a measure of the number of tonal elements in the call. Interestingly, discontinuous traces on the sonagram were almost always associated with a change in frequency.
1262
M. Vallieres, J. Kimmel and A. Shah for collecting data and maintaining the birds; and P. Colgan, R. Beninger, S. I. Rothstein and M. J. West for useful comments on the manuscript. LAURENE RATCLIFFE* RON WEISMAN'~
* Department o f Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada. t Department o f Psychology, Queen's" University, Kingston, Ontario K7L 3??6, Canada. References Becker, P. H. 1982. The coding of species-specific characteristics in bird sounds. In: Acoustic Communication in Birds, Vol. 1 (Ed. by D. E. Kroodsma & E. H. Miller), pp. 213-252. New York: Academic Press. King, A. P. & West, M. J. 1986. The experience of experience: an exogenetic program for social competence. In: Perspectives in Ethology, Vol. 7 (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 153-182, New York: Plenum Press. Rothstein, S. I., Yokel, D. A. & Fleischer, R. C. 1986. Social dominance, mating and spacing systems, female fecundity, and vocal dialects in captive and freeranging brown-headed cowbirds. Curr. Ornithol., 3, 127 185. Searcy, W. A. & Marler, P. 1981. A test for responsiveness to song structure and programming in female sparrows. Science, N. Y., 213, 92(~928. West, M. J., King, A. P., Eastzer, D. H. & Staddon, J. E. R. 1979. A bioassay of isolate cowbird song. J. comp. physiol. Psychol., 93, 124 133. (Received 12 September 1986; revised 7 January 1987," MS. number." AS-423)
Visual Assessment of Fighting Ability in the Cichlid Fish Nannacara anomala Recent theorizing about the evolution of fighting strategies in animals has strongly emphasized the importance of traits that allow assessment of fighting ability (Parker 1974; Maynard Smith & Parker 1976; Enquist & Leimar 1983). Empirical studies also show that assessment of fighting ability occurs during fights. Relative fighting ability can be defined as the opponents' relative ability to injure each other. Assessment of fighting ability may, however, be based not only on the result of attempts to injure each other but also on variables correlated with fighting ability. Such indirect assessment of fighting ability seems to be a nearly universal phenomenon and may be based on trials of strength, the ability to perform activities such as calling, and on size assessment (e.g. Parker 1974; Davies & Halliday 1978; Clutton-Brock & Albon 1979; Krebs & Dawkins 1984). In this paper we consider visual assessment of size by male cichlid fish Nannacara anomala. We used the traditional ethological technique of letting individuals interact through a glass partition to determine the extent to which the fish visually assess their opponent's size during fighting. Details of fighting behaviour of N. anomala have been described by Jakobsson et al. (1979) and Enquist & Jakobsson (1986). The origin of the fish, housing conditions and experimental routine are described in Enquist & Jakobsson (1986) and will only be summarized here. The fish used weighed 1-6 g. In all, 24 pairs of males were studied, with weight ratios (weight of lighter fish/weight of heavier fish) equally distributed in the range 0.20-0.70. The test aquarium
Table I. Correlations between various ratios and the outcome of interactions and between various size variables and weight
Size variable Weight Dorsal fin area Caudal fin area Body area Total area?
Rank correlation between ratio* Correlation between size variable and outcome and weight N=24 N=50 0.81 0.73 0.61 0.82 0.77
1.00 0.93 0-85 0.98 0.94
All rank correlations are significant at P < 0.001. * Each ratio is the weight of the smaller fish divided by the size variable of the larger fish (see text for details). t The area of the dorsal fin, the caudal fin and the body.
Short Communications was divided down the middle by an opaque partition. On the day before a test two male fish were chosen and one placed in each part. The aquarium contained two metal boxes which were used to close in the fish before the test. The opaque partition was then exchanged for a glass one. Both boxes were opened slowly and simultaneously and the interaction between the fish was filmed on video for half an hour or until one fish gave up. Giving up is associated with clear changes in behaviour and coloration. By removing the glass partition, we allowed the fish to fight after each test. For analysis, the outcomes of the interactions were divided into three categories: the smaller fish (1) gave up without showing any agonistic behaviour, (2) gave up after some interaction (0-5 rain) including lateral display and tail beating, and (3) did not give up. The results show that when the weight of the smaller fish was more than 50% of the weight of the larger one, it never gave up ( N = 7). When the smaller fish was 40 50% of the weight of the larger one, it gave up immediately in two cases, after some interaction in three cases, and did not give up in two cases. When the smaller fish was less than 40% of the weight of the larger fish, it always gave up. In eight of these cases it gave up immediately and in two cases after some interaction. The outcomes of the interactions show a highly significant correlation with relative difference in weight (see Table I). The result agrees with previous studies of the fighting behaviour of N. anomala. For example, Enquist et al. (unpublished data) staged 20 fights between fish with weight ratios of 0.45, and 40% of these ended without any tailbeating, biting, or mouth-wrestling. Although the fishes seem to estimate fighting ability by visual assessment of size the precision appears to be quite low. With a weight difference of only 10% a human observer can usually detect a size difference. In contrast, when the weight of the smaller fish is only half that of the heavier one, fights normally continue beyond the visual assessment stage. The discrepancy may arise because the fish have poor information about their own size. It might also be that in nature, variation in physical condition, as well as variation in weight, affects fighting ability. To see what variables the fish use when visually assessing fighting ability we calculated the rank correlation between the outcome (ranked I-3 as above) and various size measures of the larger fish divided by the weight of the smaller fish. We assumed that experience of own size is most related to weight. To obtain the various size measures, the fish were photographed after the test with erected fins in a thin glass chamber with transparent graphpaper attached to one of the walls. The different
1263
areas of a fish were then measured by counting the number of ram-squares covered on the photographs. The analysis (Table I) shows that weight and body area of the opponent gave the highest rank correlations with the outcome of the interaction, 0.81 and 0-82 respectively, whereas total area (body plus fins), area of the caudal fin only and dorsal fin only were less well correlated with the result of the interaction. In N. anomala the best predictor of the outcome of a fight is the weight relationship of the opponents. When the smaller fish is 90% of the weight of the heavier one, it wins less than 10% of the fights. Differences in other size parameters are less reliable predictors of the outcome (Enquist, unpublished data). With respect to this information, it is of some interest to see how well different size measures correlate with weight. We would expect the fish to be most sensitive to size measures highly correlated with weight during assessment. Correlations calculated from an independent sample of 50 fish are given in Table I. The strongest relationship is between weight and body area, whereas area of fins and total area were less well correlated with weight. In conclusion, N. anomala are able to estimate relative fighting ability by visual assessment alone. However, the precision is quite low. Furthermore, the fish were most sensitive to the area of the body which is better correlated with fighting ability than the area of fins. This will decrease the adaptive value of enlarging the fins in order to bluff the opponent. We thank Anthony Arak and Bj6rn Forkman for comments on the manuscript. The study had financial support from the Swedish Natural Science Research Council.
MAGNUS ENQUIST TOMASLJUNGBERG ANNALENAZANDOR
Department o f Zoology, Division of Ethology, University of Stockholm, Stockholm, S-106 91 Sweden. References Clutton-Brock, T. H. & Albon, S. D. 1979. The roaring of the red deer and the evolution of honest advertisement. Behaviour, 69, 145-169. Davies, N. B. & Halliday, T. R. 1978. Deep croaks and fighting assessment in toads Bulb bufo. Nature, Lond., 274, 683-685. Enquist, M. & Jakobsson, S. 1986. Assessment of fighting ability in the cichlid fish Nannacara anomala. Ethology, 72, 143 153. Enquist, M. & Leimar, O. 1983. Evolution of fighting
1264
Animal Behaviour, 35, 4
behaviour: decision rules and assessment of relative strength. J. theor. Biol., 102, 387-410. Jakobsson, S., Rades~ter, T. & J/irvi, T. t979. On the fighting behaviour of Nannacara anomala (Pisces, Cichlidae) males. Z. Tierpsychol., 49, 210220. Krebs, J. R. & Dawkins, R. 1984. Animals signals: mindreading and manipulation. In: Behavioural Ecology. 2nd edn (Ed. by J. R. Krebs & N. B. Davies), pp. 380402. Oxford: Blackwei1 Scientific Publications. Maynard Smith, J. & Parker, G. A. 1976. The logic of asymmetric contests. Anim. Behav., 24, 159-175. Parker, G. A. 1974. Assessment strategy and the evolution of fighting behaviour. J. theor. Biol., 47, 223243. (Received 21 October 1986; revised 29 December 1986," MS. number." s~-343) Effects of Deafening on the Contact Call of the Budgerigar, Melopsittaeus undulatus Vocal development is rigid and inflexible in some species of birds (i.e. the domestic chicken, Gallus domesticus, ring dove, Streptopelia risoria, and turkey, Meleagris gallopavo) while in others, notably songbirds, vocal development is guided by learning and is often critically dependent on the influence of the auditory environment (Konishi 1978, 1985). Many psittacines, including the budgerigar, Melopsittacus undulatus, are known for their ability to mimic a variety of sounds including human speech. Yet, so far as we know, the classic experiments of deafening, isolation-rearing and song tutoring aimed at delineating the roles of auditory feedback and external acoustic models have not been conducted with psittacines. One tutoring experiment has shown that budgerigars can imitate tonal patterns and song segments from other avian species (Gramza 1970), so it would not be too surprising if this mimetic capacity is also involved in the development of species-specific vocalizations. As a first step in comparing vocal development in budgerigars with that of songbirds, we sought to determine whether hearing is required for the development of normal vocalizations. Two 3-week-old male budgerigars from different broods were taken fi'om their nest boxes and deafened bilaterally by extirpation of the cochlea. The procedure for deafening the birds was similar to that described in detail by Konishi (1964). Briefly, the birds were anaesthetized with chloropent and mounted on a homemade operating table. An incision was made behind the ear exposing the neck muscles. The neck muscles were displaced, allowing access to the underlying skull. A window was cut in the skull near the crossing point of the external semicircular canals. The budgerigars were slightly different from other birds described by Konishi (1964) in that large blood sinuses in the
vicinity of the semicircular canals hampered direct access to the cochlea. All minor bleeding complications which occurred were resolved during the surgery and no post-operative complications were noted. Cochlear removals were confirmed by examination and identification of basilar papilla material under the dissecting microscope. At the conclusion of surgery, the birds were watched continuously for 1 h while they recovered from the effects of anaesthesia and then returned to their respective nest boxes. Each bird was monitored closely for the next few days to ensure that it was being fed by its parents. Each bird was allowed to develop without further experimental interference. As further evidence that the surgery was not unduly traumatic, the deafened birds fledged on schedule with their respective siblings at about 5 weeks of age (2 weeks following surgery). They were then placed in a large flight cage of about 25 budgerigars of mixed sexes, but similar ages. At the time of fledging, neither deafened bird showed any evidence of vestibular or behavioural disorders. Calls were recorded with a Tandberg Model 15 tape-recorder at a tape speed of 7-5 ips with a Uher Model M-139 microphone using Scotch Brand number 206 recording tape. A bird was placed in a small holding cage within view but several metres away from a larger cage containing several other budgerigars. Both hearing and deafened budgerigars would readily utter contact calls under these conditions, though deafened birds tended to vocalize less frequently than birds with normal hearing. Seven contact calls were recorded from each of the two deafened birds. Recording sessions for deafened birds were spaced over a period of several weeks as a check on the stability of these calls. A typical contact call from each deafened budgerigar (RD85-15 and RD85-16) is shown in Fig. 1. Contact calls were analysed with a Kay Elemetrics Digital Sonagraph using a 300 Hz analysis bandwidth and the print-expanded mode. Measurements were taken of the highest frequency, lowest frequency, bandwidth (highest frequency minus lowest frequency), duration and the number of tonal elements in the call. Tonal elements were defined as continuous traces on an expanded sonagram where the instantaneous bandwidth (and a first harmonic if present) never exceeded 500 Hz. For example, the number of tonal elements for the calls (from left to right) in Fig. 1A are five, zero and four. For the sonagrams in Fig. 1B, the number of tonal elements are four, one and five. The average rating of the three scorers served as a measure of the number of tonal elements in the call. Interestingly, discontinuous traces on the sonagram were almost always associated with a change in frequency.