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Asymmetries of eye use in birds
1582
Animal Behaviour, 34, 5
more attractive to females (Downhover & Brown 1981). What is the adaptive significance of this female behaviour? According to Ridley (1978), females of polygynous species, which preferentially mate with males who are already caring for eggs, are choosing males who have proved their ability to seduce other females (and, therefore, to generate seductive sons), and who are prepared to care for (rather than to desert) the eggs. An alternative explanation (Rohwer 1978) is that by adding her eggs to a pre-existing clutch, a female reduces the chances of her eggs being eaten by the parental male or other individuals through a 'diluting effect'. Both filial- and hetero-cannibalism have been reported for the genus Cottus (Morris 1954; Brown 1981) and previous data (Marconato 1985) have shown that the hatching percentage in nests of C. gobio increases with increasing number of egg masses. The reduction of intraspecific predation on their eggs may thus be sufficient to account for the preference of female C. gobio for spawning with males whose nests contain eggs. Whether the seductive qualities of males also play a role in determining the female's preference in this species, as suggested from field data (Marconato & Rasotto 1983), remains to be determined. We are grateful to Guglielmo Marin, Giorgio Malacarne, Lorenzo Colombo and Mario Zanforlin for their critical reading of the manuscript. ANDREA MARCONATO* ANaELO BISAZZA'~ * Dipartimento di Biologia, Universit~t di Padova, via Loredan 10, Padova, Italy. t Dipartimento di Psicologia Generale, Universith di Padova, P. za Capitaniato, 3, Padova, Italy.
References Brown, L. 1981. Patterns of female choice in mottled sculpins (Cottidae, Teleostei). Anim. Behav., 29, 375 382. Downhover, J. F. & Brown, L. 1979. Seasonal changes in the social structure of a mottled sculpin (Cottus bairdi) population. Anim. Behav., 27, 451-458. Downhover, J. F. & Brown, L. 1981. The timing of reproduction and its behavioural consequences for mottled sculpins Cottus bairdi. In: Natural Selection and Social Behavior (Ed. by R. D. Alexander & D. W. Tinkle), pp. 78-95. New York: Chiron Press. Halliday, T. R. 1983. The study of mate choice. In: Mate Choice (Ed. by P. Bateson), pp. 3-32. Cambridge: Cambridge University Press.
Hunter, J. R. 1963. The reproductive behaviour of green sunfish Lepomis cyanellus. Zoologica, 48, 13-24. Marconato, A. 1985. Reproductive behaviour and mate choice in Cottus gobio (Pisces, Cottidae). Monit. Zool. Ital. (N.S.), 19, 60-61. Marconato, A. & Rasotto, M. 1983. Mating preferences of the female river bullhead, Cottus gobio (Cottidae, Teleostei). Boll. Zool., 50, 51-54. Morris, D. 1954. The reproductive behaviour of the river bullhead (Cottus gobio), with special reference to the fanning activity. Behaviour, 7, 1 32. Ridley, M. 1978. Paternal care. AnOn. Behav., 26, 904932. Ridley, M. & Retchen, C. 1981. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour, 76, 152-161. Rohwer, S. 1978.Parent cannibalism of offspringand egg raiding as a courtship strategy. Am. Nat., 112, 429-440. (Receh)ed 30 January 1986; revised 25 March 1986; MS. number sc-289)
Asymmetries of Eye Use in Birds Lateralization of function in the central nervous system of birds was first described for the control of song (Nottebohm 1971). It is also marked in visually evoked behaviour in the domestic chick, affecting both the analysis of information (Andrew 1983a) and the likelihood of performance of species-specific behaviour such as copulation or fear responses (Rogers & Anson 1979; Andrew et al. 1982). Such specialization is revealed not only by damaging one hemisphere but also by comparing the effects of a stimulus presented to the right or left eye. Birds sometimes move their eyes independently when scanning (Andrew et al. 1982 and references therein), suggesting that lateralization might be accompanied by preferential use of right or left eye according to need. We report here evidence for such effects. Courtship in the zebra finch (Taeniopygiagu ttata eastanotis) begins with a silent 'static' phase (Morris 1954) in which the male presents his flank to the female, viewing her with one eye only. In the 'dynamic' phase, he pivots about the point of perching, fixating the female with each eye in turn. Twelve pairs of zebra finches were housed in wiremesh cages ( 6 2 x 4 2 • cm) on a 12-h light: 12-h dark cycle. Courtship occurred on two perches, which ran parallel to the cage front. Observations were made for 1 h in the afternoon over a period of 3 months, involving some 40 h of observation. All recorded static phases are shown in Fig. 1. There was a significant tendency for the whole population of males to use the right eye (departure from 1:1 ratio, Gp=24.08, P<0.02, goodness-of-fit, Sokal & Rohlf 1981). Significant
Short Communications
1583
E ~ ] FLIGHT EYE m
g
LEFT
EYE
10
E
Individual males
Cock fixating hen
between bouta of courtship dance
Figure 1. Total number of monocular fixations during static phase for 12 male zebra finches. heterogeneity (Gh = 50.81, P < 0.001) was due to one male which had a significant tendency to use the left eye: all other significant asymmetries (six) involved right-eye preference. Male and female almost always faced in the same direction during static phases, so that the female usually viewed the male with her left eye. It is possible therefore that the behaviour of females contributes to the observed asymmetry. However, the male chooses on which side of the female to land and then actively approaches, whilst the female tends to move little. Courtship displays in which the male presents one flank towards the female are widespread in passerines (see review in Andrew 1961); the possibility that they involve the preferred presentation of one flank deserves study. In the zebra finch it is impossible as yet to distinguish between three possible causal explanations: (1) the orientation of the display depends on a motor bias; (2) the right eye is preferentially used in fixating any stimulus to which response is to be directed; (3) the right eye is preferentially used only in certain types of situation, which include courtship. The Phasianidae, including the domestic fowl, also have laterally oriented courtship displays (Kruijt 1963). In the case of the domestic fowl we have experimental evidence which supports explanation 3. Young domestic chicks (Hi Sex: two replications, N = 20,24) were injected with 12.5 mg testosterone oenanthate, which results in circulating levels of androgens in the adult range (Andrew 1983b). In the first type of test, a block 7 x 11 x 4 cm covered with yellow towelling was presented for 45 s: such a stimulus evokes circling (low intensity courtship waltz) and copulation. In the second the chick was placed with another testosterone-treated
chick for 90 s; this evokes circling, fixation of the partner's nape and aggressive sparring. Copulation, circling and sparring are fully described by Andrew (1975). In both replications the right eye was preferentially used by the whole population of chicks in circling the model (P < 0-01, P < 0.005; Wilcoxon two-tailed) but the left eye was used in circling the other chick (P<0"005, in both cases). In the absence of model or other chick, chicks showed equal numbers of right and left turns during locomotion. Neither of the asymmetries is therefore likely to represent an asymmetry present in spontaneous locomotion, such as has been reported for the rat (see review in Robinson et al. 1985). They are potentially explicable instead in two broadly different ways: they may depend on differences in the evoked behaviour (e.g. copulation versus attack) or in the perceptual properties of the stimuli. L. Workman was supported by a studentship from the SERC. L. WORKMAN R. J. ANDREW
School of Biological Sciences, University of Sussex, Brighton, Sussex, U.K.
References Andrew, R. J. 1961. The displays given by passerines in courtship and reproductive fighting:a review. Ibis, 103, 315-348, 549-579. Andrew, R. J. 1975. Effects of testosterone on the
1584
Animal Behaviour, 34, 5
behaviour of the domestic chick. I. Effects present in males but not in females. Anita. Behav., 24, 139-155. Andrew, R. J. 1983a. Lateralization of emotional and cognitive function in higher vertebrates, with special reference to the domestic chick. In: Advances in Vertebrate Neuroethology (Ed. by J.-P. Ewert, R. R. Capranica & D. J. Ingle), pp. 477-509. London: Plenum Press. Andrew, R. J. 1983b. Specific short-latency effects of oestradiol and testosterone on distractibility and memory formation in the young domestic chick. In: Hormones and Behaviour in Higher Vertebrates (Ed. by J. Balthazart, E. Pr6ve & R. Gillies), pp. 463~473. Berlin: Springer-Verlag. Andrew, R. J., Mench, J. & Rainey, C. 1982. Right-left asymmetry of response to visual stimuli in the domestic chick. In: Analysis of Visual Behaviour (Ed. by D. J. Ingle, M. A. Goodale and R. J. W. Mansfield), pp. 197 210. Cambridge, Massachusetts: Massachusetts Institute of Technology Press. Kruijt, J. P. 1963. Notes o f wing display in the courtship of pheasants. Avicult. Mag. January-February, pp. 1120.
Morris, D. 1954. The reproductive behaviour of the zebra finch, with special reference to pseudofemale behaviour and displacement activities. Behaviour, 6, 271-322. Nottebohm, F. 1971. Neural lateralization of vocal control in a passerine bird I: song. J. Exp. Zool., 177, 229562. Robinson, T. E., Becker, J. B., Camp, D. M. & Mansour, A. 1985. Variation in the pattern of behavioral and brain asymmetries due to sex differences. In: Cerebral Lateralization in Nonhuman Species (Ed. by S. D. Glick), pp. 185-231. New York: Academic Press. Rogers, L. J. & Anson, J. M. 1979. Lateralisation of function in the chicken forebrain. Pharmacol. Biochem. Behav., I0, 679-868. Sokal, R. R. & Rohlf, F. J. 1981. Biometry: The Principle and Practice of Statistics in Biological Research. New York: W. H. Freeman.
(Received 10 February 1986; revised 9 April 1986; MS. number: sc-290)
photobyHugovanLawick
The Chimpanzees of Gombe Patterns of Behavior JANE GOODALL Dr Goodall now crowns her first quarter-century with the chimpanzees of Gombe by giving this comprehensive, up-to-date account of her unique work. The surprising findings of the last few years such as cannibalism, intergroup aggression and new heights of cognitive ability - are presented for the first time in book form. Belknap s Hardback 688ppillus. 0-674-11649-6 Available in N. Americafrom: 79 GardenStreet, Cambridge. MA 02138 $30.00
HARVARD UNIVERSITYPRESS 126 BuckinghamPalace Road London SW1W 9SD
Animal Behaviour, 34, 5
more attractive to females (Downhover & Brown 1981). What is the adaptive significance of this female behaviour? According to Ridley (1978), females of polygynous species, which preferentially mate with males who are already caring for eggs, are choosing males who have proved their ability to seduce other females (and, therefore, to generate seductive sons), and who are prepared to care for (rather than to desert) the eggs. An alternative explanation (Rohwer 1978) is that by adding her eggs to a pre-existing clutch, a female reduces the chances of her eggs being eaten by the parental male or other individuals through a 'diluting effect'. Both filial- and hetero-cannibalism have been reported for the genus Cottus (Morris 1954; Brown 1981) and previous data (Marconato 1985) have shown that the hatching percentage in nests of C. gobio increases with increasing number of egg masses. The reduction of intraspecific predation on their eggs may thus be sufficient to account for the preference of female C. gobio for spawning with males whose nests contain eggs. Whether the seductive qualities of males also play a role in determining the female's preference in this species, as suggested from field data (Marconato & Rasotto 1983), remains to be determined. We are grateful to Guglielmo Marin, Giorgio Malacarne, Lorenzo Colombo and Mario Zanforlin for their critical reading of the manuscript. ANDREA MARCONATO* ANaELO BISAZZA'~ * Dipartimento di Biologia, Universit~t di Padova, via Loredan 10, Padova, Italy. t Dipartimento di Psicologia Generale, Universith di Padova, P. za Capitaniato, 3, Padova, Italy.
References Brown, L. 1981. Patterns of female choice in mottled sculpins (Cottidae, Teleostei). Anim. Behav., 29, 375 382. Downhover, J. F. & Brown, L. 1979. Seasonal changes in the social structure of a mottled sculpin (Cottus bairdi) population. Anim. Behav., 27, 451-458. Downhover, J. F. & Brown, L. 1981. The timing of reproduction and its behavioural consequences for mottled sculpins Cottus bairdi. In: Natural Selection and Social Behavior (Ed. by R. D. Alexander & D. W. Tinkle), pp. 78-95. New York: Chiron Press. Halliday, T. R. 1983. The study of mate choice. In: Mate Choice (Ed. by P. Bateson), pp. 3-32. Cambridge: Cambridge University Press.
Hunter, J. R. 1963. The reproductive behaviour of green sunfish Lepomis cyanellus. Zoologica, 48, 13-24. Marconato, A. 1985. Reproductive behaviour and mate choice in Cottus gobio (Pisces, Cottidae). Monit. Zool. Ital. (N.S.), 19, 60-61. Marconato, A. & Rasotto, M. 1983. Mating preferences of the female river bullhead, Cottus gobio (Cottidae, Teleostei). Boll. Zool., 50, 51-54. Morris, D. 1954. The reproductive behaviour of the river bullhead (Cottus gobio), with special reference to the fanning activity. Behaviour, 7, 1 32. Ridley, M. 1978. Paternal care. AnOn. Behav., 26, 904932. Ridley, M. & Retchen, C. 1981. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour, 76, 152-161. Rohwer, S. 1978.Parent cannibalism of offspringand egg raiding as a courtship strategy. Am. Nat., 112, 429-440. (Receh)ed 30 January 1986; revised 25 March 1986; MS. number sc-289)
Asymmetries of Eye Use in Birds Lateralization of function in the central nervous system of birds was first described for the control of song (Nottebohm 1971). It is also marked in visually evoked behaviour in the domestic chick, affecting both the analysis of information (Andrew 1983a) and the likelihood of performance of species-specific behaviour such as copulation or fear responses (Rogers & Anson 1979; Andrew et al. 1982). Such specialization is revealed not only by damaging one hemisphere but also by comparing the effects of a stimulus presented to the right or left eye. Birds sometimes move their eyes independently when scanning (Andrew et al. 1982 and references therein), suggesting that lateralization might be accompanied by preferential use of right or left eye according to need. We report here evidence for such effects. Courtship in the zebra finch (Taeniopygiagu ttata eastanotis) begins with a silent 'static' phase (Morris 1954) in which the male presents his flank to the female, viewing her with one eye only. In the 'dynamic' phase, he pivots about the point of perching, fixating the female with each eye in turn. Twelve pairs of zebra finches were housed in wiremesh cages ( 6 2 x 4 2 • cm) on a 12-h light: 12-h dark cycle. Courtship occurred on two perches, which ran parallel to the cage front. Observations were made for 1 h in the afternoon over a period of 3 months, involving some 40 h of observation. All recorded static phases are shown in Fig. 1. There was a significant tendency for the whole population of males to use the right eye (departure from 1:1 ratio, Gp=24.08, P<0.02, goodness-of-fit, Sokal & Rohlf 1981). Significant
Short Communications
1583
E ~ ] FLIGHT EYE m
g
LEFT
EYE
10
E
Individual males
Cock fixating hen
between bouta of courtship dance
Figure 1. Total number of monocular fixations during static phase for 12 male zebra finches. heterogeneity (Gh = 50.81, P < 0.001) was due to one male which had a significant tendency to use the left eye: all other significant asymmetries (six) involved right-eye preference. Male and female almost always faced in the same direction during static phases, so that the female usually viewed the male with her left eye. It is possible therefore that the behaviour of females contributes to the observed asymmetry. However, the male chooses on which side of the female to land and then actively approaches, whilst the female tends to move little. Courtship displays in which the male presents one flank towards the female are widespread in passerines (see review in Andrew 1961); the possibility that they involve the preferred presentation of one flank deserves study. In the zebra finch it is impossible as yet to distinguish between three possible causal explanations: (1) the orientation of the display depends on a motor bias; (2) the right eye is preferentially used in fixating any stimulus to which response is to be directed; (3) the right eye is preferentially used only in certain types of situation, which include courtship. The Phasianidae, including the domestic fowl, also have laterally oriented courtship displays (Kruijt 1963). In the case of the domestic fowl we have experimental evidence which supports explanation 3. Young domestic chicks (Hi Sex: two replications, N = 20,24) were injected with 12.5 mg testosterone oenanthate, which results in circulating levels of androgens in the adult range (Andrew 1983b). In the first type of test, a block 7 x 11 x 4 cm covered with yellow towelling was presented for 45 s: such a stimulus evokes circling (low intensity courtship waltz) and copulation. In the second the chick was placed with another testosterone-treated
chick for 90 s; this evokes circling, fixation of the partner's nape and aggressive sparring. Copulation, circling and sparring are fully described by Andrew (1975). In both replications the right eye was preferentially used by the whole population of chicks in circling the model (P < 0-01, P < 0.005; Wilcoxon two-tailed) but the left eye was used in circling the other chick (P<0"005, in both cases). In the absence of model or other chick, chicks showed equal numbers of right and left turns during locomotion. Neither of the asymmetries is therefore likely to represent an asymmetry present in spontaneous locomotion, such as has been reported for the rat (see review in Robinson et al. 1985). They are potentially explicable instead in two broadly different ways: they may depend on differences in the evoked behaviour (e.g. copulation versus attack) or in the perceptual properties of the stimuli. L. Workman was supported by a studentship from the SERC. L. WORKMAN R. J. ANDREW
School of Biological Sciences, University of Sussex, Brighton, Sussex, U.K.
References Andrew, R. J. 1961. The displays given by passerines in courtship and reproductive fighting:a review. Ibis, 103, 315-348, 549-579. Andrew, R. J. 1975. Effects of testosterone on the
1584
Animal Behaviour, 34, 5
behaviour of the domestic chick. I. Effects present in males but not in females. Anita. Behav., 24, 139-155. Andrew, R. J. 1983a. Lateralization of emotional and cognitive function in higher vertebrates, with special reference to the domestic chick. In: Advances in Vertebrate Neuroethology (Ed. by J.-P. Ewert, R. R. Capranica & D. J. Ingle), pp. 477-509. London: Plenum Press. Andrew, R. J. 1983b. Specific short-latency effects of oestradiol and testosterone on distractibility and memory formation in the young domestic chick. In: Hormones and Behaviour in Higher Vertebrates (Ed. by J. Balthazart, E. Pr6ve & R. Gillies), pp. 463~473. Berlin: Springer-Verlag. Andrew, R. J., Mench, J. & Rainey, C. 1982. Right-left asymmetry of response to visual stimuli in the domestic chick. In: Analysis of Visual Behaviour (Ed. by D. J. Ingle, M. A. Goodale and R. J. W. Mansfield), pp. 197 210. Cambridge, Massachusetts: Massachusetts Institute of Technology Press. Kruijt, J. P. 1963. Notes o f wing display in the courtship of pheasants. Avicult. Mag. January-February, pp. 1120.
Morris, D. 1954. The reproductive behaviour of the zebra finch, with special reference to pseudofemale behaviour and displacement activities. Behaviour, 6, 271-322. Nottebohm, F. 1971. Neural lateralization of vocal control in a passerine bird I: song. J. Exp. Zool., 177, 229562. Robinson, T. E., Becker, J. B., Camp, D. M. & Mansour, A. 1985. Variation in the pattern of behavioral and brain asymmetries due to sex differences. In: Cerebral Lateralization in Nonhuman Species (Ed. by S. D. Glick), pp. 185-231. New York: Academic Press. Rogers, L. J. & Anson, J. M. 1979. Lateralisation of function in the chicken forebrain. Pharmacol. Biochem. Behav., I0, 679-868. Sokal, R. R. & Rohlf, F. J. 1981. Biometry: The Principle and Practice of Statistics in Biological Research. New York: W. H. Freeman.
(Received 10 February 1986; revised 9 April 1986; MS. number: sc-290)
photobyHugovanLawick
The Chimpanzees of Gombe Patterns of Behavior JANE GOODALL Dr Goodall now crowns her first quarter-century with the chimpanzees of Gombe by giving this comprehensive, up-to-date account of her unique work. The surprising findings of the last few years such as cannibalism, intergroup aggression and new heights of cognitive ability - are presented for the first time in book form. Belknap s Hardback 688ppillus. 0-674-11649-6 Available in N. Americafrom: 79 GardenStreet, Cambridge. MA 02138 $30.00
HARVARD UNIVERSITYPRESS 126 BuckinghamPalace Road London SW1W 9SD