Sexually dimorphic eggs, nestling growth and sibling competition in American Kestrels Falco sparverius

Transcription

1 Functional Ecology 1997 Sexually dimorphic eggs, nestling growth and sibling competition in American Kestrels Falco sparverius D. J. ANDERSON,* J. REEVE AND D. M. BIRD *Department of Biology, Wake Forest University, Winston-Salem NC 27109, USA, Science Department, Christ Church College, North Holmes Road, Canterbury, Kent, CT1 1QU, UK and Avian Science and Conservation Centre, Macdonald College of McGill University, 21, 111 Lakeshore Road, Ste Anne de Bellevue, QC, Canada H9X 3V9 Summary 1. American Kestrel (Falco sparverius) nestlings are sexually dimorphic, with daughters larger than sons. The larger daughters have an advantage during sibling competition for food in excess of their higher per capita food requirements, and we predicted that parents would reduce this competitive disparity by differentially enhancing the growth of sons, specifically by laying them in larger eggs. 2. In a captive breeding population, eggs producing sons were significantly larger than eggs producing daughters; laying order effects were controlled. 3. The influence of sibling egg size ratios on post-natal size relationships persisted through the nesting period, providing parents with a tool to manipulate size-related phenomena in their offspring. Key-words: Parental care, sex allocation, sexual size dimorphism Functional Ecology (1997) Ecological Society Introduction Sex-specific characteristics of nestlings influence the reproductive biology of American Kestrels (Aves: Falconidae). In parallel with the sexual size dimorphism of adults (females weigh 9% more than males (Snyder & Wiley 1976)), daughters exceed male siblings in mass by up to 17% (Anderson et al. 1993a). One consequence of this size difference is a disparity in food requirements: daughters require 7% more food than sons do during the nestling period (Anderson et al. 1993b). A second consequence is inequality during sibling competition for food: bulkier daughters are more likely than sons to seize prey delivered by parents to the nest (Anderson et al. 1993a). This competitive advantage of daughters (up to 63% more food items consumed) far exceeds their higher food requirements (7%). Thus, nestling mortality should fall more heavily on sons than on daughters, and indeed male representation in wild broods declines as fledging brood size declines (Anderson et al. 1993a). Sex allocation theory (Charnov 1982) makes a specific prediction based on these two consequences of sexual size dimorphism and resulting natural selection: parents should favour male function, both to counter the risk of excess mortality of sons and because sons require less parental care per capita. By doing so, parents approach a 1:1 distribution of their parental investment into son and daughter function, which satisfies the central prediction of Fisherian sex allocation theory (Fisher 1930). One avenue of favouritism is numerical: parents could, in principle, overproduce sons at hatching. This mechanism has the selective disadvantage of inefficiency, since some of the overproduced sons will die in sibling competition after consuming parental care. A different avenue that avoids this inefficiency is preferential direction of resources to sons, mitigating the size-related competitive disadvantage imposed by sexually dimorphic growth. We have presented data elsewhere indicating that fathers do deliver food preferentially to nestling sons in some situations (Anderson et al. 1993b). Here we test the hypothesis that mothers favour sons by providing them with larger eggs, since egg size, neonate size and postnatal growth are correlated in some bird species (Parsons 1970; Schifferli 1973; Nisbet 1978; Ricklefs, Hahn & Montevecchi 1978; Amundsen & Stokland 1990; Anderson 1995). The enhanced growth of sons would reduce the size disparity between sons and daughters. Little clear evidence exists of such prehatching sex allocation by birds (but see Bortolotti 1986; Mead, Morton & Fish 1987; Dijkstra, Daan & Buker 1990; Ziljstra, Daan & Bruinenberg-Rinsmsa 1992), engendering scepticism that birds are capable of such manipulations (Charnov 1982; Clutton-Brock 1991). Materials and methods American Kestrels are small falcons that have been the recent focus of laboratory- and field-based work 331

2 332 D. J. Anderson et al. on reproductive behavioral ecology (Bortolotti, Wiebe & Iko 1991; Wiebe & Bortolotti 1992, 1993; Bortolotti & Wiebe 1993; Anderson et al. 1993a, b; Wiebe & Bortolotti 1994, 1995; Wiebe 1996). We used the egg dimensions of 170 kestrel nestlings from five-egg clutches (the modal clutch size in the wild) produced in 1990 and 1991 in the captive breeding colony at the Avian Science and Conservation Centre, McGill University, Montreal, Canada, to test the hypothesis that mothers favour son function with larger eggs. Egg length (L) and breadth (B) accurately estimate egg volume (V) in birds (Hoyt 1979); we used the equation V = LB 2 Π/6 as an estimate of egg volume. Egg mass was not investigated because it can vary over the course of the incubation period (Ar & Rahn 1980). Because egg size may vary along the laying sequence in some bird species, we categorized the eggs both by rank in their laying sequence and their inhabitant s sex, determined at 14 days post-hatching when sexually dimorphic plumage appeared in nestlings or, in a minority of cases, by gonadal inspection in dead nestlings. For this egg dimorphism to influence post-natal size relationships in the manner that we envision, egg size must positively influence post-hatching body size. We tested this assumption with 27 male and 34 female kestrel nestlings that were hand-raised (Anderson 1993a) from hatching to 29 days, the approximate age of fledging in the wild. Every morning before beginning feeding we measured the fasted mass of each nestling on an electronic balance. Fig. 1. Volumes of eggs producing sons and daughters in captive American Kestrels (means are bracketed by standard errors). Results EGG VOLUME AND SEX The egg volume data supported the hypothesis of parental favouritism. A two-way ANOVA revealed a highly significant effect of nestling sex on egg volume (F 1,160 = 7 31, P < 0 01). As predicted, eggs that produced sons were larger, on average, than eggs that produced daughters (Fig. 1). Neither rank in the laying sequence (F 4,160 = 1 47, P = 0 21) nor sex rank interaction (F 4,160 = 0 21, P = 0 93) were statistically significant effects. EGG VOLUME AND POST-NATAL BODY SIZE The primary assumption of the hypothesis, that egg volume differences influence nestling size differences, was warranted. Linear regressions of fasted body mass on egg volume of sons showed significant positive correlations throughout the nestling period (Fig. 2 is an example), with r 2 values averaging 0 34 (Fig. 3). Correlations for daughters were significant until 12 days post-hatching, with somewhat lower r 2 values (Fig. 3). These correlations between egg size and nestling size could be products of a mutual genetic correlation Fig. 2. Least-squares linear regressions of fasted body mass on egg volume for male (solid line) and female (dotted line) hand-reared American Kestrels at 8 days post-hatching. with the mother s body size. If they were, then large mothers would lay large eggs and have large chicks, but within-brood correlations between egg size and nestling size would be zero. In this case, the assumption of egg volume effects on post-natal growth would be invalid. To examine this possibility, size relationships of seven male and 10 female same-sex dyads within broods of our hand-raised birds were examined. For example, from each brood with at least two sons, we selected the first two sons to hatch and asked whether the son from the larger egg was the larger nestling at a given age. Log-linear analysis of the resulting three-way table (egg volume rank nestling size rank age) showed that larger eggs produced larger nestlings more often than would be expected from a null model of no within-brood influence of egg volume on body size (Fig. 4; among male siblings,

3 333 Dimorphic eggs in kestrels Fig. 3. Parameter values from least-squares linear regressions of fasted mass on egg volume for hand-reared nestling kestrels (solid lines: statistical significance of age-specific regression; dotted lines: r 2 values for same regressions). Fig. 4. Influence of egg volume rank on post-natal size rank. y-axis indicates proportion of same-sex dyads in which the nestling from the larger egg had the larger body size at a given age. egg volume partial association χ 2 = 65 96, df = 1, P < 0 001; among female siblings, egg volume partial association χ 2 = 18 13, df = 1, P < 0 001). This result indicates a phenotypic effect of egg volume on hatchling body size, so post-natal size relationships within a sibship should be adjustable through manipulation of egg volume. To examine the influence of egg volume on size relationships of sibling males and females, we calculated the ratios of egg volume and of age-specific mass for 18 male female sibling dyads in the set of hand-raised birds and used a repeated measures analysis of variance. We used data for ages 3 29 days only, because some broods lacked data for ages 1 and 2 days. We categorized each dyad as either above or below the median egg volume ratio (0 994) in our sample. Egg volume ratio category had a significant effect on son daughter mass ratio (F 1,16 = 8 31, P = 0 01); the age effect (F 26,416 = , P < 0 01) and the interaction term (F 26,416 = 1 70, P = 0 01) were also significant. To examine temporal patterns of this relationship, we calculated the least-squares linear regressions of son daughter mass ratio on son daughter egg volume ratio, for all 18 dyads separately for each age from 1 to 29 days. We used the value of each slope as a datum. All 29 regression slopes were positive (Sign test, P < 0 01; range , median 0 33). The median slope was similar in the first 10 days (0 37), the second 10 days (0 32), and the last nine days (0 38), indicating no decay in the influence of volume ratio on mass ratio with nestling age throughout the nestling period of 28 days. Discussion An adaptive basis exists for sexually size dimorphic eggs in American Kestrels, and these data show that the predicted dimorphism exists. At the proximate level, we do not know how the dimorphism arises. Females are the heterogametic sex in birds, so in principle a mother preparing to form an egg of a certain size could influence the outcome of the sex-determining meiotic division prior to forming the egg around the zygote. Another possibility would require sensing the sex of a zygote in her oviduct, adjusting egg formation accordingly. We cannot presently rule out an environmental component in sex determination, in which the ovarian, oviducal, or incubation environment, or the actual egg itself, influences embryo sex. Embryonic gonads of chickens remain bipotential until at least 7 days after laying, and transformation of genetic females into phenotypic males has been accomplished by inhibiting the action of a single enzyme (Elbrecht & Smith 1992). We can gain insight into the mechanism, whatever it is, that produces the association between embryo sex and egg size by asking whether the association arose (1) at the level of individual eggs, or (2) at the level of the entire brood. An association of the first type could arise if the causal agent acted on an eggby-egg basis, associating a son and a large egg, and a daughter and a small egg. Embryo sex and egg size would be tightly linked at the individual level within and between families; the family sex ratio would have no relationship with an individual embryo s egg size. In an association of the second type, mothers would have general tendencies to lay eggs of a characteristic size and sex ratios with a characteristic bias (large eggs and son-biased families, for example). Eggs containing daughters would then tend to be larger in sonbiased clutches than in daughter-biased clutches; the reverse would hold for sons in daughter-biased broods. Re-examination of the egg volume data showed no difference between egg volumes of daughters in sonand daughter-biased clutches (Fig. 5; t = 0 36, df = 54,

4 334 D. J. Anderson et al. P = 0 72). Thus, the overall sex ratio of the clutch had no relation with daughter egg volume, consistent with the first scenario. Remarkably, a significant relationship did exist between clutch sex ratio and egg volumes of sons, consistent with the second scenario (Fig. 5; t = 3 10, df = 64, P < 0 01). It appears that the linkage of egg size and embryo sex involves discriminations at both egg and clutch levels. For example, one explanation for the pattern in Fig. 5 is that sons are distinguished from daughters in son-biased clutches but no discrimination is attempted in daughter-biased clutches. This complex discrimination significantly broadens the scope for studies of parental manipulations of avian offspring sex and provisioning. These manipulations are well known in some other taxa (e.g. Wrensch & Ebbert 1993), but offspring sex is not easily determined (by humans) in most bird species, a difficulty that has limited progress in this taxon. Nonetheless, at least four studies have found evidence of sex-specific favouritism shown by parents toward nestlings (Stamps et al. 1987; Gowaty & Droge 1991; Anderson et al. 1993b; Clotfelter 1996), and evidence is accumulating for prelaying sex allocation as well (Ankney 1982; Gowaty & Lennartz 1985; Bortolotti 1986; Olsen & Cockburn 1991; Bednarz & Hayden 1991; Dijkstra et al. 1990; Zijlstra et al. 1992; Clotfelter 1996). We are aware of one other study that found sexual size dimorphism in egg size, that of Mead et al. (1987). The interpretations of the sex biases in these studies varied, and included evolutionary interactions with cooperative breeding, the Trivers Willard (1973) hypothesis, local mate competition, Fisherian sex allocation, and management of sibling competition. The results of the present study are perhaps the strongest evidence yet of adaptive parental manipulations of sex-specific parental care prior to egg laying in birds, and we suggest, in agreement with Gowaty (1991), that the general view that birds are incapable of prelaying bias according to offspring sex is premature. This caution is timely because a number of molecular sexing techniques have recently become available (Quinn, Cooke & White 1990; Rabenold et al. 1991; Dvorak et al. 1992; Griffiths & Tiwari 1993; Longmire et al. 1993; Sabo et al. 1995), offering an escape from the problematic limitation of cryptic offspring sex in most bird species. Fig. 5. Egg volumes of sons and daughters in son-biased (S > D) and daughter-biased (S < D) broods of at least three nestlings. Acknowledgements We thank R. E. Ricklefs, W. W. Weathers, P. A. Gowaty and an anonymous reviewer for comments on an earlier version of this paper. Data collection was supported by a NATO NSF Fellowship to D.J.A. and the operating budget of the Avian Science and Conservation Centre, McGill University. We thank I. Ritchie for help during all aspects of data collection, and H. Cunningham, J. E. Martinez Gomez and S. Hutson for assistance with nestling hand-feeding. References Amundsen, T. & Stokland, J.N. (1990) Egg size and parental quality influence nestling growth in the shag. Auk 107, Anderson, D.J. (1995) The role of parents in siblicidal brood reduction of two booby species. Auk 112, Anderson, D.J., Reeve, J., Martinez Gomez, J.E., Weathers, W.W., Hutson, S., Cunningham, H.V. & Bird, D.M. (1993a) Sexual size dimorphism and food requirements of nestling birds. Canadian Journal of Zoology 71, Anderson, D.J., Budde, C., Apanius, V., Martinez Gomez, J.E., Bird, D.M. & Weathers, W.W. (1993b) Prey size influences female competitive dominance in nestling American kestrels. Ecology 74, Ankney, C.D. (1982) Sex ratio varies with egg sequence in lesser snow geese. Auk 99, Ar, A. & Rahn, H. (1980) Water in the avian egg: Overall budget of incubation. American Zoologist 20, Bednarz, J.C. & Hayden, T.J. (1991) Skewed sex ratio and sex-biased hatching sequence in Harris hawks. American Naturalist 137, Bortolotti, G.R. (1986) Influence of sibling competition on nestling sex ratios of sexually dimorphic birds. American Naturalist 127, Bortolotti, G.R. & Wiebe, K.L. (1993) Incubation behaviour and hatching patterns in the American kestrel Falco sparverius. Ornis Scandinavica 24, Bortolotti, G.R., Wiebe, K.L. & Iko, W.M. (1991) Cannibalism of nestling American kestrels by their parents and siblings. Canadian Journal of Zoology 69, Charnov, E.L. (1982) The Theory of Sex Allocation. Princeton University Press, Princeton.

5 335 Dimorphic eggs in kestrels Clotfelter, E.D. (1996) Mechanisms of facultative sex-ratio variation in zebra finches (Taeniopygia guttata). Auk 113, Clutton-Brock, T.H. (1991) The Evolution of Parental Care. Princeton University Press, Princeton. Dijkstra, C., Daan, S. & Buker, J.B. (1990) Adaptive seasonal variation in the sex ratio of kestrel broods. Functional Ecology 4, Dvorak, J., Halverson, J.L., Gulick, P., Rauen, K.A., Abbott, U.K., Kelly, B.J. & Shultz, F.T. (1992) cdna cloning of a Z- and W-linked gene in gallinaceous birds. Journal of Heredity 83, Elbrecht, A. & Smith, R.G. (1992) Aromatase enzyme activity and sex determination in chickens. Science 255, Fisher, R.A. (1930) The Genetical Theory of Natural Selection. Clarendon Press, Oxford. Gowaty, P.A. (1991) Facultative manipulation of sex ratios in birds: rare or rarely observed? Current Ornithology 8, Gowaty, P.A. & Droge, D.L. (1991) Sex ratio conflict and the evolution of sex-biased provisioning in birds. Proceedings of the XX International Ornithological Congress 2, Gowaty, P.A. & Lennartz, M.R. (1985) Sex ratios of nestling and fledgling red-cockaded woodpeckers (Picoides borealis) favor males. American Naturalist 126, Griffiths, R. & Tiwari, B. (1993) The isolation of molecular genetic markers for the identification of sex. Proceedings of the National Academy of Sciences USA 90, Hoyt, D.F. (1979) Practical methods for estimating volume and fresh weight of bird eggs. Auk 96, Longmire, J.L., Maltbie, M., Pavelka, R.W., Smith, L.M., Witte, S.M., Ryder, O.A., Ellsworth, D.L. & Baker, R.J. (1993) Gender identification in birds using microsatellite DNA fingerprint analysis Auk 110, Mead, P.S., Morton, M.L. & Fish, B.E. (1987) Sexual dimorphism in egg size and implications regarding facultative manipulation of sex in mountain white-crowned sparrows. Condor 89, Nisbet, I.C.T. (1978) Dependence of fledging success on egg-size, parental performance and egg composition among common and roseate terns, Sterna hirundo and S. dougalli. Ibis 120, Olsen, P.D. & Cockburn, A. (1991) Female-biased sex allocation in peregrine falcons and other raptors. Behavioral Ecology and Sociobiology 28, Parsons, J. (1970) Relationship between egg size and posthatching chick mortality in the herring gull (Larus argentatus). Nature (London) 228, Quinn, T.W., Cooke, F. & White, B.N. (1990) Molecular sexing of geese using a cloned Z chromosome sequence with homology to the W chromosome. Auk 107, Rabenold, P.R., Piper, W.H., Decker, M.D. & Michella, D.J. (1991) Polymorphic minisatellite amplified on avian W chromosome. Genome 34, Ricklefs, R.E., Hahn, D.C. & Montevecchi, W.A. (1978) The relationship between egg size and chick size in the laughing gull and Japanese quail. Auk 95, Sabo, T.S., Kessell, R., Halverson, J.L., Nisbet, I.T.C. & Hatch, J. (1995) PCR-based method for sexing roseate terns (Sterna dougallii). Auk 111, Schifferli, L. (1973) The effect of egg weight on the subsequent growth of nestling great tits Parus major. Ibis 115, Snyder, N.F.R. & Wiley, J.W. (1976) Sexual size dimorphism in hawks and owls of North America. Ornithological Monographs 20. Stamps, J.A., Clark, A., Arrowood, P. & Kus, B. (1987) The effects of parent and offspring gender on food allocation in budgerigars. Behaviour 101, Trivers, R.L. & Williard, D.E. (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179, Wiebe, K.L. (1996) The insurance-egg hypothesis and extra reproductive value of last-laid eggs in clutches of American kestrels. Auk 113, Wiebe, K.L. & Bortolotti, G.R. (1992) Facultative sex ratio manipulation in American kestrels. Behavioral Ecology and Sociobiology 30, Wiebe, K.L. & Bortolotti, G.R. (1993) Brood patches of American kestrels: an ecological and evolutionary perspective. Ornis Scandinavica 24, Wiebe, K.L. & Bortolotti, G.R. (1994) The role of food in determining hatching spans of birds: Energetic constraints or facultative manipulation? Ecology 75, Wiebe, K.L. & Bortolotti, G.R. (1995) Food-dependent benefits of hatching asynchrony in American kestrels (Falco sparverius). Behavioral Ecology and Sociobiology 36, Wrensch, D.L. & Ebbert, M.A., eds. (1993) Evolution and Diversity of Sex Ratio in Insects and Mites. Chapman and Hall, New York. Zijlstra, M., Daan, S. & Bruinenberg-Rinsma, J. (1992) Seasonal variation in the sex ratio of Marsh Harrier Circus aeruginosus broods. Functional Ecology 6, Received 19 January 1996; revised 30 April 1996; accepted 10 October 1996