S11.3: Sexual conflict and hatching asynchrony: A review

Department of Zoology, Norwegian University of Science and Technology, N-7491 Trondheim, Norway, fax 47 73 591309, e-mail trond.amundsen@chembio.ntnu.no

Amundsen, T. 1999. Sexual conflict and hatching asynchrony: A review. In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban: 614-623. Johannesburg: BirdLife South Africa.

Traditionally, the two parental sexes have been assumed to have the same interests regarding the onset of incubation and consequent hatching pattern in birds. Recently, however, the concept of sexual conflict has been evoked in theoretical and empirical approaches to avian hatching asynchrony. The first suggestion along this line was that the female would benefit from asynchronous hatching because she would thereby ensure a high paternal investment during hatching, and increase the male's total share of the parental duties. Experiments on Yellow Warblers and Pied Flycatchers have not provided empirical support of this hypothesis. More recently, however, it has been shown that male and female Blue Tit parents incur different survival costs in relation to hatching pattern: females benefit from synchrony, males from asynchrony. This difference has been suggested to result from sexual differences in provisioning of large and small siblings due to sex-differences in life-history or to patterns of paternity in relation to egg-laying. While recent studies provide limited support for a sex-difference in nestling provisioning, it may seem that females often care for the smaller offspring during and after fledging. However, more studies are required on parental costs from various hatching patterns, and on the interaction between offspring behaviour and parental provisioning, before any firm conclusions can be drawn regarding the potential for sexual conflict over hatching patterns. Moreover, reproductive costs probably act in concert with other selection pressures influencing optimal hatching spread. For instance, reduced sibling rivalry in asynchronous broods may lead to an improved quality of offspring.

Parental care is costly (Williams 1966). Hence, there is a fundamental disagreement between the male and female parent on how much care each should provide (Trivers 1972; Houston & Davies 1985). Although the two sexes would normally agree on the optimal amount of care to the offspring, both males and females would benefit from taking less of the parental burden themselves, provided they were able to manipulate the other parent to increase her/his care to a similar degree. This may lead to one sex deserting the brood, leaving all of the parental duties to the other sex, or to different levels of care provided by males and females (Maynard Smith 1977; Houston & Davies 1985).

The fundamental sexual conflict over parental care has received little attention in studies of avian brood reduction and hatching asynchrony. This neglect may either reflect an assumption that males and females are in evolutionary agreement over issues related to hatching spread, or simply the practical difficulties of assessing male and female provisioning behaviour. Accordingly, only about ten of the presently around 50 asynchrony experiments conducted have reported parental provisioning to the broods (Hahn 1981; Fujioka 1985; Hébert & Barclay 1986; Mock & Ploger 1987; Hillström 1992; Amundsen 1993; Hébert & Sealy 1993; Wiebe & Bortolotti 1994; Hansen 1997; Slagsvold 1997a; Stoleson & Beissinger 1997), and even fewer have distinguished between feeds made by males and females (Hillström 1992; Amundsen 1993; Hébert & Sealy 1993; Hansen 1997; Slagsvold 1997a; Stoleson & Beissinger 1997). Thus, the possibility that males and females may respond differently to variation in hatching spread, reflecting an underlying sexual conflict, is largely unexplored. This review aims to assess the merits of two recent ideas concerning sexual conflict and hatching asynchrony.

Based on studies of the Pied Flycatcher Ficedula hypoleuca, Slagsvold and Lifjeld (1989) suggested that asynchronous hatching was in the female's interest and a result of her control of the onset of incubation. They argued that asynchronous hatching might confer two kinds of benefits to females. First, it would prolong the period during which one or more young requires brooding by the female. Males often provide most of the food during this period, and asynchrony would thus force the male to take most of the care for one or a few extra days. If this initial investment is not followed by a reduction in male care later on, the total amount of male care to the nestlings would be higher with asynchronous than with synchronous hatching. Potentially, this could be costly to the male, while the female would benefit from a reduced share of the parental burden. Second, asynchronous hatching would mean that the first young hatches at least 1-2 days earlier than they would have done with synchrony, due to the earlier onset of incubation. For potentially polygynous species like Pied Flycatchers, according to Slagsvold and Lifjeld (1989), males could have used this period to attract secondary mates. By asynchronous hatching, males are ‘forced’ to refrain from extramarital activities a few days earlier, in order to provision the newly-hatched nestlings when the female is brooding. Obviously, this potential female benefit from asynchrony is only relevant to species in which males are occasionally polygynous.

Slagsvold and Lifjeld (1989) supported their idea with data from an experimental study of Pied Flycatchers. In their experiment, female parents had lower body masses close to fledging time with synchrony than with asynchrony. For males, no significant difference was found. The first finding in particular is consistent with the idea of different costs for the two parents related to hatching spread, but does not provide a critical test of the hypothesis. This is because (1) they did not record provisioning patterns by the two parental sexes, (2) the parents were not weighed before nestling provisioning; it could thus not be unambiguously concluded that females lost more mass with synchronous hatching, and (3) it is unknown whether a minor difference in parental body mass by the end of the nestling period translates into a long-term cost of reproduction.

This idea, which was originally coined the ‘sexual conflict hypothesis’ by Slagsvold and Lifjeld (1989), has been subject to only few experimental tests. Four studies in particular have addressed whether males provide more care when hatching is synchronous. Hébert and Sealy (1993) experimentally induced synchronous hatching in a group of Yellow Warbler Dendroica petechia broods during two years, and compared provisioning by males and females between these and unmanipulated asynchronous broods. Their analyses were based on provisioning rates obtained two, four and seven days after hatching of the first young. In general, the pattern of hatching had very little influence on male and female feeding rates. If anything, there was a tendency for both sexes to benefit from asynchrony, because overall such broods tended to be fed slightly less without any loss in fledgling mass (Hébert 1993). Hébert and Sealy (1993) thus refuted the sexual conflict hypotheses for the Yellow Warbler, and instead suggested that the sexes might have identical interests with respect to hatching. Amundsen (1993) manipulated Pied Flycatcher broods to become either synchronous or asynchronous during two years. He compared the feeding rates by males and females on days -2, 0, 3, 6 and 11 relative to hatching of the last-hatched nestling. On day minus two, no nestling would have hatched in synchronous broods, but about half of the young in asynchronous ones. As expected, males of asynchronous broods provided considerable nestling care at this stage, and they also fed more at asynchronous than synchronous broods on day 0. Later in the nestling period, however, this pattern appeared to be reversed, so that the total amount of male care was very similar between the two treatments. Moreover, both sexes appeared to benefit from asynchrony in terms of their body mass at fledging time, although the difference was only significant for females (Amundsen 1993). Studying the same species, Hillström (1992) did not find any consistent increase in male care with asynchronous hatching. Unfortunately, this study suffers from small sample sizes in the different treatments and consequently low statistical power. Finally, Stoleson and Beissinger (1997) manipulated the degree of asynchrony in Green-rumped Parrotlets Forpus passerinus and recorded parental provisioning (days 4, 8, 12, 16 and 23 after hatching of the first young) as well as subsequent survival. They found no difference in nestling provisioning or parental survival between synchronous and asynchronous treatments for either parental sex. It should be noted, however, that parrots show the most extreme hatching asynchrony reported for any avian taxon, with senior siblings sometimes weighing ten times that of junior ones at hatching of the latter (Beissinger & Waltman 1991; Stoleson & Beissinger 1997). Parent-offspring dynamics as well as parental tactics may therefore not be directly comparable between passerines and parrots. Taken together, none of the four studies specifically aimed to test Slagsvold and Lifjeld's (1989) idea were supportive.

A few more studies have compared male and female feeding rates between experimentally synchronous and asynchronous broods, but with other scientific aims and/or with a less complete coverage of the complete nestling period. Using a paired design in which the same parents were allowed to feed both a synchronous and an asynchronous Bluethroat Luscinia s. svecica brood during the course of the same day, by swapping whole broods between pairs, Hansen (1997) found no effect of hatching pattern on male provisioning rates. Females were unaffected by hatching pattern on day 4, but fed more at synchronous than at asynchronous broods on day 8. Although studies that do not include the earliest nestling period around hatching have limited power in testing the sexual conflict hypothesis, the absence of an effect on male feeding rates lend no support to Slagsvold and Lifjeld's idea.

I believe that any effect of Slagsvold and Lifjeld's (1989) proposed mechanism would be, at best, very weak. First, male provisioning during hatching is at a much lower level than later in the nestling period, and comprises only a minor part of his total investment in the brood. It is questionable whether a small increase in the male's effort at this stage confers any significant long-term cost. Second, males may adjust their total feeding effort by reduced provisioning later in the nestling period, or during the period of post-fledging care. Third, if a small male cost of increased provisioning during hatching exists, it may not be measurable without extremely large sample sizes, due to the multitude of other (in this context confounding) factors that also influence costs of reproduction. In summary, I find it unlikely that a slightly elevated level of male provisioning during hatching would comprise any significant selection pressure on female hatching patterns. So far, the restricted data available to test the idea have not been supportive.

Slagsvold and Lifjeld's (1989) idea has been said to apply only to species where the female alone incubates; i.e., where the female is in complete control of the onset of incubation. However, the female may be in control of the hatching pattern even in species with biparental incubation if all or most of the incubation before completion of the clutch is performed by the female. To my knowledge, little is known about which sex incubates during laying in species where both sexes incubate later. This is partly because most studies of incubation have been restricted to the period from completion of laying until the onset of hatching. Knowing the role of males and females in incubation before clutch completion, and thus in determining hatching patterns, would be of relevance to understanding hatching asynchrony in general, and not only to the sexual conflict hypothesis.

The effect of asynchronous hatching in restricting male attraction of additional mates (Slagsvold & Lifjeld 1989) is, in my view, unlikely to be important. In Pied Flycatchers, most pairs commence breeding fairly synchronously. It is doubtful whether any unmated females would be available as secondary mates during hatching, around 3-4 weeks after attainment of the first female. Clearly, this will not be the case very often, and the expected success of such late broods would also be very poor. Thus, I believe that this mechanism is unimportant as a selective agent on hatching patterns, at least in Pied Flycatchers. Whether it is relevant to understanding the onset of incubation in polygynous species with a more prolonged breeding season remains to be seen.

In conclusion, I find little support for the idea that asynchrony is a result of females forcing males to provide more care. Although a sexual conflict over provisioning around hatching cannot be excluded, it is unlikely that such a conflict would confer any selection pressure of significance in shaping avian hatching patterns.

The vast majority of experimental approaches to avian hatching patterns have focused solely on the consequences with respect to offspring quality and quantity in the current breeding attempt (Stoleson & Beissinger 1995). This is understandable for logistic reasons: recording parental survival following experimental alterations of the hatching pattern would require long-term studies including large samples of nests each year. However, it is conceivable that selection pressures related to optimal hatch spread may act on parents instead of offspring, by influencing their survival and consequent future fecundity. Specifically, Mock and co-workers have suggested that synchronous hatching may lead to an increased level of parental effort which may have detrimental effects on parental survival (Mock & Ploger 1987; Mock & Forbes 1994). They have thus argued that hatching patterns should be considered in a life-history perspective rather than on an annual basis (Mock & Forbes 1994).

Studying Blue Tits Parus caeruleus, Slagsvold and co-workers (1994) experimentally created synchronous and asynchronous broods during four years and recorded the consequent return of the parents the next year. Because Blue Tits show a high degree of site fidelity, return rates provide fairly accurate estimates of parental survival. When combining data for both sexes, they found very similar survival rates for parents having tended synchronous (37%) and asynchronous broods (36%). Thus, there was no support for the idea that synchronous broods were on average more costly to produce. When survival rates were considered for each parental sex separately, however, a surprising pattern emerged: females had higher survival rates with synchrony than with asynchrony (47% vs. 29%), while there was an opposite relationship for males (25% vs. 43%). This suggests the existence of a sexual conflict over hatching spread, but in the opposite direction to that previously suggested by Slagsvold and Lifjeld (1989). Apparently, females benefited from a relatively synchronous pattern, while for males, more asynchronous hatching would have been better. Blue Tits lay very large clutches and consequently have a potential for extreme asynchrony (up to ten days); the relatively synchronous pattern seen in natural populations (0-2 days) could thus be considered a result of females controlling hatching spread in their own interest.

What mechanisms could explain a sexual difference (and consequently an inherent conflict) in survival consequences of different hatching patterns? Slagsvold et al. (1994; 1995) suggested that males and females would invest differently in relation to different sibling size hierarchies. While males were suggested to concentrate their care on the larger offspring, females were suggested to take particular responsibility for the smaller siblings. According to Slagsvold et al. (1994), the cost of providing sufficient care for the smaller offspring in the brood would increase with an increasing size disadvantage due to asynchronous hatching. Synchronous hatching, on the other hand, would make it harder for males to concentrate their feeding efforts on a few, large offspring. In support of this scenario, Slagsvold et al. (1994) reported that, in Blue Tits, it was always the female that fed the smaller offspring after fledging of the brood. However, they did not provide any data on the feeding of nestlings. Instead, they referred to a number of previous studies claiming to demonstrate a sex difference in provisioning pattern. For instance, females had been reported to discriminate actively in favour of small offspring in Pied Flycatchers (Gottlander 1987) and Budgerigars Melopsittacus undulatus (Stamps et al. 1985). More anecdotal reports from Pied Flycatchers and Great Tits (Parus major ) pointed in the same direction (Bengtsson & Rydén 1981; Lifjeld et al. 1992).

Slagsvold et al. (1994, 1995) suggested two possible reasons why males should take responsibility for large and females for small siblings. First, in many passerines, males have generally higher survival rates than females and may thus invest less in the current brood than females (Breitwisch 1989). One way to avoid extensive investment, but with limited loss in terms of reproductive success, would be to concentrate on those offspring that would have the best survival chances; i.e. the larger siblings (Slagsvold et al. 1994). Second, males may favour larger offspring because the certainty of paternity could be higher for them than for offspring resulting from the last-laid eggs (Gottlander 1987; Westneat 1993). Empirical evidence on the relationship between paternity and laying order is so far scant and provides no conclusive picture (Riley et al. 1995; Westneat et al. 1995).

Since the ‘sexual conflict hypothesis’ term was already ‘occupied’, Slagsvold and co-workers (1994, 1995) labelled this kind of conflict the ‘exploitation of mate hypothesis’. However, it should be emphasised that both these ideas describe cases of possible sexual conflict in which one sex has the potential to exploit the other by means of controlling hatching spread in its own interest.

If the scenario suggested by the Blue Tit results is widespread among passerines, and possibly also in other taxa, it might be of great importance in understanding avian hatching patterns. So far, only one other experiment has provided data on parental survival after having tended synchronous or asynchronous broods. Stoleson and Beissinger (1997) manipulated hatching spread of Green-rumped Parrotlets during two years, and recorded parental survival during the 3-4 following years. They found no evidence of sex differences in survival between the two treatments. Clearly, many more studies of this kind are needed before the general validity of the exploitation of mate idea can be evaluated.

Although the survival consequences of potential sexual differences in parental provisioning have not been studied except for Blue Tits and Green-rumped Parrotlets, the question of whether males and females really differ in provisioning has been addressed in some recent studies (Malacarne et al. 1994; Leonard & Horn 1996; Smiseth et al. 1998). This was timely, since most previous studies reporting such differences had been based on very small sample sizes (Bengtsson & Rydén 1981; Gottlander 1987; Lifjeld et al. 1992) or, in one case, had been made on a species with unusual mechanisms for coping with extreme asynchrony (Budgerigars; Stamps et al. 1985). Thus, the robustness of previous evidence suggesting that females, in general, take more care of smaller offspring was questionable.

Two recent studies addressing this question based on reasonable sample sizes have been made on Tree Swallows Tachycineta bicolor (Leonard & Horn 1996) and Bluethroats Luscinia s. svecica (Smiseth et al. 1998). The two studies came to opposite conclusions. In Tree Swallows, males provided more care to the older offspring, while females provided more to the younger. The biases expressed by the two sexes were of the same magnitude, leading to equal amounts of food being offered to each nestling, independent of size rank (Leonard & Horn 1996). Hatching asynchrony was not manipulated in the Tree Swallow study. In a study of Bluethroats in which asynchrony was experimentally increased (and reduced), no difference in provisioning pattern was found. Both sexes provided more care to large than to small offspring, and to a very similar extent (Smiseth et al. 1998). Similar results have been reported from a non-experimental study of Pallid Swifts Apus pallidus (Malacarne et al. 1994), and in a recent small-scale experiment on American Robins Turdus migratorius (Slagsvold 1997a). Commenting on these results, Smiseth et al. (1998) questioned whether males and females should have different optima regarding the distribution of food between siblings, and argued that this would only be the case under very special circumstances.

Although there seems to be limited evidence for a sexual difference in provisioning pattern during the nestling stage, a division of the brood in relation to nestling age may take place during fledging and after the brood has fledged (Slagsvold 1997b). Brood division after fledging probably occurs for reasons other than size-related parental investment (e.g. Harper 1985; Byle 1990), but some evidence suggest that females tend to care for the smaller nestlings during fledging (Slagsvold 1997a) and thereafter (Slagsvold et al. 1994). More data are needed to evaluate Slagsvold's idea that this may lead to an overall difference in parental investment between the sexes.

In the Blue Tit study by Slagsvold et al. (1994, 1995), the effect size of the hatching pattern treatment on sex-specific parental survival was fairly large. It is questionable whether equally large effects can be expected in general, even if the proposed mechanisms are at work. Probably, in most cases, the difference in parental load related to hatching pattern would be of a relatively small magnitude. Thus, only relatively small effects on survival should be expected on average, and differences may be hard to demonstrate due to the confounding effects of other factors known to influence parental survival. A number of fairly large-scale studies is likely to be needed in order to clarify the issue on a general level.

The exploitation of mate hypothesis assumes that parents have the ability to discriminate between young begging to be fed, and that they actually do so. Whether this is the case is one of the central questions in the currently very active research area related to parent-offspring dynamics and begging. The alternative to parental control is that siblings largely determine the distribution of food within the brood by competitive interactions (e.g. Kacelnik et al. 1995; Ostreiher 1997). The nature of these interactions may to a large extent be determined by size differences between siblings, and hence be subject to indirect parental control. They may also be influenced by sex (Teather 1992; Price et al. 1996), health status (Christe et al. 1996), immediate hunger (Kilner 1995; Cotton et al. 1996; Price et al. 1996; Leonard & Horn 1998), or food availability in general (R. Bu, P.T. Smiseth, T. Amundsen and A.K. Eikenæs, unpublished data). Taken together, recent evidence from studies of begging in nestling birds suggest that parents show little if any discrimination, and instead feed the best beggar, i.e., the one begging first, most intensely, or from the best position (Smith & Montgomerie 1991; Kacelnik et al. 1995; Kilner 1995; Ostreiher 1997; reviewed by Kilner & Johnstone 1997).

If success in obtaining food from the parents is determined solely by sibling competition, there is little scope for differences in provisioning between males and females unless nestlings beg differently to the two parental sexes. At present, there is no empirical evidence nor any theoretical justification of such differences in begging behaviour. However, it has recently been suggested that males and females arrive to the nest at consistently different positions, and that large and small nestlings in consequence may position themselves differently in the nest. Thereby, large nestlings may associate with the parent bringing most of the food, while the competitively inferior smaller nestlings may associate with the less active parent (Slagsvold 1997b). Provided that one sex consistently is the more active in feeding nestlings, this could lead to a sexual difference in provisioning patterns. This scenario has received some support in a study of American Robins (Slagsvold 1997a, b). Likewise, a recent experiment on Great Tits suggests that the two parents systematically arrive at different positions and that this influences the positioning of begging nestlings (Kölliker et al. 1998). In contrast, Bluethroat parents appear to consistently arrive at the nest from the same direction (P.T. Smiseth, R. Bu, A.K. Eikenæs & T. Amundsen, unpublished data). More studies are needed in order to clarify the potential relationships between parental arrival, nestling begging, and parental provisioning patterns.

As emphasised by several authors including myself (Magrath 1990; Amundsen & Slagsvold 1991a; Slagsvold et al. 1995; Stoleson & Beissinger 1995), avian hatching spread is probably subject to a number of selection pressures acting simultaneously on the organism. Instead of considering the plethora of hypotheses as mutually exclusive and looking for one universal selective agent explaining asynchrony across taxa, each potential selection pressure should be considered for each species (and study). Likewise, possible constraints on trait evolution should be considered, as well as adaptive hypotheses aimed at explaining the onset of incubation without specific focus at its consequences after hatching (Stoleson & Beissinger 1995).

In my view, it would be premature to conclude that there is a fundamental conflict between the sexes related to hatching pattern of the brood. Although some suggestive evidence exist, the current knowledge is far too scant to evaluate whether such a conflict is widespread and important. I think, however, that the potential of the first sexual conflict proposal by Slagsvold and Lifjeld (1989) in explaining avian hatching asynchrony is very limited, for empirical and theoretical reasons. I am also in doubt whether the exploitation of mate idea, related to sex-specific provisioning patterns (Slagsvold et al. 1994), will turn out to be a major determinant of avian hatching spread. In any case, such a selection pressure will act in concert with a series of others. Today, it seems clear that Lack's (1947) initial idea of asynchrony producing more fledglings has little support (Amundsen & Stokland 1988; Amundsen & Slagsvold 1991b; Stoleson & Beissinger 1995). However, a minor modification suggesting that asynchrony leads to better instead of more fledglings merits more attention (Slagsvold et al. 1995; Amundsen & Slagsvold 1996). I believe that this may the main advantage gained from asynchronous hatching. I further believe that the quality benefit may most likely be explained by a reduced level of sibling rivalry, although the evidence on this point is not overwhelming. This view does not preclude that significant effects may also exist related to, for instance, insurance (Forbes et al. 1997), bet-hedging (Amundsen & Slagsvold 1998) or onset of incubation (Stoleson & Beissinger 1995). Sexual conflict certainly remains a useful framework for posing questions on parental care, but we have a long way to go, empirically and theoretically, before we can conclude that it is important in shaping hatching asynchrony in birds.

I thank Steve Beissinger and Elisabet Forsgren for valuable comments on a previous draft.

Amundsen, T. 1993. On the evolution of differential parental investment: hatching asynchrony, sex ratio, and egg size variation in birds. PhD thesis, University of Oslo, Norway.

Amundsen, T. & Slagsvold, T. 1991a. Asynchronous hatching in the Pied Flycatcher: an experiment. Ecology 72: 797-804.

Amundsen, T. & Slagsvold, T. 1991b. Hatching asynchrony: facilitating adaptive or maladaptive brood reduction. Acta XX Congressus Internationalis Ornithologici, New Zealand 1990: 1707-1719.

Amundsen, T. & Slagsvold, T. 1996. Lack's brood reduction hypothesis and avian hatching asynchrony: what's next? Oikos 76: 613-620.

Amundsen, T. & Slagsvold, T. 1998. Hatching asynchrony in great tits: a bet-hedging strategy? Ecology 79: 295-304.

Amundsen, T. & Stokland, J.N. 1988. Adaptive significance of asynchronous hatching in the Shag: a test of the brood reduction hypothesis. Journal of Animal Ecology 57: 329-344.

Beissinger, S.R. & Waltman, J.R. 1991. Extraordinary clutch size and hatching asynchrony of a neotropical parrot. Auk 108: 863-871.

Bengtsson, H. & Rydén, O. 1981. Development of parent-young interaction in asynchronously hatched broods of altricial birds. Zeitschrift für Tierpsychologie 56: 255-272.

Breitwisch, R. 1989. Mortality patterns, sex ratios, and parental investment in monogamous birds. Current Ornithology 6: 1-50.

Byle, P.A.F. 1990. Brood division and parental care in the period between fledging and independence in the Dunnock (Prunella modularis). Behaviour 113: 1-20.

Cotton, P.A., Kacelnik, A. & Wright, J. 1996. Chick begging as a signal: are nestlings honest? Behavioral Ecology 7: 178-182.

Christe, P., Richner, H. & Oppliger, A. 1996. Begging, food provisioning, and nestling competition in great tit broods infested with ectoparsites. Behavioral Ecology 7: 127-131.

Forbes, S., Thornton, S., Glassey, B., Forbes, M. & Buckley, N.J. 1997. When parent birds play favourites. Nature 390: 351-352.

Fujioka, M. 1985. Food delivery and sibling competition in experimentally even-aged broods of the Cattle Egret. Behavioral Ecology and Sociobiology 17: 67-74.

Gottlander, K. 1987. Parental feeding behaviour and sibling competition in the pied flycatcher Ficedula hypoleuca. Ornis Scandinavica 18: 269-276.

Hahn, D.C. 1981. Asynchronous hatching in the Laughing Gull: cutting losses and reducing rivalry. Animal Behaviour 29: 421-427.

Hansen, L.T.T. 1997. Does asynchronous hatching reduce the cost of reproduction? An experiment with bluethroats. Cand.scient. thesis, Norwegian University of Science and Technology, Trondheim, Norway.

Harper, D.G.C. 1985. Brood division in robins. Animal Behaviour 33: 466-480.

Hébert, P.N. 1993. An experimental study of brood reduction and hatching asynchrony in Yellow Warblers. Condor 95: 362-371.

Hébert, P.N. & Barclay, R.M.R. 1986. Asynchronous and synchronous hatching: effect on early growth and survivorship of Herring Gull, Larus argentatus, chicks. Canadian Journal of Zoology 64: 2357-2362.

Hébert, P.N. & Sealy, S.G. 1993. Hatching asynchrony and feeding rates in Yellow Warblers: a test of the sexual conflict hypothesis. American Naturalist 142: 881-892.

Hillström, L. 1992. Patterns of hatching and adult body mass change in the Pied Flycatcher Ficedula hypoleuca: adaptations and constraints. PhD thesis, Uppsala University, Uppsala, Sweden.

Houston, A.I. & Davies, N.B. 1985. The evolution of cooperation and life history in the Dunnock Prunella modularis. In: Sibly, R. & Smith, R. (eds) Behavioural ecology: the ecological consequences of adaptive behaviour. Oxford; Blackwell: 471-487.

Kacelnik, A., Cotton, P.A., Stirling, L. & Wright, J. 1995. Food allocation among nestling starlings: sibling competition and the scope of parental choice. Proceedings of the Royal Society of London, B 259: 259-263.

Kilner, R. 1995. When do canary parents respond to nestling signals of need? Proceedings of the Royal Society of London, B 260: 343-348.

Kilner, R. & Johnstone, R.A. 1997. Begging the question: are offspring solicitation behaviours signals of need? Trends in Ecology and Evolution 12: 11-15.

Kölliker, M., Richner, H., Werner, I. & Heeb, P. 1998. Begging signals and biparental care: nestling choice between parental feeding locations. Animal Behaviour 55: 215-222.

Lack, D. 1947. The significance of clutch size. Ibis 89: 302-352.

Leonard, M. & Horn, A. 1996. Provisioning rules in tree swallows. Behavioral Ecology and Sociobiology 38: 341-347.

Leonard, M.L. & Horn, A.G. 1998. Need and nestmates affect begging in tree swallows. Behavioral Ecology and Sociobiology 42: 431-436.

Lifjeld, J.T., Breiehagen, T. & Lampe, H.M. 1992. Pied Flycatchers failed to use nestling size as a cue to favour own genetic offspring in a communally raised brood. Ornis Scandinavica 23: 199-201.

Magrath, R.D. 1990. Hatching asynchrony in altricial birds. Biological Reviews 65: 587-622.

Malacarne, G., Cucco, M. & Bertolo, E. 1994. Sibling competition in asynchronously hatched broods of the pallid swift (Apus pallidus). Ethology Ecology & Evolution 6: 293-300.

Maynard Smith, J. 1977. Parental investment - a prospective analysis. Animal Behaviour 25: 1-9.

Mock, D.W. & Forbes, L.S. 1994. Life-history consequences of avian brood reduction. Auk 111: 115-123.

Mock, D.W. & Ploger, B.J. 1987. Parental manipulation of optimal hatch asynchrony in Cattle Egrets: an experimental study. Animal Behaviour 35: 150-160.

Ostreiher, R. 1997. Food division in the Arabian babbler nest: adult choice or nestling competition? Behavioral Ecology 8: 233-238.

Price, K., Harvey, H. & Ydenberg, R. 1996. Begging tactics of nestling yellow-headed blackbirds, Xanthocephalus xanthocephalus, in relation to need. Animal Behaviour 51: 421-435.

Riley, H.T., Bryant, D.M., Carter, R.E. & Parkin, D.E. 1995. Extra-pair fertilizations and paternity defence in house martins, Delichon urbica. Animal Behaviour 49: 495-509.

Slagsvold, T. 1997a. Is there a sexual conflict over hatching asynchrony in American robins? Auk 114: 593-600.

Slagsvold, T. 1997b. Brood division in birds in relation to offspring size: sibling rivalry and parental control. Animal Behaviour 54: 1357-1368.

Slagsvold, T., Amundsen, T. & Dale, S. 1994. Selection by sexual conflict for evenly spaced offspring in blue tits. Nature 370: 136-138.

Slagsvold, T., Amundsen, T. & Dale, S. 1995. Costs and benefits of hatching asynchrony in blue tits (Parus caeruleus). Journal of Animal Ecology 64: 563-578.

Slagsvold, T. & Lifjeld, J.T. 1989. Hatching asynchrony in birds: the hypothesis of sexual conflict over parental investment. American Naturalist 134: 239-253.

Smiseth, P.T., Amundsen, T. & Hansen, L.T.T. 1998. Do males and females differ in the feeding of large and small siblings? An experiment with the bluethroat. Behavioral Ecology and Sociobiology 42: 321-328.

Smith, H.G. & Montgomerie, R. 1991. Nestling American Robins compete with siblings by begging. Behavioral Ecology and Sociobiology 29: 307-312.

Stamps, J., Clark, A., Arrowood, P. & Kus, B. 1985. Parent-offspring conflict in Budgerigars. Behaviour 94: 1-40.

Stoleson, S.H. & Beissinger, S.R. 1995. Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period? Current Ornithology 12: 191-270.

Stoleson, S.H. & Beissinger, S.R. 1997. Hatching asynchrony, brood reduction, and food limitation in a neotropical parrot. Ecological Monographs 67: 131-154.

Teather, K.L. 1992. An experimental study of competition for food between male and female nestlings of the red-winged blackbird. Behavioral Ecology and Sociobiology 31: 81-87.

Trivers, R.L. 1972. Parental investment and sexual selection. In: Campbell, B. (ed.) Sexual selection and the descent of man. London; Aldine Publishing Company: 136-179.

Westneat, D.F. 1993. Parentage and the evolution of parental behaviour. Behavioral Ecology 4: 66-77.

Westneat, D.F., Clark, A.B. & Rambo, K.C. 1995. Within-brood patterns of paternity and parental behavior in red-winged blackbirds. Behavioral Ecology and Sociobiology 37: 66-77.

Wiebe, K.L. & Bortolotti, G.R. 1994. Energetic efficiency of reproduction: the benefits of asynchronous hatching for American kestrels. Journal of Animal Ecology 63: 551-560.

Williams, G.C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack's principle. American Naturalist 100: 687-690.