REVIEWS
Hatchingasynchrony,broodreduction and other rapidlyreproducinghypotheses Martyn J. Stenning Hatching asynchrony has been latching asynchrony (HA) Hatching asynchrony (extended hatching described as a method of inducing is the timespan (up to sevperiod) is apparently ubiquitous among adaptive infanticide”, because it eral days) across which a altricial birds, and may represent a often leads to chick mortality. Con#clutch hatches. from the striking example of adaptive family sequently, deaths resulting from hatching of the first egg to the planning. Research has focused on HA have caused extensive specuemergence of the last chick. Because evaluating various benefits to resulting lation, investigation and controversy chicks are fed and gain weight partial brood loss. Current conclusions (for example, Refs 8,9,11). A view from the time they hatch, a size fall into three major categories: that held by some is that inducing runts hierarchy is established within the hatching asynchrony is (1) an adaptation is a method of family planning or a brood that is relative to HA. Conto food availability, (2) a means of means of adjusting brood size to sequently, the smallest chicks often saving time, ultimately to increase food resources when competition llfetlme reproductive success, or die at some point between hatchis highrz. This suggests that HA is ing and fledging. If they do not, (3) a maladaptation. Almost every study a proximate mechanism for densityfledging weight is reduced or time develops a new explanation or qualifies dependent mortality. Recent work spent in the nest is increased. Recent an old one. Either most of them are on pallid swifts (Apuspaffidus)*3has work on passerines has demonwrong, or hatching asynchrony is an confirmed the general belief that strated that late-hatched chicks example of convergent evolution parents usually feed according to resulting in a behavioural trait that fledge suffer a reduced rate of the chick’s ability to beg, giving post-fledging survivali~z.Many birds, serving many functions. larger chicks a clear advantage. In both precocial and altricial, are other non-passerines, for example, quite capable of hatching their Martyn Stenning is at the School of Biological the blue-throated bee-eater (Merops clutch within a few hours, and birds Sciences, University of Sussex, Falmer, uiridis)l4,sibling aggression clearly that do so tend to have greater Brighton, UK BN19QG contributes to mortality. The genus fledging successJ. Most birds, how(
[email protected]). Merops is characterized by extreme ever, begin incubating a part comHA and generally complex breedplete clutch and induce HArelative ing systems, and is much studied to the time interval between incubation start and clutch completion. Why then has natural in this context. Cirebes, pelicans, boobies, herons, raptors, selection not eliminated a strategy that causes such high gulls and skuas, like bee-eaters, all exhibit siblicidal tendencies with the death of the youngest chick usually resulting mortality? Why do most altricial birds induce HA? Is sacrificing some young by inducing HA adaptive? If it is, then from chronic aggression from a larger sibrs. In such conhow? Here I review the most important hypotheses proflicts, parents rarely intervene. Indeed, in some species, often the dead chick is eaten by its sib or parentl6. posed to answer these questions. Theoreticians continue to keep brood reduction under Research into HA is becoming more focused as its ubiquity as a facultative or obligate phenomenon among all scrutiny. For example, Pijanowski17considers brood reducaltricial bird groups is being realized and its causes are betion, as a result of HA, to be adaptive in varying environcoming better understood. About 50 years ago, the brood ments, depending on the relative frequency of good and bad reduction hypothesis4Jwas proposed to explain frequently years for food. Thus, field workers are exhorted to examine observed chick mortality within bird broods. Brood reducthe outcome of breeding attempts under conditions of varytion can be defined generally as ‘numerically decreasing a ing levels of HAand food availability. However, Konarzewskirs sibship’6. Lack4 suggested that if this mortality was the re gives less support to the brood reduction hypothesis and suit of parentally induced HA,then its function was to allow more to the relatively recent ideas of predation avoidance8 the adult birds to trim brood size efficiently in order to meet and insurance19 against hatching failure. It is not new for unpredictable levels of food availability. Thus, for about three theoreticians to disagree on reasons for the evolution of HA. decades, workers regularly cited brood reduction as the However, accord seems to have been reached on two points: ruison d’e^trefor HA (for example, Refs 5,7). However, since that HA can be adaptive, and also that environmental varithe theory of adaptive brood reduction was challenged in the ability is a key factor governing the benefits. The latter model 1980s (Refs 8,s) by the nest failure or predation hypothesis, challenges field workers and empiricists to take account of it has lost favour among ornithologists as the unqualified ex- annual clutch-size changes, variation in food availability, planation for this puzzling behaviour, especially for passerpredation and hatching failure. ines. In brief, Clark and Wilson’Gsynthesis was that nestling death resulting from HAis an unfortunate consequence of seBrood reduction hypothesis qualified lection against total nest failure by either reducing the time The view4 that HAevolved as an adaptive, precautionary of greatest vulnerability to predation on nest contents, or to strategy that pre-empts stochastic variation in food availcatch up with diminishing food supplies. Thus, HA is adaptability is now doubted by many field workers as being the ive if, as a result of time saved, the rate of total nest failure unqualified explanation (Table 1). Scepticism arose when is reduced. However, recent dataloon a population of yellow Clark and Wilson8developed the nest failure hypothesis (for warblers (Dendroica petechia) show that the predation hy- review, see Ref. 20) and, as data from field studies that were pothesis also fails as a ubiquitous explanation for HA. begun in the 1980s are being analysed, new hypotheses are
H
TREE vol.
II,
no.
6 June
I996
0 1996, Elsevier
Science
Ltd
PII: SO169-5347(96)10030-6
243
REVIEWS
Table 1. Hypotheses based on parents inducing a size hierarchy as au adjustment to local food Hypothesis
Meaning
Supported by
Refuted/qualified/ unsupported by
Brood reduction
If food becomes short, the smallest chicks are sacrificed to benefit the remainder.
Ricklefss Curved-billed thrasher (Toxostoma curvirostre)
Refuted by Hillstrijm and Olsson33 Pied flycatcher (Ficedula hypoleuca)
Sibling rivalry
If sibs dispute, the smallest concedes, reducing overall energy consumption.
Mock and Ploger** Cattle egret (Bubulcus ibis)
Qualified by Seddon and van Heezickz3 Jackass penguin (Spheniscus demersus)
Peak load reduction
Sibs reach maximum demand sequentially, spreading parental workload.
Bryant35 House martin (De/i&on urbica)
Refuted by Lessells and Averys6 European bee-eater (Merops apiaster)
Sexual conflict
One sex exploits the other to enhance its chances of survival to breed again.
Slagsvold et a/.41 Blue tit (Parus caeruleus)
emerging. A recent trend is to adopt theories that develop the idea that HA is induced in order to save time (Table 2). Data from many studies qualify the brood reduction hypothesis by introducing empirically determined reasons for why a bird would want to risk killing some of its nestlings. Brood reduction has recently been redefined” as having a broad sense and a narrow sense. Mock11defines the broad sense as ‘some but not all members of a sibship dying from any and all causes’. He defines the narrow sense as an ‘abridgement of family size due to sibling rivalry per-se’. It is sibling rivalry that is exploited by HA, and HA is the most common cause of sib size differences. Brood asymmetry usually accelerates the death of surplus progeny (but see Refs 21-23), thus implying adaptive benefits to the strategy in the form of minimizing excess parental effort. One interpretation of HA as a mechanism for meeting a time deadline is the egg viability hypothesis24, which states that birds start incubating early in order to conserve the viability of their embryos. The viability of unincubated embryos decreases with storage time. However, there is evidence that some birds are unable to begin incubation when they want to because of environmental constraints on the female25. Data on western gulls (Larus occidentallis) yield the qualification to brood reduction (in its narrow sense) that parental age affects the efficiency of parental care. The outcome is that older, more experienced birds raise more of their (usually three) asynchronously hatched chicks. However, younger breeders, being less efficient foragers, may benefit from reduced broods because they have greater parental investment costs. This begs the question of why young birds should lay three eggs and not two, thereby reducing waste. We can only speculate that under some conditions even young gulls can raise all three chicks with sufficient fre quency to make laying three eggs adaptive. Or else the third egg laid by young gulls is their insurance against one of the others failing to hatch. Another study, this time on yellow warbler9, also gave qualified support to Lack’s4 hypothesis, namely that first hatchlings became heavier fledglings in asynchronous broods compared with those from synchronous broods. Also the quality of surviving chicks (in terms of relative mass) was higher than average in reduced broods. However, Hebert’s data showed that although older chicks derived a health advantage from asynchrony, youngest chicks were not dis244
advantaged compared to relevant synchronous broods. Hebert’s conclusion was that energy saved as a result of reduction in sibling rivalry (derived from having sibs of a dissimilar size) led to overall benefits in the absence of brood reduction. This theory, being well known and well sup ported for non-passerine.923, had never been demonstrated previously in a passerine.
Energy constraints New data have yielded a novel idea explaining why hatching is not more asynUnsupported by Hebert and Sealy42 chronous than is usually ob Yellow warblers served, namely the energy (Dendroica petechia) constraint hypothesi+30. The hypothesis proposes that birds gain the greatest advantages if they begin incubating from the time they lay the first egg, in order to generate perfect HA.However, incubation is prevented by low temperatures and limitations on food acquisition, which in turn restricts the energy a bird can devote to incubation. As a consequence, many birds start incubating later than would be optimal for inducing effective brood reduction. A further notion is that bisexual incubation releases this energy bottleneck in some specie@. That is, many species that start to incubate before the penultimate egg, share incubation between males and females, leading to greater HA.Alternatively, for species that start incubation after the penultimate egg, it is usual for only the female to incubate. It is well known that providing supplementary food for breeding birds can advance egg laying31. Nilsson’s work breaks new ground by supplementing food after laying has begun and then examining the effect on incubation. Surprisingly, Nilsson found that birds that had received supplementary food began incubating significantly earlier than controls29JO. Consequently, HA was greater for clutches whose parents were supplied with supplementary insect foodso. This appears to contradict predictions of the brood reduction hypothesis, which states that HAshould be greatest in situations where food is likely to be limiting. However, the main conclusion of the study is that it is early incubation that is adaptive and any consequent size hierarchy may be an unwanted side effect. The egg protection hypothesis32 paradoxically proposes that some birds, for example, gentoo penguins (Pygoscefis papuu), have been selected to incubate from the time the first (smaller) egg is laid in order to protect it from extreme cold and also predation. Thus, in this case, it is the cold that is a prerequisite (rather than an inhibitor) to early incubation. The second (larger) egg is laid several days after the first, thus the effect of asynchrony on relative chick size is to offset the size difference at hatching. Consequently, overall survival was not greater in asynchronous broods, and neither did HA result in more efficient parental care, these are two fundamental predictions of the lackian hypothesis. Alternatives to brood reduction Some studies appear to refute Lack’s4explanation for HA and favour absolute alternatives (for example, Ref. 33). In some marine species, it is usual for the second or third chick to survive. In these species, the explanation for HA is often TREE vol.
II,
no.
6 June
I996
REVIEWS a reduction in sibling rivalry as in the jackass penguin (Spheniscus demersus)23.It seems that chicks of unequal size fight less because the smallest chick consistently concedes, rather than meets, the challenge of its older sib. If chicks are not expending energy on fighting, they can grow more efficiently. This also benefits the adults as less food needs to be collected. It has also been shown theoretically34 and empirically35 that HA can make food collection and delivery more efficient for the parents by allowing chicks to reach the point of peak demand at different times rather than all at once. However, more recent evidence has shown that this is not true for European bee-eaters (Merops apiaster)36. It may be that the reason a bird induces HAis associated with a particular ecosystem, breeding system or taxonomic group. This is an area that requires further attention. For example, a prediction of the insurance hypothesis is that eggs laid after incubation has begun only produce fledged young if an earlier laid egg fails to hatch or dies soon after hatching. This hypothesis is often associated with birds that lay small clutches in exposed and vulnerable sites, as many water-birds do’9J7,B.If all chicks hatch, the chick from the insurance egg is usually killed by its sibl5. Furthermore, the insurance hypothesis fails to explain the consistently extreme HA induced by European bee-eater@, a species with a very different ecology to the previous examples, and one that is unusual in having an extended family breeding system. Alternatively, passerines appear to induce levels of HA within a populatior?41 that are much more variable than other bird Orders.
in order to enhance the probability of survival to the next breeding opportunity. One reason why H6rak2 found greater benefits of HA to females may be that they were exploiting the situation at a cost to the opposite sex. Slagsvold et ~1.~~found that for blue tits (Pam caerdeus), synchrony favoured the survival of female parents and asynchrony favoured the survival of the males. The ‘sexual conflict’ was, therefore, won by females who managed to delay incubation until after laying the last egg, thus ending the breeding season in better condition. However, relevant data on yellow warblers provided no support for this hypothesis42. A further environmental constraint that has been mooted as leading to the evolution of HA is a limitation on breeding opportunities43. This hypothesis proposes that when nesting opportunities are limited, through intra- or interspecific competition, birds that successfully acquire a nest site might be expected to invest more heavily than usual in reproduction and nest defence44. The reason for this is that it may be the only opportunity they get. This could lead to large clutches, incubation beginning with the first egg, followed by large hatching intervals. This hypothesis resulted from a study on the neotropical green-rumped parrotlet (Forpus passerinus)43. This species can exhibit perfect HA and, like many non-passerines, have an extended fledging period and a very slow development time (28-35 days). As a result, most of the (typically) five or six young fledge successfully.
.
Family planning for the future It is becoming increasingly clear that a variety of circumstances can lead to birds hatching their chicks asynchronously, and that the pay-offs derived from HA can be very different in nature depending on the habitat and species. The acrimony and angst of the mid-1980s is over, and ecologists are now looking at each species on its merits. There is now a healthy respect for alternative ideas and a general acknowledgement that no individual hypothesis about the function of HA is ubiquitous, simply that HA occurs in most altricial species of bird for a number of possible reasons (Tables 1 and 2). Finally, one major but little explored area of HAthat many agree requires more attention covers the environmental cues that lead a bird to begin incubation before the clutch is complete. Most authors discover a species that hatches asynchronously, choose or formulate a hypothesis about the pay-offs of HA, and then test the hypothesis. Most tests
lntrapopulation variation and exploiting the other sex An angle rarely explored when investigating HA in birds is intrapopulation variation in HA. Harper et ~1.39 tested the brood reduction hypothesis by enlarging naturally occurring synchronous and asynchronous house wren (Troglodytes aedon) broods. They found no support for Lack’s hypothesis, and later40 claim that for this species, HA is entirely nonadaptive and essentially neutral. Hillstrijm and OlssonD go one stage further and present evidence that for pied flycatchers (Ficedula hypofeuca), it is synchrony that favours offspring survival and it is the asynchronous broods that are disadvantaged. Indeed, in a recent review of experiments that manipulated size hierarchies in 20 species3, 83% showed greater fledging success when broods were made more synchronous. A solution may have been found to the puzzle about the apparent non-adaptive nature of HA. Hdrak2 provides evidence that rural female great tits (Parus major) sacrifice some offspring to enhance Table 2. Hypotheses based on parents incubating early in order to save time their own survival and not that I of remaining chicks. Indeed, Hypothesis Meaning Supported by Refuted/qualified by brood reduction is dismissed Refuted by as ‘a by-product of adaptive Nest failure HussellQ Time in the nest is reduced in order Hebert and SealylO reproductive decisions rather Snow buntings to minimize predation risk to nest Yellow warbler than a causal agent for improvcontents. (Plectrophenax nivalis) (Dendroica petechia) ing reproductive success’. Refuted by The term ‘adaptive reproducInsurance Cash and Evans19 Extra eggs are laid after incubation Lessells and Avery36 tive decisions’implies a strong American white pelican has begun in case first eggs fail to European bee-eater hatch. (Pelicanus erythrorrhynchos) (Merops apiaster) element of phenotypic plasticity that may help to solve Qualified by Egg viability Arnold24 Incubation begins before clutch Veiga and Viiiuela25 the puzzle of Hillstrijm and Prairie ducks completion in order to conserve House sparrows Olsson’s counterintuitive pied (Anas spp.) embryo viability. (Passer domesticus) flycatchers33 or Harper et d’s Limited breeding Beissinger and Waltman Incubation begins early in order to neutral house wrens39.Essenopportunities invest maximum care when nesting Green-rumped parrotlet tially, in bad years or terrisites are scarce. (Forpus passerinus) tories, it may pay a bird to minimize reproductive effort TREE
ool.
II,
no.
6 June
1996
245
REVIEWS involve brood manipulation experiments that enlarge broods or change size hierarchies. Few studies have investigated levels of phenotypic plasticity for HAor natural variation in the trait within a population. Those that have investigated this reveal a high degree of variation (for example, Refs 27,40),at least among passerines. One factor that most studies have in common is the idea that HA results from an environmental constraint, be it food, predation levels, temperature or breeding opportunities. What few have addressed is the effect of varying these constraints on the expression of HA in terms of incubation behaviour. To date, the onlyworkthat experimentally manipulates a potential cause of variation in incubation behaviour and then records its effect is that of NilssorPJO. Given the contradictory conclusions that have emerged from researching HA in an array of species, the emerging picture now allows us to draw just a few general conclusions about its function. Most hypotheses explaining the adaptive basis of HA can be placed into one of two major categories: namely, as adjustments to local food availability, or to save time, both during a breeding attempt, and over a lifetime of reproduction (Tables 1 and 2). Hatching asynchrony is now known to be ubiquitous among altricial and semi-altricial species, it is also likely to result from adaptations to a variety of environmental constraints and can, but may not always, be adaptive. Acknowledgements I thank
Daniel Osorio,
Jan-Ake
Stuart Semple, referee for useful
Nilsson,
Dorothy Lamb and an anonymous comments on the text.
References 1 Lebedeva, N.V. (1994) Nidicoious and post-nidicolous mortality of young from asynchronous broods of some passerine birds (t%sseriformes),Zool.Zhur. 73,122-131 Hdrak, P. (1995) Brood reduction facilitates female but not offspring survival in the great tit, Oecologia 102,514-519 Nilsson J-A. (1995) Parent-offspring interactton over brood size: cooperation or conflict? J. Avian Biol. 26,255-259 Lack, D. (1954) The Natural Regulation ofAnimal Numbers Clarendon Press Ricklefs,R.E.(1965) Brood reduction in the curved-billed thrasher, Condor 67,505-510 Mock, D. (1994) Brood reduction -narrow sense, broad sense, J. Avian Biol. 25,3-7 Parsons, J. (1975) Asynchronous hatching and chick mortality in the herrfng gull Lurus m-gent&us, Ibis 117,517-520 Clark,A.B. and Wilson, D.S. (1981) Avfan breeding adaptations: hatching asynchrony, brood reduction aud nest failure, Q. Rev. Biol. 56,257-277
9 Hussell, D.J.T.(1985) On the adaptive basis for hatching asynchrony: Brood reduction, nest failure and asynchronous hatching in snow buntings, Ornis Stand. 16,205-212 10 Hebert, P.N. and Scaly, S.G. (1993) Hatching asynchrony and feeding rates in yellow warblers: a test of the nest-failure hypothesis, Ornis Stand. 24, lo-14 11 Mock, D.W. (1984) Infanticide, siblicide, and avtau nestling mortality, in Infanticide: Comparative and Evolutionary Perspectives (Hausfater, G. and Hrdy, S.B., eds), pp. 3-30, Aldine 12 Stouffer, P.L. and Power, H.W. (1990) Density effects on asynchronous hatching and brood reduction in European starlings, Auk 107,359-366 13 Malacarne, G., Cucco, M. and Bertolo, E. (1994) Sibling competition in asynchronously hatched broods of the pallid-swift (Apus pallidus), Ethot. Ecol. Evol. 6,293-300 14 Bryant, D.M. and Tatner (1990) Hatching asynchrony, sibling competition and sibllcide in nestling birds: studies of swiftlets and bee-eaters, Anim. Behav. 39,657-671 15 Simmons, R. (1988) Offspring quality aud the evolution of Cafnism, Ibis 130,339-357
246
16 Bortolotti, G.R.,Wiebe, K.L.and Ike, W.M. (1991) Cannlbathan of nestling American kestrels by their parents and siblings, Can. J. Zoot. 69,1447-1453
17 Pijanowski, B.C. (1992) A revision of Lack’s brood reduction hypothesis, Am. Nat. 139,1270-1292 18 Konarzewski, M. (1993) The evolution of clutch size and hatching asynchrony in altriciai birds: The effect of environmental variability, egg failure and predation, Oikos 67,97-106 19 Cash, K.J. and Evans, R.M. (1986) Brood reduction in the American white pelican (Pelicanus erythrorhynchos), Behav. Ecol. Sociobiol. 18,413-418 20 Magrath, R.D. (1990) Hatching asynchrony in altrfcial birds, Biot. Rev. 65,587-622
21 Hebert, P.N. (1993) An experimental study of brood reduction and hatching asynchrony in yellow warblers, Condor 95,362-371 22 Mock, D.W.and Ploger, B.J. (1987) Parental manipulation of optimal hatchhrgasynchnm~ an experimentafstudy,Anim. Behav. 35,150-160 23 Seddon, P.J. and van Heezick, Y.M. (1991) Hatching asynchrony and brood reduction in the jackass penguin - an experimental study, Anim. Behav. 42,347-356 24 Arnold, T.W. (1993) Factors affecting egg viability and incubation time in prairie dabbling ducks, Can. J. Zoot. 71, 1146-l 152 25 Veiga, J.P. and Viiiuela, J. (1993) Hatching asynchrony and hatching success in the house sparrow: Evidence for the egg viability hypothesis, Ornis Stand. 24,237-242 26 Sydeman, W.J. and Emslie, S.D. (1992) Effects of parental age on hatching asynchrony, egg size and third-chick disadvantage in western gulls, Auk 109,242-248 27 Slagsvold, T. and Admunsen, T. (1992) Do great tits adjust hatching spread, egg size and offspring sex ratio to changes in clutch size? J. Anim. Ecol. 61,249-258 28 Nilsson, J-A. (1993) Bisexual incubation facilitates hatching asyuchrony, Am. Nat. 142,712-717 29 Nilsson, J-A. (1993) Energetic constrahtts on hatching asynchrony, Am. Nat. 141,158-166 30 Nilsson, J-A. (1994) Energetic bottle-necks during breeding aud the reproductivecost of breedhrgtoo early, J.Anim. Ecol. 63,200-208 31 Daan, S. et al. (1989) Food supply and the annual timing of avhm reproduction, in Proceedings of the XLX International Ornithological Congress, Ottawa, pp. 392-407, University of Ottawa Press 32 Williams, T.D. and Croxall, J.P. (1991) Chick growth and survival in gentoo penguins Pygoscelis papua: Effect of hatching asynchrony and variation in food supply, Polar Biol. 11, 197-202 33 Hillstrom, L. and Olsson, K. (1994) Advantages of hatching asynchrony in the pied flycatcher Ficedula hypoleuca, J. Avian Biol. 25,205-214 34 Mock, D.W.and Schwagmeyer, P.L. (1990) The peak load reduction hypothesis for avfan hatching asynchrony, Evol. Ecol. 3,249-260 35 Bryant, D.M. (1978) Establishment of weight hierarchies in the broods of house martins Delichon urbica, Ibis 120,16-26 36 Lessells, CM. and Avery, M.1.(1989) Hatching asynchrony in European bee-eaters Merops @aster, J. Anim. Ecot. 58,815-835 37 Bollinger, P.B., Bollinger, E.K.and Malecki, R.A. (1990) Tests of three hypotheses of hatching asynchrony in the Common Tern, Auk 107, 696-706 38 Mock, D.W. (1986) Advantages and disadvantages of egret and heron brood reduction, Evolution 40,459-470 39 Harper, R.G.,Juliano, S.A. and Thompson, CC. (1992) Hatching asynchrony in the House Wren Troglodytes aedon: A test of the brood-reduction hypothesis, Behav. Ecol. 3,76-83 40 Harper, R.G.,Juliano, S.A. and Thompson, CC. (1994) lntrapopulation variation in hatching asyuchrony in house wrens: Test of the individual-optimization hypothesis, Auk 111,516-524 41 Slagsvold, T., Amundsen, T. and Dale, S. (1995) Costs and benefits of hatching asyuchrony in blue tits Parus caeruleus, .I Anim. Ecol. 64,563-578
42 Hebert, P.N. and Scaly, S.G. (1993) Hatching asyuchrony and feeding rates in yellow warblers: a test of the sexual conflict hypothesis, Am. Nat. 142,881-892 43 Beissinger, S.R. and Waltman, J.R. (1991) Extraordiiary clutch size and hatching asyuchrony of a neotropical parrot,Auk 108,863-871 44 Martin, T.E. (1993) Evolutionary determinants of clutch size in cavity-nesting birds: nest predation or limited breeding opportunities? Am. Nat. 142,937-946 TREE uol. II,
no. 6 June
1996
