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The Evolution of Clutch Size and Reproductive Rates in Parasitic Cuckoos

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The Evolution of Clutch Size and Reproductive Rates in Parasitic Cuckoos EVOLUTION INTERNATIONAL JOURNAL OF ORGANIC EVOLUTION PUBLISHED BY THE SOCIETY FOR THE STUDY OF EVOLUTION Vol. 28 June, 1974 No.2 THE EVOLUTION OF CLUTCH SIZE AND REPRODUCTIVE RATES IN PARASITIC CUCKOOS ROBERT B. PAYNE Museum of Zoology and Department of Zoology University of Michigan, Ann Arbor, Michigan 48104 Received November 22,1972 The ultimate causes of the evolution of evolution of reproductive biology it would reproductive rates in birds have been de­ be desirable to compare not only variation bated through the century. Many biologists within a species but also related species have thought that high mortality rates in with divergent breeding ecologies. In sev­ short-lived animals favor high reproductive eral families of birds there are some species rates to insure that parents replace them­ that rear their own young, and others, the selves. In contrast, Lack (1954) and Wil­ brood parasites, that lay in the nests of liams (1966a) reasoned that the individu­ unrelated species, the fosterers or hosts, als producing more offspring will have their which gather all the food for the young. genes represented in increasing frequency Because brood parasites have evolved in­ in later generations regardless of mortality dependently (Makatsch, 1955), the differ­ rate. Lack (1954) proposed that mean ences in clutch size between the parasites clutch size is precisely adjusted within each and their nesting relatives are unlikely to be species by natural selection to match some phylogenetic sampling errors. Rather, nat­ certain maximum number of young in a ural selection will lead to differences in brood that the parents can feed. Williams clutch size between the birds that provide ( 1966a: 164) "would interpret the increased food for their own young and those that do mortality as an ecologically inevitable con­ not. Because the main difference in the sequence of the increased fecundity." Indi­ breeding of nesting and parasitic birds is vidual fitness rather than "keeping the race the presence or absence of parental care of from extinction" explains the evolution of their own offspring, one might expect that reproductive rates. the brood parasites would have larger Comparisons of the ecology of different clutches or some other measure of higher populations of a single species have been reproductive rates than their nesting rela­ made to determine the selective history of tives, if foodgathering and parental care reproductive rates, especially of clutch size, determine reproductive rates. This hypoth­ but many of the results may be explained esis was tested on cuckoos (Cuculidae), a in more than one way (Lack, 1954; Skutch, family in which brood parasitism has ap­ 1967; Hussell, 1972). To understand the parently evolved more than once and on a EVOLUTION 28:169-181. June 1974 169 170 R. B. PAYNE 120 morphological and histological techniques PARASITES 1 10 allows determination of the laying histories Ch. caprios I , 0 of birds during the two weeks prior to col­ kloos - cup reus - lection. In addition, the presence of large, Cu. c/amosus yolky follicles in the ovaries indicates addi­ solitarius - tional ovulations and layings, and, when Cl jacobinus • the growth rates of the ovarian follicles can levaillon!ii • be determined, the larger yolky follicles can qtondorius - - be predicted to ovulate within a few days NESTERS (Payne, 1966, 1969). After laying rates Phoenicophaeinoe for the two weeks were determined for each Neomorph/nae ---- bird, seasonal reproductive rates were esti­ Cenfropodinae mated from the two-week records and the Couinoe ---- --- duration of local breeding seasons. Crolophoginoe In all 2 3 -4 5 6 species sampled adequately the proportion CLUTCH SIZE of laying birds was high (50% or more) FIG. 1. Clutch size in parasitic cuckoos and throughout the breeding season. The indi­ nesting cuckoos. The mean clutch size for each vidual laying histories and local breeding species of nesting cuckoos (not individual clutches, as for the parasites) are shown. The vertical scale seasons are described elsewhere (Payne, refers not to number of individual clutches of 1973) . parasites, but to number of species of nesters. Data for nesting cuckoos are taken from many published CLUTCH SIZE sources, mainly Ali and Ripley (1969), Appert (1970), Bent (1940), McLachlan and Liversidge Most parasitic cuckoos lay only one egg (1970), Mackworth-Praed and Grant (1957, 1970), in anyone nest of the foster species. Nev­ and Wetmore (1968) and for the crotophagines from Beebe (1910) Sibley and Ahlquist (1973), ertheless, they ovulate and lay in more or and J. G. Strauch (pers. comm.). The clutches of less distinct series, or clutches, with eggs 2.5 and 3.5 for some nesters are for species with usually laid on alternate days and with clutch sizes in the literature of "2 to 3" or "3 to four to eight days between each series. 4." The data on clutch sizes are taken from illustrations (Payne, 1973) showing ovula­ tions or probable ovulations separated by world-wide basis and in which nearly half no more than 1% days in a series. The more the species are parasites. Although the obviously incomplete "clutches" with only study was planned as a test of Lack's food/ one or two post-ovulatory follicles in a parental care principle, and the results to series visible, where these were no more some extent are those expected from it, recent than 8 days, were disregarded (be­ some aspects of the evolution of reproduc­ cause slightly older ovulated follicles had tive rates in parasitic cuckoos may well be degenerated beyond recognition), as were better explained by other, more general the incompleted series of approaching ovu­ models. lations estimated entirely from yolky fol­ licles where none had yet ovulated. The MATERIALS AND METHODS clutch sizes used here (Fig. 1) thus omit Parasitic cuckoos were collected in Africa some of the smallest incomplete series illus­ in four breeding seasons from 1965 to 1972. trated. Individuals of a species varied the Ovaries were fixed in the field and later number of eggs in successive clutches; examined in gross aspect and microscopi­ some Chrysococcyx caprius, for example, cally in serial sections. The laying histories laid a clutch of two and then a clutch of of 103 individual females of nine species four. Probably the variation of number of were determined by counting and aging eggs in the series of an individual female postovulatory follicles. Use of standard accounts for much of the variation within a EVOLUTION IN PARASITIC CUCKOOS 171 TABLE 1. Seasonal reproductive data in parasitic African cuckoos. Breeding N Egg Estimated Mean body season eggs weight total eggs weight (g), Species (weeks) laidt (g)2 weight (g) females (N)" Chrysococcyx caprius 12 16-21 2.55 41-54 39 (25) C. klaas 12 20? 1.65 33 32 ( 4) C. cupreus 12 20? 2.15 43 45 ( 2) Clamator jacobinus 10 19-25 5.10 97-128 84 (22) C. levaillantii 1O? 22 ? 5.60 123 127 ( 4) C. glandarius 10 23 9.85 226 130 (10) Cuculus solitarius 1O? 20? 3.22 64 69 ( 2) C. clamosus 10 22 4.10 90 89 ( 5) 'Data on breeding seasons and estimates of the numbers of eggs are from Payne (1973). 2Egg weights are from Schonwetter (1960-66), except for C. cupreus which comes from Vernon (1970). 3 Body weights are taken from females collected in the field in the present study. species. Clutch size is variable (1-2 to aga species (Davis, 1940a; Skutch, 1959; 5-6) within each parasitic species sampled Wetmore, 1968; Strauch, unpublished ob­ well (Fig. 1), perhaps more variable than servations), and I have excluded the re­ in nesting cuckoos. In some nesting cuckoos ported large clutches (all data) for Guira with small clutches the number varies no guira which is known to nest communally more than one egg, though in others clutch (Davis, 1940b). Opisthocomus hoatzin is size varies considerably (Ali and Ripley, now regarded as a crotophagine and it lays 1967; Appert, 1970; Bent, 1940; Ohmart, small clutches (Beebe, 1909; Sibley and 1973). Statistical comparisons of variance Ahlquist, 1973). The larger clutch size in between nesting and parasitic cuckoos are the parasitic cuckoos is a difference not not possible because of the scarcity of apparently paralleled by the parasitic Icter­ published data on individual clutch sizes of idae, which lay about the same number of the nesting cuckoos. eggs in a series as nesting relatives in the Mean clutch size for eight parasitic same area (Payne, 1965). What the adap­ cuckoo species averaged 3.48 (Fig. 1) . tive significance of laying in "clutches," or Mean clutch sizes for 39 nesting species of distinct series, may be in the parasitic cuckoos averaged 2.82 in the five cuckoo cuckoos and the icterids is unknown; the subfamilies that rear their own young. The "clutches" of the parasitic cuckoos are less slightly higher average for the parasitic distinctly set off in time than in most other cuckoos is statistically significant (Ltailed birds. p = .0495, Mann-Whitney U-test). The value for clutch size of the parasites may REPRODUCTIVE RATES be an underestimate as some clutches in the Numbers of eggs laid in a season by Afri­ data may have been incomplete, and the can parasitic cuckoos are summarized in value for the nesters may be slightly high Table 1. Most parasitic cuckoos in south­ because of possible multiple clutches in the ern Africa lay 16 to 26 eggs, estimated Crotophaginae. This group of cuckoos is from the timing of clutches and the length known to sometimes have nests where more of the breeding season. In southern Africa than one female lays. I have included in where most of the samples were taken the the data only isolated nests where careful breeding season is 10 to 12 weeks (Payne, observation indicated only one laying fe­ 1973), and though some tropical cuckoos male or where the eggs laid by different may have longer breeding seasons, no quan­ females could be differentiated (the eggs of titative accounts of breeding seasons of in­ each female being a clutch) in the Crotoph- dividual birds are available in local popu- 172 R.
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