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

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 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 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 ---- , 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) 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 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. B. PAYNE lations within 10° of the equator. In than their nesting relatives was generated temperate Europe the parasitic cuckoo from Lack's principle before any data on Cuculus canorus sometimes lays as many as the African species were available. The 19 eggs in a five-week season (Chance, results of the cuckoo study were not antici­ 1940; Payne, 1973), and captive Clamator pated by the argument that "one finds no glandarius in Germany (von Frisch, 1969) evidence whatever that parental care and laid at the same rate as estimated in the fecundity are in any way dependent" (Wil­ field in South Africa. liams, 1966a:165). In the that Wil­ The numbers of eggs laid in a season by liams discussed, parental care was paternal. nesting cuckoos are less well known. In But where a female provides much maternal North America the breeding seasons of nest­ care after she lays her eggs, as in most ing cuckoos may be too short to permit fre­ birds, the apportionment of her energy be­ quent rearing of more than one or two fore and after laying is subject to selection, broods (Bent, 1940). However, cuckoos because maximizing her energy on forming may lay replacement clutches if their first eggs may affect her subsequent reserves for nesting attempts fail. Coccyzus americanus successful parental care, and one would and C. erythropthalmus lay from May expect females with much parental care to through September in Oklahoma and Michi­ lay proportionally fewer eggs than females gan, respectively, and Geococcyx californi­ with less care. anus has two breeding seasons in a year in The early formulation of Lack's (1954) Arizona (Ohmart, 1973), so some females selective principle assumed a balanced poly­ may well rear two broods in a year. In the morphism of genotypes affecting clutch tropics the breeding seasons of nesting size, with the females laying large clutches cuckoos are about the same as for para­ favored in good years, and females laying sitic cuckoos (Ali and Ripley, 1969; Mack­ small clutches leaving more young in years worth-Praed and Grant, 1953, 1970; Ben­ of inclement weather. The field work on son et al., 1971; McLachlan and Liversidge, feeding rates and survival of young in rela­ 1970). Probably some tropical nesting tion to brood size that was encouraged by cuckoos regularly lay more than two Lack's principle have resulted in necessary clutches in a season. Some other tropical revision of the theory. Whereas differences nesting cuckoos raise no more than one in clutch size were earlier thought to be brood in a year (Fogden, 1972). Nesting due to genetic differences among females, cuckoos differ from the parasites more in much variance in clutch size is independent frequency of laying clutches than in clutch of genetic differences (for example, age size. In general the nesters appear to lay differences, seasonal differences in clutch fewer eggs in a season than the parasites, size of individuals, responses to ambient as in the Icteridae (Payne, 1965). environmental food supply and weather) Female parasitic cuckoos appear gener­ (Lack, 1958; Kluyver, 1963; Klomp, 1970; ally to breed in their first year, and in the Perrins, 1971). Nongenetic variability of species with data available (Clamator glan­ clutch size is caused by selection for physi­ darius, Cuculus solitarius, and Chrysococ­ ological responsiveness to variable environ­ cyx caprius) there is no difference in mean ments. Additionally, the amount of food clutch size or in number of eggs laid be­ required by young birds in the nest is not tween first-year and older females (Payne, necessarily proportional to brood size, as 1973) . energy consumption may be lower per young in large broods because each young is PARENTAL CARE AND THE COST warmed by its nestmates (Royama, 1966); OF REPRODUCTION overheating may result (Mertens, 1969; The prediction that parasitic birds lay Royama, 1969). Third, the addition of larger clutches and more eggs in a season extra young in the broods of some altricial EVOLUTION IN PARASITIC CUCKOOS 173 birds causes decreased fledging success, but that rearing a large brood may decrease the other species can rear large broods appar­ reproductive value of the adults, particu­ ently just as well as they can smaller larly of females. broods (Lack, 1968; Perrins, 1965; Morel, An individual producing many young 1967; Hussell, 1972). early in life may have a lower reproductive A more general criticism of the original value (the likelihood that an individual at a parental care principle is that natural se­ given age will produce offspring in future lection affects both mortality and natality years and that its offspring will contribute schedules (Williams, 1966b), not simply to future generations; Fisher, 1958; Wil­ the number of young produced at anyone liams, 1966b). Nevertheless, it is unlikely time. Hence, the feeding experiments in that natality schedules of all animals maxi­ which adults are unable to rear oversized mize future reproductive values because an broods do not necessarily show that clutch that waits and maintains its poten­ size has evolved through selection to maxi­ tial value will be barren while another may mize brood size in relation to food supply, breed in the meanwhile and leave offspring, because the reduced success of large broods and competition among the offspring of may instead be accounted for by adaptive different parents may affect the net repro­ modification of adult behavior. The food/ ductive performances of the parents long parental care principle ignores the possible before their own future reproduction. Se­ effect of breeding upon the reproductive lection thus should act directly on the re­ value of the parent. If adults attempt to productive rates of individuals, not simply rear too large a brood in one year, the upon lifetime performance. stunted young may survive and breed less The notion of reproductive value may be well themselves than the young from of use in predicting some characteristics of smaller broods (Klomp, 1970), and the reproduction in parasitic birds. Parasites parents may have their own future breed­ would be expected to lay more eggs than ing attempts compromised and so lessen their nonparasitic relatives, because the their genetic contribution to future genera­ parasites do not rear their own young and tions (Williams, 1966b). Some field evi­ thus should have more energy available to dence indicates that rearing a brood affects form eggs without compromising their re­ the parents' futures. Body weights and fat productive value. Delayed reproductive or protein reserves of both males and fe­ maturity in nesters may ultimately be males in some decrease while caused by exhaustion of inexperienced they rear young (Payne, 1969; Ward, breeders (Ashmole, 1963); and as parasites 1969; Fogden, 1972; Morton and Welton, do not rear young, they may be expected to 1973). Hussell (1972) found weights of breed in their first year. The following dis­ female buntings rearing large broods to be cussion indicates the usefulness of these less than those rearing small broods and general ideas as applied to a specific group, suggested that parents of large broods may but it also brings out the importance of survive and breed less well in later years. unique attributes of a group. Kluyver (1963) found fewer birds with Egg size.-A few parasitic cuckoos have second clutches among the individuals that long been known to lay small eggs (Ma­ had reared a large first brood. Experi­ katsch, 1955; Lack, 1968). Comparison of mental reduction of broods of tits increased 28 parasites and 43 nesting species (all annual survival rate of the adults (Kluyver, those with data available) shows that para­ 1971). Some birds decrease in body weight, sitic cuckoos lay smaller eggs than do nest­ territory size, and breeding success with ing cuckoos of the same body size (Fig. 2). age (Balmer and Perrins, 1973), and per­ The selective history of egg size in the para­ haps these are effects of their individual sites for allocation of nutrients resulting in breeding histories. These data all indicate the largest number of eggs and young ap- 174 R. B. PAYNE

50 II I I III I f- -

I- - rn • f- • • 20 • • o - f- • • I IO • •• - <.9 •••• • w • o Cuculinae 5: • o 0 • Phaenicophaeinae 5 o 0 • • Cratophaqinae <.9 i- <.9 °u * *: Neomorphinae W 0 i- o 0* t:tJ* 0 ... Cauinae - o 0 000 o Centropodinae 2 o - ~OO 0

I 10 100 1000 BODY WEIGHT, 9

FIG. 2. Relation of egg size to body size in parasitic and nesting cuckoos. Open figures show mean egg weight and mean body weight for parasitic cuckoos, closed figures for nesters. Egg weights are taken mainly from Schonwctter (1960-1966) and are based on egg measurements from collections. Body weights are mainly taken from unpublished specimen weights in museums j some are from numerous articles in regional ornithological journals and museum collection reports. 1 = Clamator glandarius, 2 = Eudynamys scolopacea in , 3 = E. scolopacea in Queensland, 4 = composite body weights of Neo­ morphus geoffroyi and egg of N. rufipennis nigrogul·aris.

pears to involve the evolution of host selec­ host egg size, though no polymorphisms are tion for foster species of small body size by known for egg size within a local population the parasites. A cuckoo can probably leave of cuckoos such as occurs in the color poly­ more young by allocating its resources into morphism of cuckoo eggs, each morph mim­ forming small eggs rather than to fewer, icking the color and pattern of a different larger eggs, because small hosts local host species (Makatsch, 1955; Payne, (those much smaller than the cuckoo) are 1967) . Selection for parasitism of small more abundant locally than large passerines hosts is constrained by some minimal host (my observations), so parasites using the size as the eggs must be incubated and the smaller birds as their hosts have more total young fed. Though the egg is small and the nests available to them. Cuckoo eggs are nestling hatches in an unadvanced state, about the same size as the eggs of hosts the cuckoo is the sole nestling and it grows they parasitize; the size similarity may rapidly. The foster parents may bring it as facilitate heat transfer in incubation and much food as they would have to their en­ may mollify behavioral reactions of the tire brood. foster parent to the alien egg. Secondary Deviations from the body size/egg size to the evolution of host selection based on relationship among the parasitic cuckoos host abundance, there may be a fine-scale involve species where the young are reared adjustment by selection of egg size to mimic with the host young. The main deviant in EVOLUTION IN PARASITIC CUCKOOS 175

TABLE 2. Estimates of the caloric costs (kcal) of breeding during a 40-day period in a parasitic cuckoo of 84 g (Clamator jacobinus) and a hypothetical phcenicophaeine nesting cuckoo of the same body weight.

Parasitic cuckoo Nesting cuckoo Activities Cost/day Total cost Cost/day Total cost Existence SMR 13.0 520 13.0 520 Field existence energy ? ? Reproduction Egg formation 5.46 164 8.26 49.5 Incubation (12 days, nester) 0 0 o? o? Feeding young (22 days, nester) 0 0 13.0 282 Other ? ? Total caloric cost of breeding 164+? 332 +?

Fig. 2 is Clamator glandarius, which para­ nesting cuckoos. Incubation time ranges sitizes mainly larger crows, and several from 10 to 14 days in Coccyzus, 14 to 18 young cuckoos per nest may fledge to­ in Centropus, 16 in Crotophaga, 17 to 18 in gether with the host young (Friedmann, Geococcyx, and 19 in Piaya (Hamilton and 1964) . The eggs and young of these Hamilton, 1965; Bent, 1940; Vernon, 1971; cuckoos are somewhat smaller than those Koster, 1971; Ohmart, 1973; Skutch, 1959, of their crow hosts. The energy of these 1966a). The time from hatching to fledging female cuckoos is better allocated for larger ranges from 7 to 10 days in Crotophaga and reserves for the embryo allowing increased Coccyzus (Davis, 1940a; Skutch, 1959; competitive ability of individual young Hamilton and Hamilton, 1965) to 17 to 19 birds in a crowded nest. Although the crow days in Geococcyx (Ohmart, 1973) and a parasite in India Eudynamys scolopacea month in Centropus (Ali and Ripley, 1969). also lays several eggs per nest and the Parents may feed their young after fledging young are reared with the host young, it for two weeks on the average in the tem­ hassmall eggs, and egg size is not relatively perate region, longer in anis (Davis, 1940a; larger in India than in Australian popula­ Koster, 1971), and at least 10 weeks tions of this cuckoo that parasitize smaller beyond fledging in some tropical forest hosts (Makatsch, 1955) where the cuckoo cuckoos (Fogden, 1972). The average total may be the only survivor in the brood. time involved from laying to independence Energy allocation and the cost of breed­ of the young may be six weeks; additional ing.-Even though eggs are small, it costs time would be involved in nestbuilding and the female something to produce them, and more prolonged parental care. it would be desirable to determine the dif­ The energy requirements or cost for ferential in reproductive value that follows breeding in the two groups of cuckoos may when a cuckoo lays a different number of be compared in terms of the increase over eggs, but no data are available. Because their standard metabolic rates (SMR), one effect of breeding is depletion of an which should be the same for closely re­ adult's energy reserves and shortened life lated birds regardless of breeding. Table 2 or depleted reserves for later breeding, it is estimates the energy (calculated from the useful to consider reproductive effort in expression for SMR of Lasiewski and Daw­ terms of its time and energetic costs in son, 1967), in a cuckoo of 84 g, the weight parasites and in nesting birds. of the parasite Clamator jacobinus. Caloric The time spent in each stage of the nest­ costs for laying are based on egg size (7.25 ing cycle has been determined for a few g for C. jacobinus, Schonwetter, 1966; 11.0 176 R. B. PAYNE g for a hypothetical nesting cuckoo of 84 g only egg formation, incubation and feeding body weight, estimated from the Phaenico­ the young to two weeks after fledging, the phaeinae in Fig. 2), caloric equivalents of female parasites seem to require no more eggs (105 kcal for 100 g wet weight of eggs energy than their nesting relatives do for of small altricial birds, King, 1973), and breeding. Birds in the field would actually 70% efficiency of converting food to eggs operate at a metabolic level higher than in (King, 1973). The daily energy expendi­ the laboratory where SMR is measured, ture of egg formation would be higher for and maintaining body temperature, search­ nesting cuckoos. In a 40-day season the ing for food, avoiding predators and so on parasite would lay about 15 eggs; parasitic might increase the energy requirements in and nesting cuckoos both lay on alternate the field to as much as the 3.4 X SMR level days, and if the nester lays 3 eggs, the para­ estimated for passerine birds (King, 1973). site would use three times more energy in The cost of living, apart from breeding, is making eggs. Development of the embryo similar in parasitic and nesting cuckoos of in incubation requires heat from the parent the same body size. and the measured values of metabolic rates Other aspects of parasitic cuckoos.-Two of captive birds and heat flow from bird to unique aspects of the biology of parasitic egg suggest a caloric input equivalent to cuckoos should also be considered as they about 25% of adult SMR (Drent, 1967). account for much of the laying schedule It is uncertain, however, whether the incu­ and are not general features of life his­ bating parent must provide heat "in addi­ tories such as are incorporated into more tion to that released as a by-product of the general theories of selection for breeding energy metabolism of the nesting parent" rates. Clutch size in parasites may be (King, 1973), and at least at the warm proximately determined by availability of temperatures of the breeding season incu­ suitable nests in which to lay. A cuckoo bation may tax only the time and not the likely could track only a few nesting hosts energy requirements of nesting birds. Incu­ at any time, the number of nests under ob­ bation is listed now as costing nothing (Ta­ servation may correspond with the number ble 2). Costs of rearing young include extra of developing ovarian follicles, and the search time for food and if we include the inter-clutch interval may be the time in­ food value given to the young the cost may volved for a cue for further ovarian devel­ be a 100% increase over non-breeding food opment by finding and watching more requirements of the parents (Brisbin, 1969; nests. Although some cuckoos like Chryso­ Dunn, 1973). Additional energetic costs coccyx caprius parasitize colonial hosts of breeding include nestbuilding and terri­ (Payne and Payne, 1967), the hosts them­ torial defense, but for these activities no selves are often synchronized (Hall, 1970), good physiological determinations are avail­ so the cuckoos may not find suitable nests able for birds. Breeding female cuckoos of continuously within a colony, and cuckoos at least some parasitic species do not ap­ that parasitize colonial hosts do not have pear to spend much energy actively search­ larger mean clutches than species parasit­ ing for host nests, but most often perch and izing dispersed hosts. Increased rates of inactively observe the local nestbuilding laying in Cuculus canorus have been dem­ birds (Chance, 1940; my observations). onstrated experimentally by increasing the The strain of breeding on females may be number of available host nests in the lessened when the male feeds her during the field (Chance, 1940). The results of this nesting period, as in many nesting cuckoos, experiment do not suggest that laying rates and in some parasitic cuckoos also the male are as limited by the amount of food a feeds the female, who may get most of her female can convert into eggs, as much as food this way (my observations of Chryso­ they are by the number of available nests, coccyx caprius and C. klaas). Considering because the female was given no extra food EVOLUTION IN PARASITIC CUCKOOS 177 while it was laying. Perhaps local differ­ REPRODUCTIVE RATES AND ences in the number of host nests account MORTALITY RATES for much of the observed variation in A positive correlation between reproduc­ cuckoo clutch sizes. Cuckoos may them­ tive rates and mortality rates has been selves increase the availability of nests by documented for several populations and perturbing their nesting hosts causing them species, and Emerson ( 1949), Moreau to nest again. One laying Clamator jacob­ (1944), Skutch (1949, 1967), von Haart­ inus taken in my study had in its esophagus man (1971), and others have suggested an eggshell and developed embryo of its that reproductive rates generally are se­ host Pycnonotus barbatus. Eating host eggs lected to compensate for the mortality rates provides cuckoos with nutrients appropriate within populations. Lack (1954) however, for forming eggs themselves, and it also has explained that natural selection pro­ may increase the chance that a host will motes the genotype of individuals leaving desert and lay another clutch. If a cuckoo the most offspring to the next generation missed laying in one clutch of the host, she regardless of mortality rates, and he as­ may be timed appropriately for the second sumed the clutch size was the main way by as she could follow the nesting pair as they which birds increased their genetic contri­ renest and find their new nest readily. butions. The survival of a large brood to Though C. jacobinus do not, some cuckoos fledging or into winter nevertheless is not often remove a host egg (Chance, 1940; equivalent to the recruitment of new breed­ Makatsch, 1955; Liversidge, 1971). Egg ing adults to the population, because the removal by the cuckoos may decrease the new birds may not be able to establish likelihood that a host would desert a para­ themselves as breeders. Producing young sitized clutch because of too many eggs in numbers sometimes may ensure fewer but such an effect appears secondary to the descendants than would producing fewer nutritional benefit to the cuckoos and their young each with a substantial endowment. management of the nesting of their hosts. Small clutches and small broods may Secondly, laying rates are constrained by allow some adult birds more time to avoid developmental rates of the cuckoo embryo. predators and to compete successfully, Parasitic cuckoos lay on alternate days, and thereby increasing their own chances for by the time the eggs are laid they have visi­ survival and breeding in a later season ble embryos. The advanced development of (Cody, 1966; Gadgil and Bossert, 1970). the cuckoo embryos at laying, resulting Neither predation pressures on adults nor from a day of internal incubation in the their feeding ecologies appear to differ cuckoo oviduct, and the associated short greatly between the two groups of cuckoos, incubation periods enable the parasites' so this generalization does not seem to pre­ eggs to hatch before the host eggs (Ma­ dict cuckoo reproductive rates or clutch katsch, 1955; Jensen and Jensen, 1969; sizes. Densities of parasitic African cuckoos Payne, 1973). Newly hatched cuckoos appear similar to those of North American remove the unhatched eggs of the host nesting cuckoos, and both eat many of the same kinds of food, especially hairy (Friedmann, 1948; Makatsch, 1955) and caterpillars. Annual survival rates are un­ with them any competitors for the care of known, but museum samples show most the foster parents, or, in species that do not parasi tic cuckoos to be older than a year eject the host eggs, early hatching gives the (Payne, 1973); Chance (1940) and Blaise young a head start in competition for food (1965) found some females (identified by with the host nestmates. This competitive their eggs) to live for several years. Sur­ advantage of advanced development of the vival of eggs and nestlings may be low. young parasite appears to set an ecological Niethammer (1938) summarized data from limit on laying rates in the cuckoos. Europe showing that success of Cuculus 178 R. B. PAYNE canorus eggs from laying to hatching is 62% sons of the evolutionary ecology among and of young to fledging is 43%. The over­ populations and species (Gadgil and Sol­ all success of 27% is less than for other brig, 1972; Pianka, 1972), and indirectly European birds reared in open nests (Lack, these strategic arguments may help explain 1954: 75). Clamator jacobinus in coastal the evolution of cuckoo life histories, though South Africa had 20% fledging success, its none of these workers made specific predic­ local host Pycnonotus capensis had 19%; tions about this group. Reproductive rates both suffered many losses from predators may somehow be balanced, in the long run, (Liversidge, 1966, 1971). Adult parasitic against mortality rates in the evolution of cuckoos in several species are said to be breeding "strategies." But the balance is distasteful to predators, perhaps from nox­ not the simple one of high mortality rates ious chemicals in the caterpillars they eat directly causing high reproductive rates. (Cott, 1946-'47; Cott and Benson, 1971). Perhaps none of our general theories of I have eaten several of these cuckoos raw the evolution of reproductive rates are however and found them palatable, as did really general if they cannot predict ob­ vervet monkeys that raided my specimens. served life-historical adaptations of organ­ Aside from any possible aposematic forms, isms unlike those on which the theories cuckoos are mostly dull-plumaged and in­ were inductively based. Data on real ani­ conspicuous (Payne, 1967); both hosts and mals such as the parasitic cuckoos do not predators may overlook them. These obser­ refute these theories, but indicate their vations suggest that predation rates on inadequacies with respect to certain life adult parasitic cuckoos are not grossly history and behavioral phenomena. higher or lower than those on nesting birds. SUMMARY Much in the recent discussion of and "r" Parasitic cuckoos lay larger clutches and "K" selection and "strategies" of evolution they lay many more eggs per year than of reproductive rates has assumed that the their non-parasitic relatives. The increase selective advantage of birth rates depends in reproductive rate is accomplished through directly on mortality rates within a popu­ increasing the number of "clutches" in a lation (Lewontin, 1965; MacArthur and season more than the number of eggs in a Wilson, 1967; Cody, 1966, 1971). In popu­ clutch. In this special case, reproductive lations that frequently are under density­ effort estimated in terms of caloric costs dependent restraints on population size we involves a reallocation of energy normally might expect natural selection to favor in­ expended on nestbuilding, incubation, feed­ dividuals that can adjust their reproductive ing the young, and possibly female terri­ effort to prevailing ecological conditions. torial behavior, but the total cost of breed­ The abundance of resources available may ing appears to be less in the parasites than depend on population density, and as changes in population density are caused in in the nesting cuckoos. Specializations of part by mortality changes, it can be rea­ (a) egg size adapted to match the eggs of soned that phenotypic adaptability of re­ the more abundant hosts and of (b) ad­ productive rates are selected. It is more vanced embryonic development at laying difficult to accept the premise that long­ constrain the number of eggs laid in a sea­ term mortali ty rates over many generations son. will provide a demographic environment The results were compared with several favoring selection for high or low birth general theories of the evolution of repro­ rates independent of the resources available ductive rates, and they seem to be best ex­ to individuals. When disassociated from plained by models of parental food limita­ the implication of direct cause the rand tion (Lack, 1954) and the cost/benefit K selection concepts are useful in compari- approach of Williams (1966b). Though EVOLUTION IN PARASITIC CUCKOOS 179 reproductive rates may be adjusted evo­ BULMER, M. G., AND C. M. PERRINS. 1973. Mor­ lutionarily to prevailing mortality rates tality in the great tit (Porus major). Ibis 115: 277-281. within populations, adjustment appears to CHANCE, E. P. 1940. The truth about the be at best indirect. cuckoo. Country Life Ltd., London. CODY, M. L. 1966. A general theory of clutch ACKNOWLEDGMENTS size. Evolution 20: 174-184. --. 1971. Ecological aspects of reproduction. Research was supported by the National In D. S. Farner and J. R. King (eds.), Avian Science Foundation. Gloria Sullivan helped biology, Vol. 1. Academic Press, New York. make the serial sections. For their weight COTT, H. B. 1946-1947. The edibility of birds: data I thank the Australian Bird-banding illustrated by five years' experiments and ob­ servations (1941-1946) on the food prefer­ Scheme, CSIRO (D. Purchase), Australian ences of the hornet, cat and man j and consid­ Museum (H. J. de S. Disney), Queensland ered with special reference to the theories of Museum (D. P. Vernon), National Mu­ adaptive colouration. Proc. Zool. Soc. London seum of Victoria (A. R. McEvey), West­ 116:371-524. ern Australian Museum (G. M. Storr), COTT, H. B., AND C. W. BENSON. 1971. The palatability of birds, mainly based upon obser­ Dominion Museum, Wellington (D. C. vations of a tasting panel in Zambia. Ostrich Kinsky), Field Museum of Natural His­ Suppl. 8:357-384. tory (M. A. Traylor), Museum of Verte­ DAVIS, D. E. 1940a. Social nesting habits of the brate Zoology (N. K. Johnson), RoyalOn­ smooth-billed ani. Auk 57:179-218. --. 1940b. Social nesting habits of Guira tario Museum (R. I. Orenstein), National guira. Auk 57:472--484. Museum of Zambia (R. J. Dowsett), and DRENT, R. H. 1967. Functional aspects of incu­ National Museum of Rhodesia (M. P. S. bation in the herring gull (Larus argentatus Irwin). Martin Cody, Erica Dunn, Nelson Pont.). E. J. Brill, Leiden. Hairston, Henry Howe, Bert Murray, DUNN, E . H. 1973. Energy allocation of nest­ ling double-crested cormorants. Ph.D. disserta­ Karen Payne, Paul Sherman, Robert Storer, tion, University of Michigan. and Joe Strauch made critical comments on EMERSON, A. E. 1949. Natural selection. In W. the manuscript. C. Allee, A. E. Emerson, O. Park, T. Park, and K. P. Schmidt. Principles of animal ecology. LITERATURE CITED W. B. Saunders, Philadelphia. FISHER, R. A. 1958. The genetical theory of ALI, S., AND S. D. RIPLEY. 1969. Handbook of natural selection. 2nd revised ed. Dover, New the birds of India and Pakistan. Vol. 3. Ox­ York. ford Univ, Press, Bombay. FOGDEN, M. P. L. 1972. The seasonality and AMADON, D. 1964. The evolution of low repro­ population dynamics of equatorial forest birds ductive rates. Evolution 18: 105-110. in Sarawak. Ibis 114:307-343. ApPERT, O. 1970. Zur Biologie einiger Kua­ FRIEDMANN, H. 1948. The parasitic cuckoos of Arten Madagaskars (Aves, Cuculi). Zool. Jb. Africa. Washington Acad. Sci., Monogr, No. 1. Syst. Bd. 97:424--453. --. 1964. Evolutionary trends in the avian ASHMOLE, N. P. 1963. The regulation of num­ genus Clamator. Smithsonian Misc. Coll, 146 bers of tropical oceanic birds. Ibis 103b:458­ (4) :1-127. 473. GADGIL, M., AND W. H. BOSSERT. 1970. Life his­ BEEBE, C. W. 1909. A contribution to the ecol­ torical consequences of natural selection. Amer. ogy of the adult hoatzin. Zoologica 1:45-66. Natur. 104:1-24. BENSON, C. W., R. K. BROOKE, R. J. DOWSETT, GADGIL, M., AND O. T. SOLBRIG. 1972. The con­ AND M. P. S. IRWIN. 1971. The birds of cept of r- and K-selection: evidence from wild Zambia. Collins, London. flowers and some theoretical considerations. BENT, A. C. 1940. Life histories of North Amer­ Amer. Natur. 106:14-31. ican cuckoos, goatsuckers, hummingbirds, and HALL, A. R. 1970. Synchrony and social stim­ their allies. Bull. U.S. Nat. Museum 176. ulation in colonies of the black-headed weaver BLAISE, M. 1965. Contribution a. l'etude de la Ploceus cucullatus and Vieillot's black weaver reproduction du coucou gris Cuculus canorus Melenopteryx nigerrimus. Ibis 112:93-104. dans le nord-est de la France. L'Oiseau et HAMILTON, W. J., AND M. E. HAMILTON. 1965. R.F.O. 35:87-116. Breeding characteristics of yellow-billed cuckoos BRISBIN, 1. L. 1969. Bioenergetics of the breed­ in Arizona. Proc. Calif. Acad. Sci., 4th Ser., ing cycle of the ring dove. Auk 86:54-74. 32:405--432. 180 R. B. PAYNE

HUSSELL, D. J. T. 1972. Factors affecting clutch MOREAU, R. E. 1944. Clutch-size: a compara­ size in arctic passerines. Eco!. Monogr. 42: 317­ tive study, with special reference to African 362. birds. Ibis 86: 286-347. JENSEN, R. A. C., AND M. K. JENSEN. 1969. On MOREL, M. Y. 1967. Les oiseaux tropicaux the breeding biology of southern African elevent-ils autant de jeunes qu'iIs peuvent en cuckoos. Ostrich 40: 163-181. nourrir? Ie cas de Lagonosticta senegala. Terre KING, J. R. 1973. Energetics of reproduction in Vie 1967:77-82. birds. In D. S. Farner (ed.), Breeding Biology MORTON, M. L., AND D. E. WELTON. 1973. Post­ of birds. National Academy of Sciences, Wash­ nuptial molt and its relation to reproductive ington, D. C. cycle and body weight in mountain white­ KLOMP, H. 1970. The determination of c1utch­ crowned sparrows (Zonotrichia leucapbrys ori­ size in birds, a review. Ardea 58:1-124. antha). Condor 75:184-189. KLUYVER, H. N. 1963. The determination of NrETHAMMER, G. 1938. Handbuch der Deutschen reproductive rates in paridae. Proc. 13th Int. Vogelkunde. Band II. Akademische VerIags­ Om. Congr. 706-716. gesellschaft, Leipzig. --. 1971. Regulation of numbers in popula­ OHMART, R. D. 1973. Observations on the breed­ tions of great tits (Parus m. major). Proc. ing adaptations of the roadrunner. Condor 75: Adv. Study Inst. Dynamics Numbers Popu!. 140--149. (Oosterbeek, 1970) :507-523. PAYNE, R. B. 1965. Clutch size and numbers KOSTER, F. 1971. Zum Nistverhalten des Ani, of eggs laid by brown-headed . Con­ Crotophaga ani. Bonn. Zoo!. Beitr. 22:4-27. dor 67:44-60. LACK, D. 1954. The natural regulation of animal --. 1966. The post-ovulatory follicles of black­ numbers. Clarendon Press, Oxford. birds. J. Morph. 118:331-352. --. 1958. A quantitative breeding study of 1967. Interspecific communication signals British tits. Ardea 46:91-124. in parasitic birds. Amer. Natur. 101:363-376. 1968. Ecological adaptations for breeding 1969. Breeding seasons and reproductive in birds. Methuen, London. physiology of tricolored blackbirds and red­ LASrEWSKI, R. C., AND W. R. DAWSON. 1967. A winged blackbirds. Univ. Calif. Pub!. Zoo!. 90. re-examination of the relation between stan­ 1973. Individual laying histories and the dard metabolic rate and body weight in birds. clutch size and numbers of eggs of parasitic Condor 69: 13-23. cuckoos. Condor 75:414-438. LEWONTIN, R. C. 1965. Selection for colonizing PAYNE, R. B., AND K. PAYNE. 1967. Cuckoo ability. In H. G. Baker and G. L. Stebbins hosts in southern Africa. Ostrich 38: 135-143. (eds.), The genetics of colonizing species. Aca­ PERRINS, C. M. 1965. Population fluctuations demic Press, New York. and clutch-size in the great tit, Parus major LIVERSIDGE, R. 1966. Fluctuations in a breeding L. J. Anim. Eco!. 34:601-647. population in the eastern Cape. Ostrich Supp!. --. 1971. Population studies of the great tit, 6:419-424. Parus major. Proc. Adv. Study Inst. Dynamics 1971. The biology of the jacobin cuckoo Numbers Popu!. (Oosterbeek, 1970) :524-531. Clamator [acobinus, Ostrich Suppl, 8:117-137. PIANKA, E. R. 1912. rand K selection or band MACARTHUR, R. H., AND E. O. WILSON. 1967. d selection? Amer. Natur. 106:581-588. The theory of island biogeography. Princeton ROYAMA, T. 1966. Factors governing feeding Univ. Press, Princeton. rate, food requirement and brood size of nest­ MACKWORTH-PRAED, C. W., AND C. H. B. GRANT. ling great tits Parus major. Ibis 108:313-347. 1957. Birds of Eastern and North Eastern --., 1969. A model for the global variation of Africa. Vo!' 1, Ed. 2. Longmans, Green and clutch size in birds. Oikos 20:562-567. Co., London. SCHONWETTER, M. 1960--66. Handbuch der 001­ --. 1970. Birds of West Central and Western ogie. Akademie-VerIag, Berlin. Africa. Vo!' 1, Longmans, Green and Co., Lon­ SmLEY, C. G., AND J. E. AHLQUIST. 1973. The don. relationships of the hoatzin. Auk 90: 1-13. MAKATSCH, W. 1955. Der Brutparasitismus in SKUTCH, A. F. 1949. Do tropical birds rear as der Vogelwelt. Neumann Verlag, Radebeu!' many young as they can nourish? Ibis 91: McLACHLAN, G. R., AND R. LIVERSIDGE. 1970. 430--455. Roberts birds of South Africa. Bird Book 1959. Life history of the groove-billed ani. Fund, Cape Town. Auk 76:281-317. MERTENS, J. A. L. 1969. The influence of brood --. 1966. Life history notes on three tropical size on the energy metabolism and the water American cuckoos. Wilson Bull. 78: 139-165. loss of nestling great tits Parus major major. 1967. Adaptive limitation of the reproduc­ Ibis 111:11-16. tive rate of birds. Ibis 109:579-599. EVOLUTION IN PARASITIC CUCKOOS 181

SNOW, D. 1962. A field study of the black and WARD, P. 1969. The annual cycle of the yellow­ white manakin, M anacus manacus, in Trinidad, vented bulbul Pycnonotus goiavier in a humid W. I. Zoologica 47:199-221. equatorial environment. J. Zool. (London) VERNON, C. J. 1970. New host species for three 157:25--45. cuckoos. Ostrich 41:258. WETMORE, A. 1968. The birds of the Republic VON FRISCH, O. 1969. Die Entwicklung des of Panama. Part 2. Smithsonian Misc. ColI. Haherkuckucks (Clamator glandarius) im Nest 150. der Wirtsvogel und seine Nachzucht in Ge­ WILLIAMS, G. C. 1966a. Adaptation and natural fangenschaft. Z. TierpsychoI. 26:641-650. selection. Princeton Univ. Press, Princeton. VON HAARTMAN, L. 1971. Population dynamics. 1966b. Natural selection, the costs of In D. S. Farner and J. R. King (eds.), Avian reproduction, and a refinement of Lack's prin­ biology, vol. 1. Academic Press, New York. ciple. Amer. Natur. 100:687-692.