Costs to Host Defence and the Persistence of Parasitic Cuckoos

Costs to Host Defence and the Persistence of Parasitic CuckoosAuthor(s): Karen MarchettiSource: Proceedings: Biological Sciences, Vol. 248, No. 1321 (Apr. 22, 1992), pp. 41-45Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/49656 .

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Costs to host defence and the persistence of parasitic cuckoos

KAREN MARCHETTI Department of Zoology and Center for Population Biology, University of California, Davis, California 95616, U.S.A.

SUMMARY

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.

1. INTRODUCTION

Coexistence of parasites and their hosts may often be evolutionarily unstable (May & Anderson 1991). As host defences or parasite virulence evolve, the parasite, or the host followed by the parasite, may become extinct. One mechanism which could prevent ex- tinction of the parasite is the presence of multiple host species (Brooke & Davies 1987; Dobson & Meren- lender 1991). Even if the parasite becomes extinct on one host, it can persist by exploiting other hosts. This scenario presents a logical difficulty, however, in that eventually all suitable hosts should have evolved defences against the parasite. Here I show that in an avian brood parasitic system, host defences have maladaptive side-effects such that a measurable selective force favouring the loss of defence exists once the parasite becomes extinct on a particular host species (i.e. switches to a new host). Loss of host defences as a result of these selection pressures would enable sub- sequent re-exploitation of the host by the parasite. Thus provided there are several suitable host species, evolutionary cycling of host defences can lead to stable coexistence of the hosts and the parasite.

Parasitic cuckoos (Cuculus spp.) lay their eggs in the nests of small passerine birds. Successfully parasitized hosts raise only the cuckoo young and have zero reproductive success, resulting in strong selection for egg discrimination and rejection of unlike eggs by host species. Better host discrimination leads to improved egg mimicry by the cuckoo, creating a coevolutionary arms race between host-parasite pairs (Payne 1977; Dawkins & Krebs 1979; Mason & Rothstein 1986; Brooke & Davies 1988; Davies & Brooke 1988, 1989a, b; Rothstein 1990). This arms race is expected to continue until the host species either becomes extinct as a result of the parasite or evolves such strong

discrimination that the cuckoo is forced to switch to a different, non-discriminating host (May & Robinson 1985; Davies & Brooke 1988).

Because egg discrimination evolves under very low rates of parasitism, and the number of suitable host species is limited (host nests must be accessible to cuckoos, and cuckoo chicks require an insectivorous diet), it is difficult to envisage how cuckoos and their hosts can continue to coexist over evolutionary time. Why does the parasite not become extinct once all suitable hosts have evolved discrimination? Costs to egg rejection (e.g. rejecting or breaking one's own eggs, or nest abandonment) may persist after the parasite has become extinct on a particular host species. Such costs would select for the loss of discrimination behaviour in former hosts, and thereby enable sub- sequent re-exploitation by the parasite. Thus costs to rejection may provide a mechanism which allows for coexistence of cuckoos and their hosts.

In this study, I demonstrate rejection costs in a presumed former host, the yellow-browed leaf warbler (Phylloscopus inornatus), which has very strong egg discrimination. Perceptual ability in this species is not perfect. Some females mistakenly rejected their own (unmanipulated) eggs in response to artificial eggs placed in the nest, or when a natural egg in their clutch was painted a different colour. In addition, single eggs have occasionally disappeared from non-experimental nests, apparently as a result of ejection by the female parent (Price & Jamdar 1991; K. Marchetti, unpublished observations). If egg discrimination becomes so strong that individuals mistakenly eject their own eggs in response to variation within their own clutch (Rothstein 1982; Davies & Brooke 1988, 1989a, b) then rejection should be lost in species not currently suffering from parasitism.

Proc. R. Soc. Lond. B (1992), 248, 41-45 41 (? 1992 The Royal Society Printed in Great Britain



42 K. Marchetti Costs to host defence

2. METHODS

Phylloscopus inornatus is a small, insectivorous, ground- nesting passerine which raises a single brood in a breeding season (Price & Jamdar 1991). Its nests are easy to find and appear to be accessible to cuckoos. None the less, during a seven year study in Kashmir, India, cuckoo eggs have never been found in ca. 600 P. inornatus nests. Although it is possible that egg rejection in P. inornatus is maintained by a very low frequency of parasitism, or that there is geographic variation in egg laying by cuckoos, P. inornatus in Kashmir appears to be able to discriminate and eject all small cuckoo eggs. Presumably this has forced the cuckoo to switch to a less discriminating host. Small cuckoo (CucUIus poliocephalus) eggs and young have been found in the nests of Phylloscopus affinis, a closely related and similarly sized species which breeds in the same area as P. inornatus, and P. affinis always incubates cuckoo-sized artificial eggs (n = 7). This demonstrates that discrimination behaviour is not ubiquitous within the genus Phylloscopus.

The results of a preliminary study conducted in 1989, in which 27 0 of P. inornatus females mistakenly rejected their own eggs in response to introduced artificial eggs (n = 15), led to the more detailed experiments done in 1990 and 1991. To examine perceptual cues and costs of rejection I introduced artificial eggs, or manipulated natural eggs, in the nests of P. inornatus during May and June 1990 (n = 95) and 1991 (n = 47). All artificial eggs were made of plasticene and painted with acrylic paints, and were similar in colour to those of P. inornatus.

Nests were given one of the following treatments (table 1). 1. Introduction of control artificial eggs which were

mimetic in both size and colour to natural P. inornatus eggs in the clutch (n= 10). This allowed me to determine whether rejection occurred in response to some characteristic of the artificial egg, such as paint.

2. Introduction of artificial eggs which were mimetic in colour to those of P. inornatus, but ranged in size from slightly to substantially (1.5 x ) larger than the size of natural P. inornatus eggs within the clutch (n = 93). This allowed me to determine whether size differences were important in egg rejection.

3. Introduction of natural P. occipitalis eggs (n = 5) or small cuckoo-sized artificial eggs (n= 6 in 1990, n = 2 in 1991).

4. Manipulation of a single natural P. inornatus egg in the clutch such that it was non-mimetic in colour. I used acrylic paints to paint natural eggs either solid red (n = 29) or with black spots (n = 12). This allowed me to determine the effect of varying egg colour while controlling for possible differences in size. Of the 29 red egg treatments (but none of the black spot treatments), 21 were in nests which had already been tested for rejection by using artificial eggs. There was no obvious effect of the prior testing on response to red eggs, and data from all red egg experiments are combined.

5. Introduction of natural P. inornatus eggs taken from a different clutch (n 9). This allowed me to determine if rejection occurs in response to intraspecific brood parasitism. I define mean egg size as length x (breadth) 2, which is highly correlated with true egg volume (van Noordwijk et al. 1982).

Artificial eggs were made of plasticene. As plasticene does not completely harden, it was always possible to determine whether an artificial egg had been attacked by the host (which pecked holes in artificial eggs). Thus artificial eggs which were found in the nest, but had obviously been attacked (n= 10), were counted as rejections. In addition, plasticene allowed me to distinguish between recognition errors (incorrectly ejecting a natural egg and incubating the artificial egg) and ejection costs (accidentally damaging, and

subsequently ejecting, ones own eggs while attempting to eject the artificial egg). Recognition costs occurred most commonly, and ejection costs were observed only when individuals rejected in response to the large (cuckoo-sized) artificial eggs.

I measured length and width of eggs to examine inter- and intraspecific variability in egg size. I recorded rejection of artificial or painted eggs after 1, 2 and 7 + days. If egg rejection occurred, it was always within I or 2 days after the manipulation, and at least two birds rejected eggs within 30 min. Nest desertion (Davies & Brooke 1988, 1989) does not appear to be a method of rejection in P. inornatus, but at least one nest was abandoned after the host ejected all but one of its eggs, and another after the host broke its eggs when rejecting in response to cuckoo-sized artificial eggs. Stage of host nesting cycle was known for all nests, and most manipulations were done in the afternoon, 1-2 days after clutch completion (Davies & Brooke 1988, 1989a, b), although a few were later.

3. RESULTS

Birds ejected introduced eggs by spiking them with the bill, rolling them out of the nest, or both. At one nest, I watched a female move a red egg to the front of the nest with the bill, but she actually ejected the egg with her feet as she flew off the nest at completion of the incubation period. Egg rejection differs depending on the type of egg introduced (2 x 3 chi-square table comparing the frequencies of different rejection responses elicited by artificial against painted red eggs in 1990: 2 = 9.96, d.f. = 2, p < 0.01; rows 2 and 6 of table 1). The rate of rejection in response to aberrant size was higher than that in response to aberrant colour (figure 1), suggesting that perceptual ability (strength of rejection) varies with respect to the different egg characteristics. Although P. inornatus exhibits strong discrimination, perceptual ability is not perfect, and individuals occasionally make mistakes (ejection of a natural, unmanipulated egg) when rejecting eggs. At approximately 10 %0 of the nests, females rejected one of their own eggs rather than the manipulated egg (figure 1). They subsequently incubated the manipulated egg, which was not damaged in any way.

(a) Response to aberrant-sized eggs

Rejection occurred when artificial eggs were large (Mann-Whitney U test comparing size of artificial eggs when rejection did or did not occur in 1990: U = 284, n = 42, p < 0.01, figure 2). All cuckoo-sized artificial eggs (small cuckoo eggs are approximately 2.5 x larger than P. inornatus eggs) were rejected correctly by P. inornatus. These appeared to be more difficult to eject, and in at least four cases the host broke some of its own eggs, which remained in the nest. Females also rejected in response to the larger P. occipitalis eggs, but one ejected its own egg. When clutch size was increased by using natural, unmanipulated P. inornatus eggs (n = 9), rejection never occurred. This suggests that rejection behaviour has not evolved in response to intraspecific parasitism, nor is it due to an increase in clutch size. Control artificial eggs, mimetic to P. inornaltus in both size and colour, were almost always accepted (figure 1), suggesting that females were not using cues such as

Proc. R. Soc. Lond. B (1992)



Costs to host defence K. Marchetti 43

Table 1. The proportion of Phylloscopus inornatus treatments (n = 157) at which thefemale responded by rejecting or accepting different types of experimental eggs, or rejecting her own egg

(Artificial eggs were similar in colour to the natural eggs of P. inornatus. I classify artificial eggs in two sizes (see figure 1): artificial eggs within the size range of natural eggs in the clutch into which they were placed (n = 10), and artificial eggs varying from the maximum natural egg size in the clutch into which they were placed to approximately 1.5 x the size of the median P. inornatus egg size (n = 93). At 41 nests, I painted a natural egg red (n = 29) or with black spots (n = 12). At one nest, both a red egg and an unpainted egg were rejected, and this is excluded.)

rejection of fake/ rejection of own type of egg put in nest manipulated egg unmanipulated egg no rejection total nests

artificial egg (1989) 11 (730%) 4(270%) 0 15 artificial egg (1990) 28 (650%) 3 (70%) 12 (28%) 43 artificial egg (1991) 38 (84%) 4 (9%) 3 (70%) 45 P. occipitalis eggsa (1990) 2 (40%) 1 (20 %) 2 (40%) 5 small cuckoo-sized' artificial egg 8 (100%) 0 0 8 (1990-199 1)

P. inornatus egg painted red (1990) 8 (280%) 3 (10 %) 18 (62 %) 29 P. inornatus egg painted with black spots 1 (8O%) 1 (8%) 10 (83 %) 12 (1990)

a P. occipitalis eggs are 1.6 x the size of P. inornatus eggs (based on measurements of 10 P. occipitallis eggs). Small cuckoo eggs are approximately 2.5 x the size of P. inornatus eggs (Ali & Ripley 1983).

100

80 L

-0-60-

40-

20-

0- rejection of rejection of no manipulated unmanipulated rejection

egg egg

Figure 1. Rates of egg ejection by P. inornatus in response to different types of introduced eggs. Black columns indicate artificial egg mimetic in both size ad colour (i.e. within the size range of natural eggs in the clutch into which they were placed; n = 10), hatched columns indicate artificial eggs mimetic in colour but non-mimetic in size (n = 93; see figure 2), and grey columns inidicate natural eggs painted red (n = 29).

artificiality or paint in making a rejection decision. This is further supported by the response elicited by placing natural P. occzpitaIlis eggs in nests.

The decision to reject is apparently based on the size of eggs within the clutch, as opposed to a single threshold egg size eliciting a rejection response. This can be demonstrated via associations of average egg size within the clutch and size of rejected eggs. If an individual's decision to reject is based on its egg size, then the rejection response to artificial eggs within the natural P. inornatus size range (figure 2) should differ in individuals with relatively small as opposed to relatively large eggs in their clutches (individuals with smaller than average eggs should reject more often). I examined rejection in response to artificial eggs which approximated the size range of natural eggs, and found that the average egg size of individuals which rejected natural-sized artificial eggs was smaller than that of

60 14 NR R

(n-12) (n==31)

70

; 20-

1 9

0 1300 1500 1700 1900 2100 2300 2500

egg size / mm3 Figure 2. Distribution of natural Phylloscopus inornatus egg sizes (mean length x (breadth)2 = 1665 mm3) in 1990. Number at top of bar indicates sample size. Arrows indicate mean+ 95 % confidence limits of artificial eggs (mimetic in colour but variable in size, excluding cuckoo-sized artificial eggs) to which birds responded by not rejecting (NR) (1899+ 206 mm3) or rejecting (R) (2255+ 143 mm3). Rejec- tions include those nests where mistakes were made. Size range of artificial eggs rejected was 1728 + 3248 mm3, and of those not rejected was 1538-2271 mm3. The same result was obtained in 1991 (mean egg size- 1581 ? 292 mm3, n = 90), but is not included in the figure because of the small sample size of measured artificial eggs. Mean + 95 % confidence interval for artificial eggs causing a rejection in 1991 is 1769+ 319 mm3, n = 13; for non-rejected artificial eggs it is 1557 + 24 mm3, n = 2.

individuals which did not reject them (Student's t-test: t = 2.05, d.f. = 29, p < 0.05; mean and s.e. of average egg size of individuals which rejected natural-sized artificial eggs was 1596+ 23 mm3, n = 22 nests, and of individuals which accepted them was 1688 +41 mm3, n = 9 nests). The response to substantially larger-than- natural artificial eggs was similar in all individuals, regardless of egg-size. In addition, egg size varies between years, probably as a function of clutch size (mean natural egg size in 1990 was 1665 mm3, n = 203




44 K. Marchetti Costs to host defence

eggs and 54 clutches, and in 1991 was 1581 mm3, n = 90 eggs and 20 clutches); the size of rejected artificial eggs differs accordingly (mean and 9500 confidence intervals for artificial eggs eliciting a rejection response in 1990 was 2255+ 143 mm3, n = 31, and in 1991 was 1769 + 319 mm3, n = 13).

(b) Current costs to discrimination

(i) Own egg ejections Although the experiments suggest that egg rejection is costly in P. inornatus, the question remains as to whether individuals eject their own eggs in the natural situation without stimulus of an aberrant egg placed in the nest. Rejection decisions apparently occur based on the size of eggs in the clutch, and ejected eggs are often quite similar in size to natural eggs. This suggests that discrimination is strong enough for individuals to eject their own eggs, possibly in response to egg size variability in their clutch. In support of this hypothesis, single eggs have disappeared from at least eight out of 180 unmanipulated nests (Price & Jamdar 1991; K. Marchetti, unpublished observations). In some cases, the missing egg was found intact outside the nest, as is common with ejected experimental eggs. Own-egg ejections may actually occur much more frequently. The observations of Price & Jamdar were not rigorously collected. Before the experiments in 1991, I checked nests on the day of clutch completion and one day later, carefully search- ing the surrounding area, and found that own-egg ejections occurred at two out of 11 unmanipulated nests. Although own-egg ejections may sometimes occur for adaptive reasons, for example the female may remove broken eggs or she may remove the smallest, weakest egg in a clutch that is larger than she is capable of raising, this does not appear to have occurred at these nests. Ejected eggs were intact and alive; when replaced in the nest, they were accepted and incubated. In addition, the ejected eggs were not the smallest in the clutch (the range of egg sizes in nest 1 was 1600-1687 mm3, and the ejected egg was 1604 mm'; in nest 2 the range was 1549-1654 mm3, and the ejected egg was 1558 mm3).

(ii) Rejection in response to within-clutch variation in egg size If individuals do eject their own eggs in response to egg size variation in their clutch, two predictions follow. First, individuals with clutches that are variable in egg size are expected to make rejection mistakes more often than those with relatively uniform clutches. In support of this hypothesis, egg size in clutches of female P. inornatus which made rejection errors in response to artificial eggs is more variable (variability is measured as the size range within the clutch) than in those clutches where females correctly ejected introduced eggs (Student's t-test: t = 1.84, d.f. = 46, one- tailed p < 0.05; mean range for correct ejections is 122.04+ 11.21 s.e., n = 41, and for incorrect ejections is 175.58+25.76, n = 7). The second prediction is that selection should have acted to reduce within-clutch variability in egg size in species with strong discrimination, thereby reducing the likelihood that individuals will eject their own eggs. This is supported by the observation that within-clutch variation in egg

size is lower in P. inornatus (28 ?/% of the overall variability was within-clutch, and 72 0 between- clutch, as estimated using one-way ANOVA, n = 148 eggs and 56 nests) than in P. affinis, which is currently parasitized and does not discriminate unlike eggs (50 %o of the overall variability was within-clutch, n = 16 eggs and 6 nests).

(iii) Response to model cuckoos Mobbing and alarm calling in response to the presence of a cuckoo on the breeding territory is another common means of host defence against cuckoos (Moksnes et al. 1990; Duck- worth 1991), and may have associated costs which persist after the cuckoo has switched hosts. For example, the sight of a cuckoo near the nest may induce desertion by some hosts (Davies & Brooke 1988). In 1991, I placed a model cuckoo near four P. inornatus nests during incubation (sample size is small due to political instability in the area). The birds gave a harsh, rasping alarm call, which was markedly different from calls I have heard when predators (e.g. mice, hawks and owls) are near the nest. The model was strongly attacked, not only by the resident pair but by neighbouring pairs (at one nest, six individuals simultaneously attacked the model). One bird ejected an egg from its nest after responding to a model cuckoo at a neighbour's nest. The presence of currently parasitized species in overlapping habitats, as is observed in this system, means that cuckoos remain in the same area as their previous hosts even while exploiting new hosts.

4. DISCUSSION

How a behaviour as maladaptive as raising other species' young can continue to exist is difficult to envisage. Given that egg discrimination should evolve under very low rates of parasitism (Kelly 1987), and the number of species suitable as hosts for cuckoos is limited, why does the cuckoo not become extinct once all suitable hosts have evolved discrimination? A selective pressure against egg discrimination, in the form of costs to rejection, is probably a necessary requirement for coexistence in this system. Relative to the cost of accepting the parasitic egg (successfully parasitized hosts usually obtain zero reproductive success), rejection costs are low, and do not prevent the evolution of discrimination in currently parasitized species (Rothstein 1975; Roskaft et al. 1990). Rejection costs should, however, result in the loss of discrimination behaviour after the cuckoo switches hosts. Although it has been suggested that rejection behaviour becomes neutral in the absence of parasitism (Rothstein 1990) and this can result in the decay and loss of the behaviour, neutral behaviours are expected to be lost very slowly, if at all (Prout 1964; Coyne & Prout 1986). Thus, in the absence of a selective pressure against egg discrimination, the rate of decay of resistance may be so slow that all current and former hosts would be expected to maintain high levels of resistance, thereby driving cuckoos extinct.

This study provides the first clear demonstration of current costs to defence in a former host of parasitic cuckoos. That such costs can lead to the loss of host




Costs to host defence K. Marchetti 45

defences is supported by a rapid loss of rejection behaviour observed in a population of weaverbirds. This species, which exhibits rejection in natural populations, was introduced into a parasite-free location, where it lost virtually all rejection within approximately 200 years (Cruz & Wiley 1989). Although the authors did not identify a selective pressure against egg discrimination, it seems likely that costs to rejection have resulted in the rapid loss of the behaviour. Loss of rejection allows the parasite to re- exploit past hosts, providing it with an unlimited number of suitable, non-discriminating hosts over evolutionary time. Whereas other host-parasite systems may reach a stable coexistence with neither the host nor the parasite going extinct (Levin & Lenski 1985; May & Robinson 1985; Lenski 1988; May & Anderson 1990; Brooker & Brooker 1990; Brooker et al. 1990; Keymer & Read 1991), these require costs analogous to those demonstrated here. Such costs, which can lead to stable cycling or equilibrium coexistence, may be required if host-parasite systems are to persist.

Many thanks to M. Hack, M. Inayat Ullah, L. Liou, J. Losos, V. Marchetti, T. Price, T. Prout, S. I. Rothstein, H. B. Shaffer, C. A. Toft, A. J. van Noordwijk and A. R. Wani for help and comments on the manuscript, and to G. M. Khatana, B. Raina and M. Shah for providing invaluable assistance in the field. I am particularly indebted to Afroz Mohammed Shah who, in 1991, remained at the study site and collected data for the duration of the field season after my colleagues and I were abducted by terrorists.

REFERENCES

Ali, S. & Ripley, S. D. 1983 Handbook of the birds in India and Pakistan. Oxford University Press.

Brooke, M. de L. & Davies, N. B. 1987 Recent changes in host use by cuckoos Cuculus canorus in Britain. J. Anim. Ecol. 56, 873-883.

Brooke, M. de L. & Davies, N. B. 1988 Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature, Lond. 335, 630--632.

Brooker, L. C. & Brooker, M. G. 1990 Why are cuckoos host specific? Oikos 57, 301-309.

Brooker, L. C., Brooker, M. G. & Brooker, A. M. H. 1990 An alternative population genetics model for the evolution of egg mimesis and egg crypsis in cuckoos. J. theor. Biol. 146, 123-143.

Coyne, J. A. & Prout, T. 1986 Restoration of mutationally suppressed characters in Drosophila melanogaster. J. Hered. 75, 308-310.

Cruz, A. & Wiley, A. W. 1989 The decline of an adaptation in the absence of a presumed selective pressure. Evolution 43, 55-62.

Davies, N. B. & Brooke, M. de L. 1988 Cuckoos vs. reed warblers: adaptations and counteradaptations. Anim. Behav. 36, 262-284.

Davies, N. B. & Brooke, M. de L. 1989a An experimental study of co-evolution between the cuckoo, Cuculus canorus,

and its hosts. I. Host egg recognition. J. Anim. Ecol. 58, 207-224.

Davies, N. B. & Brooke, M. de L. 1989b An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination, and general discussion. J. Anim. Ecol. 58, 225-236.

Dawkins, R. & Krebs, J. R. 1979 Arms races between and within species. Proc. R. Soc. Lond. B 205, 489-511.

Dobson, A. P. & Merenlender, A. 1991 Coevolution of macroparasites and their hosts. In Parasite-host associations (ed. C. A. Toft, A. Aeschlimann & L. Bolis, pp. 83-10 1. Oxford University Press.

Duckworth, J. WV. 1991 Responses of breeding reed warblers Acrocephalus scircapeus to mounts of sparrowhawk Accipiter nisus, cuckoo Cuculus canorus and jay Garrulus glandarius. Ibis 133, 68-74.

Kelly, C. 1987 A model to explore the rate of spread of mimicry and rejection in hypothetical populations of cuckoos and their hosts. J. theor. Biol. 125, 293-299.

Keymer, A. E. & Read, A. F. 1991 Behavioral ecology: the impact of parasitism. In Parasite-host associations (ed. C. A. Toft, A. Aeschlimann & L. Bolis), pp. 37-61. Oxford University Press.

Lenski, R. E. 1988 Experimental studies of pleiotropy and epistasis in Escheria coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42, 425-432.

Levin, B. R. & Lenski, R. E. 1985 Resource-limited growth, competition and predation: a model system for the study of the ecology and coevolution of hosts and parasites. In Ecology and genetics of host-parasite interactions (ed. D. Rollinson & R. M. Anderson), pp. 227-242. London: Academic Press.

Mason, P. & Rothstein, S. I. 1986 Coevolution and avian brood parasitism: cowbird eggs show evolutionary response to host discrimination. Evolution 40, 1207-1214.

May, R. M. & Robinson, S. K. 1985 Population dynamics of avian brood parasitism. Am. Nat. 126, 475-494.

May, R. M. & Anderson, R. M. 1990 Parasite-host coevolution. Parasitology 100, S89-101.

Moksnes, A., Roskaft, E., Braa, A. T., Korsnes, L., Lampe, H. M. & Pedersen, H. C. 1990 Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116, 64-89.

Payne, R. B. 1977 The ecology of brood parasitism in birds. A. Rev. Ecol. Syst. 8, 1-28.

Price, T. & Jamdar, N. 1991 The breeding biology of the Yellow-browed leaf warbler in Kashmir. J. Bombay Nat. Hist. Soc. 88, 1-19.

Prout, T. 1964 Observations on structural reduction in evolution. Am. Nat. 98, 239-249.

Roskaft, E., Orians, G. H. & Beletsky, L. D. 1990 Why do red-winged blackbirds accept the eggs of brown-headed cowbirds? Evol. Ecol. 4, 35-42.

Rothstein, S. I. 1975 Evolutionary rates and host defenses against avian brood parasitism. Am. Nat. 109, 161-175.

Rothstein, S. I. 1982 Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav. Ecol. Sociobiol. 11, 229-239.

Rothstein, S. I. 1990 A model system for coevolution: avian brood parasitism. A. Rev. Ecol. Syst. 21, 481-508.

van Noordwijk, A. J., Keizer, L. C. P., van Balen, J. H. & Scharloo, W. 1981 Genetic variation in egg dimensions in natural populations of the great tit. Genetica 55, 221-232.

Received 27 January 1992; accepted 3 February 1992




Costs to Host Defence and the Persistence of Parasitic Cuckoos

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