Chick recognition and acceptance: a weakness in magpies exploited by the parasitic great spotted cuckoo

Hosts of brood parasites have evolved the ability to discriminate non-mimetic and even mimetic eggs, but not non-mimetic chicks. Here we demonstrate that the great spotted cuckoo Clamator glandarius does not provide its magpie Pica pica host with a super-normal stimulus that helps to avoid recognition, because single cuckoo chicks introduced into otherwise unparasitized magpie nests are not fed at a higher frequency than single magpie chicks introduced to parasitized magpie nests. Another series of experiments demonstrated that magpies have the ability to discriminate cuckoo chicks, mainly when these are introduced at the end of the nestling period, and especially when the cuckoo chick together with a magpie chick is presented to adult magpies outside the nest. This supports the idea that cuckoos exploit the obligatory reaction of magpies to feed all young that have been hatched in their nests and whose signatures they have learnt. Furthermore, the experimental cuckoo chicks in parasitized magpie nests were more likely to be accepted than they were in non-parasitized nests. This supports the hypothesis that magpies may learn to recognise their own nestlings as those present in the nest and may indicate that a comparison between cuckoo and magpie nestlings is the basis of discrimination.     

Does the great spotted cuckoo choose magpie hosts according to their parenting ability?

When brood parasites are about to lay an egg, they have to decide which nest to parasitize. The best nest in which to lay will depend on the parenting ability of the host. We have studied selection of magpie (Pica pica) hosts by great spotted cuckoos (Clamator glandarius). Great spotted cuckoos preferentially parasitize large host nests. Nest volume in magpies is a good indicator of territory quality, since there is a negative relationship between magpie nest size and breeding date, and timing of breeding in magpies is known to be positively related to territory quality. Moreover, magpies occupying high-quality territories have high breeding success. Therefore, nest size is positively related to the quality of magpies. Parasitized magpie nests were of greater volume than the nearest neighbouring nest not parasitized by the great spotted cuckoo. In order to test whether the great spotted cuckoos might select high-quality magpie hosts, we manipulated pairs of parasitized and non-parasitized nests with identical laying dates and habitats, introducing into each of the nests the same number of parasitic and non-parasitic eggs. The number of fledglings reared (magpie plus great spotted cuckoo chicks) in naturally parasitized nests was higher than in experimentally parasitized nests. Thus, the probability of survival of the parasite chicks increased if cuckoo eggs were laid in the nests of high-quality hosts originally chosen by the parasite.     

Great spotted cuckoo fledglings are disadvantaged by magpie host parents when reared together with magpie nestlings

The post-fledging period is a critical phase for juvenile survival, and parental care provided during this period is a key component of avian reproductive performance. Very little is known about the relationships between foster parents and fledglings of brood parasites. Here, we present the results of a 5-year study about the relationships between fledglings of the non-evictor brood parasitic great spotted cuckoo (Clamator glandarius) and its magpie (Pica pica) foster parents. Sometimes, great spotted cuckoo and magpie nestlings from the same nest can fledge successfully, but most often parasitic nestlings outcompete host nestlings and only cuckoos leave the nest. We have studied several aspects of cuckoo post-fledging performance (i.e. feeding behaviour, parental defence and fledgling survival) in experimental nests in which only cuckoos or both magpie and cuckoo nestlings survived until leaving the nest. The results indicate that great spotted cuckoo fledglings reared in mixed broods together with magpie nestlings were disadvantaged by magpie adults with respect to feeding patterns. Fledgling cuckoos reared in mixed broods were fed less frequently than those reared in only cuckoo broods, and magpie adults approached less frequently to feed cuckoos from mixed broods than cuckoos from only cuckoo broods. These results imply that the presence of host's own nestlings for comparison may be a crucial clue favouring the evolution of fledgling discrimination; and furthermore, that the risk of discrimination at the fledgling stage probably is an important selection pressure driving the evolution of the arms race between brood parasites and their hosts.     

Brood mate eviction or brood mate acceptance by brood parasitic nestlings? An experimental study with the non-evictor great spotted cuckoo and its magpie host

Some avian brood parasitic nestlings are highly virulent, destroying all host eggs or nestmates, while others accept growing up together with host nestmates. The traditional idea was that all brood parasitic nestlings would benefit from being alone in the host nest. Thus, why do nestlings of some brood parasitic species accept the company of host offspring in the nest? The trade-off hypothesis suggests that brood parasites must balance the costs and benefits of killing host young because of two major potential costs: risk of nest desertion and loss of begging assistance. Here, we test this hypothesis in a non-evictor cuckoo species, the great spotted cuckoo Clamator glandarius and its main host, the magpie Pica pica, by manipulating brood size (1–3 nestlings) and brood composition (only cuckoo, only magpie or mixed) during three consecutive breeding seasons. None of the broods were abandoned by host parents, and cuckoo nestlings alone in the nest tended to grow faster (i.e. wing length). Thus, none of the predictions of the two potential costs on which the trade-off hypothesis is based apply to the great spotted cuckoo–magpie system. Our experimental study could not directly test why chick killing has not evolved in great spotted cuckoos, but the results point in the direction of several possibilities. We suggest that chick killing in great spotted cuckoos may not be adaptive mainly because another, less costly strategy (i.e. outcompeting host nestmates for food), is efficient for successful parasitism of magpie hosts.     

Does supernormal stimulus influence parental behaviour of the cuckoo's host?

The supernormal stimulus hypothesis (SSH) states that a cuckoo chick should obtain more parental care than host young by means of exaggerated sensory signals. We tested the SSH by comparing parental care by reed warblers at parasitized and non-parasitized nests. A comparison of feeding rates to parasite and host chicks of the same size showed that parasitized nests received more food than non-parasitized ones with one host chick. There was an interesting relationship between average prey length and the mass of a cuckoo chick: prey length first increased with chick mass, but decreased after the cuckoo chick outgrew the average-sized host brood (three to four young at fledging). This might be expected if fosterers reduced the selectivity of their foraging behaviour when trying to satisfy the supernormal food demands of the parasitic chick. This suggestion is supported by the finding that the relationship between nestling mass and proportion of less economical small prey is inverse to the relationship between nestling mass and prey size. These results suggest that the parental behaviour of reed warblers is adjusted by selection to the needs of an average-sized brood. The overall proportion of insect orders was significantly different between the parasitic and host chicks. This result probably reflects the opportunistic foraging habits of the host. The qualitative difference (proportion of insect orders) between host and cuckoo nestling diets is partly a by-product of unequal length distribution of members of different taxonomic groups. The results of this study are consistent with the SSH.     

Cuckoo growth performance in parasitized and unused hosts: not only host size matters

The quality and quantity of food delivered to young are among the major determinants of fitness. A parental provisioning capacity is known to increase with body size. Therefore, brood parasitism provides an opportunity to test the effects of varying provisioning abilities of different-sized hosts on parasitic chick growth and fledging success. Knowledge of growth patterns of common cuckoo, Cuculus canorus, chicks in nests of common hosts is very poor. Moreover, no study to date has focused on any currently unused hosts (i.e., suitable cuckoo host species in which parasitism is currently rare or absent). Here, I compare the growth performance of cuckoo chicks in nests of a common host (the reed warbler, Acrocephalus scirpaceus) and two unparasitized hosts (the song thrush, Turdus philomelos, and the blackbird, Turdus merula). Parasitic chicks were sole occupants of the observed nests, thus eliminating the confounding effect of competition with host chicks. Experiments revealed striking differences in parasitic chick growth in the two closely related Turdus hosts. Cuckoo chicks cross-fostered to song thrush nests grew much quicker and attained much higher mass at fledging than those in nests of their common reed warbler host. Alternatively, parasitic chicks in blackbird nests grew poorly and did not survive until fledging. I discuss these observations with respect to host selection by parasitic cuckoos.     

Location of suitable nests by great spotted cuckoos: an empirical and experimental study

Brood parasites depend entirely on their host species to raise their nestlings until independence. Thus, brood-parasite females must discover and select nests that are at a suitable stage for parasitism, and thus, the location of each parasitic egg is crucial in determining the brood-parasite female’s fitness. In relation to host behaviour, one of the main hypotheses proposed to explain how brood-parasite females find and select a suitable nest posits that the most active hosts during nest building should undergo a higher risk of being parasitised (the “host-activity hypothesis”). Here, using the great spotted cuckoo, Clamator glandarius–magpie, Pica pica system, we found that not only cuckoo females parasitise magpie nests regardless of the location and characteristics of nests, but also that the parasite’s observation of host activity near the nest determines a cuckoo female’s decision of laying in a nest. Only one experimental nest (without host activity) was parasitised before the magpie started laying, while 34.14?% of natural active nests were parasitised before the magpie started laying. These observations support the host-activity hypothesis for nest location in great spotted cuckoos.     

Micro-evolutionary change in host response to a brood parasite

The relationship between brood parasites and their hosts is usually assumed to result in coevolution, and documentation of changes in extant populations should thus be possible. Here we describe how the ejection rate of eggs of an obligate brood parasite, the great spotted cuckoo Clamator glandarius, by its host, the magpie Pica pica, has recently increased in an area in southern Spain. The ejection rate of great spotted cuckoo eggs in naturally parasitized nests of the magpie increased at a rate of 0.5% year' during the period 1982–1992. This result was verified in a number of field experiments using nonmimetic and mimetic model eggs. The rate of increase in ejection rate was 4.7% year^-1 for mimetic eggs and 2.3% year^-1 for nonmimetic eggs. There were clear differences in parasitism by the great spotted cuckoo between study plots and years, which makes comparisons of rates of parasitism between areas difficult without considering temporal variation. The recent increase in the ejection response of magpies to great spotted cuckoo eggs was not due to magpies using the abundance of cuckoos as a cue to the intensity of parasitism.     

Red-winged blackbird parental investment following brood parasitism by brown-headed cowbirds: is parentage important?

Parental investment by red-winged blackbirds (Agelaius phoeniceus) in response to natural and experi‐mental parasitism by brown-headed cowbirds (Molothrus ater), and in response to freeze-dried, female cowbird mounts presented near redwing nests during the egg-laying period was measured. Two measures of redwing parental investment were used: nest defense effort toward a model predator, and rate of feeding nestlings. There were no significant differences in levels of parental investment among unparasitized nests, naturally parasitized nests, or experimentally parasitized nests. Similarly, parental investment did not differ between redwings that were exposed to the cowbird mount and those that were not exposed to the mount, or among redwings exposed to the cowbird mount at different distances from the nest. This suggests that red-winged blackbirds do not recognize when they have been parasitized, and hence do not associate parasitism with a decrease in their parentage, or that parentage is not an important predictor of parental investment in this species. Received: 24 January 1997 / Accepted after revision: 7 June 1997     

Post-ejection nest-desertion of common cuckoo hosts: a second defense mechanism or avoiding reduced reproductive success?

Hosts of the common cuckoo (Cuculus canorus), an avian brood parasite, develop antiparasite defense mechanisms to increase their reproductive success. Ejection of the parasite egg and desertion of the parasitized nest are the most typical adaptations in response to brood parasitism, but nest desertion may also occur in response to partial clutch reduction, independently from parasitism. Some great reed warblers (Acrocephalus arundinaceus) showed both mechanisms in the same incidence of cuckoo parasitism: in 18% of successful ejections of the parasite eggs, they deserted their nests. We studied if such cases of post-ejection nest-desertion are caused by brood parasitism or reduced clutch value. We experimentally parasitized clutches consisting of five or three host eggs with two painted conspecific eggs to mimic parasitic eggs, as multiple parasitism is frequent in the area. Although hosts ejected these parasitic eggs in both clutch categories (100% and 67% for the larger and smaller inital clutch sizes, respectively), we found that after manipulation, post-ejection nest-desertion frequently occurred at small (3-egg) clutches (40%), but rarely at large (5-egg) clutches (17%). The same phenomenon also occurred when unparasitized 3-egg clutches were reduced by two eggs, but not when 5-egg clutches were reduced in the same way. A logistic regression model revealed that only initial clutch size affected nest desertion of parasitized nests in our experiments. Therefore, we conclude that post-ejection nest-desertion is not a second antiparasite mechanism, which might serve as a redundant antiparasite defense, but a reaction to typically small and further decreased clutch size.     

Breeding success of a brood parasite is associated with social mating status of its host

Reproductive success of brood parasites varies considerably both among and within host species, mainly due to differences in host egg-rejection rates and survival of parasitic chicks. Here, we investigated the breeding success of the cuckoo (Cuculus canorus) in one of its major hosts, the great reed warbler (Acrocephalus arundinaceus), with respect to host social mating status. In this passerine, polygynous males provide less parental care to their young per nest than monogamous males. Consequently, their less-assisted females may fledge lower numbers of nestlings than monogamous females. This may be especially true for secondary females, which often receive limited or no paternal help with young at all. Based on these findings, we expected higher cuckoo reproductive success in nests of socially monogamous than polygynous great reed warbler males. More specifically, we predicted lower fledging success of cuckoo young in nests of secondary than primary or monogamous females. In line with the prediction, we found higher cuckoo fledging success in nests of monogamous than polygynous males, monogamous nests being more than twice as successful as secondary nests. We detected, however, only a tendency to lower cuckoo success in primary compared to monogamous nests and no differences between primary and secondary nests. Moreover, neither parasitism nor host egg-rejection rates differed among the nests of different status. Our results show, for the first time, that the social mating status of a host may influence the overall reproductive success of a brood parasite and thus should be considered in further studies.     

The multidimensionality of behavioural defences against brood parasites: evidence for a behavioural syndrome in magpies?

Studies of antiparasite defences against cuckoo parasites have largely neglected the possibility that behavioural components of host defence may correlate giving rise to a behavioural syndrome. Furthermore, the different contribution of the host’s sex in nest defence has traditionally been disregarded. Here, we studied magpie (Pica pica) mobbing behaviour towards dummies of great spotted cuckoo (Clamator glandarius) and non-harmful hoopoes (Upupa epops) and egg rejection of parasite eggs in a population of colour-banded magpies. We predicted a positive correlation between the intensity of nest defence and egg rejection within each sex and that females respond more intensely than males to the threat of brood parasitism as they undertake incubation. Magpie males, but not females, defended their nests more intensely in those nests in which cuckoo model eggs were rejected. Individual magpies did significantly differ in their baseline level of nest attentiveness; however, there were no individual differences once pair identity was considered. Males and females defended their nests more intensely when it was exposed to the presence of a great spotted cuckoo dummy. Males, but not females, were more prone to appear at their nests, and females, but not males, were more prone to defend more intensely when their nests were challenged by a parasite threat. Our results thus agree with the view that mobbing behaviour and egg rejection in magpies may actually constitute a pseudosyndrome and highlight the necessity to integrate interindividual variation and the sex of the host in studies of the evolution of host defences.     

The cost of host egg damage caused by a brood parasite: experiments on great spotted cuckoos (Clamator glandarius) and magpies (Pica pica)

Adult great spotted cuckoos, Clamator glandarius, frequently damage one or more eggs of their magpie host, Pica pica, without removing or eating them. The presence of damaged host eggs could signal parasitism thereby increasing the probability that the parasitic egg is ejected. This hypothesis was tested by experimentally introducing a model cuckoo egg with or without damaged host eggs. Magpie responses to experimental parasitism did not differ significantly between treatments implying that damaged host eggs are not used by magpies to assess parasitism. We followed the fate of magpie eggs naturally damaged by the great spotted cuckoo or experimentally damaged by us. Host response was very similar for naturally or experimentally damaged host eggs, but varied significantly according to the type of egg damage, eggs being removed more frequently when pecked than crushed, while cracked eggs were never removed. However, the egg damage that most readily causes egg removal is albumen leakage. Received: 30 November 1998 / Received in revised form: 7 June 1999 / Accepted: 12 June 1999     

Begging behavior and food acquisition by brown-headed cowbird nestlings

Understanding the selective forces that limit the exaggeration of begging signals is a critical issue in understanding the evolution of begging behavior. I studied the begging behavior of nestlings of the brown-headed cowbird (Molothrus ater), a brood parasite. In the nests of indigo buntings (Passerina cyanea), brown-headed cowbird nestlings received approximately twice as much food per hour than their host nestmates. I tested three hypotheses for the mechanism by which cowbirds acquired more food than their bunting nestmates: the size advantage hypothesis, the signal exaggeration hypothesis, and the novel begging behavior hypothesis. I found support for the hypotheses that cowbirds acquire more food as a result of their larger body size, and due to the exaggeration of begging signals that are not dependent on body size. I did not find support for the role of novel begging behaviors in cowbird food acquisition. These results suggest that food acquisition by host chicks in unparasitized nests could be increased by the exaggeration of begging signals. Recent work suggests that such exaggeration may be limited by the risk of nest predation, but further studies are needed. Received: 12 December 1997 / Accepted after revision: 29 December 1997     

Brood reduction in response to manipulated brood sizes in the common swift (Apus apus)

Following a brood size manipulation experiment on the common swift (Apus apus) in which different levels of parental effort were created, brood reduction occurred in all five nests manipulated to four chicks and in two of the five manipulated to three young. This provided an opportunity for looking in detail at the parental investment decisions concerning allocation strategies between parent and young during the process of brood reduction. The data recorded here were analysed on a visit-by-visit basis regarding changes in parental and chick body masses, the mass of prey delivered and the estimated mass of parental self-feeding. The results show that food delivery rates did not increase in proportion to the number of chicks in the broods. This reduction in delivery rates per chick resulted in lower chick masses and ultimately in the death of one or more chicks in the larger broods. The resulting low parental body masses for adult birds feeding larger broods suggested that these parents could not have raised all their young without risking their own survival. There was a tendency for parents from nests that experienced brood reduction to feed themselves instead of allocating most of the food gathered to the young. After brood reduction, parents regained lost body mass and their young fledged at masses only slightly lower than normal. The differential allocation decisions regarding parental self-feeding which resulted in brood reduction were largely responsible for keeping the parents in good enough condition to care for the surviving nestlings. Therefore, this study clearly demonstrates that brood reduction can operate through the differential allocation of food between parent and young in a way that can have adaptive consequences for the survival of parents and their young. Correspondence to: T.L.F. Martins     

Food delivery and sibling competition in experimentally even-aged broods of the cattle egret

Summary The age of nestlings was made even in 12 nests of cattle egrets (Bubulcus ibis) by exchanging young chicks or eggs in a breeding colory in Japan. The growth of chicks in such synchronously hatching broods (SHBs) grew almost as fast as first-hatched chicks in 38 control (asynchronously hatching) broods (AHBs). Four last-hatched chicks in AHBs but no chicks in SHBs died of starvation. The frequency of parental nest-visits with food, that of begging food by chicks, and food mass eaten by chicks were greater in SHBs than in AHBs during the first half of the nestling period and similar thereafter. Dominance rank within each SHB was formed through ritualistic fights among siblings. It was correlated with neither growth rates nor winning ratios in food contests, but in some SHBs the subordinate chicks were attacked more frequently by dominant siblings during food contests than in AHBs. The most subordinate chick in one SHB died as a direct result of such attacks. Sibling aggressions were more frequent in SHBs than in AHBs.     

Compensating for the costs of polygyny in hen harriers Circus cyaneus

In polygynous species, the adults are faced with a dilemma during chick rearing. Males must decide how to distribute food between their females and food allocation patterns are often highly unequal. In turn, the females that receive less food from males have to decide how much time to invest in additional hunting. If they spend more time hunting, then they leave their young exposed to weather and predators. However, if they stay at the nest, they increase the risk of their chicks starving. One way that birds may compensate for reduced provisioning is by increasing the size of prey caught. We tested this hypothesis by comparing prey deliveries to nests of hen harriers, Circus cyaneus, with females of different breeding status. As expected, male harriers delivered less food items to the nests of polygynous females, and especially their secondary, or β females. However, both sexes were able to compensate by delivering larger items and there was no difference in the overall mass of food delivered to nests. Moreover, females spent a similar amount of time at the nest, irrespective of status, and there were no overall differences in breeding success. Our results show that polygynous female harriers can compensate for the costs of polygyny, but we suggest that their ability to do so will vary according to the abundance of both large prey and predators.     

Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts

Common cuckoo (Cuculus canorus) parasitism drastically reduces the reproductive success of their hosts and selects for host discrimination of cuckoo eggs. In a second stage of anti-parasite adaptation, once cuckoos can lay eggs that mimic those of their hosts, a high uniformity of host egg appearance within a clutch may favour cuckoo egg discrimination. Comparative evidence provides indirect support for this hypothesis although experimental support is currently lacking. Here, we studied the effect of experimentally decreased uniformity of host egg appearance on cuckoo egg discrimination by great reed warbler (Acrocephalus arundinaceus) hosts in a population in which long-term cuckoo parasitism has led to high levels of cuckoo–host egg mimesis. We manipulated host clutch uniformity by adding extra spots to fresh host eggs just after they were laid. Rejection of non-mimetic experimental eggs added to these nests was compared with those in control nests in which uniformity was not altered. Previously, by over-painting real spots in a control group of nests, we showed a negligible effect of our paints on hosts’ perception of their eggs. We show that for the great reed warbler, non-mimetic experimental eggs were relatively more tolerated in experimental nests, i.e. with lower uniformity (40%) than in control nests (5%). This is the first experimental study, to our knowledge, which demonstrates a reduced discrimination of foreign eggs as a consequence of an increase of egg phenotypes variation perception in a cuckoo host.     

Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis

Eggs of several brood parasites have thicker and stronger shells than expected for their size. The present study evaluated the puncture resistance hypothesis for the occurrence of thick-shelled eggs in common cuckoos Cuculus canorus by investigating costs of cuckoo egg ejection in four Acrocephalus warblers—the great reed warbler A. arundinaceus, reed warbler A. scirpaceus, marsh warbler A. palustris and sedge warbler A. schoenobaenus. The three latter species all suffered ejection costs, while ejection was not costly in the larger great reed warbler. The occurrence of ejection costs was negatively related to host bill size. In the marsh warbler, we compared ejection costs in naturally parasitized nests and two experimental treatments, in which broods were parasitized artificially with great reed warbler and conspecific eggs. Hosts damaged their own eggs significantly more often when ejecting the thick-shelled cuckoo eggs than when ejecting the similarly sized but thinner-shelled great reed warbler eggs, providing some support for the puncture resistance hypothesis. Ejection of conspecific eggs did not involve any costs. Furthermore, contrary to predictions derived from the laying damage hypothesis, there was no evidence that egg damage was associated with cuckoo egg laying. Hosts damaging their own eggs during ejection were more likely to subsequently desert their clutches than those that did not. The frequency of clutches smeared with the contents of the ejected egg were positively related to the hypothesized difficulty of foreign egg puncturing. Potential advantages of thicker shells in common cuckoo eggs are discussed.     

American robin nestlings compete by jockeying for position

Summary We investigated whether nestling American robins (Turdus migratorius) were capable of influencing food distribution in their nests by perceiving that certain sectors of the nest received a relatively high proportion of feedings and positioning themselves accordingly. Feeding observations were obtained from videotape recordings taken at different stages of the nestling period. Parents generally arrived at a predictable location on the nest rim and allocated proportionally more food to nestlings in the central position. The degree of nestling movement was significantly positively correlated with variation in the predictability of parental arrival locations on the nest rim. Furthermore, nestlings moved more in broods suffering brood reduction. This suggests that when competition for food is intense and the location of parental arrival is predictable, nestlings respond by jockeying for access to the most favorable (i.e., central) position in the nest. We conclude that jockeying for position by nestlings can influence the pattern of food allocation by parents, and that hungry nestlings can improve their competitive standing against nestmates by moving to positions where parents are more likely to feed them. Correspondence to: S.B. McRae