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Journal ArticleDOI

Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host

23 Apr 2009-Biology Letters (The Royal Society)-Vol. 5, Iss: 2, pp 169-171
TL;DR: This is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them, and results show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoos eggs may avoid rejection by means of their unusually high structural strength.
Abstract: Given the high costs of avian obligate brood parasitism, host individuals are selected to reject parasitic eggs they recognize as foreign. We show that rejection may not necessarily follow egg discrimination when selective removal of the parasitic egg is difficult. We studied egg rejection behaviour in a small host of the common cuckoo Cuculus canorus, the eastern olivaceous warbler Hippolais pallida, by experimental parasitism with model and real non-mimetic cuckoo eggs and video recordings of host behaviour. Hosts pecked 87 per cent (20 out of 23) of the model eggs but eventually accepted 43.5 per cent (10 out of 23) of them. A similar pattern was found for real cuckoo eggs, which were all pecked, but as many as 47 per cent (7 out of 15) of them were accepted. To our knowledge, this is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them. Our results also show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoo eggs may avoid rejection by means of their unusually high structural strength.

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Citations
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Journal ArticleDOI
TL;DR: The results show that most hosts, regardless of the presumed evolutionary time of interaction with the parasite, have evolved some type of antiparasitic defense.
Abstract: The cowbirds (Molothrus, Icteridae) are a monophyletic group that includes five extant brood-parasitic species. The Screaming (M. rufoaxillaris), Giant (M. oryzivorus) and Shiny (M. bonar- iensis) cowbirds range mostly in South America. Screaming and Shiny cowbirds are the ancestral and most recent species of the clade, respectively, therefore, differing in how long they have coevolved with their hosts. We present new experimental data on egg-rejection in a host of the Shiny Cow- bird, the House Wren (Troglodytes aedon), review different lines of antiparasitic defenses in hosts of Screaming, Giant and Shiny cowbirds and assess whether hosts of different parasites differ in the type and extent of defenses. Hosts of all three parasites ejected non-mimetic eggs. Most hosts of Giant and Shiny cowbirds were grasp ejectors, whereas the main host of the Screaming Cowbird (the Baywing, Agelaioides badius) ejected parasitic eggs using its feet. Hosts smaller than Shiny Cowbirds neither ejected cowbird eggs nor deserted nests following parasitism. Some hosts also reacted more aggres- sively towards the parasite. The main host of Screaming Cowbird discriminated against non-mimetic chicks. Our results show that most hosts, regardless of the presumed evolutionary time of interaction with the parasite, have evolved some type of antiparasitic defense.

8 citations


Cites background from "Evidence for egg discrimination pre..."

  • ...Evidence for the equilibrium hypothesis is indirect and based on studies documenting the existence of costs associated to hosts’ antiparasitic defenses (Rohwer et al., 1989; Lotem et al., 1992; Antonov et al., 2009; Krüger, 2011)....

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  • ..., 1996; Lorenzana and Sealy, 2001]), accidental damage to host eggs during ejection attempts (Rohwer et al., 1989; Røskaft et al., 1993; Underwood and Sealy, 2006; Antonov et al., 2009), increased risk of nest failure following the desertion of parasitized nests (Krüger, 2011), and possible retaliation by adult parasites after the rejection of parasite eggs (Hoover and Robinson, 2007)....

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  • ...…and Sealy, 2001]), accidental damage to host eggs during ejection attempts (Rohwer et al., 1989; Røskaft et al., 1993; Underwood and Sealy, 2006; Antonov et al., 2009), increased risk of nest failure following the desertion of parasitized nests (Krüger, 2011), and possible retaliation by…...

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Book ChapterDOI
01 Jan 2021
TL;DR: This article found that hosts are more aggressive toward brood parasites during the high-cost laying and incubation stages compared to the low-cost nestling stage, whereas responses to nest predators were predicted to be consistently strong or even increasing toward latter nesting stages.
Abstract: Many animals have evolved fine-tuned enemy recognition (the ability to discriminate between threat types) and respond to threats based on their particular impact on survival and/or fitness. Birds represent an important and tractable behavioral study system to explore hypotheses of enemy recognition in detail: in addition to predation risk to adult and nest survival, up to 17% of avian species also face reproductive threats from brood parasitism, whereby parasites lay their eggs in other species' nests. While nest predation is detrimental to progeny fitness throughout the reproductive cycle, brood parasitism can carry different costs depending on the host's nest stage and whether the host rejects parasitic eggs or chicks. We conducted a literature review and a formal meta-analysis of studies that conducted model presentation experiments to compare aggression levels of hosts toward brood parasites vs. predators, and synthesized up-to-date findings on such avian enemy recognition patterns. We focused on whether hosts are more aggressive toward brood parasites during the high-cost laying and incubation stages compared to the low-cost nestling stage, whereas responses to nest predators were predicted to be consistently strong or even increasing toward latter nesting stages. We also evaluated whether these front-loaded defenses prior to the brood parasite's access to nests are modulated by hosts' foreign egg ejection responses (accepters vs. rejecters), brood parasitic offspring strategy (nestmate-evictors vs. nest-sharers), and host-brood parasite geographic overlap (sympatry vs. allopatry). As predicted, hosts responded more aggressively toward models of brood parasites during the laying and incubation stages compared to the nestling stage. In turn, host aggression toward nest predators increased in intensity level during the nestling stage. We also found support that host type mediates anti-brood parasitic responses, in that accepters were generally more aggressive to brood parasites than rejecters. We did not find evidence that geographic overlap significantly affected anti-parasitic responses, but we did find differences based on the brood parasite's nestling strategies (evictor vs. non-evictor). These findings indicate that avian hosts of brood parasites make adaptive decisions regarding costly nest defensive behaviors to protect their offspring depending on the type and cost of the threat.

8 citations

Journal ArticleDOI
TL;DR: This work investigated antiparasite strategies of the dickcissel, Spiza americana, whose apparent acceptance of parasitism is unlikely to be explained by lag because its historic centre of abundance overlaps with that of the cowbird.

8 citations

Journal ArticleDOI
TL;DR: It is found that males can recognize non-mimetic eggs, although their recognition abilities were less fine-tuned compared to females, who also recognized mimetic eggs.
Abstract: In the field of brood parasitism, it has been traditionally assumed that only the incubating sex rejects parasitic eggs, but this assumption has been rarely explored despite its important implications for the evolutionary relationship between brood parasites and hosts. Here, we used information on previous egg-rejection experiments to explore the recognition abilities of both males and females of Eurasian blackbirds Turdus merula towards experimental eggs with a variable degree of mimicry. We found that both sexes recognized non-mimetic eggs, supporting the idea that visits to the nest can favor the evolution of rejection abilities. In contrast, only females recognized mimetic eggs, indicating that although recognition abilities can evolve in both sexes, they are subsequently refined in females probably due to their more frequent interaction with parasitic eggs. Clutch size affected nest attendance since females, but not males, spent more time at the nest and visited it more frequently in larger clutches. Finally, our recordings showed that blackbird males are able not only to recognize, but also to eject parasitic eggs. Our results provide new insights into the main anti-parasitic defense in birds, egg rejection, and highlight the need of considering the role of the non-incubating sex in egg-rejection studies. Given the high costs associated to avian brood parasitism, both sexes are expected to evolve anti-parasitic defenses. However, in those species in which only females incubate, females have traditionally been assumed to be the responsible for egg rejection. Here, using the Eurasian blackbird (Turdus merula), we investigated the existence of egg-rejection abilities in non-incubating males and compared them to those exhibited by females. We found that males can recognize non-mimetic eggs, although their recognition abilities were less fine-tuned compared to females, who also recognized mimetic eggs. Even though females were the responsible for most documented egg-ejection events, recordings confirmed that males could also be involved in egg ejection, which could have important implication for the evolution of anti-parasitic defenses in host populations.

8 citations


Cites background from "Evidence for egg discrimination pre..."

  • ...Egg-pecking or egg-touching behavior is considered reliable proxies for egg recognition (Soler et al. 2002, 2012; Underwood and Sealy 2006; Antonov et al. 2008, 2009), even when acceptance decisions occurs (Ruiz-Raya et al. 2015; Soler et al. 2017)....

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Dissertation
01 Jan 2011
TL;DR: It is found that koel eggs were highly non-mimetic to those of common myna and long-tailed shrike, but showed good mimicry to house crow eggs, while cuckoo eggs showed excellent egg mimicry with the eggs of their black drongo hosts, as did common hawk cuckoos and piedcuckoos with their jungle babbler host.
Abstract: The interaction between brood parasitic cuckoos and their hosts represents a traditional example of coevolution, whereby obligate interspecific brood parasitic cuckoos completely rely on their hosts to do their parental care for them by laying their eggs in the host’s nest. This thesis brings together a great deal of information documenting and clarifying the interactions between different species of hosts and their respective parasitic cuckoos in Bangladesh. I recorded parasitism rates to determine the extent of brood parasitism and to identify the host species that were parasitised by sympatric cuckoos. Four parasitic cuckoos were documented: the Asian koel ( Eudynamys scolopacea), the common hawk cuckoo (Cuculus varius; previously known as Hierococcyx varius), the pied cuckoo (Clamator jacobinus) and the Indian cuckoo (Cuculus micropterus). These cuckoos were sympatric and parasitised different host species, including the house crow (Corvus splendens), the long-tailed shrike (Lanius schach), the common myna (Acridotheres tristis), the jungle babbler (Turdoides striatus) and the black drongo (Dicrurus macrocercus). All of these cuckoo species are obligate brood parasites. The Asian koel utilised the following three hosts: the house crow, the common myna and the long-tailed shrike. The latter was recorded for the first time as a host for the Asian koel in Bangladesh. We found that koel eggs were highly non-mimetic to those of common myna and long-tailed shrike, but showed good mimicry to house crow eggs. Indian cuckoos showed excellent egg mimicry with the eggs of their black drongo hosts, as did common hawk cuckoos and pied cuckoos with their jungle babbler host. The hosts accepted the eggs of all four cuckoo species. However, the common myna was more likely to abandon nests parasitised by the koel than unparasitised ones. All of the host species suffered the costs of koel parasitism, showing reduced breeding success. Proximity to fruit trees was an important predictor of the probability of parasitism in the three koel host species studied. There was a significant positive relationship between nest volume and probability of parasitism by Asian koels. Furthermore, the colonial breeding house crows suffered comparatively less parasitism than the other two koel host species. Long-tailed shrike nests close to conspecific neighbours were less likely to be parasitised, and the risk of parasitism was increased in nests lower to the ground. The risk of parasitism increased during the breeding season for house crows and common mynas. All three Asian koel hosts tolerated multiple parasitism. We investigated whether there was any interspecific competition among the sympatric cuckoos. In theory, sympatric parasites should show niche segregation through variation in host use. As predicted, each cuckoo species parasitised different host species; however, host use overlapped in common hawk cuckoos and pied cuckoos, but interspecific competition was reduced because these two cuckoo species have different breeding seasons. Furthermore, there was a significant difference in parasitism rate among the three main habitats: human habitations, mixed scrub forests and monoculture plantations. This indicated that different cuckoos favour specific habitats, even if their favourite host also occurs elsewhere. Finally, I tested responses against foreign eggs by the cuckoo hosts as well as by potential cuckoo hosts in the study area. For this purpose, I used differently sized and coloured model eggs. Common mynas and jungle babblers accepted all non-mimetic eggs, as did most of the house crows (91 %). Long-tailed shrikes rejected 75 % of the non-mimetic model eggs. Finally, black drongos turned out to be strong rejectors and could do so without damaging any of their own eggs, most likely because they grasped and ejected the non-mimetic model egg. This result indicates that the black drongo has been in a coevolutionary arms race with the Indian cuckoo since drongos accepted mimetic cuckoo eggs. Species such as the Oriental magpie robin (Copsychus saularis), red-vented bulbul (Pycnonotus cafer) and Asian pied starling (Gracupica contra), which likely have no history of interaction with cuckoos, accepted 100 % of the non-mimetic model eggs. In conclusion, our findings describe host nest use cues used by the Asian koel, which may provide background for further studies in other sympatric brood parasites. In spite of the high degree of acceptance of parasitic eggs, the breeding success of both cuckoos and hosts should be more closely studied to obtain a better understanding of the costs of parasitism. Future experimental studies are highly recommended to achieve a better understanding of host responses to Asian cuckoo species.

7 citations


Cites background from "Evidence for egg discrimination pre..."

  • ...This may have forced them to accept the cuckoo eggs (Antonov et al. 2009)....

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References
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Journal ArticleDOI
TL;DR: The variation in rejection of unlike eggs among different species of suitable cuckoo hosts is not related to the current costs or benefits of rejecting cuckoos, and it is suggested that the variation represents snap shots in evolutionary time of different stages of a species.
Abstract: SUMMARY (1) There was no difference in the distinctiveness of egg markings between species that have interacted strongly with cuckoos and species that have not, nor in intra-clutch variation, nor in inter-clutch variation within a species. In Iceland, where they are isolated from cuckoos, the eggs of meadow pipits and pied/white wagtails showed no differences in intra-clutch variation, nor inter-clutch variation, from those in parasitized populations in Britain. Thus there was no evidence that host egg patterns evolve in response to cuckoos. (2) None of the four species tested discriminated against an odd chick (another species) in their nest (chaffinch, reed warbler, reed bunting, dunnock). Hosts therefore evolve discrimination against odd eggs but not against odd chicks. (3) The variation in rejection of unlike eggs among different species of suitable cuckoo hosts is not related to the current costs or benefits of rejecting cuckoo eggs. We suggest that the variation represents snap shots in evolutionary time of different stages of a

375 citations


"Evidence for egg discrimination pre..." refers background in this paper

  • ...Avian obligate brood parasites generally impose high fitness costs on their hosts, resulting in sophisticated coevolutionary arms races (Davies & Brooke 1989; Moksnes et al. 1990)....

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  • ...However, despite the apparent benefits of rejection, there is substantial variation both among and within host species used by cuckoos in their responses to foreign eggs (Davies & Brooke 1989; Moksnes et al. 1990; Martı́n-Gálvez et al. 2007; Stokke et al. 2008)....

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  • ...Despite some indirect demonstrations of conditional host responses (Davies & Brooke 1989; Moksnes et al. 1993), there is very little direct evidence for acceptance of cuckoo eggs once host individuals have discriminated against them (Lindholm 2000; Soler et al. 2000)....

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Journal ArticleDOI
TL;DR: The results of this study lend support to the hypothesis that the differences in the degree of responses by the host species towards parasitism by the cuckoo reflect different stages in a continuous coevolutionary arms race with cuckoos.
Abstract: Responses of 33 potential host species towards a non-mimetic, dummy, cuckoo egg placed in their nest were tested (N = 372). For 22 of these species, their behavioural responses towards a dummy cuckoo placed near their nest were also tested (N = 193). The species were grouped in A) most common hosts: species which at the moment are losing out in the coevolutionary arms race with the cuckoo and which today represent favorite hosts; B) frequently-used hosts: species which at the moment are assumed to be true cuckoo hosts, but which are not so commonly used as those in group A; C) rarely-used hosts: species which would appear to be suitable hosts, but which despite of this, are rarely used. These species are assumed to be ahead of the cuckoo in the coevolutionary arms race; D) unsuitable hosts: species with a breeding biology which either prevents, or counteracts, cuckoo parasitism. They are therefore assumed never to have been engaged in a coevolutionary arms race with the cuckoo. In the most common hosts the median acceptance rate of the non-mimetic egg was 86 % , in the frequently-used hosts 33 % , in the rarely-used hosts 10 % and in the unsuitable hosts 100 %. In the most common hosts the median rate of aggression shown towards the cuckoo dummy was 50%, but the most numerous species in this group, the meadow pipit, showed aggressive behaviour in 60% of the cases. The median aggression rate both in the frequently-used hosts and the rare hosts was 100 % and in the unsuitable hosts 0%. The bluethroat was the only species which accepted the non-mimetic dummy egg at a higher rate later on during the incubation period than during earlier stages. A positive correlation was found between the power of egg discrimination and the rate of aggression shown towards the dummy cuckoo. Such aggression was stronger when both parents were present at the nest than when only one parent was present. The results of this study lend support to the hypothesis that the differences in the degree of responses by the host species towards parasitism by the cuckoo reflect different stages in a continuous coevolutionary arms race with cuckoos.

291 citations


"Evidence for egg discrimination pre..." refers background in this paper

  • ...Avian obligate brood parasites generally impose high fitness costs on their hosts, resulting in sophisticated coevolutionary arms races (Davies & Brooke 1989; Moksnes et al. 1990)....

    [...]

  • ...However, despite the apparent benefits of rejection, there is substantial variation both among and within host species used by cuckoos in their responses to foreign eggs (Davies & Brooke 1989; Moksnes et al. 1990; Martı́n-Gálvez et al. 2007; Stokke et al. 2008)....

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Journal ArticleDOI
TL;DR: It is shown that below a threshold of 19-41% parasitism, the warblers should accept mimetic cuckoo eggs because the costs of rejection outweigh the benefits, whereas above this threshold they should reject.
Abstract: Reed warblers sometimes make recognition errors when faced with a mimetic cuckoo egg in their nest and reject one or more of their own eggs rather than the foreign egg. Using the framework of signal detection theory, we analyse responses to model eggs to quantify the costs and benefits of acceptance versus rejection in parasitized and unparasitized nests. We show that below a threshold of 19-41% parasitism, the warblers should accept mimetic cuckoo eggs because the costs of rejection outweigh the benefits, whereas above this threshold they should reject. The warblers behaved as predicted; when they saw a cuckoo at their nest they usually showed rejection, but without the sight of the cuckoo they behaved appropriately for the average parasitism rate in Britain (6%) and tended to accept.

278 citations


"Evidence for egg discrimination pre..." refers background in this paper

  • ...Nevertheless, the underlying mechanisms of rejection decisions within and across the different host species are still poorly understood (Davies et al. 1996; Stokke et al. 2005)....

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  • ...Rejection costs involve recognition errors, accidental destruction of own eggs and/or simply energetic expenditure (Spaw & Rohwer 1987; Davies et al. 1996; Røskaft et al. 2002)....

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01 Jan 1998

191 citations


"Evidence for egg discrimination pre..." refers background in this paper

  • ...The most ubiquitous host antiparasite defence is egg discrimination and rejection, to which some parasites have responded by evolving mimetic eggs (Rothstein & Robinson 1998)....

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  • ...Selection should thus favour flexible host responses and hosts may recognize the foreign egg but choose to tolerate it under some circumstances (Rothstein & Robinson 1998)....

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  • ...However, even among cuckoo hosts, a higher level of phenotypic plasticity in rejection decisions is expected if ejection is costly and the risk of parasitism varies considerably (Rothstein & Robinson 1998; Lindholm 2000)....

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  • ...Possible explanations invoke a lack of necessary genetic variation underpinning egg discrimination, or discrimination developing with age/experience or having only evolved in some host populations sympatric with the brood parasite (Rothstein & Robinson 1998; Stokke et al. 2005; Røskaft et al. 2006)....

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Journal ArticleDOI
01 Apr 1991-The Auk
TL;DR: The puncture resistance hypothesis proposed to explain the adaptive value (or evolution) of strength in cowbird eggs is supported and has received support from Picman and Rohwer et al.
Abstract: --We studied the rejection behavior shown by different Norwegian cuckoo hosts towards artificial Common Cuckoo (Cuculus canorus) eggs. The hosts with the largest bills were grasp ejectors, those with medium-sized bills were mostly puncture ejectors, while those with the smallest bills generally deserted their nests when parasitized experimentally with an artificial egg. There were a few exceptions to this general rule. Because the Common Cuckoo and Brown-headed Cowbird (Molothrus ater) lay eggs that are similar in shape, volume, and eggshell thickness, and they parasitize nests of similarly sized host species, we support the puncture resistance hypothesis proposed to explain the adaptive value (or evolution) of strength in cowbird eggs. The primary assumption and prediction of this hypothesis are that some hosts have bills too small to grasp parasitic eggs and therefore must puncture-eject them, and that smaller hosts do not adopt ejection behavior because of the heavy cost involved in puncture-ejecting the thick-shelled parasitic egg. We compared our results with those for North American Brown-headed Cowbird hosts and we found a significantly higher proportion of rejecters among Common Cuckoo hosts with grasp indices (i.e. bill length x bill breadth) of <200 mm 2. Cuckoo hosts ejected parasitic eggs rather than accept hem as cowbird hosts did. Among the Common Cuckoo hosts, the cost of accepting a parasitic egg probably always exceeds that of rejection because cuckoo nestlings typically eject all host eggs or nestlings shortly after they hatch. Received 25 February 1990, accepted 23 October 1990. THE EGGS of many brood parasites have thicker shells than the eggs of other bird species of similar size (Lack 1968, Spaw and Rohwer 1987). Several hypotheses have been developed to explain this phenomenon, the most recent being that of Spaw and Rohwer (1987). Spaw and Rohwer (1987) and Rohwer and Spaw (1988) argued that the thick eggshell of the parasitic American cowbird (Molothrus) species has evolved so as to resist puncture ejection by small host species. They tested an assumption of this hypothesis by measuring the length and the width of the bill (the product of these two measurements they termed the \"grasp index\") of Brown-headed Cowbird (M. ater) hosts which had been classified as acceptors or rejecters. They concluded that some small-sized hosts are more or less forced to be acceptors because of heavy cost involved in getting rid of the thick-shelled Brown-headed Cowbird egg. This hypothesis has received support from Picman (1989) and Rohwer et al. (1989). Rothstein (1975, 1976, 1977) showed that, although many parasitized species accepted (or did not remove) introduced nonmimetic artificial eggs of Brown-headed Cowbirds, some species ejected them. He observed and inferred that these potential hosts ejected eggs from their 348 nests either by grasping the eggs or by puncturing the eggs before removal. Rohwer and Spaw (1988) used this distinction in ejection type when they considered the possibility of physical constraints to ejection for those species parasitized by Brown-headed Cowbirds. They compared the characteristic type of ejection (grasp or puncture) or lack of ejection response (acceptance) with the bill size for each of 40 parasitized passerine species. They suggest hat small bill size constrains some species from grasping the cowbird eggs for ejections, and that the strength of the cowbird eggs limits successful puncture ejections for most of these species. Rohwer and Spaw (1988) propose that the costs associated with these constraints have selected for acceptance. It is not clear from their indirect test which acceptor species are capable of successfully puncturing cowbird eggs for ejections (and would do so, given sufficient selective pressure) and which acceptor species cannot puncture the cowbird egg because the eggshell is too strong. So far only one host species of the North American Brown-headed Cowbird, the Northern Oriole (Icterus galbula), has been shown to be a true puncture ejector (Rothstein 1977). To test whether Northern Orioles experience any The Auk 108: 348-354. April 1991 April 1991] Parasite-Egg Rejection i Cuckoos 349 cost in puncture-ejecting the thick-shelled Brown-headed Cowbird egg, Rohwer et al. (1989) added Brown-headed Cowbird and control eggs into oriole nests, and found that the host species occasionally damaged some of its own eggs in the process of ejecting the cowbird

142 citations


"Evidence for egg discrimination pre..." refers background in this paper

  • ...…shells of parasitic eggs (Spaw & Rohwer 1987; Picman & Pribil 1997) may render rejection especially costly for smallbilled hosts that have to puncture the parasitic egg in order to remove it (puncture ejection) or desert the clutch (Moksnes et al. 1991; Røskaft et al. 1993; Antonov et al. 2006)....

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