Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host
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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TL;DR: Only female behavior toward the foreign egg proved to have a significant effect on the timing of egg ejection, and this results in the context of known intra- and interspecific differences in host response times toward alien eggs and cognitive mechanisms involved in host egg discrimination processes.
Abstract: The prevalent, and so far most explored, host defense against brood parasitism is egg discrimination. Not only do the hosts differ markedly in their propensity to reject parasitic eggs but rejecters even vary in their egg rejection times. The focus of the present study was to investigate factors potentially responsible for high variation in timing of host egg rejection. As a model species, we chose the great reed warbler Acrocephalus arundinaceus, a cuckoo Cuculus canorus host, with female-restricted egg ejection behavior. We presented a cuckoo dummy near host nests and experimentally parasitized the clutches with a nonmimetic egg. Immediately afterward, we continuously video recorded host behavior to determine egg ejection times accurately. We fitted a regression tree model with the timing of egg ejection as a dependent variable and female-related characteristics (body condition, eggshell coloration, and behavior) as explanatory variables. Only female behavior toward the foreign egg proved to have a significant effect on the timing of egg ejection. Females devoting more time to clutch inspection ejected the egg significantly more quickly than females inspecting their experimentally parasitized clutches only briefly. We discuss our results in the context of known intra- and interspecific differences in host response times toward alien eggs and cognitive mechanisms involved in host egg discrimination processes. Key words: Acrocephalus arundinaceus, brood parasitism, egg discrimination, egg ejection time, great reed warbler, nest inspection. [Behav Ecol]
24 citations
Cites background from "Evidence for egg discrimination pre..."
...Few authors, however, have considered the perception component of this behavior (see above), for example, through detailed monitoring of hosts immediately after parasitism (Sealy and Neudorf 1995; Soler et al. 2002; Honza et al. 2005, 2007; Antonov et al. 2008, 2009)....
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...Although egg pecking has been used as an indication of egg recognition (Antonov et al. 2008, 2009), more attention should be paid also to clutch inspection, during which egg recognition processes take place....
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TL;DR: This is the first report of a passerine bird using its feet to remove objects from the nest, and it is revealed that the Neotropical baywing, a host of the screaming cowbird and shiny cowbird, instead circumvents such constraints by kicking parasite eggs out of the nest.
Abstract: The hosts of brood parasitic birds are under strong selection pressure to recognize and remove foreign eggs from their nests, but parasite eggs may be too large to be grasped whole and too strong to be readily pierced by the host's bill. Such operating constraints on egg removal are proposed to force some hosts to accept parasite eggs, as the costs of deserting parasitized clutches can outweigh the cost of rearing parasites. By fitting microcameras inside nests, we reveal that the Neotropical baywing (Agelaioides badius), a host of the screaming cowbird (Molothrus rufoaxillaris) and shiny cowbird (Molothrus bonariensis), instead circumvents such constraints by kicking parasite eggs out of the nest. To our knowledge, this is the first report of a passerine bird using its feet to remove objects from the nest. Kick-ejection was an all-or-nothing response. Baywings kick-ejected parasite eggs laid before their own first egg and, if heavily parasitized, they ejected entire clutches and began again in the same nest. Few baywings were able to rid their nests of every parasite egg, but their novel ejection method allowed them to reduce the median parasitism intensity by 75 per cent (from four to one cowbird eggs per nest), providing an effective anti-parasite defence.
24 citations
Cites background from "Evidence for egg discrimination pre..."
...Similarly, puncture-ejection is impeded when the parasite egg’s shell is too tough to pierce [5,6]....
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TL;DR: The results considered together support the IBP hypothesis, indicating that recognition and rejection of parasitic eggs in blackbirds have probably evolved due to previous cuckoo parasitism, resulting in a successful resistance against interspecific brood parasitism.
Abstract: Traditional theory assumes that egg recognition and rejection abilities arise as a response against interspecific brood parasitism (IBP). However, rejection also appears in some species that are currently not exploited by interspecific parasites, such as Turdus thrushes. Recent evidences suggest that rejection abilities evolved in these species as a response to conspecific brood parasitism (CBP). To test these two alternative hypotheses, we performed an experimental study by parasitizing nests of the common blackbird (Turdus merula) with conspecifics or heterospecific eggs under different risk of parasitism (presence of interspecific or conspecific parasites near the nest). Common blackbird is a potential host of the common cuckoo (Cuculus canorus) but suffers low levels of CBP too. We found that blackbirds were able to recognize and eject heterospecific eggs at high rates whereas most of conspecifics eggs were not recognized and, therefore, accepted. Ejection rates of conspecific eggs did not exceed 13 %, even in situations of high risk of CBP (blackbird female placed near the nest), which contradict the main prediction derived from the CBP hypothesis. Conversely, ejection rates of experimental eggs simulating IBP were much higher (80–100 %). Furthermore, female blackbirds were more aggressive towards cuckoos than towards blackbird dummies. Our results considered together support the IBP hypothesis, indicating that recognition and rejection of parasitic eggs in blackbirds have probably evolved due to previous cuckoo parasitism. The current absence of IBP in blackbirds may be due to the highly efficient rejection abilities in this species. Thus, these abilities have been retained in absence of brood parasitism as a consequence of the low costs involved for blackbirds, resulting in a successful resistance against interspecific brood parasitism.
24 citations
Cites background from "Evidence for egg discrimination pre..."
...However, since recognition is not always followed by rejection of the parasitic egg [35, 38, 40, 42, 53], it is necessary to conduct experimental studies that provide information on both rejection and discrimination abilities....
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TL;DR: There is some support for the hypothesis that brood parasitism may select for high inter-clutch variation in eggshell colour to facilitate egg recognition and for the blackmail hypothesis, which suggests that females lay colourful eggshells to coerce males into providing additional care during incubation.
Abstract: The colourful surface of birds’ eggshells varies dramatically between species, but the selective pressures driving this variation remain poorly understood. We used a large comparative dataset to test several hypotheses proposed to explain the evolution of eggshell colouration. We tested the hypothesis that predation pressure might select for cryptic eggshells by examining the relationship between predation rate and egg colouration. We found that predation rates were positively related to eggshell brightness. The blackmail hypothesis suggests that females lay colourful eggshells to coerce males into providing additional care during incubation to keep colourful eggs covered. According to this hypothesis, conspicuous eggs should be found in situations with high risk of visual detection from predators or brood parasites. In support of this hypothesis, proportional blue-green chroma was positively related to parasitism risk, and eggs with higher proportional blue-green chroma or higher ultraviolet chroma received higher combined parental nest attendance during the incubation period. The sexual signalling hypothesis states that blue-green colour indicates female quality; however, we did not find that blue-green eggshell colour was greater in species where males participate in any form of parental care, and relative male provisioning was unrelated to blue-green eggshell chroma. We found some support for the hypothesis that brood parasitism may select for high inter-clutch variation in eggshell colour to facilitate egg recognition. In our dataset, parasitism risk was negatively related to inter-clutch repeatability of blue-green chroma. Our study highlights the diversity of selection pressures acting on the evolution of eggshell colour in birds and provides suggestions for novel areas of future key research direction.
24 citations
Cites background from "Evidence for egg discrimination pre..."
...…parasitism is an evolutionary viable strategy, although host anti-parasitic behaviours may be limited by both the visibility of eggshells within the nest and the host’s ability to reject the eggs or otherwise modify the nesting attempt (Davies 2000; Langmore et al. 2005; Antonov et al. 2009)....
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...is an evolutionary viable strategy, although host anti-parasitic behaviours may be limited by both the visibility of eggshells within the nest and the host’s ability to reject the eggs or otherwise modify the nesting attempt (Davies 2000; Langmore et al. 2005; Antonov et al. 2009)....
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TL;DR: The results corroborate the hypothesis that the different egg poles have different signal salience and may have implications for the evolution of diversity of not only egg coloration but also of egg shape in the arms race between hosts and brood parasitic birds.
Abstract: The size, patterning and coloration of bird eggs may signal different information content to nest owners, mates, predators, hosts, or brood parasites. Recent studies suggested that the pigmentation at one pole of the typically asymmetrical avian egg plays a critical role in the discrimination of own and foreign eggs by several host species parasitized by the common cuckoo (Cuculus canorus). Typically, both eggshell maculation and background colour are more consistent on the blunt pole, and hosts react more strongly to experimental changes in coloration of the blunt pole compared to the sharp pole. However, it remains unclear whether the asymmetrical shape of natural eggs per se enhances the behavioural responses of hosts to foreign eggs. To evaluate the salience of asymmetrical egg shape, we studied reactions of a rejecter cuckoo host, the great reed warbler (Acrocephalus arundinaceus), to artificial shapes of model eggs painted a non-mimetic blue colour. Artificial eggs with two blunt poles were rejected significantly more often than those with a single blunt pole or two sharp poles. These results corroborate the hypothesis that the different egg poles have different signal salience and may have implications for the evolution of diversity of not only egg coloration but also of egg shape in the arms race between hosts and brood parasitic birds.
23 citations
Cites methods from "Evidence for egg discrimination pre..."
...All three types of artificial eggs were made out of thermoset plasticine (‘Creal-therm Professional’ Modelling Material, following the protocol of Bártol et al., 2002 and Antonov et al., 2009 with a polystyrene kernel, painted dark blue with acrylic paint (PANTONE code 300C)....
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References
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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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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)....
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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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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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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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