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 visual signals, such as color and maculation, contributed to the recognition of foreign eggs by Oriental reed warblers as recognizable clues, but not the egg size, which had an impact on the type of egg rejection.
Abstract: Background Among potential hosts, the rejection of foreign eggs, which is a common and effective strategy to counter brood parasitism, depends on egg recognition. Multimodal and multicomponent recognition cues of brood parasitic eggs, which include both tactile (size, shape, and texture) and visual (size, shape, color, and maculation) cues, are potentially involved in the perception and discrimination of foreign eggs by hosts. An egg rejection experiment on the host with different types of model eggs can help to accurately assess the relative contribution of different components on egg recognition and constraints to rejection, in which videos can help identify the method of host rejection. Methods Here, we assessed egg recognition and rejection responses by Oriental reed warblers (Acrocephalus orientalis), one of the most common hosts of common cuckoos (Cuculus canorus) which breed in eastern China. We designed six groups of model eggs for rejection experiments in which sensory cues included three grades of size and two categories of visual mimicry. Results Our experiments confirmed that the multimodal traits, which included variation in size, were significant predictors of egg rejection: We detected significantly higher rejection rates of mimetic spotted model eggs than of nonmimetic blue eggs. However, large model eggs did not yield higher rejection rates and, instead, these were less likely to be rejected and more likely to be deserted compared with smaller eggs. Further video-recording data showed that there was no significant effect of egg size on the egg recognition rate (percentage of nests with evidence of egg pecking). No evidence that the egg appearance had an effect on the method of egg rejection (ejection or nest desertion) was found. Conclusions Only visual signals, such as color and maculation, contributed to the recognition of foreign eggs by Oriental reed warblers as recognizable clues, but not the egg size. The egg size had an impact on the type of egg rejection. It was less feasible for the warblers to eject large eggs and that is why they opted more often for desertion as the mean of model egg rejection. The significantly lower egg rejection rate of large eggs suggested that although some of them were recognized as foreign eggs, hosts failed to reject these eggs and finally the eggs were assumed to being accepted by the commonly used nest-checking methods.
5 citations
TL;DR: Analysis of the brood parasite system between the Asian emerald cuckoo Chrysococcyx maculatus and its host, the chestnut-crowned warbler, provides strong evidence supporting the theory that egg size recognition can be evolve in hosts as a specific anti-parasite adaptation against cuckoos.
Abstract: Abstract In the coevolutionary interactions between avian brood parasites and their hosts, egg recognition based on color and/or pattern is a common and effective defense to counter parasitism. However, for egg recognition based on size, only a few studies have found affirmative results, and they do not provide unambiguous evidence that egg size recognition in hosts has evolved as an important and specific anti-parasite adaptation against parasite eggs. We studied the brood parasite system between the Asian emerald cuckoo Chrysococcyx maculatus and its host, the chestnut-crowned warbler Phylloscopus castaniceps. The cuckoo parasitizes the warbler using non-mimetic and larger eggs at a parasitism rate of 12.9%. The warbler nests used in this experiment were built in a dark environment with the nest illuminance near 0 lux. Experiments with 2 types of model eggs with colors and patterns resembling cuckoo eggs of different sizes (cuckoo egg size or host egg size) showed that the warblers were able to reject 63.6% of cuckoo model eggs under these dim light conditions. However, model eggs with the same color and pattern similar to the warbler egg size were always accepted. This study provides strong evidence supporting the theory that egg size recognition can be evolved in hosts as a specific anti-parasite adaptation against cuckoos. We suggest that the egg size recognition of the warbler is an outcome of the tradeoff between the costs of violating the parental investment rule and suffering cuckoo parasitism.
5 citations
TL;DR: The results suggested that model eggs should be used with caution in comparative studies of egg recognition abilities among species or populations subjected to different intensities of brood parasitism, because model eggs may fail to accurately detect egg recognition in host populations with little to no risk of parasitism.
Abstract: Obligate brood parasites exert strong selective pressure on target hosts. In response, hosts typically evolve anti-parasitism strategies, of which egg recognition is one of the most efficient. Generally, host egg-recognition capacity is determined using model eggs. Previous studies have shown that some host species, which are capable of detecting parasite eggs, do not reject model eggs. However, it is unknown that whether the reaction to model eggs varies among distinct populations of the same host in relation to the degree of parasitism pressure. Here, we compared the rejection frequencies of model eggs and real eggs between mainland and island populations of the plain prinia (Prinia inornata), which are respectively sympatric and allopatric with their brood parasite, the common cuckoo (Cuculus canorus). Our results indicated that the mainland and island populations rejected real eggs at similar rates, but rejected model eggs, which were similar in size to real eggs but heavier, at significantly different rates: the island population rejected fewer model eggs, possibly because the rejection motivation of this population was lower due to absence of parasitism. Our results indicated that some factors affecting the decision to reject, such as rejection motivation, varied according to the degree of parasitism pressure, and thus influenced the frequency of egg rejection. Furthermore, our results suggested that model eggs should be used with caution in comparative studies of egg recognition abilities among species or populations subjected to different intensities of brood parasitism. That is, model eggs may fail to accurately detect egg recognition in host populations with little to no risk of parasitism.
5 citations
TL;DR: The results suggest that nest sanitation, which is an ancient behavior, is more fundamental than egg rejection, but the effect of the former on the latter is complex and needs further study.
Abstract: Egg rejection in birds is a specific adaptation toward avian brood parasitism, whereas nest sanitation is a general behavior for cleaning the nest and avoiding predation. However, both behaviors refer to the action of ejecting objects out of the nest, and nest sanitation has been proposed as a pre-adaptation for egg rejection. Here, we tested the eliciting effect of nest sanitation on egg rejection in the red-whiskered bulbul Pycnonotus jocosus, a potential host species that are sympatric with parasitic cuckoos. We conducted meta-analyses of previous studies on both nest sanitation and egg rejection, in order to evaluate the consistency of our conclusions. Our results showed that nest sanitation did not elicit egg rejection in P. jocosus. The conclusions concerning such an eliciting effect from previous studies were mixed, whereas the methodologies were inconsistent, making the studies unsuitable for comparisons. However, the ejection frequency of nest sanitation was consistently higher than the frequency of egg rejection across different host species or populations. These results suggest that nest sanitation, which is an ancient behavior, is more fundamental than egg rejection, but the effect of the former on the latter is complex and needs further study. Standardized methodologies and the integration of behavior, physiology, and modeling may provide better opportunities to explore the relationship between nest sanitation and egg rejection.
4 citations
TL;DR: It is found that egg recognition capacity is completely absent in this Asian population of tree sparrows, and this result contrasts with previous studies in European populations showing extensive ability for discriminating between own and foreign eggs.
4 citations
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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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