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

doi:10.1098/RSBL.2008.0645

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

Journal Article•DOI•

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

Anton Antonov¹, Bård G. Stokke¹, Arne Moksnes¹, Eivin Røskaft¹•Institutions (1)

Norwegian University of Science and Technology¹

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.

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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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Book Chapter•DOI•

Factors Affecting the Rates of Coevolution Between Obligate Avian Brood Parasites and Their Hosts

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Virginia E. Abernathy¹, Naomi E. Langmore¹•Institutions (1)

Australian National University¹

01 Jan 2017

TL;DR: Factors influencing the rate of coevolution between avian obligate brood parasites and their hosts are reviewed and evidence from brood parasite coev evolution studies concurs with other developments in evolutionary biology more broadly, which indicates that evolution can be a more rapid process than previously recognized and can proceed on a timescale similar to that of ecological dynamics.

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Abstract: Coevolution is a process in which two species, populations, or groups of individuals evolve reciprocal adaptations through their interactions with one another. Obligate avian brood parasitism is a model example of coevolution, and several reviews have discussed the different types of adaptations and counter-adaptations hosts and brood parasites evolve. However, there has been less focus on the rate at which this process proceeds. Here we review factors influencing the rate of coevolution between avian obligate brood parasites and their hosts. We also suggest that evidence from brood parasite coevolution studies concurs with other developments in evolutionary biology more broadly, which indicates that evolution can be a more rapid process than previously recognized and can proceed on a timescale similar to that of ecological dynamics. Finally, we discuss the difficulties of studying rates of coevolution in bird populations empirically and mention current studies that are resolving this problem by focusing on recently parasitized host populations. Understanding how rapidly hosts can evolve defenses to circumvent brood parasitism is an important step in uncovering aspects of speciation, determining which traits are actually indicative of true genetic change, and can aid in conservation decisions of endangered potential hosts, especially as brood parasites expand their breeding ranges with rising global temperatures and other environmental changes.

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1 citations

Journal Article•DOI•

Egg Size as the Main Stimulus to Discriminatory Behavior of the Yellow-Browed Warbler ( Phylloscopus inornatus , Phylloscopidae) under Brood Parasitism of the Oriental Cuckoo ( Cuculus optatus , Cuculidae)

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S. G. Meshcheryagina¹, G. N. Bachurin, O. V. Bourski¹, M. G. Golovatin¹•Institutions (1)

Russian Academy of Sciences¹

01 Dec 2020-Biology Bulletin

TL;DR: In this article, the authors investigated the behavior of the host concerning egg discrimination in three geographic populations of the Yellow-browed Warbler with different levels of brood parasitism of the Oriental Cuckoo.

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Abstract: Experimental studies were carried out on the behavior of the host concerning egg discrimination in three geographic populations of the Yellow-browed Warbler with different levels of brood parasitism of the Oriental Cuckoo. The absence of a spotted pattern on the shell of foreign eggs was shown to fail to serve as a stimulus to recognition. The acceptance or rejection of a foreign egg is determined by the ratio of the parasite to the host egg breadth, the mean size of the eggs in the individual host clutch also being of importance. This suggests that the recognition of parasite eggs by the host is based on the tactile contact of the female with the uneven surface of the clutch. The mean breadth of the Oriental Cuckoo eggs introduced into Yellow-browed Warbler nests is significantly smaller than the value at which the probability of egg rejection is equal to the probability of acceptance. As it is also smaller than in other gentes, this shows the adaptation of the brood parasite to this particular host. The acceptance of a foreign egg, ejection of it from the nest, and clutch desertion represent three stages of the same reaction in response to variation in a quantitative stimulus.

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1 citations

Perception, Cognition, and Response:A Recognition Systems Analysis of Avian Egg Rejection

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Mark E Hauber

01 Jan 2011

TL;DR: A structured experimental analysis of each of the recognition system’s components; perception, cognition, and response; in the context of avian brood parasitism is provided, which suggests that foreign egg colours are perceived similarly and rejection is triggered through comparisons with internal filters, or recognition templates, even when hosts’ own eggs are not present.

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

...…cues, and the behavioural responses (if any) to the egg, including the cases when hosts recognize the foreign eggs but are unable to pierce or grasp, or decide not to reject them (Antonov et al., 2009; Davies et al., 1996; Hauber & Sherman, 2001; Moskát & Hauber, 2007; Spottiswoode, 2010)....
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...D.2., see above), the new results reveal that the lack of behavioural responses to foreign eggs cannot be considered as necessarily being due to cognitive limitations of host birds (Antonov et al., 2009; Moskát & Hauber, 2007)....
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...…Stoddard & Stevens, 2010, 2011), while others used video-observations on duration of inspection, latency to reject, and patterns of egg-pecking to reveal that discrimination can take place before or in the absence of egg rejection (Antonov et al., 2009; Honza et al., 2007; Soler et al., 2002)....
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...  15  the eggshell, the cognitive algorithms involved in recognizing and generating a response to perceived cues, and the behavioural responses (if any) to the egg, including the cases when hosts recognize the foreign eggs but are unable to pierce or grasp, or decide not to reject them (Antonov et al., 2009; Davies et al., 1996; Hauber & Sherman, 2001; Moskát & Hauber, 2007; Spottiswoode, 2010)....
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...2007), with their thicker eggshells making it more difficult or even impossible to puncture and eject (Antonov et al., 2009)....
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Journal Article•DOI•

騙しを見破るテクニック：卵の基準，雛の基準

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田中啓太

20 Apr 2012-Japanese Journal of Ornithology

1 citations

Journal Article•DOI•

Brood parasitism risk drives birds to breed near humans

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Jinggang Zhang, Peter Santema, Jianqiang Li, Wen-hong Deng, Bart Kempenaers - Show less +1 more

01 Feb 2023-Current Biology

TL;DR: In this paper , the authors used a combination of field observations and experimental manipulations to show that Daurian redstarts, Phoenicurus auroreus, a common host of the common cuckoo, Cuculus canorus, nest in proximity to humans to avoid brood parasitism.

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Journal Article•DOI•

An experimental study of co-evolution between the cuckoo, cuculus canorus, and its hosts. ii. host egg markings, chick discrimination and general discussion

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Nicholas B. Davies, M. de L. Brooke

01 Feb 1989-Journal of Animal Ecology

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.

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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

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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 Article•DOI•

Behavioural Responses of Potential Hosts Towards Artificial Cuckoo Eggs and Dummies

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Eivin R∅Skaft¹, Lars Korsnes¹, Hans Chr. Pedersen, Arne Moksnes¹, Anders T. Braa¹, Helene M. Lampe¹ - Show less +2 more•Institutions (1)

Norwegian University of Science and Technology¹

01 Jan 1991-Behaviour

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.

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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.

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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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Journal Article•DOI•

Recognition Errors and Probability of Parasitism Determine Whether Reed Warblers Should Accept or Reject Mimetic Cuckoo Eggs

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Nicholas B. Davies¹, M. de L. Brooke¹, Alejandro Kacelnik²•Institutions (2)

University of Cambridge¹, University of Oxford²

22 Jul 1996-Proceedings of The Royal Society B: Biological Sciences

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.

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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.

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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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Parasitic birds and their hosts

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Stephen I. Rothstein, Scott K. Robinson

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 Article•DOI•

Rejection Behavior by Common Cuckoo Hosts Towards Artificial Brood Parasite Eggs

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Arne Moksnes¹, Eivin Røskaft¹, Anders T. Braa¹•Institutions (1)

Norwegian University of Science and Technology¹

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.

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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

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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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