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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.

AbstractGiven 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.

Topics: Cuckoo (67%), Common cuckoo (65%), Brood parasite (62%), Cuculus (56%)

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Citations
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Journal ArticleDOI
TL;DR: The twin hurdles of effective trickery in the face of evolving host defences and difficulties of tuning into another species' life history may together explain why obligate brood parasitism is relatively rare.
Abstract: I suggest that the cuckoo's parasitic adaptations are of two kinds: ‘trickery’, which is how adult cuckoos and cuckoo eggs and chicks evade host defences, and involves adaptations that have co-evolved with host counter-adaptations, and ‘tuning’, which is how, once accepted, cuckoo egg and chick development are then attuned to host incubation and provisioning strategies, and which might not always provoke co-evolution. Cuckoo trickery involves adaptations to counter successive lines of host defence and includes: tricks for gaining access to host nests, egg trickery and chick trickery. In some cases, particular stages of host defences, and hence their corresponding cuckoo tricks, are absent. I discuss three hypotheses for this curious mixture of exquisite adaptation and apparent lack of adaptation: different defences best for different hosts, strategy blocking and time for evolution of defence portfolios. Cuckoo tuning includes adaptations involving: host choice and monitoring of host nests, efficient incubation of the cuckoo egg, efficient provisioning and protection of the cuckoo chick, and adaptations to avoid misimprinting on the wrong species. The twin hurdles of effective trickery in the face of evolving host defences and difficulties of tuning into another species' life history may together explain why obligate brood parasitism is relatively rare.

181 citations


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

  • ...They may decide to accept if cuckoo eggs are difficult to distinguish with certainty (Antonov et al., 2009) or if acceptance is not too costly, because the cuckoo egg is often laid too late, or some host young can be raised alongside a cuckoo chick (Krüger, 2011)....

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  • ...They may decide to accept if cuckoo eggs are difficult to distinguish with certainty (Antonov et al., 2009) or if acceptance is not too costly, because the cuckoo egg is often laid too late, or some host young can be raised alongside a cuckoo chick (Krüger, 2011)....

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Journal ArticleDOI
TL;DR: An adaptive explanation of co‐evolution between brood parasites and their hosts is proposed, which centres on the relative strength of two opposing processes: strategy‐facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy‐blocking, which may relax selection on another so completely that it causes it to decay.
Abstract: Avian parents and social insect colonies are victimized by interspecific brood parasites-cheats that procure costly care for their dependent offspring by leaving them in another species' nursery. Birds and insects defend themselves from attack by brood parasites; their defences in turn select counter-strategies in the parasite, thus setting in motion antagonistic co-evolution between the two parties. Despite their considerable taxonomic disparity, here we show striking parallels in the way that co-evolution between brood parasites and their hosts proceeds in insects and birds. First, we identify five types of co-evolutionary arms race from the empirical literature, which are common to both systems. These are: (a) directional co-evolution of weaponry and armoury; (b) furtiveness in the parasite countered by strategies in the host to expose the parasite; (c) specialist parasites mimicking hosts who escape by diversifying their genetic signatures; (d) generalist parasites mimicking hosts who escape by favouring signatures that force specialization in the parasite; and (e) parasites using crypsis to evade recognition by hosts who then simplify their signatures to make the parasite more detectable. Arms races a and c are well characterized in the theoretical literature on co-evolution, but the other types have received little or no formal theoretical attention. Empirical work suggests that hosts are doomed to lose arms races b and e to the parasite, in the sense that parasites typically evade host defences and successfully parasitize the nest. Nevertheless hosts may win when the co-evolutionary trajectory follows arms race a, c or d. Next, we show that there are four common outcomes of the co-evolutionary arms race for hosts. These are: (1) successful resistance; (2) the evolution of defence portfolios (or multiple lines of resistance); (3) acceptance of the parasite; and (4) tolerance of the parasite. The particular outcome is not determined by the type of preceding arms race but depends more on whether hosts or parasites control the co-evolutionary trajectory: tolerance is an outcome that parasites inflict on hosts, whereas the other three outcomes are more dependent on properties intrinsic to the host species. Finally, our review highlights considerable interspecific variation in the complexity and depth of host defence portfolios. Whether this variation is adaptive or merely reflects evolutionary lag is unclear. We propose an adaptive explanation, which centres on the relative strength of two opposing processes: strategy-facilitation, in which one line of host defence promotes the evolution of another form of resistance, and strategy-blocking, in which one line of defence may relax selection on another so completely that it causes it to decay. We suggest that when strategy-facilitation outweighs strategy-blocking, hosts will possess complex defence portfolios and we identify selective conditions in which this is likely to be the case.

168 citations


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

  • ...The largest hosts can potentially reject a parasitic egg by grasping the whole egg within their bill, but this is impossible for smaller hosts (Antonov et al., 2009; Spaw & Rohwer, 1987) who constitute the majority of avian brood parasite victims....

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Journal ArticleDOI
TL;DR: The incorporation of frontline interactions in empirical and theoretical investigations of brood parasite–host arms races are advocated to provide a more holistic understanding of the coevolutionary processes in these systems.
Abstract: The interactions between avian interspecific brood parasites and their hosts provide tractable and informative systems for investigating coevolution. Generally, these investigations have emphasized the egg and chick stages of the coevolutionary arms race; however, recent studies demonstrate that coevolution operates at all stages of the host nesting cycle and emphasize the importance of reciprocal adaptations prior to deposition of the parasite egg in the host nest: the ‘frontline’ of the arms race. Here we review the diversity of adaptations at the frontline and its implications for our understanding of brood parasite–host relationships. Coevolution at the frontline can fundamentally shape the life histories, morphologies, physiologies and behaviours of both brood parasites and their hosts, and influences the trajectories and outcomes of their subsequent coevolutionary interactions. We advocate the incorporation of frontline interactions in empirical and theoretical investigations of brood parasite–host arms races to provide a more holistic understanding of the coevolutionary processes in these systems.

135 citations


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

  • ...In response, brood parasites have evolved counteradaptations including mimicry of host eggs (Avilés et al. 2010; Spottiswoode & Stevens 2010; Stoddard & Stevens 2010), cryptic eggs (Marchant 1972; Langmore et al. 2009b) and thickened eggshells (Brooker & Brooker 1991; Antonov et al. 2009)....

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  • ...2009b) and thickened eggshells (Brooker & Brooker 1991; Antonov et al. 2009)....

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Journal ArticleDOI
TL;DR: Hosts rejected their own eggs and manipulated (‘parasitic’) eggs above control levels in experiments when manipulated eggs were in the majority but when clutches also included a minority of own eggs, supporting a mechanism of template-based egg discrimination.
Abstract: Many avian hosts have evolved antiparasite defence mechanisms, including egg rejection, to reduce the costs of brood parasitism. The two main alternative cognitive mechanisms of egg discrimination are thought to be based on the perceived discordancy of eggs in a clutch or the use of recognition templates by hosts. Our experiments reveal that the great reed warbler (Acrocephalus arundinaceus), a host of the common cuckoo (Cuculus canorus), relies on both mechanisms. In support of the discordancy mechanism, hosts rejected their own eggs (13%) and manipulated ('parasitic') eggs (27%) above control levels in experiments when manipulated eggs were in the majority but when clutches also included a minority of own eggs. Hosts that had the chance to observe the manipulated eggs daily just after laying did not show stronger rejection of manipulated eggs than when the eggs were manipulated at clutch completion. When clutches contained only manipulated eggs, in 33% of the nests hosts showed rejection, also supporting a mechanism of template-based egg discrimination. Rejection using a recognition template might be more advantageous because discordancy-based egg discrimination is increasingly error prone with higher rates of multiple parasitism.

79 citations


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

  • ...…not always allow distinction between predictions and outcomes of the discordancy versus the template recognition mechanisms (Moskát et al., 2008c; Antonov et al., 2009), contemporary experiments are required that specifically aim to contrast the predictions of these alternative cognitive models…...

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Journal ArticleDOI
TL;DR: It is found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies, and the cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.
Abstract: Brood parasitism imposes several fitness costs on the host species. To reduce these costs, hosts of avian brood parasites have evolved various defenses, of which egg rejection is the most prevalent. In the face of variable host-parasite mimicry and the costs of egg discrimination itself, many hosts reject only some foreign eggs. Here, we experimentally varied the recognition cues to study the underlying cognitive mechanisms used by the Chalk-browed Mockingbird (Mimus saturninus) to reject the white immaculate eggs laid by the parasitic Shiny Cowbird (Molothrus bonariensis). Immaculate eggs are the only parasite eggs rejected by this host, as it accepts all polymorphic, spotted eggs laid by cowbirds. Using a within-breeding pair experimental design, we tested for the salience of spotting, UV reflectance, and brightness in eliciting rejection. We found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies. The cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.

51 citations


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

  • ...Mockingbirds do not have physical constraints of gape and beak size for grasping and ejecting cowbird eggs, which sometimes is the case in smaller hosts (Antonov et al. 2009)....

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  • ...multi-cue decision-making process might be also influenced by a perceptual polymorphism and/or cognitive variance in acceptance thresholds between individuals which results in the rejection of fewer eggs than those which are recognized as distinctly foreign (Antonov et al. 2009; Moskát and Hauber 2007)....

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  • ...…decision-making process might be also influenced by a perceptual polymorphism and/or cognitive variance in acceptance thresholds between individuals which results in the rejection of fewer eggs than those which are recognized as distinctly foreign (Antonov et al. 2009; Moskát and Hauber 2007)....

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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

363 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)....

    [...]

  • ...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.

285 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)....

    [...]


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.

270 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

190 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

136 citations


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

  • ...Furthermore, because rejection may be costly, some hosts also Received 6 November 2008 Accepted 2 December 2008 169 modify their rejection decisions according to the perceived risk of parasitism (Moksnes et al. 1993; Lindholm 2000; Soler et al. 2000)....

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  • ...Video recordings showing strong pecking followed by desertion demonstrated that at least some of the desertions represent a failure at puncture ejection rather than nest abandonment in the first place (cf. Moksnes et al. 1993)....

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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)....

    [...]