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.
Citations
More filters
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.
205 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)....
[...]
...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)....
[...]
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.
178 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....
[...]
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.
151 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)....
[...]
...2009b) and thickened eggshells (Brooker & Brooker 1991; Antonov et al. 2009)....
[...]
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.
86 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…...
[...]
TL;DR: Hosts can rely on comparisons of foreign egg colors against an internal recognition template of acceptable (own) egg phenotypes to reject foreign eggs, suggesting a role for discordancy and/or online self-referent phenotype matching.
Abstract: Many hosts have evolved diverse cognitive mechanisms to recognize and reduce the cost of social parasitism. For example, great reed warblers Acrocephalus arundinaceus can accurately reject closely mimetic eggs of brood parasitic common cuckoos Cuculus canorus. Yet, these same hosts are less effective at identifying and rejecting parasitism when the clutch is parasitized by multiple cuckoo eggs, suggesting a role for discordancy (the rejection of the egg type in the minority of the clutch) and/or online self-referent phenotype matching (the simultaneous viewing of cuckoo and own eggs in the nest) to reject foreign eggs. We tested whether the presence of host’s own eggs is required for the discrimination of foreign eggs by dyeing hosts’ own eggs with one of several colors so that clutches contained (a) 1 dyed and 4 unmanipulated eggs, (b) 3 dyed and 2 unmanipulated eggs, or 5 eggs dyed either (c1) differently or (c2) similarly. Rejection rates of dyed eggs varied widely between different colors and were highest in treatment (a), with 1 dyed egg, compared with treatments with the majority (b) or all (c1 and c2) dyed eggs. However, relative rejection rates of dyed eggs were also consistent among specific colors across treatments, including (c1) and (c2), where no unmanipulated own eggs were available for viewing and irrespective of whether eggs were dyed all different colors (c1) or the same colors (c2). We conclude that these hosts can rely on comparisons of foreign egg colors against an internal recognition template of acceptable (own) egg phenotypes.
58 citations
References
More filters
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)....
[...]
...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)....
[...]
TL;DR: The results of this study lend support to the hypothesis that the differences in the degree of responses by the host species towards parasitism by the cuckoo reflect different stages in a continuous coevolutionary arms race with cuckoos.
Abstract: Responses of 33 potential host species towards a non-mimetic, dummy, cuckoo egg placed in their nest were tested (N = 372). For 22 of these species, their behavioural responses towards a dummy cuckoo placed near their nest were also tested (N = 193). The species were grouped in A) most common hosts: species which at the moment are losing out in the coevolutionary arms race with the cuckoo and which today represent favorite hosts; B) frequently-used hosts: species which at the moment are assumed to be true cuckoo hosts, but which are not so commonly used as those in group A; C) rarely-used hosts: species which would appear to be suitable hosts, but which despite of this, are rarely used. These species are assumed to be ahead of the cuckoo in the coevolutionary arms race; D) unsuitable hosts: species with a breeding biology which either prevents, or counteracts, cuckoo parasitism. They are therefore assumed never to have been engaged in a coevolutionary arms race with the cuckoo. In the most common hosts the median acceptance rate of the non-mimetic egg was 86 % , in the frequently-used hosts 33 % , in the rarely-used hosts 10 % and in the unsuitable hosts 100 %. In the most common hosts the median rate of aggression shown towards the cuckoo dummy was 50%, but the most numerous species in this group, the meadow pipit, showed aggressive behaviour in 60% of the cases. The median aggression rate both in the frequently-used hosts and the rare hosts was 100 % and in the unsuitable hosts 0%. The bluethroat was the only species which accepted the non-mimetic dummy egg at a higher rate later on during the incubation period than during earlier stages. A positive correlation was found between the power of egg discrimination and the rate of aggression shown towards the dummy cuckoo. Such aggression was stronger when both parents were present at the nest than when only one parent was present. The results of this study lend support to the hypothesis that the differences in the degree of responses by the host species towards parasitism by the cuckoo reflect different stages in a continuous coevolutionary arms race with cuckoos.
291 citations
"Evidence for egg discrimination pre..." refers background in this paper
...Avian obligate brood parasites generally impose high fitness costs on their hosts, resulting in sophisticated coevolutionary arms races (Davies & Brooke 1989; Moksnes et al. 1990)....
[...]
...However, despite the apparent benefits of rejection, there is substantial variation both among and within host species used by cuckoos in their responses to foreign eggs (Davies & Brooke 1989; Moksnes et al. 1990; Martı́n-Gálvez et al. 2007; Stokke et al. 2008)....
[...]
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)....
[...]
...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)....
[...]
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)....
[...]
...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)....
[...]
...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)....
[...]
...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)....
[...]
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)....
[...]