Social Transmission of a Host Defense Against Cuckoo Parasitism (original) (raw)
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Direct and indirect assessment of parasitism risk by a cuckoo host
When the risk of encountering enemies varies in space or in time, this may select for plasticity of costly defenses. Hosts are known to vary both mobbing of adult cuckoos and egg rejection with spatiotemporal variation in brood parasitism, but it is unclear what parasitism cues they use to guide their defense plasticity. There is evidence that hosts use cuckoo activity near their nests as a direct cue, but cuckoos are secretive and resemble dangerous birds of prey so hosts may use indirect environmental predictors of parasitism too, such as their nest’s proximity to potential cuckoo lookout perches. Here, we compared reed warbler Acrocephalus scirpaceus nest defense responses with models of various enemies at a parasitized site and at a site where no common cuckoos Cuculus canorus were present. Reed warblers approached model cuckoos less closely and mobbed them less at the unparasitized site. However, at both sites, the warblers reduced their mobbing in a similar manner with increasing distance to the nearest potential cuckoo perch. The variation in response was specific to cuckoos and was not shown to harmless controls. Thus, hosts use both direct (cuckoo presence) and indirect cues (perch distance) of parasitism risk for modulating their costly defenses against their secretive parasite. We suggest that reciprocal selection for detection and suppression of direct and indirect cues provides a unifying feature of cuckoo–host arms races.
Testing for correlations between behaviours in a cuckoo host: why do host defences not covary?
Animal Behaviour, 2014
Fitness costs associated with brood parasitism have led host species to evolve several lines of defence. The first two lines of defence, aggression against adult parasites and egg rejection, are present at varying levels in almost all hosts. However, it remains unclear how these two fundamental defences covary at host individual level, with previous studies suggesting both positive and negative correlations. A theoretically critical yet empirically untested scenario is that variation in host antiparasite behaviour may relate to individual variation in host behavioural types or personalities. Here we examined whether host aggression against adult brood parasites and egg rejection behaviour were correlated with host behaviours displayed outside the context of brood parasitism. We selected the great reed warbler, Acrocephalus arundinaceus, a favourite cuckoo, Cuculus canorus, host as a suitable model. Only females reject foreign eggs and show high individual repeatability of both aggression towards cuckoos and nest guarding. We found that female behaviours in different situations (nest guarding, nest defence, handling in the net) were strongly correlated with each other. This is the first empirical evidence on correlation between individually consistent antiparasite adaptation (female nest defence) and behaviours that are not directly related to brood parasitism. In contrast, egg rejection/acceptance responses and latency to these responses did not correlate with any of the female defence/guarding behaviours and behaviour during handling. Proximately, this may be because nest defence and egg recognition represent cognitively and behaviourally completely different tasks. These patterns were not affected by female mating status in this polygynous cuckoo host. We hypothesize that differences in host behavioural types, rather than host egg discrimination ability, may predict host nest defence behaviour against adult brood parasites in general. Ó
Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes
Biological Reviews
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...
Strategic Variation in Mobbing as a Front Line of Defense against Brood Parasitism
Current Biology
Coevolutionary arms races, where adaptations in one party select for counter-adaptations in another and vice versa, are fundamental to interactions between organisms and their predators, pathogens, and parasites [1]. Avian brood parasites and their hosts have emerged as model systems for studying such reciprocal coevolutionary processes [2] and [3]. For example, hosts have evolved changes in egg appearance and rejection of foreign eggs in response to brood parasitism from cuckoos, and cuckoos have evolved host-egg mimicry as a counter-response [4], [5] and [6]. However, the host's front line of defense is protecting the nest from being parasitized in the first place [7], [8], [9] and [10], yet little is known about the effectiveness of nest defense as an antiparasite adaptation, and its coevolutionary significance remains poorly understood [10]. Here we show first that mobbing of common cuckoos Cuculus canorus by reed warblers Acrocephalus scirpaceus is an effective defense against parasitism. Second, mobbing of cuckoos is a phenotypically plastic trait that is modified strategically according to local parasitism risk. This supports the view that hosts use a “defense in-depth strategy,” with successive flexible lines of defense that coevolve with corresponding offensive lines of the parasite. This highlights the need for more holistic research into the coevolutionary consequences when multiple adaptations and counter-adaptations evolve in concert [11].
A parasite in wolf's clothing: hawk mimicry reduces mobbing of cuckoos by hosts
The reciprocal interactions between brood parasites and their hosts provide models for studying coevolution. For example, where hosts have evolved egg or chick discrimination, brood parasites have evolved mimicry of host eggs or chicks. Here, we suggest that there is another form of mimicry by cuckoos. A previous study has shown that naive small birds, with no evolutionary history of brood parasitism, are as afraid of adult common cuckoos Cuculus canorus as of sparrowhawks Accipiter nisus because of their physical resemblance. However, it has yet to be shown whether host species regard cuckoos as hawk like, or how hawk resemblance might benefit the cuckoo. We provide the first evidence that hawk resemblance involving barred underparts is an adaptive brood parasitic trait. We show by plumage manipulations of taxidermic models that reed warbler (Acrocephalus scirpaceus) hosts are more reluctant to approach and mob common cuckoos with barred rather than unbarred underparts. Our results indicate that reed warblers are more aggressive toward cuckoos that appear less hawk like and that hence, hawk resemblance facilitates access to host nests. Therefore, we suggest that cuckoos employ 2 forms of mimicry: To enhance parasitic laying, cuckoo adults are Batesian mimics of hawks, appearing dangerous to adult host survival, when in fact they could be safely attacked. At later stages, cuckoo eggs and chicks are aggressive mimics, appearing harmless but in fact dangerous to host reproduction. These strategies are each countered by host discrimination, providing the means for distinct coevolutionary arms races at successive stages of the host nesting cycle.
CHINESE BIRDS, 2012
Common Cuckoos (Cuculus canorus) parasitize nests of small passerines. The Cuckoo chicks cause the death of their nest-mates when evicting eggs or nestlings from the nests; consequently, hosts suffer from a high loss of reproduction. Host adaptations against parasitism, e.g., by egg discrimination behavior, and cuckoo counter-adaptations to hosts, e.g., by mimetic eggs, are often regarded as a result of the arms race between the two interacting species. In Hungary Great Reed Warblers (Acrocephalus arundinaceus) are the main hosts of cuckoos, suffering from heavy parasitism (ca. 40-65%). The Oriental Reed Warbler (A. orientalis), formerly a subspecies of the Great Reed Warbler (A. a. orientalis), is also a highly parasitized host in Japan (25-40%). We compared main characteristics of Cuckoo parasitism in these two distant areas from the Western and Eastern Palearctic by comparing cuckoo egg mimicry. We measured color characteristics of host and parasitic eggs by spectrophotometer. Visual modeling revealed lower chromatic distances between Cuckoo and host eggs in Hungary than in Japan, but high variation both in host and Cuckoo eggs may cause matching problems in Hungary. Achromatic (brightness) difference between host and Cuckoo eggs were lower in Japan than in Hungary, and it proved to be the most important factor affecting egg rejection. Hosts rejected Cuckoo eggs at similar frequencies (37% and 35% in Hungary and Japan, respectively). Host adaptation, i.e., egg rejection behavior, seems to be preceding Cuckoo counter-adaptations to hosts in Japan. We suggest that the Cuckoo-Great/Oriental Reed Warbler relationships developed in alternative ways in Japan and Hungary, and they represent different stages of their arms race.
An experimental test of host's life history traits modulation in response to cuckoo parasitism risk
PloS one, 2017
Hosts can counteract parasites through defences based on resistance and/or tolerance. The mechanistic basis of tolerance, which involve defensive mechanisms minimizing parasite damage after a successful parasitic attack, remains poorly explored in the study of cuckoo-host interactions. Here, we experimentally explore the possibility that the risk of great spotted cuckoo Clamator glandarius parasitism may induce tolerance defences in magpie Pica pica hosts through plasticity in life-history traits. We predict that magpies exposed to auditory cues indicating high parasitism risk will more likely exhibit resistance and/or modify their life-history traits to minimize parasitism costs (i.e. tolerance) compared to magpies under low parasitism risk. We found that manipulating the perceived parasitism risk did not affect host resistance (i.e. rejection of parasitic eggs) nor host life-history traits. Unexpectedly, host's egg volume increased over the season in nests exposed to auditory ...
Coevolution of an Avian Host and Its Parasitic Cuckoo
Evolution, 2003
We use a quantitative genetic model to examine the coevolution of host and cuckoo egg characters (termed ''size'' as a proxy for general appearance), host discrimination, and host and cuckoo population dynamics. A host decides whether to discard an egg using a comparison of the sizes of the eggs in her nest, which changes as host and cuckoo eggs evolve. Specifically, we assume that the probability that she discards the largest egg in her nest depends on how much larger it is than the second largest egg. This decision rule (i.e., the acceptable difference in egg sizes) also evolves, changing both the chance of successful rejection of a cuckoo egg in parasitized nests and the chance of mistaken rejection of a host egg in both parasitized and unparasitized nests. We find a stable equilibrium for coexistence of the host and cuckoo where there is cuckoo egg mimicry, evolutionary displacement of the host egg away from the cuckoo egg phenotype, and host discrimination against unusual eggs. Both host discrimination and host egg displacement are fairly weak at the equilibrium. Cuckoo egg mimicry, although imperfect, usually evolves more extensively and quickly than the responses of the host. Our model provides evidence for both the evolutionary equilibrium and evolutionary lag hypotheses of host acceptance of parasitic eggs.
The adaptiveness of defence strategies against cuckoo parasitism
2002
Host bird species of the Eurasian Cuckoo, Cuculus canorus, often display eggdiscrimination behaviour but chick-rejection behaviour has never been reported. In this paper, we analyse a host-cuckoo association in which both population dynamics and evolutionary dynamics are explored in a discrete-time model. We introduce four host types, each with their own defence behaviour, displaying either egg or chick rejection, neither or both, We also introduce fitness functions for each of these host types. Although we can characterize the long term behaviour in many cases by a simple heuristic argument which is in accordance with common views in ecology, there are a number of other phenomena that are not explained within this framework: we describe stable oscillatory behaviour and coexistence of two defensive host types. We analyse the scenarios in which chick rejection may establish itself and give a first explanation as to why this defence trait has never been recorded in nature. We find that chick rejectors generally are at an intrinsic disadvantage with respect to a host type that rejects eggs. Hosts benefit more from rejecting cuckoo eggs than cuckoo chicks, and our model suggests that this is chiefly responsible for the absence of chick rejection. Moreover, even though it seems that chick rejection must be useful as an extra defence, it is shown that hosts with both defence strategies are less likely to establish themselves in competition with egg-rejectors than
Host response to cuckoo song is predicted by the future risk of brood parasitism
Frontiers in Zoology, 2013
Introduction: Risk assessment occurs over different temporal and spatial scales and is selected for when individuals show an adaptive response to a threat. Here, we test if birds respond to the threat of brood parasitism using the acoustical cues of brood parasites in the absence of visual stimuli. We broadcast the playback of song of three brood parasites (Chalcites cuckoo species) and a sympatric non-parasite (striated thornbill, Acanthiza lineata) in the territories of superb fairy-wrens (Malurus cyaneus) during the peak breeding period and opportunistic breeding period. The three cuckoo species differ in brood parasite prevalence and the probability of detection by the host, which we used to rank the risk of parasitism (high risk, moderate risk, low risk). Results: Host birds showed the strongest response to the threat of cuckoo parasitism in accordance with the risk of parasitism. Resident wrens had many alarm calls and close and rapid approach to the playback speaker that was broadcasting song of the high risk brood parasite (Horsfield's bronze-cuckoo, C. basalis) across the year (peak and opportunistic breeding period), some response to the moderate risk brood parasite (shining bronze-cuckoo, C. lucidus) during the peak breeding period, and the weakest response to the low risk brood parasite (little bronzecuckoo, C. minutillus). Playback of the familiar control stimulus in wren territories evoked the least response.