Hosts Of Brood Parasites Research Articles

Egg Polymorphism and Egg Discrimination in the Daurian RedstartPhoenicurus auroreus, a Host of the Common CuckooCuculus canorus

The evolution of egg polymorphism based on strong egg discrimination by hosts of brood parasites may be a specific adaptation against avian brood parasitism. However, different cuckoo-host systems with egg polymorphism may differ in many other aspects during coevolution. We studied the interaction between the Common Cuckoo Cuculus canorus and its host, the Daurian Redstart Phoenicurus auroreus, and detected that cuckoos use an intermediate degree of egg monomorphism to parasitize contrasting dimorphic eggs laid by redstarts. However, redstarts only possess an intermediate ability of egg recognition of dissimilar egg phenotypes with a high degree of recognition error and long latency to rejection. We discuss possible explanations for these observations and suggest that the intermediate degree of egg mimicry in the cuckoo and egg recognition in the redstart may constitute an early stage of disruptive coevolution in egg phenotypes between cuckoos and hosts. Alternatively, intermediate polymorphism may be maintained as a result of an evolutionary equilibrium between hosts and parasites.

Brood Parasite-Host Coevolution in America Versus Europe: Egg Rejection in Large-Sized Host Species

The hosts of brood parasites have evolved egg-discrimination ability as a defence that allows them to reject parasitic eggs laid in their nests. Twenty-five years ago, Stephen Rothstein emphasised that rejection rates differed markedly between potential host species in Europe and America. The much more complete information available today supports Rothstein's conclusions, but also allows new ones, especially when considering host size. For instance, successful resistance, one of the three potential long-term outcomes of brood parasite-host coevolution, is considerably more frequent in small-sized European host species and in medium-sized and large-sized Nearctic host species, while this evolutionary outcome is rare among Neotropical hosts regardless of their size. These results have never before been discussed, despite the differences being spectacular: 17 out of 19 small hosts presenting successful resistance are from Europe and 16 out of 17 medium-sized and 11 out of 13 large hosts presenting successful resistance are from North America. Interestingly, many large Nearctic hosts with a rejection rate close to 100% are corvids. The high rejection capacity shown by large Nearctic potential hosts probably evolved as a response to a highly virulent extinct brood parasite, either a large extinct cowbird or an extinct cuckoo species, which went extinct after losing the arms race against its large hosts.

Reduced ultraviolet reflectance does not affect egg rejection by Northern Cardinals (Cardinalis cardinalis)

ABSTRACT With the discovery that the ultraviolet (UV) spectrum is visible to birds, studies have shown how this parameter can affect the ability of hosts of brood parasites to recognize eggs. However, the role UV reflectance plays in egg recognition has not been well studied in hosts of Brown-headed Cowbirds (Molothrus ater). Northern Cardinals (Cardinalis cardinalis) are common hosts that usually accept cowbird eggs, but evidence suggests that cardinals reject nonmimetic eggs more frequently. The purpose of this study was to determine if a reduction in UV reflectance of cowbird eggs would elicit a rejection response from the cardinal. Four treatments were used: (1) cowbird eggs covered with UV-block; (2) cowbird eggs covered with a control coating; (3) uncoated cowbird eggs used as a control, and (4) cardinal eggs covered with UV-block. Cowbird and cardinal eggs with UV-block were not more likely to be rejected than eggs in either of the control treatments. Cowbird and cardinal eggs are similar in both a...

Egg rejection and clutch phenotype variation in the plain prinia Prinia inornata

Avian hosts of brood parasites can evolve anti‐parasitic defenses to recognize and reject foreign eggs from their nests. Theory predicts that higher inter‐clutch and lower intra‐clutch variation in egg appearance facilitates hosts to detect parasitic eggs as egg‐rejection mainly depends on the appearance of the egg. Therefore, we predict that egg patterns and rejection rates will differ when hosts face different intensity of cuckoo parasitism. We tested this prediction in two populations of the plain prinia Prinia inornata: Guangxi in mainland China with high diversity and density of cuckoo species, and Taiwan where there is only one breeding cuckoo species, the oriental cuckoo Cuculus optatus. As expected, egg patterns were similar within clutches but different among clutches (polymorphic eggs) in the mainland population, while the island population produced more uniform egg morphs. Furthermore, the mainland population showed a high rate of egg rejection, while the island population exhibited dramatically reduced egg grasp‐rejection ability in the absence of parasitism by the common cuckoo Cuculus canorus. Our study suggests that prinias show lower intra‐clutch consistency in egg colour and lose egg‐rejecting ability under relaxed selection pressure from brood parasitism.

Brood Parasitism Is Linked to Egg Pattern Diversity within and among Species of Australian Passerines.

Bird eggs show striking diversity in color and pattern. One explanation for this is that interactions between avian brood parasites and their hosts drive egg phenotype evolution. Brood parasites lay their eggs in the nests of other species, their hosts. Many hosts defend their nests against parasitism by rejecting foreign eggs, which selects for parasite eggs that mimic those of the host. In theory, this may in turn select for changes in host egg phenotypes over time to facilitate discrimination of parasite eggs. Here, we test for the first time whether parasitism by brood parasites has led to increased divergence in egg phenotype among host species. Using Australian host and nonhost species and objective measures of egg color and pattern, we show that (i) hosts of brood parasites have higher within-species variation in egg pattern than nonhosts, supporting previous findings in other systems, and (ii) host species have diverged more in their egg patterns than nonhost species after controlling for divergence time. Overall, our results suggest that brood parasitism has played a significant role in the evolution of egg diversity and that these effects are evident, not only within species, but also among species.

Geographic variation in egg ejection rate by great tits across 2 continents

Hosts of brood parasites may vary geographically in their ability to resist parasitism. In contrast, geographic variation in defenses, such as egg rejection, is not expected to be present or vary geographically in unsuitable hosts. We examined spatial patterns of resistance in the great tit Parus major, a passerine that is a textbook example of an unsuitable host for brood parasites because of its hole-nesting habits. We experimentally tested for spatial variation in foreign egg rejection in 395 nests across latitudinal gradients in China (5 populations) and Europe (7 populations). In China, egg rejection rates were very high but showed a latitudinal gradient from 100% in the south to 52% in the north. In Europe, rejection rates were very low (on average only 4%) and did not vary latitudinally. The egg ejection rate patterns matched geographic patterns of parasitism risk with rejection probabilities decreasing with latitude (a surrogate measure of the diversity of brood parasites). The present study for the first time challenges the idea that hole-nesting birds did not evolve resistance mechanisms against brood parasites and highlights the importance of large-scale geographic comparisons in ecological research.

Disappearance of eggs from nonparasitized nests of brood parasite hosts: the evolutionary equilibrium hypothesis revisited

WL was funded by the National Natural Science Foundation of China (Nos. 31071938, 31272328, and 31472013). BGS and FF were funded by the Research Council of Norway (218144). CY was funded by the National Natural Science Foundation of China (Nos. 31101464 and 31260514) and New Century Excellent Talents in University (NCET-13-0761). CM was funded by the Hungarian National Science Fund (OTKA, No. 83217).

Cuckoo parasitism in a cavity nesting host: near absent egg‐rejection in a northern redstart population under heavy apparent (but low effective) brood parasitism

Brood parasite – host systems continue to offer insights into species coevolution. A notable system is the redstartPhoenicurus phoenicurusparasitized by the ‘redstart‐cuckoo’Cuculus canorusgens. Redstarts are the only regular cuckoo hosts that breed in cavities, which challenges adult cuckoos in egg laying and cuckoo chicks in host eviction. We investigated parasitism in this system and found high overall parasitism rates (31.1% of 360 redstart nests), but also that only 33.1% of parasitism events (49 of 148 eggs) were successful in laying eggs into redstart nest cups. The majority of cuckoo eggs were mislaid and found on the rim of the nest; outside the nest cup. All available evidence suggests these eggs were not ejected by hosts. The effective parasitism rate was therefore only 12.8% of redstart nests. Redstarts responded to natural parasitism by deserting their nests in 13.0% of cases, compared to desertion rates of 2.8% for non‐parasitized nests. Our egg parasitism experiments found low rates (12.2%) of rejection of artificial non‐mimetic cuckoo eggs. Artificial mimetic and real cuckoo eggs added to nests were rejected at even lower rates, and were always rejected via desertion. Under natural conditions, only 21 cuckoo chicks fledged of 150 cuckoo eggs laid. Adding to this low success, is that cuckoo chicks are sometimes unable to evict all host young, and were more likely to die as a result compared to cuckoo chicks reared alone. This low success seems to be mainly due to the cavity nesting strategy of the redstart which is a challenging obstacle for the cuckoo. The redstart‐cuckoo system appears to be a fruitful model system and we suggest much more emphasis should be placed on frontline defences such as nest site selection strategies when investigating brood parasite–host coevolution.

Nest sanitation elicits egg discrimination in cuckoo hosts

Nest sanitation is a nearly universal behavior in birds, while egg discrimination is a more specific adaptation that has evolved to counter brood parasitism. These two behaviors are closely related with nest sanitation being the ancestral behavior, and it has been hypothesized to constitute a preadaptation for egg discrimination. However, previous studies found little evidence to support this hypothesis. Here, we conducted an empirical test of the association between nest sanitation and egg discrimination in the barn swallow (Hirundo rustica) by inserting a single non-mimetic model egg or a non-mimetic model egg plus half a peanut shell into host nests. Compared to the rejection rate of single model eggs, barn swallows significantly increased egg rejection frequency if a half peanut shell was simultaneously introduced. Our result for the first time shows the impact of nest sanitation on egg discrimination and demonstrates that nest sanitation can elicit egg discrimination in hosts of brood parasites. This study provided evidence for nest sanitation being a preadaptation to egg discrimination by facilitating egg rejection, thereby significantly advancing our understanding of avian cognition of foreign objects. Furthermore, we suggest that egg discrimination behavior in many accepters and intermediate rejecters may be lost or diluted. Such egg discrimination can be elicited and restored after nest sanitation, implying a sensitive and rapid phenotypic response to increased risk of parasitism. Our study offers a novel perspective for investigating the role of so-called intermediate rejecter individuals or species in the long-term coevolutionary cycle between brood parasites and their hosts.

Hosts of avian brood parasites have evolved egg signatures with elevated information content.

Hosts of brood-parasitic birds must distinguish their own eggs from parasitic mimics, or pay the cost of mistakenly raising a foreign chick. Egg discrimination is easier when different host females of the same species each lay visually distinctive eggs (egg ‘signatures’), which helps to foil mimicry by parasites. Here, we ask whether brood parasitism is associated with lower levels of correlation between different egg traits in hosts, making individual host signatures more distinctive and informative. We used entropy as an index of the potential information content encoded by nine aspects of colour, pattern and luminance of eggs of different species in two African bird families (Cisticolidae parasitized by cuckoo finches Anomalospiza imberbis, and Ploceidae by diederik cuckoos Chrysococcyx caprius). Parasitized species showed consistently higher entropy in egg traits than did related, unparasitized species. Decomposing entropy into two variation components revealed that this was mainly driven by parasitized species having lower levels of correlation between different egg traits, rather than higher overall levels of variation in each individual egg trait. This suggests that irrespective of the constraints that might operate on individual egg traits, hosts can further improve their defensive ‘signatures' by arranging suites of egg traits into unpredictable combinations.

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts.

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.

Experimental shifts in egg–nest contrasts do not alter egg rejection responses in an avian host–brood parasite system

Obligate brood parasitic birds exploit their hosts to provide care for unrelated young in the nest. Potential hosts can reduce the cost of parasitism by rejecting foreign eggs from the nest. Observational, comparative, and experimental studies have concluded that most hosts use the coloration and patterning of eggshells to discriminate between own and foreign eggs in the nest. However, an alternative hypothesis is that birds use the colour contrasts between eggshells and the nest lining to identify parasitic eggs (egg-nest contrast hypothesis). In support of this hypothesis, we found that the avian perceivable chromatic contrasts between dyed eggs and unmanipulated nest linings significantly and negatively covaried with the rejection rates of different dyed eggs of the great reed warbler Acrocephalus arundinaceus, a frequently parasitized host of the common cuckoo Cuculus canorus. To experimentally test whether egg-nest contrasts influence rejection, we reciprocally dyed both eggs and the nest lining of this host species with one of two colours: orange and green. Contrary to the egg-nest contrast hypothesis, host rejection patterns in response to dyed eggs were not altered by dyeing nests, relative to unmanipulated control eggs and nests. In turn, experimental egg colour was the only significant predictor of egg rejection rate. Our results demonstrate that egg-nest contrast is a collateral, not a causal factor in egg rejection, and confirm the conclusions of previous studies that hosts can rely on the parasitic egg's appearance itself to recognize the foreign egg in the nest.

Lazy males and hardworking females? Sexual conflict over parental care in a brood parasite host and its consequences for chick growth

Due to the costs of parental care, a conflict of interests often arises between mates wherein each prefers the other to invest more. As with parents raising their own offspring, hosts of brood parasites also exhibit negotiations over investment, becoming particularly intensive when parasite demands are high. Lack of cooperation between the partners may eventually affect the condition and fledging success of the young. Here, we investigate the magnitude of sexual conflict over food provisioning in socially polygynous great reed warblers (Acrocephalus arundinaceus) rearing either a parasitic common cuckoo (Cuculus canorus) or their own nestlings and its consequences for chick growth. We found that, overall, males provided less food than females, and that polygynous males provided less food per nest than monogamous males. Moreover, polygynous males provisioning two simultaneous broods supplied their own offspring in relation to age and type (cuckoo/host) of the other brood. Females, unlike males, delivered food amount almost irrespective of social status. The difference in contribution between polygynous males and their mates was most pronounced in nests with a cuckoo. In any case, reduced paternal assistance had no significant effect on growth performance of nestlings. In cuckoos, however, this result may be biased as we could not consider a relatively high proportion of secondary cuckoos that died before their growth parameters could be ascertained. Although not detected in chick growth, host sexual conflict over food provisioning may impose a cost on cuckoos in terms of increased mortality in secondary nests.

Experimental shifts in intraclutch egg color variation do not affect egg rejection in a host of a non-egg-mimetic avian brood parasite.

Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host’s ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins’ behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.

The evolution of acceptance and tolerance in hosts of avian brood parasites.

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi-broodedness), and utilize the literature on host-pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.

Absence of egg rejection in an Asian population of house sparrow (Passer domesticus), a conspecific brood parasite in Europe

The house sparrow (Passer domesticus) is well known for conspecific brood parasitism in Europe, and there it is capable of recognizing and rejecting non-mimetic foreign eggs and even mimetic conspecific eggs. Here, we tested the egg rejection of an Asian population of house sparrows by using model eggs, sparrow eggs painted red and sparrow eggs with added brown spots, of which their mimicry to sparrow eggs were quantified by granularity analysis based on avian vision. Surprisingly, house sparrows in Asia did not show any egg rejection. We suggest that the evolutionary equilibrium theory, which was first proposed to explain the absence of egg rejection in some hosts of interspecific brood parasites, may explain the deficiency of egg rejection in house sparrows, as a result of trade-offs between the high rejection costs and the costs of raising conspecific foreign chicks.

The Value of Artificial Stimuli in Behavioral Research: Making the Case for Egg Rejection Studies in Avian Brood Parasitism

AbstractExperimentation is at the heart of classical and modern behavioral ecology research. The manipulation of natural cues allows us to establish causation between aspects of the environment, both internal and external to organisms, and their effects on animals' behaviors. In recognition systems research, including the quest to understand the coevolution of sensory cues and decision rules underlying the rejection of foreign eggs by hosts of avian brood parasites, artificial stimuli have been used extensively, but not without controversy. In response to repeated criticism about the value of artificial stimuli, we describe four potential benefits of using them in egg recognition research, two each at the proximate and ultimate levels of analysis: (1) the standardization of stimuli for developmental studies and (2) the disassociation of correlated traits of egg phenotypes used for sensory discrimination, as well as (3) the estimation of the strength of selection on parasitic egg mimicry and (4) the establishment of the evolved limits of sensory and cognitive plasticity. We also highlight constraints of the artificial stimulus approach and provide a specific test of whether responses to artificial cues can accurately predict responses to natural cues. Artificial stimuli have a general value in ethological research beyond research in brood parasitism and may be especially critical in field studies involving the manipulation of a single parameter, where other, confounding variables are difficult or impossible to control experimentally or statistically.

Hawk mimicry in cuckoos and anti‐parasitic aggressive behavior of barn swallows in Denmark and China

Hosts of brood parasites defend their nests against parasitism by aggression and subsequently, if parasitized, by rejection of the parasite egg or nestling. Cuckoos have evolved plumage mimicry with convergence towards the phenotype of Accipiter hawks that are common predators of cuckoo hosts. Here we tested two alternative hypotheses 1) whether barn swallows Hirundo rustica have evolved less aggressive behavior towards cuckoos in areas of sympatry with more abundant Accipiter hawks; and 2) whether barn swallows have evolved more aggressive anti‐parasite behavior in areas with a single species of cuckoo. We presented dummies of common cuckoo Cuculus canorus, sparrowhawk Accipiter nisus and Oriental turtledove Streptopelia orientalis (a benign control) at the nests of barn swallows during breeding, while recording intensity of response and proximity of barn swallows to the dummy. We demonstrated that cuckoos moved away when attacked aggressively and approached more closely by barn swallows showing that barn swallow behavior was efficient at driving away cuckoos. Barn swallows were significantly more aggressive and approached cuckoo and sparrowhawk dummies more closely in Denmark than in China, despite sparrowhawks being relatively more common in Denmark. Responses towards cuckoo dummies differed from responses towards sparrowhawk dummies, showing that barn swallows distinguished between the two different causes of danger. These findings are inconsistent with a less aggressive response towards cuckoo dummies in areas of sympatry with more abundant Accipiter hawks, but consistent with the alternative hypothesis that barn swallows have evolved more aggressive behavior towards cuckoos in areas with a single species of brood parasite, but not in areas with multiple species of parasites, where it is harder for hosts to tell the difference.

No evidence of conspecific brood parasitism provoking egg rejection in thrushes

No abstract.

Collective defence portfolios of ant hosts shift with social parasite pressure.

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host's nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.