Longwu Wang

Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism

Parasites may, in multi-parasite systems, block the defenses of their hosts and thus thwart host recognition of parasites by frequency-dependent selection. Nest defenses as frontline may block or promote the subsequent stage of defenses such as egg recognition. We conducted comparative studies of the defensive strategies of a host of the Oriental cuckoo Cuculus optatus, the yellow-bellied prinia Prinia flaviventris, in mainland China with multiple species of cuckoos and in Taiwan with a single cuckoo species. Cuckoo hosts did not exhibit aggression toward cuckoos in the presence of multiple cuckoo species but showed strong aggressive defenses of hosts directed toward cuckoos in Taiwan. Furthermore, the cuckoo host in populations with a single cuckoo species was able to distinguish adults of its brood parasite, the Oriental cuckoo, from adult common cuckoos (Cuculus canorus). This represents the first case in which a cuckoo host has been shown to specifically distinguish Oriental cuckoo, from other Cuculus species. Hosts ejected eggs at a higher rate in a single cuckoo species system than in a multi-species cuckoo system, which supports the strategy facilitation hypothesis. Granularity analysis of variation in egg phenotype based on avian vision modeling supported the egg signature hypothesis in hosts because Taiwanese prinias increased consistency in the appearance of their eggs within individual hosts thus favoring efficient discrimination against cuckoo eggs. This study significantly improves our knowledge of intraspecific variation in antiparasitism behavior of hosts between single- and multi-cuckoo systems.

Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs

Brood parasitism is costly to hosts, and, therefore, a number of anti-parasite defenses have evolved. Surprisingly, several high-quality hosts such as martins and swallows are rarely parasitized, raising the question why that is the case. We hypothesize that martins and swallows may avoid parasitism by breeding in close association with humans, and by building nests that are inaccessible for common cuckoos Cuculus canorus and other brood parasites. Here we show using egg rejection experiments that red-rumped swallows Hirundo daurica, house martins Delichon urbica, and barn swallows Hirundo rustica in Europe do not reject foreign eggs placed in their nests, while barn swallows in China often reject foreign eggs. The frequency of parasitism of barn swallows in Europe was significantly higher than in house martins relative to the expectation based on the abundance of the two species. Barn swallows in Europe that were parasitized by cuckoos more often placed their nests outdoors than expected by chance, suggesting that avoidance of cuckoo parasitism can be achieved by breeding indoors. These findings suggest that barn swallows in China have gained egg rejection behavior because they cannot avoid parasitism when breeding outdoors.

Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism

Previous studies suggested that nest sanitation behavior may have been a pre-adaptation from which egg rejection of brood parasite eggs evolved. We tested this hypothesis in two swallow species, the red-rumped swallow (Cecropis daurica) and the barn swallow (Hirundo rustica). Our results indicated that the red-rumped swallow, which is an accepter of foreign eggs, rejected a low percentage of non-egg-shaped objects and did so less often than the barn swallow, which is an intermediate rejecter of foreign eggs. Furthermore, the egg rejection rates of the barn swallow increased with the increase in rejection rates of non-egg-shaped objects among different populations. These results showed that nest cleaning behavior could have evolved into a means of reducing the costs of brood parasitism, suggesting that egg recognition ability has evolved from recognition of non-egg-shaped objects. This finding advances our understanding of the evolution of egg recognition behavior in birds.

Nestling recognition in red-rumped and barn swallows

Nestling recognition and rejection is a rare defense strategy against avian brood parasitism that was previously thought to be too costly to evolve. Recently, several examples of nestling recognition and rejection by fosterers have been reported. Here, we tested for chick recognition ability in red-rumped swallows (Hirundo daurica), which build closed nests and do not discriminate against foreign eggs, by using cross-fostering experiments while controlling for responses to intraspecific and interspecific parasitism in closely related swallow species. We show that red-rumped swallows do not discriminate against conspecific or barn swallow (H. rustica) nestlings, but eject or reject cuckoo nestlings cross-fostered in red-rumped swallow nests by starving the introduced chicks to death. Assuming that the behavior of red-rumped swallows evolved in response to cuckoo parasitism, this study represents novel empirical evidence showing that chick discrimination evolved when brood parasites have completely evaded host defenses at the egg stage. The evolution of such recognition ability may be explained as a defense against avian brood parasitism by small-sized cuckoos or a pre-adaptation to specific communication between host parents and offspring. Our results are consistent with the “rarer enemy” hypothesis predicting that nestling discrimination should evolve only in hosts that accept all naturally laid parasite eggs and thus do not decrease effective parasitism rate at the nestling stage. In contrast, the findings were inconsistent with a number of alternative hypotheses.

Egg recognition as antiparasitism defence in hosts does not select for laying of matching eggs in parasitic cuckoos

Recent studies have suggested that parasitic cuckoos have evolved laying behaviour resulting in matching of host and cuckoo eggs by choosing to lay eggs in host nests with host eggs that match the cuckoo eggs as an adaptation against egg recognition by the hosts. However, previous studies provided weak and indirect evidence with mixed results, leaving this question unresolved. Here, for the first time, we developed a robust methodology to provide unambiguous evidence that egg recognition in the host does not select for optimal egg matching during laying by the cuckoo. By using experiments that attracted parasitism, we showed that cuckoos, Cuculus canorus, indiscriminately laid eggs in oriental reed warbler, Acrocephalus orientalis, host nests containing real host eggs, egg-shaped models, stick models or coin models without any preference. Furthermore, cuckoos only selected to lay their eggs in nests with active hosts. These experiments provide evidence of cuckoos being indiscriminate in their choice of host nests, implying that coevolution of the egg phenotype of host and cuckoo eggs must have arisen from mechanisms other than matching of host eggs and those of the parasite.

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.

How cuckoos find and choose host nests for parasitism

Lay Summary We provide experimental evidence to confirm that the common cuckoo (Cuculus canorus) locates its Oriental reed warbler (Acrocephalus orientalis) host nests by monitoring the activities of nest owners. Cuckoos distinguished between nest types of different host species and choose to parasitize nests of the most commonly parasitized host, while cuckoos did not choose to lay eggs in nests matching the appearance of their own eggs.

Increase of clutch size triggers clutch destruction behaviour in common moorhens (Gallinula chloropus) during the incubation period

Conspecific brood parasitism (CBP) is common in a variety of animal taxa, including birds. In coots (Fulica spp.), and the closely related moorhens (Gallinula spp.), such parasitism is especially common, and hosts experience considerable costs through increased chick competition soon after hatching. Hence, these birds have evolved egg recognition and rejection abilities, e.g., egg counting, burying the foreign eggs, assigning them suboptimal positions within the mixed clutch, or deserting parasitized clutches. For common moorhens (Gallinula chloropus) it has been shown that desertion of parasitized nests pays most at the early egg laying stage. Later on, the costs of desertion exceed the costs of brood parasitism and acceptance is favoured. Here we tested moorhen egg discrimination behaviour during the incubation stage when acceptance of foreign eggs is expected. Four treatments were applied: (1) single added non-mimetic pale blue egg, (2) single added non-mimetic white chicken egg, (3) four foreign conspecific eggs added to the clutch and (4) four foreign conspecific eggs exchanged for four host eggs. Moorhens responded by egg destruction (47%) only to the increased clutch size but not to foreign egg colour and size match. In three nests where egg destruction occurred, all the eggs in the mixed clutch were destroyed by pecking, in two other nests one of the foreign eggs were pecked, while two other nests were deserted. These results are puzzling since moorhens have been shown to possess refined egg recognition abilities. To our knowledge, such destruction of parasitized clutches by moorhens during incubation has not previously been reported. We suggest that after clutch completion, moorhens use increase in clutch size as a cue to determine if they have been parasitized, and some individuals choose to reject parasitic eggs by deserting or destroying the whole clutch.

Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs

Obligate brood parasites have evolved unusually thick-shelled eggs, which are hypothesized to possess a variety of functions such as resistance to puncture ejection by their hosts. In this study, we tested the hypothesis that obligate brood parasites lay unusually thick-shelled eggs to retain more heat for the developing embryo and thus contribute to early hatching of parasite eggs. By doing so, we used an infrared thermal imaging system as a non-invasive method to quantify the temperature of eggshells of common cuckoos (Cuculus canorus) and their Oriental reed warbler (Acrocephalus orientalis) hosts in an experiment that artificially altered the duration of incubation. Our results showed that cuckoo eggshells had higher temperature than host eggs during incubation, but also less fluctuations in temperature during incubation disturbance. Therefore, there was a thermal and hence a developmental advantage for brood parasitic cuckoos of laying thick-shelled eggs, providing another possible explanation for the unusually thick-shelled eggs of obligate brood parasites and earlier hatching of cuckoo eggs compared to those of the host.

Contrasting egg recognition between European and Asian populations of tree sparrows (Passer montanus).

Although many biological phenotypes are generally regarded as consistent across the distributional range of a species, some traits such as egg discrimination behavior have been shown to display extensive intraspecific variation as a response to selection from brood parasitism. We investigated the egg recognition ability in an Asian population of tree sparrows (Passer montanus), and we compared that with the ability to recognize and reject intraspecific foreign eggs in a population in Europe. Extensive artificial parasitism with model eggs and real eggs of eight sympatric birds that vary in background color and markings revealed that egg recognition capacity is completely absent in this Asian population of tree sparrows. This result contrasts with previous studies in European populations showing extensive ability for discriminating between own and foreign eggs. Different evolutionary equilibria or differences in the risk of conspecific parasitism may account for differences in egg discrimination ability between European and Asian populations of tree sparrows.