Parasitic Cuckoos Research Articles

"Isolation by Gentes with Asymmetric Migration" shapes the genetic structure of the common cuckoo in China.

Amid coevolutionary arms races between brood parasitic birds and their diverse host species, the formation of host-specific races, or gentes, has drawn significant research focus. Nevertheless, numerous questions about gentes evolutionary patterns persist. Here, we investigated the potential for gentes evolution across multiple common cuckoo (Cuculus canorus) populations parasitizing diverse host species in China. Using maternal (mitochondrial and W-linked DNA) and biparental (autosomal and Z-linked DNA) markers, we found consistent clustering of cuckoo gentes (rather than geographical populations) into distinct clades in matrilineal gene trees, indicating robust differentiation. In contrast, biparental markers indicated intermixing of all gentes, suggesting asymmetric gene flow regardless of geography. Unlike the mitonuclear discordance commonly resulting from incomplete lineage sorting, adaptive introgression, or demographic disparities, the observed pattern in brood parasitic cuckoos might reflect biased host preferences between sexes. We hereby present the "Isolation by Gentes with Asymmetric Migration" model. According to this model, the maternal line differentiation of the common cuckoo in China is potentially driven by host preferences in females, whereas males maintained the integrity of the cuckoo species through random mating. To achieve this, cuckoo males could perform flexible migration among gentes or engage in early copulation with females before reaching the breeding sites, allowing female cuckoos to store sperm from various gentes. Future studies collecting additional samples from diverse cuckoo gentes with overlapping distribution and investigating the migratory and copulation patterns of each sex would enhance our understanding of sex-biased differentiation among cuckoo populations in China.

Low breeding synchrony of great reed warbler hosts in warmer springs does not increase their susceptibility to common cuckoo parasitism

Low breeding synchrony of great reed warbler hosts in warmer springs does not increase their susceptibility to common cuckoo parasitism

The effect of Common Cuckoo parasitism on the annual productivity of a host population

Avian interspecific brood parasitism is an excellent system for studying coevolutionary processes in nature because brood parasites directly affect host reproductive success. Most research on avian brood parasitism has, therefore, focused primarily on specific host anti-parasite behaviours and parasite counter-adaptations. However, the population-level consequences of brood parasitism for host species are poorly understood. This study investigated the effect of Common Cuckoo (Cuculus canorus) parasitism on the productivity of a local population of the Great Reed Warbler (Acrocephalus arundinaceus) host in south-western Slovakia. A total of 495 females nesting at the studied site successfully fledged 1321 of their own young and 63 young of the Common Cuckoo over the course of 15 years (2008–2022), and the annual rate of successful parasitism ranged from 18% to 44% over this period. As predicted, higher rates of successful cuckoo parasitism significantly reduced the annual productivity of the local Great Reed Warbler population, and its contribution to decreased host reproductive success was at about the same rate as overall nest failure caused by predation and other environmental factors. Such a heavily parasitized population was probably maintained by immigrants from other populations and density-dependent selection, which is also consistent with source–sink dynamics. However, further long-term studies monitoring parasitized populations are required to confirm these findings.

The risk of brood parasitism does not affect levels of extrapair paternity in a cuckoo host

Abstract In socially monogamous bird species, extrapair paternity is common, but its level varies considerably within and among species. For hosts of brood parasites, the risk of brood parasitism may influence the costs of engaging in extrapair copulations (e.g., leaving the nest undefended) and the benefits of having extrapair young (e.g., spreading the risk of nest predation). However, whether brood parasitism risk affects extrapair behavior in host species has rarely been tested. We investigated whether variation in the risk of brood parasitism affected levels of extrapair paternity in Daurian redstarts, a socially monogamous passerine. As a common host of the common cuckoo, the redstart is unique in that its first clutch of the year takes place before the arrival of cuckoos. As a consequence, redstarts experience large seasonal variation in cuckoo parasitism risk, with no parasitism in the first egg-laying period and a high risk in the second period. We genotyped 995 nestlings (and unhatched eggs) from 181 broods and found moderate levels of extrapair paternity, with 34.8% of broods containing at least one extrapair young and 11.7% of all offspring being sired by an extrapair male. However, levels of extrapair paternity did not differ between the first and the second egg-laying period. Also, experimentally simulating parasitism risk during the first egg-laying period by broadcasting cuckoo vocalizations and presenting taxidermic models of cuckoos did not affect levels of extrapair paternity in redstarts. Our results, therefore, suggest that the risk of brood parasitism does not affect host extrapair paternity.

Ritual displays by a parasitic cuckoo: nuptial gifts or territorial warnings?

Ritual displays by a parasitic cuckoo: nuptial gifts or territorial warnings?

Lack of host specialization despite selective host use in brood parasitic cuckoo catfish.

Host-parasite dynamics involve coevolutionary arms races, which may lead to host specialization and ensuing diversification. Our general understanding of the evolution of host specialization in brood parasites is compromised by a restricted focus on bird and insect lineages. The cuckoo catfish (Synodontis multipunctatus) is an obligate parasite of parental care of mouthbrooding cichlids in Lake Tanganyika. Given the ecological and taxonomic diversity of mouthbrooding cichlids in the lake, we hypothesized the existence of sympatric host-specific lineages in the cuckoo catfish. In a sample of 779 broods from 20 cichlid species, we found four species parasitized by cuckoo catfish (with prevalence of parasitism of 2%-18%). All parasitized cichlids were from the tribe Tropheini, maternal mouthbrooders that spawn over a substrate (rather than in open water). Phylogenetic analysis based on genomic (ddRAD sequencing) and mitochondrial (Dloop) data from cuckoo catfish embryos showed an absence of host-specific lineages. This was corroborated by analyses of genetic structure and co-ancestry matrix. Within host species, parasitism was not associated with any individual characteristic we recorded (parent size, water depth), but was costly as parasitized parents carried smaller clutches of their own offspring. We conclude that the cuckoo catfish is an intermediate generalist and discuss costs, benefits and constraints of host specialization in this species and brood parasites in general.

Nest desertion as an anti-parasitism strategy in hosts selects for late egg-laying behavior in cuckoos

Studies have shown that brood parasites lay their eggs early in the egg-laying sequence of their hosts, providing them with the advantage of earlier hatching. However, common cuckoos (Cuculus canorus) appear to parasitize the nests of gray bushchat (Saxicola ferreus) during the late egg-laying stage. The bushchat often abandons parasitized nests in the early stages, but not in the late egg-laying stages, thus favoring late egg-laying by cuckoos. In this study, four experiments were conducted to determine whether gray bushchats employ a nest desertion strategy targeted at cuckoo parasitism. The results showed that nest desertion was significantly correlated with parasitism cues and occurred mainly during the hosts' early egg-laying stage. Our study provides the first experimental evidence that nest desertion is an anti-parasitic strategy used by hosts in response to cuckoos. Additionally, our experiments demonstrated that the nest desertion is influenced by the trade-offs of investments in different egg-laying stages.

Random egg laying in host nests, rather than egg-matching, explains patterns of cuckoo parasitism: a comment on Zhang et al. (2023).

Random egg laying in host nests, rather than egg-matching, explains patterns of cuckoo parasitism: a comment on Zhang et al. (2023).

Eggshell spots are an important cue for the egg retrieval behavior in two tit species.

It is a common occurrence for incubating female ground- or cavity-nesting birds to accidentally roll their own eggs out of the nest cup. To correctly roll eggs that are not in the nest cup back to the nest, birds must be able to discriminate between their eggs and things around their nests that could be easily confused for their eggs (e.g., egg-shaped stones or other birds' eggs). Moreover, there may be a strong interaction between egg retrieval and egg rejection behaviors in the context of avian brood parasitism where recognition and rejection of alien eggs is an effective means for hosts to defend against cuckoo parasitism. It has been shown that green-backed tits (Parus monticolus) and Japanese tits (P. minor) in China have strong egg recognition ability and are able to reject nonmimetic eggs in the nest. Eggshell spots play an essential role in the egg rejection behavior of these two tit hosts. This study investigated the egg retrieval behavior of green-backed tits and Japanese tits by adding one experimental egg to the nest corner to explore whether eggshell spots also play a role in the process of egg retrieval. The results revealed significant differences in the retrieval rates of white-rumped munia (Lonchura striata) eggs painted with spots, Japanese tits' own true eggs, and unpainted, pure white-white-rumped munia eggs. The retrieval rate of white-white-rumped munia eggs was significantly lower than that of spotted white-rumped munia eggs and Japanese tits' own spotted eggs. For green-backed tits, the retrieval rate of spotted white-rumped munia eggs in the nest corner was significantly higher than that of pure white-white-rumped munia eggs, while the rejection rate of spotted white-rumped munia eggs was significantly lower than that of pure white-white-rumped munia eggs. These findings indicate that eggshell spots play a key role in the egg retrieval of green-backed tits and Japanese tits.

Repeatable randomness, invariant properties, and the design of biological signatures of identity.

What makes a perfect signature? Optimal signatures should be consistent within individuals and distinctive between individuals. In defense against avian brood parasitism, some host species have evolved "signatures" of identity on their eggs, comprising interindividual variation in color and pattern. Tawny-flanked prinia (Prinia subflava) egg signatures facilitate recognition and rejection of parasitic cuckoo finch (Anomalospiza imberbis) eggs. Here, we show that consistency and distinctiveness of patterns are negatively correlated in prinia eggs, perhaps because non-random, repeatable pattern generation mechanisms increase consistency but limit distinctiveness. We hypothesize that pattern properties which are repeatable within individuals but random between individuals ("invariant properties") allow hosts to circumvent this trade-off. To find invariant properties, we develop a method to quantify entire egg phenotypes from images taken from different perspectives. We find that marking scale (a fine-grained measure of size), but not marking orientation or position, is an invariant property in prinias. Hosts should therefore use differences in marking scale in egg recognition, but instead field experiments show that these differences do not predict rejection of conspecific eggs by prinias. Overall, we show that invariant properties allow consistency and distinctiveness to coexist, yet receiver behavior is not optimally tuned to make use of this information.

Common cuckoos do not mimic the size and shape of host eggs

AbstractOften considered a textbook example of coevolution, common cuckoo (Cuculus canorus) eggs are among the best-studied eggs in the world. Female cuckoos belong to genetically distinct host-races, each laying a specific egg type. When host species evolved to reject cuckoo eggs from their nests, cuckoos evolved better egg color and pattern mimicry. In this study, we asked: have cuckoos also evolved eggs that are well matched to host eggs in size and shape, and is the match better for highly discriminating hosts? We used digital image analysis to quantify the sizes and shapes of ~1230 eggs laid by ten European host species and their respective cuckoo host-races. We found that there is some variation in egg size and shape among host species. By contrast, different cuckoo host-races lay eggs that are—on average—similar in size and shape. This generic “one size and shape fits all” cuckoo egg morph is a poor match to most host egg sizes but a good match to most host egg shapes. Overall, we showed that host discrimination behavior was not correlated with the degree of egg size or shape similarity. We concluded that cuckoo females have not evolved egg size or shape mimicry. Alternative explanations for egg shape similarity include biophysical constraints associated with egg formation and selection for incubation efficiency. Finally, to place our results in a broader context, we compared the egg shapes of the common cuckoo and its hosts to those of three Australian parasitic cuckoo species and their hosts.

Defense behavior of two closely related but geographically distant host species against cuckoo parasitism: A next test for the parallel coevolution.

Interactions between avian brood parasites, such as common cuckoos (Cuculus canorus), and their hosts are one of the best-studied examples of the coevolutionary arms race. Different stages of this arms race can be seen in different races of common cuckoos and their hosts across their range. However, little is known whether selected populations of two closely related but geographically distant species with probably different coevolutionary histories with the common cuckoo are also at different stages of the arms race. In this study, we tested this prediction experimentally using the same non-mimetic model eggs and three-dimensional (3D) printed models of the gray adult common cuckoo (Cuculus canorus). We examined egg recognition and egg rejection and aggression against the common cuckoo in the great reed warbler (Acrocephalus arundinaceus) and Oriental reed warbler (Acrocephalus orientalis), in Slovakia of Europe and northeast China of Asia. The results showed that the great reed warbler exhibited stronger responses to experimental model eggs and 3D models of the common cuckoo than the Oriental reed warbler. We conclude that both the great reed warbler and Oriental reed warbler have well-developed antiparasitic behaviors against common cuckoos in the studied populations, but with different levels of defense intensity, which may be due to local differences in parasitic pressure and the risk of parasitism. This provides an opportunity to study coevolutionary processes between the brood parasite and its hosts together in both species at large geographical scales.

Revealing the roles of egg darkness and nest similarity for a cryptic parasite egg versus host's cognition: an alternate coevolutionary trajectory.

As a text-book example of coevolution, the escalating interactions between egg mimicry by parasitic cuckoos and egg recognition by their hosts constitute a key battlefield for parasitism and anti-parasitism strategies. However, some parasite-host systems have deviated from this coevolutionary trajectory because some cuckoos do not lay mimetic eggs, while the hosts do not recognize them, even under the high costs of parasitism. The cryptic egg hypothesis was proposed to explain this puzzle, but the evidence to date is mixed and the relationship between the two components of egg crypticity, egg darkness (dim egg coloration) and nest similarity (similarity to host nest appearance), remains unknown. Here, we developed a 'field psychophysics' experimental design to dissect these components while controlling for undesired confounding factors. Our results clearly show that both egg darkness and nest similarity of cryptic eggs affect recognition by hosts, and egg darkness plays a more influential role than nest similarity. This study provides unambiguous evidence to resolve the puzzle of absent mimicry and recognition in cuckoo-host systems and explains why some cuckoo eggs were more likely to evolve dim coloration rather than similarity to host eggs or host nests.

Low incidence of cannibalism among brood parasitic cuckoo catfish embryos.

Brood parasites have demanding needs of host resources. Brood parasitic offspring are highly competitive and frequently cause the failure of host broods and the survival of a single parasitic offspring. Accordingly, virulent brood parasites lay a single egg in the same host nest to avoid sibling competition. In the cuckoo catfish (Synodontis multipunctatus), which parasitize mouthbrooding cichlid fishes in Lake Tanganyika, the modes of host and parasite oviposition lead to frequent cases of multiple parasitism. We experimentally tested the prediction that multiple parasitism leads to frequent cannibalism among offspring. Cuckoo catfish embryos prey upon host offspring to obtain nourishment during their 3-week development in the host buccal cavity and may also consume conspecific embryos. The potential benefits of cannibalism in the system are, therefore, twofold; to decrease competition for limited resources (i.e., host brood with rich yolk sacs) and to directly obtain nourishment by consuming rivals. We found that cannibalism indeed provided measurable benefits in terms of increased growth of the cannibals, but cannibalism was rare and typically occurred once all host offspring had been consumed. This implies that cannibalism among cuckoo catfish embryos emerges to mitigate starvation rather than eliminate competition.

Importance of cooperation: How host nest defenses effectively prevent brood parasitism from the cuckoos

As the frontline defense against avian brood parasitism, nest defense is important in reducing nest parasitism and increasing host fitness. However, systematic studies on its effectiveness (i.e., on whether it successfully prevents cuckoo parasitism) are scarce. Based on 214 video recordings from 10 years of field observations, we evaluated the effectiveness of nest defenses of the Oriental reed warbler (Acrocephalus orientalis) in deterring common cuckoo (Cuculus canorus) parasitism. Under a breeding pair situation (≤ 2 hosts individuals), warblers were hardly effective in resisting the egg-laying of the cuckoo and many of the cuckoos under attack were able to complete the parasitic process without being harmed. However, when hosts ≥ 3 individuals, the warblers could effectively thwart the cuckoos and cause lethal damage to the cuckoo in partial cases. This indicated that the host group effectively resisted the cuckoo, demonstrating the importance of cooperation among host neighbors in resisting cuckoo parasitism.

A novel method to collect sperm from brood parasitic cuckoos: Urodeum stimulation (UroS) method

Sperm competition has been studied in numerous species as a representative example of postcopulatory sexual selection, where sampling sperm from male is the most basic and important step. Sperm collection can be tricky in birds, however, because unlike mammals, the genitals of birds are generally latent in the cloacal region and their characteristics vary among species. Various methods to collect sperm from different birds have been tested, such as cloacal massage, feces collection, and electro-stimulation, but their applicability varies depending on species. In this study, we introduced the urodeum stimulation method (UroS method) to collect sperm from Cuculus cuckoos, such as the Common Cuckoo (C. canorus). These species are expected to have interesting patterns of pair bonding and sperm competition because of their unique breeding strategy called brood parasitism; however, it remains unexplored. In this study, we described the application of our new method to expel semen from male common cuckoos, measured the volume of semen collected, checked the presence of sperm in the semen sample, and finally estimated its success rate among 82 males. Samples were successfully collected from 76 cuckoos (approximately 93%) and the colors and volumes of the samples were very diverse. Sperm was present in 43 of these samples (57%), showing a sperm observation rate approximately twice as high as that of the conventional cloacal massage method. We believe that this novel method will contribute to a better understanding of postcopulatory sexual selection in avian brood parasites and facilitate the process of sperm collection and artificial insemination in other medium-sized birds.

The mere presence of cuckoos in breeding area alters egg-ejection decisions in Daurian redstarts

AbstractBrood parasitic cuckoos and their hosts serve as model systems for studying host–parasite coevolution. Egg-rejection behavior constitutes an effective defense against brood parasitism, but some host species show phenotypic plasticity in egg-rejection behavior. Direct exposure to a cuckoo near the nest can increase egg-rejection likelihood, and long-term studies have shown that increased the egg-rejection rates generally correlate with higher parasite prevalence. However, it remains unclear whether such increases result from interactions between parasites and hosts, as these can be surprisingly common, or whether the mere presence of cuckoos in the breeding area is sufficient. Daurian redstarts Phoenicurus auroreus are a common host of the common cuckoo Cuculus canorus that defend against cuckoo parasitism mainly by ejecting the parasitic egg from the nest. This species is unique, as its first breeding attempt of the year takes place before the arrival of cuckoos, excluding the possibility for direct interactions. We simulated the ambient presence of cuckoos or hoopoes Upupa epops (control) in sub-populations of redstarts during their first egg-laying period by presenting taxidermic models and playing back vocalizations. Redstarts in cuckoo-treated plots showed significantly higher egg-ejection rates than individuals in control plots, even though females in both groups were equally likely to recognize the parasitic egg. Among females that did recognize the parasitic egg, those exposed to the cuckoo treatment were more likely to eject it than those exposed to the control treatment. Our results demonstrate unequivocally that the mere presence of cuckoos in the environment is sufficient to provoke egg-ejection behavior.

Breeding near heterospecifics as a defence against brood parasites: can redstarts lower probability of cuckoo parasitism using neighbours?

Breeding habitat choice based on the attraction to other species can provide valuable social information and protection benefits. In birds, species with overlapping resources can be a cue of good quality habitats; species with shared predators and/or brood parasites can increase joint vigilance or cooperative mobbing, while raptors may provide a protective umbrella against these threats. We tested whether the migratory common redstart (Phoenicurus phoenicurus) is attracted to breed near active nests of the great tit (Parus major), a keystone-information source for migrant passerine birds, or a top predator, the northern goshawk (Accipiter gentilis). This system is unique to test these questions because the redstart is a regular host for the common cuckoo (Cuculus canorus). Therefore, we also evaluated other possible benefits coming from the heterospecific attraction, especially in terms of reducing brood parasitism risk. We monitored redstart occupancy rates, onset of breeding, reproductive investment, and followed nest outcomes in terms of brood parasitism, nest predation risk and overall reproductive success. Redstarts avoided breeding near goshawks, but showed neither attraction nor avoidance to breed next to great tits. Both neighbours neither reduced brood parasitism risk nor affected overall nesting success in redstarts. Redstarts may not use heterospecific attraction for settlement decisions, as associations with other species can only exist when some benefits are gained. Thus, environmental cues may be more important than social information for redstarts when breeding habitat choice. Other front-line defence strategies may have a better impact reducing breeding negative interactions, such brood parasitism.

Avian brood parasites, species assemblage, and bird diversity: A case study using a grid-based survey in South Korea

Identifying proper surrogate species or groups is a challenging but critical step in the application of surrogate species approaches in biodiversity conservation because their effectiveness can vary according to biological communities. Recently, the brood parasitic common cuckoo, Cuculus canorus, has been suggested as a surrogate for describing biodiversity, primarily based on its strong parasitic relationship with other host species. However, the efficiency of cuckoo surrogates has been challenged because of the potential limitations of the methodological approaches. Furthermore, its generality rarely has been explicitly tested in other parasitic species with local biodiversity data collected through conventional schemes such as grid-based sampling. Using bird survey data obtained from a grid-based sampling scheme in South Korea, we evaluated the surrogate efficiency of five cuckoo species for bird diversity (species richness and phylogenetic diversity) and generated surrogate species groups. We found that among the five parasitic cuckoo species breeding in South Korea, the common cuckoo and the Indian cuckoo C. micropterus were effective surrogate species. Among these, only the common cuckoo belonged to the best surrogate species group together with its major host species; the Indian cuckoo showed less effective surrogate efficiency than the common cuckoo. In conclusion, our study shows that the common cuckoo, as a single species and a member of a species assemblage, is an effective indicator species for bird diversity in grid-based survey data. However, the result that not all parasitic cuckoo species performed a surrogate role effectively implies that multiple functions may be associated with the surrogate efficiency of brood parasitic cuckoos, along with the importance of host-parasite relationships.

Egg rejection based on egg size recognition as a specific strategy against parasitic cuckoos.

In the coevolutionary interactions between avian brood parasites and their hosts, egg recognition based on color and/or pattern is a common and effective defense to counter parasitism. However, for egg recognition based on size, only a few studies have found affirmative results, and they do not provide unambiguous evidence that egg size recognition in hosts has evolved as an important and specific anti-parasite adaptation against parasite eggs. We studied the brood parasite system between the Asian emerald cuckoo Chrysococcyx maculatus and its host, the chestnut-crowned warbler Phylloscopus castaniceps. The cuckoo parasitizes the warbler using non-mimetic and larger eggs at a parasitism rate of 12.9%. The warbler nests used in this experiment were built in a dark environment with the nest illuminance near 0 lux. Experiments with 2 types of model eggs with colors and patterns resembling cuckoo eggs of different sizes (cuckoo egg size or host egg size) showed that the warblers were able to reject 63.6% of cuckoo model eggs under these dim light conditions. However, model eggs with the same color and pattern similar to the warbler egg size were always accepted. This study provides strong evidence supporting the theory that egg size recognition can be evolved in hosts as a specific anti-parasite adaptation against cuckoos. We suggest that the egg size recognition of the warbler is an outcome of the tradeoff between the costs of violating the parental investment rule and suffering cuckoo parasitism.