Brood Parasitic Birds Research Articles

Highly virulent avian brood-parasitic species show elevated embryonic metabolic rates at specific incubation stages compared to less virulent and non-parasitic species.

As the avian embryo grows and develops within the egg, its metabolic rate gradually increases. Obligate avian brood-parasitic birds lay their eggs in the nests of other species to avoid the costs of parental care, and all but one of these brood-parasitic species are altricial at hatching. Yet the chicks of some altricial brood-parasitic species perform the physically demanding task of evicting, stabbing or otherwise killing host progeny within days of hatching. This implies a need for high metabolic rates in the embryo, just as precocial species require. Using flow-through respirometry in situ, we investigated embryonic metabolic rates in diverse avian brood parasite lineages which either kill host offspring (high virulence) or share the nest with host young (low virulence). High-virulence brood parasite embryos exhibited higher overall metabolic rates than both non-parasitic (parental) species and low-virulence parasites. This was driven by significantly elevated metabolic rates around the halfway point of incubation. Additionally, a fine-scale analysis of the embryos of a host-parasitic pair showed faster increases in metabolic rates in the parasite. Together these results suggest that the metabolic patterns of the embryos of high-virulence parasites facilitate their early-life demands.

"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.

Recognition and rejection of foreign eggs of different colors in Barn Swallows

Brood parasitic birds lay eggs in the nests of other birds, and the parasitized hosts can reduce the cost of raising unrelated offspring through the recognition of parasitic eggs. Hosts can adopt vision-based cognitive mechanisms to recognize foreign eggs by comparing the colors of foreign and host eggs. However, there is currently no uniform conclusion as to whether this comparison involves the single or multiple threshold decision rules. In this study, we tested both hypotheses by adding model eggs of different colors to the nests of Barn Swallows (Hirundo rustica) of two geographical populations breeding in Hainan and Heilongjiang Provinces in China. Results showed that Barn Swallows rejected more white model eggs (moderate mimetic to their own eggs) and blue model eggs (highly non-mimetic eggs with shorter reflectance spectrum) than red model eggs (highly non-mimetic eggs with longer reflectance spectrum). There was no difference in the rejection rate of model eggs between the two populations of Barn Swallows, and clutch size was not a factor affecting egg recognition. Our results are consistent with the single rejection threshold model. This study provides strong experimental evidence that the color of model eggs can has an important effect on egg recognition in Barn Swallows, opening up new avenues to uncover the evolution of cuckoo egg mimicry and explore the cognitive mechanisms underlying the visual recognition of foreign eggs by hosts.

Host learning selects for the coevolution of greater egg mimicry and narrower antiparasitic egg-rejection thresholds.

Egg rejection is an effective and widespread antiparasitic defense to eliminate foreign eggs from the nests of hosts of brood parasitic birds. Several lines of observational and critical experimental evidence support a role for learning by hosts in the recognition of parasitic versus own eggs; specifically, individual hosts that have had prior or current experience with brood parasitism are more likely to reject foreign eggs. Here we confirm experimentally the role of prior experience in altering subsequent egg-rejection decisions in the American robin Turdus migratorius, a free-living host species of an obligate brood parasite, the brown-headed cowbird Molothrus ater. We then model the coevolutionary trajectory of both the extent of mimicry of host eggs by parasitic eggs and the host's egg rejection thresholds in response to an increasing role of learning in egg recognition. Critically, with more learning, we see the evolution of both narrower (more discriminating) rejection thresholds in hosts and greater egg mimicry in parasites. Increasing host clutch size (number of eggs/nest) and increasing parasite load (parasitism rate) also have narrowing effects on the egg-rejection threshold. Together, these results suggest that learning from prior experience with egg rejection may play an important role in the coevolution of egg-mimetic lineages of brood parasites and the refined egg rejection defenses of hosts.

Imprinting in an interspecific brood parasitic bird.

Many animals learn to recognize conspecifics after an early experience with them through sexual imprinting. For brood parasitic birds, it is not possible to develop conspecific recognition using cues provided by their foster parents. One solution is that a unique species-specific signal triggers the learning of additional aspects of the conspecific's phenotype. It has been proposed that for brood parasitic cowbirds, this signal is an innate vocalization, the chatter. This vocalization might act in a cross-modal learning process through which juveniles that listen to the song learn to recognize the visual characteristics of the song's producer. We trained two groups of juvenile shiny cowbirds (Molothrus bonariensis). In one group, individuals listened to the chatter or a heterospecific call while they observed a stuffed model of the corresponding species. In the other group, individuals listened to the call of one species (cowbird or heterospecific) while they observed the stuffed model of the other species. In the preference test, juveniles chose the model associated with the chatter, regardless of whether the model was a cowbird or a heterospecific. These results show how the auditory system through a species-specific signal can lead to cross-modal learning of visual cues allowing conspecific recognition in brood parasitic cowbirds.

Automated radio tracking provides evidence for social pair bonds in an obligate brood parasite

Social monogamy predominates in avian mating systems, but this strategy seems unlikely among brood parasites, where the emancipation from parental care should lead to an increase in numbers of mates for both sexes. Despite this, there is great diversity in mating systems in brood parasitic birds. The Screaming CowbirdMolothrus rufoaxillarisis a brood parasite that specializes almost exclusively on one host, the Greyish BaywingAgelaioides badius. Field observations and a radio telemetry study have indicated that male–female pairs spend a great deal of time together through the day, suggesting that they may be socially monogamous. We tested the hypothesis of social monogamy by radio‐tracking male and female Screaming Cowbirds using an array of automated radiotracking receivers to collect data on spatial behaviour and social mating system. Monogamous pair bonds were recorded through social network analysis. These bonds endured throughout the entire breeding season, with males and females remaining associated throughout the day. In accordance with the hypothesis, paired Screaming Cowbirds spent significantly more time in proximity to their mates than to other conspecifics of the opposite sex, and had similar home‐ranges. Social monogamy in the Screaming Cowbird differed markedly from the social polygyny/promiscuity exhibited by the sympatric congener Shiny CowbirdMolothrus bonariensis, a generalist brood parasite.

The location of thrush nests on buildings affects the chance of cowbird parasitism

Nest site placement is a critical choice among passerines, being an important factor that affects their breeding success. In urban areas, human buildings offer suitable nesting sites usually less exposed to predators and brood parasitic birds and readily available to be reused for several breeding seasons. However, the extent to which the features of nest placement sites in buildings contribute to reduce nest detectability by predators and brood parasites is still unknown. Here, we tested whether the features of the nesting site (i.e., lateral concealment, distance to the building ceiling, and height above ground) affect the chance of brood parasitism by Shiny Cowbirds (Molothrus bonariensis) in Pale-breasted Thrushes (Turdus leucomelas) nests placed on buildings in a Brazilian suburban area from 2013 to 2019. Cowbird parasitism increased throughout the study years, and nests closer to ceilings, supposedly better concealed, were more likely to be parasitized. Laying date, height above ground, and lateral concealment were not related to the probability of cowbird parasitism. We suggest that less concealed nests enhance vicinity monitoring by parents, allowing a faster agonistic response to the presence of cowbirds near the nest. Our results indicate that nest site location in cities may have consequences for the breeding success of cowbird hosts.

New cases of facultative interspecific brood parasitism in Black-winged Stilt (Himantopus himantopus) and Eurasian Coot (Fulica atra)

Abstract Many hypotheses try to explain the evolution and possible relations between obligate and facultative brood parasitism in birds. To explore this, a large number of observations and data are needed. Our understanding based on the observations of facultative parasitic species published in the literature is less clear compared to the obligate parasitic species. This communication is about three cases of facultative interspecific brood parasitism. Two nests of Black-headed Gull (Chroicocephalus ridibundus) parasite by Eurasian Coot (Fulica atra) and one nest of Pied Avocet (Recurvirostra avosetta) parasite by Black-winged Stilt (Himantopus himantopus). These observations are significant as long as interspecific brood parasitism was frequently described in Gruiformes (Rallidae) but has rarely observed within Charadriiformes.

The neuroethology of avian brood parasitism

Obligate brood-parasitic birds never build nests, incubate eggs or supply nestlings with food or protection. Instead, they leave their eggs in nests of other species and rely on host parents to raise their offspring, which allows the parasite to continue reproducing throughout the breeding season. Although this may be a clever fitness strategy, it is loaded with a set of dynamic challenges for brood parasites, including recognizing individuals from their own species while growing up constantly surrounded by unrelated individuals, remembering the location of potential host nests for successful reproduction and learning the song of their species while spending time being entirely surrounded by another species during a critical developmental period, a predicament that has been likened to being 'raised by wolves'. Here, I will describe what we currently know about the neurobiology associated with the challenges of being a brood parasite and what is known about the proximate mechanisms of brood parasite evolution. The neuroethology of five behaviors (mostly social) in brood parasites is discussed, including: (1) parental care (or the lack thereof), (2) species recognition, (3) song learning, (4) spatial memory and (5) pair-bonding and mate choice. This Review highlights how studies of brood parasites can lend a unique perspective to enduring neuroethological questions and describes the ways in which studying brood-parasitic species enhances our understanding of ecologically relevant behaviors.

Adult Lesser Cuckoo Cuculus poliocephalus Killing Japanese Bush Warbler Cettia diphone Nestlings

We documented an adult Lesser Cuckoo Cuculus poliocephalus killing nine-day-old Japanese Bush Warbler Cettia diphone nestlings by ejecting them from their nest. Among the available hypotheses concerning brood-parasitic birds destroying host nest contents, only the ‘farming hypothesis’ helps to explain this case, although the attack did not force the warbler to immediately re-nesting because one nestling survived. Considering the long breeding season and frequent re-nesting habit of the Japanese Bush Warbler, as well as the delayed arrival of the Lesser Cuckoo into the breeding area, such predatory behavior seems to be effective in creating replacement clutches for future parasitism.

Pedigree simulations reveal that maternity assignment is reliable in populations with conspecific brood parasitism, incomplete parental sampling and kin structure

Modern genetic parentage methods reveal that alternative reproductive strategies are common in both males and females. Under ideal conditions, genetic methods accurately connect the parents to offspring produced by extra-pair matings or conspecific brood parasitism. However, some breeding systems and sampling scenarios present significant complications for accurate parentage assignment. We used simulated genetic pedigrees to assess the reliability of parentage assignment for a series of challenging sampling regimes that reflect realistic conditions for many brood-parasitic birds: absence of genetic samples from sires, absence of samples from brood parasites and female kin-structured populations. Using 18microsatellite markers and empirical allele frequencies from two populations of a conspecific brood parasite, the wood duck (Aix sponsa), we simulated brood parasitism and determined maternity using two widely used programs, cervus and colony. Errors in assignment were generally modest for most sampling scenarios but differed by program: cervus suffered from false assignment of parasitic offspring, whereas colony sometimes failed to assign offspring to their known mothers. Notably, colony was able to accurately infer unsampled parents. Reducing the number of markers (nine loci rather than 18) caused the assignment error to slightly worsen with colony but balloon with cervus. One potential error with important biological implications was rare in all cases-few nesting females were incorrectly excluded as the mother of their own offspring, an error that could falsely indicate brood parasitism. We consider the implications of our findings for both a retrospective assessment of previous studies and suggestions for best practices for future studies.

Carolina Chickadees (Poecile carolinensis) usurp a Prothonotary Warbler (Protonotaria citrea) nest and fledge a mixed-species brood

Apart from obligate and facultative brood parasitism in birds, mixed-species clutches and broods are uncommon. Competition among birds for limited nest sites can result in antagonistic interactions leading to nest usurpation. When one species evicts and takes over the nest of another it can, on rare occasions, result in a clutch containing eggs of both species. Here I report an instance of Carolina Chickadees (Poecile carolinensis) usurping a Prothonotary Warbler (Protonotaria citrea) nest that resulted in the first documented instance of chickadees fledging a brood containing both chickadee and warbler nestlings. During a nest box study in southern Illinois during 1994–2006, this was the only nesting attempt (n = 6,076) where there was interspecific nest usurpation. In this case, a female chickadee contributed to building the nest cup in the box and laid eggs on 3 of the same days as the female warbler. The chickadee pair usurped the nest from the warblers, and ultimately fledged a mixed brood containing 3 chickadees and 3 warblers. The displaced adult warblers nested in a nearby nest box where they fledged 3 warbler nestlings, subsequently reused the original usurped nest box for an attempt at a second brood after the chickadees' brood fledged, and fledged 5 more warbler nestlings from it. This was not a case of facultative brood parasitism because the warblers were first to start building a nest in the box, only to have the chickadees contribute to nest building before evicting the warblers after there were 3 eggs of each species in the nest. The potential for the Neotropical migrant warbler nestlings/fledglings to mis-imprint on the resident chickadees that raised them likely diminished the warblers' ability to successfully survive their first year of life and/or subsequently mate with other Prothonotary Warblers. The rarity of nest usurpation in this bottomland forest study system suggests that cavities that serve as nest sites are not limiting.

Digest: The interplay between imprinting, mimicry, and multimodal signaling can lead to sympatric speciation†

Mimicry can directly affect the evolutionary history of models, mimics, and signal receivers. Mimics often use multimodal signaling to deceive receivers. Jamie etal. showed that brood parasitic birds display multimodal signaling of mimetic traits triggered by sexual and filial imprinting on host species. These resulting adaptations can interact with premating isolation barriers to strengthen reproductive isolation and potentially drive sympatric speciation.

Empirical evidence of different egg morphs that match host eggs in the brush cuckoo (Cacomantis variolosus)

ABSTRACT One of the most efficient defences against obligate brood parasitism in birds is egg ejection, where a host recognises and removes the parasitic egg from the nest. This defence often selects for egg mimicry in parasitic species to reduce the likelihood of egg ejection. If a parasite uses multiple host species with distinctive egg types, this could lead to the evolution of egg gentes (host-specific egg types) in the parasite. There is observational evidence that the brood parasitic Brush Cuckoo (Cacomantis variolosus) might exhibit egg gentes, but there has been no objective study conducted to determine how closely eggs of this cuckoo species resemble those of its hosts from a bird’s visual perspective. Using objective measurements to quantify egg appearance, we found that Brush Cuckoos exhibit at least two egg morphs that closely match the eggs of two of its primary hosts in colour, luminance and volume. While the determination of actual egg gentes in the Brush Cuckoo was beyond the scope of our study, our results are a first and necessary step in determining whether egg gentes might exist in this species. We suggest at least a third egg morph matching another primary host (or at least the genus of that host) might exist, but more data would be necessary to confirm this. Additionally, we provide a mechanism researchers can use to help distinguish between Brush Cuckoo eggs that are closely matched to their host eggs for future studies in this system.

Spotless starlings prefer spotless eggs: conspecific brood parasites cue on eggshell spottiness to avoid ectoparasites

Avian brood parasites are expected to select host nests according to characteristics that maximize offspring fitness, such as reduced probability of ectoparasitism. Spotless starlings, Sturnus unicolor, lay immaculate blue eggs that sometimes become brownish-spotted due to the activity of the ectoparasitic fly Carnus hemapterus on incubating birds. Therefore, conspecific parasitic females should adaptively avoid parasitizing nests with spotted eggshells. Here, we manipulated perceived risk of ectoparasitism by painting the eggs with either brown spots (similar to those due to ectoparasite activity) or blue spots. A third group of nests was maintained with immaculate eggshells. Nests with nonspotted eggshells showed the highest rate of brood parasitism, while nests with brownish or bluish spots on the eggshells were parasitized at a similar lower rate. These results suggest that brood-parasitic females use the presence of spots on the eggshells in their selection of host nests. This study adds to the scarce evidence showing that brood-parasitic birds select host nests with a low risk of ectoparasitism and demonstrates that colour patterns of the eggshell (i.e. spottiness) of their potential hosts represent a major cue employed to appraise the risk of ectoparasitism.

High-level individuality in vocalizations of a well-known avian brood parasite: Asian koel (Eudynamys scolopacea L.)

ABSTRACT The Asian koel (Eudynamys scolopacea) is a well-known brood parasitic bird that visits Pakistan every summer from India. This species produces at least five loud call types that are presumed to be used in territorial and mating behaviour. We noticed vocal differences among individuals in the wild and hypothesised that Asian koels produce individually distinct vocalizations. To test this, we recorded type 1 cooee calls, coe calls, type 1 coegh calls, type 2 coegh call and wurroo calls from 46 adult birds in the wild, and measured 15 different acoustic parameters, both spectral and temporal, for each vocalization type. We also measured the Potential of Individual Coding (PIC). Parameters having PIC values ≥1.1 were further analysed through stepwise cross-validated discriminant function analysis (DFA). The DFA accurately categorised 86.5% of the type 1 cooee calls, 95.7% of coe calls, 91.5% of the type 1 coegh calls, 82.2% of type 2 coegh calls and 83.3% of wurroo calls to the individuals from which these calls were recorded. Thus, consistent with our hypothesis, our results indicate that Asian koels produce individually distinct calls.

Complex signals alter recognition accuracy and conspecific acceptance thresholds.

Many aspects of behaviour depend on recognition, but accurate recognition is difficult because the traits used for recognition often overlap. For example, brood parasitic birds mimic host eggs, so it is challenging for hosts to discriminate between their own eggs and parasitic eggs. Complex signals that occur in multiple sensory modalities or involve multiple signal components are thought to facilitate accurate recognition. However, we lack models that explore the effect of complex signals on the evolution of recognition systems. Here, we use individual-based models with a genetic algorithm to test how complex signals influence recognition thresholds, signaller phenotypes and receiver responses. The model has three main results. First, complex signals lead to more accurate recognition than simple signals. Second, when two signals provide different amounts of information, receivers will rely on the more informative signal to make recognition decisions and may ignore the less informative signal. As a result, the particular traits used for recognition change over evolutionary time as sender and receiver phenotypes evolve. Third, complex signals are more likely to evolve when recognition errors are high cost than when errors are low cost. Overall, redundant, complex signals are an evolutionarily stable mechanism to reduce recognition errors. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.

An Acoustic Password Enhances Auditory Learning in Juvenile Brood Parasitic Cowbirds.

How does a naive, young animal decide from which adults to learn behavior? Obligate brood parasitic birds, including brown-headed cowbirds (Molothrus ater), face a particular challenge in learning species-specific behaviors; they lay their eggs in the nest of another species, and juveniles are raised without exposure to adult conspecifics. Nevertheless, male cowbirds need to learn a conspecific song to attract appropriate mates, and female cowbirds need to learn to identify conspecific males for mating. Traditionally, it was thought that parasitic bird species rely purely on instinctual species recognition [1-4], but an alternative is that a species-specific trait serves as a "password" [5], a non-learned cue for naive animals that guides decisions regarding from whom to learn. Here, we tested the hypothesis that the adult "chatter call" enhances the learning of specific songs in juvenile cowbirds. We exposed acoustically naive juvenile male and female cowbirds to songs paired with chatter calls and found that the chatter call enhanced song production learning in males and induced a neurogenomic profile of song familiarity in females, even for heterospecific songs. Thus, a combination of experience-independent and -dependent mechanisms converges to explain how young cowbirds emerge from another species' nest yet learn behaviors from conspecifics. Identifying whether such password-based mechanisms relate to perceptual and behavioral learning in non-parasitic taxa will contribute to our general understanding of the development of social recognition systems.

Brood parasitic nestlings benefit from unusual host defenses against botfly larvae (Philornis spp.)

Brood parasitic birds lay their eggs into the nests of other birds, abandoning parental care of their nestlings to the unsuspecting hosts. Parasite and host nestlings may themselves be parasitized by botfly larvae (Philornis: Muscidae), which burrow under the nestlings’ skin and can seriously affect growth and survival. Here, we provide the first direct evidence that adult baywings (Agelaioides badius), the primary host of the specialist brood parasitic screaming cowbird (Molothrus rufoaxillaris), regularly remove botfly larvae from their own and parasitic nestlings by pulling them out of the nestlings’ skin. This is the only bird species known to remove botfly larvae. By combining nestling cross-fostering with video recording of baywing nests, we show that due to prompt removal, infection with botfly larvae had negligible effects on nestling growth and survival despite high prevalence. Our results provide the first direct observations for larva removal behavior in botfly hosts. Screaming cowbirds may benefit from using baywings as its main host, as larva removal by adult baywings reduces the costs of botfly parasitism. Infection by botfly larvae of the genus Philornis (Muscidae) causes nestling mortality in many Neotropical birds. Despite the lethal effects, most Philornis hosts studied so far lack specific defenses against these larvae. The grayish baywing (Agelaioides badius), primary host of the brood parasitic screaming cowbird (Molothrus rufoaxillaris), is the only species that, based on indirect evidence, would be able to remove Philornis larvae from infected nestlings. We provide the first direct evidence that adult baywings do indeed remove botfly larvae from their own nestlings as well as from parasitic cowbird nestlings and that this unusual defense may increase the survival of own and screaming cowbird nestlings at infected nests.

Size matters: shiny cowbirds secure more food than host nestmates thanks to their larger size, not signal exaggeration

Many hosts of obligate brood parasitic birds invest more in parasitic nestlings than they do in their own young. The shiny cowbird, Molothrus bonariensis, a generalist parasite, is fed at a higher proportion than its host nestmates when it is reared in nests of a smaller-bodied host, the house wren, Troglodytes aedon. We test two hypotheses that could account for this differential allocation of food by host parents. The signal exaggeration hypothesis states that cowbird chicks have visual and/or acoustic begging signals that elicit preferential feeding. The size-advantage hypothesis states that hosts preferentially feed large chicks and/or that larger chicks outcompete host chicks in a scramble competition for food. To gain insight into the relative importance of size versus species-specific signals on food allocation by house wrens, we performed audio and video recordings in nests with experimental broods of (1) a 2-day-old cowbird chick and a 2-day-old wren chick (different species, different size), (2) a 2-day-old cowbird chick and an 8-day-old wren chick (different species, same size) and (3) a 2-day-old house wren and an 8-day-old house wren (same species, different size). When cowbirds shared the nest with a same-size wren chick, both chicks received food in equal proportion. In contrast, larger chicks (both cowbirds and wrens) paired with small wren nestmates always received a higher food share. Cowbird begging behaviour and call traits differed from house wrens, but these differences did not always coincide with increased food. We conclude that, at least when cowbird nestlings are young (2 days old), their relatively large size accounts for the larger share of food they receive from house wren hosts, rather than some quality of their begging signal.