Obligate Brood Parasites Research Articles

Best of a bad job or masters of illusion: Do nest light conditions make the eggs of brood parasitic brown‐headed cowbirds (Molothrus ater) more similar to the eggs of their hosts?

AbstractBrown‐headed cowbirds (Molothrus ater) are generalist obligate brood parasites, laying in the nest of nearly 300 avian species, and successfully parasitizing well over 100 host species. Cowbird eggs are generally considered non‐mimetic, although some have suggested that cowbird eggs resemble several of their host species’ eggs. To date, no investigation has examined the level of avian‐perceived similarity between cowbird and diverse host eggs in the contexts of light characteristics at the nest and the visual system of the relevant viewer. Because the cowbird exploits a wide range of species that lay in a variety of nest types, hosts view these eggs under an array of light conditions which could facilitate or hinder egg discrimination. When considering the visual system of the relevant viewers and the light conditions at their nest, we found that the coloration of cowbird eggs was more similar to host than non‐host species’ eggs. Host responses (whether they accept or reject cowbird eggs) were not statistically different when hosts perceived a large chromatic difference between their own eggs and the cowbird's eggs. Instead, we found that host responses were predicted by the degree to which nesting light conditions facilitated color similarity between host and cowbird eggs, such that hosts typically nesting under light conditions where this color discrimination task was more challenging were more likely to reject cowbird eggs. This suggests that the nesting light environment may have selected for increased coevolved egg recognition abilities in a suite of cowbird host species, even in the absence of parasitic egg color mimicry.

Direct Estimates of Breeding Site Fidelity and Natal Philopatry in Brood Parasitic Brown-Headed Cowbirds Molothrus ater

Avian obligate brood parasitism is a specialised life history strategy that may impact the dispersal of juvenile and adult parasites when compared with non-parasitic (parental) bird species. In contrast to expectations, however, several brood parasites show a territorial spacing system while breeding, including breeding site fidelity within and across years. In comparison, data are sparse on the extent of natal philopatry in brood parasites. We estimated minimum levels of breeding site fidelity and natal philopatry in the generalist parasitic Brown-headed Cowbird Molothrus ater in two subsequent years of colour-ringing known-sexed adults and nestlings. Adults' breeding site fidelity was moderate and similar to previous reports on this species and on other non-parasitic temperate zone passerines. We recorded lower estimates for natal philopatry compared to adult Cowbird breeding site fidelity, but this still fell within the range typically reported for offspring of other North American, migratory, and parental songbirds. These results suggest that social parasitism as a reproductive strategy does not in itself appear to impact patterns of philopatric behaviours of Brown-headed Cowbirds and perhaps other brood parasites.

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.

Environmentally driven escalation of host egg rejection decimates success of an avian brood parasite

Abstract The black-headed duck (Heteronetta atricapilla) of South America is the only known avian obligate brood parasite with precocial offspring. In Argentina, it relies on two species of coots as primary hosts, which typically reject 35–65% of duck eggs. We show that environmentally driven increases in host egg rejection behavior lead to substantial reductions in the reproductive success of the brood parasite. Episodes of flooding and vegetation loss caused dramatic shifts in host egg-rejection behavior, resulting in rejection (85–95%) of almost all duck eggs. Coots respond to fluctuating water levels by building up their nest, raising their own eggs but leaving duck eggs behind. Coots can apparently recognize parasitic duck eggs, but large-scale rejection is triggered only when hosts must actively make a choice. We use a simple population model to illustrate the unique demographic challenges that black-headed ducks face with their parasitic lifestyle and to explore the potential impact of environmentally induced escalation of egg rejection. Using the best available estimates for key vital rates, we show that obligate parasitism may provide a demographically precarious existence for black-headed ducks, even under benign environmental conditions. Environmentally mediated increases in egg rejection rates by hosts could impact significantly the viability of this enigmatic species of brood parasitic duck. Our results demonstrate that egg rejection rates are not fixed properties of host populations or individuals but are strongly influenced by social and ecological factors. Shifts in these environmental drivers could have important and unforeseen demographic consequences for brood parasites.

Facultative brood parasitism by an American Robin (Turdus migratorius) in the nest of a Gray Catbird (Dumetella carolinensis)

Avian brood parasites can be classified as either obligate or facultative. Obligate brood parasites, such as Brown-headed Cowbirds (Molothrus ater), must lay their eggs in the nests of other species because they exhibit no parental care. Although facultative brood parasitism, when species that would normally lay eggs in their own nests dump eggs in the nest of another individual, may occur frequently among conspecifics, facultative interspecific brood parasitism is relatively rare. Here I report on observations made during the breeding season of 2018 of an example of facultative brood parasitism by an American Robin (Turdus migratorius) in the nest of a Gray Catbird (Dumetella carolinensis). Two robin eggs were laid in the nest of the catbird and were successfully raised by the catbird to fledging age. Although the young of obligate brood parasitic cowbirds are rarely raised successfully by catbirds, this is the first documented example, of which I am aware, of a Gray Catbird successfully raising the young of a facultative brood parasite.

Endangered White-breasted Thrashers (Ramphocinclus brachyurus) reject mimetic Shiny Cowbird (Molothrus bonariensis) eggs

Brood parasitism can decrease the reproductive success of host species and contribute to population declines, especially in small populations with naturally low fecundity. The ability of host species to recognize foreign eggs varies, as do the behavioral responses of hosts to brood parasitism. We experimentally tested the ability of a putative host, the White-breasted Thrasher (Ramphocinclus brachyurus), to recognize and reject the eggs of a recently established generalist brood parasite. The White-breasted Thrasher is an endangered songbird restricted to 2 small Caribbean islands that are not known to ever have supported obligate brood parasites. We experimentally parasitized active nests within the stronghold of the species' distribution in Saint Lucia and found that White-breasted Thrashers rejected 83% of mimetic Shiny Cowbird (Molothrus bonariensis) eggs (i.e., wooden eggs painted to look like Shiny Cowbird eggs) within 5 d of being parasitized. Rejection of mimetic eggs was not associated with nest initiation date, distance to habitat edge or agricultural area, nest-attempt number, or presence of helpers or dependent young. We conclude that White-breasted Thrashers can detect foreign eggs and possess behavioral adaptations to counter brood parasitism, and propose that these anti-parasitism traits are likely retained from ancestors that evolved in the presence of brood parasites. Our results suggest that brood parasitism by Shiny Cowbirds is unlikely to become a major threat to the White-breasted Thrasher in Saint Lucia. However, ongoing anthropogenic land alteration is likely to increase contact between the 2 species, warranting continued monitoring of their nascent relationship.

Gut microbiota in a host-brood parasite system: insights from common cuckoos raised by two warbler species.

An animal's gut microbiota (GM) is shaped by a range of environmental factors affecting the bacterial sources invading the host. At the same time, animal hosts are equipped with intrinsic mechanisms enabling regulation of GM. However, there is limited knowledge on the relative importance of these forces. To assess the significance of host-intrinsic vs environmental factors, we studied GM in nestlings of an obligate brood parasite, the common cuckoo (Cuculus canorus), raised by two foster species, great reed warblers (Acrocephalus arundinaceus) and Eurasian reed warblers (A. scirpaceus), and compared these with GM of the fosterers' own nestlings. We show that fecal GM varied between cuckoo and warbler nestlings when accounting for the effect of foster/parent species, highlighting the importance of host-intrinsic regulatory mechanisms. In addition to feces, cuckoos also expel a deterrent secretion, which provides protection against olfactory predators. We observed an increased abundance of bacterial genera capable of producing repulsive volatile molecules in the deterrent secretion. Consequently, our results support the hypothesis that microbiota play a role in this antipredator mechanism. Interestingly, fosterer/parent identity affected only cuckoo deterrent secretion and warbler feces microbiota, but not that of cuckoo feces, suggesting a strong selection of bacterial strains in the GM by cuckoo nestlings.

From micro- to macroevolution: brood parasitism as a driver of phenotypic diversity in birds.

A fundamental question in biology is how diversity evolves and why some clades are more diverse than others. Phenotypic diversity has often been shown to result from morphological adaptation to different habitats. The role of behavioral interactions as a driver of broadscale phenotypic diversity has received comparatively less attention. Behavioral interactions, however, are a key agent of natural selection. Antagonistic behavioral interactions with predators or with parasites can have significant fitness consequences, and hence act as strong evolutionary forces on the phenotype of species, ultimately generating diversity between species of both victims and exploiters. Avian obligate brood parasites lay their eggs in the nests of other species, their hosts, and this behavioral interaction between hosts and parasites is often considered one of the best examples of coevolution in the natural world. In this review, we use the coevolution between brood parasites and their hosts to illustrate the potential of behavioral interactions to drive evolution of phenotypic diversity at different taxonomic scales. We provide a bridge between behavioral ecology and macroevolution by describing how this interaction has increased avian phenotypic diversity not only in the brood parasitic clades but also in their hosts.

Avian Egg Timers: Female Cowbirds Judge Past, Present, and Future When Making Nest Parasitism Decisions

The cognitive demands associated with brood parasitism are substantial. Not only must female parasites locate nests and assess their suitability for parasitism, they must also time parasitism to correspond with the breeding behavior of the host. Keeping track of the reproductive state of hosts for a variety of nests allows the parasite to select a nest where their egg can be incubated successfully. Thus, nest selection decisions are integral to obligate brood parasites’ reproductive success. In captive breeding flocks of brown-headed cowbirds (Molothrus ater), I studied (1) females’ abilities to time a host nest’s readiness for parasitism and (2) the timing of females’ nest selection decisions. I found that cowbirds can attend to the amount of time that elapsed since a host egg was added to a nest and can use that information to choose a nest for parasitism. Females made their choice of nest during prospecting the day before they laid, and, once decided, they did not update their decisions on the day of laying. Taken together, the results reveal that female cowbirds process substantial amounts of information about location, time, number, and rate in order to plan for future parasitism. This research program reveals that species-typical decisions integrate a variety of general and specialized cognitive abilities to allow females to behave adaptively and maximize reproductive success.

Female-female aggression and male responses to the two colour morphs of female common cuckoos

Female-only colour polymorphism is rare in birds, but occurs in brood parasitic cuckoos (Cuculidae). Obligate brood parasites leave incubation and parental care to other species (hosts), so female-female interactions can play a role in how parasites guard critical resources (host nests) within their laying areas. The plumage of adult female common cuckoos (Cuculus canorus) is either rufous (typically rare) or grey (common), whereas adult male conspecifics are monochromatic (grey). In previous studies, hosts and conspecific males responded with less intensity toward the rare female morph in support of a negative frequency-dependent benefit of female plumage polychromatism. Here, we assessed responses of both conspecific females and males to vocal playbacks of female calls, coupled with one of two 3D models of the different morphs of female cuckoos. At our study population, the rufous female morph was as common as the grey morph; therefore, we predicted similarly high rates of conspecific responses in both treatments. Both female and male cuckoos responded to playbacks acoustically, which demonstrated the primary role of acoustic communication in social interactions amongst cuckoos. Following this, some cuckoos flew closer to the models to inspect them visually. As predicted, no significant differences were detected between the live cuckoos’ responses toward the two colour morphs in this population. We conclude that dichromatism in female cuckoos evolved to serve one or more functions other than conspecific signalling.

Endocrine regulation of egg rejection in an avian brood parasite host.

Parasite-host coevolution can lead to novel behavioural adaptations in hosts to resist parasitism. In avian obligate brood parasite and host systems, many host species have evolved diverse cognitive and behavioural traits to recognize and reject parasitic eggs. Our understanding of the evolution and ecology of these defences hinges on identifying the mechanisms that regulate them. We hypothesized that corticosterone, a hormone linked to stress response, vigilance and the suppression of parental behaviour, stimulates the rejection of foreign eggs by brood parasite hosts. We experimentally reduced circulating glucocorticoid levels with mitotane injections in American robins Turdus migratorius and found that the mitotane-treated birds rejected foreign eggs at a lower frequency compared to the sham-treated subjects. This is the first study to causally identify a potential mechanism of a widespread defence behaviour, and it is consistent with egg rejection being mediated by stress physiology.

Absence of anti-parasitic defenses in an Asian population of the magpie, a regular host of the great spotted cuckoo in Europe.

AbstractAntagonistic coevolution such as that between obligate brood parasites and their hosts promotes the evolution of a variety of trickeries that enhance successful rearing of their offspring. They do that by using host parental care to enhance their reproductive success, which in turn selects for host nest defenses or egg rejection. Studying these adaptations and counter-adaptations in different populations helps us to understand the complexity of coevolution between hosts and parasites. Here, we tested for anti-parasite defenses in an Asian population of magpies Pica pica, which is used as a regular host by the great spotted cuckoo Clamator glandarius in Europe. Unlike most magpie populations in Europe, cuckoo parasitism and specific anti-parasite defenses are absent from this Asian population. None of the cuckoos in the Asian population of magpies were capable of exploiting the magpies. That was due to magpies being evictors smaller than cuckoos that could not successfully utilize brood reducing hosts. Thus, the absence of cuckoo parasitism may be due to the absence of non-evictor brood parasites, while the absence of defenses is likely to be explained by the absence of coevolutionary interaction with any brood parasite in both the present and the past.

Examining the disconnect between prolactin and parental care in avian brood parasites.

Prolactin is often referred to as the "parental hormone" but there are examples in which prolactin and parental behavior are disconnected. One intriguing example is in avian obligate brood parasites; species exhibiting high circulating prolactin but no parental care. To understand this disconnect, we examined transcriptional and behavioral responses to prolactin in brown-headed (Molothrus ater) and bronzed (M aeneus) brood parasitic cowbirds. We first examine prolactin-dependent regulation of transcriptome wide gene expression in the preoptic area (POA), a brain region associated with parental care across vertebrates. We next examined prolactin-dependent abundance of seven parental care-related candidate genes in hypothalamic regions that are prolactin-responsive in other avian species. We found no evidence of prolactin sensitivity in cowbirds in either case. To understand this prolactin insensitivity, we compared prolactin receptor transcript abundance between parasitic and nonparasitic species and between prolactin treated and untreated cowbirds. We observed significantly lower prolactin receptor transcript abundance in brown-headed but not bronzed cowbird POA compared with a nonparasite and no prolactin-dependent changes in either parasitic species. Finally, estrogen-primed female brown-headed cowbirds with or without prolactin treatment exhibited significantly greater avoidance of nestling begging stimuli compared with untreated birds. Taken together, our results suggest that modified prolactin receptor distributions in the POA and surrounding hypothalamic regions disconnect prolactin from parental care in brood parasitic cowbirds.

Cross-continental test of natal philopatry and habitat-imprinting hypotheses to explain host specificity in an obligate brood parasite.

Several hypotheses have been proposed to explain the mechanisms responsible for maintenance of host-specific gentes in the common cuckoo (Cuculus canorus). Some of them expect that when adult cuckoos return to lay their eggs to their natal site (natal philopatry hypothesis) or habitat in which they were reared (habitat-imprinting hypothesis), there is a higher probability of finding nests of the host species by which they were reared. Since published evidence is ambiguous, we here evaluate the natal philopatry and habitat-imprinting hypotheses using information on habitat homogeneity and cross-continental long-term ringing data. We found no evidence for the natal philopatry hypothesis-instead of returning to their natal site, juvenile cuckoos exhibited longer dispersal movements than adults, and the difference was even larger in comparison with a wide array of cuckoo host species. On the contrary, we found support for the habitat-imprinting hypothesis-juvenile cuckoos followed similar levels of natal habitat homogeneity at 5- and 25-km scale when returning to breed in the next years. Our results suggest that preference for the particular habitat structures may help cuckoos to find appropriate hosts.

Video recordings of Brown-headed (Molothrus ater) and Shiny (M. bonariensis) cowbirds reveal oviposition from an elevated position: Implications for host–parasite coevolution

Molothrine cowbirds are obligate brood parasites that lay eggs within 5–10 s in the minutes before sunrise. Robust analysis of their position at laying has therefore only been made possible with the development of high-resolution and low-light video recording technologies. From video recordings, we observed the moment of oviposition clearly in 8 and 31 instances of egg laying by Brown-headed (Molothrus ater) and Shiny (M. bonariensis) cowbirds, respectively. Both species laid from an elevated position such that their eggs dropped into nests from an estimated height of 4–8 cm. We propose this elevated laying position has selected for high eggshell strength in cowbirds, because stronger eggshells would be less likely to be damaged during egg laying. Stronger eggshells might also damage other eggs when dropped into the nest, thereby further reducing nestling competition from nest mates and drive selection for cowbird eggshell strength. A role for laying position in the evolution of cowbird egg strength is not mutually exclusive of the view that thickly shelled eggs have evolved as a defense to egg rejection by hosts and/or egg puncture behavior of cowbirds.

Plate f of the Gundestrup “cauldron”: symbols of spring and fertility

The Gundestrup “cauldron” is a late Iron-Age silver ceremonial vessel found in Denmark in 1891. The busts depicted on the seven outer-plates – one is missing – are thought to represent deities but have not been confidently identified. This paper identifies the species of the birds on plate f and its symbolism allowing identification of the deity, the depicted event and its religious significance. The birds have the distinctive zygodactyl foot-morphology of the common cuckoo (Cuculus canorus Linnaeus, 1758). This species is also identified on a number of other widespread European artifacts where it was previously thought to be a bird of prey. The plate depicts a goddess in triplicate flanked by two cuckoos releasing the first cuckoo of spring. The bird is an obligate brood-parasite, laying its eggs in other birds' nests, leading to misconceptions of its life cycle: no females, nests or identifiable eggs. It was assumed the male birds mated with the host females. Hence, the cuckoo symbolized male fertility across its Eurasian summer range and was associated with several widespread European goddesses of fertility who were probably also associated with mead and the planet Venus. The evidence presented strongly suggests that these deities were known in the Bronze Age.

Economic and emission dispatch using cuckoo search algorithm

<p class="Default">The economic dispatch problem of power plays a very important role in the exploitation of electro-energy systems to judiciously distribute power generated by all plants. This paper proposes the use of Cuckoo Search Algorithm (CSA) for solving the economic and Emission dispatch. The effectiveness of the proposed approach has been tested on 3 generator system. CSA is a new meta-heuristic optimization method inspired from the obligate brood parasitism of some cuckoo species by laying their eggs in the nests of other host birds of other species.The results shows that performance of the proposed approach reveal the efficiently and robustness when compared results of other optimization algorithms reported in literature</p>

Non-mimetic shiny cowbird nestlings escape discrimination by baywings in absence of host nest mates

Nestlings of obligate brood parasites must obtain resources from heterospecific hosts that are attuned to the solicitation behaviours of their own progeny. Failing to match the appropriate stimuli may result in suboptimal provisioning or even the starvation of parasite young. Parasitic nestlings could overcome it by sharing the nest with host young, as long as they are able to compete efficiently for parental feedings. Here, we examined if non-mimetic shiny cowbird (Molothrus bonariensis) nestlings reared alone fail to elicit sufficient parental care from the grayish baywing (Agelaioides badius), a host that discriminates between their own and parasitic nestlings based on species-specific begging cues. We manipulated baywing broods to assess the ability of shiny cowbird nestlings to elicit parental provisioning and survive without host nest mates. Host provisioning rates and survival did not differ between shiny cowbirds reared alone and host nestlings in singleton broods. Also, growth patterns of experimental nestlings reared alone were similar to those reported for shiny cowbirds reared alongside baywing young. Hence, we did not find support for the hypothesis that non-mimetic nestlings require the assistance of host nest mates to elicit sufficient parental care from its baywing host. Furthermore, we found that shiny cowbirds that were reared alone continued receiving care from baywings after fledging, unlike shiny cowbirds from mixed broods. Our results add evidence to the idea of opposing selective pressures on the evolution of nest mate acceptance in cowbirds and suggest context-dependent host’s discrimination abilities that deserve further investigation. The evolution of nest mate killing versus tolerance strategies is a long-standing question in the study of brood parasitism. Parasitic nestlings may benefit from sharing the nest with host young if they collectively induce more parental provisioning and the parasite can benefit from it. Host nest mates could also confer protection against discrimination when hosts respond preferentially to stimuli of their own kind. We examined this idea in a generalist brood parasite, the shiny cowbird (Molothrus bonariensis), and a host able to discriminate species-specific begging cues. The results showed that shiny cowbirds reared alone performed well and circumvent host discrimination also after leaving the nest. Our study supports the existence of trade-offs on the evolution of nest mate killing behaviours and adds evidence that context-dependent host’s discrimination abilities similar to those observed towards parasitic eggs can be at play towards parasitic fledglings.

Reducing the conservation reliance of the endangered Kirtland's warbler through adaptive management

ABSTRACTSpecies are considered conservation‐reliant when their continued existence is dependent on human assistance. Conservation reliance challenges the conservation community in terms of their ability to sustain the funding and public‐private partnerships needed for indefinite management. Although increased funding for conservation is critical, reducing conservation reliance through adaptive management represents an attractive alternative. We used a large‐scale ecological experiment as a case study in the use of adaptive management to reduce conservation reliance. For >40 years, the United States Fish and Wildlife Service has trapped and lethally removed an obligate brood parasite, the brown‐headed cowbird (Molothrus ater), to protect the Kirtland's warbler (Setophaga kirtlandii) from the negative effects that brood parasitism has on its reproductive success. To determine if the conservation reliance of the Kirtland's warbler could be reduced through optimization of the cowbird control program, we used an adaptive management approach. In collaboration with stakeholders, we experimentally reduced cowbird trapping effort across nearly all of the Kirtland's warbler breeding range. We monitored the resulting cowbird abundance and rate of parasitism, and then adjusted the scale of trap reductions based on the previous year's results. Despite reducing (2015–2017) and eventually eliminating (2018) cowbird trapping, we detected only 20 cowbirds (2015–2017) and found that just 4 of 514 (<1%) nests were parasitized (2015–2018). Our results indicate that the cowbird control program can at least temporarily be suspended, thereby reducing conservation reliance in the Kirtland's warbler and freeing funds for other management. We urge the conservation community to consider the use of adaptive management to reduce conservation reliance in other threatened and endangered taxa. © 2019 The Wildlife Society.

Early life-history features associated with brood parasitism in the cuckoo catfish, Synodontis multipunctatus (Siluriformes: Mochokidae).

The cuckoo catfish, Synodontis multipunctatus, is the only known obligate brood parasite among fishes, exploiting the parental care of mouthbrooding cichlids endemic to Lake Tanganyika. Comparisons of this system to brood parasitism in birds may reveal broader principles that underlie the evolution of this life-history strategy in vertebrates. However, little is known about the features of the cuckoo catfish that enable this species to successfully parasitize cichlids. Here, we examine early ontogeny of the cuckoo catfish and compare it to that of its cichlid hosts as well as a non-parasitic congener. We found that cuckoo catfish embryos develop and hatch in advance of host embryos, and begin feeding on cichlid young just as they start to hatch. Overall timing of ontogeny in the cuckoo catfish was found to be similar to that of the substrate-spawning congener Synodontis lucipinnis, suggesting that more rapid development of the cuckoo catfish relative to cichlids is not a unique adaptation to brood parasitism. However, we found that cuckoo catfish progeny exhibit extensive morphological differences from S. lucipinnis, which may represent adaptations to brood parasitism. These life-history observations reveal both similarities and differences between the cuckoo catfish system and brood parasitism in other lineages. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.