Brood Parasitism Research Articles

Egg rejection and egg recognition mechanism in a Chinese Azure-winged Magpie (Cyanopica cyanus) population

Recognition and rejection of foreign eggs are effective defense of hosts against brood parasitism. However, brood parasitism can impose various selection pressures on different geographic populations of the same host species. In a multiple cuckoo system in China, Azure-winged Magpies (Cyanopica cyanus) are parasitized by both Indian Cuckoos (Cuculus micropterus) and Asian Koels (Eudynamys scolopaceus). In this study, egg recognition ability and recognition mechanism of the Azure-winged Magpie were investigated using a population in Fusong, southeastern Jilin, China. The results showed that 55.6% (20/36) of the Azure-winged Magpies correctly rejected quail (Coturnix japonica) eggs in their nests, while 13.9% (5/36) of the individuals experienced rejection costs by wrongly rejecting their own eggs. Azure-winged Magpies could accurately reject the experimental eggs when the number of such eggs in the nests was the same as that of the magpie eggs. However, Azure-winged Magpies do not recognize and reject conspecific eggs (0/28). The present study indicates that the Azure-winged Magpie has moderate egg recognition ability toward non-mimetic quail eggs and shows a true recognition mechanism with rejecting foreign eggs by accurately recognizing their own eggs. However, they cannot recognize conspecific eggs.

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.

Egg recognition and nestling discrimination in the Crested Myna (Acridotheres cristatellus): Size matters

Most studies exploring abilities of hosts to detect brood parasitism are based on detecting colour and/or pattern differences among parasitic and host eggs or nestlings, while only few were focused on size differences. True recognition and recognition by discordancy are used to explain cognitive mechanisms of host egg recognition; however, only a few studies have found that hosts use recognition by discordancy. This study investigated: 1) whether egg and nestling recognitions in the Crested Myna (Acridotheres cristatellus) are based on size cues; 2) whether the egg cognitive mechanism is recognition by discordancy based on size cues; and 3) whether the longer the experiment time, the higher the egg recognition rate. Our results showed that the Crested Myna uses egg or nestling size as a recognition cue while the egg and nestling colour and patterning are not associated with egg or nestling rejection, thus the cognitive mechanism of egg recognition in the Crested Myna is recognition by discordancy based on egg size cues. Furthermore, there is a rejection delay in time of egg rejection behaviour of the Crested Myna. Therefore, we suggest that the periodicity of egg rejection experiments could be appropriately extended, especially for species with relatively low egg recognition ability.

Deep Learning-Based Parasitic Egg Identification From a Slender-Billed Gull’s Nest

Intraspecific nest parasitism is a phenomenon that attracts the attention of biologists since it helps in saving the endangered species such as Slender Billed Gull. The problem comes from the fact that a parasite female lays its eggs in the nest of another female (host) of the same species which causes the abandon of the nest by the host. This behavior causes a significant reduction in future birds number and leads to the expansion of this specie. Thus, there has been an urgent necessity to clean the nest from parasitic eggs. So, our aim is to built an automatic parasitic egg identification system based on egg visual features information. Our system uses deep learning models which have proven their success for image classification. Indeed, our system conduct an egg image’s pre-processing phase followed by Fast Beta Wavelet Network (FBWN) to extract the most efficient descriptors (shape, texture, and color). Then, these features will be inputted to the Stacked AutoEncoder for egg classification. Our proposed system, has been evaluated on 91-egg dataset collected from 31 clutches of eggs in Sfax region, Tunisia. Our model has given a parasitic egg identification accuracy of 89.9% which has outperformed the state of the art method and shows the efficiency and the robustness of our system.

Breakeven Points in Nest Management of an Endangered Island Endemic Raptor

ABSTRACT Conservationists often face tradeoffs. We present a tradeoff that we recently faced involving nest management of the endangered Puerto Rican Sharp-shinned Hawk (Accipiter striatus venator). Given our logistical constraints, we determined we were able to either continue our ongoing efforts to induce laying of a second clutch (hereafter, double clutching) of four nests per year, or we could stop double clutching and apply insecticide for parasitic nest flies (Philornis spp.) to as many nests as possible. Observed fledging rates justified our assumptions that the fledging rate of unmanaged nests was approximately one young per nest per year, whereas nests sprayed with insecticide for flies fledged two young, and double-clutched nests fledged three young. These three young from double-clutched nests were a combination of the young from both the parent-raised and hand-raised clutches. Although double clutching is more effective than spraying nests, it is also more labor intensive. We developed a model to determine how many nests we would need to spray to produce the same number of fledglings as if we continued the ongoing double clutching regime. Modeling revealed that if we could find and spray at least eight nests, then cessation of double clutching was justified. We also performed sensitivity analysis and determined that our management conclusion was robust to uncertainty in the assumed values of fledging rates. Our modeling exercise presents an example of informed decision making in the face of uncertainty.

First documented case of Tawny Pipit <em>Anthus campestris</em> nest parasitism by Common Cuckoo <em>Cuculus canorus</em> in Spanish steppes

Interspecific brood or nest parasitism is a relatively common breeding behavior in birds. Through this reproductive tactic, brood-parasites avoid the costs associated with raising and maintaining chicks by laying their eggs in the nests of the host species in which they are specialized. The common cuckoo (Cuculus canorus) follows this brood parasite strategy. Female cuckoos lay their eggs in the nests of other bird species, mimicking egg shape, size, and color of the host species. In this paper we report the first documented case of parasitism of tawny pipit nests by the common cuckoo in Spanish steppe habitats, where no record of parasitism on this species has been reported to date.

Polymorphism at the nestling stage and host-specific mimicry in an Australasian cuckoo-host arms race.

Decades of research have shown that the coevolutionary arms race between avian brood parasites and their hosts can promote phenotypic diversification in hosts and brood parasites. However, relatively little is known about the role of brood parasitism in promoting phenotypic diversification of nestlings. We review field data collected over four decades in Australia, New Caledonia and New Zealand to assess potential for coevolutionary interactions between the shining bronze-cuckoo (Chalcites lucidus) and its hosts, and how diversification at the nestling stage may be generating different subspecies. The shining bronze-cuckoo is a specialist parasite of a few hosts in the family Acanthizidae. It has diversified into subspecies, of which the nestlings closely mimic the respective host nestlings in each region. Additionally, some cuckoo subspecies have polymorphic nestlings. The Acanthizidae hosts have similar breeding and nesting habits and only moderately effective frontline defences against parasitism at cuckoo egg laying or at the egg stages. However, some hosts have developed highly effective defences at the nestling stage by recognising and ejecting cuckoo nestlings from the nest. As with the cuckoo nestlings, some hosts have polymorphic nestlings. The coevolutionary interactions in each region suggest different evolutionary stages of the arms race in which either the parasite or the host is currently in the lead. The presence of moderately effective defences at the egg laying and egg stages might explain why some hosts do not have defences at the nestling stage. The south-Pacific cuckoo - host systems are excellent models to explore the evolutionary mechanisms driving the diversification at the nestling stage in the coevolutionary arms race between avian brood parasites and their hosts.

Fatal mobbing and attack of the common cuckoo by its warbler hosts.

Nest defense is an effective strategy of hosts against parasites. Typically, hosts will aggressively attack brood parasites that approach or visit their nests, which can prevent the parasites from laying eggs or may even lead to the death of the parasites. Few previous studies have specifically reported such fatal cases involving brood parasites and have attributed the cause of death to either drowning or hypothermia after falling into the water following an attack from hosts. In this study, we recorded the process of multiple host individuals of the Oriental reed warbler (Acrocephalus orientalis) mobbing and attacking a female common cuckoo (Cuculus canorus) in the field. We discovered that the immediate cause of the cuckoo's death was the fatal physical damage resulting from the aggressive defense from the hosts, suggesting that frantic pecking and scratching by the hosts is the most proximate cause of mortality among egg-laying female cuckoos. This finding enhances our essential understanding of the effectiveness of host attacks.

Evidence for a chemical arms race between cuckoo wasps of the genus Hedychrum and their distantly related host apoid wasps

BackgroundBrood parasites can exert strong selection pressure on their hosts. Many brood parasites escape their detection by mimicking sensory cues of their hosts. However, there is little evidence whether or not the hosts are able to escape the parasites’ mimicry by changing these cues. We addressed this question by analyzing cuticular hydrocarbon (CHC) profiles of Cerceris and Philanthus wasps and their brood parasites, cuckoo wasps mimicking the CHC profiles of their hosts. Some of these hosts use hydrocarbons to preserve their prey against fungal infestation and thus, they cannot significantly change their CHC composition in response to chemical mimicry by Hedychrum brood parasites.ResultsWe found that the CHC overlap between brood parasites and their hosts was lower in case of host wasps not preserving their prey than in case of prey-preserving host wasps, whose CHC evolution is constrained. Furthermore, the CHC profiles in non-preserving host wasps is more strongly diversified in females than in males, thus in the sex that is chemically mimicked by brood parasites.ConclusionOur results provide evidence for a chemical arms race between those hosts that are liberated from stabilizing selection on their chemical template and their parasites.

Multiple parasitism in an evictor brood parasite: patterns revealed by long-term monitoring, continuous video recording, and genetic analyses

Multiple parasitism in an evictor brood parasite: patterns revealed by long-term monitoring, continuous video recording, and genetic analyses

Bacterial gut microbiomes of aculeate brood parasites overlap with their aculeate hosts', but have higher diversity and specialization.

Despite growing interest in gut microbiomes of aculeate Hymenoptera, research so far focused on social bees, wasps, and ants, whereas non-social taxa and their brood parasites have not received much attention. Brood parasitism, however, allows to distinguish between microbiome components horizontally transmitted by spill-over from the host with such inherited through vertical transmission by mothers. Here, we studied the bacterial gut microbiome of adults in seven aculeate species in four brood parasite-host systems: two bee-mutillid (host-parasitoid) systems, one halictid bee-cuckoo bee system, and one wasp-chrysidid cuckoo wasp system. We addressed the following questions: (1) Do closely related species possess a more similar gut microbiome? (2) Do brood parasites share components of the microbiome with their host? (3) Do brood parasites have different diversity and specialization of microbiome communities compared with the hosts? Our results indicate that the bacterial gut microbiome of the studied taxa was species-specific, yet with a limited effect of host phylogenetic relatedness and a major contribution of shared microbes between hosts and parasites. However, contrasting patterns emerged between bee-parasite systems and the wasp-parasite system. We conclude that the gut microbiome in adult brood parasites is largely affected by their host-parasite relationships and the similarity of trophic food sources between hosts and parasites.

Egg Rejection and Nest Sanitation in an Island Population of Barn Swallows (Hirundo rustica): Probability, Response Latency, and Sex Effects.

Bird nests function as vessels for eggs and nestlings, and an environment for rearing offspring. However, foreign objects falling into bird nests and nestling eggshells may be harmful. Moreover, the smell of fecal sacs increases the risk of detection by predators. Many bird species have evolved nest sanitation to prevent damage to their nests. Furthermore, egg rejection evolved in some birds to thwart brood parasites that lay eggs in their nests. We studied 133 nests of barn swallows (Hirundo rustica) in an island population through a nest content manipulation experiment to determine nest sanitation and egg rejection behaviors and their relationship. Swallows rejected non-egg foreign objects more frequently (100% vs. 58.6%) and sooner than parasite eggs, which supports the hypothesis that nest sanitation is a pre-adaptation to egg rejection. However, nest sanitation did not increase egg rejection, either in probability or latency. Furthermore, both sexes incubated the eggs, cleaned the nests, and removed parasite eggs, implying that both are confronted with natural selection related to nest sanitation and brood parasitism. However, females invested more time in these behaviors than males. This provides evidence for the evolutionary relationship of nest sanitation and egg rejection behaviors in barn swallows.

Non-invasive elevation of circulating corticosterone increases the rejection of foreign eggs in female American robins (Turdus migratorius)

Avian obligate brood parasites rely on other species to raise their offspring. In turn, many brood parasite hosts have evolved defensive behaviors to reduce the costs of brood parasitism, yet the proximate bases underlying these defenses remain poorly understood. Recent studies regarding the potential endocrine mechanisms of foreign-egg rejection have implicated corticosterone as a physiological mediator of anti-parasitic defenses. For example, corticosterone is elevated in response to non-mimetic eggs in an egg rejecter thrush, the Eurasian blackbird (Turdus merula) and this hormone's suppression reduces egg rejection rates in the congeneric American robin (T. migratorius). American robins are also among the few host species of obligate brood parasitic brown-headed cowbirds (Molothrus ater) that readily reject foreign eggs from their nests. We non-invasively elevated corticosterone levels in incubating female robins by dissolving it in DMSO gel which was then applied onto eggs already in the clutch. Relative to controls treated with pure DMSO gel, corticosterone-treated female robins were more likely to reject a non-mimetic, cowbird-sized foreign egg (72 %) than control females (50 %) when accounting for the known effect of lower clutch sizes on greater egg rejection. Future studies are needed to assess the sensory and cognitive impact(s) of corticosterone, as well as other hormones essential for parental care, in this and other hosts' defense behaviors against avian brood parasitism.

Egg Rejection: Getting Rid of a Parasite in the Nest

Some species of birds, called brood parasites, lay their eggs in the nests of other species (called the hosts). Male and female hosts take care of the parasitic offspring. In most cases, the hosts raise only the parasitic chicks, which reduces the breeding success of the host birds. However, hosts can defend themselves from brood parasitism by developing the ability to recognize and reject parasitic eggs from their nests. In this article, we explore how host age influences the ability to reject foreign eggs. We show that female magpies improve their ability to reject foreign eggs added to their nests as they age, and we discuss what this might mean for both the magpies and cuckoos. Our results might ultimately help us to better understand how animals and humans defend themselves against the disease-causing parasites that infect them.

Brood parasitism of Hooded Warblers by Brown-headed Cowbirds: Severe impact on individual nests but modest consequences for seasonal fecundity and conservation

Abstract Brood parasitism by Brown-headed Cowbirds (Molothrus ater) often has pronounced negative effects on host nests. However, the extent to which parasitism reduces annual reproduction and presents conservation challenges for host species is unclear. We address this issue with data from a color-banded population of Hooded Warblers (Setophaga citrina) in Pennsylvania, where Hooded Warblers have increased dramatically despite frequent nest parasitism. Our analysis is based on both an extensive dataset (8 years, 847 nests) on the per-nest impacts of cowbird parasitism and female-based stochastic simulations that accurately reflect the reproductive biology and parasitism rate (30%) of our study population. Cowbird parasitism has multiple negative consequences for Hooded Warbler nests, including (1) reduced host clutch size; (2) increased nest abandonment; (3) increased risk of complete failure due to predation; and (4) in surviving nests increased egg loss, hatching failure, and nestling mortality. We estimate that parasitism reduces success of Hooded Warbler nests 68%, from 1.29 to 0.41 fledglings per nest. For females and populations, however, the consequences of nest parasitism are considerably less extreme; female annual fecundity decreases 25% for each nesting attempt parasitized, and population-level fecundity drops 5.6% for each 10% increase in the frequency of parasitism. These more modest impacts are attributable to (1) steep declines in rates of cowbird parasitism as the nesting season progresses, (2) rapid renesting following abandonment or failure of parasitized nests, and (3) regular double brooding, with second broods initiated in late June and July when the incidence of cowbird parasitism is low. Our results help resolve the paradox of how cowbird parasitism can have both severe consequences for individual host nests but more modest and sustainable conservation impacts on the seasonal fecundity of females and populations. They further underscore the importance of determining population-level effects of brood parasites before investing in costly management efforts.

The Complete Genome Sequence of Protonotaria citrea, the Prothonotary Warbler.

The Prothonotary Warbler (Protonotaria citrea) is a nearctic-neotropical migratory songbird that breeds in forested swamps and riparian areas in the eastern-central United States and southern Ontario. It is the sole eastern North American wood-warbler that nests in cavities, the only species in the genus Protonotaria, and is one of the few hole-nesting hosts of the Brown-headed Cowbird (Molothrus ater), an obligate brood parasite. We present the whole genome sequence of this wood-warbler species. Illumina sequencing was performed on a genetic sample from a single female individual. The reads were assembled using a de novo method followed by a finishing step. The raw and assembled data is publicly available via Genbank: Sequence Read Archive (SRR19579445) and Assembly (JAOYNP000000000).

Reuse of nests in the Great Reed Warbler Acrocephalus arundinaceus: A behavior to save time and energy and to deter nest parasites?

The reproductive period in animals is a demanding part in their life history. In birds, environmental factors, such as adverse weather, predation, or brood parasitism; and/or anthropogenic disturbance, can limit breeding success, resulting in failure of clutches. The nest loss in open‐cup nesting passerines is usually replaced with a new nest with a new clutch, however, in some cases the clutch replacement may occur in unusual forms. In this study, we report on three cases of within‐season nest reuse in the Great Reed Warbler. In the first case, a nest was reused for two times in the same season after unsuccessful nesting attempts (two‐time nest reuse). After the nest was depredated the first time, the female laid new eggs that were depredated again, then again the female laid new eggs that produced four fledglings. In the second case, the first clutch was depredated, after which the female laid a new clutch in the same nest that was again depredated. In the third case, the female laid new eggs among the eggs that failed to hatch previously. Our observations tend not to be consistent with the predator avoidance hypothesis because the depredated nests were reused by the parents. The time/energy saving hypothesis or possible deterrence of nest parasitism could explain nest reuse in this study, but because of low number of nests reused compared to the total number of nests found, this phenomenon needs further clarification.

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.

Interspecific forced copulations generate most hybrids in broadly sympatric ducks

Although rare, hybrids are more common in broadly sympatric waterfowl than in any other avian family; yet, the behavioral ecology explaining their generation has remained controversial. Leading hypotheses are forced interspecific copulations, mis-imprinting caused by mixed broods, and scarcity of conspecific mates. Using a large sample of hybrid ducks solicited from North American hunters we evaluated these hypotheses by genetically determining the mother and father species of F1 hybrids. Based on abundances in areas where their breeding ranges overlap, the frequency of hybrids varied greatly from expectations, with hybrids between species within recently derived clades being much more frequent than those between more divergent clades. Forced copulations, as measured by large phallus-length asymmetries between parentals, strongly predicted the father species of most F1 hybrids. Thus, most Anas acuta x A. platyrhynchos (Northern Pintail x Mallard) F1s were sired by A. acuta, and most A. platyrhynchos x Mareca strepera (Mallard x Gadwall) F1s were sired by A. platyrhynchos. Siring asymmetries were consistent with phallus length asymmetries in five additional parental combinations, but none had samples large enough to be individually statistically significant. The exception to this trend was our sample of nine A. platyrhynchos x Mareca americana (Mallard x Gadwall) F1s, for which a large phallus asymmetry failed to predict the father species. Hybrids were rare in brood parasitic species, suggesting mis-imprinting to be an unlikely cause of most hybrids; however, our samples of hybrids from regular brood parasites were inadequate to strongly address this hypothesis. We could test the scarcity of mates hypothesis for only a single hybrid combination and it contradicted our prediction: most F1 M. Penelope x M. americana (Eurasian x American Wigeon) were sired by M. penelope, strongly contradicting our prediction that female M. penelope wintering in enormous flocks of M. americana (American Wigeon) on the west coast of North America would have difficulty finding conspecific mates. In general, our results support interspecific forced copulations as the predominant behavioral mechanism generating hybrids in North temperate waterfowl.

Niche construction through a Goldilocks principle maximizes fitness for a nest-sharing brood parasite.

Generalist brood parasites that share nests with host nestlings can optimize resource acquisition from host parents by balancing the benefits that host nest-mates provide, including attracting increased provisions to the nest, against the costs of competing with the same host young over foster parental resources. However, it is unclear how parasitic chicks cope when faced with more nest-mates than are optimal for their survival upon hatching. We suggest that, in the obligate brood parasitic brown-headed cowbird (Molothrus ater), chicks use a niche construction strategy and reduce larger, more competitive host broods to maximize the parasites' survival to fledging. We experimentally altered brood sizes to test for Goldilocks principle patterns (i.e. a 'just right' intermediate brood size) of cowbird survival in nests of prothonotary warbler (Protonotaria citrea) hosts. We found that intermediate brood sizes of two host nestlings maximized cowbird fledging success relative to 0 or 4 host nest-mates at hatching. Specifically, cowbird nestlings lowered host brood sizes towards this optimum when placed in broods with more host nestlings. The results suggest that cowbirds reduce, but do not eliminate, host broods as a niche construction mechanism to improve their own probability of survival.