Egg discrimination by hosts and obligate brood parasites:a historical perspective and new synthesis

With the knowledge that cuckoos and cowbirds lay their eggs parasitically,and that some hosts eject parasitic eggs,ornithologists began to ponder the question of how host females discriminate between a foreign egg and their own eggs,wondering how hosts 'know' which egg to remove.Results of one of the rst uncontrolled experiments were inappropriately interpreted to imply ejection was based on discordancy,with hosts simply ejecting the egg in the minority,or the 'odd-looking' egg.Controlled experiments eventually revealed that hosts rst learn the appearance of own their eggs and discriminate between them and any odd egg in their nest,regardless of which egg type is in the minority.Recent work has shown that discordancy may play a role in discrimination by males mated successively with females that lay polymorphic eggs.We examine the details of the early experiments,in light of recent advances in studies of egg recognition.An ability to recognize eggs also has been extended,implicitly,to include obligate brood parasites,as it underlies several hypotheses in explanation of the behavior of parasites toward their hosts.Egg recognition in parasites,however,has not been experimentally con rmed,nor has a mechanism been identi ed by which parasites could discriminate between their own eggs and the other eggs in a nest.We review hypotheses(parasite competition,egg removal and multiple parasitism,ma a,farming) that require the ability of obligate brood parasites to discriminate eggs at di erent levels and the potential mechanisms used by parasites to recognize their own eggs and suggest experiments to test for egg discrimination.An assessment of the egg recognition ability of parasites is germane to our understanding of how parasites counteract defenses of hosts.

Coevolution of acoustical communication between obligate avian brood parasites and their hosts

The mutually antagonistic processes producing adaptations and counter-adaptations in avian brood parasites and their hosts provide a model system for the study of coevolution;this topic has long been an area of focus in ornithology and evolutionary biology.Although there is an extensive body of literature dealing with avian brood parasitism,few empirical studies have considered the effects of the coevolutionary processes associated with brood parasitism on the acoustic characteristics of parent–offspring communication.Under the strong selection pressures associated with brood parasitism,parasitic birds may,for instance,produce deceptive songs.The host may in turn evolve the ability to recognize these sounds as deceptive.At present,the mechanisms underlying the different competitive strategies employed by hosts and parasitic birds remain unclear.Here,we reviewed previous studies that investigated acoustic traits in scenarios of brood parasitism,highlighting possible adaptive functions.Using a meta-analysis,we identified no heterogeneity among studies of begging call adaptations in parasitic nestlings.However,our results may have been affected by the small number of applicable papers available for analysis.Our meta-analysis also suggested that studies of acoustic communication and transmission in adult hosts were highly heterogenous,suggesting that research methods were inconsistent among studies.Finally,we identified knowledge gaps and proposed several lines of future research.

Patterns of host use by a precocial obligate brood parasite, the Black-headed Duck: ecological and evolutionary considerations

The Black-headed Duck (Heteronetta atricapilla) is unique among obligate avian brood parasites because its highly precocial young leave the host nest shortly after hatching and impose no post-hatching costs on their hosts. Accordingly, we might expect host-parasite interactions in this parasite to differ strikingly from those of other brood parasites — they should be able to parasitize a broad diversity of hosts and be highly successful with these hosts. We conducted the second detailed study ever completed on patterns of host use in Black-headed Ducks. Based on four years of systematic searches of multiple marshes in Argentina, we found no evidence that Black-headed Ducks ever had nests of their own, confirming the previous conclusion that Black-headed Ducks are, indeed, true obligate brood parasites. Contrary to expectation, however, we found that Heteronetta is ecologically dependent on a surprisingly small number of host species — two species of coots and a gull — all of which are widespread and locally abundant species. Other species are numerically less important as hosts either because they are relatively uncommon, or because they are avoided by the ducks. In the three main host species, hatching success of the duck eggs was also surprisingly low (≤ 28%), based on expectations for a precocial parasite, mainly due to host rejection or neglect. Mortality due to predation on host nests, in contrast, was low for all three primary host species. These observations corroborate Weller’s observations from a single-year study. The combination of a dependence on few primary hosts and a relatively low hatching success are inconsistent with some previous hypotheses for the evolution of obligate brood parasitism in Heteronetta. Instead, our observations, and those of Weller, suggest that intense nest predation in Austral wetlands, coupled with an abundance of a few common host species that aggressively defend their nests and obtain high nest success rates, may have been an important factor in the evolution of obligate parasitism in this enigmatic duck.

The Brown-headed Cowbird: North America’s avian brood parasite

There are five species of parasitic cowbirds (Molothrus) and the Brown-headed Cowbird (M. ater) is the only widespread species in North America. The Brown-headed Cowbird is a host generalist and is typically found in open habitats and forest edges. The cowbirds are of a more recent origin than many other brood parasites and perhaps as a result, cowbird adaptations for parasitism and their hosts’ counter-adaptations to thwart parasitism do not appear as sophisticated as those of other brood parasite-host systems. Because of its generalist nature, the cowbird has the potential to negatively impact endangered host species whose populations are limited due to anthropogenic habitat loss. As a consequence, the Brown-headed Cowbird is one of the few brood parasitic species that is the subject of control programs to limit its effects on such hosts.

Do brood parasitic Common Cuckoos develop brood patches during the breeding season?

Many birds develop brood patches on their ventral apterium under hormonal regulation to effectively transmit body heat to eggs during incubation.The developed patch has several characteristics,including de-feathering,vascularization,and edema.However,little is known about whether avian brood parasites that do not incubate their eggs exhibit brood patch development during the breeding season.In this study,we measured the size of the ventral apterium in 114 Common Cuckoos(Cuculus canorus)captured in the field throughout the breeding season and examined the appearance of the ventral apterium to confirm the development of brood patches.We also examined whether morphological traits and various factors correlated with the size of the ventral apterium(sternal apterium and abdominal apterium)and how it changed during the breeding season.We found no clear signs of brood patch development in Common Cuckoos captured throughout the breeding season,indicating that they likely did not develop brood patches on the ventral apterium during this period.We also found that ventral apterium size was positively correlated with wing length and body weight.In addition,Common Cuckoos with newly growing feathers on the boundary of the ventral apterium with pteryla were frequently observed as seasons progressed to the end.In conclusion,Common Cuckoos exhibit neither brood patch development nor the vestigial characteristics of ancestral brood patches,except for the growth of feathers on boundary the ventral apterium.Further studies examining brood patches across different groups of avian brood parasites are valuable for enhancing our understanding of the developmental and physiological adaptations of avian brood parasites.

The ghosts of parasitism past:lingering frontline anti-brood parasite defenses in a former host

Coevolutionary arms races between brood parasites and hosts provide tractable systems for understanding antagonistic coevolution in nature;however,little is known about the fate of frontline antiparasite defenses when the host“wins”the coevolutionary arms race.By recreating bygone species interactions,using artificial parasitism experiments,lingering defensive behaviors that evolved in the context of parasitism can be understood and may even be used to identify the unknown agent of parasitism past.Here we present the first study of this type by evaluating lingering“frontline”nest defenses that have evolved to prevent egg laying in a former brood parasite host.The Australian reed warbler Acrocephalus australis is currently not parasitized but is known to exhibit fine-tuned egg discrimination—a defensive behavior indicative of a past brood parasite–host arms race and common in closely related parasitized species.Here,using 3D-printed models of adult brood parasites,we examined whether the Australian reed warbler also exhibits frontline defenses to adult brood parasites,and whether we could use these defenses to identify the warbler’s“ghost of parasitism past.”Our findings provide evidence that the Australian reed warbler readily engages in frontline defenses that are considered adaptive specifically in the context of brood parasitism.However,individuals were unable to discriminate between adults of different brood parasite species at their nest.Overall,our results demonstrate that despite a relaxation in selection,defenses against brood parasitism can be maintained across multiple stages of the host’s nesting cycle,and further suggest that,in accordance with previous findings,that learning may be important for fine-tuning frontline defense.

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.

Why do brood parasitic birds lay strong-shelled eggs?

Brood parasitic birds constitute a model system for the study of coevolution.Such parasites are unique by having evolved unusually thick eggshells for their body size.ick eggshells have been hypothesized to evolve as 1) a means of preventing damage to parasite eggs when the brood parasite lays its egg at a distance from the host clutch(the laying damage hypothesis);2) a consequence of host puncture ejection(the puncture resistance hypothesis);3) a means for the brood parasite to allocate calcium to development of a disproportionately large skeleto-muscular system in evicting parasite chicks(the chick vigour hypothesis);or 4) a means of protecting the cuckoo embryo from microorganisms in the nest of the host(the anti-bacterial protection hypothesis).Here we review the literature studying the evolutionary mechanisms promoting thick eggshells in avian brood parasites,and provide proposals for future studies to test their validity.Available data are insu cient to rigorously test exclusive predictions and assumptions of these not necessarily exclusive hypotheses,although the laying damage and the puncture resistance hypotheses seem to currently be the most well supported alternatives.We discuss how quanti cation of rejection modes(grasp ejection,puncture ejection and desertion) may disclose the validity of the puncture resistance hypothesis,and nally we provide perspectives for future research on testing this speci c hypothesis.

Oriental Reed Warblers do not abandon Common Cuckoo chicks during prolonged nestling periods

The Oriental Reed Warbler(Acrocephalus orientalis)is one of the most commonly used hosts for the parasitic Common Cuckoo(Cuculus canorus).However,as hosts that feed unrelated parasitic nestlings may suffer extra reproductive costs,they may be less willing to care for nestlings that have prolonged nestling periods.To test this hypothesis,the duration of feeding by Oriental Reed Warblers under natural conditions for their own nestlings was compared with the duration of feeding under natural conditions for Common Cuckoo nestlings and for artificially prolonged cuckoo nestlings.The results showed that Oriental Reed Warblers did not starve,drive away,or desert any of the nestlings in the experiment,and neither parent was left alone.Our experimental study indicates that both Oriental Reed Warbler parents were willing to care for nestlings with a prolonged nestling period(up to 30 days,twice the average duration time that the Oriental Reed Warblers fed their own chicks in natural conditions).However,further experiments and observations are required in other host bird species to examine whether both parents or one of the parents may exhibit the behavior of abandoning nestlings with a prolonged nestling period.

Common Cuckoo(Cuculus canorus)nestlings adapt their begging behavior to the host signal system

Common Cuckoos(Cuculus canorus)dependent on parental care for post-hatching demonstrate an intriguing ability to modify their begging vocalizations to ensure maximum care and resources from their interspecific foster parents.Here,we compared begging calls of the Common Cuckoo nestlings fed by four host species,the Grey Bushchat(Saxicola ferreus),Siberian Stonechat(Saxicola maurus),Daurian Redstart(Phoenicurus auroreus),and Oriental Magpie-robin(Copsychus saularis).Results showed that begging calls of the stonechat-,redstart-,and robin-cuckoo resemble those of host species'nestlings in various aspects like low frequency,high frequency,frequency bandwidth and peak frequency,while the bushchat-cuckoo chicks'begging calls were only comparable to their host species in terms of how long they lasted and their peak frequency.In addition,cuckoo nestlings raised in different host nests displayed significant variations in their begging calls in low and peak frequency.This study suggests that cuckoo nestlings do not mimic host species nestlings'begging calls throughout the nestling period,but may tune their begging calls according to host species,while begging calls vary with cuckoo and host species nestlings'ages.Future research should study the parents'reactions to these calls in different host species for a better understanding of the mechanisms underlying such adaptations.

Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand

Different lineages of birds show varying sensitivity to light in the ultraviolet(UV) wavelengths.In several avian brood parasite-host systems,UV-re ectance of the parasite eggs is important in discriminating own from foreign eggs by the hosts.In turn,for parasitic females it may be bene cial to lay eggs into host clutches where eggs more closely match the parasite's own eggs.While the visual sensitivities of numerous cuckoo-and cowbird-host species have been described,less is known about those of their respective parasites.Such sensory characterization is important for understanding the mechanisms underlying potential perceptual coevolutionary processes between hosts and parasites,as well as for better understanding each species' respective visual sensory ecology.We sequenced the short wavelength-sensitive type 1(SWS1) opsin gene to predict the degree of UVsensitivity in both of New Zealand's obligate parasitic cuckoo species,the Shining Cuckoo(Chalcites [Chrysococcyx] lucidus) and the Long-tailed Cuckoo(Urodynamis [Eudynamis] taitensis).We show that both species are predicted to possess SWS1 opsins with maximal sensitivity in the human-visible violet portion of the short-wavelength light spectrum,and not in the UV.Future studies should focus on the(mis)matching in host-parasite visual sensitivities with respect to host-parasite egg similarity as perceived by the avian visual system and the behavioral outcomes of foreign egg rejection.

Linking individual attributes and host specialization in brood parasitic cuckoos

Generalist avian brood parasites vary considerably in their degree of host specialization(e.g.,number of hosts);some parasitize the nests of just a few host species,whereas others exploit more than 100 species.Several factors,including habitat range,habitat type,and geographic location,have been suggested to account for these variations.However,inter-specific differences in individual attributes,such as personality and plasticity,have rarely been considered as potential factors of such variation,despite their potential relationship to,for example,range expansion.Using cage experiments,we tested the hypothesis that parasitic species exploiting more host species may be more active and exploratory.To this end,we quantified behaviors exhibited by two Cuculus cuckoos(Common Cuckoo C.canorus and Oriental Cuckoo C.optatus)that vary greatly in their number of host species.Specifically,we evaluated exploratory behavior displayed by birds in the cage,such as the number of movements,head-turning,wing-flapping,and stepping.The Common Cuckoo,which has a higher number of host species,tended to exhibit higher levels of exploratory behaviors than the Oriental Cuckoo.Our study showed that the two cuckoo species exhibited different exploratory levels,as predicted by the differences in their number of hosts.Further studies regarding the causality between individual attributes and host specialization with improved experimental methodology would greatly enhance our understanding of the role of individual characteristics in the coevolution of avian brood parasites and their hosts.

Australian cuckoos and their adaptations for brood parasitism

The strategies used by parasitic cuckoos to fool their hosts have intrigued naturalists and ornithologists for centuries. Here I review some of the tricks used by Australian parasitic cuckoos to increase host nest availability, access host nests, and fool their hosts into accepting their eggs and chicks. Some of these strategies are widely used by cuckoo species around the world, but other traits, such as cryptic eggs and mimetic chicks, appear to be largely restricted to the Australasian cuckoos. Generalist cuckoos face greater challenges than specialists if they must fool multiple host species, and this provides a possible explanation for why different species of cuckoos have evolved different strategies for host deception.

Avian brood parasitism — a growing research area in behavioral ecology (part Ⅱ)

正We are pleased to publish the second special issue on avian brood parasitism and to be responsible guest editors for the two special issues of Chinese Birds (Vol. 3, No. 4, 2012 and Vol. 4, No. 1, 2013), entitled "Avian Brood Parasitism - A Growing Research Area in Behavioral Ecology". The first issue was published in December 2012. The goal of the two special issues is to publish accumulated knowledge and some of the recent developments

Intra-clutch variation in egg appearance assessed by human vision does not relate to rejection of parasite eggs in Iberian Azure-winged Magpies

e coevolutionary arms race between cuckoos and their hosts predicts that low variation in egg features within a host clutch would facilitate discrimination of mimetic parasite eggs.Here,we experimentally examine this prediction by using arti cial and natural parasite eggs showing contrasting level of matching with host eggs.We quanti ed,based on human assessment,intra-clutch variation in egg appearance and egg discrimination in the Iberian Azure-winged Magpie(Cyanopica cyanus),a presumed former host of the Great Spotted Cuckoo(Clamator glandarius).Azure-winged Magpies rejected parasitic eggs in relation to their degree of dissimilarity with own eggs:Great Spotted Cuckoo model eggs were relatively more o en rejected(73.7%) than real Great Spotted Cuckoo eggs(44.4%) and the less contrasting conspeci c eggs(35.5%).Contrary to our predictions,we found that,irrespective of mimicry level of parasitic eggs,intra-clutch variation in host egg appearance did not di er signi cantly between rejecters and acceptors.We found,however,that individuals with higher variation in egg-size were almost signi cantly more prone to be rejecters than individuals showing lower variation in egg size.Our results do not support the hypothesis that the extent of intraclutch variation in egg discrimination varied with parasite egg mimicry in this particular system,and add to previous ndings suggesting that perhaps an increase in intra-clutch variation in egg appearance,rather than a decrease,might be advantageous when discriminating against non-mimetic Great Spotted Cuckoo eggs.

The 3rd International Symposium on Avian Brood Parasitism

正Invited participants on the 3rd International Symposium on Avian Brood Parasitism, sponsored by Hainan Normal University (HNU), China, Norwegian University of Science and Technology (NTNU), Norway, the Research Council of Norway, and China Ornithological Society (COS).

Timing of breeding as a determinant of nest success of the vulnerable Chestnut Seedeater(Sporophila cinnamomea)in grasslands of southern South America

The breeding traits of Sporophila seedeaters have been relatively well studied in recent years;nevertheless,a group of ten species in the genus,known as southern capuchinos,remain understudied.That is the case with Chestnut Seedeater(Sporophila cinnamomea),a species vulnerable to extinction,which breeds in the grasslands of southeast South America and,after reproduction,migrates towards the Cerrado region in central Brazil.Here,we investigated breeding ecology and calculated average clutch size,productivity,the sex ratio of nestlings,and estimated nest success.Then we tested(1)whether there is a relationship between the number of active nests and environmental variables,(2)whether the nestling sex ratio deviates from the 1:1 ratio,(3)whether clutch size varies between breeding seasons,and(4)whether the nest success is related to starting date,nest age,plant support,nest height from the ground,and clutch size.During two breeding seasons(October-March 2018-2020),we monitored 98 nests.We generated survival models with five interacting covariates to assess the survival of the nests.We recorded the entire breeding period for Chestnut Seedeater,which was estimated to be 4.6 months,similar to other migratory seedeaters.Clutch size did not differ between breeding seasons.The sex ratio of nestlings was not significantly different from the 1:1 ratio.Nest success was 31%,and predation was the leading cause of unsuccessful nests(83%).The daily survival rate was 0.95±0.01.The main predictor of nest survival was the covariate starting date.These findings,added to other aspects of the species’natural history described here,may help illuminate the ecology and behavior of Chestnut Seedeater and other southern endangered capuchinos,and grassland-dependent species of South America.

Impacts of brood parasitism by shiny cowbird Molothrus bonariensis on the breeding success of a small host, the black-backed water tyrant Fluvicola albiventer

The shiny cowbird Molothrus bonariensis parasitizes many species with different life-history traits and has a detrimental effect on the survival of the progeny of the hosts.In response,hosts have developed numerous antiparasitic defenses.Here,we examined the effects of brood parasitism by shiny cowbird on the clutch and brood sizes(83 nests)in a small host,the black-backed water tyrant Fluvicola albiventer.We also studied whether the death of parasite nestlings was related to the care of the foster parents and whether the host had any antiparasitic defense against the shiny cowbird.Our results indicate that brood parasitism significantly decreased the host hatching and fledging successes.The majority of nest failures(57%)were caused by brood parasitism.Shiny cowbird parasitism occurred in 52%of nests and the intensity of parasitism was 1.23±0.53 eggs per parasitized nest.Of the total host eggs,54%were damaged.During the incubation stage,20 nests(47%)were abandoned because of egg punctures by shiny cowbirds females.Only two parasitic fledglings were recorded,while the remaining nestlings either died from starvation(n=12)or predation(n=3).Foster parents abandoned parasitic nestlings between 5 and 10 days old.Our findings demonstrate that the shiny cowbird has very low rates of fledging success when parasitizing black-backed water tyrant.Also,parasitism had a high reproductive cost in the black-backed water tyrant because a very low proportion(7%)of the parasitized nests(n=43)were successful.

Diversity of parasitic cuckoos and their hosts in China

In this exposé we provide the first review of host use by brood parasitic cuckoos in a multiple-cuckoo system in China, based on our own long-term field data and a compilation of observations obtained from the literature. In total, we found that 11 species of cuckoos utilized altogether 55 host species. These hosts belong to 15 families, in which Sylviidae, Turdidae and Timaliidae account for 22.6%, 20.8% and 17.0% of parasitism records, respectively. The Common Cuckoo (Cuculus canorus) had the widest range of host species, accounting for 45.5% of the total number of parasitized species (25 in 10 families) of all parasitism records and is the most frequent brood parasite in the country. Cuckoo species differed in their egg coloration and the extent of egg polymorphism with most of them, e.g. the Common Cuckoo, the Lesser Cuckoo (C. poliocephalus) and the Plaintive Cuckoo (Cacomantis merulinus) laying well mimetic eggs with respect to their hosts based on human being’s visual observations, while others such as the Large Hawk-cuckoo (C. sparverioides), the Himalayan Cuckoo (C. saturatus) and the Asian Emerald Cuckoo (Chrysococcyx maculatus) usually laid non-mimetic eggs. The use of cuckoo hosts and egg color variation in China are compared with those in other parts of their ranges in Asia.

Egg-spot matching in common cuckoo parasitism of the oriental reed warbler: effects of host nest availability and egg rejection

Background: The success of cuckoo parasitism is thought to depend largely on the extent of egg matching between cuckoo and host eggs, since poor-matching cuckoo egg would lead to more frequent egg rejection by the host. In this study, we investigated how egg-spot matching between the Common Cuckoo(Cuculus canorus) and its host, the Oriental Reed Warbler(Acrocephalus orientalis) is affected by the local parasitism rate, nest availability in breeding synchronization and egg rejection.Methods: We used the paired design of parasitized and their nearest non-parasitized nests where breeding occurred simultaneously to compare egg-spot matching. The image analysis was used to compare four eggshell pattern variables, namely spot size, density, coverage on the different areas of egg surface, and the distribution on the whole egg surface. Egg recognition experiments were conducted to test the effect of egg spots on egg rejection by the host.Results: Our results show that much better matching in almost all spot parameters tested on the side of the egg and the spot distribution on the whole egg occurred in parasitized nests than in non-parasitized nests. Matching of spot density between cuckoo and host eggs in parasitized nests increased with the synchronization between temporal availability of nests and the egg-laying period of female cuckoos. Egg recognition experiments in which the warbler eggs were deliberately painted with extra spots led to a significantly higher egg rejection rate(78.3%) than of unpainted eggs.Conclusion: Our data suggest that both the high temporal encounter rate between cuckoo and warbler nests as well as the high egg rejection ability of the host are important factors for egg-spot matching of the cuckoos.