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

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).

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.

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.

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

A fun dame ntal 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 phe no type of species,ultimately gen erating diversity betwee n 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.

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.

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.

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.

Geographic variation in parasitism rates of two sympatric cuckoo hosts in China

Rates of brood parasitism vary extensively among host species and populations of a single host species. In this study, we documented and compared parasitism rates of two sympatric hosts, the Oriental Reed Warbler （Acrocephalus orientalis） and the Reed Parrotbill （Paradoxornis heudei）, in three populations in China. We found that the Common Cuckoo （Cuculus canorus） is the only parasite using both the Oriental Reed Warbler and Reed Parrotbill as hosts, with a parasitism rate of 22.4%-34.3% and 0%-4.6%, respectively. The multiple parasitism rates were positively correlated with local parasitism rates across three geographic populations of Oriental Reed Warbler, which implies that higher pressure of parasitism lead to higher multiple parasitism rate. Furthermore, only one phenotype of cuckoo eggs was found in the nests of these two host species. Our results lead to two conclusions： （1） The Oriental Reed Warbler should be considered the major host of Common Cuckoo in our study sites; and （2） obligate parasitism on Oriental Reed Warbler by Common Cuckoo is specialized but flexible to some extent, i.e., using Reed Parrotbill as a secondary host. Further studies focusing on egg recognition and rejection behaviour of these two host species should be conducted to test our predictions.

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.

Egg rejection behavior does not explain the lack of cowbird parasitism on an eastern North American population of Red-winged Blackbirds

Background:Red-winged Blackbirds(Agelaius phoeniceus),hereafter red-wings,are much less frequently parasitized by Brown-headed Cowbirds(Molothrus ater)in eastern North America than in central North America and had not been recorded as hosts in our study area in southeastern Pennsylvania.Although hosts of Old World cuckoos(Cuculidae)often show geographic variation in egg rejection behavior,cowbird hosts typically exhibit uniform responses of all acceptance or all rejection of cowbird eggs.Thus,geographic variation in cowbird parasitism frequencies might reflect a different behavioral response to parasitism by hosts where only some populations reject parasitism.In this study,we tested whether egg rejection behavior may explain the lack of parasitism observed in our eastern red-wing population,which may provide insight into low parasitism levels across eastern North America.Methods:We parasitized red-wing nests with model cowbird eggs to determine their response to parasitism.Nests were tested across three nest stages and compared to control nests with no manipulations.Because rejection differed significantly by stage,we compared responses separately for each nest stage.We also monitored other songbird nests to identify parasitism frequencies on all potential hosts.Results:Red-wings showed significantly more rejections during the building stage,but not for the laying and incubation stages.Rejections during nest building involved mostly egg burials,which likely represent a continuation of the nest building process rather than true rejection of the cowbird egg.Excluding these responses,red-wings rejected 15%of cowbird eggs,which is similar to rejection levels from other studies and populations.The overall parasitism frequency on 11 species surveyed in our study area was only 7.4%.Conclusions:Egg rejection behavior does not explain the lack of parasitism on red-wings in our eastern population.Alternatively,we suggest that cowbird preference for other hosts and the low abundance of cowbirds in the east might explain the lack of parasitism.Future research should also explore cowbird and host density and the makeup of the host community to explain the low levels of parasitism on red-wings across eastern North America because egg rejection alone is unlikely to explain this broad geographic trend.

First record of Common Tailorbird(Orthotomus sutorius)parasitism by Plaintive Cuckoo(Cacomantis merulinus)in Bangladesh

The Plaintive Cuckoo(Cacomantis merulinus) is a widespread brood parasite in Asia, but no data on host species utilization in Bangladesh exist. By searching for nests of all possible host species of the Plaintive Cuckoo at Jahangirnagar university campus, north of Dhaka, we were able to determine which hosts were used in this area. We found that the Common Tailorbird(Orthotomus sutorius) was the only potential host used by Plaintive Cuckoos, and parasitism rate was rather high(31.3 %, n = 16). However, both host and cuckoo breeding success was poor(0 %, n = 16) due to frequent nest predation. Details on host and cuckoo egg appearance are provided. Our findings indicate that Common Tailorbirds are common hosts of the Plaintive Cuckoo in Central Bangladesh.

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.

Cuckoo parasitism on two closely-related Acrocephalus warblers in distant areas:a case of parallel coevolution?

Common Cuckoos(Cuculus canorus) parasitize nests of small passerines.e Cuckoo chicks cause the death of their nest-mates when evicting eggs or nestlings from the nests;consequently,hosts su er from a high loss of reproduction.Host adaptations against parasitism,e.g.,by egg discrimination behavior,and cuckoo counter-adaptations to hosts,e.g.,by mimetic eggs,are often regarded as a result of the arms race between the two interacting species.In Hungary Great Reed Warblers(Acrocephalus arundinaceus) are the main hosts of cuckoos,su ering from heavy parasitism(ca.40-65%).e Oriental Reed Warbler(A.orientalis),formerly a subspecies of the Great Reed Warbler(A.a.orientalis),is also a highly parasitized host in Japan(25-40%).We compared main characteristics of Cuckoo parasitism in these two distant areas from the Western and Eastern Palearctic by comparing cuckoo egg mimicry.We measured color characteristics of host and parasitic eggs by spectrophotometer.Visual modeling revealed lower chromatic distances between Cuckoo and host eggs in Hungary than in Japan,but high variation both in host and Cuckoo eggs may cause matching problems in Hungary.Achromatic(brightness) di erence between host and Cuckoo eggs were lower in Japan than in Hungary,and it proved to be the most important factor a ecting egg rejection.Hosts rejected Cuckoo eggs at similar frequencies(37% and 35% in Hungary and Japan,respectively).Host adaptation,i.e.,egg rejection behavior,seems to be preceding Cuckoo counter-adaptations to hosts in Japan.We suggest that the Cuckoo-Great/Oriental Reed Warbler relationships developed in alternative ways in Japan and Hungary,and they represent di erent stages of their arms race.

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.

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.

Does landscape structure contribute to the long-term maintenance of generalized parasitism in cowbirds?

Unlike most brood parasites, several species of cowbird (Molothrus) are generalists that parasitize multiple host species across their range and within the same communities; likewise, there is little evidence that individuals within a population specialize on host species. This situation has variously been attributed to the recency of cowbird evolution (the 'evolutionary lag' hypothesis) or to hidden costs of rejection by hosts (the 'equilibrium' hypothesis). Both hypotheses have some support as cowbirds are indeed a relatively young clade compared with more specialized cuckoos and cowbirds are capable of sophisticated behaviors such as retaliation against rejection ('mafia' behaviors) that would select for acceptance of cowbird eggs. Nevertheless, many species in the Americas have evolved specialized defenses against cowbird parasitism, almost all of which live in more open habitats (e. g., grasslands, shrublands, riparian strips), which indicates that coevolutionary processes can operate in ways that select for host defenses in spite of cowbird counterdefenses. We propose that the structure of landscapes in North America may explain why forest-nesting birds lack defenses against parasitism and reinforce the long-term maintenance of generalized brood parasitism in cowbirds. Because cowbirds require open habitats in which to feed, they are rare or absent in large forest tracts, which dominate much of the forest cover of the Americas. These tracts act as 'source habitats' that produce surplus young that recolonize populations in smaller, fragmented forest patches in which rates of both cowbird parasitism and nest predation are very high ('sink' habitats). Evolution of antiparasite adaptations would be very slow in this situation because most hosts are produced in areas where there is little or no cowbird parasitism. In addition, the interplay of host breeding dispersal, source-sink metapopulation dynamics, and fragmented forest habitat could further deter the evolution of host defenses against parasitism. Therefore, as long as large forest tracts remain widespread in North America, most forest birds will likely continue to lack defenses against cowbird parasitism, guaranteeing a steady supply of na ve hosts in forest habitats, even in fragmented landscapes. This situation will, in turn, favor host generalist cowbirds that actively avoid more open habitats in favor of parasitizing forest bird communities. These forest communities may also act as source populations for cowbirds, which might pump surplus generalist cowbirds into more open habitats further slowing the coevolutionary process. As long as large forest tracts are a common part of the landscape, generalist parasitism may persist indefinitely.

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.

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.