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).

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.

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.

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.

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.

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.

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.

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.

Function of note strings in Japanese Tit alarm calls to the Common Cuckoo:a playback experiment

Background: Birds produce alarm calls to convey information about threats. Some Passerine alarm calls consist of several note strings, but few studies have examined their function. Previous studies have shown that Japanese Tits(Parus minor) can alter the calling rate and number and combination of notes in response to predators. We previously found the combinations of note types in Japanese Tit alarm calls to be significantly different in response to the Sparrowhawk(Accipiter nisus) and Common Cuckoo(Cuculus canorus).Methods: Through playback experiments, we tested whether the note strings in Japanese Tit alarm calls to the Common Cuckoo have different functions in conveying information. The note strings of selected alarm calls were divided into the categories of C and D, and different calls were then constructed separately based on the two note string categories. Original alarm calls(C–D), C calls and D calls were played back to male Japanese Tits during the incubation period.Results: Male Japanese Tits had a significantly stronger response to C calls than to C–D calls, and they showed a significantly stronger response to both C and C–D calls than to D calls, suggesting that Japanese Tits discriminated between the C and D calls.Conclusions: Our study demonstrated that the C-and D-category note strings of Japanese Tit alarm calls to the Common Cuckoo have different functions, which supports the previous finding that different note strings in an alarm call can provide different information to receivers. However, the exact meanings of these note strings are not yet known, and further investigation is therefore required.

Comparing vocal structures of the parasitic and nonparasitic groups in Cuculinae

Background: Avian brood parasitism is a breeding strategy in which brood parasites lay their eggs in the nest of other species.This behavior is closely related to aspects of the biological evolution of the parasitic species such as reduced female body size and plumage color polymorphism.However,not much is known whether it is associated with the evolution of vocalization.Methods: We collected samples of the typical male calls of 67 species belonging to the sub?family Cuculinae.Using the calls,we measured five acoustic parameters for each samples to test the differences in vocal structures between parasitic and nonparasitic species.To control for potential phylogenetic effects,we also performed phylogenetic independent contrast analyses.Results: We found that vocal structures were relatively similar among the parasitic species with a tendency to simple and low?frequency calls.In addition,harmonic structures were observed more frequently in the nonparasitic group.Conclusions: Overall,these results support the idea that brood parasitic behavior with associated ecological condi?tions may play a role in vocal evolution,a better understanding of which may greatly improve our knowledge of vocal diversification in non?oscine birds.

Light matters:Nest illumination alters egg rejection behavior in a cavity-nesting bird

Egg discrimination by cavity-nesting birds that build nests under dim light conditions was presumed to depend on nest luminance,although this hypothesis has rarely been tested.Tests of egg discrimination ability by cavity-nesting tits under dim light conditions may reveal the selection pressure from brood parasitism that they encounter under natural interactions.We manipulated the intensity of luminance of nests of the Green-backed Tit(Parus monticolus),a potential cuckoo host that possesses a strong discrimination ability of non-mimetic foreign eggs.We performed experiments to test their egg discrimination ability under different light conditions.Our results showed that Green-backed Tits discriminate against non-mimetic foreign eggs under normal light conditions in nest boxes,and this ability persisted at nest luminance as low as 4.78±1.31 lux that is several times lower than normal luminance(38.11±24.02 lux).However,egg discrimination by Green-backed Tits disappeared when nest luminance was reduced to a minimum of 0.35±0.15 lux.The latter value represents total darkness for humans.The present study shows that nest luminance plays a key role in egg discrimination by Green-backed Tits that build nests under dim light conditions.This study provides strong experimental evidence for nest illumination altering egg rejection behavior in cavity-nesting birds.

Egg recognition in Cinereous Tits(Parus cinereus):eggshell spots matter

Background:Brood parasitic birds such as cuckoos(Cuculus spp.)can reduce their host’s reproductive success.Such selection pressure on the hosts has driven the evolution of defense behaviors such as egg rejection against cuckoo parasitism.Studies have shown that Cinereous Tits(Parus cinereus)in China have a good ability for recognizing foreign eggs.However,it is unclear whether egg spots play a role in egg recognition.The aims of our study were to investigate the egg recognition ability of two Cinereous Tit populations in China and to explore the role of spots in egg recognition.Methods:To test the effect of eggshell spots on egg recognition,pure white eggs of the White-rumped Munia(Lonchura striata)and eggs of White-rumped Munia painted with red brown spots were used to simulate experimental parasitism.Results:Egg experiments showed that Cinereous Tits rejected 51.5%of pure white eggs of the White-rumped Munia,but only 14.3%of spotted eggs of the White-rumped Munia.There was a significant difference in egg recognition and rejection rate between the two egg types.Conclusions:We conclude that eggshell spots on Cinereous Tit eggs had a signaling function and may be essential to tits for recognizing and rejecting parasitic eggs.

Experimental evidence that cuckoos preferentially parasitize host nests early in their laying cycle

Brood parasites,such as the Common Cuckoo(Cuculus canorus),rely on manipulating hosts from other species to raise their offspring.Selection should favor individuals that are able to identify and choose host nests that closely match the incubation stage of their own eggs.While intuitive,and supported by the findings of numerous longterm monitoring studies,experimental evidence of this remains sparse.By using video monitoring,we used three experimental groups to explore whether Common Cuckoos preferentially choose host Oriental Reed Warbler(Acrocephalus orientalis)nests that are early in their laying cycle.We found that Common Cuckoos preferentially parasitize nests of the host Oriental Reed Warbler that are earlier in their laying(less vs.more eggs)or nesting cycle(eggs vs.chicks),and videos of our experiments provide direct insights into their decision making process.Our results provide strong experimental evidence that Common Cuckoos are able to assess nesting stage and strategically choose nests that increase the likelihood of successful parasitism.

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.

Threat recognition and response in an avian brood-parasite host from New Caledonia

Nest predation and avian brood parasitism are the main sources of nest failure in many passerine birds.Large predators threaten both brood and parents,whereas brood parasites pose only a danger to eggs or nestlings.The fan-tailed gerygone Gerygone flavolateralis from New Caledonia is subjected to high rates of nest predation by the New Caledonian crow Corvus moneduloides(responsible for about 20-40%of predation)and moderate rates of brood parasitism by the shining bronze-cuckoo Chalcites lucidus(parasitizing about 18%of nests),which also depredates nests that are too advanced for parasitism(13%of nests).To test if fan-tailed gerygones are able to discriminate predators from brood parasites,we presented 3 bird models at active gerygone nests:a brood parasite/small nest predator(shining bronze-cuckoo),a large nest predator(crow),and a small non-native bird(common chaffinch Fringilla coelebs),which is unknown to the gerygone,as a control.We assessed the response of adult gerygones to the presentation of each model by measuring the minimum approach distance,number of alarm calls,number of attacks,and time to first nest visit after the presentation(latency).Adult gerygones often attacked the cuckoo,approached but never attacked the chaffinch and always avoided the crow.Latency was shorter after an attack response and during brooding,but similar among models.We did not find any link between the cuckoo model presentation and later ejection of cuckoo nestlings.We conclude that adult fan-tailed gerygones discriminate between different models and respond accordingly to the level of threat but do not show awareness of parasitism risk and increase of nestling ejection rates following exposure to the cuckoo model.

Imperfect mimicry of host begging calls by a brood parasitic cuckoo:a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues,and the evolution of visual mimicry of host eggs or chicks by brood parasites.Hosts may also base rejection of brood parasite nestlings on vocal cues,which would in turn select for mimicry of host begging calls in brood parasite chicks.In cuckoos that exploit multiple hosts with different begging calls,call structure may be plastic,allowing nestlings to modify their calls to match those of their various hosts,or fixed,in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages.In our study of the little bronze-cuckoo(LBC)Chalcites minutillus and its primary host,the large-billed gerygone Gerygone magnirostris,we tested whether:(1)hosts use nestling vocalizations as a cue to discriminate cuckoo chicks;(2)cuckoo nestlings mimic the host begging calls throughout the nestling period;and(3)the cuckoo begging calls are plastic,thereby facilitating mimicry of the calls of different hosts.We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching(when rejection by hosts typically occurs)but become less similar as cuckoo chicks get older.Begging call structure may be used as a cue for rejection by hosts,and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks.We found no evidence that LBC begging calls were plastic.

Cognition and the brain of brood parasitic cowbirds

Cowbirds are brood parasites.Females lay their eggs in the nests of other species,which then incubate the cow­bird eggs and raise the young cowbirds.Finding and returning to heterospecific nests presents cowbirds with several cognitive challenges.In some species,such as brown-headed cowbirds(Molothrus ater),females but not males search for and remember the locations of potential host nests.We describe recent research on sex dif­ferences in cognition and the hippocampus associated with this sex difference in search for host nests.Female brown-headed cowbirds perform better than males on some,but not all,tests of spatial memory and females show a pattern of adult hippocampal neurogenesis not found in males or in closely related non-parasitic birds.Because of the apparent specialization of the hippocampus,brown-headed cowbirds may be a good model in which to examine spatial information processing in the avian hippocampus and we also describe recent research on the spatial response properties of brown-headed cowbird hippocampal neurons.