Cowbirds, conservation, and coevolution: potential misconceptions and directions for future research

Avian brood parasitism is a model system for studies of coevolution and ecological interactions between parasites and their hosts. However, recent work may have led to misconceptions concerning the Brown-headed Cowbird (Molothrus ater), the most widely studied brood parasitic bird in the world, and its effects on host species. Potential misconceptions about this species that could affect management issues are as follows: cowbird populations are increasing; cowbirds are relatively new to North America; recently exposed hosts are defenseless against parasitism; cowbirds have caused widespread declines of songbirds; and cowbird control is always effective in increasing the size of endangered host populations. Potential coevolutionary misconceptions are that cowbirds are typically 'host tolerant'; cowbirds evict host nestmates; and the mafia effect is widespread. It is important to clarify these issues because such misconceptions could hinder our understanding of parasite-host interactions, and thus obscure the direction of basic research and of management efforts taken to limit cowbird impacts on endangered species. We discuss these issues and suggest future research directions to enhance our understanding of this fascinating species.

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.

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.

Antiparasitic defenses in hosts of South American cowbirds

The cowbirds (Molothrus, Icteridae) are a monophyletic group that includes five extant brood-parasitic species. The Screaming (M. rufoaxillaris), Giant (M. oryzivorus) and Shiny (M. bonariensis) cowbirds range mostly in South America. Screaming and Shiny cowbirds are the ancestral and most recent species of the clade, respectively, therefore, differing in how long they have coevolved with their hosts. We present new experimental data on egg-rejection in a host of the Shiny Cowbird, the House Wren (Troglodytes aedon), review different lines of antiparasitic defenses in hosts of Screaming, Giant and Shiny cowbirds and assess whether hosts of different parasites differ in the type and extent of defenses. Hosts of all three parasites ejected non-mimetic eggs. Most hosts of Giant and Shiny cowbirds were grasp ejectors, whereas the main host of the Screaming Cowbird (the Baywing, Agelaioides badius) ejected parasitic eggs using its feet. Hosts smaller than Shiny Cowbirds neither ejected cowbird eggs nor deserted nests following parasitism. Some hosts also reacted more aggressively towards the parasite. The main host of Screaming Cowbird discriminated against non-mimetic chicks. Our results show that most hosts, regardless of the presumed evolutionary time of interaction with the parasite, have evolved some type of antiparasitic defense.

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.

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.

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.

Could diffuse coevolution explain the generic eggshell color of the brown-headed cowbird?

The brown-headed cowbird(hereafter cowbird)is an avian brood parasite that produces an egg dissimilar to those produced by the majority of its diverse host community.The cowbird’s generic egg may result from a Jack-of-all-trades strategy;however,the evolutionary mechanisms that select for their generic eggs are unclear.Here we propose that the cowbird’s eggshell phenotypes have evolved via diffuse coevolution,which results from community-level selective pressures,rather than via pairwise coevolution that occurs between a particular host species and its brood parasite.Under diffuse coevolution the cowbird’s host community,with varying eggshell phenotypes and recognition abilities,would select for a cowbird eggshell phenotype intermediate to those of its host community.This selection is exerted by hosts that reject cowbird eggs,rather than those that accept them;therefore,we expect cowbird eggshell colors can be approximated by both the phenotypes and rejection abilities of their host community.Here we use eggshell reflectance data from 43 host species to demonstrate that the cowbird eggshell phenotypes are reasonably predicted(within 2 just noticeable differences)by the eggshell phenotypes and rejection rates of their hosts.These findings suggest that cowbird eggshell phenotypes,and potentially those of other some generalist parasites,may evolve via diffuse coevolution.Importantly,this research provides insight into the underlying evolutionary processes that explain observed phenotypic variation and provides a framework for studying selection on both specialist and generalist parasites’traits.

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.