María C. De Mársico

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasites reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.

Chapter 3 – Host Use by Generalist and Specialist Brood-Parasitic Cowbirds at Population and Individual Levels

Abstract We analyzed host use at population and individual levels in the host-generalist shiny cowbird ( Molothrus bonariensis ) and in the host-specialist screaming cowbird ( M. rufoaxillaris ). At the population level, shiny cowbirds were less generalists than previously assumed and host use varied considerably among regions. There was, however, no clear preference for host species, since we found no associations between frequency of parasitism and hosts body mass, type of nest, or genetic distance between host and parasite. Regarding screaming cowbirds, frequency and intensity of parasitism varied among host populations. Parasitic eggs and chicks were equally successful in the primary and secondary hosts, but they experienced high mortality rates when transferred to other suitable, but unused hosts. Screaming and shiny cowbirds overlapped little in host use and had no apparent effect on each others success when reared together in a common host. At the individual level, there was an association between mtDNA haplotypes of shiny and screaming cowbird chicks and the hosts in whose nests they were found, indicating that nest choice by parasitic females is not random. We discuss how host imprinting by females can lead to the formation of host-specific races and how the occurrence of recognition errors and social learning can lead to the colonization of new hosts.

Brood parasitism disproportionately increases nest provisioning and helper recruitment in a cooperatively breeding bird

Obligate avian brood parasites lay their eggs in nests of other species (hosts), which raise parasitic young. Parasitic nestlings are likely to influence host’s parental behaviours as they typically beg for food more vigorously than young host for a given hunger level. However, few studies have tested this idea, with conflicting results. These prior studies were largely limited to biparental hosts, but little is known about the effect of brood parasitism on parental behaviours in hosts that breed cooperatively. We followed a multimodel approach to examine the effect of brood parasitism on nest provisioning and helper recruitment in the baywing (Agelaioides badius), a cooperative breeder parasitised by screaming (Molothrus rufoaxillaris) and shiny (Molothrus bonariensis) cowbirds. Multimodel inference results indicated that feeding visits increased with nestling age, cooperative group size and number of cowbird nestlings in the brood. Brood size had little influence on feeding visits, which further suggests that baywings adjusted their provisioning effort in response to cowbird parasitism. In addition, nests parasitised artificially with shiny cowbird eggs or hatchlings recruited more helpers than unmanipulated nests having only host or screaming cowbird young. Our results provide novel evidence that brood parasitism and cooperative breeding interact in determining the levels of nest provisioning.

A novel method of rejection of brood parasitic eggs reduces parasitism intensity in a cowbird host

The hosts of brood parasitic birds are under strong selection pressure to recognize and remove foreign eggs from their nests, but parasite eggs may be too large to be grasped whole and too strong to be readily pierced by the hosts bill. Such operating constraints on egg removal are proposed to force some hosts to accept parasite eggs, as the costs of deserting parasitized clutches can outweigh the cost of rearing parasites. By fitting microcameras inside nests, we reveal that the Neotropical baywing (Agelaioides badius), a host of the screaming cowbird (Molothrus rufoaxillaris) and shiny cowbird (Molothrus bonariensis), instead circumvents such constraints by kicking parasite eggs out of the nest. To our knowledge, this is the first report of a passerine bird using its feet to remove objects from the nest. Kick-ejection was an all-or-nothing response. Baywings kick-ejected parasite eggs laid before their own first egg and, if heavily parasitized, they ejected entire clutches and began again in the same nest. Few baywings were able to rid their nests of every parasite egg, but their novel ejection method allowed them to reduce the median parasitism intensity by 75 per cent (from four to one cowbird eggs per nest), providing an effective anti-parasite defence.

Reproductive Success and Nestling Growth of the Baywing Parasitized by Screaming and Shiny Cowbirds

Abstract We studied the breeding biology of the Baywing (Agelaioides badius), a shared host of Screaming (Molothrus rufoaxillaris) and Shiny (M. bonariensis) cowbirds. We monitored 193 nests from December 2002 to March 2007 in the Province of Buenos Aires, Argentina. Baywings used a wide variety of nesting sites, mainly old nests of furnarids. Their breeding season lasted from late November to February and was closely matched by that of Screaming Cowbirds. The breeding season for Shiny Cowbirds started in late September but overlapped that of Baywings. Frequency and intensity of Screaming Cowbird parasitism were 93% and 5 eggs per parasitized nest, while for Shiny Cowbirds they were 16% and 1.4 eggs. Host clutch size was 4.0 ± 0.1 eggs and did not vary with time of breeding. Weight at hatching and age of maximum growth were similar for host and Screaming Cowbird nestlings. Shiny Cowbird nestlings had higher weight at hatching and lower age of maximum growth than the other two species. Screaming and Shiny cowbird nestlings had higher growth rates and asymptotic weights than host nestlings. Sex-specific growth curves of Screaming Cowbirds indicated males had higher growth rate and asymptotic weight than females. Only 19% of the nests produced fledglings. Host egg survival, hatching success, and nestling survival were 0.92, 0.88, and 0.94, respectively. Excluding nest failures, hosts fledged 0.78 chicks per egg laid. Baywings were smaller than Screaming and Shiny cowbirds, and experienced a high frequency and intensity of parasitism. However, the effect of parasitism on host hatching success and chick survival was low and comparable to that observed in larger hosts.

Egg-Laying Behavior in Screaming Cowbirds: Why Does a Specialist Brood Parasite Waste so Many Eggs

Abstract Obligate brood parasites should synchronize parasitism with host laying to maximize egg hatchability and chick survival. While the generalist Shiny (Molothrus bonariensis), Brown-headed (M. ater), and Bronzed (M. aeneus) Cowbirds frequently synchronize parasitism with host laying, specialist Screaming Cowbirds (M. rufoaxillaris) very often fail to do so in nests of their main host, the Bay-winged Cowbird (Agelaioides badius). The poor synchronization of Screaming Cowbird parasitism may be the result of low availability of host nests at the time of laying, higher nest attentiveness by the host during laying, or unpredictable host laying behavior. We used a large set of observational data to test these hypotheses. The rate of Screaming Cowbird parasitism occurring during host prelaying was 31%, while during laying and incubation, it was 50% and 19%, respectively. Synchronization of parasitism was not associated with availability of host nests at laying or with changes in host nest attentiveness through the nesting cycle. The length of the prelaying period varied from one to 19 days and was not associated with latency of parasitism after nest completion. Nests with prelaying periods of 4–6 days received fewer eggs than nests with shorter or longer periods. Shiny Cowbirds also parasitized Bay-winged Cowbirds during prelaying more frequently (48%) than in other studied hosts (1%–8%). Our results indicate that Bay-winged Cowbird prelaying behavior precludes synchronization between parasitism and host laying and therefore may act as an antiparasitic defense, as it decreases the incidence of successful parasitism.

Brood Parasitism Increases Mortality of Bay-Winged Cowbird Nests

Abstract. Brood-parasitic cowbirds (Molothrus spp.) can cause total nest failure directly by inducing nest desertion or by destroying the hosts clutch or indirectly by facilitating nest predation. We examined the relationship between brood parasitism and nest survival in the Bay-winged Cowbird (Agelaioides badius), the primary host of the Screaming Cowbird (M. rufoaxillaris) and a secondary host of the Shiny Cowbird (M. bonariensis). We used the program MARK to model daily nest-survival rates, including hypothesized effects of intensity of parasitism, egg losses caused by cowbirds, and total clutch size. Support for each model was evaluated by an information-theoretic approach. More than 50% of the nests failed before incubation was completed, mainly because of the ejection or desertion of parasitized clutches. The model of daily nest survival with best support included the additive effects of intensity of parasitism and number of eggs lost, which were negatively related to nest survival. The model including the effect of clutch size did not receive support. The predicted probability of a nest surviving the entire nesting cycle was 35% for unparasitized nests without egg loss, whereas under the levels of parasitism observed during this study the probability of nest survival varied between 0 and 32%. Nest predation during the egg and nestling stages was positively related to the number of cowbird eggs and chicks, respectively, suggesting that parasitism by Screaming and Shiny Cowbirds may also facilitate depredation of Bay-winged Cowbird nests.

High frequency but low impact of brood parasitism by the specialist Screaming Cowbird on its primary host, the Baywing

Abstract Brood-parasitic cowbirds (Molothrus spp.) exploit the parental care of other species (hosts) that raise their offspring. Parasitism by cowbirds reduces host reproductive success in several ways and quantifying such costs is an important step to better understand evolutionary interactions in host-parasite associations. We estimated the costs of parasitism by the host-specialist Screaming Cowbird (M. rufoaxillaris) to the reproductive success of its primary host, the Baywing (Agelaioides badius). We tested the effect of Cowbird parasitism on egg survival, hatching success, nestling survival and body mass at fledging of Baywings in a population of eastern Argentina where the frequency of parasitism by Screaming Cowbirds exceeds 90% of Baywing nests. Egg survival decreased with the number of Screaming Cowbird eggs laid during the egg-stage and, on average, host clutch-size was reduced by 10% per parasitic event. However, contrary to our expectations, we did not find any clear effect of parasitism on hatching success, nestling survival and body mass at fledging of Baywings. Our results suggest that, despite its high frequency, parasitism by Screaming Cowbirds has a rather little effect on the viability of Baywing offspring. We discuss how clutch rejection behaviour and flexible nest-provisioning rules of the hosts might help to explain this paradoxical result.

Experimental evidence for an antipredatory function of egg rejection behaviour in a common host of the brood-parasitic shiny cowbird

The rejection of foreign eggs is the most effective adaptation against brood parasitism in birds. Many hosts, however, show suboptimal responses towards parasitic eggs, which could reflect a compromise between the benefits and costs of egg rejection. Some large-sized hosts of the shiny cowbird (Molothrus bonariensis) accept any spotted parasite egg but reject a rarer pure white egg morph that occurs only in some parts of the parasite’s distribution. This behaviour is intriguing because it is not an effective defence against parasitism and recent evidences suggest that large-sized hosts could benefit from accepting cowbird eggs as this may dilute the risk of host egg losses at multiply parasitized nests. We studied whether rejection of pure white cowbird eggs can be driven by the increased predation risk of host nests parasitized with this conspicuous egg morph. We conducted a nest predation experiment using artificial clutches placed in natural, inactive nests of a large-sized host, the chalk-browed mockingbird (Mimus saturninus). Clutches consisted of two eggs resembling either one host plus one pure white cowbird egg, one host plus one spotted cowbird egg or two host eggs. Clutches with pure white eggs were more likely to be predated than those having either two host eggs or one host and one spotted cowbird egg, supporting an antipredatory function of egg rejection behaviour in mockingbirds. These results suggest that nest predation could operate as part of larger fitness trade-offs shaping host responses towards foreign eggs. Considering the role of nest predation in the studies of host rejection decisions would help to better understand the evolution and expression of antiparasite defences, especially when the hosts seem to behave suboptimally against costly brood parasitism.Significance statementOne major goal in avian brood parasitism research is to explain the evolution of host defences against parasite eggs and young. Some large-sized hosts of the shiny cowbird (Molothrus bonariensis) show an intriguing behaviour: they accept spotted cowbird eggs but reject a rare pure white egg morph that occurs only in some parts of the parasite’s distribution. Such behaviour provides little protection against parasitism, but it may serve as an antipredatory defence if conspicuous pure white eggs facilitate the detection of host nests to potential predators. Our study supports this idea by showing that pure white eggs increase the risk of nest predation compared to spotted host and cowbird eggs in a common large-sized host, the chalk-browed mockingbird (Mimus saturninus). These findings highlight the importance of considering the role of nest predation in the expression of hosts’ strategies against parasitism.

Host provisioning behavior favors mimetic begging calls in a brood-parasitic cowbird

Brood-parasitic screaming cowbird nestlings manipulate host parent care via a begging call structure that matches that of the host’s own young. Using playback of calls at nests, we investigated the role of begging call structure in stimulating parental provisioning by a host (baywing) to 2 brood parasites. Baywings provisioned more in response to screaming cowbird calls, which closely match those of its own young, than to shiny cowbird calls, which do not.