Juan C. Reboreda

Costs of brood parasitism and the lack of defenses on the yellow-winged blackbird: shiny cowbird system

Abstract The shiny cowbird (Molothrus bonariensis) is a generalist brood parasite that lays either white-immaculate or spotted egg morphs in eastern Argentina and Uruguay. Some hosts accept both morphs, others accept spotted eggs and reject the white morph, but no host has been found to accept white eggs and reject spotted ones. It has been suggested that the yellow-winged blackbird (Agelaius thilius) may be that type of host. The finding of a white acceptor-spotted rejector species would help to explain the occurrence and maintenance of the parasite egg polymorphism. We studied the incidence of shiny cowbird parasitism on this host, its costs for their reproductive success and the presence of antiparasitic defenses in the yellow-winged blackbird - shiny cowbird system. The parasite affected the reproductive success of the host in two ways. Cowbirds punctured host eggs causing a reduction in clutch size, and yellow-winged blackbirds deserted their nests whenever they suffered high egg loss. In addition, parasitized nests suffered higher predation during the nestling stage, but not during egg stages, indicating that the difference found was related to the presence of the cowbird chick, and not to higher exposure of parasitized nests to both parasites␣and predators. Despite the costs imposed by the parasite, yellow-winged blackbirds have not evolved antiparasitic defenses. This host did not reject any egg morph of the shiny cowbird nor desert parasitized nests unless it had suffered high egg loss. Current explanations for the host lack of defenses, the “time lag” and the “equilibrium” hypothesis, are discussed.

Brood parasitism of the shiny cowbird, Molothrus bonariensis, on the brown-and-yellow marshbird, Pseudoleistes virescens

We studied the relationship between a generalist brood parasite, the Shiny Cowbird (Molothrus bonariensis) and one of its hosts, the Brown-and-Yellow Marshbird (Pseudoleistes virescens). Seventy-four percent of the nests found were parasitized. Although the parasite lays both white and spotted eggs, most of the cowbird eggs found in the nests of this host were spotted. Artificial parasitism experiments showed that the host rejected the cowbird white eggs. Shiny cowbird parasitism reduced the nesting success of the Brownand-Yellow Marshbird mainly by punctures or cracks of the host eggs. The reduction of the nesting success of the parasite was due mostly to the loss of eggs in multiple parasitized nests. Shiny cowbird chicks were not outcompeted for food although they are smaller than the host chicks. The Brown-and-Yellow Marshbird appears to be a very good host, capable of rearing up to four cowbird chicks in a nest. We compared the nesting success of the Shiny Cowbird in Brown-and-Yellow Marshbird nests with its nesting success in the other sympatric hosts studied.

Brood parasite eggs enhance egg survivorship in a multiply parasitized host

Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests. We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this ‘dilution effect’, comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection.

Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite

Brood parasitism imposes several fitness costs on the host species. To reduce these costs, hosts of avian brood parasites have evolved various defenses, of which egg rejection is the most prevalent. In the face of variable host-parasite mimicry and the costs of egg discrimination itself, many hosts reject only some foreign eggs. Here, we experimentally varied the recognition cues to study the underlying cognitive mechanisms used by the Chalk-browed Mockingbird (Mimus saturninus) to reject the white immaculate eggs laid by the parasitic Shiny Cowbird (Molothrus bonariensis). Immaculate eggs are the only parasite eggs rejected by this host, as it accepts all polymorphic, spotted eggs laid by cowbirds. Using a within-breeding pair experimental design, we tested for the salience of spotting, UV reflectance, and brightness in eliciting rejection. We found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies. The cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.

Nesting success in Brown-and-yellow Marshbirds : Effects of timing, nest site, and brood parasitism

--The Brown-and-yellow Marshbird (Pseudoleistes virescens) is a nonterritorial blackbird with helpers at the nest that inhabits temperate marshy areas and humid grasslands of Argentina, Uruguay, and Brazil. We estimated nesting success of marshbirds throughout the breeding season (late September to mid-December) and analyzed the effects of brood parasitism and nest-site selection (i.e. nesting substrate) on daily survival rates at different stages of the nesting cycle. Most nests were started in November, and these nests had a higher daily survival rate than those initiated in October or December. Only 13.3% of the nests fledged chicks. Predation accounted for 77% of nest losses, whereas the other failures resulted from nest desertion, in most cases after the loss of several eggs. Sixty-five percent of the nests were parasitized by Shiny Cowbirds (Molothrus bonariensis), but brood parasitism did not reduce nest survival. Daily survival rates increased from egg laying and incubation to the brood-rearing stage. Nesting success was three times higher in nests built in native black rushes and pampa grasses than in nests built in two exotic species of thistle. Eighty-nine percent of the nests were built in thistles, which were the most abundant plants in the study area. However, many black rushes and pampa grasses remained unoccupied. Received 6 June 1997, accepted 18 February 1998. FOOD LIMITATION is an important factor that shapes life-history variation in birds (Lack 1968, Drent and Daan 1980). Nesting success, in particular nest predation, also may exert an important influence on life-history variation (Slagsvoid 1982, Martin 1995). Several factors affect nesting success in birds. Most species show a decline in nesting success as the breeding season progresses (Perrins 1970, Daan et al. 1988). This decline is thought to result from seasonal variation in the environment (Hochachka 1990), differences in quality between early and late breeders (Nilsson 1994), or a combination of both factors (Verhulst et al. 1995). The site at which the nest is built affects its detectability and therefore the probability of predation (Best and Stauffer 1980, Martin and Roper 1988). In addition, brood parasitism may influence nesting success in some species. Some hosts abandon the nest when parasitized (Rothstein 1990), whereas others desert the nest as a consequence of egg losses (removals or punctures) caused by the parasite (Zimmerman 1983, Wiley 1985, Sedgwick and Knopf 1988, Hill and Sealy 1994). Moreover, the louder begging calls of some parasite chicks (Briskie et al. 1994, Lichtenstein 1997) could increase E-mail: mermoz@proteus.dna.uba.ar the detection of parasitized nests by predators (Hudson 1874). Predation risk is not constant through the nesting cycle. Most studies of nesting success have found that nest loss is highest during the brood-rearing stage and have attributed these losses to the higher frequency of visits by adults and to the begging activities of nestlings, both of which could make the nest more conspicuous to predators (Skutch 1949, Nice 1957, Redondo and Castro 1992, Schaub et al. 1992). However, a few studies have found that nest loss is highest during the laying and incubation stages (Roseberry and Klimstra 1970, Best and Stauffer 1980). This effect has been attributed to increased nest defense by the parents as the nesting season progresses (Andersson et al. 1980). Several studies have analyzed nest predation in the tropics and in north temperate areas (Skutch 1949, 1985; Martin 1995), but almost no information is available on nesting success in south temperate areas (see Martin 1996). In this paper, we present data on nesting success of the Brown-and-yellow Marshbird (Pseudoleistes virescens) and examine the effects of brood parasitism and nest-site selection on daily survival rates at different stages of the nesting cycle. The Brown-and-yellow Marshbird is an insectivorous blackbird that inhabits marshy areas and

EFFECTS OF CLUTCH SIZE AND TIMING OF BREEDING ON REPRODUCTIVE SUCCESS OF GREATER RHEAS

Greater Rheas (Rhea americana) have an unusual breeding system that com- bines harem-defense polygyny, communal egg laying, and exclusive male parental care. We studied survivorship of eggs and nests in relation to clutch size and timing of breeding and estimated the reproductive success of males and females. The number of eggs in a nest varied from 8 to 56, although in most cases it was between 20 and 30. Nests with more than 30 to 35 eggs had longer laying periods, lost more eggs during incubation, and had lower hatch- ability. As a result, the number of chicks hatched per nest increased with clutch size up to 30 to 35 eggs but decreased for larger clutches. More than 65% of the nests were deserted during incubation, and only 5 to 6% of the male population bred successfully each year. Nest- ing success was inversely correlated with rainfall during the breeding season and positively correlated with time of the breeding season. Chick survival during the first months after hatching averaged 60%. We suggest that the proportion of males that are able to attempt breeding is limited by energetic constraints. Received 16 December 1996, accepted 21 August

A COMPARATIVE STUDY OF SHINY COWBIRD PARASITISM OF TWO LARGE HOSTS, THE CHALK-BROWED MOCKINGBIRD AND THE RUFOUS-BELLIED THRUSH

Abstract It is usually accepted that generalist brood parasites should avoid using hosts larger than themselves because host chicks may outcompete parasite chicks for food. We studied the interactions between the Shiny Cowbird (Molothrus bonariensis) and two common hosts larger than the parasite, the Chalk-browed Mockingbird (Mimus saturninus) and the Rufous-bellied Thrush (Turdus rufiventris). For each host we determined (1) frequency and intensity of parasitism during the breeding season, (2) nesting success, egg survival, hatching success, and chick survival in unparasitized and parasitized nests, and (3) antiparasitic defenses. We also determined Shiny Cowbird egg survival, hatching success, and chick survival in both hosts. Parasitism reached 50% in mockingbirds and 66% in thrushes. In both species the main cost of parasitism was egg destruction through punctures. Hatching success, survival of host chicks, and nest survival did not differ between unparasitized and parasitized nests. Both hosts rejected parasitic white-morph eggs but accepted spotted-morph ones, even though they were significantly smaller than host eggs. The proportion of cowbirds fledged per egg laid in successful mockingbird and thrush nests was 0.4 and 0.6, respectively. Considering nest survival, reproductive success of Shiny Cowbirds was 0.15 in mockingbird nests and 0.17 in thrush nests. These values are similar to or higher than cowbird success with smaller hosts. Our results indicate that host quality is not only determined by host-parasite differences in body size, and that other factors, such as host defenses and nest survivorship, should be considered. Un Estudio Comparado del Parasitismo de Molothrus bonariensis en dos Hospedadores de Gran Tamaño, Mimus saturninus y Turdus rufiventris Resumen. Es aceptado generalmente que los parásitos de cría generalistas deberían evitar utilizar hospedadores de mayor tamaño corporal porque los pichones del hospedador podrían desplazar a sus pichones en la competencia por alimento. Se estudiaron las interacciones entre Molothrus bonariensis y dos hospedadores frecuentes de mayor tamaño que el parásito, Mimus saturninus y Turdus rufiventris. Para cada hospedador se determinó (1) frecuencia e intensidad de parasitismo durante la temporada reproductiva, (2) éxito de nidificación, supervivencia de huevos, éxito de eclosión y supervivencia de pichones en nidos no parasitados y parasitados, y (3) defensas antiparasitarias. También se determinó el éxito reproductivo del parásito en ambos hospedadores. El porcentaje de nidos parasitados fue 50% en Mimus saturninus y 66% en Turdus rufiventris. En ambas especies, el principal costo del parasitismo fue la destrucción de huevos por picaduras. El éxito de eclosión, la supervivencia de pichones y el éxito de nidificación fueron semejantes entre nidos no parasitados y parasitados. Ambos hospedadores rechazaron los huevos parásitos del morfo blanco pero aceptaron los del morfo manchado, si bien éstos fueron de menor tamaño que los del hospedador. La proporción de volantones de Molothrus bonariensis por huevo puesto en nidos exitosos de Mimus saturninus y Turdus rufiventris fue 0.4 y 0.6, respectivamente. Considerando la supervivencia de los nidos, el éxito reproductivo fue 0.15 en Mimus saturninus y 0.17 en Turdus rufiventris. Estos valores son similares o mayores que los reportados para hospedadores de menor tamaño que el parásito. Nuestros resultados indican que la calidad del hospedador no está sólo determinada por las diferencias en tamaño corporal entre el hospedador y el parásito y que otros factores, como defensas del hospedador y supervivencia de los nidos, deberían ser considerados.

COSTS OF EGG PUNCTURES AND PARASITISM BY SHINY COWBIRDS (MOLOTHRUS BONARIENSIS) AT CREAMY-BELLIED THRUSH (TURDUS AMAUROCHALINUS) NESTS

Abstract Most studies on cowbird parasitism have focused on its effects on parasitized nests, whereas few have considered the costs at nests that cowbirds visit but at which they do not lay eggs. Shiny Cowbirds (Molothrus bonariensis) peck and puncture host eggs both in nests where they lay eggs and in unparasitized nests. We analyzed the effect of egg punctures in unparasitized and parasitized nests of a large host, the Creamy-bellied Thrush (Turdus amaurochalinus; hereafter “thrush”), as well as the costs of Shiny Cowbird eggs and chicks in this host’s nests. We determined thrush egg survival, hatching success, and chick survival in successful nests, and nest survival during the egg and nestling stages. Frequency of parasitism was 60%, and its intensity 1.6 ± 0.1 eggs nest−1. Number of host eggs punctured was positively associated with intensity of parasitism. The host’s eggs were frequently punctured in parasitized nests (71%) and in unparasitized nests (42%). Egg punctures reduced the number of eggs at hatching in 23% and 49% of unparasitized and parasitized nests, respectively. Nests with egg punctures had a lower survival rate than nests without them, but nest survival was not associated with parasitism. Presence of a Shiny Cowbird egg was associated with a decrease in the hatching success of host eggs, but presence of a Shiny Cowbird chick did not have any detrimental effect on either the survival and growth rate of host chicks in successful nests or the survival of the whole nest. Our results show that egg punctures were the primary determinant of thrush reproductive success. Consequently, comparison of unparasitized and parasitized nests gives an incomplete estimation of the effects of Shiny Cowbirds on host reproductive success, because the cost of egg punctures is also important in nests where there is no Shiny Cowbird egg laying. Costos de la Perforación de Huevos y el Parasitismo por Molothrus bonariensis en Nidos de Turdus amaurochalinus

Cues used by shiny cowbirds (Molothrus bonariensis) to locate and parasitise chalk-browed mockingbird (Mimus saturninus) nests

Unlike other birds, shiny cowbirds (Molothrus bonariensis) must locate host nests where to lay their eggs and then decide whether to parasitise them. They should also synchronise their laying with that of the host to increase the survival of parasite egg and young. Shiny cowbirds can discover nests using host behaviour as a cue, or by searching the habitat without need for the presence of a host. Besides, they can synchronise parasitism with host laying by monitoring nests during building and laying, or directly by assessing the degree of development of embryos through the puncture of host eggs. Alternatively, synchronization can arise by lower nest attentiveness during host laying. We determined the extent of synchronization between laying of shiny cowbirds and chalk-browed mockingbirds (Mimus saturninus) and estimated if parasitism was negatively associated with host nest attentiveness. We also conducted an experiment to test if host activity was necessary to locate nests, and if puncture of host eggs was a cue for deciding parasitism. Shiny cowbirds synchronised parasitism with host laying in 75% of the cases and synchronization was not explained by lower host nest attentiveness during laying. Shiny cowbirds located nests without need for presence of a host, but the decision of parasitising the nest depended on host activity at the nest. The information that shiny cowbirds could obtain through egg punctures was not necessary for deciding parasitism. Our results indicate that shiny cowbirds rely on the precise timing of their eggs and avoid laying in unsuitable nests.

Egg puncture allows shiny cowbirds to assess host egg development and suitability for parasitism

Parasitic cowbirds and cuckoos generally reduce the clutch size of the hosts they parasitize by removing or destroying some of their eggs. Shiny cowbirds (Molothrus bonariensis) puncture their hosts eggs both when parasitizing the nests and also when they do not parasitize them. We propose that, by puncturing the hosts eggs, shiny cowbirds gain an informational benefit. They assess the degree of development of the hosts embryos and so avoid laying in nests that would not provide enough incubation time for the parasitic eggs to hatch. Two predictions follow: (i) punctures should occur in advance or immediately before parasitic events, and (ii) the occurrence of parasitism should depend on the degree of development of the hosts embryos when punctures occurred, i.e. on the stage of incubation. Both predictions are supported by our data of shiny cowbirds parasitizing yellow–winged blackbirds (Agelaius thilius). Egg punctures are not used to reset the hosts nesting attempt when shiny cowbirds do not parasitize the nests. We discuss the potential mechanisms implicated in egg development assessment and propose a critical experiment to test this hypothesis.