Spencer G. Sealy

Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations

The brown‐headed cowbird (Molothrus ater) is a widespread, obligate brood parasite of North American passerine birds. In southern Manitoba, where hosts are sympatric with cowbirds, American robins (Turdus migratorius) ejected parasitic eggs from all experimentally parasitized clutches (N = 25) and no eggs were accepted for more than four days. In contrast, robins in northern Manitoba, an area where cowbirds do not breed, accepted parasitic eggs in 33% of nests (N = 18) for at least five days. Acceptance of experimental cowbird eggs by a second host, the yellow warbler (Dendroica petechia), was similar in allopatric (100% of 20 nests) and sympatric (88.6% of 35 nests) populations, but models of a female cowbird elicited greater nest defense by warblers in the area of sympatry. Neither host rejected eggs of conspecifics, thus, rejection of cowbird eggs was not an epiphenomenon of conspecific brood parasitism. These results support the hypothesis that recognition of cowbirds and their eggs evolved as adaptations to counter cowbird parasitism and not some other selection pressure. The expression of anti‐parasite defenses by some individuals within allopatric populations further suggests these traits may be controlled genetically but persist in such areas either through the continued introgression of rejecter genes from sympatric populations or because of the low cost of rejection behavior when parasitism is absent or rare.

CORRELATES OF EGG REJECTION IN HOSTS OF THE BROWN-HEADED COWBIRD

Abstract We conducted a comparative analysis of eight potential correlates of egg rejection in hosts of the parasitic Brown-headed Cowbird (Molothrus ater) to test the evolutionary equilibrium and evolutionary lag hypotheses as explanations for the acceptance of cowbird parasitism. The analyses generally supported evolutionary lag. Historic contact with cowbirds may explain why hosts that have recently come into contact with cowbirds accept parasitism, but it does not account for acceptance by hosts with long histories of contact with cowbirds. Egg predation by hosts, nest sanitation, population size, and egg appearance were not correlated with rejection. Larger species that typically build larger nests were more likely to reject. Large hosts may have been parasitized more frequently in the past, possibly due to their more easily found nests or superiority as hosts, and as a result, may have had more opportunity to evolve rejection. Rejection was also correlated with taxonomic affiliation, suggesting that once rejection evolves it is maintained, which implies that rejection is not costly and thus argues against an evolutionary equilibrium. Not surprisingly, hosts with large bills were more likely to reject. This may be a corollary of the tendency for large hosts, which tend to have larger bills, to reject. An evolutionary equilibrium may exist for hosts with eggs that resemble cowbird eggs, depending on the costs to host reproductive success and the likelihood of committing recognition errors. Nevertheless, some hosts have been in contact with cowbirds for a long time, build large nests, have large bills, have a “favorable” phylogeny, and lay eggs that differ from cowbird eggs, yet accept cowbird parasitism. Chance may play a role in the accumulation of the necessary recombinants and mutations necessary for the evolution of rejection. Factores Correlacionados con el Rechazo de Huevos por parte de Hospederos de Molothrus ater Resumen. Realizamos un análisis comparativo de ocho factores que potencialmente podrían estar correlacionados con el rechazo de huevos por parte de hospederos del parásito de cría Molothrus ater para poner a prueba las hipótesis de equilibrio evolutivo y de demora en la respuesta evolutiva propuestas para explicar la aceptación del parasitismo. Los análisis generalmente apoyaron la hipótesis de la demora en la respuesta evolutiva. El contacto histórico con Molothrus podría explicar por qué hospederos que sólo recientemente han entrado en contacto con estas aves aceptan el parasitismo, pero no explica por qué hay hospederos que tienen largas historias de contacto con el parásito y aceptan ser parasitadas. La depredación de huevos por parte del hospedero, el comportamiento de aseo del nido, el tamaño poblacional y la apariencia de los huevos no estuvieron correlacionados con el rechazo de huevos parásitos. Las especies grandes, que típicamente construyen nidos más grandes, presentaron una probabilidad más alta de rechazar huevos. Los hospederos más grandes podrían haber sido parasitados más frecuentemente en el pasado, posiblemente debido a que sus nidos se encuentran con mayor facilidad o a que son mejores hospederos y, como resultado, podrían haber tenido mayores oportunidades evolutivas para desarrollar el comportamiento de rechazar huevos. El comportamiento de rechazo también estuvo correlacionado con la filiación taxonómica, lo que sugiere que una vez que éste evoluciona se mantiene, implicando que no es costoso, lo que a su vez es un argumento en contra de la hipótesis del equilibrio evolutivo. De forma poco sorprendente, los hospederos con picos grandes fueron más propensos a rechazar huevos. Esto podría ser un corolario de la tendencia de los hospederos grandes (los cuales tienden a tener picos más grandes) a rechazar huevos. Es posible que exista un equilibrio evolutivo para los casos de hospederos que tienen huevos que se asemejan a los de Molothrus, dependiendo de los costos sobre el éxito reproductivo del hospedero y la probabilidad de cometer errores de reconocimiento. Sin embargo, algunos hospederos han estado en contacto con Molothrus por períodos prolongados, construyen nidos grandes, tienen picos grandes, tienen afinidades filogenéticas “favorables” y ponen huevos que difieren de los del parásito, y aún así aceptan el parasitismo. El azar podría jugar un papel importante en la acumulación de los recombinantes y mutaciones necesarios para que el comportamiento de rechazo pueda evolucionar.

Evolution of host defenses against brood parasitism : Implications of puncture-ejection by a small passerine

-In Manitoba, Warbling Vireos (Vireo gilvus) rejected eggs of the Brown-headed Cowbird (Molothrus ater) from 1 naturally parasitized nest and 16 experimentally parasitized nests studied in 1992 and 1993. Vireos rejected single, real cowbird eggs in 16 cases by ejection and 1 by desertion. Observations at nests during the first hour after parasitism showed that: (1) females carried out four ejections, whereas two of three unsuccessful ejection attempts were by males; and (2) the four observed egg removals were by puncture-ejection (entire cowbird egg removed or pieces of shell removed after egg contents consumed). These are the first observations of puncture-ejection by the Warbling Vireo, which is now the smallest species (15 g) known to eject cowbird eggs in this manner. Two competing hypotheses, evolutionary lag and evolutionary equilibrium, have been advanced to explain acceptance of brood parasitism by hosts parasitized with nonmimetic eggs. One prediction of the equilibrium hypothesis, that small hosts incur greater costs than large hosts when ejecting eggs, was examined by comparing the costs of rejection at experimentally parasitized nests of Warbling Vireos and larger Northern Orioles (Icterus galbula, 33 g). Warbling Vireos lost or damaged 5 of their own eggs while rejecting the 17 cowbird eggs, or 0.29 vireo eggs for every cowbird egg rejected. The cost to Northern Orioles of this behavior was 0.38 oriole eggs per cowbird egg ejected, which was not significantly different from the cost incurred by Warbling Vireos. My results by default support the evolutionary-lag hypothesis because the smaller species did not incur greater costs during puncture-ejection than the larger species. Warbling Vireos in and east of the Great Plains, V. g. gilvus, reject cowbird eggs, whereas individuals in a population west of the Great Plains, V. g. swainsonii (12 g), apparently accept the eggs. The different responses to cowbird eggs possibly reflect differences between two sibling species that have been in contact with cowbirds for different lengths of time, assuming that individuals in the western population are not below the minimum value for size of an ejecter. Received 16 August 1994, accepted 27 January 1995. MOST HOSTS THAT ACCEPT the eggs or nestlings of parasitic Brown-headed Cowbirds (Molothrus ater) appear to behave nonoptimally (Rothstein 1982) because this parasitism often lowers their reproductive output (Friedmann 1963, Rothstein 1975a, Payne 1977, May and Robinson 1985). Thus, hosts should be expected to evolve antiparasite strategies, especially because cowbird eggs are distinguishable from the eggs of most host species. Although highly effective nest defense would eliminate the need for egg recognition, many nests of some aggressive hosts are still parasitized (Neudorf and Sealy 1992, 1994). Thus, it is puzzling that most hosts accept cowbird eggs when effective adaptations for the rejection of parasitic eggs have been evolved by some species, often in the same evolutionary lineages (Hamilton and Orians 1965, Rothstein 1975a, 1982, 1990, Rich and Rothstein 1985, Ortega and Cruz 1988). Evolutionary lag versus equilibrium are two general views that have been proposed to explain acceptance by many hosts parasitized with nonmimetic eggs (Rothstein 1990). Under the evolutionary-lag hypothesis, rejection would be adaptive, but has not yet become common or even detectable because it takes time for new genetic variants to appear and increase as a result of selection (Mayfield 1965, Rothstein 1975a, 1982, Davies and Brooke 1988). Once the rejection behavior appears in a species, it will be fixed rapidly (Rothstein 1982). No physical constraints are assumed here because large hosts can remove cowbird eggs by grasping them in their bills, and small hosts can puncture or break the eggs and then remove them or desert their

Responses of yellow warblers to the threat of cowbird parasitism

Abstract Responses of yellow warblers, Dendroica petechia , to a model of a female brown-headed cowbird, Molothrus ater , and a fox sparrow, Passerella iliaca , control were tested during the nest-building, egg-laying, incubation and nestling stages of the nesting cycle. Testing pairs only once avoided the risk of habituation to models. Females rarely responded aggressively to models or showed distraction displays. Instead, a nest-protection behaviour involving ‘seet’ calling and a rush to sit in the nest was observed, primarily in response to the cowbird model. Yearlings did not show this behaviour as frequently as older or previously parasitized birds. Females gave fewer seet calls when they defended cryptic compared with exposed nests. They gave more seet calls and fewer ‘chip’ calls in response to the cowbird model than the control. The frequency of seet calling by females was highest during egg laying when they were most susceptible to cowbird parasitism. Males responded infrequently to all models and were first to arrive in only 5% of trials.

Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds

Field observations and model-presentation experiments have shown that yellow warblers (Dendroica petechia) produce “seet” calls preferentially in response to brood-parasitic brown-headed cowbirds (Molothrus ater). In this study, we investigated whether seet calls are functionally referential alarm calls denoting cowbirds by determining whether female warblers responded appropriately to seet calls in the absence of a cowbird, whether alarm calling by warblers varied with response urgency, and how warblers in a population allopatric with cowbirds responded to cowbird and avian predator models and seet playbacks. As a control, we presented “chip” calls, which are elicited by nest predators as well as by non-threatening intruders, but are not strongly associated with cowbirds. Yellow warblers responded differently to playbacks of seet than chip calls. To seet playbacks, almost 60% of females gave seet calls and rushed to sit in their nests, responses typically elicited by cowbirds, whereas these responses were given infrequently in response to chip calls. Yellow warblers seet called equally in situations that simulated low, medium and high risk of parasitism, which suggests that these calls did not vary with response urgency. In a population allopatric with cowbirds, seet calls were rarely produced in response to cowbird or avian nest predator models and never to seet playbacks. These results suggest that seet calls are functionally referential signals denoting cowbirds and that cowbird parasitism was a strong selective pressure in the evolution of functional referentiality in the seet call of yellow warblers.

NEST DEFENCE BY YELLOW WARBLERS: RECOGNITION OF A BROOD PARASITE AND AN AVIAN NEST PREDATOR

Yellow warblers (Dendroica petechia) were exposed to taxidermic mounts of a brood parasite (brown-headed cowbird, Molothrus ater), avian nest predator (common grackle, Quiscalus quiscula) and control (fox sparrow, Passerella iliaca) during their laying and nestling stages to determine whether nest owners distinguish between the threats of brood parasitism and predation. Yellow warblers responded more intensely to the cowbird at the laying stage, performing two unique behaviours (seet calling and nest-protection behaviour) in response to this threat. By contrast, yellow warbler responses to the grackle were greater at the nestling stage, consisting largely of alarm calls (chip, metallic chip and warble calls). The sparrow model infrequently elicited aggressive behaviour from nest owners at either stage. These responses support the hypothesis that yellow warblers discriminate between threats of brood parasitism and nest predation. Yellow warblers may perform specific behaviours to cowbirds because defensive behaviours used against predators may be incompatible with cowbird deterrence. Female nest owners responded more frequently than males at the laying stage, and more intensely than males at both nesting stages. The distance that females and males approached the models and several aggressive behaviours were positively correlated. The greater responsiveness of females may be because they dominate their mates and because females are more experienced with intruders near the nest.

Biology of Nesting Ancient Murrelets

The breeding biology of the Ancient Murrelet (Synthliboramphus antiquus) previously has not been studied intensively. Contributions of C. Littlejohn (in Bendire 1895) from Alaska, Ishizawa (1933) from Korea, and Murata (1958) from Japan generally are incomplete and deal only with short periods. Observations made intermittently between 1946 and 1952 on Langara Island, British Columbia, by C. J. Guiguet (in Drent and Guiguet 1961, unpubl. observ.) provide important comparative data. In this paper I examine the breeding ecology of the Ancient Murrelet on Langara Island, Queen Charlotte Islands, British Columbia (fig. 1).

Responses of naive yellow warblers to a novel nest predator

Abstract Naive parental yellow warblers, Dendroica petechia , were tested with a mounted eastern grey squirrel, Sciurus carolinensis , a novel predator on the study site, during the nest-building, egg-laying, incubation and nestling stages of the nesting cycle. Testing parents only once avoided the possibility that the nest defence behaviour of the parents was modified by reinforcement and loss of fear. In 96% of 80 trials, the female parent responded first to the model. Males rarely showed nest defence behaviour. Female nest defence as measured by defensive vocalizations (i.e., ‘chipping’), closest and modal distance of approach to the model, distraction displays, strikes, and close passes or hovers, did not increase significantly over the breeding season. ‘Chipping’ frequency by both sexes tended to increase after the incubation period but not significantly so. Distraction displays increased significantly only between nest-building and nestling stages. Age, clutch or brood size, and nest success were not correlated with the intensity of nest defence. Females defending exposed nests gave more distraction displays than those defending cryptic nests.

Differential parasitism of least flycatchers and yellow warblers by the brown-headed cowbird

SummaryBrown-headed cowbirds (Molothrus ater) parasitized yellow warblers (Dendroica petechia) six times more frequently than least flycatchers (Empidonax minimus) nesting in the same riparian habitat in southern Manitoba. This difference was surprising because least flycatchers were higher quality hosts; flycatchers always accepted cowbird eggs while warblers did so on only about half the occasions. Both hosts were equally good foster parents, at least until fledging; thus, once an egg was accepted there was probably no further advantage in parasitizing one species over the other. The probability that a nest was parasitized decreased with increasing nest height, perhaps as a consequence of the cowbirds habit of searching for nests close to the ground. Since least flycatchers nested higher in the canopy than yellow warblers, a greater proportion of flycatcher nests probably were not detected by cowbirds. Nevertheless, nest height alone could not account fully for the lower incidence of parasitism on flycatchers. Clutch initiation in flycatchers peaked 6 days after warbler clutch initiations and 5 days after that of cowbirds. Despite the later peak in initiations, flycatcher nests were always available as potential hosts over the entire cowbird laying season and it was not until new clutch initiations by warblers declined in late summer that flycatchers were actually used as hosts. Because least flycatchers responded more aggressively than yellow warblers to a model female cowbird at the nest, we concluded that greater nest defense by flycatchers may have also reduced the rate of brood parasitism in this host. Together, our results suggest the large difference in the frequency of parasitism between these two hosts was primarily a product of nest location but that differences in host nest-defense and breeding season asynchrony may have contributed to preferential host selection.

Dynamics of Seabird Multispecies Feeding Flocks: Age-Related Feeding Behaviour

Multispecies feeding flocks of seabirds were studied in Barkley Sound, British Columbia. The flocks occurred during the post-breeding dispersal of migrant adult and juvenile seabirds. A consideration of comparative foraging success indicated that juvenile seabirds were less skilled at locating and capturing prey. Juveniles did not initiate flocks, were less adept at finding food, and had lower feeding success rates. The juveniles appeared to compensate for these inadequacies by using a different foraging strategy than adults. They increased the amount of time spent feeding and appeared to be more attracted to the presence of other feeding birds. Juveniles were less able to recognize good potential feeding areas and accessible food items. Juveniles had a greater tendency to loaf on the centrally located terrestrial loafing sites, thus increasing their chances of sighting feeding flocks. Our results demonstrated how improved post-fledging survival was achieved for juvenile seabirds feeding in the flocks. Our findings support the interpretations put forth by others to explain delayed maturity, reduced clutches in younger birds and prolonged parental care, all characteristic of seabirds.