Evolution of Host Defenses against Brood Parasitism: Implications of Puncture-Ejection by a Small Passerine

Abstract

-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