NEST PARASITISM Scott K. Robinson* and Stephen I. Rothstein† *University of Illinois at Urbana-Champaign and †University of California at Santa Barbara I. Natural History ized nests (usually with renesting), or a new cup II. Coevolution between Brood Parasites and Their built over a parasitized clutch. Hosts evolutionary equilibrium hypothesis The hypothesis III. Modeling Host–Parasite Coevolution that frequencies of acceptance of brood parasitism IV. Impacts on Host Population Dynamics reflect an equilibrium between costs and benefits of V. Ecology and Social Behavior of Brood Parasites host defenses against parasitism. VI. Conspecific Brood Parasitism evolutionary lag hypothesis The hypothesis that hosts VII. Conclusions and Research Needs lack defenses against brood parasites because the defenses have not yet had time to evolve. generalist brood parasites Species that parasitize many (up to more than 200) host species. GLOSSARY gentes (singular gens) Lineages of cuckoos in which individual females specialize on a single host and lay mimetic eggs. acceptance Hosts treat brood parasitic eggs as if they host The individual that is parasitized. were their own eggs. interspecific brood parasites Brood parasites that lay coevolution Cycles of adaptation and counteradapta- their eggs in the nests of other species. tion that occur between interacting lineages. mafia effect Interspecific brood parasites that may de- coevolutionary arms race The continuing bouts of co- stroy clutches from which parasitic eggs have been evolving defenses and counterdefenses that occur ejected by the host. between hosts and parasites. mimicry Brood parasitic eggs or nestlings that closely conspecific brood parasites Brood parasites that lay match those of the hosts. their eggs in the nests of other individuals of the specialist brood parasites Species that parasitize only same species. one or a few host species. cowbirds American blackbirds in the genus Molothrus, which contains important brood parasites. cuckoos A family of birds of which approximately half the species (61 of 125) are obligate interspecific brood parasites. BROOD PARASITISM, also called social parasitism, is egg rejection Host responses to parasitism that include the exploitation by one individual (the brood parasite) ejection of parasitic eggs, abandonment of parasit- of the parental care of another (the host). Brood para- Encyclopedia of Biodiversity, Volume 4 Copyright 2001 by Academic Press. All rights of reproduction in any form reserved. 365 366 NEST PARASITISM sites can deposit eggs in the nests or broods of another well-studied common cuckoo, the species as a whole individual of the same (conspecific brood parasitism) is a generalist, but each individual female is a specialist or of a different (interspecific brood parasitism) species. member of a ‘‘gens.’’ Any one region has only one to Hosts often raise young of the brood parasite, typically several coexisting gentes but different arrays of gentes at the expense of their own young. This article presents occur in different regions. a comprehensive overview of the natural history, evolu- Brood parasitic nestlings also have a variety of mech- tion, and consequences of brood parasitism, with a spe- anisms that enhance their ability to compete with host cial focus on birds, the taxon in which it has been nestlings. Cuckoo nestlings have concave backs that best studied. they use to push out host eggs and nestlings, whereas several other brood parasites have specialized bill hooks that they use to kill nestmates. Some brood parasites apparently increase the amount of food hosts bring to I. NATURAL HISTORY them by mimicking the juvenile plumages or complex mouth markings (the ‘‘gapes’’) of host nestlings or by Brood parasites lay their eggs in the nests of other having large mouths and intense begging behavior. individuals, which then raise the parasitic young at Because brood parasites do not have to engage in the expense of part or all of their own brood. Brood costly breeding activities such as incubation and nest- parasitism was noted by Aristotle and even earlier (ap- ling feeding, they often have more time and energy proximately 2000 B.C.) in India. Brood parasitism is to devote to egg production. Some generalist brood best known in birds, approximately 1% of which are parasites lay 40 or more eggs in a season; estimates for obligate interspecific brood parasites that only lay their one tropical brood parasite suggest that more than 100 eggs in the nests of other species. Interspecific brood eggs/year are typical. Other brood parasites, however, parasitism, however, has also been documented in in- may be only slightly more fecund than their hosts. sects and fish. Conspecific brood parasitism, in which individuals facultatively lay eggs in nests of conspecific individuals, is more widespread. B. A Survey of Avian Brood Parasites Brood parasites have generated intense interest in There are 90–95 species of obligate avian brood para- the public and scientific communities. Brood parasites sites in five unrelated families (Table I). tend to be vilified in the media because of a human tendency to moralize about such things as killing baby 1. Cuculidae birds (which parasitic birds often do) and because at The cuckoos are a diverse family that contains both least some may pose a conservation threat to some parasitic and nonparasitic species. The Cuculinae has of their hosts. Among scientists, brood parasites have traditionally been recognized as an Old World subfam- generated intense debate about the coevolutionary pro- ily, all of whose approximately 50 species are obligate cesses that may be responsible for the seemingly mal- adaptive acceptance of parasitic eggs by hosts. A. Adaptations of Obligate Avian TABLE I Brood Parasites Major Groups of Avia Brood Parasites Brood parasites search for host nests, synchronize their Taxon (family/subfamily) No. of species laying with that of the host, and often remove a host Old World cuckoos (Cuculinae)a 50 egg from nests they parasitize. Brood parasitic eggs often New World cuckoos (Neomorphinae)3 have unusually thick eggshells, are usually small rela- Honeyguides (Africa and Asia) (Indicatoridae) 17? tive to the size of the parasite (but large relative to the Viduine finches (Africa) (Ploceidae)14 size of the host), often mimic the coloration of the Cuckoo-finch (Africa) (Ploceidae)1 hosts’ eggs, and have rapidly developing embryos. All Cowbirds (New World) (Icteridae)5 these traits increase fitness of the parasite by reducing Black-headed duck (South America) (Anatidae)1 competition with host nestmates and making parasitic eggs more difficult to detect and remove. Egg mimicry a Recent work indicates that at least one genus in this subfamily is most pronounced in specialist brood parasites. In the belongs in another cuckoo subfamily (see text). NEST PARASITISM 367 brood parasites. Most species are host specialists that warblers in grasslands. Recently reported DNA evi- are relatively uncommon and only a few have been well dence suggests that parasitism evolved once in a single studied (the common cuckoo and the great spotted lineage that then gave rise to both Anomalospiza and cuckoo). Another traditionally recognized subfamily, the Viduines. the Neomorphinae or New World ground cuckoos, has 11 species, 3 of which are relatively rare obligate para- 5. Icterinae sites. The latter tend to parasitize hosts that build domed nests and are poorly known overall. Nestlings The five species of New World brood parasitic cowbirds of one species, Tapera naevia, have pincer-like bills that include the most generalized of all brood parasites, they use to kill host nestlings, a case of covergence on the brown-headed and shiny cowbirds, both of which honeyguides (Indicatorinae). Recently published DNA parasitize more than 200 host species. Another species, sequence data indicate that at least 1 genus (Clamator) the tropical giant cowbird, parasitizes almost exclu- within the Cuculinae is more closely related to the sively colonial American blackbirds. Of the two re- Phaenicophaeinae, a subfamily of New World cuckoos. maining species, the bronzed cowbird is a host general- Ͼ None of the currently recognized members of the Phae- ist ( 80 host species), whereas the screaming cowbird nicophaeinae are obligate parasites but some parasitize is one of the most specialized of all brood parasites. It conspecifics and occasionally other species. These new mainly parasitizes a single species of blackbird, which DNA data place obligate parasitism within three groups was formerly thought to be a species of cowbird. Unlike of cuckoos, two of which have both parasitic and non- most brood parasites, cowbirds are often more abundant parasitic species, and indicate that parasitism evolved than many of their hosts and can pose a significant separately up to three times in cuckoos or that some threat to populations of rare, localized host species. parasitic cuckoo lineages reverted to parental behavior. Most cowbirds benefit greatly from changes in the land- scape caused by humans, which has enabled several 2. Indicatoridae species to expand their geographic ranges and increase The honeyguides, a family named for the habit of one their population sizes. As a result, they are coming into species that guides people and the African honey badger contact with new hosts that have not had recent contacts or ratel to beehives, has 17 obligately parasitic species. with brood parasitism. Some of these new hosts suffer The species of Indicator and two related genera parasit- extremely high levels of parasitism. Cowbirds appear ize cavity nesters, whereas 3 species of Protodiscus para- to be extremely fecund; the shiny cowbird may lay more sitize open-cup nesters. Most species are poorly known than 100 eggs a year. The invasion of North America and the eggs of many species have never been described. by this cowbird may pose an additional threat to species Some honeyguides have raptorial hooks on their bills, that are not currently being parasitized by the brown- which they use to kill host nestlings. headed cowbird. The brown-headed cowbird may be the most intensively studied North American bird.