Brood parasite

Brood parasitism is a form of parasitism.

A Common Cuckoo being raised by a Reed Warbler.

Brood parasites are organisms that use the strategy of brood parasitism, a kind of kleptoparasitism found among birds, fish or insects, involving the manipulation and use of host individuals either of the same (intraspecific brood-parasitism) or different species (interspecific brood-parasitism) to raise the young of the brood-parasite. This relieves the parasitic parent from the investment of rearing young or building nests, enabling them to spend more time foraging, producing offspring etc. Additionally, the risk of egg loss to raiders such as raccoons is mitigated, by having distributed the eggs amongst a number of different nests.^[1] As this behaviour is damaging to the host, it will often result in an evolutionary arms race between parasite and host.^[2][3]

Avian brood parasites

The Goldeneye duck lays its eggs in the nests of other females.

In many monogamous bird species, there are extra-pair matings resulting in males outside the pair bond siring offspring and used by males to escape from the parental investment in raising their offspring.^[4] This form of cuckoldry is taken a step further when females lay their eggs in the nests of other individuals. Intraspecific brood parasitism is seen in a number of duck species with females laying their eggs in the nests of others for example in the Goldeneye, Bucephala clangula.^[5]

Interspecific brood-parasites include the Old World cuckoos in Eurasia and Australia, cowbirds and Black-headed Ducks in the Americas, and indigobirds, whydahs, and the honeyguides in Africa. Seven independent origins of obligate interspecific brood parasitism in birds have been proposed. While there is still some controversy over when and how many origins of interspecific brood parasitism have occurred, recent phylogenetic analyses suggest two origins in Passeriformes (once in New World cowbirds: Icteridae, and once in African Finches: Viduidae); three origins in Old World and New World cuckoos (once in Cuculinae, Phaenicophaeinae, and in Neomorphinae-Crotophaginae); a single origin in Old World honeyguides (Indicatoridae); and in a single species of waterfowl, the black-headed duck (Heteronetta atricapilla).^[6][7][8]

Most avian brood parasites are specialists which will only parasitize a single host species or a small group of closely related host species, but four out of the five parasitic cowbirds are generalists, which parasitize a wide variety of hosts; the Brown-headed Cowbird has 221 known hosts. They usually only lay one egg per nest, although in some cases, particularly the cowbirds, several females may use the same host nest.

The Common Cuckoo presents an interesting case in which the species as a whole parasitizes a wide variety of hosts, but individual females specialize in a single species. Genes regulating egg coloration appear to be passed down exclusively along the maternal line, allowing females to lay mimetic eggs in the nest of the species they specialize in. Females are thought to imprint upon the host species which raised them, and subsequently only parasitize nests of that species. Male Common Cuckoos will fertilize females of all lines, maintaining sufficient gene flow among the different maternal lines.^[9]

The mechanisms of host selection by female cuckoos are somewhat unclear, though several hypotheses have been suggested in attempt to explain the choice. These include genetic inheritance of host preference, host imprinting on young birds, returning to place of birth and subsequently choosing a host randomly ("natal philopatry"), choice based on preferred nest site (nest-site hypothesis), and choice based on preferred habitat (habitat-selection hypothesis). Of these hypotheses the nest-site selection and habitat selection have been most supported by experimental analysis.^[9][10]

Common adaptations of avian brood parasites

Among specialist avian brood parasites, mimetic eggs are a nearly universal adaptation. There is even some evidence that the generalist Brown-headed Cowbird may have evolved an egg coloration mimicking a number of their hosts.^[11]

Most avian brood parasites will remove a host egg when they lay one of their own in a nest. Depending upon the species, this can happen either in the same visit to the host nest or in a separate visit before or after the parasitism. This both prevents the host species from realizing their nest has been parasitized and reduces competition for the parasitic nestling once it hatches.

A Shiny Cowbird chick being fed by a Rufous-collared Sparrow

Most avian brood parasites have very short egg incubation periods and rapid nestling growth. This gives the parasitic nestling a head start on growth over its nestmates, allowing it to outcompete them. In cases where the host nestlings are significantly smaller than the parasite nestling, the host nestlings will often starve to death. Some brood parasites will eliminate all their nestmates shortly after hatching, either by ejecting them from the nest or killing them with sharp mandible hooks which fall off after a few days.

"Mafia hypothesis"

It has often been a question why the majority of the hosts of brood parasites care for the nestlings of their parasites. Not only do these brood parasites usually differ significantly in size and appearance, but it is highly probable that they reduce the reproductive success of their hosts. So what possible benefits are gained from providing this parental care? Through studies in an attempt to answer this question evolved the "Mafia hypothesis". This hypothesis revolves around host manipulations induced by behaviors of the brood parasite. Upon the detection and rejection of a brood parasite's egg, the host's nest is depredated upon, its nest destroyed and nestlings injured or killed. This threatening response is indirectly enhancing selective pressures favoring aggressive parasite behavior that may result in positive feedback between Mafia-like parasite and compliant host behaviors.^[12]

There are two avian species that have been speculated to portray this mafia-like behavior, the brown-headed cowbird of North America, Molothrus ater, and the Great Spotted Cuckoo of Europe, Clamator glandarius. The Great Spotted Cuckoo lays the majority of its eggs in the nests of the European Magpie, Pica pica. It has been observed that the Great Spotted Cuckoo repeatedly visits the nests that it has parasitised, a precondition for the Mafia hypothesis.^[12] An experiment was run by Soler et al. from April to July, 1990–1992 in the high-altitude plateau Hoya de Guadix, Spain. They observed the effects of the removal of cuckoo eggs on the reproductive success of the magpie, and measured the magpie's reaction; the egg was considered accepted if it remained in the nest, ejected if gone in between visits, or abandoned if the eggs were present but cold. If any nest contents were gone between consecutive visits, the nests were considered to have been depredated. The magpie's reproductive success was measured by number of nestlings that survived to their last visit, which was just before the nestling had been predicted to fledge from the nest. The results from these experiments show that after the removal of the parasitic eggs from the Great Spotted Cuckoo, these nests are predated at much higher rates than those where the eggs were not removed. Through the use of plasticine eggs that model those of the magpie, it was confirmed that the nest destruction was caused by the Great Spotted Cuckoo. This destruction benefits the cuckoo, for the possibility of re-nesting by the Magpie allows another chance for the cuckoo egg to be accepted.

Another similar experiment was done in 1996–2002 by Hoover et al. on the relationship between the parasitic Brown-headed Cowbird and a host, the Prothonotary Warbler, Protonotaria citrea. In their experiment, they manipulated the cowbird egg removal and cowbird access to the predator proof nests of the warbler.^[13] They found that 56% of egg ejected nests were depredated upon in comparison to 6% of non-ejected nests when cowbirds were not prevented from getting to the hosts' nest.^[13] Of the nests that were rebuilt by hosts that had previously been predated upon, 85% of those were destroyed.^[13] The number of young produced by the hosts that ejected eggs dropped 60% compared to those that accepted the cowbird eggs.

Nest-site hypothesis

In this hypothesis, female cuckoos select a group of host species with similar nest sites and egg characteristics to her own. This population of potential hosts is monitored and a nest is chosen from within this group.^[14]

Research of nest collections has illustrated a significant level of similarity between cuckoo eggs and typical eggs of the host species. A low percentage of parasitized nests were shown to contain cuckoo eggs not corresponding to the specific host egg morph. In these mismatched nests a high percent of the cuckoo eggs were shown to correlate to the egg morph of another host species with similar nesting sites. This has been pointed to as evidence for nest- site selection.^[14]

A criticism of the hypothesis is that it provides no mechanism by which nests are chosen, or which cues might be used to recognize such a site.^[15]

Host responses

Given the detrimental effects avian brood parasites can have on their hosts' reproductive success, host species have come up with various defenses against this unique threat.

Given that the cost of egg removal concurrent with parasitism is unrecoverable, the best defense for hosts is avoiding parasitism in the first place. This can take several forms, including selecting nest sites which are difficult to parasitize, starting incubation early so they are sitting on the nests when parasites visit them early in the morning, and aggressive territorial defense. Birds nesting in aggregations can also benefit from group defense.

Once parasitism has occurred, the next most optimal defense is to eject the parasitic egg. Recognition of parasitic eggs is based on identifying pattern differences or changes in the number of eggs.^[16] This can be done by grasp ejection if the host has a large enough beak, or otherwise by puncture ejection. Ejection behavior has some costs however, especially when host species have to deal with mimetic eggs. In that case, hosts will inevitably mistake one of their own eggs for a parasite egg on occasion and eject it. In any case, hosts will sometimes damage their own eggs while trying to eject a parasite egg.

Among hosts not exhibiting parasitic egg ejection, some will abandon parasitized nests and start over again. However, at high enough parasitism frequencies, this becomes maladaptive as the new nest will most likely become reparasitized.

Other behavior can include modifying the nest to exclude the parasitic egg, either by weaving over the egg or in some cases rebuilding a new nest over the existing one.

Insect brood parasites

A cuckoo bee from the genus Nomada.

There are many different types of cuckoo bees, all of which are brood-parasitic insects, laying their eggs in the nest cells of other bees, but they are normally referred to as kleptoparasites, rather than as brood parasites. A family of Cuckoo wasps also exist, many of which lay their eggs in the nests of Potter and Mud dauber wasps, and many other lineages of wasps in various families have evolved similar habits.

See also

• Host-parasite mimicry

References

1. ^ David Attenborough (1998) [First published 1998]. The Life of Birds. New Jersey: Princeton University Press. p. 246. ISBN 069101633X. 
2. ^ Payne, R. B. 1997. Avian brood parasitism. In D. H. Clayton and J. Moore (eds.), Host-parasite evolution: General principles and avian models, 338–369. Oxford University Press, Oxford.
3. ^ Rothstein, S.I, 1990. A model system for coevolution: avian brood parasitism. Annual Review of Ecology and Systematics 21: 481-508.
4. ^ Stephen M. Yezerinac, Patrick J. Weatherhead 1997. Extra-Pair Mating, Male Plumage Coloration and Sexual Selection in Yellow Warblers (Dendroica petechia). Proc. R. Soc. London B. 264(1381):527–532
5. ^ Andersson, M. & Eriksson, M.O.G. 1982 Nest parasitism in goldeneyes Bucephala clangula: some evolutionary aspects. American Naturalist 120, 1–16 (1982)
6. ^ Aragon, S., A. P. Møller, J. J. Soler, and M. Soler, 1999. Molecular phylogeny of cuckoos supports a polyphyletic origin of brood parasitism. Journal of Evolutionary Biology 12: 495–506
7. ^ Sorenson, M.D, and R.B. Payne, 2001. A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution. Evolution: 55: 2550-2567
8. ^ Sorenson, M.D., and R.B. Payne, 2002. Molecular genetic perspectives on avian brood parasitism. Integrative and Comparative Biology 42: 388–400
9. ^ ^{a b} Vogl W., M. Taborsky, B. Taborsky, Y. Teuschl, and M. Honza. (2002) Cuckoo females preferentially use specific habitats when searching for hot nests. Animal Behavior 64: 843–850
10. ^ Teuschl Y, B Taborsky, and M Taborsky. (1998) How do cuckoos find their hosts? The role of habitat imprinting. Animal Behavior 56: 1425-1433
11. ^ Brian Peer, Scott Robinson, and James Herkert in The Auk 117(4):892–901
12. ^ ^{a b} Soler, M., J. J. Soler, J. G. Martinez, A. P. Moller (1995). Magpie host manipulation by great spotted cuckoos: Evidence for an avian mafia? Evolution. 49, 770–775
13. ^ ^{a b c} Hoover, J.P., & Robinson, S.K. (2007). Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proceedings of the National Academy of Sciences of the United States of America. 104, 4479–4483
14. ^ ^{a b} Moksnes A, and E Roskaft. 1995 Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs form European museums and collections. J. Zool 236: 625–648
15. ^ Vogl W, M Taborsky, B Taborsky, Y Teuschl, and M Honza. 2002 Cuckoo females preferentially use specific habitats when searching for hot nests. Animal Behavior 64: 843–850
16. ^ Lyon, Bruce E. (2003) Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422:495–499

External links

• Lowther, Peter E. (2005–2007). "Brood Parasitism". The Field Museum. http://fm1.fieldmuseum.org/aa/staff_page.cgi?staff=lowther&id=417. Retrieved 2007-01-09.  Includes links to host lists for all known brood-parasitic bird species.
• Parasitism Research - Parasitism articles and links.