Cleaner Birds: An Overview For The Neotropics [aves Limpadoras: Uma Visão Geral Para Os Neotrápicos]

Several bird species feed on a variety of external parasites and epibionts, organic debris, dead and wounded tissue, clots and blood, and secretions from the body of other vertebrates (hosts or clients). We present an overview of so called cleaner birds from the Neotropics based on field records, literature, and photo survey. We found that 33 bird species in 16 families practice cleaning even if some of them do so very occasionally. The birds range from the Galápagos ground finch Geospiza fuliginosa to the widespread black vulture Coragyps atratus. Clients mostly are large herbivores such as capybaras, deer, and livestock, but also include medium-sized herbivores such as iguanas and tortoises, and carnivores such as boobies and seals - a few bird species associate with these latter marine mammals. No carnivorous terrestrial mammal client is recorded to date except for a domestic dog, from whose hair black vultures picked organic debris. Some clients adopt particular inviting postures while being cleaned, whereas others are indifferent or even disturbed by the activity of cleaner birds. Capybaras, giant tortoises, and iguanas are among the inviting clients, whereas boobies try to dislodge the 'vampire' finch Geospiza difficilis. Most of the Neotropical cleaner birds may be lumped in one broad category (omnivores that dwell in open areas and associate with large to medium-sized herbivores). A second, restricted category accommodates some species from Patagonia and the Galápagos Islands (omnivores that dwell in open areas and associate with carnivorous marine mammals, or seabirds and marine reptiles). Two still more restricted categories accommodate the following: 1) forest-dwelling cleaner birds; and 2) marine coastal cleaners. Additional records of Neotropical cleaner birds will mostly fall in the broad category.104195203(2010) Introduction, , http://www.africanbirdclub.org, African Bird Club, last access on 31/07/2010Anderson, D.J., Porter, E.T., Ferree, E.D., Non-breeding Nazca boobies (Sula granti) show social and sexual interest in chicks: Behavioural and ecological aspects (2004) Behaviour, 141 (8), pp. 959-977Anjos, L., Family Corvidae (crows) (2009) Handbook of the Birds of the World, 14, pp. 494-640. , Bush-shrikes to Old World sparrows (J. del Hoyo, A. Elliot & D.A. Christie, ed.). Lynx Editions, BarcelonaBradshaw, C.J.A., White, W.W., Rapid development of cleaning behaviour by Torresian crows Corvus orru on non-native banteng Bos javanicus in northern Australia (2006) J. Avian Biol, 37 (4), pp. 409-411Burger, A.E., Family Chionidae (sheathbills) (1996) Handbook of the Birds of the World, 3, pp. 546-555. , Hoatzin to auks (J. del Hoyo, A. Elliot & J. Sargatal, ed.). Lynx Editions, Barcelona(2010) CBRO - Comitê Brasileiro de Registros Ornitológicos, , Listas das aves do Brasil. 9. ed. 18/10/2010Christian, K.A., Cleaning/feeding symbiosis between birds and reptiles of the Galápagos Islands: New observations of inter-island variability (1980) Auk, 97 (4), pp. 887-889Cody, M.L., Family Mimidae (mockingbirds and thrashers) (2005) Handbook of the Birds of the World, 10, pp. 448-495. , Cuckoo-shrikes to thrushes (J. del Hoyo, A. Elliot & D.A. Christie, ed.). Lynx Editions, BarcelonaCôté, I.M., Evolution and ecology of cleaning symbiosis in the sea (2000) Ocean. Mar. Biol. Ann. Rev, 38, pp. 311-355Craig, A.J.F.K., Family Buphagidae (oxpeckers) (2009) Handbook of The Birds of the World, 14, pp. 642-653. , Bush-shrikes to Old World sparrows (J. del Hoyo, A. Elliot & D.A. Christie, ed.). Lynx Editions, BarcelonaCraig, A.J.F.K., Feare, C.J., Family Sturnidae (starlings) (2009) In Handbook of the Birds of the World, 14, pp. 654-758. , Bush-shrikes to Old World sparrows (J. del Hoyo, A. Elliot & D.A. Christie, ed.). Lynx Editions, BarcelonaCurry, R.L., Anderson, D.J., Interisland variation in blood drinking by Galápagos mockingbirds (1987) Auk, 104 (3), pp. 517-521Dean, W.R.J., Macdonald, I.A.W., A review of African birds feeding in association with mammals (1981) Ostrich, 52, pp. 135-155Grant, P.R., (1986) Ecology and Evolution of Darwin's Finches, p. 492. , Princeton University Press, PrincetonGriffiths, C.S., Barroughclough, J.G., Groth, J.G., Martz, L., Phylogeny of Falconidae (Aves): A comparison of the efficacy of morphological, mitochondrial, and nuclear data (2004) Mol. Phylog. Evol, 32 (1), pp. 101-109Groch, K.R., Cases of harassment by kelp gulls (Larus dominicanus) on right whales (Eubalaena australis) of southern Brazil (2001) Biotemas, 14 (1), pp. 147-156Grutter, A.S., Cleaning mutualism in the sea (2005) Marine Parasitology, pp. 264-278. , (K. Rohde, ed.). CSIRO Publishing, CollingwoodIsenhart, F.R., Desante, D.F., Observations of scrub jays cleaning ectoparasites from black-tailed deer (1985) Condor, 87 (1), pp. 145-147Jaramillo, A., Burke, P., (1999) New World Blackbirds: The Icterids, p. 432. , Princeton University Press, PrincetonJohnson, K., Peer, B.D., Great-tailed Grackle (Quiscalus mexicanus) (2001) The Birds of North America, , http://bna.birds.cornell.edu/bna/species/576, (A. Poole, ed.). Cornell Lab of Ornithology, Ithaca, last access on 28/05/2010Kilham, L., Cleaning/feeding symbioses of common crows with cattle and feral hogs (1982) J. Field Ornithol, 53 (3), pp. 275-276King, B., Feeding behaviour of gulls in association with seal and sun fish (1978) Bristol Ornithol, 11, p. 33Losey, G.S., Cleaning symbiosis (1987) Symbiosis, 4 (1), pp. 229-258Love, M., (1996) Probably More Than You Want to Know about the Fishes of the Pacific Coast, p. 381. , 2nd ed. Really Big Press, Santa BarbaraMacfarland, C.G., Reeder, W.G., Cleaning symbiosis involving Galápagos tortoises and two species of Darwin's finches (1974) Z. Tierpsychol, 34, pp. 464-483Marcus, M.J., Feeding associations between capybaras and jacanas: A case of interspecific grooming and possibly mutualism (1985) Ibis, 127 (2), pp. 240-243Martin, P., Bateson, P., (1986) Measuring Behaviour, An Introductory Guide, p. 200. , Cambridge University Press, CambridgeMartínez-Vilalta, A., Motis, A., Family Ardeidae (herons) (1992) Handbook of the Birds of the World, 1, pp. 376-429. , Ostrich to ducks. (J. del Hoyo, A. Elliot & J. Sargatal, eds.). Lynx Editions, Barcelona(2010) The Neotropical Region, , http://neotropicbirding.com/blog/the-neotropical-region, Neotropical Birding, last access on 31/05/2010Peres, C.A., Ungulate ectoparasite removal by Black Caracaras and Pale-winged Trumpeters in Amazonian forests (1996) Wilson Bull, 108 (1), pp. 170-175Reeves, R.R., Stewart, B.S., Clapham, P.J., Powell, J.A., (2002) Guide to Marine Mammals of the World, p. 527. , Alfred A. Knopf, New YorkRemsen, J.V., Family Furnariidae (ovenbirds) (2003) Handbook of the Birds of the World, 8, pp. 162-357. , Broadbills to tapaculos (J. del Hoyo, A. Elliot & D.A. Christie, ed.). Lynx Editions, BarcelonaRuggiero, R.G., Eves, H.E., Bird-mammal associations in forest openings of northern Congo (Brazzaville) (1988) Afr. J. Ecol, 36, pp. 183-193Sazima, I., Unexpected cleaners: Black Vultures (Coragyps atratus) remove debris, ticks, and peck at sores of capybaras (Hydrochoerus hydrochaeris), with an overview of tick-removing birds in Brazil (2007) Rev. Bras. Ornitol, 15 (3), pp. 417-426Sazima, I., The jack-of-all-trades raptor: Versatile foraging and wide trophic role of the Southern Caracara (Caracara plancus), with comments on feeding habits of the Caracarini (2007) Rev. Bras. Ornitol, 15 (4), pp. 592-597Sazima, I., Validated cleaner: The cuculid bird Crotophaga ani picks ticks and pecks at sores of capybaras in southeastern Brazil (2008) Biota Neotrop, 8 (1), pp. 213-216. , http://www.biotaneotropica.org.br/v8n1/pt/abstract?article+bn00308012008Sazima, I., Black Vultures (Coragyps atratus) pick organic debris from the hair of a domestic dog in southeastern Brazil (2010) Rev. Bras. Ornitol, 18 (1), pp. 45-48Sazima, I., What coatis and mongooses have in common? (2010) Biota Neotrop, 10 (3), pp. 1-5. , http://www.biotaneotropica.org.br/v10n3/en/abstract?short-communication+ bn02410032010Sazima, I., Cleaner birds: A worldwide overview Rev. Bras. Ornitol, , In pressSazima, I., Sazima, C., Cleaner birds in Brazil: Update and brief reappraisal (2010) Biota Neotrop, 10 (1), pp. 327-331. , http://www.biotaneotropica.org.br/v10n1/pt/abstract?article+bn0071001201 0Schluter, D., Grant, P.R., Determinants of morphological patterns in communities of Darwin's finches (1984) Am. Nat, 123, pp. 856-869Sick, H., (1997) Ornitologia Brasileira, p. 862. , Nova Fronteira, Rio de JaneiroStrange, I., (1996) The Striated Caracara (Phalcoboenus Australis) in the Falkland Islands, , Philip Myers, CheshireSwash, A., Still, R., (2005) Birds, Mammals, and Reptiles of the Galápagos Islands, p. 168. , 2nd ed. Christopher Helm, LondonTibby, R.B., Notes on the ocean sunfish (1936) Mola mola. Calif. Fish Game, 22 (1), pp. 49-50Tomazzoni, A.C., Pedó, E., Hartz, S.M., Feeding associations between capybaras Hydrochoerus hydrochaeris (Linnaeus) (Mammalia, Hydrochaeridae) and birds in the Lami Biological Reserve, Porto Alegre, Rio Grande do Sul (2005) Brazil. Rev. Bras. Zool, 22 (3), pp. 713-716Weeks, P., Red-billed oxpeckers: Vampires or tickbirds? (2000) Behav. Ecol, 11 (2), pp. 154-160White, C.M., Olson, P.D., Kiff, L.F., Family Falconidae (falcons and caracaras) (1994) Handbook of the Birds of the World, 2, pp. 206-275. , New World vultures to guineafowl (J. del Hoyo, A. Elliot & J. Sargatal, ed.). Lynx Editions, Barcelon