Anti-brood parasite strategies of naïve populations of nesting birds in Puerto Rico
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Abstract: The Shiny Cowbird (Molothrus bonariensis), a generalist brood parasite, arrived in Puerto Rico in the 1940s or early 1950s. No previous record of brood parasites exists for Puerto Rico, so the avian communities had no defenses specialized to counter cowbird parasitism. Nevertheless, some native species were parasitized at high rates, whereas others were able to avoid cowbird parasitism. I examined native bird behaviors that reduced the chance of parasitism, with the prediction that some ecological or behavioral mechanisms used to counter nest depredation may effectively counter parasitism. Certain habitat components (e.g., placement of nests low in dense stands of vegetation) associated with reduced nest depredation may also be effective in concealing nests from brood parasites. Similar to avian populations with long histories of coevolution with brood parasites, the recently exposed populations of nesting birds in Puerto Rico were divided into discrete categories of acceptors and rejectors of alien eggs. Regularly parasitized species were characteristically acceptors, whereas species with low rates of nest parasitism were rejectors. Nest guarding is an effective strategy in countering brood parasitism. Species displaying high nest attentiveness experienced a lower incidence of parasitism than species showing low attendance. Nesting species that were aggressive toward all territory invaders incurred low rates of parasitism. Heavily parasitized species showed lower aggression toward cowbirds than toward other species. Aggressive individuals also incurred lower parasitism rates than did individuals showing lower aggressive responses to nest territory intruders. Individuals of colony-nesting species that nested within colonies incurred lower rates of parasitism than did birds nesting outside the area defended by neighbors. Also, non-aggressive species were afforded some protection against cowbird parasitism by the more vigorous territorial defense of neighboring species. The data reported here are among the earliest collected on Shiny Cowbird-host interactions in Puerto Rico and, as such, can serve as baselines against which changes in behavior and ecology can be measured over time.
Keywords: aggression, anti-parasite defenses, brood parasitism, egg rejection, habitat selection, host nest defense, Molothrus bonariensis, nest guarding, Shiny Cowbird, territory defense, West Indies
Resumen: Las estrategias anti-parásitos de nidada de las ingenuas poblaciones de aves nidificantes en Puerto Rico- Molothrus bonariensis es un parásito de nidada generalista que llegó a Puerto Rico en la década de los 1940 o principios de los 1950. No existen registros previos de parásitos de nidada en Puerto Rico por lo que las comunidades de aves no tienen defensas especializadas para contrarrestar el parasitismo de esta especie. Sin embargo, algunas especies nativas tuvieron altas tasas de parasitismo mientras que otras fueron capaces de evitarlo. Examiné las conductas de especies nativas que redujeron la posibilidad de ser parasitadas con la predicción de que algunos mecanismos ecológicos y conductuales utilizados para evitar la depredación de nidos pueden contrarrestar el parasitismo. Determinados componentes del hábitat (ej. ubicación baja de los nidos en sitios densos de vegetación) asociados con una reducida depredación de nidos pueden también ser efectivos en ocultar los nidos a los parásitos de nidada. Similares a las poblaciones de aves con largas historias de coevolución con estos parásitos, las recientemente expuestas poblaciones de aves nidificantes en Puerto Rico fueron divididas en categorías discretas de aceptores y aquellos que rechazan huevos ajenos. Las especies parasitadas regularmente fueron típicamente aceptores mientras que aquellas con bajas tasas de parasitismo de nido fueron del grupo de rechazo. El cuidado del nido es una estrategia efectiva para evitar el parasitismo de nidada. Las especies que muestran una alta atención del nido experimentaron una incidencia más baja de parasitismo que aquellas que mostraron una baja atención. Las especies nidificantes que fueron agresivas con todos los intrusos en su territorio incurrieron en bajas tasas de parasitismo. Las especies altamente parasitadas mostraron ser menos agresivas hacia Molothrus bonariensis que hacia otras especies. Individuos agresivos también tuvieron tasas de parasitismo más bajas que aquellos que mostraron respuestas menos agresivas hacia los intrusos en los territorios de los nidos. Los individuos de especies coloniales que nidificaron dentro de las colonias tuvieron tasas más bajas de parasitismo que aquellos que nidificaron fuera de las áreas defendidas por sus vecinos. También a las especies no agresivas les fue concedida cierta protección contra el parasitismo del Pájaro Vaquero por las especies vecinas más fuertes en la defensa del territorio. Los datos registrados aquí están entre los primeros colectados en las interacciones del Pájaro Vaquero-huésped en Puerto Rico y como tal pueden servir como línea base en relación con cuáles cambios conductuales y ecológicos pueden ser medidos en el tiempo.
Palabras clave: agresión, Antillas, Caribe insular, cuidado del nido, defensas anti-parásito, defensa del territorio, defensa del nido del huésped, parasitismo de nidada, rechazo de huevos, Molothrus bonariensis, Pájaro Vaquero
Résumé: Les stratégies des populations indigènes d’oiseaux nicheurs contre le parasitisme de couvée a Porto Rico- Le Vacher luisant (Molothrus bonariensis), une espèce généraliste parasitant les couvées, est arrivé à Porto Rico dans les années quarante ou au début des années cinquante. Il n’existe pas de données antérieures de parasitisme de couvée à Porto Rico, ainsi les communautés d’oiseaux n’avaient pas de défenses pour faire face au Vacher. Toutefois, certaines espèces indigènes étaient fortement touchées alors que d’autres étaient capables d’éviter le parasitisme du Vacher. J’ai examiné des comportements des oiseaux indigènes qui diminuaient les risques de parasitisme, avec l’hypothèse que certains mécanismes écologiques ou comportementaux utilisés pour contrer la prédation des nids pourraient efficacement contrer le parasitisme. Certaines composantes de l'habitat (p. ex. une position basse des nids dans une végétation dense) associées à une faible prédation des nids pourraient également être efficaces pour dissimuler les nids aux oiseaux parasites de couvée. Comme les populations d’oiseaux ayant longuement coévolué avec les espèces parasites de couvée, les populations d'oiseaux nicheurs récemment exposées à ce phénomène à Porto Rico étaient divisées en catégories distinctes acceptant ou rejetant les œufs exogènes. Les espèces régulièrement parasitées les acceptaient de façon caractéristique, alors que les espèces peu parasitées les rejetaient. La surveillance du nid constitue une stratégie efficace dans la lutte contre le parasitisme. Les espèces portant une grande attention à leur nid étaient plus faiblement touchées que les espèces peu présentes. Les espèces nicheuses agressives envers tous les intrus pénétrant sur leur territoire présentaient de faibles taux de parasitisme. Les espèces fortement parasitées se montraient moins agressives envers les vachers qu’envers d'autres espèces. Les individus agressifs présentaient également des taux de parasitisme inférieurs à ceux des individus moins agressifs vis-à-vis des intrusions dans leur territoire de nidification. Les individus appartenant à des espèces coloniales et nichant à l’intérieur des colonies étaient moins touchés par le parasitisme que les oiseaux nichant en dehors de la zone défendue par des voisins. Ainsi, les espèces non-agressives bénéficiaient d'une certaine protection contre le parasitisme du Vacher grâce à la défense territoriale plus vigoureuse des espèces voisines. Les données présentées ici sont parmi les premières recueillies à Porto Rico sur les interactions Vacher luisant / hôte parasité et, à ce titre, peuvent servir de repères pour mesurer des changements du comportement et de l'écologie au fil du temps.
Mots clés: agression, Antilles, défenses antiparasites, défense du nid hôte, défense du territoire, Molothrus bonariensis, parasitisme de couvée, rejet d’œuf, sélection de l’habitat, surveillance du nid, Vacher luisant
References
(http://www.aou.org/checklist/north/index.php; accessed 20 January 2010).
ARENDT, W. J. 2006. Adaptations of an avian supertramp: distribution, ecology, and life history of the Pearly-eyed Thrasher (Margarops fuscatus). General Technical Report 27. Puerto Rico: U. S. Department of Agriculture, Forest Service, International Institute of Tropical Forestry.
BERGER, A. L. 1951. The cowbird and certain host species in Michigan. Wilson Bulletin 63:26–34.
BLANCHER, P. L., AND R. J. ROBERTSON. 1982. Kingbird aggression: does it deter predation? Animal Behaviour 30:929–930.
BRISKIE, J. V., S. G. SEALY, AND K. A. HOBSON. 1990. Differential parasitism of Least Flycatchers and Yellow Warblers by the Brown-headed Cowbird. Behavioral Ecology and Sociobiology 27:403–410.
________. 1992. Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46:334–340.
BUELL, P. F., AND P. DANSEREAU. 1966. Analysis and mapping of the Roosevelt Roads areas. Pp. 46–287 in Special Publication No. 1. Mayagüez, Puerto Rico: Institute of Caribbean Science.
BURGHAM, M. C. J., AND J. PICMAN. 1989. Effects of Brown-headed Cowbirds on the evolution of Yellow Warbler anti-parasite strategies. Animal Behaviour 38:298–308.
CANNELL, P. F., AND B. A. HARRINGTON. 1984. Interspecific egg dumping by a Great Egret and Black-crowned Night Herons. Auk 101:889–891.
CARTER, M. D. 1987. An incident of brood parasitism by the Verdin. Wilson Bulletin 99:136.
CHESNESS, R. A., M. M. NELSON, AND W. H. LONGLEY. 1968. The effect of predator removal on pheasant reproductive success. Journal of Wildlife Management 32:683–697.
CLARK, K. L., AND R. J. ROBERTSON. 1979. Spatial and temporal multi-species nesting aggregations in birds as anti-parasite and anti-predator defenses. Behavioral Ecology and Sociobiology 5:359–371.
________. 1981. Cowbird parasitism and evolution of anti-parasite strategies in the Yellow Warbler. Wilson Bulletin 93:249–258.
COLLIAS, N. E., AND E. C. COLLIAS. 1984. Nest building and bird behavior. Princeton, New Jersey: Princeton University Press.
CRUZ, A., R. LÓPEZ-ORTIZ, E. A. VENTOSA-FEBLES, J. W. WILEY, T. K. NAKAMURA, K. R. RAMOS-ALVAREZ, AND W. POST. 2005. Ecology and management of Shiny Cowbirds (Molothrus bonariensis) and endangered Yellow-shouldered Blackbirds (Agelaius xanthomus) in Puerto Rico. Pp. 38-44 in Management of cowbirds and their hosts: balancing science, ethics, and mandates (Ortega, C. P., J. F. Chase, and B. D. Peer, eds.). American Ornithologists’ Union Ornithological Monographs 57.
________, T. MANOLIS, AND J. W. WILEY. 1985. The Shiny Cowbird: a brood parasite expanding its range in the Caribbean region. Pp. 607–620 in Neotropical ornithology (Buckley, P.A., M.S. Foster, E.S. Morton, R.S. Ridgely, and F.G. Buckley, eds.). American Ornithologists’ Union Ornithological Monograph No. 36.
________, J. W. WILEY, T. NAKAMURA, AND W. POST. 1989. The Shiny Cowbird Molothrus bonariensis in the West Indian region — biogeographical and ecological implications. Pages 519–540 in Biogeography of the West Indies past, present, & future (Woods, C.A., ed.). Gainesville, Florida: Sandhill Crane Press, Inc.
DONOVAN, T. M., P. W. JONES, E. M. ANNAND, AND F. R. THOMPSON III. 1997. Variation in local-scale edge effects: mechanisms and landscape context. Ecology 78:2064–2075.
DWERNYCHUK, L. W., AND D. A. BOAG. 1972. How vegetative cover protects duck nests from egg-eating birds. Journal of Wildlife Management 36:955–958.
EWEL, J. J., AND J. L. WHITMORE. 1973. The ecological life zones of Puerto Rico and the U.S. Virgin Islands. Forest Service Research Paper ITF-18. New Orleans, Louisiana: U. S. Department of Agriculture, Southern Research Station.
FOLKERS, K. L. 1982. Host behavioral defenses to cowbird parasitism. Kansas Ornithological Society Bulletin 33:32–34.
________, AND P. E. LOWTHER. 1985. Responses of nesting Red-winged Blackbirds and Yellow Warblers to Brown-headed Cowbirds. Journal of Field Ornithology 56:175–177.
FRIEDMANN, H., L. F. KIFF, AND S. I. ROTHSTEIN. 1977. A further contribution to knowledge of host relations of the parasitic cowbirds. Smithsonian Contributions in Zoology No. 235.
GARCÍA, J. R., C. SCHMITT, C. HEBERER, AND A. WINTER. 1998. La Parguera, Puerto Rico, USA. Pp. 195–212 in Caribbean coral reef, seagrass and mangrove sites (Kjerfve, B., ed.). Paris, France: UNESCO, Coastal Region and Small Islands Papers No. 3.
GOCHFELD, M. 1979. Brood parasites and host coevolution: interactions between Shiny Cowbirds and two species of meadowlarks. American Naturalist 113:855–870.
GREIG-SMITH, P. W. 1980. Parental investment in nest defense by Stone-Chats (Saxicola torquata). Animal Behaviour 28:604–619.
HAMILTON, W. J., III, AND G. H. ORIANS. 1965. Evolution of brood parasitism in altricial birds. Condor 67:361–382.
HAMMOND, M. C., AND W. R. FORWARD. 1956. Experiments on causes of duck nest predation. Journal of Wildlife Management 20:243–247.
HANN, H. W. 1937. Life history of the Oven-bird in southern Michigan. Wilson Bulletin 49:145–237.
HOLCOMB, L. C. 1967. Mourning Dove egg in nests of catbird and robin. Wilson Bulletin 79:450–451.
HOLLANDER, M., AND D. A. WOLFE. 1973. Nonparametric statistical methods. New York: John Wiley and Sons, Inc.
HOY, G., AND J. OTTOW. 1964. Biological and oological studies of the molothrine cowbirds (Icteridae) of Argentina. Auk 81:186–203.
HUDSON, W. H. 1870. Letter on the ornithology of Buenos Ayres. Proceedings of the Zoological Society of London 1870:671–673.
JAMES, F. C., AND H. H. SHUGART, JR. 1970. A quantitative method of habitat description. Audubon Field Notes 24:727–736.
JONES, R. E., AND K. E. HUNGERFORD. 1972. Evaluation of nesting cover as protection from magpie predation. Journal of Wildlife Management 36:727–732.
KLEINBAUM, D. G., AND L. L. KUPPER. 1978. Applied regression analysis and other multivariable methods. North Scituate, Massachusetts: Duxbury Press.
LITTLE, E. L., JR., AND F. H. WADSWORTH. 1964. Common trees of Puerto Rico and the Virgin Islands. Washington, DC: U. S. Department of Agriculture, Agriculture Handbook No. 249.
________, R. O. WOODBURY, AND F. H. WADSWORTH. 1974. Trees of Puerto Rico and the Virgin Islands. Second Volume. Washington, DC: U. S. Department of Agriculture, Agriculture Handbook No. 449.
LÓPEZ-ORTIZ, R., E. A. VENTOSA-FEBLES, K. R. RAMOS-ÁLVAREZ, R. MEDINA-MIRANDA, AND A. CRUZ. 2006. Reduction in host use suggests host specificity in individual Shiny Cowbirds (Molothrus bonariensis). Ornitología Neotropical 17:259–269.
MARTIN, T. E., AND J. J. ROPER. 1988. Nest predation and nest site selection of a western population of the Hermit Thrush. Condor 90:51–57.
MASON, P. 1987. Pair formation in cowbirds: evidence found for Screaming but not Shiny cowbirds. Condor 89:349–356.
________, AND S. I. ROTHSTEIN. 1986. Coevolution and avian brood parasitism: cowbird eggs show evolutionary response to host discrimination. Evolution 40:1207–1214.
MASSONI, V., AND J. C. REBOREDA. 2002. A neglected cost of brood parasitism: egg punctures by Shiny Cowbirds during inspection of potential host nests. Condor 104:407–412.
MAYFIELD. H. 1965. The Brown-headed Cowbird, with old and new hosts. Living Bird 4:13–28.
MCLAREN, C. M., AND S. G. SEALY. 2000. Are nest predation and brood parasitism correlated in Yellow Warblers? A test of the cowbird predation hypothesis. Auk 117:1056¬1060.
MØLLER, A. P. 1987. Intraspecific nest parasitism and anti-parasite behaviour in swallows, Hirundo rustica. Animal Behaviour 35:247–254.
________. 1989. Intraspecific nest parasitism in the swallow Hirundo rustica: the importance of neighbors. Behavioral Ecology and Sociobiology 25:33–38.
NIE, H. H., C. HADLAI HULL, J. G. JENKINS, K. STEINBRENNER, AND D. H. BENT. 1975. SPSS: Statistical package for the social sciences. New York: McGraw-Hill Book Company.
ODIN, C. R. 1957. California Gull predation on waterfowl. Auk 74:185–202.
ORTEGA, J. C., AND C. P. ORTEGA. 2000. Effects of Brown-headed Cowbirds and predators on the nesting success of Yellow Warblers in southwestern Colorado. Journal of Field Ornithology 71:516–524.
OTERO, J. I., R. A. TORO, AND L. PAGÁN DE OTERO. 1945. Catálogo de los nombres vulgares y científicos de algunas plantas puertorriqueñas. 2ª Ed. Río Piedras: Estación Experimental Agricultura, Universidad de Puerto Rico, Boletín 37.
PAYNE, R. B. 1973. The breeding season of a parasitic bird, the Brown-headed Cowbird, in central California. Condor 75:80–99.
________. 1977. The ecology of brood parasitism in birds. Annual Review of Ecology and Systematics 8:1–28.
PÉREZ-RIVERA, R. A. 1986. Parasitism by the Shiny Cowbird in the interior parts of Puerto Rico. Journal of Field Ornithology 57:99–104.
PIELOU, E. C. 1977. Mathematical ecology. New York: John Wiley and Sons.
POST, W., A. CRUZ, AND D. B. MCNAIR. 1993. The North American invasion pattern of the Shiny Cowbird. Journal of Field Ornithology 64:32–41.
________, AND J. W. WILEY. 1977a. The Shiny Cowbird in the West Indies. Condor 79:119–121.
________. 1977b. Reproductive interactions of the Shiny Cowbird and the Yellow-shouldered Blackbird. Condor 79:176–184.
PUERTO RICO DEPARTMENT OF NATURAL RESOURCES. 1976. The master plan for Commonwealth forests of Puerto Rico. San Juan, Puerto Rico: Puerto Rico Department of Natural Resources.
RICKLEFS, R. E. 1969. An analysis of nesting mortality in birds. Smithsonian Contributions in Zoology 9:1–48.
ROBERTSON, R. J., AND R. F. NORMAN. 1977. The function and evolution of aggressive host behavior towards the Brown-headed Cowbird (Molothrus ater). Canadian Journal of Zoology 55:508–518.
ROTHSTEIN, S. I. 1971. Observations and experiment in the analysis of interactions between brood parasites and their hosts. American Naturalist 105:71–74.
________. 1975a. An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271.
________. 1975b. Mechanisms of avian egg-recognition: do birds know their own eggs? Animal Behaviour 23:268–278.
________. 1975c Evolutionary rates and host defenses against avian brood parasitism. American Naturalist 109:161–179.
SEALY, S. G. 1989. Incidental “egg dumping” by the House Wren in a Yellow Warbler nest. Wilson Bulletin 101:491–493.
________. 1995. Burial of cowbird eggs by parasitized Yellow Warblers: an empirical and experimental study. Animal Behavior 49:877–889.
SHUGART, H. H., JR., AND B. C. PATTEN. 1972. Niche quantification and the concept of niche pattern. Pp. 283–325 in Systems analysis and simulation in ecology, Vol. 2 (Patten, B. C., ed.). New York: Academic Press.
SMITH, K. G. 1977. Distribution of summer birds along a forest moisture gradient in an Ozark watershed. Ecology 58:810–819.
SOUTHEAST REGIONAL CLIMATE CENTER. 2010. Historical climate summaries for Puerto Rico and the U.S. Virgin Islands.
(http://www.sercc.com/climateinfo/historical/historical-pr.html; accessed 16 January 2010).
TEWKSBURY, J. J., S. J. HEIL, AND T. E. MARTIN. 1998. Breeding productivity does not decline with increasing fragmentation in a western landscape. Ecology 79:2890–2903.
VINCENTY, M., A. G. TOSSAS, F. J. BIRD-PICÓ, R. LÓPEZ-ORTIZ, AND E. A. VENTOSA-FEBLES. 2009. Yellow Warbler (Dendroica petechia) breeding success in relation to Shiny Cowbird (Molothrus bonariensis) brood parasitism in Boquerón, Puerto Rico. Ornitología Neotropical 20:523–533.
WIENS, J. A. 1965. Nest parasitism of the Dickcissel by the Yellow-billed Cuckoo in Marshall County, Oklahoma. Southwest Naturalist 10:142.
________. 1971. “Egg-dumping” by the Grasshopper Sparrow in a Savannah Sparrow nest. Auk 88:185–186.
________. 1976. Population responses to patchy environments. Annual Review of Ecology and Systematics 7:81–120.
WILEY, J. W. 1982. Ecology of avian brood parasitism at an early interfacing of host and parasite populations. Ph.D. dissertation. Coral Gables, Florida: University of Miami.
________. 1985. Shiny Cowbird parasitism in two avian communities in Puerto Rico. Condor 87:165–176.
________, W. POST, AND A. CRUZ. 1991. Conservation of the Yellow-shouldered Blackbird Agelaius xanthomus, an endangered West Indian species. Biological Conservation 55:119–138.
________, AND B. N. WILEY. 1979. The biology of the White-crowned Pigeon. Wildlife Monograph No. 64.
WOODWORTH, B. L. 1997. Brood parasitism, nest predation, and season-long reproductive success of a tropical island endemic. Condor 99:605–621.
ZAR, J. H. 1974. Biostatistical analysis. Englewood Cliffs, New Jersey: Prentice-Hall, Inc.
