Cambio ambiental global, parásitos y la salud de sus hospedadores: las moscas parásitas del género Philornis en pichones de aves

Darío E. Manzoli; Leandro R. Antoniazzi; Pablo M. Beldomenico

doi:10.56178/eh.v26i1.695

Articles Published 01 August 2011 https://doi.org/10.56178/eh.v26i1.695

Global environmental change, parasites and their host’s health: flies of the genus Philornis parasitizing bird nestlings

climate change conservation deforestation global change Philornis pollution

Darío E. Manzoli Laboratorio de Ecología de Enfermedades, Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral. Rdo. Kreder 2805, S3080HOF Esperanza, Santa Fe, Argentina

Leandro R. Antoniazzi Laboratorio de Ecología de Enfermedades, Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral. Rdo. Kreder 2805, S3080HOF Esperanza, Santa Fe, Argentina

Pablo M. Beldomenico Laboratorio de Ecología de Enfermedades, Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral. Rdo. Kreder 2805, S3080HOF Esperanza, Santa Fe, Argentina | Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) | Global Health Program, Wildlife Conservation Society

Abstract

Human activity is causing considerable changes on our planet, which entail misbalances in one of the systems that regulate animal population dynamics: the host-parasite relationship. In this article we show, using documented examples, the direct action of pollution, habitat fragmentation and climate change, as well as their interactions, on the health of wildlife populations and their pathogens. We present the case of myiasis caused by flies of the genus Philornis, whose larvae show parasitic behaviour that affects bird nestlings. The occurrence of these parasites depends on climatic variables, being more abundant during periods of high precipitation and temperature, which is influenced by climate change. Their abundance is also related to nest density, which is affected by forest fragmentation. Therefore, the net effect of global environmental change on the impact of this parasitism depends on at least two of their interacting factors: climate change and deforestation.

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References

AIZEN M, GARIBALDI L Y DONDO M (2009) Expansiónde la soja y diversidad de la agricultura argentina.Ecología Austral 19:45–54
ALBRIGHT T, PIDGEON A, RITTENHOUSE C, CLAYTON M,FLATHER C, CULBERT P, WARDLOW B Y RADELOFF V(2010) Effects of drought on avian communitystructure. Global Change Biology 16:2158–2170
ANTONIAZZI LR, MANZOLI DE, ROHRMANN D, SARAVIAMJ, SILVESTRI L Y BELDOMENICO PM (2011) Climatevariability affects the impact of parasitic flies onArgentinean forest birds. Journal of Zoology 283:126–134
BELDOMENICO PM Y BEGON M (2010) Disease spread,susceptibility and infection intensity: vicious circles?Trends in Ecology and Evolution 25:21–27
BELDOMENICO PM, JOLY D, UHART M Y KARESH W(2008a) Wildlife health as an indicator of climatechange. Pp. 179–197 en: RELMAN DA, HAMBURG MA,CHOFFNES ER Y MACK A (eds) Global climate changeand extreme weather events: understanding thecontributions to infectious disease emergence. TheNational Academies, Washington DC
BELDOMENICO PM, TELFER S, GEBERT S, LUKOMSKI L,BENNETT M Y BEGON M (2008b) Poor condition andinfection: a vicious circle in natural populations.Proceedings of the Royal Society B Biological Sciences275:1753–1759
BELDOMENICO PM Y UHART M (2008) Ecoepidemio-logía de los virus de influenza aviar. FAVE, CienciasVeterinarias 7:23–40
BERGER L, SPEARE R, DASZAK P, GREEN DE, CUNNINGHAMAA, GOGGIN CL, SLOCOMBE R, RAGAN MA, HYATT AD,MCDONALD KR, HINES HB, LIPS KR, MARANTELLI GY PARKES H (1998) Chytridiomycosis causesamphibian mortality associated with populationdeclines in the rain forests of Australia and CentralAmerica. Proceedings of the National Academy ofSciences 95:9031–9036
BERNARDOS J Y ZACCAGNINI ME (2011) El uso de insecti-cidas en cultivos agrícolas y su riesgo potencial paralas aves en la Región Pampeana. Hornero 26:55–64
BLANCHET S, MEJEAN L, BOURQUE JF, LEK S, THOMAS F,MARCOGLIESE DJ, DODSON JJ Y LOOT G (2009) Whydo parasitized hosts look different? Resolving the“chicken-egg” dilemma. Oecologia 160:37–47
BLEHERT DS, HICKS AC, BEHR M, METEYER CU,BERLOWSKI-ZIER BM, BUCKLES EL, COLEMAN JT,DARLING SR, GARGAS A, NIVER R, OKONIEWSKI JC,RUDD RJ Y STONE WB (2009) Bat white-nosesyndrome: an emerging fungal pathogen? Science323:227
BORG K (1966) Mercury poisoning in Swedish wildlife.Journal of Applied Ecology 3:171
BOTH C, BOUWHUIS S, LESSELLS CM Y VISSER ME (2006)Climate change and population declines in a long-distance migratory bird. Nature 441:81–83
CHASAR A, LOISEAU C, VALKIUNAS G, IEZHOVA T, SMITHTB Y SEHGAL RN (2009) Prevalence and diversitypatterns of avian blood parasites in degradedAfrican rainforest habitats. Molecular Ecology18:4121–4133
COURI M, ANTONIAZZI L, BELDOMENICO P Y QUIROGAM (2009) Argentine Philornis Meinert species(Diptera: Muscidae) with synonymic notes. Zootaxa2261:52–62
DAWSON R, HILLEN K Y WHITWORTH T (2005) Effectsof experimental variation in temperature on larvaldensities of parasitic Protocalliphora (Diptera:Calliphoridae) in nests of tree swallows (Passeri-formes: Hirundinidae). Environmental Entomology34:563–568
DEEM S, SPELMAN L, YATES R Y MONTALI R (2000)Canine distemper in terrestrial carnivores: a review.Journal of Zoo and Wildlife Medicine 31:441–451
DUDANIEC R Y KLEINDORFER S (2006) Effects of theparasitic flies of the genus Philornis (Diptera:Muscidae) on birds. Emu 106:13–20
FERREYRA H (2011) Municiones de plomo y contami-nación: un viejo problema mundialmente conocidopero localmente desatendido. Hornero 26:65–72
FERREYRA H, ROMANO M Y UHART M (2009) Recent andchronic exposure of wild ducks to lead in human-modified wetlands in Santa Fe Province, Argentina.Journal of Wildlife Diseases 45:823–827
FISHER IJ, PAIN DJ Y THOMAS VG (2006) A review oflead poisoning from ammunition sources interrestrial birds. Biological Conservation 131:421–432
GIUFFRÉ L (2003) Impacto ambiental en agroecosistemas.Editorial Facultad de Agronomía, Buenos Aires
GIUSTI L (2009) A review of waste managementpractices and their impact on human health. WasteManagement 29:2227–2239
GOERKE H, WEBER K, BORNEMANN H, RAMDOHR S YPLÖTZ J (2004) Increasing levels and biomagnifica-tion of persistent organic pollutants (POPs) inAntarctic biota. Marine Pollution Bulletin 48:295–302
GRIER JW (1982) Ban of DDT and subsequent recoveryof reproduction in bald eagles. Science 218:1232–1235
HARVELL CD, MITCHELL CE, WARD JR, ALTIZER S,DOBSON AP, OSTFELD RS Y SAMUEL MD (2002) Climatewarming and disease risks for terrestrial and marinebiota. Science 296:2158–2162
HEEB P, KÖLLIKER M Y RICHNER H (2000) Bird-ectoparasite interactions, nest humidity, andectoparasite community structure. Ecology81:958–968
HOUGHTON JT, DING Y, GRIGGS DJ, NOGUER M, VA NDERLINDEN PJ, DAI X, MASKELL K Y JOHNSON CA (2001)Climate change 2001: the scientific basis. CambridgeUniversity Press, Cambridge
HUDSON PJ, DOBSON AP Y NEWBORN D (1998)Prevention of population cycles by parasiteremoval. Science 282:2256–2258
HUDSON PJ, RIZZOLI A, GRENFELL BT, HEESTERBEEK H YDOBSON AP (2002) The ecology of Wildlife Diseases.Oxford University Press, Oxford
JETZ W, WILCOVE DS Y DOBSON AP (2007) Projectedimpacts of climate and land-use change on theglobal diversity of birds. PLoS Biology 5:1211–1219
KLAASSEN C (2007) Toxicology: the basic science of poisons.McGraw-Hill, Nueva York
LAURANCE W Y WILLIAMSON G (2001) Positive feed-backs among forest fragmentation, drought, andclimate change in the Amazon. Conservation Biology15:1529–1535LOISELLE B, GRAHAM C, GOERCK J Y RIBEIRO M (2010)Assessing the impact of deforestation and climatechange on the range size and environmental nicheof bird species in the Atlantic forests, Brazil. Journalof Biogeography 37:1288–1301MARI M, NADAL M, SCHUHMACHER M Y DOMINGO JL(2009) Exposure to heavy metals and PCDD/Fs bythe population living in the vicinity of a hazardouswaste landfill in Catalonia, Spain: Health riskassessment. Environment International 35:1034–1039MARTIN PA, CAMPBELL D, HUGHES K Y MCDANIEL T(2008) Lead in the tissues of terrestrial raptors insouthern Ontario, Canada, 1995–2001. Science of theTotal Environment 391:96–103MCCALLUM H (2008) Tasmanian devil facial tumourdisease: lessons for conservation biology. Trends inEcology and Evolution 23:631–637MUÑOZDE TORO M, BELDOMENICO HR, GARCÍA SR,STOKER C, DE JESÚS JJ, BELDOMENICO PM, RAMOS JGY LUQUE EH (2006) Organochlorine levels in adiposetissue of women from a littoral region of Argentina.Environmental Research 102:107–112
NOBRE C, SELLERS P Y SHUKLA J (1991) Amazoniandeforestation and regional climate change. Journalof Climate 4:957–988
NOYES PD, MCELWEE MK, MILLER HD, CLARK BW, VANTIEM LA, WALCOTT KC, ERWIN KN Y LEVIN ED (2009)The toxicology of climate change: environmentalcontaminants in a warming world. EnvironmentInternational 35:971–986
O’CONNOR JA, SULLOWAY FJ, ROBERTSON J YKLEINDORFER S (2010) Philornis downsi parasitism isthe primary cause of nestling mortality in thecritically endangered Darwin’s medium tree finch(Camarhynchus pauper). Biodiversity and Conservation19:853–866
PACHAURI RK Y REISINGER A (2008) Climate change 2007:synthesis report. IPCC Secretariat, Ginebra
PARUELO J, GUERSCHMAN J, PIÑEIRO G, JOBBÁGY E,VERÓN S, BALDI G Y BAEZA S (2006) Cambios en eluso de la tierra en Argentina y Uruguay: marcosconceptuales para su análisis. Agrociencia 10:47–61
PEDERSEN AB, JONES K, NUNN C Y ALTIZER S (2008)Infectious diseases and extinction risk in wildmammals. Conservation Biology 21:1269–1279
PÉREZ AA, ZACCAGNINI ME Y PEREDA AJ (2011) LaInfluenza Aviar y sus implicancias para la salud de lasaves silvestres de América del Sur. Hornero 26:29–44
REDFORD K, AMATO G, BAILLIE J, BELDOMENICO P,BENNETT E, CLUM N, COOK R, FONSECA G, HEDGES S,LAUNAY F, LIEBERMAN S, MACE G, MURAYAMA A,PUTNAM A, ROBINSON J, ROSENBAUM H, SANDERSONE, STUART S, THOMAS P Y THORBJARNARSON J (2011)What does it mean to successfully conserve a(vertebrate) species? BioScience 61:39–48
SEHGAL R (2010) Deforestation and avian infectiousdiseases. Journal of Experimental Biology 213:955–960
SMITH K, ACEVEDO-WHITEHOUSE K Y PEDERSEN AB(2009) The role of infectious diseases in biologicalconservation. Animal Conservation 12:1–12
SPALDING M, MARTINS J, WALSH P, MORIN K, DUNMORED Y FORRESTER D (2002) Burrowing fly larvae(Philornis porteri) associated with mortality ofeastern bluebirds in Florida. Journal of WildlifeDiseases 38:776–783
TEIXEIRA DM (1999) Myiasis caused by obligatoryparasites. Ib. General observations on the biologyof species of the genus Philornis Meinert, 1890(Diptera, Muscidae). Pp. 71–96 en: GUIMARÃES JH YPAPAVERO N (eds) Myiasis in man and animals in theNeotropical region. Bibliographic database. EditoraPlêiade y FAPESP, San Pablo
THUILLER W (2007) Biodiversity: climate change andthe ecologist. Nature 448:550–552
UHART M Y ZACCAGNINI ME (2001) Manual de procedi-mientos operativos estandarizados de campo para docu-mentar incidentes de mortandad de fauna silvestre.Comisión Interinstitucional para la Conservaciónde la Vida Silvestre en Agroecosistemas, INTA,Buenos Aires
VANDE POL M, ENS B, HEG D, BROUER L, KROL J, MAIERM, EXO K, OOSTERBEEK K, LOK T, EISING C Y KOFFIJBERGK (2010) Do changes in the frequency, magnitudeand timing of extreme climatic events threaten thepopulation viability of coastal birds? Journal ofApplied Ecology 47:720–730
WOBESER GA (1994) Investigation and management ofdisease in wild animals. Plenum, Nueva York

How to cite

Darío E. Manzoli , Leandro R. Antoniazzi, Pablo M. Beldomenico (2011). Global environmental change, parasites and their host’s health: flies of the genus Philornis parasitizing bird nestlings. El Hornero, Vol. 26 No. 1 (2011), 45-53. https://doi.org/10.56178/eh.v26i1.695

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[1] AIZEN M, GARIBALDI L Y DONDO M (2009) Expansiónde la soja y diversidad de la agricultura argentina.Ecología Austral 19:45–54

[2] ALBRIGHT T, PIDGEON A, RITTENHOUSE C, CLAYTON M,FLATHER C, CULBERT P, WARDLOW B Y RADELOFF V(2010) Effects of drought on avian communitystructure. Global Change Biology 16:2158–2170

[3] ANTONIAZZI LR, MANZOLI DE, ROHRMANN D, SARAVIAMJ, SILVESTRI L Y BELDOMENICO PM (2011) Climatevariability affects the impact of parasitic flies onArgentinean forest birds. Journal of Zoology 283:126–134

[4] BELDOMENICO PM Y BEGON M (2010) Disease spread,susceptibility and infection intensity: vicious circles?Trends in Ecology and Evolution 25:21–27

[5] BELDOMENICO PM, JOLY D, UHART M Y KARESH W(2008a) Wildlife health as an indicator of climatechange. Pp. 179–197 en: RELMAN DA, HAMBURG MA,CHOFFNES ER Y MACK A (eds) Global climate changeand extreme weather events: understanding thecontributions to infectious disease emergence. TheNational Academies, Washington DC

[6] BELDOMENICO PM, TELFER S, GEBERT S, LUKOMSKI L,BENNETT M Y BEGON M (2008b) Poor condition andinfection: a vicious circle in natural populations.Proceedings of the Royal Society B Biological Sciences275:1753–1759

[7] BELDOMENICO PM Y UHART M (2008) Ecoepidemio-logía de los virus de influenza aviar. FAVE, CienciasVeterinarias 7:23–40

[8] BERGER L, SPEARE R, DASZAK P, GREEN DE, CUNNINGHAMAA, GOGGIN CL, SLOCOMBE R, RAGAN MA, HYATT AD,MCDONALD KR, HINES HB, LIPS KR, MARANTELLI GY PARKES H (1998) Chytridiomycosis causesamphibian mortality associated with populationdeclines in the rain forests of Australia and CentralAmerica. Proceedings of the National Academy ofSciences 95:9031–9036

[9] BERNARDOS J Y ZACCAGNINI ME (2011) El uso de insecti-cidas en cultivos agrícolas y su riesgo potencial paralas aves en la Región Pampeana. Hornero 26:55–64

[10] BLANCHET S, MEJEAN L, BOURQUE JF, LEK S, THOMAS F,MARCOGLIESE DJ, DODSON JJ Y LOOT G (2009) Whydo parasitized hosts look different? Resolving the“chicken-egg” dilemma. Oecologia 160:37–47

[11] BLEHERT DS, HICKS AC, BEHR M, METEYER CU,BERLOWSKI-ZIER BM, BUCKLES EL, COLEMAN JT,DARLING SR, GARGAS A, NIVER R, OKONIEWSKI JC,RUDD RJ Y STONE WB (2009) Bat white-nosesyndrome: an emerging fungal pathogen? Science323:227

[12] BORG K (1966) Mercury poisoning in Swedish wildlife.Journal of Applied Ecology 3:171

[13] BOTH C, BOUWHUIS S, LESSELLS CM Y VISSER ME (2006)Climate change and population declines in a long-distance migratory bird. Nature 441:81–83

[14] CHASAR A, LOISEAU C, VALKIUNAS G, IEZHOVA T, SMITHTB Y SEHGAL RN (2009) Prevalence and diversitypatterns of avian blood parasites in degradedAfrican rainforest habitats. Molecular Ecology18:4121–4133

[15] COURI M, ANTONIAZZI L, BELDOMENICO P Y QUIROGAM (2009) Argentine Philornis Meinert species(Diptera: Muscidae) with synonymic notes. Zootaxa2261:52–62

[16] DAWSON R, HILLEN K Y WHITWORTH T (2005) Effectsof experimental variation in temperature on larvaldensities of parasitic Protocalliphora (Diptera:Calliphoridae) in nests of tree swallows (Passeri-formes: Hirundinidae). Environmental Entomology34:563–568

[17] DEEM S, SPELMAN L, YATES R Y MONTALI R (2000)Canine distemper in terrestrial carnivores: a review.Journal of Zoo and Wildlife Medicine 31:441–451

[18] DUDANIEC R Y KLEINDORFER S (2006) Effects of theparasitic flies of the genus Philornis (Diptera:Muscidae) on birds. Emu 106:13–20

[19] FERREYRA H (2011) Municiones de plomo y contami-nación: un viejo problema mundialmente conocidopero localmente desatendido. Hornero 26:65–72

[20] FERREYRA H, ROMANO M Y UHART M (2009) Recent andchronic exposure of wild ducks to lead in human-modified wetlands in Santa Fe Province, Argentina.Journal of Wildlife Diseases 45:823–827

[21] FISHER IJ, PAIN DJ Y THOMAS VG (2006) A review oflead poisoning from ammunition sources interrestrial birds. Biological Conservation 131:421–432

[22] GIUFFRÉ L (2003) Impacto ambiental en agroecosistemas.Editorial Facultad de Agronomía, Buenos Aires

[23] GIUSTI L (2009) A review of waste managementpractices and their impact on human health. WasteManagement 29:2227–2239

[24] GOERKE H, WEBER K, BORNEMANN H, RAMDOHR S YPLÖTZ J (2004) Increasing levels and biomagnifica-tion of persistent organic pollutants (POPs) inAntarctic biota. Marine Pollution Bulletin 48:295–302

[25] GRIER JW (1982) Ban of DDT and subsequent recoveryof reproduction in bald eagles. Science 218:1232–1235

[26] HARVELL CD, MITCHELL CE, WARD JR, ALTIZER S,DOBSON AP, OSTFELD RS Y SAMUEL MD (2002) Climatewarming and disease risks for terrestrial and marinebiota. Science 296:2158–2162

[27] HEEB P, KÖLLIKER M Y RICHNER H (2000) Bird-ectoparasite interactions, nest humidity, andectoparasite community structure. Ecology81:958–968

[28] HOUGHTON JT, DING Y, GRIGGS DJ, NOGUER M, VA NDERLINDEN PJ, DAI X, MASKELL K Y JOHNSON CA (2001)Climate change 2001: the scientific basis. CambridgeUniversity Press, Cambridge

[29] HUDSON PJ, DOBSON AP Y NEWBORN D (1998)Prevention of population cycles by parasiteremoval. Science 282:2256–2258

[30] HUDSON PJ, RIZZOLI A, GRENFELL BT, HEESTERBEEK H YDOBSON AP (2002) The ecology of Wildlife Diseases.Oxford University Press, Oxford

[31] JETZ W, WILCOVE DS Y DOBSON AP (2007) Projectedimpacts of climate and land-use change on theglobal diversity of birds. PLoS Biology 5:1211–1219

[32] KLAASSEN C (2007) Toxicology: the basic science of poisons.McGraw-Hill, Nueva York

[33] LAURANCE W Y WILLIAMSON G (2001) Positive feed-backs among forest fragmentation, drought, andclimate change in the Amazon. Conservation Biology15:1529–1535LOISELLE B, GRAHAM C, GOERCK J Y RIBEIRO M (2010)Assessing the impact of deforestation and climatechange on the range size and environmental nicheof bird species in the Atlantic forests, Brazil. Journalof Biogeography 37:1288–1301MARI M, NADAL M, SCHUHMACHER M Y DOMINGO JL(2009) Exposure to heavy metals and PCDD/Fs bythe population living in the vicinity of a hazardouswaste landfill in Catalonia, Spain: Health riskassessment. Environment International 35:1034–1039MARTIN PA, CAMPBELL D, HUGHES K Y MCDANIEL T(2008) Lead in the tissues of terrestrial raptors insouthern Ontario, Canada, 1995–2001. Science of theTotal Environment 391:96–103MCCALLUM H (2008) Tasmanian devil facial tumourdisease: lessons for conservation biology. Trends inEcology and Evolution 23:631–637MUÑOZDE TORO M, BELDOMENICO HR, GARCÍA SR,STOKER C, DE JESÚS JJ, BELDOMENICO PM, RAMOS JGY LUQUE EH (2006) Organochlorine levels in adiposetissue of women from a littoral region of Argentina.Environmental Research 102:107–112

[34] NOBRE C, SELLERS P Y SHUKLA J (1991) Amazoniandeforestation and regional climate change. Journalof Climate 4:957–988

[35] NOYES PD, MCELWEE MK, MILLER HD, CLARK BW, VANTIEM LA, WALCOTT KC, ERWIN KN Y LEVIN ED (2009)The toxicology of climate change: environmentalcontaminants in a warming world. EnvironmentInternational 35:971–986

[36] O’CONNOR JA, SULLOWAY FJ, ROBERTSON J YKLEINDORFER S (2010) Philornis downsi parasitism isthe primary cause of nestling mortality in thecritically endangered Darwin’s medium tree finch(Camarhynchus pauper). Biodiversity and Conservation19:853–866

[37] PACHAURI RK Y REISINGER A (2008) Climate change 2007:synthesis report. IPCC Secretariat, Ginebra

[38] PARUELO J, GUERSCHMAN J, PIÑEIRO G, JOBBÁGY E,VERÓN S, BALDI G Y BAEZA S (2006) Cambios en eluso de la tierra en Argentina y Uruguay: marcosconceptuales para su análisis. Agrociencia 10:47–61

[39] PEDERSEN AB, JONES K, NUNN C Y ALTIZER S (2008)Infectious diseases and extinction risk in wildmammals. Conservation Biology 21:1269–1279

[40] PÉREZ AA, ZACCAGNINI ME Y PEREDA AJ (2011) LaInfluenza Aviar y sus implicancias para la salud de lasaves silvestres de América del Sur. Hornero 26:29–44

[41] REDFORD K, AMATO G, BAILLIE J, BELDOMENICO P,BENNETT E, CLUM N, COOK R, FONSECA G, HEDGES S,LAUNAY F, LIEBERMAN S, MACE G, MURAYAMA A,PUTNAM A, ROBINSON J, ROSENBAUM H, SANDERSONE, STUART S, THOMAS P Y THORBJARNARSON J (2011)What does it mean to successfully conserve a(vertebrate) species? BioScience 61:39–48

[42] SEHGAL R (2010) Deforestation and avian infectiousdiseases. Journal of Experimental Biology 213:955–960

[43] SMITH K, ACEVEDO-WHITEHOUSE K Y PEDERSEN AB(2009) The role of infectious diseases in biologicalconservation. Animal Conservation 12:1–12

[44] SPALDING M, MARTINS J, WALSH P, MORIN K, DUNMORED Y FORRESTER D (2002) Burrowing fly larvae(Philornis porteri) associated with mortality ofeastern bluebirds in Florida. Journal of WildlifeDiseases 38:776–783

[45] TEIXEIRA DM (1999) Myiasis caused by obligatoryparasites. Ib. General observations on the biologyof species of the genus Philornis Meinert, 1890(Diptera, Muscidae). Pp. 71–96 en: GUIMARÃES JH YPAPAVERO N (eds) Myiasis in man and animals in theNeotropical region. Bibliographic database. EditoraPlêiade y FAPESP, San Pablo

[46] THUILLER W (2007) Biodiversity: climate change andthe ecologist. Nature 448:550–552

[47] UHART M Y ZACCAGNINI ME (2001) Manual de procedi-mientos operativos estandarizados de campo para docu-mentar incidentes de mortandad de fauna silvestre.Comisión Interinstitucional para la Conservaciónde la Vida Silvestre en Agroecosistemas, INTA,Buenos Aires

[48] VANDE POL M, ENS B, HEG D, BROUER L, KROL J, MAIERM, EXO K, OOSTERBEEK K, LOK T, EISING C Y KOFFIJBERGK (2010) Do changes in the frequency, magnitudeand timing of extreme climatic events threaten thepopulation viability of coastal birds? Journal ofApplied Ecology 47:720–730

[49] WOBESER GA (1994) Investigation and management ofdisease in wild animals. Plenum, Nueva York