Parasitismo por moscas en aves paseriformes del Monte central de Argentina durante años lluviosos y secos

Eduardo T. Mezquida

doi:10.56178/eh.v35i1.453

Articles Published 01 August 2020 https://doi.org/10.56178/eh.v35i1.453

Botfly parasitism in passerine birds in the central Argentine Monte during wet and dry years

Monte biome climatic conditions Philornis parasite prevalence host use

Eduardo T. Mezquida Instituto de Ciencias de la Tierra y Ambientales de La Pampa, Consejo Nacional de Investigaciones Científicas y Técnicas & Centro para el Estudio y Conservación de las Aves Rapaces en Argentina, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa. Mendoza 109, 6300 Santa Rosa, La Pampa, Argentina | Departamento de Ecología, Universidad Autónoma de Madrid & Centro de Investigación en Biodiversidad y Cambio Global, Universidad Autónoma de Madrid, Madrid, España

Abstract

Avian parasites may exert an important selective pressure on host populations, although their impact may vary depending on environmental conditions. The Neotropical flies of the genus Philornis include species whose larvae parasitize the nestlings of several bird species. Here, I analyze the prevalence of parasitic flies in passerine species nesting in a semiarid area in the central Monte of Argentina, during four breeding seasons with contrasting weather conditions. Specifically, I quantify the prevalence in different avian hosts, its inter-annual and seasonal variation, the influence of precipitation and host availability, and the effect of parasitism on nestling mortality. Botfly parasitism was observed in 8 of the 21 passerine species for which nestling development could be followed. Prevalence for parasitized species was, on average, 15%, mainly affecting species in Thraupidae (21%), Mimidae (14%), and Tyrannidae (7%). Botfly parasitism occurred at the end of the breeding season in two of the four years studied, coinciding with increased late spring precipitations. Environmental conditions also favored greater host availability. Nestling mortality due to botfly parasitism was found in 10% of parasitized nests. Results indicate that the prevalence of botfly parasitism is relatively low in the central Monte, and it is positively related to wet conditions during late spring, mainly affecting avian species that breed later in the season. However, future global change scenarios could increase the negative effect of this parasite, particularly in host species of conservation concern.

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References

antoniazzi l, manzoli d, roHrmann d, SaraVia m, SilVeStril Y Beldomenico P (2011) Climate variability affects the impact of parasitic flies on Argentinean forest birds. Journal of Zoology 283:126–134
arendt wJ (1985a) Philornis ectoparasitism of pearly–eyed thrashers. I. Impact on growth and develop-ment of nestlings. Auk 102:270–280
arendt wJ (1985b) Philornis ectoparasitism of Pearly–eyed Thrashers. II. Effects on adults and reproduc-tion. Auk 102:281–292
arendt wJ (2000) Impact of nest predators, competi-tors, and ectoparasites on Pearly–eyed Thrashers, with comments on the potential implications for Puerto Rican Parrot recovery. Ornitologia Neotropi-cal 11:13–63
Bulgarella m Y HeimPel GE (2015) Host range and community structure of avian nest parasites in the genus Philornis (Diptera: Muscidae) on the island of Trinidad. Ecology and Evolution 5:3695–3703
Bulgarella m, quiroga ma Y HeimPel ge (2019) Additive negative effects of Philornis nest parasitism on sma-ll and declining Neotropical bird populations. Bird Conservation International 29:339–360
comBeS c (2001) Parasitism: the ecology and evolu-tion of intimate interactions. University of Chica-go Press, Chicago202027
couri mS (1999) Myiasis caused by obligatory pa-rasites. Ia. Philornis Meinert (Muscidae). Pp. 44–70 en: guimaraeS J Y PaPaVero n (eds) Myia-sis in man and animals in the Neotropical region. Editora Pleiade, Sao Paulo
crawleYmJ (2007) The R Book. John Wiley & Sons, West Sussex
dominguez m, reBoreda Jc Y maHler B (2015) Impact of Shiny Cowbird and botfly parasitism on the repro-ductive success of the globally endangered Yellow Cardinal Gubernatrix cristata. Bird Conservation Inter-national 25:294–305
dudaniec rY Y KleindorFer S (2006) Effects of the para-sitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu 106:13–20
dudaniec rY, FeSSl B Y KleindorFer S (2007) Interannual and interspecific variation in intensity of the para-sitic fly, Philornis downsi, in Darwin’s finches. Biologi-cal Conservation 139:325–332
FeSSl B, HeimPel ge Y cauSton CE (2018) Invasion of an avian nest parasite, Philornis downsi, to the Gala-pagos Islands: colonization history, adaptations to novel ecosystems, and conservation challenges. Pp. 213–266 en: ParKer Pg (ed) Disease ecology. Social and ecological interactions in the Galapagos Islands. Sprin-ger, Switzerland
goulSon d, derwent lc, HanleY me, dunn dw Y aBolinSSr (2005) Predicting calyptrate fly populations from the weather, and probable consequences of climate change. Journal of Applied Ecology 42:795–804
HeeB P, KölliKer m Y ricHner H (2000) Bird–ectopara-site interactions, nest humidity, and ectoparasite community structure. Ecology 81:958–968
HudSon P, rizzoli a, grenFell B, HeeSterBeeK H Y doBSon a(2002) The ecology of wildlife diseases. Oxford Univer-sity Press, Oxford
KleindorFer S Y dudaniec rY (2009) Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin’s tree finches. Be-havioral Ecology and Sociobiology 63:731–739
le Houérou H, BingHam r Y SKerBeK w (1988) Relations-hip between the variability of primary production and the variability of annual precipitation in world arid lands. Journal of Arid Environments 15:1–18
leHmann t (1993) Ectoparasites: direct impact on host fitness. Parasitology Today 9:8–13
löwenBerg–neto P (2008) The structure of the para-site–host interactions between Philornis (Diptera: Muscidae) and neotropical birds. Journal of Tropical Ecology 24:575–580
maenza ra, agoSta ea Y Bettolli ml (2017) Climate change and precipitation variability over the wes-tern ‘Pampas’ in Argentina. International Journal of Climatology 37:445–463
manzoli de, antoniazzi lr Y Beldomenico Pm (2011) Cambio ambiental global, parásitos y la salud de sus hospedadores: las moscas parásitas del género Philornis en pichones de aves. Hornero 26:45–53
manzoli de, antoniazzi lr, SaraVia mJ, SilVeStri l, rorH-mann d Y Beldomenico Pm (2013) Multi–level determi-nants of parasitic fly infection in forest passerines. PloS One 8:e67104
martin te Y geuPel gr (1993) Nest–monitoring plots: Methods for locating nests and monitoring success. Journal of Field Ornithology 64:507–519
martínezdela Puente J, merino S, loBato e, riVerodeaguilar J, del cerro S, ruizde caStañeda r Y moreno J(2010) Nest–climatic factors affect the abundance of biting flies and their effects on nestling condi-tion. Acta Oecologica 36:543–547
maSon P (1985) The nesting biology of some passeri-nes of Buenos Aires, Argentina. Ornithological Mono-graphs 36:954–972
merino S Y møller aP (2010) Host–parasite interac-tions and climate change. Pp. 213–226 en: mølleraP, Fiedler w Y BertHold P (eds) Effects of climate change on birds. Oxford University Press, New York
mezquida et (2001a) La reproducción de algunas espe-cies de Dendrocolaptidae y Furnariidae en el desier-to del Monte central, Argentina. Hornero 16:23–30
mezquida et (2001b) Aspects of the breeding biology of the Crested Gallito. Wilson Bulletin 113:104–109mezquida et (2002) Nidificación de ocho especies de Tyrannidae en la Reserva de Ñacuñán, Mendoza, Argentina. Hornero 17:31–40
mezquida et (2003) La reproducción de cinco especies de Emberizidae y Fringillidae en la Reserva de Ña-cuñán, Argentina. Hornero 18:13–20
mezquida et (2004) Nest site selection and nesting success of five species of passerines in a South American open Prosopis woodland. Journal of Orni-thology 145:16–22
mezquida et Y marone l (2001) Factors affecting nesting success of a bird assembly in the central Monte De-sert, Argentina. Journal of Avian Biology 32:287–296
mezquida et Y marone l (2003) Comparison of the reproductive biology of two Poospiza warbling–finches of Argentina in wet and dry years. Ardea91:251–262
møller aP (1997) Parasites and the evolution of host life history. Pp. 105–127 en: claYton d Y moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford
møller aP, allander K Y duFVa r (1990) Fitness effects of parasites on passerine birds: a review. Pp. Artículo ParaSitiSmoPormoScaSenaVeSdel monte 28269–280 en: Blondel J, goSler a, leBreton Jd Y mc-cleerY r (eds) Population biology of passerine birds. Springer, Berlin
morello JH (1958) La provincia fitogeográfica del Monte. Opera Lilloana 2:1–155
noreS ai (1995) Botfly ectoparasitism of the Brown Cacholote and the Firewood–gatherer. Wilson Bulle-tin 107:734–738
noY–meir i (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systema-tics 4:25–51
nuñez–roSaS le, ramírez–garcía e, lara c Y arizmendim (2018) Observación del parasitismo por moscas (Philornis bellus) en tres especies de colibríes del Oc-cidente de México. Revista Mexicana de Biodiversidad89:847–853
oJeda ra, camPoS cm, gonnet Jm, BorgHi ce Y roig Vg(1998) The MaB Reserve of Ñacuñán, Argentina: its role in understanding the Monte Desert biome. Journal of Arid Environments 39:299–313
quiroga ma Y reBoreda Jc (2012) Lethal and sublethal effects of botfly (Philornis seguyi) parasitism on hou-se wren nestlings. Condor 114:197–202
quiroga ma, reBoreda Jc Y Beltzer aH (2012) Host use by Philornis sp. in a passerine community in cen-tral Argentina. Revista Mexicana de Biodiversidad83:110–116
quiroga ma, monJe ld, arraBal JP Y Beldomenico Pm (2016) New molecular data on subcutaneous Philor-nis (Diptera: Muscidae) from southern South Ame-rica suggests the existence of a species complex. Revista Mexicana de Biodiversidad 87:1383–1386
raBuFFetti Fl Y reBoreda Jc (2007) Early infestation by bot flies (Philornis seguyi) decreases chick survival and nesting success in chalk–browed mocking-birds (Mimus saturninus). Auk 124:898–906
SalVador S Y Bodrati a (2013) Aves víctimas del parasi-tismo de moscas del género Philornis en Argentina. Nuestras Aves 58:16–21
Segura ln Y reBoreda Jc (2011) Botfly parasitism effects on nestling growth and mortality of Red–crested Cardinals. Wilson Journal of Ornitholo-gy 123:107–115
teixeira d (1999) Myiasis caused by obligatory parasi-tes. Ib. General observations on the biology of spe-cies of the genus Philornis Meinert, 1890 (Diptera, Muscidae). Pp. 51–70 en: guimaraeS J Y PaPaVero n(eds) Myiasis in man and animals in the Neotropical re-gion. Editora Pleiade, Sao Paulo
urSino ca, de márSico mc Y reBoreda Jc (2019) Brood parasitic nestlings benefit from unusual host de-fenses against botfly larvae (Philornis spp.). Behavio-ral Ecology and Sociobiology 73:146
Young Be (1993) Effects of the parasitic botfly Philor-nis carinatus on nestling house wrens, Troglodytes aedon, in Costa Rica. Oecologia 93:256–262

How to cite

Eduardo T. Mezquida (2020). Botfly parasitism in passerine birds in the central Argentine Monte during wet and dry years. El Hornero, Vol. 35 No. 1 (2020), 20-28. https://doi.org/10.56178/eh.v35i1.453

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[1] antoniazzi l, manzoli d, roHrmann d, SaraVia m, SilVeStril Y Beldomenico P (2011) Climate variability affects the impact of parasitic flies on Argentinean forest birds. Journal of Zoology 283:126–134

[2] arendt wJ (1985a) Philornis ectoparasitism of pearly–eyed thrashers. I. Impact on growth and develop-ment of nestlings. Auk 102:270–280

[3] arendt wJ (1985b) Philornis ectoparasitism of Pearly–eyed Thrashers. II. Effects on adults and reproduc-tion. Auk 102:281–292

[4] arendt wJ (2000) Impact of nest predators, competi-tors, and ectoparasites on Pearly–eyed Thrashers, with comments on the potential implications for Puerto Rican Parrot recovery. Ornitologia Neotropi-cal 11:13–63

[5] Bulgarella m Y HeimPel GE (2015) Host range and community structure of avian nest parasites in the genus Philornis (Diptera: Muscidae) on the island of Trinidad. Ecology and Evolution 5:3695–3703

[6] Bulgarella m, quiroga ma Y HeimPel ge (2019) Additive negative effects of Philornis nest parasitism on sma-ll and declining Neotropical bird populations. Bird Conservation International 29:339–360

[7] comBeS c (2001) Parasitism: the ecology and evolu-tion of intimate interactions. University of Chica-go Press, Chicago202027

[8] couri mS (1999) Myiasis caused by obligatory pa-rasites. Ia. Philornis Meinert (Muscidae). Pp. 44–70 en: guimaraeS J Y PaPaVero n (eds) Myia-sis in man and animals in the Neotropical region. Editora Pleiade, Sao Paulo

[9] crawleYmJ (2007) The R Book. John Wiley & Sons, West Sussex

[10] dominguez m, reBoreda Jc Y maHler B (2015) Impact of Shiny Cowbird and botfly parasitism on the repro-ductive success of the globally endangered Yellow Cardinal Gubernatrix cristata. Bird Conservation Inter-national 25:294–305

[11] dudaniec rY Y KleindorFer S (2006) Effects of the para-sitic flies of the genus Philornis (Diptera: Muscidae) on birds. Emu 106:13–20

[12] dudaniec rY, FeSSl B Y KleindorFer S (2007) Interannual and interspecific variation in intensity of the para-sitic fly, Philornis downsi, in Darwin’s finches. Biologi-cal Conservation 139:325–332

[13] FeSSl B, HeimPel ge Y cauSton CE (2018) Invasion of an avian nest parasite, Philornis downsi, to the Gala-pagos Islands: colonization history, adaptations to novel ecosystems, and conservation challenges. Pp. 213–266 en: ParKer Pg (ed) Disease ecology. Social and ecological interactions in the Galapagos Islands. Sprin-ger, Switzerland

[14] goulSon d, derwent lc, HanleY me, dunn dw Y aBolinSSr (2005) Predicting calyptrate fly populations from the weather, and probable consequences of climate change. Journal of Applied Ecology 42:795–804

[15] HeeB P, KölliKer m Y ricHner H (2000) Bird–ectopara-site interactions, nest humidity, and ectoparasite community structure. Ecology 81:958–968

[16] HudSon P, rizzoli a, grenFell B, HeeSterBeeK H Y doBSon a(2002) The ecology of wildlife diseases. Oxford Univer-sity Press, Oxford

[17] KleindorFer S Y dudaniec rY (2009) Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin’s tree finches. Be-havioral Ecology and Sociobiology 63:731–739

[18] le Houérou H, BingHam r Y SKerBeK w (1988) Relations-hip between the variability of primary production and the variability of annual precipitation in world arid lands. Journal of Arid Environments 15:1–18

[19] leHmann t (1993) Ectoparasites: direct impact on host fitness. Parasitology Today 9:8–13

[20] löwenBerg–neto P (2008) The structure of the para-site–host interactions between Philornis (Diptera: Muscidae) and neotropical birds. Journal of Tropical Ecology 24:575–580

[21] maenza ra, agoSta ea Y Bettolli ml (2017) Climate change and precipitation variability over the wes-tern ‘Pampas’ in Argentina. International Journal of Climatology 37:445–463

[22] manzoli de, antoniazzi lr Y Beldomenico Pm (2011) Cambio ambiental global, parásitos y la salud de sus hospedadores: las moscas parásitas del género Philornis en pichones de aves. Hornero 26:45–53

[23] manzoli de, antoniazzi lr, SaraVia mJ, SilVeStri l, rorH-mann d Y Beldomenico Pm (2013) Multi–level determi-nants of parasitic fly infection in forest passerines. PloS One 8:e67104

[24] martin te Y geuPel gr (1993) Nest–monitoring plots: Methods for locating nests and monitoring success. Journal of Field Ornithology 64:507–519

[25] martínezdela Puente J, merino S, loBato e, riVerodeaguilar J, del cerro S, ruizde caStañeda r Y moreno J(2010) Nest–climatic factors affect the abundance of biting flies and their effects on nestling condi-tion. Acta Oecologica 36:543–547

[26] maSon P (1985) The nesting biology of some passeri-nes of Buenos Aires, Argentina. Ornithological Mono-graphs 36:954–972

[27] merino S Y møller aP (2010) Host–parasite interac-tions and climate change. Pp. 213–226 en: mølleraP, Fiedler w Y BertHold P (eds) Effects of climate change on birds. Oxford University Press, New York

[28] mezquida et (2001a) La reproducción de algunas espe-cies de Dendrocolaptidae y Furnariidae en el desier-to del Monte central, Argentina. Hornero 16:23–30

[29] mezquida et (2001b) Aspects of the breeding biology of the Crested Gallito. Wilson Bulletin 113:104–109mezquida et (2002) Nidificación de ocho especies de Tyrannidae en la Reserva de Ñacuñán, Mendoza, Argentina. Hornero 17:31–40

[30] mezquida et (2003) La reproducción de cinco especies de Emberizidae y Fringillidae en la Reserva de Ña-cuñán, Argentina. Hornero 18:13–20

[31] mezquida et (2004) Nest site selection and nesting success of five species of passerines in a South American open Prosopis woodland. Journal of Orni-thology 145:16–22

[32] mezquida et Y marone l (2001) Factors affecting nesting success of a bird assembly in the central Monte De-sert, Argentina. Journal of Avian Biology 32:287–296

[33] mezquida et Y marone l (2003) Comparison of the reproductive biology of two Poospiza warbling–finches of Argentina in wet and dry years. Ardea91:251–262

[34] møller aP (1997) Parasites and the evolution of host life history. Pp. 105–127 en: claYton d Y moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford

[35] møller aP, allander K Y duFVa r (1990) Fitness effects of parasites on passerine birds: a review. Pp. Artículo ParaSitiSmoPormoScaSenaVeSdel monte 28269–280 en: Blondel J, goSler a, leBreton Jd Y mc-cleerY r (eds) Population biology of passerine birds. Springer, Berlin

[36] morello JH (1958) La provincia fitogeográfica del Monte. Opera Lilloana 2:1–155

[37] noreS ai (1995) Botfly ectoparasitism of the Brown Cacholote and the Firewood–gatherer. Wilson Bulle-tin 107:734–738

[38] noY–meir i (1973) Desert ecosystems: environment and producers. Annual Review of Ecology and Systema-tics 4:25–51

[39] nuñez–roSaS le, ramírez–garcía e, lara c Y arizmendim (2018) Observación del parasitismo por moscas (Philornis bellus) en tres especies de colibríes del Oc-cidente de México. Revista Mexicana de Biodiversidad89:847–853

[40] oJeda ra, camPoS cm, gonnet Jm, BorgHi ce Y roig Vg(1998) The MaB Reserve of Ñacuñán, Argentina: its role in understanding the Monte Desert biome. Journal of Arid Environments 39:299–313

[41] quiroga ma Y reBoreda Jc (2012) Lethal and sublethal effects of botfly (Philornis seguyi) parasitism on hou-se wren nestlings. Condor 114:197–202

[42] quiroga ma, reBoreda Jc Y Beltzer aH (2012) Host use by Philornis sp. in a passerine community in cen-tral Argentina. Revista Mexicana de Biodiversidad83:110–116

[43] quiroga ma, monJe ld, arraBal JP Y Beldomenico Pm (2016) New molecular data on subcutaneous Philor-nis (Diptera: Muscidae) from southern South Ame-rica suggests the existence of a species complex. Revista Mexicana de Biodiversidad 87:1383–1386

[44] raBuFFetti Fl Y reBoreda Jc (2007) Early infestation by bot flies (Philornis seguyi) decreases chick survival and nesting success in chalk–browed mocking-birds (Mimus saturninus). Auk 124:898–906

[45] SalVador S Y Bodrati a (2013) Aves víctimas del parasi-tismo de moscas del género Philornis en Argentina. Nuestras Aves 58:16–21

[46] Segura ln Y reBoreda Jc (2011) Botfly parasitism effects on nestling growth and mortality of Red–crested Cardinals. Wilson Journal of Ornitholo-gy 123:107–115

[47] teixeira d (1999) Myiasis caused by obligatory parasi-tes. Ib. General observations on the biology of spe-cies of the genus Philornis Meinert, 1890 (Diptera, Muscidae). Pp. 51–70 en: guimaraeS J Y PaPaVero n(eds) Myiasis in man and animals in the Neotropical re-gion. Editora Pleiade, Sao Paulo

[48] urSino ca, de márSico mc Y reBoreda Jc (2019) Brood parasitic nestlings benefit from unusual host de-fenses against botfly larvae (Philornis spp.). Behavio-ral Ecology and Sociobiology 73:146

[49] Young Be (1993) Effects of the parasitic botfly Philor-nis carinatus on nestling house wrens, Troglodytes aedon, in Costa Rica. Oecologia 93:256–262