Population dynamics of an invasive bird parasite, Philornis downsi (Diptera: Muscidae), in the Galapagos Islands

Autoři: Charlotte E. Causton aff001;  Roger D. Moon aff002;  Arno Cimadom aff003;  Rebecca A. Boulton aff004;  Daniel Cedeño aff001;  María Piedad Lincango aff001;  Sabine Tebbich aff003;  Angel Ulloa aff001
Působiště autorů: Charles Darwin Research Station, Charles Darwin Foundation, Puerto Ayora, Santa Cruz Island, Galapagos Islands, Ecuador aff001;  Department of Entomology, University of Minnesota, St. Paul, MN, United States of America aff002;  Department of Behavioural Biology, University of Vienna, Vienna, Austria aff003;  College of Life and Environmental Sciences, University of Exeter, Cornwall, United Kingdom aff004;  Facultad De Ciencias Agrícolas, Universidad Central Del Ecuador, Quito, Pichincha, Ecuador aff005
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224125


The invasive parasitic fly, Philornis downsi (Muscidae), is one of the greatest threats to the avifauna of the Galapagos Islands. The larvae of this fly feed on the blood and tissues of developing nestlings of at least 18 endemic and native birds. The aim of the current study was to investigate biotic and abiotic factors that may influence the population dynamics of this invasive parasite. To study the influence of vegetation zone and related climatic factors on fly numbers, a bi-weekly monitoring program using papaya-baited traps was carried out at a dry, lowland site and at a humid, highland site on Santa Cruz Island between 2012–2014. Female flies, a large proportion of which were inseminated and gravid, were collected throughout the year at both sites, indicating females were active during and between the bird breeding seasons. This is the first evidence that female flies are able to persist even when hosts are scarce. On the other hand, catch rates of male flies declined between bird breeding seasons. Overall, catch rates of P. downsi were higher in the drier, lowland habitat, which may be a consequence of host or resource availability. Time was a stronger predictor of adult fly numbers than climate, further suggesting that P. downsi does not appear to be limited by its environment, but rather by host availability. Seasonal catch rates suggested that populations in both habitats were continuous and multivoltine. Numbers of adult female flies appeared to be regulated chiefly by simple direct density dependence, and may be governed by availability of bird nests with nestlings. Nevertheless, confounding factors such as the existence of reservoir hosts that perpetuate fly populations and changes in behavior of P. downsi may increase the vulnerability of bird hosts that are already IUCN red-listed or in decline.

Klíčová slova:

Animal sexual behavior – Birds – Humidity – Islands – Larvae – Population dynamics – Seasons – Nesting habits


1. Atkinson CT, LaPointe DA. Introduced avian diseases, climate change, and the future of Hawaiian honeycreepers. J Avian Med Surg. 2009; 23: 53–63. doi: 10.1647/2008-059.1 19530408

2. Szabo JK, Khwaja N, Garnett ST, Butchart SHM. Global patterns and drivers of avian axtinctions at the species and subspecies level. PLoS One. 2012; 7: e47080. doi: 10.1371/journal.pone.0047080 23056586

3. Pimm SL, Jenkins CN, Abell R, Brooks TM, Gittleman JL, Joppa LN, et al. The biodiversity of species and their rates of extinction, distribution, and protection. Science. 2014; 344: 1246752. doi: 10.1126/science.1246752 24876501

4. Niebuhr CN, Poulin R, Tompkins DM. Is avian malaria playing a role in native bird declines in New Zealand? Testing hypotheses along an elevational gradient. PLoS One. 2016; 11: e0165918. doi: 10.1371/journal.pone.0165918 27802326

5. Fessl B, Heimpel GE, Causton CE. Invasion of an avian nest parasite, Philornis downsi, to the Galapagos Islands: colonization history, adaptations to novel ecosystems, and conservation challenges. In: Parker PG editor. Disease ecology, social and ecological interactions in the Galapagos Islands. Springer International Publishing AG. 2018; doi: 10.1007/978-3-319-65909-1_9 pp. 213–268.

6. Kleindorfer S, Dudaniec RY. 2016. Host-parasite ecology, behavior and genetics: a review of the introduced fly parasite Philornis downsi and its Darwin’s finch hosts. BMC Zool. 2016; 1: 1.

7. McNew SM, Clayton DH. Alien invasion: biology of Philornis flies highlighting Philornis downsi, an introduced parasite of Galápagos birds. Annu Rev Entomol. 2018; 63:369–387. doi: 10.1146/annurev-ento-020117-043103 29058976

8. Bulgarella M, Heimpel GE. Host range and community structure of avian nest parasites in the genus Philornis (Diptera: Muscidae) on the island of Trinidad. Ecol Evol. 2015; 5: 3695–3703. doi: 10.1002/ece3.1621 26380698

9. Causton C, Cunninghame F, Tapia W. Management of the avian parasite Philornis downsi in the Galapagos Islands: a collaborative and strategic action plan. In: GNPS, GCREG, CDF and GC editors. Galapagos report 2011–2012. Puerto Ayora, Galapagos, Ecuador; 2013. pp 167–173.

10. Bulgarella M, Quiroga MA, Brito Vera GA, Dregni JS, Cunninghame F, Mosquera Muñoz DA, et al. Philornis downsi (Diptera: Muscidae), an avian nest parasite invasive to the Galapagos Islands, in mainland Ecuador. Ann Entomol Soc Am. 2015; 108: 242–250.

11. Fessl B, Couri M, Tebbich S. Philornis downsi Dodge and Aitken, new to the Galápagos Islands, (Diptera, Muscidae). Stud Dipterol. 2001; 8: 317–322.

12. Fessl B, Sinclair BJ, Kleindorfer S. The life-cycle of Philornis downsi (Diptera: Muscidae) parasitizing Darwin's finches and its impacts on nestling survival. Parasitol. 2006; 133: 739–747.

13. Cimadom A, Causton C, Cha DH, Damiens D, Fessl B, Hood-Novotny R, et al. Darwin's finches treat their feathers with a natural repellent. Sci Rep. 2016; 6: 34559; doi: 10.1038/srep34559 27721475

14. Kleindorfer S, Peters KJ, Custance G, Dudaniec RY, O'Connor JA. Changes in Philornis infestation behavior threaten Darwin's finch survival. Curr Zool. 2014; 60: 542–550.

15. Lahuatte PF, Lincango MP, Heimpel GE, Causton CE. Rearing larvae of the avian nest parasite, Philornis downsi (Diptera: Muscidae), on chicken blood-based diets. J Insect Sci. 2016; 16: 84: 1–7. https://doi.org/10.1093/jisesa/iew064

16. Jäger H, Buchholz S, Cimadom, A, Tebbich S, Rodríguez J, Barrera D, et al. Restoration of the blackberry-invaded Scalesia forest: Impacts on the vegetation, invertebrates, and birds. In: GNPS, GCREG, CDF and GC editors. Galapagos Report 2015–2016. Puerto Ayora, Galapagos, Ecuador; 2017. pp 142–148.

17. Trueman M, d'Ozouville N. Characterizing the Galapagos terrestrial climate in the face of global climate change. Noticias de Galapagos. 2010; 67: 26–37.

18. Lincango P, Causton C. Ensayos de atrayentes para la captura de la mosca parásito, Philornis downsi (Diptera: Muscidae) en las Islas Galápagos. Puerto Ayora, Galapagos, Ecuador: Charles Darwin Foundation; 2009.

19. Cimadom A, Ulloa A, Meidl P, Zöttl E., Fessl B, Nemeth E. Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin's finches. PLoS One. 2014; 9: e107518. doi: 10.1371/journal.pone.0107518 25248092

20. R Core Team. R: A language and environment for statistical computing, v. 3.1.3. R Foundation for Statistical Computing, Vienna, Austria; 2015. URL http://www.R-project.org/.

21. Harrison XA. A comparison of observation-level random effect and Beta-Binomial models for modelling overdispersion in Binomial data in ecology & evolution. PeerJ. 2015; 3: e1114. doi: 10.7717/peerj.1114 26244118

22. Royama T. Analytical population dynamics. London, United Kingdom: Chapman & Hall; 1992.

23. Turchin P. Complex population dynamics: A theoretical/empirical synthesis. Princeton, New Jersey: Princeton University Press; 2003.

24. Berryman A, Turchin P. Identifying the density‐dependent structure underlying ecological time series. Oikos. 2001; 92:265–70.

25. Grant PR. Ecology and evolution of Darwin's finches. Princeton, NJ, USA: Princeton University Press; 1986.

26. Cha DH, Mieles AE, Lahuatte P, Cahuana A, Lincango MP, Causton CE. Identification and optimization of microbial attractants for Philornis downsi, an invasive fly parasitic on birds. J Chem Ecol. 2016; 42:1101–1111. doi: 10.1007/s10886-016-0780-1 27744622

27. Díaz-Fleischer F, Pinero JC, Shelly TE. Interactions between tephritid fruit fly physiological state and stimuli from baits and traps: looking for the pied piper of Hamelin to lure pestiferous fruit flies. In: Shell N, Epsky ND, Jang EB, Reyes-Flores J, Vargas R editors. Trapping and the detection, control, and regulation of tephritid fruit flies. Heidelberg, New York, London: Springer, Dordrecht; 2014. pp 145–172.

28. Upakut S, Sukontason KL, Bunchu N, Pereira RM, Sukontason K. Behavioral response of house fly, Musca domestica L. (Diptera: Muscidae) to natural products. Southeast Asian J Trop Med Public Health. 2017; 48: 561–9.

29. Sontigun N, Sukontason KL, Klong-Klaew T, Sanit S, Samerjai C, Somboon P, et al. Bionomics of the oriental latrine fly Chrysomya megacephala (Fabricius) (Diptera: Calliphoridae): temporal fluctuation and reproductive potential. Parasit Vectors. 2018; 11: 415. doi: 10.1186/s13071-018-2986-2 30005704

30. Fletcher BS, Pappas S, Kapatos E. Changes in the ovaries of olive flies (Dacus oleae Gmelin]) during the summer, and their relationship to temperature, humidity and fruit availability. Ecol Entomol. 1978; 3: 99–107.

31. Venkatesh K, Morrison PE. Some aspects of oögenesis in the stable fly Stomoxys calcitrans (Diptera: Muscidae). J Insect Physiol. 1980; 26: 711–715.

32. Vogt WG Walker JM. Potential and realized fecundity in the bush fly, Musca vetutisima under favourable and unfavourable protein-feeding regimes. Entomol Exp Appl. 1987; 44: 115–122.

33. Fessl B, Tebbich S. Philornis downsi—a recently discovered parasite on the Galapagos archipelago—a threat to Darwin's finches? Ibis 2002; 144: 445–451

34. Dudaniec RY, Fessl B, Kleindorfer S. Interannual and interspecific variation in intensity of the parasitic fly, Philornis downsi, in Darwin's finches. Biol Conserv. 2007; 139: 325–332.

35. Wiedenfeld DA, Jimenez UGA, Fessl B, Kleindorfer S, Valarezo JC. Distribution of the introduced parasitic fly Philornis downsi (Diptera: Muscidae) in the Galapagos Islands. Pac Conserv Biol. 2007; 13: 14–19.

36. Heleno R, Olesen J, Nogales M, Vargas P, Traveset A. Seed dispersal networks in the Galapagos and the consequences of alien plant invasions. Proc R Soc Lond B Biol Sci. 2013; 280: 20122112

37. Renteria JL, Gardener MR, Panetta FD, Atkinson R, Crawley MJ. Possible impacts of the invasive plant Rubus niveus on the native vegetation of the Scalesia forest in the Galapagos islands. PLoS One. 2012; 7:e48106. doi: 10.1371/journal.pone.0048106 23118934

38. Taylor LR. Analysis of the effect of temperature on insects in flight. J Anim Ecol. 1963; 12: 99–112.

39. Berry IL, Nelson AK, Broce AB. Effects of weather on capture of stable flies (Diptera: Muscidae) by Alsynite fiber glass traps. Environ Entomol. 1963; 15: 706–709.

40. Grüebler MU, Morand M, Naef-Daenzer B. A predictive model of the density of airborne insects in agricultural environments. Agric Ecosyst Environ. 2008; 123: 75–80.

41. Dudaniec RY, Gardner MG, Kleindorfer S. Offspring genetic structure reveals mating and nest infestation behaviour of an invasive parasitic fly (Philornis downsi) of Galapagos birds. Biol Invasions. 2010; 12:581–592. https://doi.org/10.1007/s10530-009-9464-x

42. Hardy ICW, Boulton RA. Sex allocation, sex ratios and reproduction. In: Choe J editor. Encyclopedia of animal behavior 2nd Edition. Oxford: Elsevier. 2019. pp 464–471.

43. Koop JAH, Le Bohec C, Clayton DH. Dry year does not reduce invasive parasitic fly prevalence or abundance in Darwin's finch nests. Reports Parasitol. 2013; 3: 11–17.

44. Fessl B, Young HG, Young RP, Rodríguez-Matamoros J, Dvorak M, Tebbich S, et al. How to save the rarest Darwin's finch from extinction: the mangrove finch on Isabela Island. Philos Trans R Soc Lond B Biol Sci. 2010; 365: 1019–1030. doi: 10.1098/rstb.2009.0288 20194165

45. O'Connor JA, Sulloway FJ, Robertson J, Kleindorfer S. Philornis downsi parasitism is the primary cause of nestling mortality in the critically endangered Darwin’s medium tree finch (Camarhynchus pauper). Biodivers Conserv. 2010; 19:853–866. https://doi.org/10.1007/ s10531-009-9740-1

46. Young HG, Cunninghame F, Fessl B, Vargas HF. Mangrove finch Camarhynchus heliobates: an obligate mangrove specialist from the Galapagos islands. In: Gleason G, Victor T editors. Mangrove ecosystems, biogeography, genetic diversity and conservation strategies. New York: Nova Science Publisher; 2013. pp 107–121.

47. Dvorak M, Nemeth E, Wendelin B, Herrera P, Mosquera D, Anchundia D, et al. Conservation status of landbirds on Floreana: the smallest inhabited Galápagos Island. J Field Ornithol. 2017; 88: 132–45.

48. Koop JA, Kim PS, Knutie SA, Adler F, Clayton DH. An introduced parasitic fly may lead to local extinction of Darwin's finch populations. Journal of Applied Ecology. 2016 Apr 1;53(2):511–8. doi: 10.1111/1365-2664.12575 26980922

49. Knutie SA, Owen JB, McNew SM, Bartlow AW, Arriero E, Herman JM, et al. Galapagos mockingbirds tolerate introduced parasites that affect Darwin's finches. Ecol. 2016; 97:940–950. https://doi.org/10.1890/15-0119

50. Heimpel GE, Hillstrom A, Freund D, Knutie SA, Clayton DH. Invasive parasites and the fate of Darwin’s finches in the Galapagos Islands: the case of the vegetarian finch. Wilson J Ornithol. 2017; 129: 345–49

51. Ortiz-Catedral L, Sevilla S, Young, G and Rueda D. Natural history and conservation prospects of the Floreana mockingbird (Mimus trifasciatus). In: GNPS, GCREG, CDF and GC, editors. Galapagos Report 2015–2016. Puerto Ayora, Galapagos, Ecuador; 2017. pp 169–172.

52. McNew SM, Knutie SA, Goodman GB, Theodosopoulos A, Saulsberry A, Yépez R. J, et al. 2019. Annual environmental variation influences host tolerance to parasites. Proceedings of the Royal Society B: Biological Sciences http://doi.org/10.1098/rspb.2019.0049

53. Greenman JV, Hudson PJ. Parasite-mediated and direct competition in a two-host shared macroparasite system. Theor Popul Biol. 2000; 57: 13–34. doi: 10.1006/tpbi.1999.1435 10708626

54. Lafferty KD, Gerber LR. Good medicine for conservation biology: the intersection of epidemiology and conservation theory. Conserv Biol. 2002; 16: 593–604.

55. Heimpel GE, Neuhauser C, Hoogendoorn M. Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecol Letters. 2003; 6: 556–566.

56. Collignon RM. Semiochemicals of Philornis downsi (Dipter: Muscidae), a parasite of passerine birds of the Galapagos Islands. M.Sc. Thesis, State University of New York College of Environmental Science and Forestry. 2011.

57. Mieles García, AE. Semiochemical attractants of the parasitic fly Philornis downsi in the Galapagos. PhD. Thesis, State University of New York College of Environmental Science and Forestry. 2018.

Článek vyšel v časopise


2019 Číslo 10