Effect of introduced parasites on the survival and microbiota of nestling cactus finches (Geospiza scandens) in the Galápagos Islands

Abstract

Introduced parasites and pathogens have colonized the Galápagos Islands of Ecuador. For example, a parasitic nest fly, Philornis downsi, was introduced to the Galápagos and has since caused significant nestling mortality for some endemic Darwin’s finches. However, some larger bodied species of birds in the Galápagos, including vegetarian finches (Platyspiza crassirostris) and Galápagos mockingbirds (Mimus parvulus), can be less affected by the parasite. Our study explores the effects of P. downsi on a small population of common cactus finches (Geospiza scandens) across two breeding seasons on San Cristóbal Island, Galápagos. Specifically, we experimentally manipulated P. downsi abundance and characterized the gut and skin microbiota, and survival of nestling finches. Because cactus finches are medium-sized birds and small- and medium-sized birds are generally negatively affected by P. downsi, we predicted that the parasite would have a similar detrimental effect on fledging success. We also determined the effect of P. downsi on the microbiota because other studies have shown that the bacterial community can be beneficial for host health (e.g., conferring immunity and nutrient absorption). Although the overall skin and gut microbiota differed, we found that parasite treatment did not affect the microbiota in either tissue. However, nestlings from parasitized nests had significantly lower fledging success (25%, on average) compared to nestlings from non-parasitized nests (79%). We found that, similar to other medium-sized species, cactus finches are negatively affected by P. downsi, which could have implications for their risk of extirpation from the island. The results of this study should be considered when managing this population of concern.

Zusammenfassung

Auswirkungen eingeschleppter Parasiten auf Überlebensraten und Mikrobiome von Nestlingen des Kaktusgrundfinks ( Geospiza scandens ) auf den Galapagosinseln

Die ekuadorianischen Galapagosinseln sind durch eingeschleppte Parasiten und Pathogene besiedelt. So wurde beispielsweise die parasitäre Fliege Philornis downsi auf Galápagos eingeführt und hat seither bei manchen endemischen Darwinfinkenarten Nestlingssterblichkeit von signifikantem Ausmaß ausgelöst. Jedoch können einige größere Vogelarten auf Galápagos, darunter Dickschnabel-Darwinfinken (Platyspiza crassirostris) und Galapagosspottdrosseln (Mimus parvulus), weniger durch den Parasiten betroffen sein. Unsere Studie befasst sich mit den Auswirkungen von P. downsi auf eine kleine Population des Kaktusgrundfinks (Geospiza scandens) während zweier Brutsaisons auf der Insel San Cristóbal, Galápagos. Konkret veränderten wir im Experiment die Häufigkeit von P. downsi und erfassten die Mikrobiome im Darm und auf der Haut sowie die Überlebensraten der Finkennestlinge. Da es sich bei Kaktusgrundfinken um mittelgroße Vögel handelt, und kleine und mittelgroße Vogelarten gemeinhin negativ durch P. downsi beeinflusst werden, erwarteten wir, dass der Parasit eine vergleichbar nachteilige Auswirkung auf ihren Ausfliegeerfolg haben würde. Außerdem bestimmten wir den Effekt von P. downsi auf die Mikrobiome, da in anderen Untersuchungen gezeigt wurde, dass diese Bakteriengemeinschaften der Wirtgesundheit förderlich sein können (beispielsweise durch die Verleihung von Immunität und durch Nährstoffabsorption). Obgleich sich die Mikrobiome von Haut und Darm insgesamt unterschieden, stellten wir fest, dass die Parasitenbehandlung die Mikrobiomzusammensetzung bei keinem der beiden Gewebstypen beeinflusste. Nestlinge aus parasitierten Nestern wiesen allerdings einen signifikant geringeren Ausfliegeerfolg (im Durchschnitt 25%) auf, verglichen mit Nestlingen aus parasitenfreien Nestern (79%). Wir stellten fest, dass Kaktusgrundfinken, ähnlich wie andere mittelgroße Vogelarten, durch P. downsi negativ beeinflusst werden, was Konsequenzen für das Risiko hat, dass sie von der Insel verschwinden. Daher sollten die Ergebnisse dieser Studie bei Managemententscheidungen bezüglich dieser gefährdeten Population berücksichtigt werden.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Data availability

All raw data are available on FigShare (DOI: https://doi.org/10.6084/m9.figshare.12585497) and sequences have been uploaded to GenBank (BioProject accession number: PRJNA640644).

References

  1. Agaisse H, Perrimon N (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev 198:72–82. https://doi.org/10.1111/j.0105-2896.2004.0133.x

    CAS  Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  3. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  4. Boag PT, Grant PR (1984) Darwin’s finches (Geospiza) on Isla Daphne Major, Galápagos: Breeding and feeding ecology in a climatically variable environment. Ecol Monogr 54:463–489. https://doi.org/10.2307/1942596

    Article  Google Scholar 

  5. Bukhari S, Mertz AF, Naik S (2019) Eavesdropping on the conversation between immune cells and the skin epithelium. Int Immunol 31:415–422. https://doi.org/10.1093/intimm/dxy088

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Cimadom A, Ulloa A, Meidl P et al (2014) Invasive parasites, habitat change and heavy rainfall reduce breeding success in Darwin’s finches. PLoS ONE 9:e107518. https://doi.org/10.1371/journal.pone.0107518

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Cogen AL, Nizet V, Gallo RL (2008) Skin microbiota: a source of disease or defence? Br J Dermatol 158:442–455. https://doi.org/10.1111/j.1365-2133.2008.08437.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Costello EK, Lauber CL, Hamady M et al (2009) Bacterial community variation in human body habitats across space and time. Science 326:1694–1697. https://doi.org/10.1126/science.1177486

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287:443–449

    CAS  Article  Google Scholar 

  10. Daszak P, Strieby A, Cunningham AA et al (2004) Experimental evidence that the bullfrog (Rana catesbeiana) is a potential carrier of chytridiomycosis, an emerging fungal disease of amphibians. Herpetol J 14:201–207

    Google Scholar 

  11. Davidson C, Benard MF, Shaffer HB et al (2007) Effects of chytrid and carbaryl exposure on survival, growth and skin peptide defenses in foothill yellow-legged frogs. Environ Sci Technol 41:1771–1776. https://doi.org/10.1021/es0611947

    CAS  Article  PubMed  Google Scholar 

  12. Dodge HR, Aitken THG (1968) Philornis Flies from Trinidad (Diptera: Muscidae). J Kansas Entomol Soc 41:134–154

    Google Scholar 

  13. Dudaniec RY, Kleindorfer S, Fessl B (2006) Effects of the introduced ectoparasite Philornis downsi on haemoglobin level and nestling survival in Darwin’s small ground finch (Geospiza fuliginosa). Austral Ecol 31:88–94. https://doi.org/10.1111/j.1442-9993.2006.01553.x

    Article  Google Scholar 

  14. Dudaniec RY, Fessl B, Kleindorfer S (2007) Interannual and interspecific variation in intensity of the parasitic fly, Philornis downsi, in Darwin’s finches. Biol Conserv 139:325–332. https://doi.org/10.1016/j.biocon.2007.07.006

    Article  Google Scholar 

  15. Dvorak M, Fessl B, Nemeth E et al (2019) Survival and extinction of breeding landbirds on San Cristóbal, a highly degraded island in the Galápagos. Bird Conserv Int. https://doi.org/10.1017/s0959270919000285

    Article  Google Scholar 

  16. Edgar RC, Haas BJ, Clemente JC et al (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Federici E, Rossi R, Fidati L et al (2015) Characterization of the skin microbiota in Italian stream frogs (Rana italica) infected and uninfected by a cutaneous parasitic disease. Microbes Environ 30:262–269. https://doi.org/10.1264/jsme2.ME15041

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fessl B, Couri MS (2001) Philornis downsi Dodge & Aitken, new to the Galápagos Islands (Diptera, Muscidae). Stud Dipterologica 8:317–322

    Google Scholar 

  19. Fessl B, Tebbich S (2002) Philornis downsi—a recently discovered parasite on the Galápagos archipelago—a threat for Darwin’s finches? Ibis 144:445–451. https://doi.org/10.1046/j.1474-919X.2002.00076.x

    Article  Google Scholar 

  20. Fessl B, Kleindorfer S, Tebbich S (2006) An experimental study on the effects of an introduced parasite in Darwin’s finches. Biol Conserv 127:55–61. https://doi.org/10.1016/j.biocon.2005.07.013

    Article  Google Scholar 

  21. Fessl B, Young GH, Young RP et al (2010) How to save the rarest Darwin’s finch from extinction: the mangrove finch on Isabela Island. Philos Trans R Soc London B 365:1019–1030. https://doi.org/10.1098/rstb.2009.0288

    Article  Google Scholar 

  22. Fessl B, Heimpel GE, Causton CE (2018) Invasion of an Avian Nest Parasite, Philornis downsi, to the Galápagos Islands: Colonization History, Adaptations to Novel Ecosystems, and Conservation Challenges. In: Parker P (ed) Disease Ecology. Social and Ecological Interactions in the Galapagos Islands. Springer, Cham

  23. Fox J, Weisberg S (2019) An {R} companion to applied regression, Third Edition. Sage, Thousand Oaks CA . URL: https://socialsciences.mcmaster.ca/jfox/Books/Companion/

  24. Gallo RL, Hooper LV (2012) Epithelial antimicrobial defence of the skin and intestine. Nat Rev Immunol 12:503–516. https://doi.org/10.1038/nri3228

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Godoy-Vitorino F, Goldfarb KC, Karaoz U et al (2012) Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. ISME J 6:531–541. https://doi.org/10.1038/ismej.2011.131

    CAS  Article  PubMed  Google Scholar 

  26. Grant P (1999) Ecology and evolution of Darwin’s finches. Princeton University Press, Princeton

    Google Scholar 

  27. Grant PR, Grant BR (1980) Annual variation in finch numbers, foraging and food supply on Isla Daphne Major, Galápagos. Oecologia 46:55–62. https://doi.org/10.1007/BF00346966

    CAS  Article  PubMed  Google Scholar 

  28. Grant BR, Grant PR (1981) Exploitation of Opuntia cactus by birds on the Galápagos. Oecologia 49:179–187. https://doi.org/10.1007/BF00349186

    CAS  Article  PubMed  Google Scholar 

  29. Grindstaff JL, Brodie ED, Ketterson ED (2003) Immune function across generations: Integrating mechanism and evolutionary process in maternal antibody transmission. Proc R Soc B Biol Sci 270:2309–2319. https://doi.org/10.1098/rspb.2003.2485

    Article  Google Scholar 

  30. Grond K, Sandercock BK, Jumpponen A, Zeglin LH (2018) The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol 49:1–19. https://doi.org/10.1111/jav.01788

    Article  Google Scholar 

  31. Heimpel GE, Hillstrom A, Freund D et al (2017) Invasive parasites and the fate of Darwin’s finches in the Galapagos Islands: the case of the vegetarian finch (Platyspiza crassirostris). Wilson J Ornithol 129:345–349. https://doi.org/10.1107/S0907444904010972

    CAS  Article  Google Scholar 

  32. Huttenhower C, Gevers D, Knight R et al (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214. https://doi.org/10.1038/nature11234

    CAS  Article  Google Scholar 

  33. Keesing F, Belden LK, Daszak P et al (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652. https://doi.org/10.1038/nature09575

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 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 1:1. https://doi.org/10.1186/s40850-016-0003-9

    Article  Google Scholar 

  35. Knutie SA (2018) Relationships among introduced parasites, host defenses, and gut microbiota of Galapagos birds. Ecosphere 9:e02286. https://doi.org/10.1002/ecs2.2286

    Article  Google Scholar 

  36. Knutie SA (2020) Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species. J Appl Ecol 57:536–547. https://doi.org/10.1111/1365-2664.13567

  37. Knutie SA, McNew SM, Bartlow AW et al (2014) Darwin’s finches combat introduced nest parasites with fumigated cotton. Curr Biol. https://doi.org/10.1016/j.cub.2014.03.058

    Article  PubMed  Google Scholar 

  38. Knutie SA, Owen JP, Mcnew SM et al (2016) Galápagos mockingbirds tolerate introduced parasites that affect Darwin’s finches. Ecology 97:940–950. https://doi.org/10.1890/15-0119.1

    Article  PubMed  Google Scholar 

  39. Kohl KD (2017) An introductory “how-to” guide for incorporating microbiome research into integrative and comparative biology. Integr Comp Biol 57:674–681. https://doi.org/10.1093/icb/icx013

    Article  PubMed  Google Scholar 

  40. Koop J, Le BC, Clayton D (2013a) Dry year does not reduce invasive parasitic fly prevalence or abundance in Darwin’s finch nests. Rep Parasitol 3:11–17. https://doi.org/10.2147/RIP.S48435

    Article  Google Scholar 

  41. Koop JAH, Owen JP, Knutie SA et al (2013b) Experimental demonstration of a parasite-induced immune response in wild birds: Darwin’s finches and introduced nest flies. Ecol Evol 3:2514–2523. https://doi.org/10.1002/ece3.651

    Article  PubMed  PubMed Central  Google Scholar 

  42. Koop JAH, Kim PS, Knutie SA et al (2016) An introduced parasitic fly may lead to local extinction of Darwin’s finch populations. J Appl Ecol 53:511–518. https://doi.org/10.1111/1365-2664.12575

    Article  PubMed  Google Scholar 

  43. Kozich JJ, Westcott SL, Baxter NT et al (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. https://doi.org/10.1128/AEM.01043-13

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Kumar PS, Mason MR, Brooker MR, O’Brien K (2012) Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol 39:425–433. https://doi.org/10.1111/j.1600-051X.2012.01856.x

    Article  PubMed  PubMed Central  Google Scholar 

  45. Leung JM, Graham AL, Knowles SCL (2018) Parasite-microbiota interactions with the vertebrate gut: synthesis through an ecological lens. Front Microbiol 9:1–20. https://doi.org/10.3389/fmicb.2018.00843

    Article  Google Scholar 

  46. Loo WT, Dudaniec RY, Kleindorfer S, Cavanaugh CM (2019) An inter-island comparison of Darwin’s finches reveals the impact of habitat, host phylogeny, and island on the gut microbiome. PLoS ONE 14:e0226432. https://doi.org/10.1371/journal.pone.0226432

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. McNew SM, Clayton DH (2018) Alien invasion: biology of Philornis flies highlighting Philornis downsi, an introduced parasite of Galápagos birds. Annu Rev Entomol 63:369–387

    CAS  Article  Google Scholar 

  48. Michel AJ, Ward LM, Goffredi SK et al (2018) The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome 6:167. https://doi.org/10.1186/s40168-018-0555-8

    Article  PubMed  PubMed Central  Google Scholar 

  49. Millington SJ, Grant PR (1983) Feeding ecology and territoriality of the cactus finch Geospiza scandens on Isla Daphne Major, Galápagos. Oecologia 58:76–83. https://doi.org/10.1007/BF00384545

    CAS  Article  PubMed  Google Scholar 

  50. Morgan XC, Tickle TL, Sokol H et al (2012) Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 13:79–97

    Article  Google Scholar 

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

    Article  Google Scholar 

  52. O’Connor JA, Robertson J, Kleindorfer S (2014) Darwin’s finch begging intensity does not honestly signal need in parasitised nest. Ethology 120:228–237. https://doi.org/10.1111/eth.12196

    Article  Google Scholar 

  53. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) vegan: Community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan

  54. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci 100:1803–1807. https://doi.org/10.1073/pnas.0335320100

    CAS  Article  PubMed  Google Scholar 

  55. Owen JP, Delany ME, Cardona CJ et al (2009) Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum). Int J Parasitol 39:789–799. https://doi.org/10.1016/j.ijpara.2008.12.008

    Article  PubMed  Google Scholar 

  56. Pasparakis M, Haase I, Nestle FO (2014) Mechanisms regulating skin immunity and inflammation. Nat Rev Immunol 14:289–301. https://doi.org/10.1038/nri3646

    CAS  Article  PubMed  Google Scholar 

  57. Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: imporved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/Nar/Gks1219

    CAS  Article  PubMed  Google Scholar 

  58. Round JL, Mazmanian SK (2009) The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9:313–323. https://doi.org/10.1038/nri2515

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  59. Sampson TR, Mazmanian SK (2015) Control of brain development, function, and behavior by the microbiome. Cell Host Microbe 17:565–576. https://doi.org/10.1016/j.chom.2015.04.011

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. Schloss PD, Westcott SL, Ryabin T et al (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. https://doi.org/10.1128/AEM.01541-09

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  61. Shchipkova AY, Nagaraja HN, Kumar PS (2010) Subgingival microbial profiles of smokers with periodontitis. J Dent Res 89:1247–1253. https://doi.org/10.1177/0022034510377203

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  62. Sorci G, Faivre B (2009) Inflammation and oxidative stress in vertebrate host-parasite systems. Philos Trans R Soc B Biol Sci 364:71–83. https://doi.org/10.1098/rstb.2008.0151

    Article  Google Scholar 

  63. Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. https://doi.org/10.1126/science.1103538

    CAS  Article  PubMed  Google Scholar 

  64. Thaiss CA, Zmora N, Levy M, Elinav E (2016) The microbiome and innate immunity. Nature 535:65–74. https://doi.org/10.1038/nature18847

    CAS  Article  PubMed  Google Scholar 

  65. Tomás G, Martín-Gálvez D, Ruiz-Castellano C et al (2018) Ectoparasite activity during incubation increases microbial growth on avian eggs. Microb Ecol 76:555–564. https://doi.org/10.1007/s00248-017-1140-6

    Article  PubMed  Google Scholar 

  66. van Riper C, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344. https://doi.org/10.2307/1942550

    Article  Google Scholar 

  67. Videvall E, Strandh M, Engelbrecht A et al (2018) Measuring the gut microbiome in birds: comparison of faecal and cloacal sampling. Mol Ecol Resour 18:424–434. https://doi.org/10.1111/1755-0998.12744

    CAS  Article  PubMed  Google Scholar 

  68. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. https://doi.org/10.1128/AEM.00062-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  69. Warner RE (2007) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70:101–120. https://doi.org/10.2307/1365954

    Article  Google Scholar 

  70. Wickham H (2007) Reshaping data with the reshape package. J Stat Softw. https://doi.org/10.18637/jss.v021.i12

    Article  Google Scholar 

  71. Wickham H (2011) The split-apply-combine strategy for data analysis. J Stat Softw. https://doi.org/10.18637/jss.v040.i01

    Article  Google Scholar 

  72. Wickham H, Henry L (2020) tidyr: Tidy messy data. R package version 1.0.2. https://CRAN.R-project.org/package=tidyr

  73. Wilkinson TJ, Cowan AA, Vallin HE et al (2017) Characterization of the microbiome along the gastrointestinal tract of growing turkeys. Front Microbiol 8:1–11. https://doi.org/10.3389/fmicb.2017.01089

    Article  Google Scholar 

  74. Zaiss MM, Harris NL (2016) Interactions between the intestinal microbiome and helminth parasites. Parasite Immunol 38:5–11. https://doi.org/10.1111/pim.12274

    CAS  Article  PubMed  Google Scholar 

  75. Zhu L, Wu Q, Dai J et al (2011) Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci USA 108:17714–17719. https://doi.org/10.1073/pnas.1017956108

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Karla Vasco for her assistance and logistical support and Kendra Maas at the University of Connecticut Microbial Analysis, Resources, and Services for workshop training and advice on the Mothur bioinformatics. We would like to thank the Galápagos Science Center and the Galápagos National Park for support.

Funding

The work was supported by start-up funds, a Research Excellence Program Grant from the University of Connecticut, and a National Science Foundation Grant (DEB-1949858) to SAK and an Office of Undergraduate Research IDEA grant to AMA.

Author information

Affiliations

Authors

Contributions

SAK conceived the study; AMA and SAK conducted the data analyses, and wrote the manuscript; JAH, GJV, LA, TA, KC, SS, TBV collected data; JC provided logistical support. All authors revised and approved the manuscript.

Corresponding author

Correspondence to Sarah A. Knutie.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Our work in 2018–2019 was done under GNP permits PC 03-18 and PC 28-19 and Genetic Access permit MAE-DNB-CM-2016-0041.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by F. Bairlein.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 22 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Addesso, A.M., Harvey, J.A., Vaziri, G.J. et al. Effect of introduced parasites on the survival and microbiota of nestling cactus finches (Geospiza scandens) in the Galápagos Islands. J Ornithol 161, 1011–1019 (2020). https://doi.org/10.1007/s10336-020-01793-6

Download citation

Keywords

  • Darwin’s finch
  • Extirpation
  • Invasive species
  • Microbiome