Understanding spatiotemporal effects of food supplementation on host-parasite interactions using community-based science.
citizen science
disease ecology
ectoparasites
food supplementation
host–parasite interactions
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
24 Jul 2024
24 Jul 2024
Historique:
received:
06
12
2023
accepted:
11
07
2024
medline:
26
7
2024
pubmed:
26
7
2024
entrez:
25
7
2024
Statut:
aheadofprint
Résumé
Supplemental feeding can increase the overall health of animals but also can have variable effects on how animals defend themselves against parasites. However, the spatiotemporal effects of food supplementation on host-parasite interactions remain poorly understood, likely because large-scale, coordinated efforts to investigate them are difficult. Here, we introduce the Nest Parasite Community Science Project, which is a community-based science project that coordinates studies with bird nest box 'stewards' from the public and scientific community. This project was established to understand broad ecological patterns between hosts and their parasites. The goal of this study was to determine the effect of food supplementation on eastern bluebirds (Sialia sialis) and their nest parasite community across the geographic range of the bluebirds from 2018 to 2021. We received 674 nests from 69 stewards in 26 states in the eastern United States. Nest box stewards reported whether or not they provided mealworms or suet near nesting bluebirds, then they followed the nesting success of the birds (number of eggs laid and hatched, proportion that hatched, number and proportion of nestlings that successfully fledged). We then identified and quantified parasites in the nests. Overall, we found that food supplementation increased fledging success. The most common nest parasite taxon was the parasitic blow fly (Protocalliphora sialia), but a few nests contained fleas (Ceratophyllus idius, C. gallinae and Orchopeas leucopus) and mites (Dermanyssus spp. and Ornithonyssus spp.). Blow flies were primarily found at northern latitudes, where food supplementation affected blow fly prevalence. However, the direction of this effect varied substantially in direction and magnitude across years. More stewards fed bluebirds at southern latitudes than at northern latitudes, which contradicts the findings of other community-based science projects. Overall, food supplementation of birds was associated with increased host fitness but did not appear to play a consistent role in defence against these parasites across all years. Our study demonstrates the importance of coordinated studies across years and locations to understand the effects of environmental heterogeneity, including human-based food supplementation, on host-parasite dynamics.
Identifiants
pubmed: 39049456
doi: 10.1111/1365-2656.14155
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Science Foundation, Directorate for Biological Sciences
ID : DEB-2211287
Organisme : National Science Foundation, Directorate for Biological Sciences
ID : IOS-2143899
Organisme : University of Connecticut: Start-up Funds and Summer Undergraduate Research Fellowship
Organisme : Summer Undergraduate Research Fellowship from the University of Connecticut
Organisme : North American Bluebird Society: Research Grant
Organisme : Wissenschaftskolleg zu Berlin: College for Life Sciences Fellowship
Informations de copyright
© 2024 The Author(s). Journal of Animal Ecology © 2024 British Ecological Society.
Références
Albert, L., Rumschlag, S., Parker, A., Vaziri, G., & Knutie, S. A. (2023). Elevated nest temperature has opposing effects on host species infested with parasitic nest flies. Oecologia, 201(4), 877–886. https://doi.org/10.1007/s00442‐023‐05343‐8
Albery, G. F., Becker, D. J., Kenyon, F., Nussey, D. H., & Pemberton, J. M. (2019). The fine‐scale landscape of immunity and parasitism in a wild ungulate population. Integrative and Comparative Biology, 59(5), 1165–1175. https://doi.org/10.1093/icb/icz016
Albery, G. F., Sweeny, A. R., Becker, D. J., & Bansal, S. (2022). Fine‐scale spatial patterns of wildlife disease are common and understudied. Functional Ecology, 36(1), 214–225. https://doi.org/10.1111/1365‐2435.13942
Bailey, R. L., & Bonter, D. N. (2022). Large‐scale supplemental feeding alters lay date and nest survival in Eastern Bluebirds but not in two species of chickadees. Ornithological Applications, 124(1), duab046. https://doi.org/10.1093/ornithapp/duab046
Becker, D. J., Hall, R. J., Forbes, K. M., Plowright, R. K., & Altizer, S. (2018). Anthropogenic resource subsidies and host–parasite dynamics in wildlife. Philosophical Transactions of the Royal Society, B: Biological Sciences, 373(1745), 20170086. https://doi.org/10.1098/rstb.2017.0086
Becker, D. J., Streicker, D. G., & Altizer, S. (2015). Linking anthropogenic resources to wildlife–pathogen dynamics: A review and meta‐analysis. Ecology Letters, 18(5), 483–495. https://doi.org/10.1111/ele.12428
Burtt, E. H., Jr., Chow, W., & Babbitt, G. A. (1991). Occurrence and demography of mites of tree swallow, house wren, and eastern bluebird nests. In Bird‐parasite interactions (pp. 104–122). Oxford University Press.
Christe, P., Oppliger, A., & Richner, H. (1994). Ectoparasite affects choice and use of roost sites in the great tit, Parus major. Animal Behaviour, 47(4), 895–898. https://doi.org/10.1006/anbe.1994.1121
Coop, R. L., & Kyriazakis, I. (2001). Influence of host nutrition on the development and consequences of nematode parasitism in ruminants. Trends in Parasitology, 17(7), 325–330. https://doi.org/10.1016/S1471‐4922(01)01900‐6
Cornelius Ruhs, E., Vézina, F., & Karasov, W. H. (2019). Physiological and immune responses of free‐living temperate birds provided a gradient of food supplementation. Physiological and Biochemical Zoology, 92(1), 106–114. https://doi.org/10.1086/701389
Cox, D. T. C., & Gaston, K. J. (2016). Urban bird feeding: Connecting people with nature. PLoS One, 11(7), e0158717. https://doi.org/10.1371/journal.pone.0158717
Cox, D. T. C., & Gaston, K. J. (2018). Human–nature interactions and the consequences and drivers of provisioning wildlife. Philosophical Transactions of the Royal Society, B: Biological Sciences, 373(1745), 20170092. https://doi.org/10.1098/rstb.2017.0092
Datta, F. U., Nolan, J. V., Rowe, J. B., & Gray, G. D. (1998). Protein supplementation improves the performance of parasitised sheep fed a straw‐based diet. International Journal for Parasitology, 28(8), 1269–1278. https://doi.org/10.1016/S0020‐7519(98)00104‐0
Di Palma, A., Giangaspero, A., Cafiero, M. A., & Germinara, G. S. (2012). A gallery of the key characters to ease identification of Dermanyssus gallinae (Acari: Gamasida: Dermanyssidae) and allow differentiation from Ornithonyssus sylviarum (Acari: Gamasida: Macronyssidae). Parasites & Vectors, 5(1), 104. https://doi.org/10.1186/1756‐3305‐5‐104
Dunn, E. H., & Tessaglia‐Hymes, D. L. (2001). Birds at your feeder: A guide to feeding habits behavior distribution and abundance. WW Norton & Company.
Galbraith, J. A., Beggs, J. R., Jones, D. N., McNaughton, E. J., Krull, C. R., & Stanley, M. C. (2014). Risks and drivers of wild bird feeding in urban areas of New Zealand. Biological Conservation, 180, 64–74. https://doi.org/10.1016/j.biocon.2014.09.038
Gowaty, P. A., & Plissner, J. H. (2020). Eastern bluebird (Sialia sialis). In A. F. Poole (Ed.), Birds of the world (1st ed.). Cornell Lab of Ornithology. https://doi.org/10.2173/bow.easblu.01
Grab, K. M., Hiller, B. J., Hurlbert, J. H., Ingram, M. E., Parker, A. B., Pokutnaya, D. Y., & Knutie, S. A. (2019). Host tolerance and resistance to parasitic nest flies differs between two wild bird species. Ecology and Evolution, 9(21), 12144–12155. https://doi.org/10.1002/ece3.5682
Holland, G. P. (1951). Notes on some bird fleas, with the description of a new species of. The Canadian Entomologist, 83(11), 281–289. https://doi.org/10.4039/Ent83281‐11
Holland, G. P. (1985). The fleas of Canada, Alaska, and Greenland (Siphonaptera). The Memoirs of the Entomological Society of Canada, 117(S130), 3–632. https://doi.org/10.4039/entm117130fv
Horn, D. J., & Johansen, S. M. (2013). A comparison of bird‐feeding practices in the United States and Canada. Wildlife Society Bulletin, 37(2), 293–300. https://doi.org/10.1002/wsb.281
Howick, V. M., & Lazzaro, B. P. (2014). Genotype and diet shape resistance and tolerance across distinct phases of bacterial infection. BMC Evolutionary Biology, 14(1), 56. https://doi.org/10.1186/1471‐2148‐14‐56
Jones, D. (2011). An appetite for connection: Why we need to understand the effect and value of feeding wild birds. Emu ‐ Austral Ornithology, 111(2), i–vii. https://doi.org/10.1071/MUv111n2_ED
Knee, W., & Proctor, H. (2006). Keys to the families and genera of blood and tissue feeding mites associated with Albertan birds. Canadian Journal of Arthropod Identification, 2(2), 1–18. https://doi.org/10.3752/cjai.2006.02
Knutie, S. A. (2020). Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species. Journal of Applied Ecology, 57(3), 536–547. https://doi.org/10.1111/1365‐2664.13567
Knutie, S. A., & Albery, G. F. (2024). Data from: Understanding spatiotemporal effects of food supplementation on host‐parasite interactions using community‐based science. Figshare. figshare. https://doi.org/10.6084/m9.figshare.26045368.v1
Lack, D. (1947). The significance of clutch‐size. Ibis, 89(2), 302–352. https://doi.org/10.1111/j.1474‐919X.1947.tb04155.x
Lewis, R. E. (2000). A taxonomic review of the North American genus Orchopeas Jordan, 1933 (Siphonaptera: Ceratophyllidae: Ceratophyllinae). Journal of Vector Ecology, 25(2), 164–189.
Lindgren, F., & Rue, H. (2015). Bayesian spatial modelling with R‐INLA. Journal of Statistical Software, 63(19), 1–25. http://www.jstatsoft.org/v63/i19
Lindgren, F., Rue, H., & Lindström, J. (2011). An explicit link between Gaussian fields and Gaussian Markov random fields: The stochastic partial differential equation approach. Journal of the Royal Statistical Society, Series B: Statistical Methodology, 73(4), 423–498. https://doi.org/10.1111/j.1467‐9868.2011.00777.x
Lochmiller, R. L., & Deerenberg, C. (2000). Trade‐offs in evolutionary immunology: Just what is the cost of immunity? Oikos, 88(1), 87–98. https://doi.org/10.1034/j.1600‐0706.2000.880110.x
Lochmiller, R. L., Vestey, M. R., & Boren, J. C. (1993). Relationship between protein nutritional status and immunocompetence in northern bobwhite chicks. The Auk, 110(3), 503–510. https://doi.org/10.2307/4088414
Moon, R. D. (1980). Effects of larval competition on face fly 1. Environmental Entomology, 9(3), 325–330. https://doi.org/10.1093/ee/9.3.325
Murillo, A. C., & Mullens, B. A. (2017). A review of the biology, ecology, and control of the northern fowl mite, Ornithonyssus sylviarum (Acari: Macronyssidae). Veterinary Parasitology, 246, 30–37. https://doi.org/10.1016/j.vetpar.2017.09.002
Murray, M. H., Becker, D. J., Hall, R. J., & Hernandez, S. M. (2016). Wildlife health and supplemental feeding: A review and management recommendations. Biological Conservation, 204, 163–174. https://doi.org/10.1016/j.biocon.2016.10.034
Musgrave, K., Bartlow, A. W., & Fair, J. M. (2019). Long‐term variation in environmental conditions influences host–parasite fitness. Ecology and Evolution, 9(13), 7688–7703. https://doi.org/10.1002/ece3.5321
Orros, M. E., & Fellowes, M. D. (2015). Wild bird feeding in an urban area: intensity, economics and numbers of individuals supported. Acta Ornithologica, 50(1), 43–58. https://doi.org/10.3161/00016454AO2015.50.1.006
Phillips, T., & Dickinson, J. (2009). Tracking the nesting success of North America's breeding birds through public participation in NestWatch. In Proceedings of the Fourth International Partners in Flight Conference: Tundra to tropics (pp. 633–640). McAllen.
Pinkowski, B. C. (1977). Foraging behavior of the eastern bluebird. The Wilson Bulletin, 89(3), 404–414. https://www.jstor.org/stable/4160942
Proctor, H., Owens, I., Proctor, H., Owens, I., Proctor, H., Owens, I., Proctor, H., Owens, I., Proctor, H., & Owens, I. (2000). Mites and birds: Diversity, parasitism and coevolution. Trends in Ecology & Evolution, 15(9), 358–364. https://doi.org/10.1016/S0169‐5347(00)01924‐8
R Core Team. (2023). R: A language and environment for statistical computing [Computer software]. R Foundation for Statistical Computing. https://www.R‐project.org/
Read, A. F., Graham, A. L., & Råberg, L. (2008). Animal defenses against infectious agents: Is damage control more important than pathogen control. PLoS Biology, 6(12), e1000004. https://doi.org/10.1371/journal.pbio.1000004
Robb, G. N., McDonald, R. A., Chamberlain, D. E., & Bearhop, S. (2008). Food for thought: Supplementary feeding as a driver of ecological change in avian populations. Frontiers in Ecology and the Environment, 6(9), 476–484. https://doi.org/10.1890/060152
Sánchez, C. A., Becker, D. J., Teitelbaum, C. S., Barriga, P., Brown, L. M., Majewska, A. A., Hall, R. J., & Altizer, S. (2018). On the relationship between body condition and parasite infection in wildlife: A review and meta‐analysis. Ecology Letters, 21(12), 1869–1884. https://doi.org/10.1111/ele.13160
Sabrosky, C. W., Bennett, G. F., & Whitworth, T. L. (1989). Bird blow flies (Protocalliphora) in North America (Diptera: Calliphoridae) with notes on Palearctic species. Smithsonian Institution Press.
Sauer, J. R., & Droege, S. (1990). Recent population trends of the eastern bluebird. The Wilson Bulletin, 102(2), 239–252. https://www.jstor.org/stable/4162862
Schmidt, C. D., & Blume, R. R. (1973). Laboratory‐reared horn flies:1 relationships between width of head and weight of pupa in both sexes and between these measurements and number of Ovarioles in females. Annals of the Entomological Society of America, 66(6), 1307–1308. https://doi.org/10.1093/aesa/66.6.1307
Shaw, A., Miller, K. K., & Wescott, G. (2017). Australian native gardens: Is there scope for a community shift? Landscape and Urban Planning, 157, 322–330. https://doi.org/10.1016/j.landurbplan.2016.07.009
Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade‐offs in evolutionary ecology. Trends in Ecology & Evolution, 11(8), 317–321. https://doi.org/10.1016/0169‐5347(96)10039‐2
Strandin, T., Babayan, S. A., & Forbes, K. M. (2018). Reviewing the effects of food provisioning on wildlife immunity. Philosophical Transactions of the Royal Society, B: Biological Sciences, 373(1745), 20170088. https://doi.org/10.1098/rstb.2017.0088
Sullivan, B. L., Wood, C. L., Iliff, M. J., Bonney, R. E., Fink, D., & Kelling, S. (2009). eBird: A citizen‐based bird observation network in the biological sciences. Biological Conservation, 142(10), 2282–2292. https://doi.org/10.1016/j.biocon.2009.05.006
Tollington, S., Ewen, J. G., Newton, J., McGill, R. A. R., Smith, D., Henshaw, A., Fogell, D. J., Tatayah, V., Greenwood, A., Jones, C. G., & Groombridge, J. J. (2019). Individual consumption of supplemental food as a predictor of reproductive performance and viral infection intensity. Journal of Applied Ecology, 56(3), 594–603. https://doi.org/10.1111/1365‐2664.13303
Tschirren, B., Bischoff, L. L., Saladin, V., & Richner, H. (2007). Host condition and host immunity affect parasite fitness in a bird–ectoparasite system. Functional Ecology, 21(2), 372–378. https://doi.org/10.1111/j.1365‐2435.2007.01235.x
US Fish and Wildlife Service (2012) 2011 National survey of fishing, hunting, and wildlife‐associated recreation ‐ National Overview, http://wsfrprograms.fws.gov/Subpages/NationalSurvey/National_Survey.html
Whitworth, T. (2003a). A key to the puparia of 27 species of North American Protocalliphora Hough (Diptera: Calliphoridae) from bird nests and two new puparial descriptions. Proceedings of the Entomological Society of Washington, 104, 995–1033.
Whitworth, T. (2003b). A new species of North American Protocalliphora hough (Diptera: Calliphoridae) from bird nests. Proceedings of the Entomological Society of Washington, 105, 801–811.
Wilcoxen, T. E., Horn, D. J., Hogan, B. M., Hubble, C. N., Huber, S. J., Flamm, J., Knott, M., Lundstrom, L., Salik, F., Wassenhove, S. J., & Wrobel, E. R. (2015). Effects of bird‐feeding activities on the health of wild birds. Conservation Physiology, 3(1), cov058. https://doi.org/10.1093/conphys/cov058
Winkler, D. W. (1993). Use and importance of feathers as nest lining in tree swallows (Tachycineta Bicolor). The Auk, 110(1), 29–36. https://www.jstor.org/stable/4088228
Winkler, D. W., Luo, M. K., & Rakhimberdiev, E. (2013). Temperature effects on food supply and chick mortality in tree swallows (Tachycineta bicolor). Oecologia, 173(1), 129–138. https://doi.org/10.1007/s00442‐013‐2605‐z