Abstract
Global plastic production has increased exponentially since the 1940s, resulting in the increased presence of anthropogenic debris in the environment. Recent studies have shown that birds incorporate anthropogenic debris into their nests, which can reduce nest ectoparasite loads. However, we know little about the long-term history of interactions among birds, anthropogenic debris, and ectoparasites. Our study took a unique approach to address this issue by determining the prevalence of anthropogenic debris and ectoparasitic nest flies (Protocalliphora and Passeromyia spp.) in 893 bird nests from 224 species between 1832 and 2018, which were sourced from Australian museum collections. The prevalence of anthropogenic material increased from approximately 4% in 1832 to almost 30% in 2018. This change was driven by an increase in the incorporation of synthetic rather than biodegradable anthropogenic debris (by 2018 ~ 25% of all nests contained synthetics), with the first synthetic item being found in a nest from 1956 in the city of Melbourne. Nest parasite prevalence increased over time but contrary to other studies, there was no relationship between habitat type or anthropogenic material and parasite presence. Our study is the first to use museum specimens to quantify temporal and spatial impacts of anthropogenic material on birds, the results of which justifies contemporary concerns regarding the ubiquitous nature of human impacts on terrestrial wildlife.
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References
Addesso AM, Harvey JA, Vaziri GJ et al (2020) Effect of introduced parasites on the survival and microbiota of nestling cactus finches (Geospiza scandens) in the Galápagos Islands. J Ornithol. https://doi.org/10.1007/s10336-020-01793-6
Antczak M, Hromada M, Czechowski P et al (2010) A new material for old solutions: the case of plastic string used in Great Grey Shrike nests. Acta Ethologica 2:87–91. https://doi.org/10.1007/s10211-010-0077-2
Barnes DKA, Galgani F, Thompson RC, Barlaz M (2009) Accumulation and fragmentation of plastic debris in global environments. Philos Trans R Soc 364:1985–1998. https://doi.org/10.1098/rstb.2008.0205
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Batish DR, Singh HP, Kohli RK, Kaur S (2008) Eucalyptus essential oil as a natural pesticide. For Ecol Manag 256:2166–2174. https://doi.org/10.1016/j.foreco.2008.08.008
Benedict L, Covy NE, Love PA, Stier ST (2020) Human presence outweighs non-anthropogenic factors as a driver of avian nest parasite loads. J Ornithol. https://doi.org/10.1007/s10336-020-01810-8
Blem CR, Blem LB, Harmata PJ (2002) Twine causes significant mortality in nestling ospreys. Wilson J Ornithol 114:528–529. https://doi.org/10.1676/0043-5643(2002)114[0528:TCSMIN]2.0.CO;2
Bond AL, Montevecchi WA, Guse N et al (2012) Prevalence and composition of fishing gear debris in the nests of northern gannets (Morus bassanus) are related to fishing effort. Mar Pollut Bull 64:907–911. https://doi.org/10.1016/j.marpolbul.2012.03.011
Breistøl A, Högstedt G, Lislevand T (2015) Pied Flycatchers Ficedula hypoleuca prefer ectoparasite-free nest sites when old nest material is present. Ornis Norvegica 38:9–13. https://doi.org/10.15845/on.v38i0.871
Bush SE, Clayton DH (2018) Anti-parasite behaviour of birds. Philos Trans R Soc 373:20170196. https://doi.org/10.1098/rstb.2017.0196
Callaghan CT, Major RE, Wilshire JH et al (2019) Generalists are the most urban-tolerant of birds: a phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization. Oikos 128:845–858. https://doi.org/10.1111/oik.06158
Carbó-Ramírez P, González-Arrieta RA, Zuria I (2015) Breeding Biology of the Rufous-backed Robin (Turdus rufopalliatus) in an Urban Area Outside its Original Distribution Range. Wilson J Ornithol 127:515–521. https://doi.org/10.1676/14-056.1
Cartography Associates (2021) David Rumsey historical map collection. The Collection. https://www.davidrumsey.com/. Accessed 20 May 2021
Clayton DH, Koop JAH, Harbison CW et al (2010) How birds combat ectoparasites. Open Ornithol J 3:1
Conole LE, Kirkpatrick JB (2011) Functional and spatial differentiation of urban bird assemblages at the landscape scale. Landsc Urban Plan 100:11–23. https://doi.org/10.1016/j.landurbplan.2010.11.007
de Machado AAS, Kloas W, Zarfl C et al (2018) Microplastics as an emerging threat to terrestrial ecosystems. Glob Change Biol 24:1405–1416. https://doi.org/10.1111/gcb.14020
Delgado-V CA, French K (2012) Parasite–bird interactions in urban areas: Current evidence and emerging questions. Landsc Urban Plan 105:5–14. https://doi.org/10.1016/j.landurbplan.2011.12.019
Department of Agriculture, Water and the Environment ABARES (2018) Australia’s State of the Forests Report. Commonwealth of Australia, Canberra. https://www.agriculture.gov.au/sites/default/files/abares/forestsaustralia/documents/sofr_2018/web%20accessible%20pdfs/SOFR_2018_web.pdf
DeSimone JG, Clotfelter ED, Black EC, Knutie SA (2018) Avoidance, tolerance, and resistance to ectoparasites in nestling and adult tree swallows. J Avian Biol 49:jav-01641. https://doi.org/10.1111/jav.01641
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
Edworthy AB (2016) Avian hosts, prevalence and larval life history of the ectoparasitic fly Passeromyia longicornis (Diptera : Muscidae) in south-eastern Tasmania. Aust J Zool 64:100–106. https://doi.org/10.1071/ZO15060
Edworthy AB, Langmore NE, Heinsohn R (2019) Native fly parasites are the principal cause of nestling mortality in endangered Tasmanian pardalotes. Anim Conserv 22:96–103. https://doi.org/10.1111/acv.12444
Gall SC, Thompson RC (2015) The impact of debris on marine life. Mar Pollut Bull 92:170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041
Grab KM, Hiller BJ, Hurlbert JH et al (2019) Host tolerance and resistance to parasitic nest flies differs between two wild bird species. Ecol Evol 9:12144–12155. https://doi.org/10.1002/ece3.5682
Gwinner H, Berger S (2005) European starlings: nestling condition, parasites and green nest material during the breeding season. J Ornithol 146:365–371. https://doi.org/10.1007/s10336-005-0012-x
Hanmer HJ, Thomas RL, Beswick GJF et al (2017) Use of anthropogenic material affects bird nest arthropod community structure: influence of urbanisation, and consequences for ectoparasites and fledging success. J Ornithol 158:1045–1059. https://doi.org/10.1007/s10336-017-1462-7
Hartwig E, Clemens T, Heckroth M (2007) Plastic debris as nesting material in a Kittiwake (Rissa tridactyla) colony at the Jammerbugt, Northwest Denmark. Mar Pollut Bull 54:595–597. https://doi.org/10.1016/j.marpolbul.2007.01.027
Harvey JA, Chernicky K, Simons SR et al (2020) Urban living influences the reproductive success of Darwin’s finches in the Galápagos Islands. bioRxiv. https://doi.org/10.1101/2020.07.08.193623
Harvey JA, Chernicky K, Simons SR et al (2021) Urban living influences the nesting success of Darwin’s finches in the Galápagos Islands. Ecol Evol 11:5038–5048. https://doi.org/10.1002/ece3.7360
Henry P-Y, Wey G, Balança G (2011) Rubber Band Ingestion by a Rubbish Dump Dweller, the White Stork (Ciconia ciconia). Cowa 34:504–508. https://doi.org/10.1675/063.034.0414
Huber SK (2008) Effects of the introduced parasite Philornis downsi on nestling growth and mortality in the medium ground finch (Geospiza fortis). Biol Cons 141:601–609. https://doi.org/10.1016/j.biocon.2007.11.012
Jagiello ZA, Dylewski Ł, Winiarska D et al (2018) Factors determining the occurrence of anthropogenic materials in nests of the white stork Ciconia ciconia. Environ Sci Pollut Res 25:14726–14733. https://doi.org/10.1007/s11356-018-1626-x
Jagiello Z, Dylewski Ł, Tobolka M, Aguirre JI (2019) Life in a polluted world: a global review of anthropogenic materials in bird nests. Environ Pollut 251:717–722. https://doi.org/10.1016/j.envpol.2019.05.028
Jagiello Z, López-García A, Aguirre JI, Dylewski Ł (2020) Distance to landfill and human activities affects the debris incorporation into the white stork nests in urbanized landscape in central Spain. Environ Sci Pollut Res 27:30893–30898. https://doi.org/10.1007/s11356-020-09621-3
Kenyon KW, Kridler E (1969) Laysan albatrosses swallow indigestible matter. Auk 86:339–343. https://doi.org/10.2307/4083505
Kleindorfer S, Dudaniec RY (2009) Love thy neighbour? Social nesting pattern, host mass and nest size affect ectoparasite intensity in Darwin’s tree finches. Behav Ecol Sociobiol 63:731–739. https://doi.org/10.1007/s00265-008-0706-1
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
Kumar P, Mishra S, Malik A, Satya S (2012) Compositional analysis and insecticidal activity of Eucalyptus globulus (family: Myrtaceae) essential oil against housefly (Musca domestica). Acta Trop 122:212–218. https://doi.org/10.1016/j.actatropica.2012.01.015
Lee K, Jang YC, Hong S et al (2015) Plastic marine debris used as nesting materials of the endangered species black-faced spoonbill platalea minor decreases by conservation activities. J Korean Soc Mar Environ Energy 18:45–49. https://doi.org/10.7846/JKOSMEE.2015.18.1.45
Liu X, Chen Q, Wang Z et al (2008) Allelopathic effects of essential oil from Eucalyptus grandis × E. urophylla on pathogenic fungi and pest insects. Front China 3:232–236. https://doi.org/10.1007/s11461-008-0036-5
Loye JE, Zuk M (eds) (1991) Bird-parasite interactions: ecology, evolution and behaviour. Oxford University Press, Oxford
Malizia A, Monmany-Garzia AC (2019) Terrestrial ecologists should stop ignoring plastic pollution in the Anthropocene time. Sci Total Environ 668:1025–1029. https://doi.org/10.1016/j.scitotenv.2019.03.044
Martínez-de la Puente J, Merino S, Tomás G et al (2011) Nest ectoparasites increase physiological stress in breeding birds: an experiment. Naturwissenschaften 98:99–106. https://doi.org/10.1007/s00114-010-0746-z
Mennerat A, Perret P, Caro SP et al (2008) Aromatic plants in blue tit Cyanistes caeruleus nests: no negative effect on blood-sucking Protocalliphora blow fly larvae. J Avian Biol 39:127–132. https://doi.org/10.1111/j.0908-8857.2008.04400.x
Mennerat A, Mirleau P, Blondel J et al (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855. https://doi.org/10.1007/s00442-009-1418-6
Mennerat A, Charmantier A, Perret P et al (2018) Parasite intensity is driven by temperature in a wild passerine bird. BioRxiv 49:323311. https://doi.org/10.1101/323311
Mo M (2015) The Red-whiskered Bulbul Pycnonotus jocosus in Australia: a global perspective, history of introduction, current status and potential impacts. Aust Zool 37:461–471. https://doi.org/10.7882/AZ.2015.014
Møller AP (2017) Fashion and out of fashion: appearance and disappearance of a novel nest building innovation. Avian Res 8:14. https://doi.org/10.1186/s40657-017-0072-7
Montevecchi WA (2011) Incidence and types of plastic in gannets’ nests in the northwest Atlantic. Can J Zool 69:295–297. https://doi.org/10.1139/z91-047
Moore E, Lyday S, Roletto J et al (2009) Entanglements of marine mammals and seabirds in central California and the north-west coast of the United States 2001–2005. Mar Pollut Bull 58:1045–1051. https://doi.org/10.1016/j.marpolbul.2009.02.006
Ontiveros D, Caro J, Pleguezuelos JM (2008) Green plant material versus ectoparasites in nests of Bonelli’s eagle. J Zool 274:99–104. https://doi.org/10.1111/j.1469-7998.2007.00364.x
PlasticsEurope (2010) Plastics – the Facts 2010: An analysis of European plastics production, demand and recovery for 2009. Association of Plastics Manufacturers, Brussels. https://www.plasticseurope.org/en/resources/publications/171-plastics-facts-2010
Podolsky RH, Kress SW (1989) Plastic debris incorporated into double-crested cormorant nests in the Gulf of Maine. J Field Ornithol 60:248–250
Quiroga MA, Hayes TI, Hayes CD et al (2020) More than just nestlings: incidence of subcutaneous Philornis (Diptera: Muscidae) nest flies in adult birds. Parasitol Res 119:2337–2342. https://doi.org/10.1007/s00436-020-06696-2
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Reynolds SJ, Davies CS, Elwell E et al (2016) Does the urban gradient influence the composition and ectoparasite load of nests of an urban bird species? Avian Biology Research 9:224–234. https://doi.org/10.3184/175815516X14725499175665
Reynolds SJ, Ibáñez-Álamo JD, Sumasgutner P, Mainwaring MC (2019) Urbanisation and nest building in birds: a review of threats and opportunities. J Ornithol 160:841–860. https://doi.org/10.1007/s10336-019-01657-8
Ryan PG, Moore CJ, van Franeker JA, Moloney CL (2009) Monitoring the abundance of plastic debris in the marine environment. Philos Trans R Soc 364:1999–2012. https://doi.org/10.1098/rstb.2008.0207
Sabrosky CW, Bennett GF, Whitworth TL (1989) Bird blow flies (Protocalliphora) in North America (Diptera: Calliphoridae) with notes on Palearctic species. Smithsonian Institution Press, Washington
Scholl PJ, Colwell DD, Cepeda-Palacios R (2019) Chapter 19: myiasis (Muscoidea, Oestroidea). In: Mullen GR, Durden LA (eds) Medical and veterinary entomology, 3rd edn. Academic Press, London, pp 383–419
Scott-Baumann JF, Morgan ER (2015) A review of the nest protection hypothesis: does inclusion of fresh green plant material in birds’ nests reduce parasite infestation? Parasitology 142:1016–1023. https://doi.org/10.1017/S0031182015000189
Sergio F, Blas J, Blanco G et al (2011) Raptor nest decorations are a reliable threat against conspecifics. Science 331:327–330. https://doi.org/10.1126/science.1199422
Suárez-Rodríguez M, Garcia CM (2014) There is no such a thing as a free cigarette; lining nests with discarded butts brings short-term benefits, but causes toxic damage. J Evol Biol 27:2719–2726. https://doi.org/10.1111/jeb.12531
Suárez-Rodríguez M, Garcia CM (2017) An experimental demonstration that house finches add cigarette butts in response to ectoparasites. J Avian Biol 48:1316–1321. https://doi.org/10.1111/jav.01324
Suárez-Rodríguez M, López-Rull I, Macías Garcia C (2013) Incorporation of cigarette butts into nests reduces nest ectoparasite load in urban birds: new ingredients for an old recipe? Biol Let 9:20120931. https://doi.org/10.1098/rsbl.2012.0931
Sukontason KL, Boonchu N, Sukontason K, Choochote W (2004) Effects of eucalyptol on house fly (Diptera: Muscidae) and blow fly (Diptera: Calliphoridae). Rev Inst Med Trop Sao Paulo 46:97–101. https://doi.org/10.1590/S0036-46652004000200008
Tavares DC, da Costa LL, Rangel DF et al (2016) Nests of the brown booby (Sula leucogaster) as a potential indicator of tropical ocean pollution by marine debris. Ecol Ind 70:10–14. https://doi.org/10.1016/j.ecolind.2016.06.005
Thompson FR, Burhans DE (2003) Predation of songbird nests differs by predator and between field and forest habitats. J Wildl Manag 67:408–416. https://doi.org/10.2307/3802781
Thompson RC, Moore CJ, vom Saal FS, Swan SH (2009) Plastics, the environment and human health: current consensus and future trends. Philos Trans R Soc 364:2153–2166. https://doi.org/10.1098/rstb.2009.0053
Tomás G, Merino S, Martínez-de la Puente J et al (2012) Interacting effects of aromatic plants and female age on nest-dwelling ectoparasites and blood-sucking flies in avian nests. Behav Proc 90:246–253. https://doi.org/10.1016/j.beproc.2012.02.003
Townsend AK, Barker CM (2014) Plastic and the Nest Entanglement of Urban and Agricultural Crows. PLoS ONE 9:e88006. https://doi.org/10.1371/journal.pone.0088006
Verlis KM, Campbell ML, Wilson SP (2014) Marine debris is selected as nesting material by the brown booby (Sula leucogaster) within the Swain Reefs, Great Barrier Reef, Australia. Mar Pollut Bull 87:180–190. https://doi.org/10.1016/j.marpolbul.2014.07.060
Votier SC, Archibald K, Morgan G, Morgan L (2011) The use of plastic debris as nesting material by a colonial seabird and associated entanglement mortality. Mar Pollut Bull 62:168–172. https://doi.org/10.1016/j.marpolbul.2010.11.009
Wang YW, Chen SC, Jiang PJ, Ding PD (2008) Black-billed Magpies (Pica pica) adjust nest characteristics to adapt to urbanization in Hangzhou, China. Can J Zool 86:676–684. https://doi.org/10.1139/Z08-045
Wang Y, Chen S, Blair RB et al (2009) Nest Composition Adjustments by Chinese Bulbuls Pycnonotus sinensis in an Urbanized Landscape of Hangzhou (E China). Acta Ornithologica 44:185–192. https://doi.org/10.3161/000164509X482768
Acknowledgements
We thank Leo Joseph from CSIRO in Canberra and Karen Roberts from Melbourne Museum for access to collections. Funding for this project was provided by DAAD Rise Worldwide and a USC internal grant.
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DAP conceived and designed the study, DAP, FO, and KAT undertook data collection and initial data interpretation, FO and DAP conducted statistical analyses and wrote the first manuscript draft, DAP, FO, and SAK produced figures, and DAP, FO, KAT, and SAK contributed to further results interpretation, background research, writing and editing of the manuscript.
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Potvin, D.A., Opitz, F., Townsend, K.A. et al. Use of anthropogenic-related nest material and nest parasite prevalence have increased over the past two centuries in Australian birds. Oecologia 196, 1207–1217 (2021). https://doi.org/10.1007/s00442-021-04982-z
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DOI: https://doi.org/10.1007/s00442-021-04982-z