Abstract
Globally, grassland and farmland birds have experienced population declines due to habitat loss associated with increasing agricultural land-use intensity. These modified environments can reduce insect availability for aerial insectivorous birds and agricultural development is a leading hypothesis for declines in this guild. Our objective was to investigate the relationship between landscape composition and diet of nestling Barn Swallows (Hirundo rustica) raised in a mixed agroecosystem in southern Ontario, Canada. We used nestling feather stable-isotope (δ13C and δ15N) measurements and DNA barcoding of nestling fecal matter to elucidate nestling diets. Nestling feather isotope values were related to agricultural land use, indicating differences in diet, or diet source that varied with proportion of agricultural crops. In 1 year, we found reduced diet richness in areas with increased amounts of row crop, otherwise measures of taxonomic richness and composition of nestling diet showed no relationship with the proportion of row crop, which suggests similar diets in heavily cropped and less cropped landscapes. Additionally, amount of water in the surrounding landscape was associated with increased diet richness. Overall, isotopic measurements and fecal barcoding suggest that nestling Barn Swallows raised within our agroecosystem were provisioned insects from agricultural food webs for at least part of their diet. There was little evidence to support nestling diet composition or richness changes with increased agricultural intensity, at current (low) nesting densities.
Zusammenfassung
Nahrung von Nestlingen der Rauchschwalbe in einem Agrarökosystem: Erkenntnisse aus DNA-Barcoding von Kotproben und Stabilen Isotopen (δ13C, δ15N) von Federn
Weltweit sind die Populationen von Wiesen- und Feldvögeln aufgrund von Lebensraumverlusten in Verbindung mit zunehmender landwirtschaftlicher Landnutzung zurückgegangen. Diese veränderten Landschaften können die Insektenverfügbarkeit für Vögel, die sich von flugfähigen Insekten ernähren, reduzieren und die landwirtschaftliche Entwicklung ist eine zentrale Hypothese für den Rückgang in diesen Bereich. Unser Ziel war es, die Beziehung zwischen der Landschaftszusammensetzung und der Ernährung von Nestlingen der Rauchschwalbe (Hirundo rustica) zu untersuchen, die in einem gemischten Agrarökosystem im Süden Ontarios, Kanada, aufwuchsen. Wir verwendeten Messungen von Stabilen Isotopen (δ 13 C und δ 15 N) in den Federn und DNA-Barcoding aus dem Kot von Nestlingen, um die Ernährung der Nestlinge aufzuklären. Die Federisotopenwerte der Nestlinge konnten mit der landwirtschaftlichen Nutzung in Beziehung gesetzt werden, was auf Unterschiede in der Nahrungszusammensetzung oder -quelle hindeutet, die mit dem Anteil der landwirtschaftlichen Kulturpflanzen variierten. In einem Jahr fanden wir einen geringeren Nahrungsreichtum in Gebieten mit erhöhtem Anteil an Reihenkulturen. Ansonsten zeigten die Messungen des taxonomischen Reichtums und der Zusammensetzung der Nestlingsnahrung keinen Zusammenhang mit dem Anteil an Reihenkulturen, was auf eine ähnliche Ernährung in stark und weniger stark bewirtschafteten Landschaften schließt lässt. Zusätzlich war die Wassermenge in der umgebenden Landschaft mit einem erhöhtem Nahrungsreichtum verbunden. Zusammenfassend deuten die isotopischen Messungen und das Barcoding der Kotproben darauf hin, dass die Nestlinge der Rauchschwalben, die in dem von uns untersuchten Agrarökosystem aufwuchsen, zumindest einen Teil ihrer Nahrung aus Insekten aus landwirtschaftlichen Nahrungsnetzen bezogen. Bei den derzeitigen (niedrigen) Nestdichten gab es wenige Hinweise darauf, dass sich die Zusammensetzung oder der Reichtum der Nestlingsnahrung mit zunehmender landwirtschaftlicher Intensität ändert.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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References
Agriculture and Agri-Food Canada (2016) Annual Crop Inventory 2016. Government of Canada. https://www5.agr.gc.ca/atlas/rest/services/servicesimage/inventaire_des_cultures_2016/ImageServer. Accessed 17 May 2017
Agriculture and Agri-Food Canada (2017) Annual Crop Inventory 2017. Government of Canada. https://www5.agr.gc.ca/atlas/rest/services/imageservices/annual_crop_inventory_2017/ImageServer. Accessed 26 Mar 2018
Aizpurua O, Budinski I, Georgiakakis P et al (2017) Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: evidence from DNA metabarcoding. Mol Ecol 27:815–825. https://doi.org/10.1111/mec.14474
Ambrosini R, Rubolini D, Trovo P et al (2012) Maintenance of livestock farming may buffer population decline of the Barn Swallow Hirundo rustica. Bird Conserv Int 22:411–428. https://doi.org/10.1017/S0959270912000056
Anderson C, Cabana G (2005) δ15N in riverine food webs: effects of N inputs from agricultural watersheds. Can J Fish Aquat Sci 62:333–340. https://doi.org/10.1139/f04-191
Anderson M, Gorley R, Clarke K (2008) PEzRMANOVA+ for PRIMER: Guide to Software and Statistical Methods. Plymouth, UK
Arbeiter S, Schulze M, Tamm P, Hahn S (2016) Strong cascading effect of weather conditions on prey availability and annual breeding performance in European bee-eaters Merops apiaster. J Ornithol 157:155–163. https://doi.org/10.1007/s10336-015-1262-x
Attwood S, Maron M, House A, Zammit C (2008) Do arthropod assemblages display globally consistent responses to intensified agricultural land use and management? Glob Ecol Biogeogr 17:585–599. https://doi.org/10.1111/j.1466-8238.2008.00399.x
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
Bellavance V, Bélisle M, Savage J et al (2018) Influence of agricultural intensification on prey availability and nestling diet in Tree Swallows (Tachycineta bicolor). Can J Zool 96:1053–1065. https://doi.org/10.1139/cjz-2017-0229
Bender MM (1971) Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation. Phytochemistry 10:1239–1244. https://doi.org/10.1016/S0031-9422(00)84324-1
Benton TG, Bryant DM, Cole L, Crick HQP (2002) Linking agricultural practice to insect and bird populations: a historical study over three decades. J Appl Ecol 39:673–687. https://doi.org/10.1046/j.1365-2664.2002.00745.x
Boynton C, Mahony N, Williams T (2020) Barn Swallow (Hirundo rustica) fledglings use crop habitat more frequently in relation to its availability than pasture and other habitat types. The Condor 122:1–14. https://doi.org/10.1093/condor/duz067
Brickle NW, Harper DGC, Aebischer NJ, Cockayne SH (2000) Effects of agricultural intensification on the breeding success of Corn Buntings Miliaria calandra. J Appl Ecol 37:742–755. https://doi.org/10.1046/j.1365-2664.2000.00542.x
Brown CR, Brown MB (1999) Barn Swallow (Hirundo rustica). Birds North Am Online. https://doi.org/10.2173/bna.452
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer-Verlag, New York
Clarke K, Gorley R (2006) Primer v6 Permanova+. PRIMER-E Ltd., Plymouth, UK
Deagle BE, Tollit DJ (2007) Quantitative analysis of prey DNA in pinniped faeces: potential to estimate diet composition? Conserv Genet 8:743–747. https://doi.org/10.1007/s10592-006-9197-7
Donald PF, Sanderson FJ, Burfield IJ, van Bommel FPJ (2006) Further evidence of continent-wide impacts of agricultural intensification on European farmland birds, 1990–2000. Agric Ecosyst Environ 116:189–196. https://doi.org/10.1016/j.agee.2006.02.007
Elgin AS, Clark RG, Morrissey CA (2020) Tree Swallow selection for wetlands in agricultural landscapes predicted by central-place foraging theory. Ornithological Applications 122:duaa039. https://doi.org/10.1093/condor/duaa039
Environment and Climate Change Canada (2018) Historical Climate Data. Contains information licensed under the Open Government License – Canada. [retreived from http://climate.weather.gc.ca/index_e.html]
ESRI (2011) ArcGIS Desktop: release 10. Version v 10. Environmental Systems Research Institute, Redlands, CA: Environmental Systems Research Institute
Evans DR, Hobson KA, Kusack JW et al (2020) Individual condition, but not fledging phenology, carries over to affect post-fledging survival in a Neotropical migratory songbird. Ibis 162:331–344. https://doi.org/10.1111/ibi.12727
France R (1995) Critical examination of stable isotope analysis as a means for tracing carbon pathways in stream ecosystems. Can J Fish Aquat Sci 52:651–656. https://doi.org/10.1139/f95-065
France RL, Schlaepfer MA (2000) 13C and 15N depletion in components of a foodweb from an ephemeral boreal wetland compared to boreal lakes: putative evidence for microbial processes. Hydrobiologia 439:1–6. https://doi.org/10.1023/A:1004131228183
Fry B (2006) Stable isotope ecology. Springer, New York
Ghilain A, Bélisle M (2008) Breeding success of Tree Swallows along a gradient of agricultural intensification. Ecol Appl 18:1140–1154. https://doi.org/10.1890/07-1107.1
Halekoh U, Højsgaard S (2014) A Kenward-Roger approximation and parametric bootstrap methods for tests in linear mixed models - the R package pbkrtest. J Stat Softw. 59:1–30. https://doi.org/10.18637/jss.v059.i09
Haroune L, Cassoulet R, Lafontaine M-P et al (2015) Liquid chromatography-tandem mass spectrometry determination for multiclass pesticides from insect samples by microwave-assisted solvent extraction followed by a salt-out effect and micro-dispersion purification. Anal Chim Acta 891:160–170. https://doi.org/10.1016/j.aca.2015.07.031
Heaton THE (1986) Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a review. Chem Geo Isot Geosci 59:87–102. https://doi.org/10.1016/0168-9622(86)90059-X
Hebert CE, Wassenaar LI (2001) Stable nitrogen isotopes in waterfowl feathers reflect agricultural land use in western Canada. Environ Sci Technol 35:3482–3487. https://doi.org/10.1021/es001970p
Hobson KA (1999) Stable-carbon and nitrogen isotope ratios of songbird feathers grown in two terrestrial biomes: implications for evaluating trophic relationships and breeding origins. Condor 101:799–805. https://doi.org/10.2307/1370067
Hobson KA, Bairlein F (2003) Isotopic fractionation and turnover in captive Garden Warblers (Sylvia borin): implications for delineating dietary and migratory associations in wild passerines. Can J Zool 81:1630–1635. https://doi.org/10.1139/z03-140
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18. https://doi.org/10.3354/meps084009
Hobson KA, Kardynal KJ, Van Wilgenburg SL et al (2015) A continent-wide migratory divide in North American breeding Barn Swallows (Hirundo rustica). PLoS ONE 10:e0129340. https://doi.org/10.1371/journal.pone.0129340
Imlay TL, Mann HAR, Leonard ML (2017) No effect of insect abundance on nestling survival or mass for three aerial insectivores. Avian Conserv Ecol 12:19. https://doi.org/10.5751/ACE-01092-120219
Kendall C (1998) Tracing nitrogen sources and cycling in catchments. In: McDonnell J (ed) Isotope Tracers in Catchment Hydrology. Elsevier, Amsterdam, pp 519–576
Keough JR, Sierszen ME, Hagley CA (1996) Analysis of a Lake Superior coastal food web with stable isotope techniques. Limnol Oceanogr 41:136–146. https://doi.org/10.4319/lo.1996.41.1.0136
Kusack JW, Mitchell GW, Evans DR et al (2020) Effects of agricultural intensification on nestling condition and number of young fledged of barn swallows (Hirundo rustica). Sci Total Environ 709:136195. https://doi.org/10.1016/j.scitotenv.2019.136195
Lysyk TJ (2011) Arthropods associated with livestock grazing systems. Arthropods of Canadian Grasslands: Inhabitants of a Changing Landscape. Biological Survey of Canada, Ottawa, Canada, pp 45–69
Marshall JD, Brooks JR, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Lajtha K, Michener R (eds) Stable Isotopes in Ecology and Environmental Science, 2nd edn. Blackwell Publishing, Oxford, pp 22–60
Mazzi D, Dorn S (2012) Movement of insect pests in agricultural landscapes. Ann Appl Biol 160:97–113. https://doi.org/10.1111/j.1744-7348.2012.00533.x
McCarty JP, Winkler DW (1999) Foraging ecology and diet selectivity of Tree Swallows feeding nestlings. Condor 101:246–254. https://doi.org/10.2307/1369987
McClenaghan B, Nol E, Kerr KCR (2019) DNA metabarcoding reveals the broad and flexible diet of a declining aerial insectivore. Auk 136:1–11. https://doi.org/10.1093/auk/uky003
Mengelkoch JM, Niemi GJ, Regal RR (2004) Diet of the nestling Tree Swallow. Condor 106:423–429. https://doi.org/10.1650/7341
Michel NL, Smith AC, Clark RG et al (2016) Differences in spatial synchrony and interspecific concordance inform guild-level population trends for aerial insectivorous birds. Ecography 39:774–786. https://doi.org/10.1111/ecog.01798
Morris AJ, Wilson JD, Whittingham MJ, Bradbury RB (2005) Indirect effects of pesticides on breeding Yellowhammer (Emberiza citrinella). Agric Ecosyst Environ 106:1–16. https://doi.org/10.1016/j.agee.2004.07.016
Nebel S, Mills A, McCracken JD, Taylor PD (2010) Declines of aerial insectivores in North America follow a geographic gradient. Avian Conserv Ecol 5:1. https://doi.org/10.5751/ACE-00391-050201
Nocera JJ, Blais JM, Beresford DV et al (2012) Historical pesticide applications coincided with an altered diet of aerially foraging insectivorous Chimney Swifts. Proc R Soc B 279:3114–3120. https://doi.org/10.1098/rspb.2012.0445
North American Bird Conservation Initiative Canada (2019) The state of Canada’s Birds, 2019. Environment and Climate Change Canada, Ottawa, Canada
Oksanen J, Blanchet FG, Friendly M, et al (2019) vegan: Community Ecology Package. R Package version 25–6
Ontario Ministry of Agriculture, Food, and Rural Affairs (2017) Insects and pests of field crops. Agronomy Guide for Field Crops. [retrieved from http://www.omafra.gov.on.ca/english/crops/pub811/pub811ch15.pdf]
Orłowski G, Karg J, Karg G (2014) Functional invertebrate prey groups reflect dietary responses to phenology and farming activity and pest control services in three sympatric species of aerially foraging insectivorous birds. PLoS ONE 9:e114906. https://doi.org/10.1371/journal.pone.0114906
Pinhero J, Bates D (2000) Mixed-effects models in S and S-PLUS. Springer-Verlag, New York
Put JE, Mitchell GW, Fahrig L (2018) Higher bat and prey abundance at organic than conventional soybean fields. Biol Conserv 226:177–185. https://doi.org/10.1016/j.biocon.2018.06.021
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rioux Paquette S, Garant D, Pelletier F, Bélisle M (2013) Seasonal patterns in Tree Swallow prey (Diptera) abundance are affected by agricultural intensification. Ecol Appl 23:122–133. https://doi.org/10.1890/12-0068.1
Rosenberg KV, Dokter AM, Blancher PJ, Sauer JR, Smith AC, Smith PA, Stanton JC, Panjabi A, Helft L, Parr M, Marra PP (2019) Decline of the North American avifauna. Science 366:120. https://doi.org/10.1126/science.aaw1313
RStudio Team (2020) RStudio: integrated development for R. RStudio Inc, Boston, MA
Stanton RL, Morrissey CA, Clark RG (2018) Analysis of trends and agricultural drivers of farmland bird declines in North America: a review. Agric Ecosyst Environ 254:244–254. https://doi.org/10.1016/j.agee.2017.11.028
Taylor DB, Moon RD, Campbell JB et al (2010) Dispersal of Stable Flies (Diptera: Muscidae) from larval development sites in a Nebraska landscape. Environ Entomol 39:1101–1110. https://doi.org/10.1603/EN10057
Teeri JA, Schoeller DA (1979) δ13C values of an herbivore and the ratio of C3 to C4 plant carbon in its diet. Oecologia 39:197–200. https://doi.org/10.1007/BF00348068
Tieszen LL, Boutton TW (1989) Stable carbon isotopes in terrestrial ecosystem research. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable Isotopes in Ecological Research. Springer, New York, pp 167–195
Tscharntke T, Klein AM, Kruess A et al (2005) Landscape perspectives on agricultural intensification and biodiversity – ecosystem service management. Ecol Lett 8:857–874. https://doi.org/10.1111/j.1461-0248.2005.00782.x
Twining CW, Brenna JT, Lawrence P et al (2016) Omega-3 long-chain polyunsaturated fatty acids support aerial insectivore performance more than food quantity. Proc Natl Acad Sci 113:10920–10925. https://doi.org/10.1073/pnas.1603998113
Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117. https://doi.org/10.1016/j.tree.2008.09.011
Zeale MR, Butlin RK, Barker GL et al (2011) Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Mol Ecol Resour 11:236–244. https://doi.org/10.1111/j.1755-0998.2010.02920.x
Zuur A, Ieno EN, Walker N et al (2009) Mixed effects models and extensions in ecology with R. Springer Science & Business Media, New York
Acknowledgements
We acknowledge the kind cooperation of the landowners for allowing us to study Barn Swallows on their property. We thank Antonio Salvadori for pioneering this long-term monitoring project and Kaelyn Bumelis for help in the field. This research was conducted with approval from Western University’s Animal Care Committee (Approval #: 2017-005) and in accordance with Canadian Bird Banding Office (Permit #: 10865).
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This study was supported with funding from Environment and Climate Change Canada operating grants to GWM and MDC, a Natural Sciences and Engineering Research Council Discovery Grant (RS474A03) to KAH, Western University to DRE, JWK, and KAH, W.E. Saunders Ontario Graduate Scholarship and Natural Sciences and Engineering Research Council Canadian Graduate Scholarship Masters to DRE.
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JWK, GWM, DRE, MDC, and KAH helped with study conception and design. JWK, DRE, and MDC conducted field work. MDC managed the Barn Swallow monitoring program which provides a base for this work. JWK and JLM analyzed the data. JWK wrote the manuscript with help from GWM, JLM, and KAH. All authors provided edits to the manuscript.
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Communicated by C. G. Guglielmo.
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Kusack, J.W., Mitchell, G.W., Evans, D.R. et al. Diet of nestling Barn Swallows in an agroecosystem: insights from fecal DNA barcoding and feather stable isotopes (δ13C, δ15N) . J Ornithol 163, 137–150 (2022). https://doi.org/10.1007/s10336-021-01917-6
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DOI: https://doi.org/10.1007/s10336-021-01917-6