Abstract
Increased demand for renewable energy has led to growth in the use of land for electricity generation and associated infrastructure. Land-based wind farms are amongst the commonest generators of renewable energy. To date, most research on the effects of wind farms on wildlife have focussed on birds and bats, with very little work on terrestrial taxa. We hypothesised that widely reported negative effects of wind farms on predatory birds might benefit potential prey species. We focussed on reptiles due to concerns over worldwide declines in this group. We compared avian attack rates on clay model snakes at a site in Caithness UK within a wind farm relative to a control site of the same topography and habitat class, 1 km away, using life-sized clay models of adder Vipera berus, a widespread but declining Palaearctic species. Attack rates at the control site were comparable with similar studies elsewhere in Europe. However, we found that attack rates were lower within wind farm arrays, although several species of bird known to prey on reptiles were observed both within the wind farm and the control site. Therefore, given the high rate of loss to avian predators experienced in reptile reintroduction and reinforcement projects, wind farm sites may offer safe-havens, representing a neglected opportunity in reptile conservation. Grazing by sheep severely offset this benefit, presumably through removal of plant cover which was apparent in those areas of the wind farm where sheep were allowed access; grazing must thus be managed carefully for these benefits to be realised.
Similar content being viewed by others
References
Agha M, Lovich JE, Ennen JR, Augustine B, Arundel TR, Murphy MO, Meyer-Wilkins K, Bjurlin C, Delaney D, Briggs J, Austin M, Madrak S, Price SJ (2015) Turbines and terrestrial vertebrates: variation in tortoise survivorship between a wind energy facility and an adjacent undisturbed wildland area in the desert southwest (USA). Environ Manag 56:332–341
Agha M, Smith AL, Lovich JE, Delaney D, Ennen JR, Briggs J, Tennant LA, Puffer SR, Walde A, Arundel TR, Price SJ, Todd BD (2017) Mammalian mesocarnivore visitation at tortoise burrows in a wind farm. J Wildlife Manag 81:1117–1124. https://doi.org/10.1002/jwmg.21262
Allison, TD, Diffendorfer JE, Baerwald EF, Beston JA, Drake D, Hale A, Hein CD, Huso MM, Loss SR, Lovich JE, Strickland MD, Williams K, Winder VL (2019) Impacts to wildlife of wind energy siting and operation in the United States. Iss Ecol. Report No. 21
Anderson L, Burgin S (2008) Patterns of bird predation on reptiles in small woodland remnant edges in peri-urban north-western Sydney, Australia. Landsc Ecol 23:1039–1047
Andren C (1982) Effect of prey density on reproduction, foraging and other activities in the adder, Vipera berus. Amphibia-Reptilia 3:81–96
Andrews KM, Nanjappa P, Riley SP (eds) (2015) Roads and ecological infrastructure: concepts and applications for small animals. JHU Press, Baltimore
Avery R (1993) The relationship between disturbance, respiration rate and feeding in common lizards (Lacerta vivipara). Herp J 3:136–139
Barrios L, Rodriguez A (2004) Behavioural and environmental correlates of soaring-bird mortality at on-shore wind turbines. J Appl Ecol 41:72–81
Bateman PW, Fleming PA, Wolfe AK (2017) A different kind of ecological modelling: the use of clay model organisms to explore predator–prey interactions in vertebrates. J Zool 301:251–262
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
Beebee TJ, Griffiths RA (2000) The new naturalist. Amphibians and reptiles. A natural history of the British Herpetofauna. Harper Collins, London, pp 45–56
Bittner T (2003) Polymorphic clay models of Thamnophis sirtalis suggest patterns of avian predation. Ohio J Sci 103:62–66
Boarman WI (2003) Managing a subsidized predator population: reducing common raven predation on desert tortoises. Environ Manag 32:205–217
Brodie E (1993) Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:227–235
Buckley LB, Jetz W (2007) Insularity and the determinants of lizard population density. Ecol Lett 10:481–489. https://doi.org/10.1111/j.1461-0248.2007.01042.x
Burger J (1998) Antipredator behaviour of hatchling snakes: effects of incubation temperature and simulated predators. Anim Behav 56:547–553
Cramp S, Perrins CM (eds) (1994) The birds of the Western Palearctic vol. 8. Oxford University Press, Oxford
Cramp S, Simmons KEL (eds) (1979) The birds of the Western Palearctic vol. 2. Oxford University Press, Oxford
de Lucas M, Perrow MR (2017) Birds: collision. Wildlife and wind farms-conflicts and solutions, volume 1: onshore: potential effects. Pelagic, Exeter, pp 155–191
de Lucas M, Janss GF, Whitfield DP, Ferrer M (2008) Collision fatality of raptors in wind farms does not depend on raptor abundance. J Appl Ecol 45:1695–1703
Drewitt AL, Langston RH (2006) Assessing the impacts of wind farms on birds. Ibis 148:29–42
EU (2009) Renewable Energy Directive 2009/28/EC. https://eur-lex.europa.eu/legal-content/EN/ALL/?uri=celex%3A32009L0028. Accessed 17th August 2019
Evans DM, Redpath SM, Elston DA, Evans SA, Mitchell RJ, Dennis P (2006) To graze or not to graze? Sheep, voles, forestry and nature conservation in the British uplands. J Appl Ecol 43:499–505. https://doi.org/10.1111/j.1365-2664.2006.01158.x
Everaert J, Stienen E (2007) Impact of wind turbines on birds in Zeebrugge (Belgium). Biodivers Conserv 16:3345–3359
Farallo V, Forstner M (2012) Predation and the maintenance of color polymorphism on a habitat specialist squamate. PLoS One 7:e30316. https://doi.org/10.1371/journal.pone.0030316
Ferrer M, de Lucas M, Janss GF, Casado E, Munoz AR, Bechard MJ, Calabuig CP (2012) Weak relationship between risk assessment studies and recorded mortality in wind farms. J Appl Ecol 49:38–46
Garvin JC, Jennelle CS, Drake D, Grodsky SM (2011) Response of raptors to a windfarm. J Appl Ecol 48:199–209. https://doi.org/10.1111/j.1365-2664.2010.01912.x
Gibbons J, Scott D, Ryan T, Buhlmann K, Tuberville T, Metts B, Winne C (2000) The global decline of reptiles, Deja Vu Amphibians. BioScience 50:653–666
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Graham IM, Redpath SM, Thirgood SJ (1995) The diet and breeding density of common buzzards Buteo buteo in relation to indices of prey abundance. Bird Study 42:165–173
Halpern B (2014) Final report on LIFE project conservation of Hungarian meadow viper (Vipera ursinii rakosiensis) in the Carpathian-basin. EU-LIFE. http://ec.europa.eu/environment/life/project/Projects/index.cfm?fuseaction=home.showFile&rep=file&fil=LIFE07_NAT_H_000322_FTR.pdf. Accessed 11/09/2018
Halpern B, Péchy T, Somlai T, Dankovics R, Sós E, Walzer C (2017) Survival, area use and thermoregulation of reintroduced Hungarian meadow vipers (Vipera ursinii rakosiensis). 19th European Congress of Herpetology, Salzburg, Austria. 18-23 September
Hansen NA, Sato CF, Michael DR, Lindenmayer DB, Driscoll DA (2019) Predation risk for reptiles is highest at remnant edges in agricultural landscapes. J Appl Ecol 56:31–43
Harris S, Yalden DW (eds) (2008) Mammals of the British Isles: handbook, vol 106. Mammal society, London
Hilton-Taylor C, Jonathan B, Stuart S (2004) 2004 IUCN red list of threatened species: a global species assessment. IUCN. https://portals.iucn.org/library/node/9830. Accessed 08/12/2018
Hötker H (2017) Birds: displacement. In: Perrow (ed) Wildlife and wind farms-conflicts and solutions, volume 1: onshore: potential effects. Pelagic, Exeter, pp 119–155
Hötker H, Dürr T (2017) Lessons from the wind turbine collision register in Germany. In: Perrow (ed) Wildlife and wind farms-conflicts and solutions, volume 1: onshore: potential effects. Pelagic, Exeter, pp 161–164
Hunt G, Hunt T (2006) The trend of Golden eagle territory occupancy in the vicinity of the Altamont pass wind resource area: 2005 survey. California Energy Commission. http://www.westernsunsystems.comorwww.gosolarcalifornia.org/2006publications/CEC-500-2006-056/CEC-500-2006-056.PDF
IPBES (2019) Global assessment on biodiversity and ecosystem services. Secretariat of the Intergovernmental Platform for Biodiversity and Ecosystem Services, Bonn
JNCC (2010) UK priority species data collation: Vipera berus version 2, Joint Nature Conservation Committee. Available: http://jncc.defra.gov.uk/_speciespages/2695.pdf
Keehn JE, Feldman CR (2018) Predator attack rates and anti-predator behavior of side-blotched lizards (Uta stansburiana) at Southern California wind farms, USA. Herpetol Conserv Biol 13:194–204
Keehn JE, Shoemaker KT, Feldman CR (2019) Population-level effects of wind farms on a desert lizard. J Wildlife Manag 83:145–157
Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33. https://CRAN.R-project.org/package=lmerTes
Laurance WF (2018) Conservation and the global infrastructure tsunami: disclose, debate, delay! Trends Ecol Evol 33(8):568–571
Lindenmayer DB, Blanchard W, Crane M, Michael D, Sato C (2018) Biodiversity benefits of vegetation restoration are undermined by livestock grazing. Restor Ecol 26:1157–1164
Lovich JE, Daniels R (2000) Environmental characteristics of desert tortoise (Gopherus agassizii) burrow locations in an altered industrial landscape. Chelonian Conserv Bi 3:714–721
Lovich JE, Ennen JR (2017) Reptiles and amphibians. In: Perrow MR (ed) Wildlife and wind farms-conflicts and solutions, volume 1: onshore: potential effects. Pelagic, Exeter, pp 97–119
Lovich JE, Ennen JR, Madrak S, Meyer K, Loughran C, Bjurlin C, Arundel T, Turner W, Jones C, Groenendaal GM (2011) Effects of wind energy production on growth, demography and survivorship of a desert tortoise (Gopherus agassizii) population in southern California with comparisons to natural populations. Herpetol Conserv Biol 6:161–174
Lovich JE, Yackulic CB, Freilich J, Agha M, Austin M, Meyer KP, Arundel TR, Hansen J, Vamstad MS, Root SA (2014) Climatic variation and tortoise survival: has a desert species met its match? Biol Conserv 169:214–224
Maclagan SJ, Coates T, Ritchie EG (2018) Don't judge habitat on its novelty: assessing the value of novel habitats for an endangered mammal in a peri-urban landscape. Biol Conserv 223:11–18
Martin J, Lopez P (1996) Avian predation on a large lizard (Lacerta lepida) found at Low population densities in Mediterranean habitats: an analysis of bird diets. Copeia 3:772–726
Mazerolle M (2015) AICcmodavg: model selection and multimodel inference based on (Q)AIC(c)
McClure CJ, Westrip JR, Johnson JA, Schulwitz SE, Virani MZ, Davies R, Symes A, Wheatley H, Thorstrom R, Amar A, Buij R (2018) State of the world's raptors: distributions, threats, and conservation recommendations. Biol Conserv 227:390–402
McInerny C, Minting P (2016) Amphibians and reptiles of Scotland. Glasgow Natural History Society, Glasgow
Meiri S, Bauer AM, Allison A, Castro-Herrera F, Chirio L, Colli G, Das I, Doan TM, Glaw F, Grismer LL, Hoogmoed M (2018) Extinct, obscure or imaginary: the lizard species with the smallest ranges. Divers Distrib 24:262–273
NBN (2018) https://nbnatlas.org/. Accessed 8 April 2018
Neumeyer R (1987) Density and seasonal movements of the adder (Vipera berus L. 1758) in a subalpine environment. Amphibia-Reptilia 8:259–275
Pearce-Higgins JW, Stephen L, Langston RH, Bainbridge IP, Bullman R (2009) The distribution of breeding birds around upland wind farms. J Appl Ecol 46:1323–1331
Perrow MR (ed) (2017) Wildlife and wind farms-conflicts and solutions, volume 1: onshore: potential effects. Pelagic, Exeter
Prestt I (1971) An ecological study of the viper (Vipera berus) in southern Britain. J Zool Lond 164:373–418
R core team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna https://www.R-project.org/
Rabin LA, Coss RG, Owings DH (2006) The effects of wind turbines on antipredator behavior in California ground squirrels (Spermophilus beecheyi). Biol Conserv 131:410–420
Randall JA, Matocq MD (1997) Why do kangaroo rats (Dipodomys spectabilis) footdrum at snakes? Behav Ecol 8:404–413
Reading C, Luiselli LM, Akani GC, Bonnet X, Amori G, Ballouard JM, Rugiero L (2010) Are snake populations in widespread decline? Biol Lett 6:777–780. https://doi.org/10.1098/rsbl.2010.0373
Reidar VS, Tveiten R, Aanonsen OM (2007) Diet of common buzzards (Buteo buteo) in southern Norway determined from prey remains and video recordings. Ornis Fennica 84:97–104
Rotem G, Gavish Y, Shacham B, Giladi I, Bouskila A, Ziv Y (2016) Combined effects of climatic gradient and domestic livestock grazing on reptile community structure in a heterogeneous agroecosystem. Oecologia 180:231–242
Salo P, Banks PB, Dickman CR, Korpimaki E (2010) Predator manipulation experiments: impacts on populations of terrestrial vertebrate prey. Ecol Monogr 80:531–546
Sánchez-Zapata JA, Clavero M, Carrete M, DeVault TL, Hermoso V, Losada MA, Polo MJ, Sánchez-Navarro S, Pérez-García JM, Botella F, Ibáñez C (2016) Effects of renewable energy production and infrastructure on wildlife. Current Trends in Wildlife Research:97–123
Santos M, Bastos R, Travassos P, Bessa R, Repas M, Cabral JA (2010) Predicting the trends of vertebrate species richness as a response to wind farms installation in mountain ecosystems of Northwest Portugal. Ecol Indic 10:192–205
Scott R (2011) Atlas of Highland land mammals. Highland Biological Recording Group, Inverness
Steen R, Low LM, Sonerud GA (2011) Delivery of common lizards (Zootoca (Lacerta) vivipara) to nests of Eurasian kestrel (Falco tinnunculus) determined by solar height and ambient temperature. Can J Zool 89:199–205
Stewart GB, Pullin AS, Cole CF (2005) Effects of wind turbines on bird abundance. CEE review 04-002 (SR4). Collaboration for Environmental Evidence. www.environmentalevidence.org/SR4.html
Tapia L, Dominguez J, Romeu M (2007) Diet of common buzzard (Buteo buteo) (Linnaeus, 1758) in an area of North-Western Spain as assessed by direct observation from blinds. Nova Acta Ci Compostelana Secc Biol 16:145–149
Thaker M, Zambre A, Bhosale H (2018) Wind farms have cascading impacts on ecosystems across trophic levels. Nat Ecol Evol 2:1854–1858
Torres A, Jaeger JA, Alonso JC (2016) Assessing large-scale wildlife responses to human infrastructure development. Proc Natl Acad Sci U S A 113:8472–8477
UN Sustainable Development Goal 9 (2019) https://sustainabledevelopment.un.org/sdg9. Accessed 17th August 2019
Val J, Travers SK, Oliver I, Koen TB, Eldridge DJ (2019) Recent grazing reduces reptile richness but historic grazing filters reptiles based on their functional traits. J Appl Ecol 56:833–842
Valkonen J, Niskanen M, Bjorklund M, Mappes J (2011) Disruption or aposematism? Significance of dorsal zigzag pattern of European vipers. Evol Ecol 25:1047–1063. https://doi.org/10.1007/s10682-011-9463-0
Webb JK, Whiting MJ (2005) Why don't small snakes bask? Juvenile broad-headed snakes trade thermal benefits for safety. Oikos 110:515–522
Wheeler P (2008) Effects of sheep grazing on abundance and predators of field vole (Microtus agrestis) in upland Britain. Agric Ecosyst Environ 123:49–55
Whitfield DP, Fielding AH, McLeod DRA, Haworth PF (2004) Modelling the effects of persecution on the population dynamics of Golden eagles in Scotland. Biol Conserv 119:319–333
Wilkinson JW, Arnell AP (2013) NARRS report 2007–2012: establishing the baseline (HWM Edition). ARC Research Report. http://narrs.org.uk/documents/NARRS%20Report%202007-2012.pdf
Wüster W, Allum CS, Bjargardottir IB, Bailey KL, Dawson KJ, Lewis J, Pollard CP (2004) Do aposematism and Batesian mimicry require bright colours? A test, using European viper markings. Proc Roy Soc Lond B Biol Sci 271:2495–2499. https://doi.org/10.1098/rspb.2004.2894
Young BA (2003) Snake Bioacustics: towards a richer understanding of the behavioural ecology of snakes. Q Rev Biol 78:303–325
Young BA, Aguiar A (2002) Response of western diamondback rattlesnakes Crotalus atrox to airborne sounds. J Exp Biol 205:3087–3092
Acknowledgements
We would like to thank Professor Bob Furness for his comments on an earlier draft of this manuscript, and the staff of Camster Wind Farm for their cooperation. Two anonymous reviewers provided comments that greatly improved the text.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is part of the Topical Collection on Road Ecology
Guest Editor: Marcello D’Amico
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Law, C., Lancaster, L., Hall, J. et al. Quantifying the differences in avian attack rates on reptiles between an infrastructure and a control site. Eur J Wildl Res 66, 54 (2020). https://doi.org/10.1007/s10344-020-01393-y
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-020-01393-y