{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T16:48:40Z","timestamp":1792082920460,"version":"4.4.0"},"reference-count":61,"publisher":"MDPI AG","issue":"24","license":[{"start":{"date-parts":[[2023,12,16]],"date-time":"2023-12-16T00:00:00Z","timestamp":1702684800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Non-target species are commonly exposed to anticoagulant rodenticides worldwide, which may pose a key threat to declining species. However, the main pathway of exposure is usually unknown, potentially hindering conservation efforts. This study aimed to examine whether baits mixed with the biomarker rhodamine B can be used to track invertebrate consumption of rodenticides in a field environment, using this to observe whether invertebrate prey are a potential vector for anticoagulant rodenticides in the diet of insectivores such as the European hedgehog (Erinaceus europaeus). Rhodamine B baits were found to create an observable response. Uptake was negligible in captured insects; however, 20.7% of slugs and 18.4% of snails captured showed uptake of bait. Maximum temperature, distance from bait, proximity to buildings, and the addition of copper tape to bait boxes all influenced the rate of bait uptake in molluscs. Based on these data, it seems likely that molluscs could be a source of rodenticide poisoning in insectivores. This research demonstrates which prey may pose exposure risks to insectivores and likely environmental factors, knowledge of which can guide effective mitigation measures. We suggest that further investigation into using mollusc repellents around bait boxes should be considered.<\/jats:p>","DOI":"10.3390\/ani13243873","type":"journal-article","created":{"date-parts":[[2023,12,18]],"date-time":"2023-12-18T08:55:29Z","timestamp":1702889729000},"page":"3873","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Consumption of Rodenticide Baits by Invertebrates as a Potential Route into the Diet of Insectivores"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-1921-2617","authenticated-orcid":false,"given":"Emily J.","family":"Williams","sequence":"first","affiliation":[{"name":"School of Life and Environmental Sciences, University of Lincoln, Lincoln LN6 7TS, UK"},{"name":"UK Centre for Ecology & Hydrology, Wallingford, Oxon OX10 8BB, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sheena C.","family":"Cotter","sequence":"additional","affiliation":[{"name":"School of Life and Environmental Sciences, University of Lincoln, Lincoln LN6 7TS, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8808-5210","authenticated-orcid":false,"given":"Carl D.","family":"Soulsbury","sequence":"additional","affiliation":[{"name":"School of Life and Environmental Sciences, University of Lincoln, Lincoln LN6 7TS, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,12,16]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1016\/j.envpol.2018.02.004","article-title":"Long-term increase in secondary exposure to anticoagulant rodenticides in European polecats Mustela putorius in Great Britain","volume":"236","author":"Sainsbury","year":"2018","journal-title":"Environ. Pollut."},{"key":"ref_2","first-page":"186","article-title":"The Changing Role of Rodenticides and Their Alternatives in the Management of Commensal Rodents","volume":"13","author":"Witmer","year":"2019","journal-title":"Hum. Wildl. Interact."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.scitotenv.2014.07.049","article-title":"Spatial and temporal exposure patterns in non-target small mammals during brodifacoum rat control","volume":"496","author":"Geduhn","year":"2014","journal-title":"Sci. Total Environ."},{"key":"ref_4","unstructured":"Shore, R.F., Walker, L.A., Potter, E.D., Chaplow, J.S., Pereira, M.G., Sleep, D., and Hunt, A.G. (2019). Second Generation Anticoagulant Rodenticide Residues in Barn Owls 2018, NERC\/Centre for Ecology & Hydrolog."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1016\/j.envpol.2009.07.017","article-title":"Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus)","volume":"158","author":"Dowding","year":"2010","journal-title":"Environ. Pollut."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1111\/j.1365-2664.2005.00997.x","article-title":"Exposure of non-target small mammals to rodenticides: Short-term effects, recovery and implications for secondary poisoning","volume":"42","author":"Brakes","year":"2005","journal-title":"J. Appl. Ecol."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Smith, R., and Shore, R. (2015). Environmental Impacts of Rodenticides, CABI.","DOI":"10.1079\/9781845938178.0330"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.scitotenv.2007.10.061","article-title":"Second generation anticoagulant rodenticides in tawny owls (Strix aluco) from Great Britain","volume":"392","author":"Walker","year":"2008","journal-title":"Sci. Total Environ."},{"key":"ref_9","first-page":"110","article-title":"Anticoagulant rodenticide brodifacoum detected in dead nestlings of an insectivorous passerine","volume":"38","author":"Masuda","year":"2014","journal-title":"N. Z. J. Ecol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1016\/j.scitotenv.2017.08.117","article-title":"Accumulation of anticoagulant rodenticides (chlorophacinone, bromadiolone and brodifacoum) in a non-target invertebrate, the slug, Deroceras reticulatum","volume":"610\u2013611","author":"Alomar","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_11","first-page":"7","article-title":"Assessing Individual and Population-Level Effects of Anticoagulant Rodenticides on Wildlife","volume":"13","author":"Quinn","year":"2019","journal-title":"Hum. Wildl. Interact."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1372","DOI":"10.1016\/j.scitotenv.2018.04.069","article-title":"Anticoagulant rodenticide use, non-target impacts and regulation: A case study from Australia","volume":"634","author":"Lohr","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3106","DOI":"10.1016\/j.envpol.2011.03.028","article-title":"Does small mammal prey guild affect the exposure of predators to anticoagulant rodenticides?","volume":"159","author":"Tosh","year":"2011","journal-title":"Environ. Pollut."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1016\/j.scitotenv.2018.06.063","article-title":"The prevalence and correlates of anticoagulant rodenticide exposure in non-target predators and scavengers in Finland","volume":"642","author":"Koivisto","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"138218","DOI":"10.1016\/j.scitotenv.2020.138218","article-title":"Toxic time bombs: Frequent detection of anticoagulant rodenticides in urban reptiles at multiple trophic levels","volume":"724","author":"Lettoof","year":"2020","journal-title":"Sci Total Env."},{"key":"ref_16","unstructured":"Booth, L.H., Fisher, P., Heppelthwaite, V., and Eason, C.T. (2003). Toxicity and Residues of Brodifacoum in Snails and Earthworms, Department of Conservation."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Barker, G.M. (2004). Natural Enemies of Terrestrial Molluscs, CABI.","DOI":"10.1079\/9780851993195.0000"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"6133","DOI":"10.1007\/s11356-018-04064-3","article-title":"Exposure of non-target small mammals to anticoagulant rodenticide during chemical rodent control operations","volume":"26","author":"Elmeros","year":"2019","journal-title":"Environ. Sci. Pollut. Res."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"144160","DOI":"10.1016\/j.scitotenv.2020.144160","article-title":"Exposure of passerine birds to brodifacoum during management of Norway rats on farms","volume":"762","author":"Walther","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_20","first-page":"235","article-title":"Mortality of northern New Zealand dotterels (Charadrius obscurus aquilonius) following an aerial poisoning operation","volume":"53","author":"Dowding","year":"2006","journal-title":"Notornis"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1080\/03014223.2005.9518416","article-title":"Residues of brodifacoum and other anticoagulant pesticides in target and non-target species, Nelson Lakes National Park, New Zealand","volume":"32","author":"Spurr","year":"2005","journal-title":"N. Z. J. Zool."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.scitotenv.2014.12.042","article-title":"Interspecific and geographical differences in anticoagulant rodenticide residues of predatory wildlife from the Mediterranean region of Spain","volume":"511","author":"Camarero","year":"2015","journal-title":"Sci. Total Environ."},{"key":"ref_23","unstructured":"The Royal Parks (2016). Appendix 8 Post-Mortem Analysis of Hedgehog Liver Tissue Samples for Second-Generation Rodenticides, The Royal Parks Foundation."},{"key":"ref_24","unstructured":"Wilson, E., and Wembridge, D. (2018). The State of Britain\u2019s Hedgehogs 2018, People\u2019s Trust for Endangered Species."},{"key":"ref_25","unstructured":"BTO (2023, November 24). Spotted Flycatcher. Available online: https:\/\/www.bto.org\/understanding-birds\/birdfacts\/spotted-flycatcher."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1111\/ibi.13156","article-title":"Demography of Common Swifts (Apus apus) breeding in the UK associated with local weather but not aphid biomass","volume":"165","author":"Finch","year":"2023","journal-title":"Ibis"},{"key":"ref_27","first-page":"116","article-title":"Recent declines in populations of woodland birds in Britain","volume":"98","author":"Fuller","year":"2005","journal-title":"Br. Birds"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1673\/1536-2442(2006)6[1:IORBIM]2.0.CO;2","article-title":"Incorporation of rhodamine B into male tobacco budworm moths Heliothis virescens to use as a marker for mating studies","volume":"6","author":"Blanco","year":"2006","journal-title":"J. Insect Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1603\/033.046.0521","article-title":"Evaluation of Rhodamine B as an Orally Delivered Biomarker for Rodents and a Feed-Through Transtadial Biomarker for Phlebotomine Sand Flies (Diptera: Psychodidae)","volume":"46","author":"Mascari","year":"2009","journal-title":"J. Med. Entomol."},{"key":"ref_30","unstructured":"ProRep (2023, November 25). Bug Gel. Available online: https:\/\/www.pro-rep.co.uk\/portfolio\/bug-gel\/."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1503","DOI":"10.1016\/j.jenvman.2010.12.014","article-title":"User behaviour, best practice and the risks of non-target exposure associated with anticoagulant rodenticide use","volume":"92","author":"Tosh","year":"2011","journal-title":"J. Environ. Manag."},{"key":"ref_32","unstructured":"Cranshaw, W. (1997). Attractiveness of Beer and Fermentation Products to the Gray Garden Slug, Agriolimax Reticulatum (Muller) (Mollusca: Limacidae), Colorado State University: Colorado State University Agricultural Experiment Station."},{"key":"ref_33","unstructured":"World Weather Online (2021, September 01). World Weather API and Weather Forecast. Available online: https:\/\/www.worldweatheronline.com\/."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1033","DOI":"10.1016\/S0261-2194(03)00120-0","article-title":"Barriers, repellents and antifeedants for slug and snail control","volume":"22","author":"Port","year":"2003","journal-title":"Crop Prot."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v067.i01","article-title":"Fitting Linear Mixed-Effects Models Using {lme4}","volume":"67","author":"Bates","year":"2015","journal-title":"J. Stat. Softw."},{"key":"ref_36","unstructured":"RStudioTeam (2020). RStudio: Integrated Development Environment for R, RStudio, PBC."},{"key":"ref_37","unstructured":"Fox, J., and Weisberg, S. (2019). An {R} Companion to Applied Regression, Sage. [3rd ed.]."},{"key":"ref_38","unstructured":"Wickham, H. (2006). ggplot2: Elegant Graphics for Data Analysis, Springer."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1007\/s10661-013-3422-x","article-title":"Exposure pathways of anticoagulant rodenticides to nontarget wildlife","volume":"186","author":"Elliott","year":"2014","journal-title":"Environ. Monit. Assess."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/S0964-8305(00)00066-4","article-title":"Broadcast application of a placebo rodenticide bait in a native Hawaiian forest","volume":"45","author":"Dunlevy","year":"2000","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1007\/s13364-017-0341-1","article-title":"Comparative analysis of the diet of feral and house cats and wildcat in Europe","volume":"63","author":"Purger","year":"2018","journal-title":"Mammal Res."},{"key":"ref_42","first-page":"167","article-title":"Invertebrates feeding on baits used for vertebrate pest control in new zealand","volume":"23","author":"Spurr","year":"1999","journal-title":"N. Z. J. Ecol."},{"key":"ref_43","unstructured":"Morgan, D.R., Wright, G., Ogilvie, S.C., Pierce, R., and Thomson, P. (2021, October 17). Assessment of the Environmental Impact of Brodifacoum during Rodent Eradication Operations in New Zealand. Available online: https:\/\/digitalcommons.unl.edu\/vpc17\/38\/."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"966","DOI":"10.1111\/een.12869","article-title":"Traits reveal ecological strategies driving carrion insect community assembly","volume":"45","author":"Evans","year":"2020","journal-title":"Ecol. Entomol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1016\/j.scitotenv.2018.04.403","article-title":"Activity of invasive slug Limax maximus in relation to climate conditions based on citizen\u2019s observations and novel regularization based statistical approaches","volume":"637\u2013638","author":"Morii","year":"2018","journal-title":"Sci. Total Environ."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1007\/s00114-018-1560-2","article-title":"Shell colour, temperature, (micro)habitat structure and predator pressure affect the behaviour of Cepaea nemoralis","volume":"105","author":"Rosin","year":"2018","journal-title":"Sci. Nat."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"12940","DOI":"10.1002\/ece3.5607","article-title":"Snails in the sun: Strategies of terrestrial gastropods to cope with hot and dry conditions","volume":"9","author":"Schweizer","year":"2019","journal-title":"Ecol. Evol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"cox007","DOI":"10.1093\/conphys\/cox007","article-title":"Conservation at a slow pace: Terrestrial gastropods facing fast-changing climate","volume":"5","author":"Nicolai","year":"2017","journal-title":"Conserv. Physiol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"144386","DOI":"10.1016\/j.scitotenv.2020.144386","article-title":"Intensive livestock farming as a major determinant of the exposure to anticoagulant rodenticides in raptors of the Canary Islands (Spain)","volume":"768","author":"Zumbado","year":"2021","journal-title":"Sci. Total Environ."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"van den Brink, N.W., Elliott, J.E., Shore, R.F., and Rattner, B.A. (2017). Anticoagulant Rodenticides and Wildlife, Springer International Publishing AG.","DOI":"10.1007\/978-3-319-64377-9"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.landurbplan.2017.04.003","article-title":"Habitat use by barn owls across a rural to urban gradient and an assessment of stressors including, habitat loss, rodenticide exposure and road mortality","volume":"164","author":"Hindmarch","year":"2017","journal-title":"Landsc. Urban Plan."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1171","DOI":"10.1002\/ps.942","article-title":"The behavioural response of slugs and snails to novel molluscicides, irritants and repellents","volume":"60","author":"Port","year":"2004","journal-title":"Pest Manag. Sci."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s13364-015-0256-7","article-title":"Mortality, diseases and diet of European hedgehogs (Erinaceus europaeus) in an urban environment in Finland","volume":"61","author":"Rautio","year":"2016","journal-title":"Mammal Res."},{"key":"ref_54","first-page":"364","article-title":"The food of the hedgehog erinaceus europaeus studies of stomach contents of hedgehogs from schleswig holstein west germany","volume":"211","author":"Grosshans","year":"1983","journal-title":"Zool. Anz."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"401","DOI":"10.4098\/AT.arch.76-39","article-title":"The food of the hedgehog in England","volume":"21","author":"Yalden","year":"1976","journal-title":"Acta Theriol."},{"key":"ref_56","unstructured":"Wroot, A.J. (1984). Feeding ecology of the European hedgehog Erinaceus europaeus. [Ph.D. Thesis, Royal Holloway, University of London]."},{"key":"ref_57","first-page":"147","article-title":"Field Notes: Notes on Suburban Hedgehogs","volume":"101","author":"Howes","year":"1976","journal-title":"Naturalis"},{"key":"ref_58","first-page":"III-129","article-title":"Predators and anti-predator behaviour of the black-headed gull (Larus ridibundus L.)","volume":"11","author":"Kruuk","year":"1964","journal-title":"Behaviour. Suppl."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"South, A. (1992). Terrestrial Slugs: Biology, Ecology and Control, Springer.","DOI":"10.1007\/978-94-011-2380-8"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1593","DOI":"10.1111\/j.1600-0706.2011.20462.x","article-title":"Food resources and foraging habits of the common shrew, Sorex araneus: Does winter food shortage explain Dehnel\u2019s phenomenon?","volume":"121","author":"Churchfield","year":"2012","journal-title":"Oikos"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1124\/dmd.116.073791","article-title":"Management of Rodent Populations by Anticoagulant Rodenticides: Toward Third-Generation Anticoagulant Rodenticides","volume":"45","author":"Espana","year":"2017","journal-title":"Drug Metab. Dispos."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/24\/3873\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:39:54Z","timestamp":1760132394000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/24\/3873"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,12,16]]},"references-count":61,"journal-issue":{"issue":"24","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["ani13243873"],"URL":"https:\/\/doi.org\/10.3390\/ani13243873","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,12,16]]}}}