Factors affecting bait uptake by the grey squirrel (Sciurus carolinensis) and the future delivery of oral contraceptives
Sarah E. Beatham
A B * , Julia Coats A , Philip A. Stephens B and Giovanna Massei C
A National Wildlife Management Centre, APHA, Sand Hutton, York YO41 1LZ, UK.
B Conservation Ecology Group, Department of Biosciences, Durham University, South Road, Durham DH1 3LE, UK.
C Department of Environment and Geography, Botstiber Institute for Wildlife Fertility Control, University of York, Wentworth Way, Heslington, York YO10 5NG, UK.
Abstract
Invasive species negatively affect natural communities and human activities. The grey squirrel is an invasive species in the UK, causing damage to forestry and the decline of the native red squirrel. Oral contraceptives have the potential to reduce numbers of grey squirrels; however, to be effective a sufficient proportion of a population must consume a bait containing contraceptives.
The objective of this study was to estimate the efficacy of delivering baits via feeders to grey squirrels and to determine the factors most important to bait uptake.
Bait uptake was measured using the bait marker Rhodamine B mixed with 100% hazelnut butter and delivered to grey squirrels via purpose-designed feeders. Different concentrations of Rhodamine B were first trialled on captive grey squirrels for their palatability and detectability in the hair. Bait-uptake field trials were then conducted in 10 UK woodlands by using the preferred concentration.
In captive trials, it was found that a concentration of 0.18% Rhodamine B mixed in hazelnut butter was palatable to grey squirrels and that individuals needed to consume only small amounts (<5 g) for it to be detected in the flank hair by using an ultraviolet microscope. It was possible to deliver bait to the majority of grey squirrels in 6 of 10 woods within 4 days. Season, feeder density and squirrel density were important factors affecting bait uptake, with more squirrels consuming bait in summer than in winter and from three feeders per hectare rather than from one per hectare.
This study demonstrated that baits delivered via feeders can target the majority of grey squirrels in woodland environments.
Oral contraceptives could offer a cost-effective tool to reduce numbers of grey squirrels across the UK landscape and mitigate the negative impacts they have on native wildlife and tree health.
Keywords: bait uptake, fertility control, invasive species, population control, Rhodamine B, wildlife management.
References
Beatham SE, Goodwin D, Coats J, Stephens PA, Massei G (2021) A PIT-tag–based method for measuring individual bait uptake in small mammals. Ecological Solutions and Evidence 2(2), e12081.
| Crossref | Google Scholar |
Croft S, Chauvenet ALM, Smith GC (2017) A systematic approach to estimate the distribution and total abundance of British mammals. PLoS ONE 12(6), e0176339.
| Crossref | Google Scholar |
Croft S, Aegerter JN, Beatham S, Coats J, Massei G (2021) A spatially explicit population model to compare management using culling and fertility control to reduce numbers of grey squirrels. Ecological Modelling 440, 109386.
| Crossref | Google Scholar |
Dunn M, Marzano M, Forster J, Gill RMA (2018) Public attitudes towards ‘pest’ management: perceptions on squirrel management strategies in the UK. Biological Conservation 222, 52-63.
| Crossref | Google Scholar |
Fernandez JR-R, Rocke TE (2011) Use of rhodamine B as a biomarker for oral plague vaccination of prairie dogs. Journal of Wildlife Diseases 47(3), 765-768.
| Crossref | Google Scholar |
Fisher P (1999) Review of using Rhodamine B as a marker for wildlife studies. Wildlife Society Bulletin 27, 318-329.
| Google Scholar |
Gurnell J, Lurz PWW, Shuttleworth CM (2016) Ecosystem impacts of an alien invader in Europe, the grey squirrel Sciurus carolinensis. In ‘The grey squirrel: ecology & management of an invasive species in Europe’. (Eds CM Shuttleworth, PWW Lurz, J Gurnell) pp. 307–328. (European Squirrel Initiative: Stoneleigh Park, Warwickshire, UK)
Haley BS, Berentsen AR, Engeman RM (2019) Taking the bait: species taking oral rabies vaccine baits intended for raccoons. Environmental Science and Pollution Research 26(10), 9816-9822.
| Crossref | Google Scholar |
Jacoblinnert K, Jacob J, Zhang Z, Hinds LA (2022) The status of fertility control for rodents: recent achievements and future directions. Integrative Zoology 17, 964-980.
| Crossref | Google Scholar |
Lawton C, Shuttleworth CM, Kenward RE (2016) Ranging behaviour, density and social structure in grey squirrels. In ‘The grey squirrel: ecology and management of an invasive species in Europe’. (Eds CM Shuttleworth, PWW Lurz, J Gurnell) pp. 133–152. (European Squirrel Initiative: Stoneleigh Park, Warwickshire, UK)
Massei G (2018) Oral contraceptives for grey squirrels. QJ Forestry 112, 39-41.
| Google Scholar |
Massei G, Cowan D (2014) Fertility control to mitigate human–wildlife conflicts: a review. Wildlife Research 41(1), 1-21.
| Crossref | Google Scholar |
Massei G, Cowan D, Eckery D, Mauldin R, Gomm M, Rochaix P, Hill F, Pinkham R, Miller LA (2020) Effect of vaccination with a novel GnRH-based immunocontraceptive on immune responses and fertility in rats. Heliyon 6, e03781.
| Crossref | Google Scholar |
McRae JE, Schlichting PE, Snow NP, Davis AJ, VerCauteren KC, Kilgo JC, Keiter DA, Beasley JC, Pepin KM (2020) Factors affecting bait site visitation: area of influence of baits. Wildlife Society Bulletin 44(2), 362-371.
| Crossref | Google Scholar |
Merrill JA, Cooch EG, Curtis PD (2003) Time to reduction: factors influencing management efficacy in sterilizing overabundant white-tailed deer. The Journal of Wildlife Management 67, 267-279.
| Crossref | Google Scholar |
Prentice JC, Fox NJ, Hutchings MR, White PCL, Davidson RS, Marion G (2019) When to kill a cull: factors affecting the success of culling wildlife for disease control. Journal of The Royal Society Interface 16(152), 20180901.
| Crossref | Google Scholar |
R Core Team (2019) ‘R: a language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org [Accessed 20 February 2021]
Richards SA (2008) Dealing with overdispersed count data in applied ecology. Journal of Applied Ecology 45(1), 218-227.
| Crossref | Google Scholar |
Robinson L, Cushman SA, Lucid MK (2017) Winter bait stations as a multispecies survey tool. Ecology and Evolution 7(17), 6826-6838.
| Crossref | Google Scholar |
Rushton SP, Lurz PWW, Gurnell J, Nettleton P, Bruemmer C, Shirley MDF, Sainsbury AW (2006) Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain. Epidemiology and Infection 134(3), 521-533.
| Crossref | Google Scholar |
Saunders G, McIlroy J, Berghout M, Kay B, Gifford E, Perry R, van de Ven R (2002) The effects of induced sterility on the territorial behaviour and survival of foxes. Journal of Applied Ecology 39, 56-66.
| Crossref | Google Scholar |
Secretariat of the Convention on Biological Diversity (2006) Global biodiversity Outlook 2. Available at https://www.cbd.int/gbo2 [Accessed 20 February 2021]
Steele MA, Wauters LA (2016) Diet and food hoarding in eastern grey squirrels (Sciurus carolinensis): implications for an invasive advantage. In ‘The grey squirrel: ecology and management of an invasive species in Europe’. (Eds CM Shuttleworth, PWW Lurz, J Gurnell) pp. 97–114. (European Squirrel Initiative: Stoneleigh Park, Warwickshire, UK)
The Mammal Society (2021) Species – red squirrel. Available at https://www.mammal.org.uk/species-hub/full-species-hub/discover-mammals/species-red-squirrel/ [Accessed 23 July 2021]
The Royal Forestry Society (2021) An analysis of the cost of grey squirrel damage to woodland. Available at https://rfs.org.uk/insights-publications/rfs-reports/an-analysis-of-the-cost-of-grey-squirrel-damage-to-woodland/ [Accessed 23 July 2021]
Thompson DC (1977) Diurnal and seasonal activity of the grey squirrel (Sciurus carolinensis). Canadian Journal of Zoology 55(7), 1185-1189.
| Crossref | Google Scholar |
van Eeden LM, Dickman CR, Ritchie EG, Newsome TM (2017) Shifting public values and what they mean for increasing democracy in wildlife management decisions. Biodiversity and Conservation 26(11), 2759-2763.
| Crossref | Google Scholar |
Weerakoon MK, Price CJ, Banks PB (2013) Hair type, intake, and detection method influence Rhodamine B detectability. The Journal of Wildlife Management 77(2), 306-312.
| Crossref | Google Scholar |
Whisson DA, Salmon TP (2009) Assessing the effectiveness of bait stations for controlling California ground squirrels (Spermophilus beecheyi). Crop Protection 28(8), 690-695.
| Crossref | Google Scholar |
White PCL, Lewis AJG, Harris S (1997) Fertility control as a means of controlling bovine tuberculosis in badger (Meles meles) populations in south-West England: predictions from a spatial stochastic simulation model. Proceedings of the Royal Society of London. Series B: Biological Sciences 264(1389), 1737-1747.
| Crossref | Google Scholar |
Woodroffe R, Donnelly CA, Cox DR, Bourne FJ, Cheeseman CL, Delahay RJ, Gettinby G, Mcinerney JP, Morrison WI (2006) Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis. Journal of Applied Ecology 43(1), 1-10.
| Crossref | Google Scholar |
