The dynamics of pine marten predation on red and grey squirrels Twining, J. P., Montgomery, W. I., & Tosh, D. G. (2020). The dynamics of pine marten predation on red and grey squirrels. Mammalian Biology. https://doi.org/10.1007/s42991-020-00031-z Published in: Mammalian Biology Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights Copyright 2020 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:27. Sep. 2021 Mammalian Biology https://doi.org/10.1007/s42991-020-00031-z ORIGINAL ARTICLE The dynamics of pine marten predation on red and grey squirrels Joshua P. Twining1 · W. Ian Montgomery1 · David G. Tosh2 Received: 12 October 2019 / Accepted: 3 April 2020 © The Author(s) 2020 Abstract Invasive alien species pose one of the greatest threats to global biodiversity. In parts of Europe, introduced eastern grey squir- rels (Sciurus carolinensis) have caused regional extinctions of the native red squirrel (Sciurus vulgaris). However, exposure to pine martens (Martes martes) has been demonstrated to reverse the competitive outcome between red and grey squirrels. The mechanism whereby this efect occurs remains unclear. It is hypothesised that direct predation, facilitated by a lack of behavioural response, is the mechanism driving this relationship. We review the literature and reanalyse a new dataset to provide further data on the occurrence of both squirrel species in the scats of pine marten. Both squirrel species occurred in the scats of pine marten confrming its role as a predator of these species. Predation of grey squirrels was signifcantly higher than red squirrels and was recorded only in spring and summer. Our review provides evidence for the mechanism driving the current decline in grey squirrels in Ireland and Scotland and supports the hypothesis that in the presence of a shared predator, direct predation infuences the outcome of species interactions between native red and non-native grey squirrels. Keywords Pine marten · Diet · Grey squirrel · Red squirrel · Predation · Invasive species · Prey switching Introduction cost that has likely increased due to continued increases of many IAS. Mitigation of these losses can take the form of Invasive alien species (IAS) arise when non-native species direct culling (e.g. Schuchert et al. 2014), the use of poisons become established in a new environment and negatively (Witmer et al. 2007) or biocontrol via the introduction of a impact the naive ecosystem. Impacts by IAS on native bio- predator (Lindquist et al. 1992) or a pathogen (Cooke and diversity, to which IAS are a global threat (ISAC 2006), have Fenner 2002). The introduction of disease or predators from been widely reported. Awareness, and the ability to meas- the native range of an IAS (Simberlof and Stiling 1996; ure impacts, of IAS on economies, health and ecosystem Shine 2010) may lead to unintended negative consequences, services is increasingly being recognised and documented e.g. the development of resistance or predation on non-target (Charles and Dukes 2008; Kelly et al. 2013; Pimental et al. species (Hays and Conant 2007; O’Donnell et al. 2017). 2000). The annual economic cost of IAS to Europe in 2009 One IAS of widespread concern in Europe is the eastern was estimated at €12 billion p. a. (Kettunen et al. 2009), a grey squirrel (Sciurus carolinensis). Introduced from North America to Great Britain and Ireland in the nineteeth and Handling editor: Raquel Monclús. twentieth centuries (Lloyd 1968), it is now in Italy where its presence poses a risk to the rest of continental Europe (Ber- * Joshua P. Twining tolino et al. 2014). The species negatively impacts forestry [email protected] (Mayle and Broome 2013) and native biodiversity (Hewson W. Ian Montgomery and Fuller 2003; Newson et al. 2010), particularly the red [email protected] squirrel which has been replaced across much of its former David G. Tosh range in Britain (Lloyd 1968). Replacement of red by grey [email protected] squirrels is due to factors including: larger individual mass 1 School of Biological Sciences, Queen’s University and greater population densities of grey squirrels; decreases of Belfast, 17 Chlorine Gardens, Belfast BT9 5AJ, in red squirrel fecundity, residency and recruitment (Wauters Northern Ireland, UK and Gurnell 1999; Gurnell et al. 2004). Recent research sug- 2 National Museums Northern Ireland, 153 Bangor Road, gests that alterations to microparasite communities (Romeo Holywood BT18 0EU, Northern Ireland, UK Vol.:(0123456789)1 3 J. P. Twining et al. et al. 2015) and personality (Wauters et al. 2019) in red marten recovery could have the observed efect of causing squirrels during co-occurrence may also play a role. How- declines in grey squirrel populations (Sheehy and Lawton ever, the most important factor remains grey squirrels acting 2014; Sheehy et al. 2018; Flaherty and Lawton 2019), with- as a vector for squirrel pox virus (SQPV) causing mortality out squirrels being a frequently recorded item in the diet. in red, but not grey squirrels (Tompkins et al. 2003; Rushton Most dietary studies on pine marten either focus on single et al. 2006). In order to prevent a repeat of this situation in feld sites or sampling periods (Helldin 2000; Lynch and Italy and continental Europe, eforts are required to manage McCann 2007; Zalewski 2007; Sheehy et al. 2013; O’Meara or eradicate grey squirrels [Regulation (EU) 1143/2014]. et al. 2014). The pine martens arboreality means it is the Control of the grey squirrel has been attempted in Britain only mammalian predator in Ireland and Britain capable of and Ireland via culling to mitigate their impacts. However, targeting squirrels in their dreys. It may have a strong abil- success has been localised and arguably inefective, with ity, therefore, to regulate prey populations lacking refugium few successful outcomes (Schuchert et al. 2014). Cost and from predation (Menge and Sutherland 1976). efort required impedes successful control both locally and In order to investigate the potential mechanism for the nationally in Great Britain and Ireland (Manchester and reversal of squirrel replacement, we reviewed published Bullock 2001), whilst in Italy, objections by animal rights studies to compile available information on the occurrence groups have hindered control eforts (Genovesi and Bertolini of red and grey squirrels in the diet of the European pine 2001; Lioy et al. 2019). At present, culling is the only means marten, and reanalysed Twining et al. (2019), a new dataset available to control grey squirrels as eforts to develop an of 918 scats. These were collected from twenty sites across immuno-contraceptive for grey squirrels continue with no the pine martens range in Northern Ireland accounting for practical and deliverable method yet available (Barr et al. the presence of red and grey squirrels at each site (Tosh 2002). Consequently, a new approach is needed to provide 2015). We aim to determine whether there is evidence for efective control of the grey squirrel in European landscapes, pine marten predation to be a potential mechanism for the reducing their economic cost (> £10 million per annum in observed reversal of the replacement of red squirrels by Britain alone, Mayle and Broome 2013) and reversing their grey squirrels in Britain and Ireland (Sheehy and Lawton replacement of the native red squirrel. 2014; Sheehy et al. 2018; Flaherty and Lawton 2019), and The recent research suggests a potential new approach to to highlight potential nuances in squirrel predation by the control grey squirrels may involve a recovering native preda- pine marten elsewhere in Europe. tor, the European pine marten (Martes martes). Negative, spatial correlations between pine marten and the presence of grey squirrels has been recorded in Ireland (Sheehy and Methods Lawton 2014) and Scotland (Sheehy et al. 2018). The latter suggests exposure to pine martens negatively impacts grey, Peer reviewed and unpublished literature on European pine but not red squirrel occupancy (Sheehy et al. 2018) and that marten diet was searched for via the Web of Science and exposure to pine martens reverses the typical outcome of Google Scholar. Searches conducted utilised the terms “pine resource and disease mediated competition between the two marten diet squirrel”, “pine marten predation squirrel”. sciurids. The recent research has demonstrated that native Publications were selected using the following criteria: (1) red squirrels possess anti-predator behaviours to pine mar- diet composition was estimated by analysis of scats with a tens, while invasive grey squirrels do not (Twining et al. minimum sample size of 100; (2) results were reported for 2020). This suggests behavioural diferences may enable the each prey species as frequency of occurrence (FO %), or red squirrel to avoid pine martens more successfully than as number of times an item occurred and total sample size greys which, as a result, are more vulnerable to predation number to FO % could be calculated manually and (3) red by pine martens than red squirrels.