Predation is a strong evolutionary force acting upon multiple species traits including size, morphology, colouration, and behaviour (Werner et al. 1993; Maynard-Smith & Harper 2003; Scott-Phillips 2008). These traits ultimately predict the distribution, composition, size, and ecological function of a population or community (Hall et al. 1976; Kneitel and Chase 2004; Beauchamp et al. 2007; Hawlena and Schmitz 2010; Letnic et al. 2012). At the individual level, predation can result in reduced growth, fecundity, foraging efficiency, survival, and ultimate fitness of prey (Sih 1980; Lima and Dill 1990; Peckarsky et al. 1993; Abrams et al. 1996; Peacor and Werner 1997; Zanette et al. 2011).
Mammalian predators frequently use chemical scents to transmit information about sexual condition, group membership, social status, and territory ownership (Sankar and Archunan 2008; Gelperin 2008), as well as optimising the use of food caches (Henry 1977), the defence of food resources (Piñeiro and Barja 2015), and for active defence (Medill et al. 2011). In the case of territory ownership, scent cues enable territorial boundaries to be delineated without the need for direct contact between conspecifics, thus reducing the risk of conflict and injury (Relyea 2003; Kusch et al. 2004; Ferrari et al. 2006; Hawkins et al. 2007; Smith et al. 2008). In these contexts, scent markers are used actively and deliberately. In addition to deliberate scent cues, some are left inadvertently by individuals as they commute, often in the form of skin cells and/or fur (dander) (Apfelbach et al. 2005). These scents, as well as those associated with urine, faeces, and excretions from scent glands (Burger 2005), contain a complex mixture of compounds that vary in their molecular weight and can vary over time as the different compounds aerosolise at different rates (Riffell et al. 2008; McFrederick et al. 2009). Consequently, conspecifics are likely able to use the composition of these chemical cues to indicate the time since their deposition and hence the likely presence or absence of an individual (Wyatt 2014). Prey species consider the presence of predator chemical cues when choosing habitats (Turley and Findlay 2009; Ferrero et al. 2011). Upon detection of chemicals associated with predators, known as kairomones (Schoeppner & Relyea 2009), prey may lower activity and feeding levels or increase the use of refugia to lessen the chances of an encounter (Mathis 2003; Foam et al. 2005; Šmejkal et al. 2018). The extent of a prey individual’s response to the detection of kairomones may be relative to the predator species detected (Schoeppner and Relyea 2009). The presence of predators creates a ‘landscape of fear’ (LOF), within which prey species ‘fear’ one or more predatory species and thus avoid regions deemed high-risk (Kohl et al. 2018).
Avoidance may have wider ecological impacts; for example, increased vegetation and crop growth in areas that are avoided by prey species (Manning et al. 2009). Crops have been protected from African elephants (Loxodonta africana) by using active African beehives (Apis mellifer scutellata) (Vollrath and Douglas-Hamilton 2002; King et al. 2007, 2009). Furthermore, LOFs could be used to inform pest management plans that focus on areas considered by prey individuals to be of low predation risk, with research showing that damage to trees from rodent pests reduced in the presence of predatory odours (Sullivan et al. 1988; Krijger et al. 2017). Thus, a LOF could be induced artificially with the presence of predatory odours to reduce the settlement and persistence of problematic prey species. Such an intervention may prove useful in invasive species management.
Since its introduction to Britain more than 140 years ago, the range of eastern grey squirrels (Sciurus carolinensis) has increased substantially (Gurnell et al. 2009). The expansion of grey squirrels is often associated with the decline of the native Eurasian red squirrel (Sciurus vulgaris), through a range of factors including the transmission of squirrel poxvirus (SQPV) (Sainsbury et al. 2000; Gurnell et al. 2012), superior foraging efficiency (Mazzamuto et al. 2016), behavioural dominance (Gurnell et al. 2004), and forest cover (Gurnell et al. 2014). Currently, grey squirrel management may be achieved through trapping and shooting (BASC 2016). These methods may effectively remove individuals but are unlikely to significantly reduce populations. Other methods, including immunocontraception and gene editing, are being pursued with little evidence of successful application thus far.
Grey squirrel management may be achieved through reintroducing native predators that have since been extirpated. Pine martens (Martes martes), which have been confined to Scotland and Ireland since the late 1800s and 1900s due to severe persecution and habitat loss (Langley and Yalden 1977; Birks et al. 2005; Couzens et al. 2017), have recently been introduced to receptor sites in England and Wales (Vincent Wildlife Trust 2022). Though considered predators of both red and grey squirrels, pine martens potentially predate upon greys more than reds and their presence is negatively correlated with grey squirrel presence (Sheehy and Lawton 2014; Sheehy et al. 2018). Recovering pine marten numbers have also been linked to a decline of grey squirrels in Ireland (Sheehy and Lawton 2014). Consequently, there is interest in how the spatial distribution patterns of grey squirrels may change over time as pine marten populations increase and expand, and how this might encourage the recovery of red squirrels in England and Wales.
Though there are numerous studies demonstrating the effects a LOF has upon prey behaviour, little is known on the concept in grey squirrel populations. This study aimed to investigate whether grey squirrel activity at artificial feeders was reduced under the simulated presence of (a) domestic cats (Felis catus), an invasive predator, and (b) pine martens, a native predator, through the application of chemical cues. The behavioural response of grey squirrels under the perceived presence of these predators, and any discrepancies between the duration or extent to which these behaviours are displayed, may shed light on the LOF concept and its potential applications in invasive species management.
H 0 = Eastern grey squirrels would show no significant alteration in their observed foraging behaviour in the presence of predator olfactory cues, compared to control cues.
H 1 = Eastern grey squirrels would significantly reduce foraging efforts in the presence of predator olfactory cues, compared to control cues.