Native and invasive squirrels show different behavioural responses to scent of a shared native predator

Invasive species pose a serious threat to native species. In Europe, invasive grey squirrels ( Sciurus carolinensis ) have replaced native red squirrels ( Sciurus vulgaris ) in locations across Britain, Ireland and Italy. The European pine marten ( Martes martes ) can reverse the replacement of red squirrels by grey squirrels, but the underlying mechanism of how pine martens suppress grey squirrels is little understood. Research suggests the reversal process is driven by direct predation, but why the native red squirrel may be less susceptible than the invasive grey squirrel to predation by a commonly shared native predator, is unknown. A behavioural difference may exist with the native sciurid being more effective at avoiding predation by the pine marten with which they have a shared evolutionary history. In mammals, olfactory cues are used by prey species to avoid predators. To test whether anti-predator responses differ between the native red squirrel and the invasive grey squirrel, we exposed both species to scent cues of a shared native predator and quantified the responses of the two squirrel species. Red squirrels responded to pine marten scent by avoiding the feeder, increasing their vigilance and decreasing their feeding activity. By contrast, grey squirrels did not show any anti-predator behaviours in response to the scent of pine marten. Thus, differences in behavioural responses to a shared native predator may assist in explaining differing outcomes of species interactions between native and invasive prey species depending on the presence, abundance and exposure to native predators.

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Habitat mediates coevolved but not novel species interactions

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2021.2338 ◽

2022 ◽

Vol 289 (1966) ◽

Author(s):

Joshua P. Twining ◽

Chris Sutherland ◽

Neil Reid ◽

David G. Tosh

Keyword(s):

Species Interactions ◽

Prey Species ◽

Positive Influence ◽

Habitat Modification ◽

Red Squirrel ◽

Pine Marten ◽

Grey Squirrel ◽

Landscape Modification ◽

Anthropogenic Habitat ◽

Invasive Prey

Ongoing recovery of native predators has the potential to alter species interactions, with community and ecosystem wide implications. We estimated the co-occurrence of three species of conservation and management interest from a multi-species citizen science camera trap survey. We demonstrate fundamental differences in novel and coevolved predator–prey interactions that are mediated by habitat. Specifically, we demonstrate that anthropogenic habitat modification had no influence on the expansion of the recovering native pine marten in Ireland, nor does it affect the predator's suppressive influence on an invasive prey species, the grey squirrel. By contrast, the direction of the interaction between the pine marten and a native prey species, the red squirrel, is dependent on habitat. Pine martens had a positive influence on red squirrel occurrence at a landscape scale, especially in native broadleaf woodlands. However, in areas dominated by non-native conifer plantations, the pine marten reduced red squirrel occurrence. These findings suggest that following the recovery of a native predator, the benefits of competitive release are spatially structured and habitat-specific. The potential for past and future landscape modification to alter established interactions between predators and prey has global implications in the context of the ongoing recovery of predator populations in human-modified landscapes.

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The enemy of my enemy is my friend: native pine marten recovery reverses the decline of the red squirrel by suppressing grey squirrel populations

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.2603 ◽

2018 ◽

Vol 285 (1874) ◽

pp. 20172603 ◽

Cited By ~ 24

Author(s):

Emma Sheehy ◽

Chris Sutherland ◽

Catherine O'Reilly ◽

Xavier Lambin

Keyword(s):

Native Species ◽

Site Occupancy ◽

Apparent Competition ◽

Red Squirrel ◽

Pine Marten ◽

Grey Squirrel ◽

Capture Recapture ◽

Contrast Exposure ◽

The Impact ◽

Grey Squirrels

Shared enemies may instigate or modify competitive interactions between species. The dis-equilibrium caused by non-native species introductions has revealed that the outcome of such indirect interactions can often be dramatic. However, studies of enemy-mediated competition mostly consider the impact of a single enemy, despite species being embedded in complex networks of interactions. Here, we demonstrate that native red and invasive grey squirrels in Britain, two terrestrial species linked by resource and disease-mediated apparent competition, are also now linked by a second enemy-mediated relationship involving a shared native predator recovering from historical persecution, the European pine marten. Through combining spatial capture–recapture techniques to estimate pine marten density, and squirrel site-occupancy data, we find that the impact of exposure to predation is highly asymmetrical, with non-native grey squirrel occupancy strongly negatively affected by exposure to pine martens. By contrast, exposure to pine marten predation has an indirect positive effect on red squirrel populations. Pine marten predation thus reverses the well-documented outcome of resource and apparent competition between red and grey squirrels.

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Natural strongholds for red squirrel conservation in Scotland

Nature Conservation ◽

10.3897/natureconservation.43.62864 ◽

2021 ◽

Vol 43 ◽

pp. 93-108

Author(s):

Andrew Slade ◽

Andy White ◽

Kenny Kortland ◽

Peter W. W. Lurz

Keyword(s):

Management Practice ◽

Management Policy ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Grey Squirrel ◽

Case Scenario ◽

Red Squirrels ◽

Worst Case ◽

Standard Management ◽

Grey Squirrels

The Eurasian Red Squirrel (Sciurus vulgaris) is under threat from the invasive North American eastern Grey Squirrel (Sciurus carolinensis) with 80% of the remaining red squirrel populations in the British Isles found in Scotland. In this study we develop a spatially explicit mathematical model of the red and grey squirrel system and use it to assess the population viability of red squirrels across Scotland. In particular, we aim to identify existing forests – natural strongholds for red squirrels – that can successfully support red squirrels under UK Forestry Standard management and protect them from potential disease-mediated competition from grey squirrels. Our model results indicate that if current levels of grey squirrel control, which restrict or reduce the distribution of grey squirrels, are continued then there will be large expanses of forests in northern Scotland that support viable red squirrel populations. Model results that represent (hypothetical) scenarios where grey squirrel control no longer occurred indicated that grey squirrel range expansion and the process of red squirrel replacement would be slow. Model results for an assumed worst-case scenario where grey squirrels have expanded to all regions in Scotland identified forest regions – denoted natural strongholds – that could currently support red squirrels under UK Forestry Standard management practice. The results will be used to inform forest management policy and support a strategic review of red squirrel management by land management agencies and other stakeholders.

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Disease threats posed by alien species: the role of a poxvirus in the decline of the native red squirrel in Britain

Epidemiology and Infection ◽

10.1017/s0950268805005303 ◽

2005 ◽

Vol 134 (3) ◽

pp. 521-533 ◽

Cited By ~ 85

Author(s):

S. P. RUSHTON ◽

P. W. W. LURZ ◽

J. GURNELL ◽

P. NETTLETON ◽

C. BRUEMMER ◽

...

Keyword(s):

Population Control ◽

Disease Model ◽

Red Squirrel ◽

Grey Squirrel ◽

Red Squirrels ◽

Contact Rates ◽

The United Kingdom ◽

Model Predictions ◽

Grey Squirrels

Red squirrels are declining in the United Kingdom. Competition from, and squirrel poxvirus (SQPV) disease carried by, grey squirrels are assumed to be determining the decline. We analyse the incidence of disease and changes in distribution of the two species in Cumbria, from 1993 to 2003 and compare these to the predictions of an individual-based (IB) spatially explicit disease model simulating the dynamics of both squirrel species and SQPV in the landscape. Grey squirrels increased whilst red squirrels declined over 10 years. The incidence of disease in red squirrels was related to the time since grey squirrels arrived in the landscape. Analysis of rates of decline in red squirrel populations in other areas showed that declines are 17–25 times higher in regions where SQPV is present in grey squirrel populations than in those where it is not. The IB model predicted spatial overlap of 3–4 years between the species that was also observed in the field. The model predictions matched the observed data best when contact rates and rates of infection between the two species were low. The model predicted that a grey squirrel population control of >60% effective kill was needed to stop the decline in red squirrel populations in Cumbria.

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An Opportunistic Assessment of the Impact of Squirrelpox Disease Outbreaks upon a Red Squirrel Population Sympatric with Grey Squirrels in Wales

Animals ◽

10.3390/ani12010099 ◽

2022 ◽

Vol 12 (1) ◽

pp. 99

Author(s):

Craig M. Shuttleworth ◽

David Everest ◽

Paul Holmes ◽

Suzi Bell ◽

Rachel Cripps

Keyword(s):

Survival Rates ◽

Disease Outbreaks ◽

Sciurus Carolinensis ◽

Red Squirrel ◽

Grey Squirrel ◽

Red Squirrels ◽

Local Survival ◽

Temporal And Spatial ◽

The Impact ◽

Grey Squirrels

Native red squirrels (Sciurus vulgaris) persisted in the coastal mainland woodlands of northern Gwynedd whilst sympatric with an invasive grey squirrel (Sciurus carolinensis) population suppressed by culling. Squirrelpox disease in the red squirrel population was recorded in 2017 and 2020/21. An autumn 2020 outbreak was associated with only 17.4% of animals caught and marked in the preceding June known to be present in March 2021. Despite an opportunistic data collection lacking the rigour of empirical experimental design, we observed low local survival rates similar to previously published accounts reported during major squirrelpox outbreaks. The use of a conservation dog to detect red squirrel carcasses resulted in positive detection and confirmation of a temporal and spatial expansion of one disease outbreak. The study is the first in Wales to use conservation dogs and the findings reinforce the vital strategic importance of geographical isolation reducing sympatry of red with grey squirrels in European regions where the introduced congener is a source of the squirrelpox infection.

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The preference for yew (Taxus baccata) by a red (Sciurus vulgaris) only squirrel population

Wildlife Research ◽

10.1071/wr15009 ◽

2015 ◽

Vol 42 (5) ◽

pp. 426 ◽

Cited By ~ 3

Author(s):

Amy Haigh ◽

Ruth O'Riordan ◽

Fidelma Butler

Keyword(s):

Tree Species ◽

Tree Planting ◽

Taxus Baccata ◽

Grey Squirrel ◽

Red Squirrels ◽

Coniferous Species ◽

Coniferous Tree Species ◽

Term Maintenance ◽

Grey Squirrels

Context As invasive grey squirrels continue to spread, red only areas are becoming rarer. It has been reported that red squirrels can outcompete greys only in pure coniferous woodland. In areas of sympatry with grey squirrels, there are concerns about red squirrels’ dependence on certain coniferous tree species in light of recent tree diseases. Aims This study aimed to investigate tree selection by red squirrels in an area vulnerable to the spread of the grey squirrel, but currently free of this species. Methods During 2013–14, squirrels were trapped and monitored on a 315-ha managed island, with a woodland characterised by a mixture of deciduous and coniferous species. Radio-tracking revealed that squirrels clustered their activity along a network of yew trees, a preference they showed throughout the year. Trap success was also higher in traps placed on yew trees. Yew and beech were selected most commonly, but squirrels were also observed foraging on other items, such as sycamore flowers and lichen. Squirrels spent 35% of their time foraging, utilising the greatest number of tree species in June (n = 13). In spring, squirrels foraged to a greater extent on the ground than in the trees, and exploited a lower number of tree species. Conclusions There has been little previous data on the use of yew trees by red squirrels, but they have previously been listed as a species that is preferred by red squirrels rather than greys. This study has further emphasised the importance of this tree species to red squirrels. Implications The continued spread of the grey squirrel may lead to red squirrels becoming restricted to areas of intense management such as parks and, accordingly, optimum tree planting is required from the onset for the long-term maintenance of red squirrels. With recent concern about the disease vulnerability of other coniferous species, this study emphasises the relative importance of yew and other tree species in the distribution of red squirrels.

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Imagining Rabbits and Squirrels in the English Countryside

Society and Animals ◽

10.1163/156853001753639260 ◽

2001 ◽

Vol 9 (2) ◽

pp. 163-175 ◽

Cited By ~ 1

Author(s):

Hilda Kean

Keyword(s):

Red Squirrel ◽

Way Of Life ◽

Grey Squirrel ◽

Red Squirrels ◽

The Past ◽

Country Life ◽

Post War

AbstractDrawing on contemporary coverage, particularly in The Field and Country Life, this article considers the construction of rabbits and squirrels as images of the past in England. By the 1930s, the red squirrel had become increasingly rare in the English countryside. Particularly in towns and suburbs, the population of the grey squirrel was growing rapidly. Those who saw themselves as the custodians of the countryside depicted the grey squirrel as a foreign force inimical to a mythical English way of life as epitomized by the red squirrel. In the post war period, the debate resurfaced about the nature of the countryside and who had a right to defend it. The focus then was upon the spread of myxomatosis from France, which was depicted as a foreign disease. Wild rabbits, who died in the thousands from this infection, became appropriated, as red squirrels before them, as symbols of a lyrical and ordered past in the countryside.

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Epidemiology of squirrelpox virus in grey squirrels in the UK

Epidemiology and Infection ◽

10.1017/s0950268810000816 ◽

2010 ◽

Vol 138 (7) ◽

pp. 941-950 ◽

Cited By ~ 26

Author(s):

C. M. BRUEMMER ◽

S. P. RUSHTON ◽

J. GURNELL ◽

P. W. W. LURZ ◽

P. NETTLETON ◽

...

Keyword(s):

Disease Transmission ◽

Structural Equation ◽

Reservoir Host ◽

Red Squirrel ◽

Grey Squirrel ◽

Management Options ◽

Contact Points ◽

Squirrelpox Virus ◽

The Uk ◽

Grey Squirrels

SUMMARYThe dramatic decline of the native red squirrel in the UK has been attributed to both direct and disease-mediated competition with the grey squirrel where the competitor acts as a reservoir host of squirrelpox virus (SQPV). SQPV is threatening red squirrel conservation efforts, yet little is known about its epidemiology. We analysed seroprevalence of antibody against SQPV in grey squirrels from northern England and the Scottish Borders in relation to season, weather, sex, and body weight using Generalized Linear Models in conjunction with Structural Equation Modelling. Results indicated a heterogeneous prevalence pattern which is male-biased, increases with weight and varies seasonally. Seroprevalence rose during the autumn and peaked in spring. Weather parameters had an indirect effect on SQPV antibody status. Our findings point towards a direct disease transmission route, which includes environmental contamination. Red squirrel conservation management options should therefore seek to minimize squirrel contact points.

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Invading parasites: spillover of an alien nematode reduces survival in a native species

Biological Invasions ◽

10.1007/s10530-021-02611-7 ◽

2021 ◽

Author(s):

Claudia Romeo ◽

Anna Pia Piscitelli ◽

Francesca Santicchia ◽

Adriano Martinoli ◽

Nicola Ferrari ◽

...

Keyword(s):

Body Mass ◽

North American ◽

Native Species ◽

Resource Competition ◽

Viral Disease ◽

Red Squirrels ◽

Local Survival ◽

Survival And Reproduction ◽

The Impact ◽

Grey Squirrels

AbstractIt is widely assumed that spillover of alien parasites to native host species severely impacts naïve populations, ultimately conferring a competitive advantage to invading hosts that introduced them. Despite such host-switching events occurring in biological invasions, studies demonstrating the impact of alien macroparasites on native animal hosts are surprisingly few. In Europe, native red squirrels (Sciurus vulgaris) are replaced by introduced North American grey squirrels (S. carolinensis) mainly through resource competition, and, only in the United Kingdom and Ireland, by competition mediated by a viral disease. In Italy such disease is absent, but spillover of an introduced North American nematode (Strongyloides robustus) from grey to red squirrels is known to occur. Here, we used long-term (9 years) capture-mark-recapture and parasitological data of red squirrels in areas co-inhabited by grey squirrels in Northern Italy to investigate the impact of this alien helminth on naïve native squirrels’ body mass, local survival, and reproduction of females. We found no negative effect of the alien parasite on body mass or reproductive success, but intensity of infection by S. robustus reduced survival of both male and female squirrels. Significantly, survival of squirrels co-infected by their native nematode, Trypanoxyuris sciuri, was less affected by S. robustus, suggesting a protective effect of the native helminth against the new infection. Hence, we demonstrate that alien S. robustus spillover adds to the detrimental effects of resource competition and stress induced by grey squirrels, further reducing the fitness of the native species in the presence of the invasive competitor.

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