18. Grey squirrel nesting ecology and the use of nest

18. Grey squirrel nesting ecology and the use of nest sites in European population management CRAIG M SHUTTLEWORTH, VESA SELONEN and JOHN L KOPROWSKI

Summary Grey squirrels (Sciurus carolinensis) are an arboreal species that construct leaf nests (dreys) high in the woodland canopy. They will also den within tree cavities and inside artificial den sites such as wooden boxes. Occasionally, individuals will build a nest within the eaves or attic roof spaces of buildings. In this paper, we review the nesting behaviour of grey squirrels, examine nest site occupancy as a means of monitoring population abundance, review the control of grey squirrels whilst using different nest sites, and consider how an understanding of nesting behaviour might help evolve grey squirrel control programmes in Europe. Although there are several detailed studies of nest box use in North American populations, across Europe there remain only limited data with respect to artificial dens. We report nest box use by grey squirrels in Britain before highlighting opportunities for future ecological study, which may assist in managing this invasive pest species. In this context, we make reference to findings of long-term nest box studies of European red squirrel (S. vulgaris) and flying squirrels that require replication.

Introduction Mature forest stands with a dense canopy structure are important for arboreal tree squirrels in the genus Sciurus; particularly those habitats with a high tree species richness providing favourable seed crops and secondary food items (buds, shoots and fungi) (Gurnell 1983; Koprowski 2005). Tree stems and branches provide locations for the construction of dreys (leaf and branch nests) and naturally formed cavities offer den sites. In Europe, the grey squirrel (Sciurus carolinensis) is an invasive species which has significant ecological impacts upon the native red squirrel (Sciurus vulgaris) (Gurnell et al. 2015) and causes damage to hardwood stands by bark stripping (Rowe & Gill 1985). An understanding of nesting ecology is therefore an important element in the development of population management strategies within this continent.

Dreys/tree leaf nests Grey squirrels use a combination of dens (tree cavities: Edwards & Guynn 1995) and dreys (leaf nests: Uhlig 1956; Don 1985) for protection from the elements,

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The Grey Squirrel: Ecology & Management of an Invasive Species in Europe

refuge from threats, as sleeping locations and as sites to rear their young (kittens). Dreys are a particularly conspicuous sign of grey squirrel occupancy in a woodland, in broadleaved habitats during the winter months when the tree canopy has shed all its leaves (Shorten 1951). However, an absence of dreys does not mean that squirrels are absent, because animals may be using den sites and dreys can be difficult to detect in some woodland habitats especially when built in dense foliage, within ivy (Hedera helix) or other climbers such as honeysuckle (Lonicera spp.). Detectability of nests has not been systematically examined. Individuals construct their dreys on branches or a tree limb in the tree canopy commonly at 50 to 65% of the total tree height (Brown & Twigg 1965; Kyle 2009). These nests typically consist of a platform of twigs (generally 10 to 20 cm length) upon which a compacted layer of fragmented and often decaying matter forms a floor. The outer framework is constructed of leaves and twigs and shredded organic material, provides a soft and warm internal lining (Shorten 1962; Koprowski 1994) e.g. moss, lichen, soft bark such as Wellingtonia spp. (Gurnell 1987) and grass (Laidler 1980). Both leafless and foliated twigs are collected from the forest canopy and are used in nest building (Middleton 1931). These components are obtained from a range of local tree species (Fitzwater & Frank 1944). In many cases, the majority of twigs are collected from the tree that the drey is located within (Brown & Twigg 1965). The volume of nests can vary from 18 to 147 litres (l) (mean = 47.25 l) with a mass of 450 to 4,450 g (mean = 1,300 g: Fitzwater & Frank 1944). Animals may, over time, continue to add material to a completed drey. However, as the size of a drey is influenced by the nature of the support of branches upon which it is constructed, size is not a reliable indication of the age of a drey. In addition to the large compact dreys described above, grey squirrels also build more temporary ‘saucer-shaped’ platforms (Shorten 1962; Tittensor 1970) situated on smaller branches away from the main trunk (Brown & Twigg 1965). These light structures are used as rest sites during daylight hours particularly in the summer months and may be a useful means for animals to escape heavy parasite loads (e.g. fleas Orchopeas howardi, see Brit & Molyneux 1979) that often accumulate within the denser spherical dreys (Shorten 1962). Both dreys and temporary platforms constructed by grey squirrels are also constructed by the native Eurasian red squirrel (Wauters & Dhondt 1990). Seasonal variation in drey building activity has been observed in North America. An initial peak occurs in July, coinciding with a pulse in parturition dates, and a second in late October and November (Uhlig 1956). In Britain, most nest building similarly occurs across this period (Shorten 1962). Although populations may select a wide variety of tree species within which to build dreys, some preferences for specific tree species have been recorded including pines (Pinus spp.) and oak (Quercus spp.) (Edwards & Guynn 1995, United

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Grey squirrel nesting ecology

States of America (USA), oak (Shorten 1951, England), hickories (Carya spp.), red maple (Acer rubrum) (Sanderson et al. 1976, USA), Lebanon cedar (Cedrus libani), sweet chestnut (Castanea sativa) or beech (Fagus sylvatica) (Brown & Twigg 1965, England), red oak (Quercus rubra), pendunculate oak (Q. robur), cherry (Prunus spp.) and Robinia spp. (Currado et al. 1987, Italy). Nest site selection is likely to be influenced by a variety of additional factors including individual tree height, canopy connectivity, the presence of ivy and proximity of a tree to areas of high food supply, and is similar between urban and rural areas (Williams 2011).

Tree dens Natural cavities form from decay inside the tree heart wood. This can be as a direct consequence of disease or rot within the stem, decay as a result of physiological stress causing branches to break away, or excavation by woodpeckers (Picidae spp.). Smaller cavities may provide grey squirrels with a temporary hiding place if disturbed (classed as escape dens) whilst those larger cavities (e.g. 15 to 18 centimetre (cm) diameter and 38 cm depth - as described in Sanderson 1975) that remain dry will offer a suitable den site for a nest (Sanderson et al. 1976). The formation of suitable den cavities can take many decades (Baumgartner 1939) and as such, cavities are a feature associated with mature woodland habitats. Grey squirrels nest within cavities formed inside a variety of mature deciduous tree species both in North America (see Sanderson et al. 1976) and in Britain where oak, beech, sweet chestnut, maple (Acer spp.), cherry, poplar (Populus spp.) and birch (Betula spp.) cavities have been recorded (see Shorten 1962). An entrance of 5 to 20 cm diameter is attractive (Edwards et al. 2003) and where necessary, grey squirrels can chew wood to maintain or enlarge an opening (Sanderson 1975; Sanderson et al. 1976; Stone et al. 1996). Cavities may be used by a range of other wildlife at different times, and thus may be a means of grey squirrels picking up their ectoparasites (such as ticks) and infections such as Borrelia garinii (see Millins et al. this volume, Chapter 10). In one detailed North American study of grey squirrel nesting site selection in mixed deciduous woodland, dens (two to four per hectare (ha)) were more frequent than dreys (0.5 to two per ha); with a typical den entrance height of around eight metres from ground level (Sanderson et al. 1976). Nixon & Hanson (1987) reported that dreys were used most frequently in the warmer months of the year and den use peaked in the winter period. Subsequent radiotracking studies also showed grey squirrel use of cavities was greatest in winter (Edwards & Guynn 1995). Den use may reflect benefits afforded from greater protection from the elements and/or predators (Barkalow & Soots 1965a and b) as well as offering thermoregulatory benefits (Havera 1979) particularly when grey squirrels nest communally (Koprowski 1996).

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Given the obvious importance that den sites play in grey squirrel ecology (Edwards & Guynn 1995), population management in North America includes prescriptions to maintain or enhance den availability. Actions include preferentially maintaining tree species that have a high probability of producing cavities, extending forest stand rotation length, deliberately girdling the bark from large branches to facilitate cavity formation in individual trees and the provision of artificial dens (Sanderson 1975). Such activities also benefit the wider range of fauna that are specialised or opportunistic users of tree cavities (see Carey & Gill 1983; Aiken & Martin 2012). An individual grey squirrel will have more than one nest site within its home range, often averaging four or five (Steele & Koprowski 2001), and animals will share construction (Koprowski & Koprowski 1987) and occupancy of some of these with other individuals sometimes communally (Koprowski 1996; Taylor 1969). Koprowski (1996) reported a long term population study (1986 to 1990) in a black walnut (Juglans nigra) and oak dominated 4.2 ha Kansas parkland woodland. Trapped grey squirrels were visually marked and animals commonly observed to nest communally in groups of two to nine squirrels within tree dens. The largest groups were found in the autumn and winter months. Kinship affected the probability of nest sharing. Of 52 nesting groups which contained more than one adult female, related females (the coefficient of relationship r > 0.25) exclusively were together in 82.5% of the nests (Koprowski 1996).

Nest boxes & artificial dens sites North American studies have shown that grey squirrels readily use wooden nest boxes (Barkalow & Soots 1965a; Ackerman & Weigl 1970; Edwards et al. 2003; Fokidis & Risch 2005) and are observed to opportunistically nest in attic roof spaces (Nowak 1999). Barkalow and Soots (1965a) were the first to demonstrate that the availability of wooden nest boxes increased grey squirrel carrying capacity in their sub-climax woodland study areas. A subsequent study using ‘rubber tyre dens’ in woodland where tree cavities were scarce and food supplies favourable, also led to an increase in population density (x1.6 to 2.2 fold) via improved survival of both young and adults (Burger 1969; Telford 1986). Nixon and Donohoe (1979) similarly reported that in their study, the provision of six to eight artificial dens per hectare increased grey squirrel density within 30 to 60 year-old hardwood stands. The erection of artificial den sites clearly benefits grey squirrels, and den studies have provided valuable population data (Barkalow & Soots 1965a; Barkalow et al. 1970) and have been a useful tool in quantifying patterns of habitat use by the species (Steele & Koprowski 2001). In Europe where the grey squirrel is an invasive non-native with significant impacts on native ecosystems (Gurnell 1996) the species will opportunistically

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use nest boxes erected for owls (Barn Owl Trust 2012). There are however few studies into the use of artificial dens by grey squirrels. A notable example is Gurnell & Taylor (1989) who monitored boxes in an area of sympatric red and grey squirrel populations (Table 1), and found box use varied from 33% to 65%. The presence of individual grey squirrels discovered within red squirrel nest boxes has facilitated their control (Shuttleworth et al. 2009) but such isolated examples of culling using boxes are opportunistic rather than proactive in nature. Table 1. Grey squirrel nest box use in pine stands within Thetford Forest, England, Europe (Reproduced from Gurnell & Taylor 1989).

Study Area

Number of nest boxes

Month

Carcasses recovered

Grey squirrel hairs on tape

% Seasonal box use

SA2

17

Apr

1

8

47%

Jul

3

11

65%

Feb

1

11

65%

Apr

0

10

55%

Jul

0

8

44%

Feb

1

6

33%

SA3

18

More recently, short term nest box research has taken place in broadleaved habitat within the counties of Conwy and Gwynedd (north Wales). In late March 2014, twenty grey squirrel nest boxes constructed of two centimetre wide plyboard (Table 2) were erected within a 6.7 ha block of mixed woodlands in the grounds of the Welsh Mountain Zoo, Conwy, north Wales. The woodland was continuous with adjacent stands including residential areas of Colwyn Bay town. The boxes were filled with loosely packed hay to a level just below the entrance hole (following Shuttleworth & Schuchert 2014) and double-sided sticky tape placed beneath the entrance hole to catch hairs from animals using these artificial dens. Monthly box inspections indicated that a proportion (30 to 75%) of boxes were used each month through the late spring, summer and early autumn period (Figure 1) after which the population in the zoo grounds was heavily culled using cage trapping and then ad hoc shooting. During the box checks, six litters were discovered (Figure 2). Dead kittens were removed and those live young that could be caught were euthanized. These bodies were then made available to parallel viral infection studies (Everest et al. 2015, 2016). Mean litter size was 4.17 ± 0.47 (s.e) kittens. This is a population within mature mixed deciduous woodland and with ad hoc access to supplemental feeding from many zoo enclosures and hence densities are high. Culling removed 35 adults in three days equivalent to 5.2 adults per hectare.

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Table 2. Examples of nest box designs used by grey squirrels in the USA & Europe (EU)

Nest hole diameter

Box dimensions

Height fixed

Habitat Characteristics

Reference

6.4 cm

24x23x23 cm (internal)

2.7 to 4.6 m

Oak (Quercus spp.), sweetgum (Liquidambar styraciflua), blackgum (Nyssa sylvatica) & hickory (Carya spp.)

Stone et al. (1996); Arkansas, USA.

6.35 cm

18x18x45 cm high (external)

3.0 to 7.6 m

7 cm 8 cm (a square hole) 9 cm

Pines (Pinus spp.), hickories (C. glabra & C. tomentosa) & oak (Quercus spp.) Corsican pine (Pinus nigra)

28x34x36 cm high (external) 24.5x27x61 high (internal)

5.0 to 8.0 m 8.0 m

Corsican pine (Pinus nigra) & Scots pine (P. sylvestris).

28x26x34 high (internal)

4.0 to 5.0 m

Mixed mature woodland with Sycamore, birch, oak, beech, hazel and a variety of exotic coniferous species including Sitka spruce and Douglas fir in Cochwillan, and Scots pine, larch in the Zoo site.

Barkalow & Soots (1965b); North Carolina, USA. Barkalow & Soots (1965a); North Carolina, USA. Shuttleworth et al. (2009), Everest et al. 2009; Anglesey, Wales, EU Gurnell & Taylor (1989), Gurnell & Pepper (1994); Thetford, England, EU Shuttleworth unpublished data; Cochwillan & Welsh Mountain zoo sites, north Wales, EU

Thirty nest boxes identical in design and content to those used in the zoo were erected in Cochwillan, a discrete 19.7 ha river valley woodland (Gwynedd, north Wales) in May 2014. In November 2014, 73 adult and subadult grey squirrels were culled from the site. Nest box occupation was recorded from April to June 2015 (Figure 1), during which time a single litter was discovered. Following the last box check in early July, trap locations were baited for two weeks and in early August 2015, 16 traps were set for 17 days (272 trap days). A total of 125 individuals (including 98 animals weighing > 470g which were classified as adults) were removed (Shuttleworth, unpublished data). The data show that a disturbed (i.e. one exposed to earlier culling) grey squirrel population (5.0 adults per ha) will use boxes and this behaviour consequently provided very modest but useful data on box occupancy with respect to population size. Grey squirrels brought a range of nest material into boxes in north Wales, much as described for dreys (above), and which was collected from a variety of tree and shrub species. Boxes were often packed full of material including green leaved branches (Figure 3). Earlier studies have observed that female grey squirrels are more aggressive when they have dependent young and will defend nest sites from conspecifics (Shorten 1951; Sanderson 1975; Gurnell 1987). In Wales it was noteworthy that if nursing females returned to, or were present within, their nest box during inspection, they were extremely aggressive and frequently came within 1 to 1.5 m of the field worker. Animals would move around rapidly in the tree canopy above and would repeatedly approach the fieldworker from multiple directions - from beneath, from above and from the side of the tree trunk. 354


Figure 1. Nest box use in north Wales by two grey squirrel populations in mature mixed woodlands. Twenty boxes were available at the Welsh Mountain Zoo and thirty in Cochwillan. The Welsh Mountain Zoo population had access to supplemental foods and the Cochwillan population had been partially culled the previous year.

0.8

Welsh Mountain Zoo (2014)

Proportion of boxes used

0.7

Cochwillan (2015)

0.6 0.5 0.4 0.3 0.2 0.1 0 Apr

May

Jun

Jul

Aug

Sep

Month

Figure 2. A grey squirrel litter in a nest box in north Wales. Originally the litter would have been concealed within a cavity formed within the hay, but at seven weeks of age the kittens have moved out and compacted the nest material.

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Figure 3. Grey squirrel nest box full of green foliated beech twigs.

Figure 4. Flying squirrel nest boxes in Finland. Image kindly provided by Toni Laaksonen.

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Grey squirrel nest site management in Europe Drey abundance as a population monitoring technique In Europe, red squirrel abundance and the number of dreys detected in small woodland plots have been strongly correlated (Wauters & Dhondt 1986) with Wauters & Dhondt (1988, 1990) recording 4.5 to 5.0 dreys per red squirrel. The presence of active dreys is a reliable indicator of squirrel presence but although grey squirrels often build larger nests than their congener, there is no characteristic to reliably differentiate a drey constructed by a red squirrel from one built by a grey squirrel. Thus, in sympatric red/grey squirrel populations the use of dreys to estimate relative squirrel abundance is not practical. However in landscapes where the red squirrel is absent, dreys do offer a means to manage grey squirrel populations. In southern England, Don (1985) used drey data collected from woodland sites containing only grey squirrels, and observed a significant correlation (0.84 coefficient) between log drey density and log grey squirrel density (derived from mark-recapture studies). In those study sites repeatedly surveyed, the changes in squirrel density were reflected in observed changes in drey numbers thus offering a means of estimating population densities and relative change. The number of grey squirrels per ha could be estimated by number of dreys per ha x 0.75 (Don 1985). This calculation however only reliably applies in hardwood stands because in denser coniferous habitat more limited canopy visibility will lead to a differential drey detection rate (relative den cavity availability may also be a factor to consider). Detectability of nests has not been adequately assessed for grey squirrels and is a necessity for rigorous population estimation. Nevertheless, the potential value of drey counts was further highlighted by Bertolino & Genovesi (2003) in the context of tackling an invasive grey squirrel population in Piedmont, Italy. Counts in 1996 provided an inexpensive population estimate within a six km2 area comprised of mixed woodland (79.5%) and poplar plantation (20.5%). The analysis (see Wauters et al. 1997) suggested 0.5 squirrels per ha and in the absence of other census data, such a measure proved useful when Bertolino & Genovesi (2003) later projected rates of population expansion, although they pointed out it would be an underestimate due to animals also using tree dens. Nest abundance not only provides a means of estimating population size, but as unmaintained dreys are unlikely to persist for more than one or two years, they can be used to examine habitat preferences and occupancy. Fitzgibbon (1993) observed that dreys were more likely to occur in larger English woodlands and in stands, that were closer to a neighbouring woodland of five ha or greater in size, those that contained oak, beech or hazel (Corylus avellana) and sites with a high hedgerow density in the surrounding countryside.

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Nest site management Drey poking The characteristic shape, construction and position of dreys, lends itself to the control of grey squirrels using these leaf nests in areas where native red squirrels are absent. In some instances, an observer may find it challenging and sometimes impossible, to be able to differentiate between a drey and the nests of other species (such as corvids) due to a nest being partially obscured by foliage and branches, but nevertheless, large numbers of dreys can be identified with confidence. In Britain, grey squirrels are flushed from dreys in the late autumn and winter months by dislodging the structures from the trees using long extendable aluminium poles (Rowe 1983; Gurnell 1987). Flushed animals are then shot with a shotgun, or less frequently, a 0.22 calibre rifle. Mayle et al. (2007) and Lawton (2003) suggest that control via drey poking is generally ineffective at reducing squirrel populations in order to, for example, prevent bark stripping damage because the animals killed are rapidly replaced from adjacent uncontrolled populations. Fitzgibbon (1993), noted too, that squirrel presence in southern England woodlands was not affected by shooting. There is however, a value if the control technique is integrated alongside trapping operations and within a wider landscape control programme - particularly poking in February and March (Mayle et al. 2007) which follows the main period of grey squirrel dispersal and winter mortality. During the latter stages of grey squirrel eradication from Anglesey, drey poking was used to remove existing nests and use the construction of new dreys to reveal the presence of animals in two woodland sites (Porthamel & Felin Rhosgerrig). An eradication programme in a few small isolated islands of the Florida Keys, USA, used drey poking with success for the Mexican red-bellied squirrel (S. aureogaster), the only species that nests in dreys within the canopy there (Pernas & Clark 2011). The population was introduced in 1938 to Elliott Key and had spread to three neighbouring keys by the 1970s (Palmer et al. 2014). Dreys were surveyed and georeferenced then visited at night, when most likely to be occupied. Nests were destroyed by shooting and the carcasses collected and this indicated that an individual was removed for every 43 dreys removed. Wooden nest boxes and camera traps with baited stations were used to monitor efficacy of the removal (Pernas & Clark 2011). The technique is believed to have resulted in successful eradication of red-bellied squirrels by 2011 (Pernas & Clark 2011). Removal or reduction in cavity availability Woodland coverage dramatically declined to 4.7% in Britain at the start of the last century and though it has increased to 13% (Atkinson & Townsend 2011), this is largely through the establishment of short rotation spruce dominated

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coniferous plantation, a habitat type within which cavities are less likely to form relative to native hardwood stands. In the absence of appropriate field studies, the extent to which den site scarcity may have retarded grey squirrel densities remains unclear. In the USA, den reduction has been applied as a tool to reduce populations in small parkland areas (see Hadidian et al. 1987). Deliberately removing den trees as a wider landscape strategy could theoretically reduce European grey squirrel densities, but it would be an unrealistic proposal. The process would be expensive and detrimental to other species as natural cavities benefit a wide range of animals (Carey & Gill 1983). Patterns of likely den availability are nevertheless an important variable to consider when predicting relative grey abundance, and yet to date it does not seem to factor into the development of strategic control in Europe. We believe this is an omission that should be addressed, even if it relies upon making assumptions of cavity abundance based upon stand age and species composition. Provision of nest boxes (artificial dens) Shuttleworth (1995) suggested that nest boxes could lend themselves to the control of grey squirrel populations in geographical areas of Britain with heavy public access that precluded control via trapping, poisoning or shooting. Night time inspections would yield adults and dependent young in a manner to that described by Barkalow and Soots (1965b). However, although there are few examples of nest boxes being used in this way, regional red squirrel conservation projects are increasingly using boxes to conceal either kill traps or live capture traps placed within them in community parkland habitats (see Willis 2015). Everest et al. (2009, 2015, 2016) opportunistically used nest boxes to obtain pre-weaned grey squirrels in north Wales and discovered index cases of adenovirus infection and exposure to squirrelpox virus in culled kittens. These are useful studies, but there have been few other attempts to use nest boxes to investigate social organisation (see Koprowski 1996) or aspects of grey squirrel ecology in Europe. How the availability of additional dens sites affects grey squirrel populations, is also still not understood for the species as a European invasive (Gurnell & Taylor 1989) and this clearly remains a key area for further research. In contrast, studies on European flying squirrels and red squirrels have demonstrated the value of nest boxes not only as an aid in ecological research, but also as a valuable tool in the management of squirrels. Similarly, edible dormice (Glis glis) readily use nest boxes and studies have been invaluable in understanding hibernation, reproduction and survival (Bieber 1998; Ruf et al. 2006; Lebl et al. 2010; see also Fietz & Weis-Dootz 2012). The findings from these and box studies of native European squirrels highlight opportunities with regard to potential grey squirrel research.

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Nest box studies in native European squirrel species Flying squirrels depend on cavities as nesting sites and, thus, in many areas willingly accept nest boxes for nesting (Carey et al. 1997; Selonen et al. 2001; Fokidis & Reisch 2005). Consequently, nest box occupation has aided research of Siberian flying squirrels (Pteromys volans) and Southern and Northern flying squirrels (Glaucomys volans and sabrinus). The ease of capturing and handling of individuals from nest boxes has enhanced research into reproductive behaviour and mating system (Selonen et al. 2013), communal nesting (Layne & Raymond 1994; Selonen et al. 2014), survival and density (Ransome & Sullivan 2004; Lampila et al. 2009) and radio-telemetry (Selonen et al. 2001; Selonen & Hanski 2010). Interestingly, in Siberian flying squirrel studies, it is observed that communal nesting patterns (Selonen et al. 2014) or reproductive success (Hanski & Selonen, unpublished data) do not differ between natural cavities and nest boxes designed to resemble natural cavities (Figure 4). The Siberian flying squirrel uses cavities with an entrance hole size that prevents most natural enemies entering the cavity (nest box). This may be a reason that Siberian flying squirrels seldom abandon the cavity or nest box when disturbed, which eases capturing of individuals (V. Selonen, personal observation). For example, long-term monitoring and population research of Siberian flying squirrels occupying nest boxes in western Finland has been ongoing since 1992 (Lampila et al. 2009; Selonen et al. 2014; Wistbacka & Selonen et al., unpublished data). In this area, 500 to 600 nest boxes designed for flying squirrels are checked annually and the majority of boxes are in use by flying squirrels, providing data on population size and also individual reproductive success. Red squirrels are less dependent on cavities for nesting than flying squirrels and consequently, nest boxes have had a lesser role in their conservation. However, there are useful studies on nest-box occupancy and on those individuals caught from nest boxes within different parts of Europe: •

• •

•

•

In Italy, Mortelliti et al. (2009, 2011) and Zapponi et al. (2013) used nest boxes and hair tubes to study effects of habitat fragmentation on occurrence of red squirrels in forest patches surrounded by agricultural land. Hämäläinen (2014) and Fey et al. (2016) used nest boxes to trap individuals for radio-telemetry studies in Finland. Selonen et al. (2015) used the number of squirrel nests and litters found in nest boxes to infer the effect of food fluctuations on variation in squirrel population size. Shuttleworth and Schuchert (2014) found that around 20 to 30% of nest boxes were occupied by red squirrels (60 boxes studied) in Wales in a nine year long study. In a low density red squirrel area in western Finland, the species utilized nest boxes designed for Tengmalm’s owls (Aegolius funereus) (Korpimäki 360


•

& Hakkarainen 2012; Selonen et al. 2015). Around 13% of boxes contained squirrel nest material from 1982 to 2014 (400 to 500 boxes were available yearly) and the number of nests varied considerably between years depending on the masting of Norway spruce (Picea abies). In Finland, within an urban environment in the city of Turku, almost all available boxes (18 out of 22) designed for jackdaws (Corvus monedula) were used by red squirrels (contained nest material of squirrels; year 2013, V. Selonen, unpublished data), while jackdaws did not use these boxes. Observations of use of these boxes support the conclusions of Shuttleworth and Schuchert (2014) who observed that nest boxes (with seven cm entrance hole diameter) were not preferred by breeding red squirrel females. In Turku, red squirrel juveniles were located from jackdaw nest-boxes (with eight cm entrance hole diameter) only after weaning; whereas few new-born litters were located from smaller boxes designed for starlings with five cm entrance hole (entrance hole being little enlarged by the squirrels).

The wide geography and varying ecological communities encompassed by European squirrel nest box studies described above is clearly lacking for the grey squirrel. Such research has helped answer a raft of ecological questions, evolved techniques, including the use of hand nets, to capture animals leaving boxes (V. Selonen, personal observation) and provided observations of the relative use of different box designs. Research has illuminated the types of features that will encourage squirrel occupation and selection of a box as a breeding site.

Discussion Clear opportunities exist for the management of grey squirrel nest sites to be integrated into the wider control of this invasive species in Europe. For example, mapping the changing abundance and distribution of dreys, in landscapes where populations are exposed to intensive control, would provide a relative index of population decline and patterns of stand occupancy by residual populations. In broadleaved habitats, where it is difficult to use feeding signs to estimate squirrel abundance, drey counts might offer a potential alternative (Don 1985), but managers should always be aware that there are a paucity of detectability studies to help interpret results from habitats, where nests may be difficult to observe. The predilection for nesting within tree cavities has resulted in grey squirrels readily taking to suitable nest box designs. This behaviour offers a range of opportunities for scientific study. The effects of climatic change upon nest parasite loads, rates and transmission of pathological and asymptomatic viral and bacterial infections, in pre-weaned kittens and adults, patterns of communal nesting, habitat preferences, and of course data on parturition, litter size and 361


causes of natural mortality in populations are all areas of obvious investigation in Europe. Tree cavities present a difficulty with respect to systematic sampling (Fokidis & Risch 2005) and hence, nest boxes offer a means of looking at such den behaviour and also inter-specific interactions with other European cavity nesting species which compete with grey squirrels such as great tit (Parus major) (Shuttleworth & Schuchert 2014), other passerines (see Friesen et al. 2013), jackdaw (Shuttleworth 2001) and the red squirrel (Wauters & Dhondt 1990). If double-sided tape is placed inside the box directly beneath the entrance holes it can catch hairs which can be used in genetic studies. As we have described, long-term studies of native European tree squirrels using nest boxes have provided useful ecological data but these are sadly lacking for grey squirrels on this continent. North American findings have shown that increasing den availability increases population density. Although such a positive correlation might be expected in Europe there are sadly no data to demonstrate if this is indeed the case. It is noteworthy that whilst European populations are not exposed to raccoons (Procyon lotor), which are significant grey squirrel nest predators (see Barkalow & Soots 1965b), in Ireland, there is a strong negative correlation between the distribution of high density pine marten (Martes martes) populations and declines of established grey squirrel populations (Sheehy & Lawton 2014). Ireland currently has 8% woodland cover, but historically, had as little as 1% woodland cover in 1905. This means that the grey squirrels in this landscape may encounter relatively few tree cavities which North American research indicates confer higher survival rates relative to dreys. Although pine martens are able to widen a cavity entrance hole by chewing (Dave Tosh, personal communication), a possibility still exists that forest habitat structure might play a role in increasing their predation of nesting adults and dependent young, in squirrel populations dependent upon dreys as nest sites. The more aggressive behaviour of nursing grey squirrel females may also expose them to higher risk of predation by pine martens and other carnivores active at a leaf nest containing young, than is the case for the native red squirrel. This further highlights the need for research and consideration of nesting behaviour and nest site availability when assessing management of this invasive species in Europe.

Acknowledgements The authors would like to thank Toni Laaksonen for use of the photograph of a flying squirrel nest box and John Gurnell for providing data from grey squirrel nest box studies in Thetford forest. Liz Halliwell, Matt Hayward and Dave Tosh very generously provided useful comment on an earlier draft manuscript.

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References Ackerman R, Weigl PD (1970) Dominance relations of red and grey squirrels. Ecology 51: 332-334. Aiken KEH, Martin K (2012) Experimental test of nest-site limitation in mature mixed forests of central British Columbia, Canada. The Journal of Wildlife Management 76: 557-565. Atkinson S, Townsend M (2011) The state of the UK’s forests, woods and trees. A report to mark the international year of forests 2011. Woodland Trust, Lincolnshire, UK. Barkalow FS, Hamilton RB, Soots, RF (1970) The vital statistics of an unexploited gray squirrel population. The Journal of Wildlife Management 34: 489-500. Barkalow FS, Soots RF (1965a) Analysis of the effect of artificial nest boxes on a gray squirrel population. Transactions of the North American Wildlife and Natural Resources Conference 30: 349-360. Barkalow FS, Soots RF (1965b) An improved grey squirrel nest box for ecological and management studies. Journal of Wildlife Management 29: 679-684. Barn Owl Trust (2012) Barn owl conservation handbook: a comprehensive guide for ecologists, surveyors, land managers and ornithologists. Pelagic Publishing. Exeter, England. Baumgartner LL (1939) Fox squirrel dens. Journal of Mammalogy 20: 456-465. Bertolino S, Genovesi P (2003) Spread and attempted eradication of the grey squirrel (Sciurus carolinensis) in Italy, and consequences for the red squirrel (Sciurus vulgaris) in Eurasia. Biological Conservation 109: 351-358. Bieber C (1998) Population dynamics, sexual activity, and reproduction failure in the fat dormouse (Myoxus glis). Journal of Zoology 244: 223-229. Brit D, Molyneux DH (1979) Parasites of grey squirrels in Cheshire, England. Journal of Parasitology 65: 408. Brown JC, Twigg GI (1965) Some observations on grey squirrel dreys in an area of mixed woodland in Surrey. Notes on British mammals. Proceedings of the Zoological Society of London 144: 131152. Burger GV (1969) Response of grey squirrels to nest boxes at Remington Farms, Maryland. Journal of Wildlife Management 33: 796-801. Carey AB, Gill JD (1983) Direct habitat improvements - Some recent advances In: Snag Habitat Management: Proceedings of the Symposium, 80. Gen. Tech. Rep. RM-GTR-99. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain forest and Range Experiment Station. Carey AB, Wilson TM, Maguire CC, Biswell DBL (1997) Dens of northern flying squirrels in the Pacific Northwest. Journal of Wildlife Management 61: 684-699. Currado I, Scarramozzino PL, Brussino G (1987) Note sulla presenza dello scotiattolo grigio (Sciurus carolinensis Gmelin, 1788) in Piemonte (Rodentia: Sciuridae). Ann. Fac. Sci. Agr. Univ. Torino. 14: 307-331. Don BAC (1985) The use of drey counts to estimate grey squirrel populations. Journal of Zoology, London 206: 282-286. Edwards JW, Ford M, Guynn DC (2003) Fox and grey squirrels Sciurus niger & Sciurus carolinensis. In Feldhamer GA, Thompson BC, Chapman JA (eds) Wild Mammals of North America Biology, Management, and Conservation, 248-267. 2nd Edition. The John Hopkins University Press, Baltimore, Maryland. Edwards JW, Guynn Jr. DC (1995) Nest characteristics of sympatric populations of fox and gray squirrels. Journal of Wildlife Management 59: 103-110.

363


Everest DJ, Dastjerdi A, Cowan D, Gomm M, Shuttleworth CM, McInnes CJ, Deane D, Coulter L, Mill A, Rushton SP, Jackson NL, Litherland P (2015) Adenovirus detected from juvenile squirrels. Veterinary Record 177: 373-374. Everest DJ, Dastjerdi A, Cowan D, Gomm M, Shuttleworth CM, McInnes CJ, Deane D, Coulter L, Mill A, Rushton SP, Jackson NL, Litherland P (2016) SQPV antibody detection in juvenile squirrels. Veterinary Record 179: 101-102 DOI: 10.1136/vr.i3995. Everest DJ, Grierson SS, Stidworthy MF, Shuttleworth C (2009) PCR detection of adenovirus in grey squirrels on Anglesey. Veterinary Record 165: 482. Fey K, Hämäläinen S, Selonen V (2016). Roads are no barrier for dispersing red squirrels in an urban environment. Behavioural Ecology 27: 741-747. Fietz J, Weis-Dootz T (2012) Stranded on an island: consequences of forest fragmentation for body size variations in an arboreal mammal, the edible dormouse (Glis glis). Population Ecology 54: 313-320. Fitzgibbon CD (1993) The distribution of grey squirrel dreys in far, woodland: the influence of wood area, isolation and management. Journal of Applied Ecology 30: 736-742. Fitzwater WD Jr, Frank WJ (1944) Leaf nests of gray squirrel in Connecticut. Journal of Mammalogy 25: 160-170. Fokidis HB, TS Risch (2005) The use of nest boxes to sample arboreal vertebrates. South Eastern Naturalist 4: 447-458. Friesen LE, Casbourn G, Martin V, Mackay RJ (2013) Nest predation in an anthropogenic landscape. Wilson Journal of Ornithology 125: 562-569. Gurnell J (1983) Squirrel numbers and the abundance of tree seeds. Mammal Review 13: 133-148. Gurnell J (1987) The natural history of squirrels. Christopher Helm, Kent, England. Gurnell J (1996) The grey squirrel in Britain: problems for management and lessons for Europe. Proceedings of the 1st European Congress of Mammalogy. Museu Bocage. Lisboa. pp. 67-81. Gurnell J, Lurz PWW, Wauters LA (2015) Years of interaction and conflict in Europe: competition between Eurasian red squirrels and North American grey squirrels. In Shuttleworth CM, Lurz PWW, & Haywood MW (eds) Red squirrels: Ecology, Conservation and Management in Europe, 19-37. European Squirrel Initiative, Suffolk, England. Gurnell J, Pepper H (1994) Red squirrel conservation: field methods. Forest Information Note 255. Forestry Commission, Alice Holt, England. Gurnell J, Taylor J (1989) The conservation of red squirrels in relation to forest management. Forestry Commission, England. Hadidian J, Manski D, Flyger V, Cox C, Hodge G (1987) Urban gray squirrel damage and population management: a case history. Third Eastern Wildlife damage Control Conferences: 219-227. Hämäläinen S (2014) Dispersal behaviour of young red squirrels (Sciurus vulgaris) - decision-making and difference in dispersal distance between urban and rural environment (thesis in Finnish). MSc thesis, University of Turku, Finland. Havera SP (1979) Temperature variation in a fox squirrel nest box. The Journal of Wildlife Management 43: 251-253. Koprowski JL (1994) Sciurus carolinensis. Mammalian Species 480: 1-9. Koprowski JL (1996) Natal philopatry, communal nesting, and kinship in fox squirrels and eastern gray squirrels. Journal of Mammalogy 77: 1006-1016. Koprowski JL (2005) Management and conservation of tree squirrels: the importance of endemism, species richness, and forest condition. In Gottfried GJ, Gebow BS, Eskew LG, Edminster CB (eds) Connecting Mountain Islands and Desert Seas: Biodiversity and Management of the Madrean Archipelago II, 245-250. Proc. RMRS-P-36. Fort Collins, CO: U.S. Department of agriculture, 364


Forest Service, Rocky Mountain Research Station. Koprowski JL, Koprowski NM (1987) Joint nest-building activity in the eastern gray squirrel, Sciurus carolinensis. Canadian Field Naturalist 101: 610-611. Korpimäki E, Hakkarainen H (2012) The boreal owl: ecology, behaviour and conservation of a forestdwelling predator. Cambridge University Press, Cambridge. 359 pp. Kyle A (2009) A comparison of grey squirrel (Sciurus carolinensis) densities between an urban park and semi-rural woodland in Glasgow. The Glasgow Naturalist 25: 23-26. Laidler K (1980) Squirrels in Britain. David & Charles, Newton Abbot, England. Lampila S, Wistbacka A, Mäkelä A, Orell M (2009) Survival and population growth rate of the threatened Siberian flying squirrel (Pteromys volans) in a fragmented forest landscape. Ecoscience 16: 66-74. Lawton C (2003) Controlling grey squirrel damage in Irish broadleaved woodlands. COFORD Connects, Silviculture/Management No. 7, Council for Forestry Research and Development. Layne JN, Raymond MAV (1994) Communal nesting of southern flying squirrels in Florida. Journal of Mammalogy 75: 110-120. Lebl K, Kürbisch K, Bieber C, Ruf T (2010) Energy or information? The role of seed availability for reproductive decisions in edible dormice. Journal of Comparative Physiology B 180: 447-456. Mayle B, Ferryman M, Pepper H (2007) Controlling grey squirrel damage to woodlands. Forest Practice Note 4. Forestry Commission. Middleton (1931) The grey squirrel. Sidgewick & Jackson. London. Mortelliti A, Amori G, Capizzi D, Cervone C, Fagiani S, Pollini B, Boitani L (2011) Independent effects of habitat loss, habitat fragmentation and structural connectivity on the distribution of two arboreal rodents. Journal of Applied Ecology 48: 163-172. Mortelliti A, Santulli Sanzo G, Boitani L (2009) Species surrogacy for conservation planning: caveats from comparing the response of three arboreal rodents to habitat loss and fragmentation. Biodiversity and Conservation 18: 1131-1145. Nixon CM, Donohoe RW (1979) Squirrel nest boxes - are they effective in young hardwood stands? Wildlife Society Bulletin 7: 283-284. Nixon CM, Hansen LP (1987) Managing forests to maintain populations of gray and fox squirrels. Illinois Department of Conservation Technical Bulletin 5:1-35. Nowak RM (1999) Walker’s mammals of the world. 6th ed. Vol. II. The John Hopkins University Press, Baltimore and London. Palmer GH, Koprowski JL, Pernas AJ (2014) Distribution and spread of an introduced insular population of red-bellied squirrels (Sciurus aureogaster) in Florida. Mammalia 78: 67-73. Pernas AJ, Clark DW (2011) A summary of the current progress toward eradication of the Mexican gray squirrel (Sciurus aureogaster F. Cuvier, 1829) from Biscayne National Park, Florida, USA. In Veitch CR, Clout MN, Towns DR (eds). Island Invasives: Eradication and Management, 222-224. IUCN, Gland, Switzerland. Ransome DB, Sullivan TP (2004) Effects of food and densite supplementation on populations of Glaucomys sabrinus and Tamiasciurus douglasii. Journal of Mammalogy 85: 206-215. Rowe J (1983) Squirrel management. Mammal Review 54: 173-181. Rowe J, Gill RMA (1985) The susceptibility of tree species to bark-stripping damage by grey squirrels (Sciurus carolinensis) in England and Wales. Quarterly Journal of Forestry 79: 183-190. Ruf T, Fietz J, Schlund W, Bieber C (2006) High survival in poor years: life history tactics adapted to mast seeding in the edible dormouse. Ecology 87: 372-381. Sanderson HR (1975) Den-tree management for gray squirrels. Wildlife Society Bulletin 3: 124-31. 365


Sanderson HR, Healey WM, Pack JC, Gill JD, Ward Thomas J (1976) Gray squirrel habitat and nest tree preference. Proc. Ann. Conf. SE Assoc. Game & Fish Comm. 30: 609-16. Selonen V, Hanski IK (2010) Condition-dependent, phenotype-dependent and genetic-dependent factors in the natal dispersal of a solitary rodent. Journal of Animal Ecology 79: 1093-1100. Selonen V, Hanski IK, Stevens P (2001) Space use of Siberian flying squirrel Pteromys volans in fragmented forest landscapes. Ecography 24: 588-600. Selonen V, Hanski IK, Wistbacka R (2014) Communal nesting is explained by subsequent mating rather than kinship or thermoregulation in the Siberian flying squirrel. Behavioral Ecology and Sociobiology 68: 971-980. Selonen V, Painter JN, Rantala S, Hanski IK (2013) Mating system and reproductive success in Siberian flying squirrels. Journal of Mammalogy 94: 1266-1273. Selonen V, Varjonen R, Korpimäki E (2015) Immediate or lagged responses of red squirrel population to pulsed resources. Oecologia 177: 401-411. Sheehy E, Lawton C (2014) Population crash in an invasive species following the recovery of a native predator: the case of the American grey squirrel and the European pine marten in Ireland. Biodiversity and Conservation 23: 753-744. Shorten M (1951) Some aspects of the biology of the grey squirrel (Sciurus carolinensis) in Great Britain. Proceedings of the Zoological Society London 121: 427-51. Shorten M (1962) Grey squirrels. In Matthews LH (ed) Animals of Britain, 5:1-24. Sunday Times book publications, London. Shuttleworth CM (1995) Red squirrels (Sciurus vulgaris) on the Sefton Coast: The conservation value of nest boxes. In Hughes DG, Tew T (eds) 2nd NPI Red Alert UK Forum for Red Squirrel Conservation. The Federation of Zoological Gardens of Great Britain and Ireland. Shuttleworth CM (2001) Interactions between the red squirrel (Sciurus vulgaris), great tit (Parus Major) and jackdaw (Corvus monedula) whilst using nest boxes. Journal of Zoology London 255: 269-272. Shuttleworth CM, Kenward RE, Jackson N (2009) The reintroduction of the red squirrel Sciurus vulgaris to Newborough forest, north Wales: A five year project review. Report to Countryside Council for Wales, Wildlife Trust, Forestry Commission Wales & Grantscape. Shuttleworth CM, Schuchert P (2014) Are nest boxes a useful tool in regional red squirrel conservation programs? Hystrix, Italian Journal of Mammalogy 25: 91-94. Steele MA, Koprowski JL (2001) North American tree squirrels. Smithsonian Institution Press. USA. Stone KD, Heidt GA, Baltosser WH, Caster PT (1996) Factors affecting nest box use by southern flying squirrels (Glaucomys volans) and gray squirrels (Sciuruis carolinensis). American Midland Naturalist 135: 9-13. Taylor, JC (1969) Social structure and behaviour in a grey squirrel population. PhD thesis, University of London, London, UK. Telford JW (1986) Squirrel nest boxes. US Army Engineer Technical Report EL-86-11. US Army Engineer Waterways Experiment Station, Vicksburg. USA. Tittensor AM (1970) Red squirrel dreys. Notes from the Mammal Society no. 21. Journal of Zoology 162: 528-533. Uhlig HG (1956) A theory on leaf nests built by gray squirrels on Seneca State Forest, West Virginia. The Journal of Wildlife Management 20:263-266. Wauters LA, Dhondt AA (1986) The use of red squirrel Sciuris vulgaris dreys to estimate population density. Journal of Zoology, London 214: 179-187. Wauters LA, Dhondt AA (1988) The use of red squirrel (Sciurus vulgaris) dreys to estimate population density. Journal of Zoology, London 214: 179-187. 366


Wauters LA, Dhondt AA (1990) Nest-use by red squirrels (Sciurus vulgaris, Linnaeus 1758). Mammalia 54377-54389. Wauters LA, Gurnell J, Currado I, Mazzoglio PJ (1997) Grey squirrel management in Italy—squirrel distribution in a highly fragmented landscape. Wildlife Biology 3: 117-124. Williams E (2011) A comparison of eastern gray squirrel (Sciurus carolinensis) nesting behavior among habitats differing in anthropogenic disturbance. MSc thesis, Georgia Southern University, Statesboro. Willis S (2015) Grey squirrel control in the urban landscape. In Shuttleworth CM, Lurz PWW, Halliwell EC (eds) Shared experience of red squirrel conservation practice, 13-20. ESI, England. Zapponi L, Del Bianco M, Luiselli L, Catorci A, Bologna MA (2013) Assessing environmental requirements effects on forest fragmentation sensitivity in two arboreal rodents. Mammalian Biology - Zeitschrift für Säugetierkunde 78: 157-163.

367


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