In 1876, four gray squirrels from North America were introduced to Henbury Park, Cheshire, England (Middleton, 1931; Shorten, 1954). This was the beginning of a series of introductions of gray squirrels to Britain, Ireland and Italy over the ensuing 150 years. The gray squirrel is native to the eastern and midwestern United States of America and to some southerly provinces in Canada. It is a resilient and adaptable species that has not only been introduced to Britain, Ireland and Italy, but also to other places around the world, such as Melbourne, Ballarat and Adelaide in Australia (now extinct, Peacock, 2009), and South Western Cape, South Africa (Gurnell, 1987), as well as western Canada (Larsen, 2016) and several places in the western United States (Tran et al., 2022). After the first introduction to Britain, there were at least 8 further introductions form North America and approximately 19 secondary introductions or translocations to different places within Britain (including several translocations to Scotland) and Ireland until 1929 (Middleton, 1931; Shorten, 1954). Many of the first recorded introductions to Britain, Ireland and later to Italy were made by landowners to embellish their large country estates. DNA profiling approaches in Britain, Ireland and Italy indicate that human help has been a critical factor in the successful spread of this species (Signorile et al., 2014b, 2016).

Often the numbers of gray squirrels introduced to a location were low, in single figures. Shorten (1954) noted that many small introductions throughout the country may have gone unrecorded and hypothesized that the escape of gray squirrels kept as pets might have played a relevant role in the spread of the species. As well as the wider countryside, gray squirrels readily moved into towns and cities and were frequently recorded, often in high numbers, in parks and common areas (Shorten, 1954; Merrick et al., 2016; Lawton et al., 2020). Despite an increasing number of attempts to control gray squirrels (Gurnell and Pepper, 2016), by the mid-1980s, gray squirrels were to be found throughout mainland central and southern England and Wales, and in the Central Lowlands in Scotland (Lloyd, 1983; Gurnell, 1987). Thereafter, their range continued to expand into northern England, southern and central Scotland and up the east coast of Scotland to Aberdeen (with a separate introduction to the city). This range expansion was not straightforward because of concerted efforts by various organizations and volunteers, especially in the north of England and Scotland, to control gray squirrels for red squirrel conservation (Seward and O'Hare, 2015; Shuttleworth et al., 2020). Thus, especially at the local scale, gaps occur within their range, sometimes temporary, as gray squirrels are removed (Gurnell et al., 2014).

Gray squirrels were first introduced to Ireland when six pairs were translocated from the Woburn Estate in England to Castle Forbes in County Longford in 1911 (Lawton et al., 2015). Subsequently there have been 19 distribution surveys of gray (and red) squirrels in Ireland between 1932 and 2019 (O'Teangana et al., 2000a; for full list see Lawton et al., 2020). By 2007 gray squirrels had colonized the eastern half of the island, although absences in previously occupied areas in the midlands were noted, and this has been attributed to the re-appearance of the pine marten, Martes martes (Sheehy and Lawton, 2014; Lawton et al., 2015). Twining et al. (2022a) analysis of survey data indicates that the range of the gray squirrel decreased by 41% between 2007 and 2019 with a commensurate increase of 51% in the range of the red squirrel and a 205% increase in range of the pine marten. Further, emphasizing the impact of pine martens on gray squirrels, gray squirrels had disappeared from 85% of the 100 km² grid squares occupied by both species in 2007 during the following 12 years (Twining et al., 2022a).

Gray squirrels were introduced from North America into Italy from 1948 onwards and the first introduction (1948) was of four individuals from Washington D.C. to Candiolo, close to the Stupinigi forests just south of Turin (Currado et al., 1987; Bertolino and Genovesi, 2003; Bertolino, 2008). A second introduction was to Genoa Nervi in 1966 and thereafter many illegal releases and translocations, some recorded and many not, occurred through to 2010 (Bertolino, 2008; Martinoli et al., 2010; Signorile et al., 2014a). In particular, the many populations registered in Lombardy by 2010 (see Table 1 and Figure 1 in Martinoli et al., 2010), all of unknown origin, have subsequently increased their abundance and distribution over the past 12 years, causing a strong reduction and/or extinction of local red squirrel populations, despite (limited) control attempts in some areas during the LIFE EC-SQUARE LIFE09/NAT/IT/000095 “rossoscoiattolo” project. In fact, gray squirrel control and/or red squirrel conservation measures in Italy have been sporadic and without any continuous effort, with additional pressure for “no action” by animal welfare groups exacerbating the situation (Lioy et al., 2019). Necessary, but by itself insufficient, legal restrictions, implemented first at national and subsequently at the EU-level (Bertolino et al., 2013), included a trade-ban and the prohibition to keeping gray squirrels in captivity. These measures were an important step to prevent further illegal releases but were unsuccessful in stopping illegal translocations (authors unpubl. data). Despite these serious issues, some local eradication actions of the invasive alien species (IAS) have succeeded (in Perugia, La Morgia et al., 2017 and in Genoa Nervi, Scapin et al., 2019). Further information on introductions to Piedmont, Lombardy, Umbria and Veneto are provided by Bertolino et al. (2015), but detailed records of introductions are often lacking or fragmentary.

Although little is known about the fate of many introductions, there is evidence that many were successful (Shorten, 1954; Signorile et al., 2016). The general pattern appears to be that, after a period of consolidation from a small founding population, gray squirrels start to spread from their places of introduction. A typical scenario can be seen from the first introduction of gray squirrels to the Stupinigi forests (Piedmont) in Italy in 1948. Gray squirrels only started to expand their range in the late 1970s, when animals dispersed mainly along river corridors and started to colonize the highly fragmented surrounding landscape (Wauters et al., 1997; Bertolino et al., 2014). The Piedmont metapopulation's expansion was monitored until 2015 (Bertolino et al., 2014): in this period gray squirrels increased their range from 900 km² in 1990 to more than 2000 km² in 2012.

Many introductions and translocations of gray squirrels over wide geographic areas in Britain, Ireland and Italy over many years have made it difficult to contain the spread of the invading species. There have been some hard-won successes, such as the removal of gray squirrels from the island of Anglesey (Wales), or ongoing control of gray squirrels in parts of the north of England, Scotland, Ireland and Italy (Gurnell et al., 2014; Seward and O'Hare, 2015; Bertolino et al., 2016). Landscape features may slow down spread, such as movement to the west of the River Shannon in Ireland (Lawton et al., 2020), although as discussed above, this may at least in part be predator related. At the same time, tree and river corridors have facilitated dispersal through farmland, moorland or fragmented habitats (Bertolino et al., 2014; Shuttleworth et al., 2016).

The invading gray squirrels are in competition with native red squirrels. As gray squirrels have spread, they have replaced red squirrels in most habitats in a process that appears inevitable without some form of human intervention, and with the possible exception of the return of the pine marten in Ireland and more recently parts of Scotland (see Section 5.4). In simple terms, red squirrels eventually disappear as the gray squirrels expand their range. The replacement may however not be immediate, and some habitats, such as commercial Sitka spruce (Picea sitchensis) dominated forests in Britain (also see Halliwell et al., 2016), may provide refuges for red squirrels, assuming proper management of tree species diversity and forest age structure to ensure a dependable food supply. In Italy, after the first introduction in Stupinigi (Piedmont), between 1970 and 2010 local red squirrel populations disappeared and went extinct in 62% of tetrads (ca. 1,689 km²) in the 2016 km² area colonized by gray squirrels (Bertolino et al., 2014).

This red squirrel-gray squirrel paradigm has received a considerable amount of attention in the last 50 years, and, based on a systematic review of the literature, we ask the question: “Is the ecological replacement of red by gray squirrels really inevitable?” We particularly look at the mechanisms of competition between the two species and to what extent they are mediated by pathogens as well as predators. In fact, we consider the evidence for interference, exploitation, and apparent competition. We also consider whether human intervention can reverse the outcome of competition.

A systematic literature search was undertaken in April 2022 following the PRISMA protocols (Page et al., 2021). We used Web of Science, Scopus and Google Scholar to conduct a literature search using the following terms: (“red squirrel^*” OR “Sciurus vulgaris”) AND (“gray squirrel^*” OR “gray squirrel^*” OR “Sciurus carolinensis”) AND (“interaction^*” OR “competition”). All results listed on Web of Science and Scopus were collected, while only the first 200 articles of Google Scholar were included, following the threshold of relevance used in other reviews (Lison et al., 2020; Fingland et al., 2022).

We only included articles written in English and published in peer-reviewed journals; we did not collect theses, book chapters, reports and conference proceedings. There were no restrictions regarding the year of publication. The screening was conducted using the following criteria:

We collected a total of 599 articles, of which 102 were retained after screening. We added 6 articles and 14 publications that did not appear in our search but which were present in our personal libraries and relevant for the objectives of the present systematic review. The PRISMA flowchart is provided as Figure 1, and the list of the publications included in the qualitative synthesis is presented in Supplementary material, with the extra 20 publications highlighted in bold.

Among competing mammal species, being larger and heavier has physiological benefits related to thermoregulation and body fat reserves that might affect the outcome of competition. Morphologically, gray squirrels are larger and heavier than red squirrels. Comparing the relationship between shin length (average 70.5 mm in red and 78.0 mm in gray squirrels) and body mass (average over different seasons: 277–303 g in red and 542–659 g in gray squirrels), gray squirrels are proportionally heavier for their body size than red squirrels (79–138% greater weight against the 35% difference expected; Kenward and Tonkin, 1986). In deciduous and mixed forests with a high availability of large tree seeds (acorns, beechnuts, chestnuts, and hazelnuts) this is associated with a greater capacity to accumulate subcutaneous body fat in autumn when high-energy food resources are abundant. In fact, where autumn weight increase in red squirrels is about 10%, gray squirrels can increase their body mass by 17–23% from the seasonal low in summer to peak mass in late autumn in deciduous habitats (Kenward and Tonkin, 1986; Wauters and Dhondt, 1989; Koprowski, 1994; Lurz et al., 2005). In contrast, in large man-made spruce-dominated conifer plantations in northern England, neither red nor gray squirrels increased their body mass in the autumn-winter period (Lurz and Lloyd, 2000). In coniferous forests fat accumulation is likely to be less pronounced than in mixed deciduous woods because autumn and winter food supplies are more predictable, and maneuverability to feed on cones in the canopy is important (Lurz and Lloyd, 2000; Wauters et al., 2007; Tranquillo et al., 2022). The different body shapes and interspecific differences in fat accumulation capacity are most likely genetically determined, since studies on size and weight variation in red squirrels over a variety of habitat types suggest local selection for smaller or larger size, based on quality and quantity of primary food resources (tree seeds) (Wauters et al., 2007; Cox et al., 2020; Tranquillo et al., 2022).

Gray squirrels have higher Daily Energy Expenditure (DEE) than red squirrels. However, the difference between the two species was not separable from the predicted effect of body mass on DEE (Bryce et al., 2001), and their DEEs were in accordance with allometric predictions based on body mass and ambient temperature. DEEs for gray squirrels varied with body mass, fluctuating between a low of 300 kJ day⁻¹ to a maximum of 1,150 kJ day⁻¹ with most values between 500 and 700 kJ day⁻¹. The autumn mean DEE for gray squirrels was about 200 kJ day⁻¹ higher than the winter mean (Bryce et al., 2001). Red squirrels showed less seasonal difference, with the highest DEE in spring and the lowest in autumn (spring 389.8 ± 122 kJ day⁻¹; autumn 314 ± 281 kJ Day⁻¹; Bryce et al., 2001). These authors argued that the higher energy requirements of gray squirrels, linked to higher consumption of limited high-quality food resources, could exert greater interspecific competition than the intraspecific competition red squirrels undergo in the natural situation (areas without grays), driving populations of the native species where they co-occur with the IAS to such low numbers that they are no longer viable. Hence, gray squirrels have a morphological advantage to cope with fluctuating deciduous seed-crops; this, together with their physiological (higher capacity to digest tannins; Kenward and Holm, 1993) and behavioral adaptations (female kin-groups, intensive caching, better spatial memory and problem-solving ability, Gurnell et al., 2001; Chow et al., 2018), contributed to the observed faster replacement of red by gray squirrels in broadleaf habitats (compared to conifer) in Northern Italy and the British Isles. Replacement of red by gray squirrels is therefore complex, highly context dependent and loss rates are influenced by habitat type (and thus also food availability), morphological as well as behavioral adaptations and disease (see also disease-mediated competition in Section 5.3 and community level impacts in Section 8).

The role of habitat type as environmental driver of the replacement process and the speed of replacement has long been recognized (e.g., Gurnell and Pepper, 1993; O'Teangana et al., 2000b; Di Febbraro et al., 2013). Red squirrels thrive in Scots pine dominated woodlands and in large, conifer forests with a high proportion of Norway spruce (Kenward et al., 1998; Wauters et al., 2004, 2008; Lurz et al., 2005; Santicchia et al., 2018); gray squirrels reach high densities in oak dominated woodlands and in suburban or even urban areas (Kenward and Holm, 1993; Gurnell, 1996; Kenward et al., 1998; Santicchia et al., 2018, 2019). It should be noted, that red squirrel populations also do well in broadleaf habitats in the absence of the invader (e.g., North Italy, Wauters et al., 2001b; Belgium, Wauters et al., 2004; Isle of Wight, Gurnell et al., 2015b) although they live at a similar range of densities as in conifer woodlands and at lower densities than gray squirrels in similar habitats (Kenward and Holm, 1993; Gurnell, 1996; Kenward et al., 1998). Similarly, large-scale surveys of presence/absence of the two species in the landscape tend to find associations of red squirrels with larger and conifer dominated forests and of gray squirrels with deciduous woods, parklands, and gardens (e.g., O'Teangana et al., 2000b in Northern Ireland). For red squirrel persistence, the degree of habitat fragmentation and the distance to the nearest gray squirrel population can be important factors (O'Teangana et al., 2000b).

These habitat effects raise the question to what extent there is niche partitioning in space- and habitat use. In an upland mixed-species conifer plantation in N. England, the habitat niche (tree species used) overlap between red and gray squirrels was high (75%). Red squirrels selected pure Sitka spruce stands and used mixed Sitka spruce-Scots pine; but they avoided the pure Scots pine stand, heavily used by gray squirrels, and potentially the “best” habitat for reds. Patterns of both intra-specific and inter-specific core-area overlap further confirmed that intraspecific (and intrasexual) competition among adult red squirrels was mainly determining red squirrel spacing behavior at this red-gray site, and that interspecific competition with the IAS had only a limited impact (Wauters et al., 2000). Hence, there was only limited space- or habitat-niche partitioning between the two species, suggesting a poor capacity for red squirrels to avoid interspecific resource competition at least at spatial and habitat levels in both conifer-dominated and broadleaf-dominated woodlands and forests (Wauters et al., 2000, 2002a).

A different example of at least partial niche partitioning was observed in Craigvinean Forest in Scotland where the two species co-existed for up to 30 years (Bryce et al., 2002), again suggesting the importance of landscape and habitat composition in determining the rate of replacement. Although the home ranges of red and gray squirrels overlapped, gray squirrels selected riparian corridors of mixed woodland with deciduous trees, while native reds favored foraging in Norway spruce trees within their home range (Bryce et al., 2002). Overall, niche-overlap was considerable (77%) and the authors did not find evidence for fine-scale (temporal) avoidance between the two species (Bryce et al., 2002). Their work suggests that determining the spatial scale at which some form of co-existence occurs can be informative.

To what extent did this high niche-overlap (ca. 75%) and lack of spatial segregation between red and gray squirrels in conifer plantations affect squirrel demography? Although the red-gray site had, overall, a higher tree-seed production, red squirrel densities (Minimum Number Alive) did not differ between red-only (0.17 to 0.30/ha) and red-gray sites (0.26 to 0.33/ha). But, even in these upland conifer forests dominated by Sitka spruce, gray squirrel density was about 4 times higher (0.92 to 1.1/ha) and they tended to have higher breeding rates than the native congener (44% of red squirrel females breeding in both spring and summer, against, respectively, 70 and 54% of gray squirrel females; Wauters et al., 2000; Gurnell et al., 2004). There were no differences in red squirrel adult survival or female breeding rate between the two populations, but juvenile recruitment in the red-gray site (13%) was much lower than in the red-only site (50%). Hence, in conifer plantations, adult red squirrels seemed to be little affected by the high number of grays residing in the study area, and the key demographic result of interspecific competition for food and space was the reduced juvenile and subadult recruitment (Wauters et al., 2000; Gurnell et al., 2004).

Comparing tree-species selection by the two species in mixed deciduous woods in N. Italy, the relative, seasonal use of tree species differed between red and gray squirrels. Gray squirrels positively selected and used oaks more frequently than native red squirrels (ca. 41% by reds, 63% by grays), while red squirrels foraged often in walnut trees (Juglans regia) in autumn. Because of greater specialization in feeding on oak buds, flowers, insects (spring-summer), and acorns (autumn) by the alien species, it had a narrower niche width than the native one: overall niche overlap between the two species was 0.73 in spring-summer and 0.69 in autumn-winter (Wauters et al., 2002a). Diets of both red and gray squirrels were highly variable, but whereas acorns are high-energy staple food for grays, red squirrels eat only one to a few acorns in a day and acorns are never preferred over other hard mast (Wauters et al., 2001a); this seems related to their low ability to tolerate and neutralize acorn polyphenols (high tannin contents in acorns, Kenward and Holm, 1993). In captive-held gray and red squirrels kept on an acorn diet, the former thrived while the latter had a comparative digestive efficiency of only 59% and several animals died during the experiment (Kenward and Holm, 1993).

Gray squirrels spend more time on the ground than reds, and, having evolved in North American deciduous woods with large-seeded trees (e.g., oaks, hickory, and black walnut), cache (and retrieve) larger amounts of acorns and other nuts (Kenward and Tonkin, 1986; Wauters et al., 2002a,b). However, in mixed broadleaf woodlands in their European range, each year in autumn, both species scatterhoard numerous hazelnuts (Corylus avellana), chestnuts (Castanea spp.), beechnuts (Fagus sylvatica), and acorns (Quercus spp.) in small caches in the ground, retrieving these high-energy food items between late autumn and the following spring (Koprowski, 1994; Wauters and Casale, 1996; Wauters et al., 2001a, 2002b). The recovery and consumption of these cached seeds enhances summer reproduction of female red squirrels (Wauters et al., 1995). Foraging more on the ground, gray squirrels could potentially pilfer and partially deplete seeds cached by red squirrels, since naïve individuals are known to find and retrieve seeds cached by other squirrels (in most cases of the same species), by visual observation or by olfactory cues (Leaver et al., 2007; Robin and Jacobs, 2022).

Red squirrels show marked seasonal variation in both the proportion of ground foraging (more frequent in autumn-winter and in spring) and in tree-species niche width: the latter is smallest in spring when in mixed deciduous woods they spend a lot of time in oaks feeding on flowers and caterpillars (Wauters et al., 2001a, 2002a). Both red and gray squirrels were frequently observed moving and feeding on the ground (reds 27 and 37% of observations in spring-summer and autumn-winter respectively; grays 29 and 43% respectively; Wauters et al., 2002a). Consequently niche-overlap for ground vs. tree use was extremely high (0.98 in spring-summer; 0.94 in autumn-winter), and the proportion of ground foraging by red squirrels varied greatly between habitats, in relationship to the availability of cacheable autumn tree-seeds (hazelnuts, chestnuts, beechnuts, and walnuts) (Wauters and Casale, 1996; Wauters et al., 2002a,b).

The relative occurrence of different personality traits in red squirrels, measured through arena tests by recording the behavior of the animals placed in a standardized box-shaped arena with a controlled environment (see Mazzamuto et al., 2019), was studied in sites with only red squirrels and sites with gray squirrels also present (Wauters et al., 2019). It was found that the presence of gray squirrels did not influence the proportion of time spent in behaviors related to the personality traits activity or shyness. However, sociability behaviors were expressed more in sites with the presence of gray squirrels (Wauters et al., 2019). These results could indicate a fitness advantage for more sociable red squirrels in the red-gray sites. However, none of the personality traits were correlated with the probability to survive to the next year, or with the probability for females to produce a litter (Wauters et al., 2019). That personality-fitness relationships were not affected by the presence or absence of gray squirrels suggests that the higher expression of sociability by red squirrels in the red-gray sites was not due to natural selection, but probably the result of context-related benefits when co-existing with gray squirrels. In general, more studies are needed to understand whether interspecific competition influences the selection of personality phenotypes which would allow native species to cope more efficiently with invasive alien species.

Few studies have looked at interspecific differences in memory or problem-solving abilities. In a preliminary study on few individuals, Macdonald (1997) showed that gray squirrels' spatial memory was accurate, allowing them to precisely relocate cache sites compared to less long-lasting memory of red squirrels. In a more recent study, Chow et al. (2018), compared the level of behavioral flexibility among invasive gray and native red squirrels using two food extraction tasks, an easy and a difficult one. Both species showed flexibility and the solution time for solving the easy task was comparable between the native and alien species (Chow et al., 2018). But a higher proportion of gray (93%) than red squirrels (50%) solved the problem at the first attempt. Likewise, more gray than red squirrels solved the more difficult task but, for the individuals that did solve it, efficiency was comparable between the two species. Overall, the authors suggested that the on average more successful problem-solving ability exhibited by gray squirrels could have facilitated invasion success and become a competitive advantage in replacing native red squirrels.

The Interference Competition Hypothesis (ICH) was long retained a likely mechanism behind the replacement of native red by alien gray squirrels. The ICH suggests three ways in which gray squirrels could directly interact with native red squirrels: direct aggressive interactions; interrupting red squirrel mating chases; or forcing native squirrels to actively avoid areas of the woodland intensively used by the invasive congener (Wauters and Gurnell, 1999). These authors explicitly tested six predictions of this hypothesis, using data on activity patterns, behavior and reproductive performance of red squirrels, and comparing them between a red-only and a red-gray site in Italy (Wauters and Gurnell, 1999).

Red squirrels only slightly increased time spent interacting with other squirrels (both species in the Experimental site) and interactions with gray squirrels were rarely observed. Moreover, where, in both sites, most within-sex (males with males or females with females) interactions between two red squirrels were aggressive, this was not the case for encounters between a red and a gray squirrel of the same sex. Hence, the prediction that gray squirrels replaced reds by direct aggressive interactions was rejected (Wauters and Gurnell, 1999). The same study also showed that gray squirrels did not interfere with red squirrel mating chases, or affected mating success.

Activity patterns (time spent active/hour) of both species were similar in all seasons (in the red-gray site) and red squirrels' activity rhythm did not differ between the two study sites. In the red-gray site in N. Italy, correlations of the proportion of time spent active in each 1-h period between red and gray squirrels were high in all seasons (all r > 0.73; see Figure 1 in Wauters et al., 2002a). Hence, red squirrels did not avoid the invasive congener by shifting their activity to times of day when gray squirrels were less active (Wauters and Gurnell, 1999; Wauters et al., 2002a). Finally, detailed analyses of red squirrel home-range and core-area size, intra- and interspecific core-area overlap and between-year shifts in core-areas of red squirrels in relation with the amount of overlap with gray squirrels, indicated that any observed shifts of red squirrel core-areas were not caused by a local increase in gray squirrel density. Furthermore, sex-specific core-area overlap among red squirrels did not differ from the same sex-specific combinations between red and gray squirrels (details in Table 5 in Wauters and Gurnell, 1999; see also Wauters et al., 2002a). In other words, red squirrels did not avoid gray squirrels more strongly than they avoided other red squirrels. The conclusion to these studies was that there was no home-range niche partitioning between the two squirrel species and no evidence to support the ICH. Thus, interference competition can be dismissed as a mechanism behind the replacement process.

Exploitation competition is a form of direct competition between species for (limited) resources, such as food or nest sites. Red and gray squirrels eat similar foods, but do gray squirrels exploit certain shared foods more efficiently, reducing their availability to red squirrels? Red squirrels spent more time foraging in red-only than in red-gray sites in N. Italy in spring and in winter, but the absolute differences were small (less than 20 min day⁻¹; Wauters et al., 2001a). In both sites, native squirrels selected smaller, early maturing seeds in late spring and summer, and larger later maturing nuts in autumn. Overall, there was no clear evidence that interspecific competition for important food resources in the presence of gray squirrels caused large changes in red squirrel food choice. However, estimating average daily rates of energy intake (DEI) by red squirrels in three periods (autumn, early winter, and late winter), DEI was higher in the red-only than in the red-gray site in early winter (December), but not in the other seasons (Wauters et al., 2001a). Hence, food competition with gray squirrels seemed to have a limited impact on the energy-intake of adult red squirrels.

Regardless of this, observations on caching and retrieval behavior of radio-tagged squirrels of both species revealed some interesting findings. For example, gray squirrels mainly cached acorns, walnuts and black walnuts, but they also retrieved hazelnuts and walnuts that were cached by red squirrels (Wauters et al., 2002b). Also, and although the total seed-energy cached by red squirrels did not differ between the red-only and red-gray sites the average ratio of seed-energy recovered to seed-energy cached by red squirrels was estimated at 99.8% at the red-only site, but only 66% at the red-gray site (Table 2 in Wauters et al., 2002b). At the individual level, daily energy-intake from consumption of cached seeds was not related to interspecific core-area overlap in winter; however, in the following spring, when caches were gradually depleted, red squirrels with high interspecific core-area overlap had lower daily energy-intake than low-overlap squirrels (Figure 1b in Wauters et al., 2002b). In addition, spring body mass of red squirrels was negatively correlated with % core-area overlap with the congener. In summary, the pilfering of red squirrels' food caches by the IAS seems to result in a reduced energy-intake and loss of body mass, mainly in spring, of those animals that were strongly overlapped by gray squirrels (Wauters et al., 2002b). Whether the opposite also occurs (red squirrels pilfering gray squirrels' seed caches) still needs to be investigated.

How do these differences in food choice and energy-intake affect phenotype? Comparing right hind foot length (index of body size) and body mass of red squirrels between the red-only and the red-gray sites, both in coniferous and deciduous habitats, individuals of the native species were larger and weighed more in the absence than in the presence of the IAS (Wauters et al., 2000, 2001a). However, differences in body mass between the sites were mainly explained by the variation in foot length; hence adult red squirrels weighed less when co-occurring with gray squirrels because they were smaller than in the control areas without the alien congener (Wauters et al., 2000, 2001a).

Parasite-mediated (or disease-mediated) competition is an asymmetric form of apparent (indirect) competition (Holt and Bonsall, 2017) that may arise between two host species when they share a common parasite (sensu Anderson and May, 1979) that has a differential impact on them (Hudson and Greenman, 1998). Biological invasions may represent an optimal scenario for such parasite-mediated interactions to occur, as alien and native species will have likely co-evolved with different enemies and will thus have a different susceptibility and tolerance to shared pathogens, either native or introduced (Dunn et al., 2012; Lymbery et al., 2014). It is likely that an alien parasite introduced by the invading host will be more virulent to naïve native species that lack any previous exposure to it. In this case, if spillover occurs, the parasite will facilitate the invader, leading to a so-called disease-mediated invasion (Strauss et al., 2012).

Predator-mediated apparent competition occurs when a shared predator influences the outcome of competition between two prey species.

In 2014, Sheehy and Lawton (2014) investigated the regional reduction in gray squirrel presence in the Irish midlands, where the distribution of the alien species had crashed over an estimated area of 9,000 km² and red squirrels were returning after an absence of 30 years. At the same time, pine marten recolonized much of the area and there was a positive correlation between pine marten and red squirrel occurrence, whereas the correlation between pine martens and gray squirrels was negative. This dramatic impact of a native predator on red-gray squirrel interactions was also confirmed in a follow-on study in Scotland where Sheehy et al. (2018) similarly demonstrated a highly asymmetrical impact of recovering pine marten populations on red and gray squirrels with gray squirrel distribution being strongly negatively affected. A synthesis of available data by Twining et al. (2022a) argues that: “evolutionary naivety of invasive species to native predators and lack of local refuges results in higher predation of naive compared to coevolved prey”. The authors also suggest that a depauperate vertebrate predator population has increased ecosystem vulnerability to non-native species invasion. They raise concern about gray squirrels persisting in urban and suburban areas, where pine marten cannot establish, that may act as source populations for continuous immigration into more natural habitats (Twining et al., 2021).

In short, studies over the past decade on the role of pine marten in the outcome of interspecific and disease mediated competition between red and gray squirrels indicate that the recovery of pine marten populations in Britain and Ireland can hinder replacement of red by gray squirrels or locally even reverse the process through the reduction or exclusion of the invasive species (Table 1). This will depend, however, on different ecological variables such as forest and woodland suitability for pine marten establishment and for supporting red squirrel populations, landscape structure enhancing pine marten dispersal and colonization of new areas, and the degree of urbanization of a region (Slade et al., 2022a,b; Twining et al., 2022a). So far, urbanized areas are not colonized by pine marten, while gray squirrels thrive in urban and suburban woodlands, parks and gardens. Therefore, these areas are likely to act as sources in a potential source-sink dynamics from where gray squirrels will continuously disperse toward rural habitats (Table 1). Multi-species population dynamics modeling (Slade et al., 2022b) suggests that fluctuations in the abundance of other prey species (in particular voles) can create predator-prey dynamics that are temporarily more favorable for gray squirrels (switch to abundant high density vole prey with concomitant low marten pressure on gray squirrels and thus increased competition with red squirrels and higher disease transmission, Table 1). Whether such temporal changes in abundance of alternative prey can influence the red-gray squirrel system needs further empirical evidence.

Gray squirrels can be considered as an environmental stressor when they invade red squirrel areas. Boonstra (2013) defined an environmental stressor as an unpredictable and/or noxious environmental stimulus that threatens (or is perceived to threaten) survival and/or homeostasis. Vertebrates cope with those stimuli using a suite of behavioral and physiological responses that allow them to maintain or return to homeostasis and reduce fitness loss. Short-term elevation (acute stress) of glucocorticoids (GCs), namely, cortisol and cortisone via activation of the hypothalamic–pituitary–adrenal (HPA) axis, help individuals to cope with life-threatening events (Romero, 2004; Breuner et al., 2013), while a long-term production of GCs (chronic stress), due to a prolonged or repeated exposure to stressor, might result in negative effects on survival and reproduction (Romero, 2004; Bonier et al., 2009; Cyr and Romero, 2009). In free-living animals, fecal glucocorticoid metabolites concentrations (FGMs) have been used as an estimate of long-term physiological stress (Boonstra, 2013; Palme, 2019). This measure has been validated for the Eurasian red squirrel (Dantzer et al., 2016).

By comparing FGMs between red squirrels from red-only (control) sites and animals from red-gray sites (red squirrel sites colonized by gray squirrels), Santicchia et al. (2018) found that FGMs (260 samples from 166 individuals) were on average three times higher in the latter (red-gray n = 135, mean ± SD = 78,133 ± 61,074 ng g⁻¹ dry feces; red-only n = 125, 24,890 ± 20,566 ng g⁻¹ dry feces), and this increase in FGMs was similar for both sexes. Moreover, comparing FGMs in animals from the same populations before and after stressor initiation, in other words, before and after the first gray squirrels colonized these sites, FGMs in the native red squirrels increased with respect to pre-colonization concentrations (see Figure 2 in Santicchia et al., 2018). This difference over time was conversely not found in control areas where no colonization by the alien species occurred (Figure 2 in Santicchia et al., 2018). These findings suggested that the presence of gray squirrels contributed to the increase in FGMs in the red squirrels, thus acting as an environmental stressor. These results were further supported by the removal of gray squirrels which resulted in a significant decrease in FGMs in co-occurring red squirrels over a 2-months interval (for details see Table 1 in Santicchia et al., 2018).

Habituation in the red squirrel stress response to the presence of gray squirrels has been observed over a longer time period (Santicchia et al., 2022a). FGMs of red squirrels increased following the early stages of invasion by gray squirrels, but then gradually decreased over time in a curvilinear way. FGMs in individual red squirrels decreased more markedly as they experienced a prolonged contact with invasive gray squirrels, whereas for those with little experience with the invasive species there was no or very little reduction in FGMs. On average, it took red squirrels about a year to habituate physiologically to the presence of gray squirrels (Santicchia et al., 2022a). These studies highlighted that the increase in physiological stress in red squirrels, caused by the presence of the invasive gray squirrel, should be considered as one of the factors that can affect the outcome of interspecific competition between these species, worsening the impact of exploitation competition on body mass/growth and possibly making red squirrels more susceptible to infections.

The physiological responses discussed above may covary with behavioral responses and this association is called a coping-style (Koolhaas et al., 1999). Individuals can be considered proactive with low GCs and a bold, more active-explorative, more aggressive personality; or reactive with high GCs and a more shy, less explorative and less aggressive personality. In theory, when a population of a native species comes in contact with an invasive species the associations between physiological and behavioral responses (i.e., coping-style) as well as among personality traits (i.e., behavioral syndrome, sensu Sih et al., 2004), might be disrupted in response to the pressure imposed by the presence of the competing invasive species (Sih et al., 2012). A recent study on red squirrels found that variation in FGMs was not correlated with any of the personality traits considered (activity, exploration, and a measure of sociability derived from arena tests); this was similar in study sites with only red squirrels and in sites where also gray squirrel occurred (see Figure 2 in Santicchia et al., 2022b). Conversely, they found a strong correlation among the personality traits in the study sites with only red squirrels, but no such correlation was found where red squirrels had to compete with the invasive congener (see Figure 2 in Santicchia et al., 2022b), suggesting a disruption of the behavioral syndrome caused by, or as a consequence of, the presence of the invasive competitor.

Population dynamics of red squirrels in natural situations (no IAS present) are mainly determined by the abundance of tree seed-crops in different types of forest habitat (Kenward and Holm, 1993; Kenward et al., 1998; Wauters et al., 2004, 2008). In these studies, carried out in areas without pine martens, most population processes are bottom-up, with important seed-crops (hazelnuts in British oak-hazel woods; chestnuts or beechnuts; Scots and/or Corsican pine cone -crops; Norway spruce; and Arolla pine seed-crops) significantly affecting reproductive success, recruitment rates, and in some populations adult survival rates and/or immigration rates. However, as squirrel abundance increases, density-dependent dispersal and/or recruitment tend to reduce population growth rate (with negative per-capita growth rate at high density; Wauters et al., 2004), reducing density fluctuations and regulating the abundance around an equilibrium density for a particular habitat. The role predation might play in single species (red or gray squirrels) or mixed species dynamics, and how it interacts with bottom-up processes, requires further study. There is evidence from human-modified landscapes in Northern Ireland that habitat may influence the interactions between pine martens and red squirrels in the absence of gray squirrels (Twining et al., 2022b). Red squirrels were negatively affected by the presence of pine martens in large, structurally simple conifer plantations but not so in broadleaf woodlands. In contrast, pine martens suppressed gray squirrels regardless of habitat (see Section 5.4). Evidence for the influence of predators on red and/or gray squirrels in Italy is lacking, and the studies on exploitation or parasite-mediated competition were carried out in areas without pine martens.

Comparisons of red squirrel population processes (reproductive rate, recruitment, and adult survival) between red-only and red-gray study sites in both deciduous (in north Italy) and coniferous habitats (in north England), showed that adult survival in the native species was not reduced when gray squirrels were present (Gurnell et al., 2004). Breeding rate (% females producing a litter) of female red squirrels in spring was also similar between both sites, but there was much lower summer breeding in the red-gray (ca. 20%) than in the red-only sites (ca 50%). This resulted in no, or very few, females raising two litters/year when gray squirrels were present. Reduced summer breeding could be related to the lower body mass of females, particularly in late spring-early summer when they need to enter oestrus, possibly caused by gray squirrels pilfering food caches of sympatric red squirrels (Wauters et al., 2001a, 2002b; Gurnell et al., 2004). Moreover, recruitment of red squirrels (all age-classes but mainly juveniles) was strongly reduced in the presence of gray squirrels compared to red-only sites (Italy: 12% against 26%; England: 13% against 50%), and recruitment decreased with increasing gray squirrel density. This is probably the most important demographic process behind the replacement of red by gray squirrels, with recruitment no longer compensating for emigration and mortality. Further studies are needed on why juvenile red squirrels do not settle near their birthplace when gray squirrels are present, and whether it is related to competition for space and higher mortality, lower foraging efficiency, slower growth rates and/or increases in stress in young red squirrels.

Within this basal scenario, the other described mechanisms may or may not operate to accelerate (disease-mediated competition) or hinder/reverse (predator-mediated competition) the replacement of the native species by the invader (Figure 2).