Stress in biological invasions: Introduced invasive grey squirrels increase physiological stress in native Eurasian red squirrels

Abstract

Invasive alien species can cause extinction of native species through processes including predation, interspecific competition for resources or disease-mediated competition. Increases in stress hormones in vertebrates may be associated with these processes and contribute to the decline in survival or reproduction of the native species. Eurasian red squirrels (Sciurus vulgaris) have gone extinct across much of the British Isles and parts of Northern Italy following the introduction of North American invasive grey squirrels (Sciurus carolinensis). We extracted glucocorticoid metabolites from faecal samples to measure whether the presence of the invasive species causes an increase in physiological stress in individuals of the native species. We show that native red squirrels in seven sites where they co-occurred with invasive grey squirrels had glucocorticoid concentrations that were three times higher than those in five sites without the invasive species. Moreover, in a longitudinal study, stress hormones in native red squirrels increased after colonisation by grey squirrels. When we experimentally reduced the abundance of the invasive grey squirrels, the concentration of faecal glucocorticoid metabolites in co-occurring red squirrels decreased significantly between pre- and postremoval periods. Hence, we found that the invasive species acts as a stressor which significantly increases the concentrations of glucocorticoids in the native species. Given that sustained elevations in glucocorticoids could reduce body growth and reproductive rate, our results are consistent with previous studies where the co-occurrence of the invasive grey squirrel was associated with smaller size and lower reproductive output in red squirrels.

Interspecific competition affects the expression of personality-traits in natural populations

“…In woodlands occupied by both species, the interspecific overlap of the foraging-niche, daily activity pattern and home ranges (core-areas) are high 19,26 and more sociable red squirrels are likely to sustain such pressure, that increase with grey squirrel density, better than individuals with a tendency to avoid conspecifics. Also, higher sociability could be related with a lower susceptibility to physiological stress induced by the invader 35 . Conversely, dispersal as a conditional strategy 36 , could result in red squirrels with a strong avoidance personality being the first to emigrate from woodlands invaded by grey squirrels, as supported also by low local recruitment rates of juvenile red squirrels in areas of co-occurrence 20 .…”

Experimental removals reveal dietary niche partitioning facilitates coexistence between native and introduced species

“…In addition to this potential competition deficit for MGRS, daily interactions with Abert's squirrels may cause chronic stress leading to reduced individual fitness in the endangered native species. This possibility was recently demonstrated by a removal experiment where elevated glucocorticoid concentrations in Eurasian red squirrels dropped following removal of invasive eastern gray squirrels in Lombardy, Italy (Santicchia et al, ).…”

Reproductive Traits of an Invasive Alien Population of Grey Squirrel (Sciurus carolinensis) in Central Italy

“…The negative interaction between the two species has been attributed to competition for food resources and habitats, thus reducing breeding and recruitment [3,18], but it also due to the chronic stress induced by co-existing in the same habitat [19], and to interspecific competition leading to behavioural changes [20].…”