Native species exhibit physiological habituation to invaders: a reason for hope

Abstract

Animals cope with environmental perturbations through the stress response, a set of behavioural and physiological responses aimed to maintain and/or return to homeostasis and enhance fitness. Vertebrate neuroendocrine axis activation in response to environmental stressors can result in the secretion of glucocorticoids (GCs), whose acute increases may be adaptive, while chronic elevation may be detrimental. Invasive grey squirrels ( Sciurus carolinensis ) act as a stressor eliciting elevation of GCs in native red squirrels ( Sciurus vulgaris ). Here we used 6-year data of variation in faecal glucocorticoid metabolite (FGM) concentrations following invasion by grey squirrels in three red squirrel populations, to identify if red squirrels showed physiological habituation to this stressor. The decrease in FGMs over time was more pronounced shortly after invasion and at high densities of grey squirrels while it decreased less strongly and was no longer influenced by the invader density as time since invasion elapsed. At the individual level, FGMs also decreased more markedly as each red squirrel experienced prolonged contact with the invader. Our study provides compelling new data suggesting that native species in the wild can habituate to prolonged contact with invasive species, showing that they may avoid the potentially harmful effects of chronic elevations in GCs.

Social phenotype-dependent selection of social environment in wild great and blue tits: an experimental study

“…A previous study in the Wytham population showed that fast-exploring individuals had a greater number of weak social associations than slow explorers [63]. However, estimated correlations between sociability and exploration have ranged from negative to positive in an array of animal systems [64][65][66][67]. Thus, further work is needed to better understand the tendency for sociability and exploration to be linked within and across species, and therefore the potential for such a behavioural syndrome to drive results such as ours.…”

Interactions between native and invasive species: A systematic review of the red squirrel-gray squirrel paradigm

“…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.…”

“…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.…”

The impact of urbanisation on chipmunks, arboreal and flying squirrels: a global systematic review

“…2017; habituation: Santicchia et al. 2022b), which ultimately could enhance fitness. However, none of the studies reported here is informative about the adaptation of individuals, since they did not explore whether changes in the physiological stress response affected fitness parameters of individual squirrels with respect to urbanisation and/or human disturbance.…”