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.

Keywords: endocrine plasticity; faecal cortisol metabolites; free-living animals; habituation; invasive alien species; stressor experience.

Figure 1.

Relationship between FGMs and days since invasion in red squirrels at different levels of grey squirrel density. The line represents the predicted relationship (calculated from the selected model excluding the interaction of sex with reproductive conditions) at low (dotted line, value equal to −1), medium (dashed line, value equal to 0) and high (solid line, value equal to 1) grey squirrel density. Shaded areas represent the 95% CIs, symbols show observed values (full circles).

Figure 2.

Relationship between FGMs and grey squirrel experience in red squirrels (n = 302; ID = 129). The bold face line represents the predicted relationship (calculated from the selected model excluding the interaction of sex with reproductive conditions). Shaded areas represent the 95% CIs, symbols show observed values (full circles).

Figure 3.

Concentrations of FGMs at increasing number of days of grey squirrel experience, data grouped by six-months periods. Before arrival of grey squirrels (grey squirrel experience = 0). Boxplots show median (solid horizontal line), mean (black diamonds) and 1st (25%) and 3rd (75%) quartiles.