Physiology of invasion: cane toads are constrained by thermal effects on physiological mechanisms that support locomotor performance

Abstract

Understanding the mechanisms that constrain the invasiveness of introduced animals is essential for managing invasions and for predicting their limits. In most vertebrate species, the capacity for invasion relies upon the physiological systems that support locomotion, and oxygen transport and metabolism may become limiting as environmental temperatures increase as predicted by the oxygen limitation hypothesis. Here we test the oxygen limitation hypothesis and propose the alternative hypothesis that within-individual plasticity will compensate for thermal variation. We show that during exercise in the invasive cane toad (Rhinella marina) oxygen transport by the cardiovascular system was maximised in warm-acclimated toads at high (30°C) temperatures, and that oxygen content of arterial blood was not affected by temperature. Resting oxygen consumption remained stable across a 10°C temperature range (20-30°C) when toads were allowed to acclimate, so that there was no increase in resting oxygen demand that could lead to a decrease in aerobic scope at high temperatures. Additionally, temperature acclimation had no effect on arterial-venous differences in oxygen partial pressures. Toads relied more on glycolytic ATP production at low temperatures to support locomotor activity. Mitochondrial capacities (citrate synthase and cytochrome c oxidase activities) were greatest at warmer temperatures. Interestingly, the metabolic cost of exercise increased at low temperatures. In contradiction to predictions by the oxygen limitation hypothesis, aerobic performance was not limited by high temperatures. On the contrary, the relatively slow advance of cane toads to cooler climates can be explained by the constraints of low temperatures on the physiological systems supporting locomotion. It is likely that human-induced global warming will facilitate invasions of environments that are currently too cool to support cane toads.