Island tameness: An altered cardiovascular stress response in Galápagos marine iguanas

Abstract

Island tameness is a widely documented phenomenon in which island species, particularly those that have evolved with no or few natural predators, show a greatly reduced behavioral response when faced with unfamiliar predators. This insufficient anti-predator response has led to widespread population declines among many island species exposed to novel predators, and has become a serious conservation problem. Despite its prevalence, the underlying physiology of island tameness is not known. Here we report that although Galápagos marine iguanas (Amblyrhynchus cristatus) initiated flight from an evolutionarily recent and unfamiliar potential predator (humans), they failed to show the cardiovascular stress response that facilitates successful escape, even after a prior capture experience. In contrast, when approached by a native predator (the Galápagos hawk; Buteo galapagoensis), marine iguanas show markedly increased heart rate independent of initiating escape movement. The secretion of catecholamines appears to be central to the initiation of escape behavior: naïve animals remotely injected with epinephrine immediately increased flight initiation distance, whereas those injected with corticosterone did not. Our results provide the first evidence that muted escape behavior in predator-naïve species is indicative of both a cognitive deficit in recognizing potential predators and a catecholamine deficit in response. Understanding how the response to predators differs in predator-naïve species could enable the design of maximally effective techniques for inducing an anti-predator response in these vulnerable species.

Introduction

Many native species face difficulties in adapting to novel predators [1], [2], [3]. Particularly at risk are those that have spent much of their evolutionary history isolated from all or most major suites of predators [4], [5]. These species often lack generalized anti-predator behavior, a phenomenon known as ‘island tameness’. Although decreased wariness can be adaptive in an environment in which novel threats are exceedingly rare, the inability to recognize and respond appropriately to introduced predators has resulted in severe population declines in a variety of species [6], [7], [8].

Attempts to train island species to respond appropriately to introduced predators have met with limited and variable success. Several studies have shown that classical conditioning (pairing a model of an unfamiliar predator with an unpleasant stimulus) can induce an escape response during subsequent presentations of the model [9], [10], [11], [12]. At least in some species, however, this acquired escape behavior is insufficient to avoid predation. The flight distance of Galápagos marine iguanas (Amblyrhynchus cristatus) increases after exposure to unfamiliar predators, but remains an order of magnitude too low to enable successful escape [13], [14].

Although the absence of a generalized anti-predator response in evolutionarily naïve species is a well-documented phenomenon, it is not known whether or how the physiological stress response differs in these species. The normal physiological stress response is highly conserved across taxa and consists of coordinated cardiovascular and endocrine elements that are considered vital for surviving challenges [15], [16], [17]. A fundamental component of this response is the rapid secretion of catecholamines that trigger an elevation in heart rate and stroke volume in preparation for extreme physical exertion.

We studied the relationship between anti-predator behavior and the initiation of a cardiovascular stress response in the classically tame Galápagos marine iguana. Adult iguanas face no native terrestrial predators, and only a single aerial predator: the Galápagos hawk (Buteo galapagoensis). Relatively recent introductions of novel terrestrial predators (feral dogs and cats) have resulted in the widespread decline of marine iguana populations on inhabited islands. Although marine iguanas attempt to evade novel predators, this behavioral response is largely unsuccessful: affected populations can suffer 27% annual mortality from feral dogs [18], and recruitment on some islands with introduced predators approaches zero [19].