Island tameness: An altered cardiovascular stress response in Galápagos marine iguanas
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].
Section snippets
Experiment 1
We studied the cardiovascular stress response of 11 adult male marine iguanas on the island of Santa Fe, Galápagos (90°2′W, 0°50′S), in July of 2003. Santa Fe is not inhabited by humans or introduced predators, and visual encounters with humans prior to the start of the study are likely to have been rare: iguanas are highly site faithful [20] and the present study site is inaccessible to tourists and separate from our long-term study colony. Study males were implanted with miniaturized data
Experiment 1
When approached by a Galápagos hawk, marine iguanas immediately elevated heart rate over baseline levels (Fig. 1; paired samples t-test, t = − 3.56, df = 8, p = 0.007, d = 1.39). This response was independent of the initiation of escape behavior, and is indicative of epinephrine release upon visual contact with a known predator. During approaches by an unfamiliar predator with which they had a prior stressful experience (capture and handling) marine iguanas failed to display an elevation in heart rate
Discussion
Our findings indicate that the physiological stress response of marine iguanas differs when faced with a known vs. an evolutionarily recent and unfamiliar potential predator (hereafter referred to as an unfamiliar predator). The typical vertebrate stress response includes the secretion of catecholamines (epinephrine and norepinephrine), that increase heart rate and prepare the musculoskeletal system for increased energetic demands, and the activation of the hypothalamic-pituitary-adrenal (HPA)
Acknowledgements
We would like to thank J. Adelman, D. Blumstein, M. Hau, M. Niemack, R. Safran, K. Vitousek, D. Wilcove, and two anonymous reviewers for helpful comments on previous versions of the manuscript, A. Woakes for providing the data loggers, and G. Florant for help in the field. This work was supported by the National Science Foundation (DEB 0545744 and DEB 0545592), and Princeton University. The Charles Darwin Research Station and the Galápagos National Park Service provided permission and
References (32)
- et al.
Teaching an endangered mammal to recognize predators
Biol Conserv
(1996) - et al.
Learning specificity in acquired predator recognition
Anim Behav
(2001) - et al.
Effects of predator training on behavior and post-release survival of captive prairie dogs (Cynomys ludovicianus)
Biol Conserv
(2006) - et al.
Behavioral and physiological adjustments to new predators in an endemic island species, the Galápagos marine iguana
Horm Behav
(2007) Physiological stress in ecology: lessons from biomedical research
Trends Ecol Evol
(2004)- et al.
Heart rate and behavior are regulated independently of corticosterone following diverse acute stressors
Gen Comp Endocrinol
(2003) - et al.
The role of introduced species in shaping the distribution and abundance of island reptiles
Evol Ecol
(1991) - et al.
The role of introduced species in the degradation of island ecosystems: a case history of Guam
Annu Rev Ecol Syst
(1998) - et al.
Alien predators are more dangerous than native predators to prey populations
Proc R Soc Lond B
(2007) The causes and consequences of geographic variation in antipredator behavior: perspectives from fish populations
The loss of anti-predator behaviour following isolation on islands
Proc R Soc Lond B
Mammal extinctions on Australian islands: causes and conservation implications
J Biogeogr
Avian extinctions and mammalian introductions on Oceanic islands
Science
Invasive species are a leading cause of animal extinctions
Trends Ecol Evol
Training captive-bred or translocated animals to avoid predators
Cons Biol
Tameness and stress physiology in a predator-naïve island species confronted with novel predation threat
Proc R Soc Lond B
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