Invader danger: Lizards faced with novel predators exhibit an altered behavioral response to stress

Department of Biology, Pennsylvania State University, PA 16802, USA.
Hormones and Behavior (Impact Factor: 4.63). 04/2011; 60(2):152-8. DOI: 10.1016/j.yhbeh.2011.04.001
Source: PubMed


Animals respond to stressors by producing glucocorticoid stress hormones, such as corticosterone (CORT). CORT acts too slowly to trigger immediate behavioral responses to a threat, but can change longer-term behavior, facilitating an individual's survival to subsequent threats. To be adaptive, the nature of an animal's behavior following elevated CORT levels should be matched to the predominant threats that they face. Seeking refuge following a stressful encounter could be beneficial if the predominant predator is a visual hunter, but may prove detrimental when the predominant predator is able to enter these refuge sites. As a result, an individual's behavior when their CORT levels are high may differ among populations of a single species. Invasive species impose novel pressures on native populations, which may select for a shift in their behavior when CORT levels are high. We tested whether the presence of predatory invasive fire ants (Solenopsis invicta) at a site affects the behavioral response of native eastern fence lizards (Sceloporus undulatus) to elevated CORT levels. Lizards from an uninvaded site were more likely to hide when their CORT levels were experimentally elevated; a response that likely provides a survival advantage for lizards faced with native predatory threats (e.g. birds and snakes). Lizards from a fire ant invaded site showed the opposite response; spending more time moving and up on the basking log when their CORT levels were elevated. Use of the basking log likely reflects a refuge-seeking behavior, rather than thermoregulatory activity, as selected body temperatures were not affected by CORT. Fleeing off the ground may prove more effective than hiding for lizards that regularly encounter small, terrestrially-foraging fire ant predators. This study suggests that invasive species may alter the relationship between the physiological and behavioral stress response of native species.

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    • "We applied 6lL of the appropriate dose to provide 6 lg (''low'' dose) or 18 lg (''high,'' but physiologically relevant, dose) of CORT (= $0.66 lg or 2 lg CORT/g lizard respectively; Fig. 1). Topical oil and oil-CORT solutions were applied using a repeat pipette, resulting in elevated CORT levels 30 min after application (Trompeter and Langkilde, 2011). Patches were constructed from the padded section of an adhesive bandage, which held the oil or oil-CORT solution, and electrical tape and transparent surgical adhesive, which secure the patch to the back of a lizard (Knapp and Moore, 1997). "
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    ABSTRACT: Stress is typically characterized as "acute" (lasting from minutes to hours) or "chronic" (lasting from days to months). These terms are of limited use as they are inconsistently used and only encompass one aspect of the stressor (duration). Short and long duration stress are generally thought to produce specific outcomes (e.g. acute stress enhances while chronic stress suppresses immune function). We propose that aspects of stress other than duration, such as frequency and intensity, are important in determining its outcome. We experimentally manipulated duration, frequency, and intensity of application of exogenous corticosterone, CORT, in Sceloporus undulatus (Eastern fence lizards) and measured the immune outcomes. Our findings reveal that immune outcomes of stress are not easily predicted from the average amount or duration of CORT elevation, but that intensity plays an important role. Although three of our treatments received the same average amount of CORT, they produced different effects on immune outcomes (hemagglutination). As predicted by the literature, short-duration exposure to low-dose CORT enhanced hemagglutination; however, short-duration exposure to high-dose CORT suppressed hemagglutination, suggesting that stressor intensity affects immune outcomes of stress. While both are traditionally termed "acute' based on duration, these treatments produced different immune outcomes. Long-duration ("chronic") exposure to CORT did not produce the expected suppression of hemagglutination. Frequency of CORT application did not alter immune outcomes at low intensities. These results highlight the need to quantify more than just the duration of a stressor if we are to understand and manage the ecological consequences of stress. Specifically, we should consider stressor frequency and intensity, as well as duration, for a more complete characterization and understanding of stress. Copyright © 2015 Elsevier Inc. All rights reserved.
    Full-text · Article · Jul 2015 · General and Comparative Endocrinology
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    • "Behavioural interference occurs when an invasive species elicits a change in the behaviour of a native species. This change can result from direct interactions with the invader, such as avoidance of agonistic behaviours or predation (Usio et al. 2001; Trompeter and Langkilde 2011), or be induced simply by the invader's presence or associated cues (D'Amore et al. 2009; Polo-Cavia et al. 2009). Specifically, invaders might disrupt intraspecific communication systems in native species, including acoustic communication systems that function to attract mates and deter rival competitors (Duellman and Trueb 1986; Johnson and Searcy 1996; Rebar et al. 2009). "
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    ABSTRACT: Invasive species can disrupt the communication systems that native biota use for reproductive interactions. In tropical Australia, invasive cane toads (Rhinella marina) breed in many of the same waterbodies that are used by native frogs, and males of both the invader and the native taxa rely on vocal signals to attract mates. We conducted playback experiments to test the hypothesis that calls of toads may influence the calling behaviour of frogs (Limnodynastes convexiusculus and Litoria rothii). Male L. convexiusculus adjusted their calling rate and the variance in inter-call interval in response to a variety of sounds, including the calls of cane toads as well as those of other native frog species, and other anthropogenic noise, whereas L. rothii did not. Within the stimulus periods of playbacks, male L. convexiusculus called more intensely during long silent gaps than during calling blocks. Thus, males of one frog species reduced their calling rate, possibly to minimise energy expenditure during periods of acoustic interference generated by cane toads. In spite of such modifications, the number of overlapping calls (within stimulus periods) did not differ significantly from that expected by chance. In natural conditions, the calls of cane toads are continuous rather than episodic, leaving fewer gaps of silence that male frogs could exploit. Future work could usefully quantify the magnitude of temporal (e.g. diel and seasonal) and spatial overlap between calling by toads and by frogs and the impact of call-structure shifts on the ability of male frogs to attract receptive females.
    Full-text · Article · Feb 2015 · Behavioral Ecology and Sociobiology
    • "Significant variation in baseline and stress concentrations of corticosterone can arise due to interactions between internal and external influences, including environmental conditions (i.e. free-ranging or rehabilitation setting), geographical location, seasonal patterns, nutritional, disease and reproductive status (Ott et al., 2000; Jessop et al., 2004a, b; Jessop and Hamann, 2004; Kahn et al., 2007; Zachariah et al., 2009; Cote et al., 2010; Hare and Cree, 2010; Klukowski, 2011; Trompeter and Langkilde, 2011; French et al., 2012; Hunt et al., 2012). It is possible that corticosterone responses due to handling stress may vary among the same species at different locations; therefore , the results of this study may be specific to the Jekyll Island population of loggerhead sea turtles. "
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    ABSTRACT: The evaluation of hormonal responses to stress in reptiles relies on acquisition of baseline corticosterone concentrations; however, the stress associated with the restraint needed to collect the blood samples can affect the results. The purpose of this study was to determine a time limit for the collection of blood samples to evaluate baseline corticosterone, haematological and biochemical results in nesting (n = 11) and rehabilitating (n = 16) loggerhead sea turtles (Caretta caretta). Blood samples were collected from the dorsal cervical sinus of each turtle immediately after touching the animal (t0; 0-3 min) and 3 (t3; 3-6 min), 6 (t6; 6-9 min; nesting turtles only), 10 (t10; 10-13 min) and 30 min (t30; rehabilitating turtles only) after the initial hands-on time. Consistent between the rehabilitating and nesting turtles, there was a subtle yet significant increase in white blood cell counts over time. Despite the fact that white blood cell counts increased during the sampling period, there was no direct correlation between white blood cell count and corticosterone in the sampled turtles. In the nesting turtles, significant elevations in corticosterone were noted between t0 and t3 (P = 0.014) and between t0 and t6 (P = 0.022). Values at t10 were not significantly different from those at t0 (P = 0.102); however, there was a trend for the corticosterone values to continue to increase. These results suggest that sampling of nesting loggerhead sea turtles within 3 min of handling will provide baseline corticosterone concentrations in their natural environment. Significant elevations in corticosterone were also noted in the rehabilitating loggerhead sea turtles between t0 and t10 (P = 0.02) and between t0 and t30 of sampling (P = 0.0001). These results suggest that sampling of loggerhead sea turtles within 6 min of handling should provide baseline corticosterone concentrations in a rehabilitation setting. The delay in the corticosterone response noted in the rehabilitating turtles may be associated with the daily contact (visual or direct) they have with their human caretakers.
    No preview · Article · Jan 2015 · Conservation Physiology
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