Elsevier

Physiology & Behavior

Volume 139, February 2015, Pages 145-149
Physiology & Behavior

Behavioral and physiological antipredator responses of the San Marcos salamander, Eurycea nana

https://doi.org/10.1016/j.physbeh.2014.11.013Get rights and content

Highlights

  • Salamanders showed higher antipredator response to chemical cues of a fish predator with lower temporal encounter frequency.

  • Salamanders only showed a corticosterone response to a fish predator with a lower temporal encounter frequency.

  • Salamanders may mute behavioral and corticosterone responses to predators with high temporal encounter frequencies.

Abstract

Exposure to predatory stimuli typically results in the elevation of circulating glucocorticoid levels and a behavioral response of freezing or escape behavior in many prey species. Corticosterone (CORT) is the main glucocorticoid in amphibians and is known to be important in modulating many behaviors and developmental functions. The federally threatened San Marcos salamander, Eurycea nana, decreases activity in response to both native and introduced predatory fish, however, experience may further influence these interactions. To better understand the indirect effects of fish predators on this salamander, we examined both the antipredator behavior and water-borne CORT release rates in response to chemical cues (kairomones) from two fish species that varied in temporal risk of predation: (1) a low encounter frequency predator (largemouth bass, Micropterus salmoides), (2) a high encounter frequency predator (redbreast sunfish, Lepomis auritus), and (3) a blank water control. Salamanders reduced activity (antipredator response) after exposure to both predator treatments, but not to the blank water control, and the response to M. salmoides was significantly stronger than that to L. auritus. The CORT response (post-stimulus/pre-stimulus release rates) did not differ between the blank water control and L. auritus treatments, and both were significantly less than the CORT response to M. salmoides. Overall, E. nana showed a decreased antipredator response and no CORT response towards the high encounter frequency L. auritus as compared to the low encounter frequency M. salmoides. Eurycea nana may mute antipredator and CORT responses to high temporal frequency predators. There was, however, no correlation between CORT release rates and antipredator behavior, which suggests that the presence of predators may be affecting CORT response and behavior independently.

Introduction

Predators can influence prey fitness either directly, through the consumption of individuals, or indirectly, through costs accrued from antipredator behavior [1]. In aquatic systems, predator recognition may result in prey species forming groups [2], increasing refugia use [3], [4], or reducing overall activity levels [5], [6]. Although these behaviors may decrease the immediate threat of predation, predators can have lingering, nonlethal effects on prey species, which may persist through time [7]. Nonlethal effects are important considerations for the fitness of species, even though they may not be as apparent as direct predation upon individuals. One such example includes the predatory influence on circulating stress hormone levels in prey species that may be involved in escape behaviors [8]. Additionally, stress hormones may also be important for responding appropriately in subsequent encounters with predators, as stress hormones may play a role in learned predator recognition [9], [10], [11].

Most vertebrates respond to stressors with a rapid elevation of glucocorticoid (GC) hormones, where the intensity of the stressor can affect the degree of the GC response [12]. Elevated GC levels trigger the metabolism of lipids, proteins, and carbohydrates, enhancing functions necessary for immediate survival of an individual [13], [14]. However, over longer periods of time, chronically elevated GC levels can directly suppress immune responses, reproduction, growth, and decrease expression of androgen-mediated mating behaviors [13], [15]. Acute stress responses are likely beneficial, but chronic activation of the stress system to prolonged predation pressure may have fitness consequences. Prior studies have assumed that as exposure to stressors increase, so do baseline levels of corticosterone (CORT; a major GC), and chronically higher levels of CORT are associated with reduced relative fitness of individuals or populations, also known as the Predation Stress Hypothesis [16] or the CORT-Fitness Hypothesis [17].

Direct predator exposure or indirect exposure through chemical cues (kairomones) can cause immediate increases in circulating GC levels in prey [18], [19] but not always [16]. Elevated CORT levels can enhance antipredator response [11], [20] and may modulate subsequent behavioral and morphological responses to predators. Hossie et al. [21] experimentally demonstrated that Lithobates (Rana) pipiens tadpoles, when exposed to a CORT receptor inhibitor, showed decreased behavioral and morphological responses to predators when compared to control groups. A second study by Middlemis Maher et al. [22] found that long-term exposure to CORT might enhance survivorship of Lithobates sylvaticus (Rana sylvatica) tadpoles through the induction of morphological changes in tail shape. Both Fraker et al. [23] and Middlemis Maher et al. [22] found lower levels of CORT immediately following predator exposure in L. sylvaticus tadpoles. This decrease in CORT levels is contrary to what has previously been seen in other vertebrate groups, even though the antipredator response (freezing behavior) is similar [24]. These differences across vertebrate groups suggest that the expression of CORT and the subsequent modulation of behaviors vary across taxa.

Another factor in antipredator (and possibly CORT response) to predators may be perceived risk levels. Lima and Bednekoff [25] developed the Risk Allocation Hypothesis (RAH) that suggests that prey foraging under temporal variation in risk of predation face problems in how to optimally display antipredator behavior. For example, if predators are encountered infrequently and periods of risk are brief, then foraging prey should exhibit heightened antipredator behavior; any costs to foraging or mating can be regained during periods of low or no risk. Alternatively, if predators are common and periods of predation risk are prolonged, prey should exhibit reduced antipredator behavior, and should continue to forage during these high-risk periods. At the same time, chronic CORT levels can have negative fitness consequences and therefore, blunted CORT responses may be expected when prey are exposed to common, abundant predators.

We examined the antipredator and CORT responses of the San Marcos salamander, Eurycea nana, to temporal variation in risk of predation by fish predators. Eurycea nana is a federally threatened, IUCN red-listed, neotenic (fully aquatic) salamander endemic to the headwaters of the San Marcos River, Hays County, Texas [26]. Previous studies have demonstrated the use of chemical stimuli in the detection of both conspecifics [27] and fish predators [6], [28]. Eurycea nana shows the antipredator behavior of freezing in response to chemical cues emitted by a variety of fish predators (Lepomis cyanellus, Lepomis auritus, Micropterus salmoides, Herichthys cyanoguttatum) [6], [28] including the allopatric species Lepomis gibbosus indicating a generalized antipredator response [6]. In this closed system, both M. salmoides and L. auritus are the most abundant species and they have significantly increased in abundance compared to other large, predatory fish species over the past three decades [29]. Because E. nana shows a generalized antipredator response to Lepomis, we propose that this species will be perceived as a higher temporal risk than M. salmoides. We examine the antipredator and CORT responses of wild-caught (predator experienced) E. nana to M. salmoides and L. auritus, and predict that E. nana will show antipredator and CORT responses to both species but will have a muted antipredator and CORT response to the temporally abundant L. auritus.

Section snippets

Predator species

To further understand any differences in the effects that predatory fish have on E. nana, we collected chemical cues from two centrarchid (Perciformes: Centrarchidae) fish: the redbreast sunfish (L. auritus) and the largemouth bass (M. salmoides). The diet of L. auritus within the San Marcos River is primarily aquatic invertebrates (Diptera, Ephemeroptera, and Trichoptera), suggesting that this species is a generalist benthic feeder [30]. Examination of the diet of M. salmoides suggests that it

Results

There were significant differences in the activity indices among the three treatments (ANOVA: F2,57 = 24.75, p < 0.0001; Fig. 1). The activity index from the blank water control was significantly greater than the mean activity index from both the introduced redbreast sunfish (L. auritus) treatment (Tukey's HSD: p = 0.0002) and the native largemouth bass (M. salmoides) treatment (p < 0.0001). Additionally, the activity index for the M. salmoides treatment was significantly lower than that of the L.

Discussion

Eurycea nana significantly reduced activity (antipredator behavior) in response to chemical cues from both the largemouth bass (M. salmoides) and the redbreast sunfish (L. auritus) when compared to the blank water treatment, and the response to M. salmoides was significantly stronger than the response to L. auritus. The CORT response to the blank water treatment and L. auritus did not differ statistically; however, the CORT response to M. salmoides was significantly greater than both the

Acknowledgments

We thank T. Brandt, J. Fries, V. Cantu, and the San Marcos Aquatic Resources Center (SMARC) for logistical support and use of facilities, and A. Wallendorf and the Aquarena Center for assistance in fish collection. Helpful comments on this manuscript were provided by A. Davis, K. Epp, J. Fries, J. Ott, and C. Siler. This experiment was approved by Texas State University IACUC (#1021_0614_20). Fish were collected under a Texas Parks and Wildlife Scientific Research Permit (SPR-0511-126) to DRD.

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