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Analyzing a Predator-Prey Interaction: Muscular Performance in Boas (Boa Constrictor) and Cardiovascular Response in Rats During

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Analyzing a Predator-Prey Interaction: Muscular Performance in Boas (Boa Constrictor) and Cardiovascular Response in Rats During Dickinson College Dickinson Scholar Student Honors Theses By Year Student Honors Theses 5-22-2011 Analyzing a Predator-Prey Interaction: Muscular Performance in Boas (Boa Constrictor) and Cardiovascular Response in Rats During Constriction Katelyn Josephine McCann Dickinson College Follow this and additional works at: http://scholar.dickinson.edu/student_honors Part of the Biology Commons Recommended Citation McCann, Katelyn Josephine, "Analyzing a Predator-Prey Interaction: Muscular Performance in Boas (Boa Constrictor) and Cardiovascular Response in Rats During Constriction" (2011). Dickinson College Honors Theses. Paper 123. This Honors Thesis is brought to you for free and open access by Dickinson Scholar. It has been accepted for inclusion by an authorized administrator. For more information, please contact [email protected]. Analyzing a Predator-Prey Interaction: Muscular Performance in Boas (Boa constrictor) and Cardiovascular Response in Rats during Constriction By Katelyn J. McCann With the collaboration of Kevin Wood Pat McNeal and Emmett Blankenship, DVM Submitted in partial fulfillment of Honors Requirements for the Department of Biology Dr. Scott Boback, Supervisor Dr. Charles Zwemer, Supervisor Dr. Carol Loeffler, Reader May 19, 2011 Abstract: Constricting snakes must balance the energetic cost of constriction with the potential danger in releasing their prey too early. Therefore, it would be advantageous for these snakes to possess a mechanism to determine the minimum pressure and duration required to ensure that a prey item has been subdued and is no longer capable of inflicting harm. We hypothesized that Boas (Boa constrictor) modulate their constriction based on endogenous cues from their prey such as a heartbeat. In previous work we demonstrated that Boas respond to a simulated heartbeat in a deceased rat model by constricting with greater pressure and duration than when constricting rats without a simulated heartbeat. We extended this work in the current study by testing how Boas respond to a more realistic model; a rat whose cardiovascular system fails during the constriction event. We presented snakes with rats with a simulated heartbeat that "failed" halfway into the constriction. Analysis of these data demonstrated that constriction events with a simulated heart which fails ten minutes into the constriction are of intermediate duration and total pressure when compared to constriction tests with no simulated heart and a continuously beating simulated heart. We have also conducted experiments to test the snake's response while constricting live, anesthetized rats. This system allows us to observe the snake's response to an actual rat heartbeat while simultaneously monitoring cardiovascular function in the rat during the constriction. Analyses of these data support our hypothesis that cardiac arrest, rather than suffocation, is the proximate cause of death in rats during constriction. Introduction: Predators have evolved prey capture techniques that balance success in capturing and incapacitating prey with the safety in doing so. Retaliation from prey is typical and predators 1 must have strong selective pressures to minimize risks associated with their prey capture and subduing strategies. Further, the energy expenditure associated with prey capture can be costly to the predator which may be left vulnerable to additional attacks while engaged with its prey. Therefore, the evolution of efficient and successful prey capture methods is of paramount importance to predators' fitness. Snakes are notorious for their unique specializations used to subdue and swallow enormous prey which can exceed their own body mass (Greene, 1997). As limbless, elongate predators, snakes have evolved methods to restrain and incapacitate their bulky and often dangerous prey including envenomation, constriction, or a combination of the two (Shine, 1993). The method of subduing prey varies amongst species of snakes and often within a species depending on the type of prey being captured (Mehta and Burghardt, 2008). Relative to Caenophidians (superfamily of advanced snakes), most extant Henophidians (superfamily of basal snakes) show less variation in prey restraint behavior, employing constriction and coiling, regardless of prey type (Greene and Burghardt, 1978). Recent work has demonstrated that prey restraint behavior varies within some Henophidian groups while others exhibit little flexibility in feeding and prey restraint behavior (Mehta and Burghardt, 2008). Regardless, the consistency in behavioral pattern by those basal snakes was reported by Greene and Burghardt (1978) as evidence that early snakes utilized constriction to restrain and subdue prey and that this feature may have been a key innovation which determined the success of the snake radiation. Boas (Boa constrictor), members of the Henophidia, are non-venomous constrictors feeding on a wide range of prey including lizards, birds and mammals (Greene, 1983). Constriction in Boas is initiated by a strike (typically at the anterior portion of the 2 prey: Mehta and Burghardt, 2008) whereby the snake rapidly propels the anterior portion of its body forward contacting the prey prior to its maximum strike distance. The momentum of the strike carries the snakes' head forward and facilitates the formation of the first coil with a downward movement of the braincase (Cundall and Deufel, 1999). As the head moves ventrally, the snakes body bends laterally creating what is referred to as a ventral-lateral coil. This type of coil orients the prey item horizontal to the substrate and .p laces the snake's ventral and lateral surfaces in contact with the prey, typically over the thorax (Mehta and Burghardt, 2008). Constriction is both energetically costly and potentially dangerous as the snake remains intimately engaged with the prey throughout the constriction. During this time the snake is vulnerable to retaliatory attacks from the prey itself (Erberle and Kappeler, 2008), and it is defenseless to its own predators and even additional prey (e.g., altruistic aggression from kin: Janzen, 1970) as its sensory apparati and means of defense are occupied by the constriction. In addition, Canjani et al. (2003) examined the aerobic metabolism of Boa constrictor amarali during constriction and found constriction times of up to sixteen minutes and rates of oxygen consumption up to 0.325 ml 02 g-1 h-1, an eight-fold increase from resting levels. Therefore, it would be advantageous for these snakes to have a mechanism to determine the minimum pressure and duration of constriction required to ensure that a prey item has been subdued and is no longer capable of inflicting harm. Moon (2000) proposed a heartbeat, lung ventilations, and body movements as potential signals exploited by snakes during constriction to determine exactly when a prey item has expired. Snakes have been shown to possess mechanoreceptors in their skin with high vibrational sensitivity (Proske, 1969), and therefore would likely have the ability to 3 detect changes in such endogenous signals from the prey item. However, in preliminary tests Moon (2000) found that the presence of a heartbeat and ventilatory movements in a dead mouse did not elicit increased constriction pressure or duration in a Caenophidian species, the Kingsnake (Lampropeltis getula). Despite the absence of a response to these endogenous signals in the Kingsnake, it is possible that other species may have a response to such signals. A response may be evident especially in Henophidian snakes because these species retain conservative constriction behavior. Based on the mode of constriction and the wide range of prey items consumed by Boas, it is possible that their constriction is modulated by physiologic cues received from their prey during constriction rather than a pre-strike assessment on the basis of prey size, temperature, or movement (Shine and Sun, 2003). In a previous study conducted in our lab, it was determined that Boas constricting prey with a continuously beating, simulated heart did so for longer and with greater total pressure as compared to snakes constricting prey without a simulated heart (Hall et al., 2010, Figure 1 ). These findings suggest that Boas have the ability to detect the presence of heart contractions in their prey and use this stimulus as feedback to determine the necessary duration and total pressure of constriction. However, these tests (heart beating continuously throughout the constriction event vs. no heart beating) do not precisely replicate the full heartbeat signal that would be present in a live prey item. When snakes constrict live prey, the prey would have a beating heart when first constricted, and then at some undetermined time the heart would likely fail. The widely held belief (cited by at least 32 other herpetological books) that constricting snakes kill their prey by suffocation (Mushinsky, 1987) has recently been challenged in support of the theory that prey are killed via circulatory failure (Hardy, 1994; 4 Moon, 2000). To maximize efficiency of constriction, snakes would presumably have the ability to detect the proximate cause of death in their prey and use this as a cue to release. If the cause of death in prey is indeed circulatory failure then snakes likely possess some ability to determine when cardiac arrest has occurred. Therefore, to more fully understand the dynamic interaction between constricting snakes and their prey, it is important to determine how and when death occurs in prey. In order
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