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A Game of Patience Between Predator and Prey: Waiting for Opponent's Action Determines Successful Capture Or Escape

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A Game of Patience Between Predator and Prey: Waiting for Opponent's Action Determines Successful Capture Or Escape Canadian Journal of Zoology A game of patience between predator and prey: waiting for opponent’s action determines successful capture or escape Journal: Canadian Journal of Zoology Manuscript ID cjz-2019-0164.R2 Manuscript Type: Article Date Submitted by the 20-Dec-2019 Author: Complete List of Authors: Nishiumi, Nozomi; National Institute for Basic Biology, Laboratory of Neurophysiology Mori, Akira; Kyoto University, Graduate School of Science, Department of ZoologyDraft Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: optimal escape theory, flight initiation distance, antipredator strategy, Keyword: predator-prey interaction, Japanese striped snake (Elaphe quadrivirgata), Black-spotted pond frog (Pelophylax nigromaculatus) https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 27 Canadian Journal of Zoology TITLE PAGE (i) Title “A game of patience between predator and prey: waiting for opponent’s action determines successful capture or escape” (ii) Authors’ names NN AM (iii) Affiliation and address NN: Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo, Kyoto 606-8502, JAPAN [email protected] AM: Draft Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwakecho, Sakyo, Kyoto 606-8502, JAPAN [email protected] current affiliation of NN National Institute for Basic Biology, 5-1 Higashiyama, Myodaiji, Okazaki, Aichi 444-8787, JAPAN [email protected] (iv) The author responsible for correspondence Nozomi Nishiumi National Institute for Basic Biology, 5-1 Higashiyama, Myodaiji, Okazaki, Aichi 444-8787, JAPAN +81-564-59-5596 [email protected] https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 27 Nozomi Nishiumi (NN), Akira Mori (AM) “A game of patience between predator and prey: waiting for opponent’s action determines successful capture or escape” Abstract When predator and prey animals face to each other, preemptive actions by both sides are considered to mediate successful capture or escape. However, in spite of the general presumption, some animals, such as predatory snakes and their frog prey, occasionally remain motionless or move slowly for a while before striking or escaping, respectively. To clarify the possible advantages of this behaviour, we examined interactions between snakes (Elaphe quadrivirgata, Boie, 1826) and frogs (Pelophylax nigromaculatus, Hallowell, 1861), focusing especially on kinematic features of strike behaviour of snakes and flight behaviour of frogs in close quarters. Staged encounter experiments and field observations revealed thatDraft counteractions against an opponent’s preemptive actions are effective for both snakes and frogs until a certain distance because they are hardly able to change their trajectories once they initiate strike or escape behaviours. Snakes and frogs also appropriately switched their behaviour from waiting for the opponent’s action to taking preemptive action at this threshold distance. These results suggested the occurrence of a game of patience between snakes and frogs, in which they wait for the opponent’s action so as to achieve effective countermeasures. Our study provides new insights for predicting optimal decision-making by predators and prey, and will contribute to a better understanding of their strategies. Key words: Japanese striped snake (Elaphe quadrivirgata), Black-spotted pond frog (Pelophylax nigromaculatus), Flight initiation distance, optimal escape theory, antipredator strategy, predator-prey interaction https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 27 Canadian Journal of Zoology Introduction Predation avoidance is essential for prey animals, and thus they have evolved to make decisions to use suitable anti-predator tactics in different situations (Edmunds 1974; Dawkins and Krebs 1979). Escape behaviour is a typical countermeasure used against the approach of predators, and it should be initiated appropriately so as to maximize the fitness of the prey animals because it includes several costs and risks to the prey (Cooper and Blumstein 2015). The optimal timing for escape initiation has been discussed in theoretical biology. Representative theories are based on an economic model, which predicts the optimal predator-prey distance at which escape should be initiated by considering the balance between the cost of staying and the cost of escaping: whereas escaping too late reduces the probability of successful escape, escaping too early results in a loss of benefits from activities in which the prey may currently be engaged,Draft such as acquiring food or a mate (Ydenberg and Dill 1986; Cooper and Frederick 2007). This economic escape model has also been developed while considering the costs of monitoring predators (Blumstein 2010; Cooper et al. 2015). Another escape initiation model developed from a different point of view predicts the optimal timing to initiate escape from an inconspicuous motionless state, which considers the balance between the probability of successful hiding and the probability of successful escape: whereas escaping too late reduces the probability of successful escape, escaping too early results in attracting predators that would pass by without recognizing the presence of the prey (Broom and Ruxton 2005). In spite of the development of escape initiation theories, the mechanisms of successful escape have not been sufficiently considered in these theories. The above models simply assume that escape initiated at shorter predator-prey distance results in a lower probability of successful escape (Ydenberg and Dill 1986; Broom and Ruxton 2005; Cooper and Frederick 2007). However, many prey animals are known to initiate escape not immediately upon seeing predators and this delay allows the predators to come closer, even when they have no chance to acquire any benefits assumed in the above models such as food, a mate and avoiding detection by predators (Brodie et al. 1974; Ducey https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 27 and Brodie 1983; Lagos et al. 2014). Thus, it is important to empirically clarify the effect of escape initiation timing on the outcome of the escape attempt. Previous studies dealing with the above mentioned escape theories mostly used a simulated predator, such as a human approaching the prey, and therefore were not able to test the effect of escape initiation timing on escape success (Kramer and Bonenfant 1997; Samia et al. 2015). Herein, we analysed predator-prey interactions using snakes and frogs to explore the factors that affect successful escape by focusing on kinematic features of predatory and escape behaviours. Frogs rely on jumping to escape from predators (Toledo et al. 2011), which brings them into mid-air for a moment. Because of the absence of friction with the ground during a jump, frogs are scarcely able to change their direction of escape in the air. On the other hand, capture of prey by snakes is basically achieved by sneaking and crawling up to the prey and subsequently striking at it over a short distance (Cundall andDraft Greene 2000). At the strike, snakes open their jaws and project the head, head and neck, or the anterior part of the body rapidly toward the prey (Cundall and Greene 2000). During a strike, a third or less of the trunk is recruited to move the head, with the remainder of the trunk remains essentially stationary to serve as an inertial launching platform for the head (Cundall and Greene 2000). Thus, it is likely that once snakes initiate a strike, they are scarcely able to change their direction of strike. Moreover, the strike requires preparatory postures that consist of curve(s) of the snake’s body to create rapid forward movement by subsequently straightening the curved section(s) (Kardong and Bels 1998). This implies that once a snake fails to capture prey by strike, they are not able to strike again until they remake the curve(s) in their trunks. Overall, we assumed that frogs and snakes can scarcely change their moving direction for a while after launching into a jumping escape or strike, respectively. Thus, the timing of flight initiation relative to the initiation of a snake strike would be an important factor determining the outcome of the predation event, which has not been considered in the above theories. The present study aimed to examine the function of the non-immediate predatory/escape responses in terms of the kinematic features of frogs and snakes at the initiation of their flight and strike behaviours. We first measured https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 27 Canadian Journal of Zoology the duration and spatial scale of predation events between frogs and snakes under natural conditions. To clarify the advantages of the non-immediate escape responses, we then experimentally investigated the sequence of events in predator-prey interactions between snakes and frogs, and measured the kinematic features of their escape and predatory actions that would determine the outcome of predation events. Materials and Methods Subjects The subjects of this study were a ranid frog, Pelophylax nigromaculatus (Hallowell, 1861), and a colubrid snake, Elaphe quadrivirgata (Boie, 1826). Pelophylax nigromaculatus is a common pond frog that is distributed over a large part of East Asia, includingDraft Japan, Korea, China, and the Amur Basin of Russia (Maeda and Matsui 1990; Zhang et al. 2008). Elaphe quadrivirgata is a diurnal snake that is widely distributed
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