Tentacled Snakes Innately Predict Future Prey Behavior
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Born Knowing: Tentacled Snakes Innately Predict Future Prey Behavior Kenneth C. Catania* Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee, United States of America Abstract Background: Aquatic tentacled snakes (Erpeton tentaculatus) can take advantage of their prey’s escape response by startling fish with their body before striking. The feint usually startles fish toward the snake’s approaching jaws. But when fish are oriented at a right angle to the jaws, the C-start escape response translates fish parallel to the snake’s head. To exploit this latter response, snakes must predict the future location of the fish. Adult snakes can make this prediction. Is it learned, or are tentacled snakes born able to predict future fish behavior? Methods and Findings: Laboratory-born, naı¨ve snakes were investigated as they struck at fish. Trials were recorded at 250 or 500 frames per second. To prevent learning, snakes were placed in a water container with a clear transparency sheet or glass bottom. The chamber was placed over a channel in a separate aquarium with fish below. Thus snakes could see and strike at fish, without contact. The snake’s body feint elicited C-starts in the fish below the transparency sheet, allowing strike accuracy to be quantified in relationship to the C-starts. When fish were oriented at a right angle to the jaws, naı¨ve snakes biased their strikes to the future location of the escaping fish’s head, such that the snake’s jaws and the fish’s translating head usually converged. Several different types of predictive strikes were observed. Conclusions: The results show that some predators have adapted their nervous systems to directly compensate for the future behavior of prey in a sensory realm that usually requires learning. Instead of behavior selected during their lifetime, newborn tentacled snakes exhibit behavior that has been selected on a different scale—over many generations. Counter adaptations in fish are not expected, as tentacled snakes are rare predators exploiting fish responses that are usually adaptive. Citation: Catania KC (2010) Born Knowing: Tentacled Snakes Innately Predict Future Prey Behavior. PLoS ONE 5(6): e10953. doi:10.1371/journal.pone.0010953 Editor: Sarah Frances Brosnan, Georgia State University, United States of America Received April 10, 2010; Accepted May 13, 2010; Published June 16, 2010 Copyright: ß 2010 Kenneth C. Catania. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding was provided by the National Science Foundation award # 0844743 and a MacArthur Award. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The author has declared that no competing interests exist. * E-mail: [email protected] Introduction C-start escape response exhibited by fish [9–11]. When hunting, a snake assumes a J-shaped position with its head forming the base Aquatic tentacled snakes (Erpeton tentaculatus) live and breed in of the J. From this rigid posture, it waits cryptically for fish to stagnant or slow moving water in Thailand, Cambodia, and South approach and most often strikes when fish have entered the Vietnam [1,2]. They are often called the ‘‘fishing snake’’ and this concave region between its head and body (Movie S1). Just before name is well earned, as they feed exclusively on fish and have a strike is initiated, the snake moves its body in a ‘‘feint’’ that unique anatomical and behavioral specializations for capturing usually triggers the fish escape response away from the body and their elusive prey [3–5]. Their most obvious, defining specializa- toward the head [12]. When fish are oriented parallel to the long tion is a pair of tentacles that protrude from the rostral margins of axis of the head, the body feint provides an obvious advantage by the head (Figure 1). The tentacles are sensitive mechanoreceptors most often startling fish in the wrong direction (from the fish that respond to nearby water movements [5]. Mechanosensory perspective) - toward the snake’s approaching jaws (Figure 2A). information from the tentacles projects to the optic tectum [5], a But when fish are oriented at a right angle to the jaws, the escape brain structure dominated by visual inputs but that also receives response translates fish parallel to the snake’s head -to either the and integrates information from other modalities to guide left or the right - rather than toward the strike. To exploit this attention and orientation movements [6–8]. Tentacle inputs latter response, the snake feints with its body and then biases its activate cells primarily in deep layers of the tectum. These strike to the future location of the escaping fish’s head findings are consistent with behavioral observations that suggest (Figure 2B,C). This is remarkable, because the ballistic strikes vision plays the dominant role in guiding strikes at fish, with the are initiated before fish begin to move, and thus the snake must tentacles providing additional information that becomes increas- predict the future behavior of fish [12]. Is this prediction learned, ingly important as vision is degraded at night or in turbid water. or has evolution tailored the snake’s nervous system to compensate In addition to the mechanoreceptive appendages, tentacled for future fish movements from birth? The most likely answer is snakes have a remarkable behavior that takes advantage of the not obvious, because the body feint prior to striking is adaptive for PLoS ONE | www.plosone.org 1 June 2010 | Volume 5 | Issue 6 | e10953 Tentacled Snakes Figure 1. The unusual anatomy of the tentacled snake’s head under the scanning electron microscope. The scaled tentacles are sensitive mechanoreceptors that respond to water movements [5]. These appendages likely aid snakes in locating fish at night, with the eyes the playing the dominant role under lighted conditions. doi:10.1371/journal.pone.0010953.g001 a range of fish approach angles that do not require a predictive strike. In this investigation high-speed video analysis of snake strikes and fish escape responses reveal that naı¨ve tentacled snakes can make an accurate prediction of future prey movement for some fish positions and orientations. In addition to these observations, prey handling time and potential predator avoidance strategies [4] are discussed for both juvenile and adult tentacled snakes. Results Predictive Strikes by Naı¨ve Snakes An obvious challenge for this investigation was to prevent learning, throughexperiencewithfishC-starts,whenthenewbornsnakeswere Figure 2. Tentacled snake hunting posture and strategy. A. fed fish during the course of this study. This was addressed by feeding When fish approach the concave area between head and body, the snake feints with its body before striking, generating a water snakes dead fish by hand, which they readily accepted. To examine disturbance that usually startles fish toward the striking jaws [12]. B. strikes at live fish while preventing learning, snakes were placed in a When fish approach the jaws at a right angle, the body feint usually shallow water container with a clear transparency sheet (n = 10 startles fish away from the body. Adult tentacled snakes bias their strike snakes) or glass bottom (n = 2 snakes). The chamber was placed over a to predict this future fish movement (C). The current study examines channel in a separate aquarium such that a fish (a fathead minnow, this behavior in naı¨ve, juvenile tentacled snakes. Trials were included in Pimephales promelas the present investigations if long axis of the fish intersected line ) could swim below (Figure 3 and see methods for segment ‘‘R’’ in B, drawn from the tip of the tentacle through the long more details). Thus snakes could see and strike at the fish, without axis of the snake’s jaw to the neck, and included strikes at both contact. Surprisingly, the snake’s body feint elicited C-starts in the fish approaching and receding fish. The average intersection point for the below the transparency sheet, allowing the accuracy of the snake’s long axis of fish on the snake’s jaws is indicated at ‘‘I’’, 11.6 mm from strike direction to be measured in relationship to the C-starts. C-starts the tip of the head not counting the tentacle. The standard deviation were never elicited through the glass barrier, indicating that acoustic for the intersection point was 5.6 mm for the 100 trails examined using a plastic barrier between snake and fish (see text and Figure 3). or hydrodynamic (rather than visual) components of the body feint doi:10.1371/journal.pone.0010953.g002 elicit the C-starts through the plastic barrier [9,11,13–18]. PLoS ONE | www.plosone.org 2 June 2010 | Volume 5 | Issue 6 | e10953 Tentacled Snakes Figure 3. Schematic illustrating the paradigm used to prevent learning from experience. A. Top view (camera view) of the apparatus. An upper water chamber with a bottom formed from a transparent plastic barrier contained the snake and was placed into the larger, lower chamber containing the fish. The upper chamber rests on two clear plastic supports creating a channel below the snake, separated from the snake by the clear barrier. A single fish was introduced in the channel. Thus snakes could see and strike at the fish without making contact. B. Side view showing the relationship between the two water chambers. doi:10.1371/journal.pone.0010953.g003 In 100 trials (10 for each of 10 snakes with fish approaching or behavior trials (see Movie S2, Clips 16–25). Examples of these receding at an approximate right angle to the jaw) using the plastic downward strikes were later observed when the plastic barrier was barrier, C-starts were elicited 88 times.