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Visual Navigation and Terrestrial Locomotion of the Intertidal Killifish Fundulus Heteroclitus

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Visual Navigation and Terrestrial Locomotion of the Intertidal Killifish Fundulus Heteroclitus Look before you leap: Visual navigation and terrestrial locomotion of the intertidal killifish Fundulus heteroclitus Honors Thesis Presented to the College of Arts and Scienes Cornell University in Partial Fulfillment of the Requirements for the Biological Sciences Honors Program by Noah Bressman May 2016 Supervisor Dr. William Bemis RESEARCH ARTICLE Look Before You Leap: Visual Navigation and Terrestrial Locomotion of the Intertidal Killifish Fundulus heteroclitus NOAH R. BRESSMAN1*, 1 2 STACY C. FARINA , AND ALICE C. GIBB 1Cornell University, Ithaca, New York 2Northern Arizona University, Flagstaff, Arizona ABSTRACT Mummichogs (Fundulus heteroclitus; Cyprinodontiformes) are intertidal killifish that can breathe air and locomote on land. Our goals were to characterize the terrestrial locomotion of mummichogs and determine their method of navigation towards water in a terrestrial environment. We used high-speed video to record behavior during stranding experiments and found that mummichogs use a tail-flip jump to move overland, similarly to other Cyprinodontiformes. However, mummichogs also prop themselves upright into a prone position between each jump, a previously undescribed behavior. After becoming prone, mummichogs rotate about their vertical axis, directing the caudal fin towards the water. Then, they roll back onto their lateral aspect and use a tail-flip behavior to leap into a caudally-directed, ballistic flight path. We conducted experiments to determine the sensory stimulus used to locate a body of water by placing mummichogs on a square platform with one side adjacent to a sea table. Under artificial light, mummichogs moved towards the sea table with a higher frequency than towards the other sides. Under dark conditions, mummichogs did not show a preference for moving towards the sea table. When the surface of the water was covered with reflective foil, mummichogs moved towards it as if it were a body of water. These results suggest that mummichogs primarily use visual cues, specifically reflected light, to orient towards the water. The uprighting behavior that mummichogs perform between terrestrial jumps may provide an opportunity for these fish to receive visual information that allows them to safely return to the water. J. Exp. Zool. 325A:57–64, 2016. © 2015 Wiley Periodicals, Inc. How to cite this article: Bressman NR, Farina S, Gibb A. 2016. Look before you leap: Visual fi Fundulus heteroclitus J. Exp. Zool. navigation and terrestrial locomotion of the intertidal killi sh . J. Exp. 325A:57–64, 2016 Zool. 325A:57–64. The intertidal zone is a dynamic habitat, immersed in water during high tide and exposed to the air during low tide. When the tide recedes, tidepools may lose their connection with the ocean, Grant sponsor: Andrew W. Mellon Foundation; grant sponsor: National isolating intertidal fishes in these pools. Because these pools are Science Foundation; grant number: DEB-1310812. stagnant and often exposed to intense sunlight, they can quickly Additional supporting information may be found in the online version of this article at the publisher's web-site. become hypoxic, develop high concentrations of salt and waste, ÃCorrespondence to: Noah Ryan Bressman, 11 Pine Cliff Road, or dry up completely; all of these conditions will create a Chappaqua, NY, 10514. E-mail: [email protected] physiologically challenging environment for fishes (Martin and Received 3 July 2015; Revised 15 October 2015; Accepted 15 October Bridges, '99; Taylor et al., 2008). Because tidepools may disappear 2015 or become inhospitable, many intertidal fishes display adapta- DOI: 10.1002/jez.1996 Published online 5 November 2015 in Wiley Online Library tions for surviving brief periods out of water, including the ability (wileyonlinelibrary.com). to navigate between bodies of water (Mast, '15; Goodyear, '70; © 2015 WILEY PERIODICALS, INC. 58 BRESSMAN ET AL. Aronson, '71), locomote on land (Gibb et al., 2011; King et al., to navigate a terrestrial environment. It seems unlikely that fishes 2011; Gibb et al., 2013), and extract oxygen from the air (Hughes can use their lateral line system when on land, as this system and Singh, '70; Gervais and Tufts, '98; Martin and Bridges, '99; relies on near-field fluid movements, and the spatial extent of the Ong et al., 2007). These adaptations make intertidal fishes ideal near field is greatly reduced in air when compared with water subjects for experiments that investigate behavioral, sensory, and (Harris and van Bergeijk, '62; Coombs and Montgomery, '99). locomotor strategies for surviving on land. Some cyprinodontiform fishes, like Gambusia affinis, use the The mummichog (Fundulus heteroclitus) is a widespread otolith-vestibular system to obtain sensory information on land species of killifish (Cyprinidontiformes) that is commonly found (Boumis et al., 2014), but this system can only provide in intertidal habitats, including marshes, sandbars, and rocky information about body position; it is unlikely that the otolith- tidepools along the Atlantic coast of North America, from Nova vestibular system can aid in locating a body of water when the Scotia to Georgia (Martin and Bridges, '99). Many killifishes that fish is positioned on flat ground. In some situations, fishes may live at the water's edge in ponds, streams, or in the intertidal, use their vision to detect celestial cues when navigating toward exhibit amphibious adaptations. For example, mummichogs and water: a study by Goodyear ('70) found that Fundulus notti were the mangrove rivulus (Kryptolebias marmoratus) can extract able to use the sun as a compass to return to the water. Because oxygen from the air using their gills and skin (Halpin and Martin, the refractive properties of water and air are very different, it is '99; Martin and Bridges, '99; Ong et al., 2007). The mangrove unlikely that mummichogs (Fundulus heteroclitus) can focus well rivulus can survive on land for weeks at a time in a moist enough in air to distinguish physical landmarks in their environment (Ong et al., 2007; Taylor et al., 2008). In addition, environment. However, some animals, such as beetles, follow killifishes and livebearing cyprinodontiform fishes (e.g., Gambu- the reflection of light off surfaces to locate water sources sia affinis) can perform terrestrial jumps (Gibb et al., 2011; Mast, (Szentkiralyi et al., 2003). We hypothesize that, in the absence of '15) and will use jumping and other behaviors to move over land celestial cues, mummichogs navigate across land by searching for from one body of water to another (Mast, '15; Goodyear, '70). light reflecting off the surface of water. Locomotion on land is challenging for fishes, at least in part Because mummichogs are found in pools throughout the because they lack the ability to lift their center of mass off the intertidal zone and may often become stranded, they represent an ground using two sets of paired limbs (Gibb et al., 2013). Instead, intermediate modality between fishes that frequently leave the many ray-finned fishes employ ballistic behaviors in which they water voluntarily (e.g., K. marmoratus and Periopthalmus spp.) launch their center of mass into the air (Gibb et al., 2013). One and fishes that are fully-aquatic and never voluntarily leave the apparently widespread terrestrial behavior is the tail-flip jump, water. Therefore, the overarching objective of this study is to during which high-curvature bending of the body away from the answer the question: “how do mummichogs navigate their substrate is followed by contralateral flexion of the posterior environment to return to the water?” From this question, we body, which pushes the caudal peduncle against the ground to developed three specific goals: (1) to characterize the terrestrial launch the fish into a ballistic trajectory (Gibb et al., 2011; Gibb locomotion of mummichogs, including describing non-propul- et al., 2013; Boumis et al., 2014). The tail-flip jump allows a fish to sory behaviors that may be used to aid the fish in gathering move overland, even if an incline is not present. However, sensory information, (2) to assess the success of mummichogs in another type of ballistic behavior is seen in mudskippers and locating a body of water under controlled conditions, and (3) to other fishes that frequently emerge from water: prone jumping. determine the importance of vision in the terrestrial navigation of Prone jumpers, such as mudskippers (Periopthalmus spp.) and mummichogs and identify the cues associated with visual Pacific leaping blennies (e.g., Alticus arnoldorum), move from an navigation. upright position, in which their ventral surface rests on the substrate (Swanson and Gibb, 2004; Hsieh, 2010; Gibb et al., MATERIALS AND METHODS 2013); this orientation has been proposed to improve a fish's On July 31st, 2013, we used minnow traps to collect 30 ability to acquire sensory information while on land by allowing mummichogs (ranging from 3 to 6 cm in total length (TL; as it to observe the environment from an upright position (Gibb defined as the length from the tip of the snout to the end of the et al., 2013). Sitting in an upright position will elevate a fish's eyes caudal fin) and 2–6 g in mass) from tidepools on Appledore Island above the ground and improve their visual field, thus allowing at Shoals Marine Lab (SML) in the Gulf of Maine. Fish were held in them to better search for prey, predators, conspecifics, or water. a sea table with flowing seawater pumped from the surface of the When in water, fishes navigate through their habitats using a waters around the marine station for 48 hr before the experiments combination of vision (Hawryshyn, '92), mechanoreception (the were conducted. These individuals were used for a preliminary vestibular system, the lateral line, and hearing; Webb et al., 2008), navigation experiment to assess whether mummichogs can and olfaction (Hara, '75). However, when fishes are on land, the successfully navigate towards a body of water in an unfamiliar change in the physics of their environment likely impacts their terrestrial environment.
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