Thrash, Flip, or Jump: The Behavioral and Functional Continuum of Terrestrial Locomotion in Teleost Fishes

• Published in: Integrative and comparative biology 2013-08, Vol.53 (2), p.295-306
• Main Authors: Gibb, Alice C., Ashley-Ross, Miriam A., Hsieh, S. Tonia
• Format: Article
• Language: English
• Subjects: Adaptation, Physiological - physiology; Anatomy & physiology; Animal behavior; Animals; Behavior, Animal - physiology; Biological Evolution; Biomechanical Phenomena - physiology; Caudata; Ecosystem; Environment; Fish; Fishes - physiology; Freshwater; Gambusia; Kinematics; Locomotion - physiology; Micropterus; Micropterus salmoides; Morphology; Motor ability; Musculoskeletal Physiological Phenomena; Phylogeny; Pisces; Teleostei; Terrestrial ecosystems; Vertebrate Land Invasions – Past, Present, and Future
• ISSN: 1540-7063; 1557-7023
• DOI: 10.1093/icb/ict052

Moving on land versus in water imposes dramatically different requirements on the musculoskeletal system. Although many limbed vertebrates, such as salamanders and prehistoric tetrapodomorphs, have an axial system specialized for aquatic locomotion and an appendicular system adapted for terrestrial locomotion, diverse extant teleosts use the axial musculoskeletal system (body plus caudal fin) to move in these two physically disparate environments. In fact, teleost fishes living at the water’s edge demonstrate diversity in natural history that is reflected in a variety of terrestrial behaviors: (1) species that have only incidental contact with land (such as largemouth bass, Micropterus) will repeatedly thrash, which can roll an individual downhill, but cannot produce effective overland movements, (2) species that have occasional contact with land (like Gambusia, the mosquitofish, which evade predators by stranding themselves) will produce directed terrestrial movement via a tail-flip jump, and (3) species that spend more than half of their lives on land (like the mudskipper, Periopthalmus) will produce a prone-jump, a behavior that allows the fish to anticipate where it will land at the end of the flight phase. Both tail-flip and prone jumps are characterized by a two-phase movement consisting of body flexion followed by extension—a movement pattern that is markedly similar to the aquatic fast-start. Convergence in kinematic pattern between effective terrestrial behaviors and aquatic fast starts suggests that jumps are an exaptation of a neuromuscular system that powers unsteady escape behaviors in the water. Despite such evidence that terrestrial behaviors evolved from an ancestral behavior that is ubiquitous among teleosts, some teleosts are unable to move effectively on land—possibly due to morphological trade-offs, wherein specialization for one environment comes at a cost to performance in the other. Indeed, upon emergence onto land, gravity places an increased mechanical load on the body, which may limit the maximum size of fish that can produce terrestrial locomotion via jumping. In addition, effective terrestrial locomotor performance may require a restructuring of the musculoskeletal system that directly conflicts with the low-drag, fusiform body shape that enhances steady swimming performance. Such biomechanical trade-offs may constrain which teleost species are able to make the evolutionary transition to life on land. Here, we synthesize the cur