Thrash, flip, or jump: The behavioral and functional continuum of terrestrial locomotion in teleost fishes

Alice C Gibb, Miriam A. Ashley-Ross, S. Tonia Hsieh

Research output: Contribution to journalArticle

34 Scopus citations

Abstract

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 current knowledge of intermittent terrestrial locomotion in teleosts and demonstrate that extant fishes represent an important model system for elucidating fundamental evolutionary mechanisms and defining the physiological constraints that must be overcome to permit life in both the aquatic and terrestrial realms.

Original languageEnglish (US)
Pages (from-to)295-306
Number of pages12
JournalIntegrative and Comparative Biology
Volume53
Issue number2
DOIs
StatePublished - Aug 2013

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ASJC Scopus subject areas

  • Animal Science and Zoology
  • Plant Science

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