Abstract
Aquatic C-start escape responses in teleost fishes are driven by a well-studied network of reticulospinal neurons that produce a motor pattern of simultaneous contraction of axial muscle on the side of the body opposite the threatening stimulus, bending the fish into the characteristic C shape, followed by a traveling wave of muscle contraction on the contralateral side that moves the fish away from the threat. Superficially, the kinematics of the terrestrial tail-flip resemble the C-start, with the anterior body rolling up and over the tail into a tight C shape, followed by straightening as the fish launches off of the caudal peduncle into ballistic flight. We asked whether similar motor control is used for both behaviors in the amphibious mangrove rivulus, Kryptolebias marmoratus Fine-wire bipolar electrodes were percutaneously inserted into repeatable paired axial locations in five individual fish. Electromyograms synchronized with high-speed video were made of aquatic C-starts, immediately followed by terrestrial tail-flips. Tail-flips took longer to complete than aquatic escapes; correspondingly, muscles were activated for longer durations on land. In the tail-flip, activity was seen in contralateral posterior axial muscle for an extended period of time during the formation of the C shape, likely to press the caudal peduncle against the ground in preparation for launch. Tail-flips thus appear to be produced by modification of the motor pattern driving the aquatic C-start, with differences consistent with the additional requirement of overcoming gravity.
Highlights
The mangrove rivulus, Kryptolebias marmoratus Poey 1880 (Cyprinodontiformes), is an amphibious fish that makes temporary excursions onto land for various reasons: actively pursuing prey at the water–land interface, purposefully leaving the water as a result of poor conditions such as high levels of hydrogen sulfide or anoxia, being stranded at low tide or escaping an aquatic predator (Abel et al, 1987; Regan et al, 2011; Pronko et al, 2013)
To standardize our comparisons of the maximum body curvature reached at the end of Stage 1 and the duration to complete Stage 1 in both media, we calculated the curvature coefficient (Webb, 1978b; Brainerd and Patek, 1998). We slightly modified this dimensionless number by measuring the chord length (CL), which we described as the distance from the tip of the snout to the caudal peduncle when the fish was bent, divided by the standard length (SL) of the body when the fish was straight
We conclude that a modification of the motor pattern producing the aquatic C-start behavior drives the terrestrial tail-flip
Summary
The mangrove rivulus, Kryptolebias marmoratus Poey 1880 (Cyprinodontiformes), is an amphibious fish that makes temporary excursions onto land for various reasons: actively pursuing prey at the water–land interface, purposefully leaving the water as a result of poor conditions such as high levels of hydrogen sulfide or anoxia, being stranded at low tide or escaping an aquatic predator (Abel et al, 1987; Regan et al, 2011; Pronko et al, 2013). Gobies, sculpins and some other groups of teleost fishes are capable of finding themselves on land through active and passive means (Gibb et al, 2013). Once there, these fish must contend with the demands of the terrestrial environment: buoyant support is lacking, gravity must be overcome and new predators such as birds or snakes may be encountered. The mangrove rivulus and many other small fishes lacking modified fins for terrestrial support and locomotion move by means of a ‘tailflip’, a coordinated movement in which the fish, lying on its side, Wake Forest University, Department of Biology, 1834 Wake Forest Road, Winston-Salem, NC 27106, USA. An unanswered question is how the tail-flip behavior is generated
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