Comparative kinematics of the forelimb during swimming in red-eared slider (Trachemys scripta) and spiny softshell (Apalone spinifera) turtles

Softshell turtles (Family Trionychidae) possess extensive webbing between the digits of the manus, suggesting that the forelimb may serve as an effective thrust generator during aquatic locomotion. However, the hindlimb has previously been viewed as the dominant propulsive organ in swimming freshwater turtles. To evaluate the potential role of the forelimb in thrust production during swimming in freshwater turtles, we compared the forelimb morphology and three-dimensional forelimb kinematics of a highly aquatic trionychid turtle, the spiny softshell Apalone spinifera, and a morphologically generalized emydid turtle, the red-eared slider Trachemys scripta. Spiny softshells possess nearly twice as much forelimb surface area as sliders for generating drag-based thrust. In addition, although both species use drag-based propulsion, several aspects of forelimb kinematics differ significantly between these species. During the thrust phase of the forelimb cycle, spiny softshells hold the elbow and wrist joints significantly straighter than sliders, thereby further increasing the surface area of the limb that can move water posteriorly and increasing the velocity of the distal portion of the forelimb. These aspects of swimming kinematics in softshells should increase forelimb thrust production and suggest that the forelimbs make more substantial contributions to forward thrust in softshell turtles than in sliders. Spiny softshells also restrict forelimb movements to a much narrower dorsoventral and anteroposterior range than sliders throughout the stroke, thereby helping to minimize limb movements potentially extraneous to forward thrust production. These comparisons demonstrate considerable diversity in the forelimb kinematics of turtles that swim using rowing motions of the limbs and suggest that the evolution of turtle forelimb mechanics produced a variety of contrasting solutions for aquatic specialization

Heads or Tails: Do Stranded Fish (Mosquitofish, <i>Gambusia affinis</i>) Know Where They Are on a Slope and How to Return to the Water?

<div><p>Aquatic vertebrates that emerge onto land to spawn, feed, or evade aquatic predators must return to the water to avoid dehydration or asphyxiation. How do such aquatic organisms determine their location on land? Do particular behaviors facilitate a safe return to the aquatic realm? In this study, we asked: will fully-aquatic mosquitofish (<i>Gambusia affinis</i>) stranded on a slope modulate locomotor behavior according to body position to facilitate movement back into the water? To address this question, mosquitofish (n = 53) were placed in four positions relative to an artificial slope (30° inclination) and their responses to stranding were recorded, categorized, and quantified. We found that mosquitofish may remain immobile for up to three minutes after being stranded and then initiate either a “roll” or a “leap”. During a roll, mass is destabilized to trigger a downslope tumble; during a leap, the fish jumps up, above the substrate. When mosquitofish are oriented with the long axis of the body at 90° to the slope, they almost always (97%) initiate a roll. A roll is an energetically inexpensive way to move back into the water from a cross-slope body orientation because potential energy is converted back into kinetic energy. When placed with their heads toward the apex of the slope, most mosquitofish (>50%) produce a tail-flip jump to leap into ballistic flight. Because a tail-flip generates a caudually-oriented flight trajectory, this locomotor movement will effectively propel a fish downhill when the head is oriented up-slope. However, because the mass of the body is elevated against gravity, leaps require more mechanical work than rolls. We suggest that mosquitofish use the otolith-vestibular system to sense body position and generate a behavior that is “matched” to their orientation on a slope, thereby increasing the probability of a safe return to the water, relative to the energy expended.</p></div

During the experimental trials, most (39 out of 51) mosquitofish (Gambusia affinis) rolled downslope in response to stranding.

<p>Columns represent the number of responses recorded for a given behavior: tail-flip jumps (a type of leap, n = 9), C-leaps (n = 3), J-rolls (n = 9), and C-rolls (n = 30).</p

Male (n = 11) and female (n = 11) mosquitofish (<i>Gambusia affinis</i>) produced only rolls (and never leaps) in response to being stranded with the dorsal aspect of the body oriented toward the top of the slope (Fisher’s Exact test df = 1, n = 21, <i>p</i> = 1); however, male fish produced two types of rolls, whereas females only produced C-rolls.

<p>Although females tended to fail to reach the bottom of the arena more often than males (B), males and females were not statistically different in this ability (Fisher’s Exact test df = 1, n = 22, <i>p</i> = 0.395).</p

Mosquitofish (<i>Gambusia affinis</i>) placed in both perpendicular-to-the-slope (n = 33) and parallel-to-the-slope (n = 18) body orientations moved downslope within the filming arena to produce a mean response trajectory of ∼0° (upper panel).

<p>However, although both movement classes (leaps vs. rolls) performed in response to stranding generated similar mean response trajectories, leaps (n = 12) were characterized by a larger variance in movement trajectory (lower panel). Rolls (n = 39) were characterized by a smaller variance in movement trajectory and roll-type behaviors were more likely to move a mosquitofish directly down the center of the arena (lower panel); see text for additional details.</p

There is little effect of body size on latency and landing times for mosquitofish (<i>Gambusia affinis</i>) stranded on a slope.

<p>There was no monotonic relationship between body size and the time to respond to stranding as measured by latency time: (A) body mass vs. latency time and (B) standard length vs. latency time. There was a weak monotonic relationship between body size and the total duration of the movement produced in response to stranding as measured by landing time: (C) body mass vs. landing time and (D) standard length vs. landing time. Relationships between size and timing were assessed using Spearman’s rank correlation analysis under the <i>a priori</i> hypothesis that larger fish are slower and the null hypothesis of no change in timing with size; see text for additional details.</p

Mosquitofish (<i>Gambusia affinis</i>) produced four distinct behavioral responses to being stranded on a slope: tail-flip jumps (a type of leap), C-leaps, J-rolls, and C-rolls.

<p>During leaps (tail-flip jumps and C-leaps), mosquitofish produced sufficient momentum to elevate the body above the substrate. During rolls (C-rolls and J-rolls), axial body movements destabilized the fish’s mass, enabling the fish to tumble downslope.</p

Initial body orientation was associated with the production of certain behaviors (leaps vs. rolls) when mosquitofish (<i>Gambusia affinis</i>) were stranded on a slope, but movement outcome (success vs. failure) was independent of body orientation and movement class.

<p>(A) When placed with the body’s long axis perpendicular (at 90°) to the slope (n = 32), mosquitofish were more likely to produce a roll than a leap (Fisher’s Exact test, df = 1, n = 51, <i>p</i> = 0.00002); in contrast, when mosquitofish were placed with the body’s long axis parallel to the slope (n = 19), rolls and leaps occurred at approximately the same frequency. (B) The probability of successfully moving downslope was similar from either initial body orientation (Fisher’s Exact test, df = 1, n = 53, <i>p</i> = 0.779). (C) The probability of successfully moving downslope was also similar for both leap and roll behaviors (Fisher’s Exact test, df = 1, n = 51, <i>p</i> = 0.497). See text for additional details.</p

An artificial slope apparatus was used to examine the response of individual mosquitofish (<i>Gambusia affinis</i>) to being stranded on land.

<p>(A) A photography armature held a digital camcorder and commercial-grade LED lights directly over a plastic box that was filled with damp sand and positioned at 30° inclination. Fish were placed on the damp sand and the response to stranding was recorded with the digital camera to a flash memory card. (B) Four initial body positions were used in the slope trials; for two of these positions, the long axis of the body was oriented perpendicular (at 90°) to the slope (dorsal-aspect up-slope and ventral-aspect up-slope); for the other two positions, the long axis of the body was oriented parallel to the slope (cranial-aspect up-slope and caudal-aspect up-slope). One trial at a randomly assigned body position was conducted for each individual included in the study, with a minimum of n = 9 for a given position and a total n = 53; see text for details.</p

Mosquitofish (<i>Gambusia affinis</i>) responded similarly to being stranded in ventral-aspect up-slope (n = 11) and dorsal-aspect up-slope (n = 21) body positions, but produced different behaviors in response to being stranded in cranial-end up-slope vs. caudal-end up-slope body positions.

<p>When stranded cranial-end up-slope (n = 9), mosquitofish most often produced tail-flip jumps. When mosquitofish were stranded caudal-end up-slope (n = 10), all four behaviors were equally likely to occur (that is, each behavior occurred ∼25% of the time).</p