Sensory-evoked turning locomotion in red-eared turtles: kinematic analysis and electromyography (original) (raw)
Related papers
Journal of Experimental Biology, 2013
Animals that swim using appendages do so by way of rowing and/or flapping motions. Often considered discrete categories, rowing and flapping are more appropriately regarded as points along a continuum. The pig-nosed turtle, Carettochelys insculpta, is unusual in that it is the only freshwater turtle to have limbs modified into flippers and swim via synchronous forelimb motions that resemble dorsoventral flapping, traits that evolved independently from their presence in sea turtles. We used high-speed videography to quantify forelimb kinematics in C. insculpta and a closely related, highly aquatic rower (Apalone ferox). Comparisons of our new data to those previously collected for a generalized freshwater rower (Trachemys scripta) and a flapping sea turtle (Caretta caretta) allow us to (1) more precisely quantify and characterize the range of limb motions used by flappers versus rowers, and (2) assess whether the synchronous forelimb motions of Carettochelys insculpta can be classified as flapping (i.e. whether they exhibit forelimb kinematics and angles of attack more similar to closely related rowing species, or more distantly related flapping sea turtles). We found that the forelimb kinematics of previously recognized rowers (T. scripta and A. ferox) were most similar to each other, but that those of Carettochelys were more similar to rowers than to flapping Caretta. Nevertheless, of the three freshwater species, Carettochelys was most similar to flapping Caretta. "Flapping" in Carettochelys is achieved through very different humeral kinematics than in Caretta, with Carettochelys exhibiting significantly more anteroposterior humeral motion and protraction, and significantly less dorsoventral humeral motion and depression. Based on several intermediate kinematic parameters and angle of attack data, Carettochelys may in fact represent a synchronous rower or hybrid rower-flapper, suggesting that traditional views of Carettochelys as a flapper should be revised. more common and ancestral form of swimming in turtles (Joyce and Gauthier, 2004) and has 1 been reported as the exclusive swimming mode for all but one freshwater species (Fig. 1). In 1 rowing turtles, the forelimb of one side moves essentially in phase with the contralateral 1 hindlimb, so that forelimbs (and hindlimbs) of opposite sides move asynchronously (Pace et al., 1 2001; Rivera et al., 2006; Rivera and Blob, 2010; Rivera, G. et al., 2011). Rowing species also 1 tend to possess moderate to extensive webbing between the digits of the forelimb and hindlimb 1 (Pace et al., 2001) [i.e. distally expanded and paddle-shaped (Walker and Westneat, 2002b)] 1 (Fig. 2). Synchronous flapping is a much rarer locomotor style among turtles, definitively 1 employed by the seven extant species of sea turtle (Wyneken, 1997) (Fig. 1). Flapping turtles swim via synchronous motions of forelimbs that have been modified into flat, elongate, semi-1 rigid flippers [i.e. distally tapering wing-like appendages (Walker and Westneat, 2002b)] (Fig. 1 2). Foreflippers may produce thrust on both upstroke and downstroke, but the hindlimbs have a 1 negligible propulsive role (Walker, 1971, 1973; Davenport et al., 1984; Renous and Bels, 1993; of T. scripta) and dorsoventral (less than a third that of T. scripta) motions of the forelimb (Pace 1 et al., 2001). These findings indicate that in addition to differences in kinematics between modes 1 of locomotion (i.e. flapping versus rowing), significant variation can also exist within locomotor 1 modes. Finally, the lack of data on the angle of attack of limbs, for all but a few species of sea 1 turtle (Davenport et al., 1984) , limits the ability to fully interpret the hydrodynamic significance 1 of kinematic results found in the literature. 1 The goals of this study were to (1) examine forelimb kinematics within and between 1 locomotor modes across turtle species to more precisely quantify and characterize the range of 1 limb motions used by flappers and rowers, and (2) determine how Carettochelys insculpta uses 1 synchronous forelimb movements to swim, allowing us to evaluate whether the limb motions 1 displayed by this distinctive freshwater species are more strongly correlated with its phylogenetic 1 relationships to other species, or its locomotor mode (i.e. synchronous use of the foreflippers).
The Journal of Experimental Biology, 2011
Novel functions in animals may evolve through changes in morphology, muscle activity or a combination of both. The idea that new functions or behavior can arise solely through changes in structure, without concurrent changes in the patterns of muscle activity that control movement of those structures, has been formalized as the neuromotor conservation hypothesis. In vertebrate locomotor systems, evidence for neuromotor conservation is found across evolutionary transitions in the behavior of terrestrial species, and in evolutionary transitions from terrestrial species to flying species. However, evolutionary transitions in the locomotion of aquatic species have received little comparable study to determine whether changes in morphology and muscle function were coordinated through the evolution of new locomotor behavior. To evaluate the potential for neuromotor conservation in an ancient aquatic system, we quantified forelimb kinematics and muscle activity during swimming in the loggerhead sea turtle, Caretta caretta. Loggerhead forelimbs are hypertrophied into wing-like flippers that produce thrust via dorsoventral forelimb flapping. We compared kinematic and motor patterns from loggerheads with previous data from the redeared slider, Trachemys scripta, a generalized freshwater species exhibiting unspecialized forelimb morphology and anteroposterior rowing motions during swimming. For some forelimb muscles, comparisons between C. caretta and T. scripta support neuromotor conservation; for example, the coracobrachialis and the latissimus dorsi show similar activation patterns. However, other muscles (deltoideus, pectoralis and triceps) do not show neuromotor conservation; for example, the deltoideus changes dramatically from a limb protractor/elevator in sliders to a joint stabilizer in loggerheads. Thus, during the evolution of flapping in sea turtles, drastic restructuring of the forelimb was accompanied by both conservation and evolutionary novelty in limb motor patterns.
2011
Novel functions in animals may evolve through changes in morphology, muscle activity or a combination of both. The idea that new functions or behavior can arise solely through changes in structure, without concurrent changes in the patterns of muscle activity that control movement of those structures, has been formalized as the neuromotor conservation hypothesis. In vertebrate locomotor systems, evidence for neuromotor conservation is found across evolutionary transitions in the behavior of terrestrial species, and in evolutionary transitions from terrestrial species to flying species. However, evolutionary transitions in the locomotion of aquatic species have received little comparable study to determine whether changes in morphology and muscle function were coordinated through the evolution of new locomotor behavior. To evaluate the potential for neuromotor conservation in an ancient aquatic system, we quantified forelimb kinematics and muscle activity during swimming in the loggerhead sea turtle, Caretta caretta. Loggerhead forelimbs are hypertrophied into wing-like flippers that produce thrust via dorsoventral forelimb flapping. We compared kinematic and motor patterns from loggerheads with previous data from the redeared slider, Trachemys scripta, a generalized freshwater species exhibiting unspecialized forelimb morphology and anteroposterior rowing motions during swimming. For some forelimb muscles, comparisons between C. caretta and T. scripta support neuromotor conservation; for example, the coracobrachialis and the latissimus dorsi show similar activation patterns. However, other muscles (deltoideus, pectoralis and triceps) do not show neuromotor conservation; for example, the deltoideus changes dramatically from a limb protractor/elevator in sliders to a joint stabilizer in loggerheads. Thus, during the evolution of flapping in sea turtles, drastic restructuring of the forelimb was accompanied by both conservation and evolutionary novelty in limb motor patterns.
Journal of Experimental Biology, 2010
SUMMARY Turtles use their limbs during both aquatic and terrestrial locomotion, but water and land impose dramatically different physical requirements. How must musculoskeletal function be adjusted to produce locomotion through such physically disparate habitats? We addressed this question by quantifying forelimb kinematics and muscle activity during aquatic and terrestrial locomotion in a generalized freshwater turtle, the red-eared slider (Trachemys scripta), using digital high-speed video and electromyography (EMG). Comparisons of our forelimb data to previously collected data from the slider hindlimb allow us to test whether limb muscles with similar functional roles show qualitatively similar modulations of activity across habitats. The different functional demands of water and air lead to a prediction that muscle activity for limb protractors (e.g. latissimus dorsi and deltoid for the forelimb) should be greater during swimming than during walking, and activity in retractors (...
Biology Letters, 2013
Changes in muscle activation patterns can lead to new locomotor modes; however, neuromotor conservation-the evolution of new forms of locomotion through changes in structure without concurrent changes to underlying motor patterns-has been documented across diverse styles of locomotion. Animals that swim using appendages do so via rowing (anteroposterior oscilations) or flapping (dorsoventral oscilations). Yet few studies have compared motor patterns between these swimming modes. In swimming turtles, propulsion is generated exclusively by limbs. Kinematically, turtles swim using multiple styles of rowing (freshwater species), flapping (sea turtles) and a unique hybrid style with superficial similarity to flapping by sea turtles and characterized by increased dorsoventral motions of synchronously oscillated forelimbs that have been modified into flippers (Carettochelys insculpta). We compared forelimb motor patterns in four species of turtle (two rowers, Apalone ferox and Trachemys scripta; one flapper, Caretta caretta; and Carettochelys) and found that, despite kinematic differences, motor patterns were generally similar among species with a few notable exceptions: specifically, presence of variable bursts for pectoralis and triceps in Trachemys (though timing of the non-variable pectoralis burst was similar), and the timing of deltoideus activity in Carettochelys and Caretta compared with other taxa. The similarities in motor patterns we find for several muscles provide partial support for neuromotor conservation among turtles using diverse locomotor styles, but the differences implicate deltoideus as a prime contributor to flapping limb motions.
The pattern of motor coordination underlying the roll in the lamprey
Journal of Experimental Biology, 2003
The lamprey swims by caudally directed lateral undulations of its body. During swimming the animal is oriented with its dorsal side up, and any deviation from this posture (roll tilt) elicits a corrective motor response aimed at restoring the normal orientation. Video recording was used to study the kinematic pattern of the response to a 90°roll tilt imposed in the intact lamprey. The corrective responses were associated with specific modifications of the swimming movements. The plane of locomotor undulations deviated from the normal, i.e. frontal plane in one direction at the beginning of the rotation and in the opposite direction at its end. A similar motor pattern was also observed in the anterior part of the body of lampreys in which the spinal cord had been transected in the mid-body area, when performing postural corrections. It could also be observed during roll turns performed by lampreys after a rostral hemisection of the spinal cord. We argue that these modifications of the locomotor pattern generate the moments of force necessary for initiation and termination of the corrective roll turn. Possible neuronal mechanisms causing the corrective movements are discussed.
Responses of hatchling sea turtles to rotational displacements
Journal of Experimental Marine Biology and Ecology, 2003
After emerging from underground nests, sea turtle hatchlings migrate through the surf zone and out to the open ocean. During this migration, both waves and water currents can disrupt hatchling orientation by unpredictably rotating the turtles away from their migratory headings. In addition, waves cause turtles to roll and pitch, temporarily impeding forward swimming by forcing the hatchlings into steeply inclined positions. To maintain seaward orientation and remain upright in the water column, hatchlings must continuously compensate for such displacements. As a first step toward determining how this is achieved, we studied the responses of loggerhead (Caretta caretta L.) sea turtle hatchlings to rotational displacements involving yaw, roll, and pitch. Hatchlings responded to rotations in the horizontal plane (yaw) by extending the rear flipper on the side opposite the direction of rotation. Thus, the flipper presumably acts as a rudder to help turn the turtle back toward its original heading. Turtles responded to rotations in the roll plane with stereotypic movements of the front flippers that act to right the hatchlings with respect to gravity. Finally, hatchlings responded to rotations in the pitch plane with movements of the hind flippers that appear likely to curtail or counteract the pitching motion. Thus, the results of these experiments imply that young sea turtles emerge from their nests possessing a suite of stereotypic behavioral responses that function to counteract rotational displacements, enable the animals to maintain equilibrium, and facilitate efficient movement toward the open sea.