SUMMARYAnimals 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 with 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 C. 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 C. insculpta were more similar to rowers than to flapping C. caretta. Nevertheless, of the three freshwater species, C. insculpta was most similar to flapping C. caretta. ʻFlappingʼ in C. insculpta is achieved through humeral kinematics very different from those in C. caretta, with C. insculpta 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, C. insculpta may in fact represent a synchronous rower or hybrid rower-flapper, suggesting that traditional views of C. insculpta as a flapper should be revised. Supplementary material available online at

SUMMARYTurtles 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 (e.g. coracobrachialis and pectoralis for the forelimb) should be greater during walking than during swimming. Differences between aquatic and terrestrial forelimb movements are reflected in temporal modulation of muscle activity bursts between environments, and in some cases the number of EMG bursts as well. Although patterns of modulation between water and land are similar between the fore-and hindlimb in T. scripta for propulsive phase muscles (retractors), we did not find support for the predicted pattern of intensity modulation, suggesting that the functional demands of the locomotor medium alone do not dictate differences in intensity of muscle activity across habitats. Supplementary material available online at

SUMMARYNovel 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. Supplementary material available online at

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SUMMARYHydrodynamic stability is the ability to resist recoil motions of the body produced by destabilizing forces. Previous studies have suggested that recoil motions can decrease locomotor performance, efficiency and sensory perception and that swimming animals might utilize kinematic strategies or possess morphological adaptations that reduce recoil motions and produce more stable trajectories. We used high-speed video to assess hydrodynamic stability during rectilinear swimming in the freshwater painted turtle (Chrysemys picta). Parameters of vertical stability (heave and pitch) were non-cyclic and variable, whereas measures of lateral stability (sideslip and yaw) showed repeatable cyclic patterns. In addition, because freshwater and marine turtles use different swimming styles, we tested the effects of propulsive mode on hydrodynamic stability during rectilinear swimming, by comparing our data from painted turtles with previously collected data from two species of marine turtle (Caretta caretta and Chelonia mydas). Painted turtles had higher levels of stability than both species of marine turtle for six of the eight parameters tested, highlighting potential disadvantages associated with 'aquatic flight'. Finally, available data on hydrodynamic stability of other rigid-bodied vertebrates indicate that turtles are less stable than boxfish and pufferfish.

Synopsis Though ultimately descended from terrestrial amniotes, turtles have deep roots as an aquatic lineage and are quite diverse in the extent of their aquatic specializations. Many taxa can be viewed as ''on the fence'' between aquatic and terrestrial realms, whereas others have independently hyperspecialized and moved ''all in'' to aquatic habitats. Such differences in specialization are reflected strongly in the locomotor system. We have conducted several studies to evaluate the performance consequences of such variation in design, as well as the mechanisms through which specialization for aquatic locomotion is facilitated in turtles. One path to aquatic hyperspecialization has involved the evolutionary transformation of the forelimbs from rowing, tubular limbs with distal paddles into flapping, flattened flippers, as in sea turtles. Prior to the advent of any hydrodynamic advantages, the evolution of such flippers may have been enabled by a reduction in twisting loads on proximal limb bones that accompanied swimming in rowing ancestors, facilitating a shift from tubular to flattened limbs. Moreover, the control of flapping movements appears related primarily to shifts in the activity of a single forelimb muscle, the deltoid. Despite some performance advantages, flapping may entail a locomotor cost in terms of decreased locomotor stability. However, other morphological specializations among rowing species may enhance swimming stability. For example, among highly aquatic pleurodiran turtles, fusion of the pelvis to the shell appears to dramatically reduce motions of the pelvis compared to freshwater cryptodiran species. This could contribute to advantageous increases in aquatic stability among predominantly aquatic pleurodires. Thus, even within the potential constraints of a body plan in which the body is encased by a shell, turtles exhibit diverse locomotor capacities that have enabled diversification into a wide range of aquatic habitats.

Previous studies of limb bone loading in walking turtles indicate that the ground reaction force exerts a flexor moment at the ankle during stance, requiring extensor muscle activity to maintain joint equilibrium. Of four proposed ankle extensors in turtles, two (gastrocnemius medialis, pronator profundus) originate on the tibia and fibula, respectively, while the other two (flexor digitorum longus, gastrocnemius lateralis) originate from the distal femur, crossing the flexor aspect of the knee and potentially eliciting compensatory forces from antagonist knee extensor muscles that could contribute to femoral stress. Published bone stress models assume all four proposed ankle extensors are active during stance in turtles. However, if only the ankle extensors that cross the knee were active then femoral stresses might be higher than predicted by published models, whereas if only extensors that do not cross the knee were active then femoral stresses might be lower than predicted. We analyzed synchronized footfall and electromyographic activity patterns in slider turtles (Trachemys scripta) and found that all four proposed ankle extensors were active during at least part of stance phase in most individuals, corroborating bone stress models. However, activation patterns were complex, with multiple bursts in many ankle extensors that frequently persisted into swing phase. In addition, two hypothesized ankle flexors (tibialis anterior, extensor digitorum communis) were frequently active during stance. This might increase the joint moment that ankle extensors must counter, elevating the forces they transfer across the knee joint and, thereby, raising femoral stress. Recognition of these activity patterns may help reconcile differences between evaluations of loads on turtle limbs based on force platform versus in vivo strain studies. Moreover, while some variation in motor patterns for the distal hind limbs of turtles may reflect functional compartmentalization of muscles, it may also indicate flexibility in the control of their limb movements.

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.