Forelimb kinematics during swimming in the pig-nosed turtle, Carettochelys insculpta, compared with other turtle taxa: rowing versus flapping, convergence versus intermediacy

Abstract

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 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. 'Flapping' 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.

Fig. 1.

Recent phylogeny of turtles based on 14 nuclear genes, showing familial relationships. Solid lines indicate asynchronous anteroposterior rowing motions of forelimbs and hindlimbs for swimming (presumptive ancestral condition), dashed line indicates synchronous dorsoventral flapping motions of forelimbs for swimming in sea turtles (derived), and dotted line indicates swimming in Carettochelys insculpta (the only extant member of the family Carettochelyidae, and the only freshwater turtle species with forelimbs modified into flippers that swims using synchronous forelimb motions). The family Emydidae includes Trachemys scripta, Chelonioidea includes Caretta caretta and Trionychoidea includes Apalone ferox. Branch lengths do not reflect time since divergence. Time since divergence of focal lineages is indicated at nodes: 1=175 mya; 2=155 mya; 3=94 mya. Phylogeny is based on Barley et al. (Barley et al., 2010). Estimates of divergence times are based on Near et al. (Near et al., 2005).

Fig. 2.

Ventral view of the left forelimb showing skeletal anatomy and outlines of the paddle/flipper in (A) Apalone ferox, (B) Trachemys scripta, (C) Carettochelys insculpta and (D) Caretta caretta. Outlines of the paddle/flipper end mid-humerus to indicate where the limb protrudes from the shell. Stippling on the humerus of A. ferox (A) indicates the depression of the intertubercular fossa. The humerus of T. scripta (B) is rotated 90 deg posteriorly, providing a posterior view that highlights the dorsally oriented curvature of the bone. The radius is anterior, lateral and ventral to the ulna for each species. Digits I–V are indicated. Images are redrawn and modified from source material [A. ferox (Sheil, 2003), T. scripta (Hall, 2000; Sheil and Portik, 2008), C. insculpta (Walther, 1921) and C. caretta (Wyneken, 2001; Sanchez-Villagra et al., 2007)].

Fig. 3.

Representative still images from lateral (A,C) and ventral (B,D) videos showing landmarks digitized for kinematic analysis. (A,B) Apalone ferox. Points 1–9 are the same in lateral and ventral view; points 10–13 are only visible in ventral view. Landmarks include: 1, tip of the nose; 2, shoulder; 3, elbow; 4, wrist; 5, digit 1; 6, digit 3; 7, digit 5; 8, anterior point on bridge; 9, posterior point on bridge; 10, point on left side of plastron; 11, point on right side of plastron; 12, posterior point on plastron; and 13, anterior point on plastron. (C,D) Carettochelys insculpta. Points 1–8 are the same in lateral and ventral view; points 9–12 are only visible in ventral view. Landmarks include: 1, tip of the nose; 2, shoulder; 3, elbow; 4, digit 1; 5, digit 3; 6, digit 5; 7, anterior point on bridge; 8, posterior point on bridge; 9, point on left side of plastron; 10, point on right side of plastron; 11, posterior point on plastron; and 12, anterior point on plastron. A representative video of swimming in C. insculpta is provided in supplementary material Movie 1.

Fig. 4.

Mean kinematic profiles of swimming in four species of turtle: Carettochelys insculpta (red squares), rowing Apalone ferox (inverted blue triangles), rowing Trachemys scripta (green triangles) and flapping Caretta caretta (black circles). Data for T. scripta were provided by Rivera and Blob (Rivera and Blob, 2010). Data for C. caretta were provided by Rivera et al. (Rivera, A. R. V. et al., 2011). Each trial was normalized to the same duration and angle values were interpolated to represent 0–100% of the limb cycle. For C. insculpta, A. ferox and T. scripta, the limb cycle is defined as protraction of the humerus followed by retraction; for C. caretta, the limb cycle is defined as elevation of the humerus followed by depression. Mean ± s.e.m. angle values are plotted for every third increment (every 3% through the cycle) for all individuals. Solid vertical lines demarcate the switch from protraction to retraction in A. ferox and T. scripta at 43% of the limb cycle. Dashed vertical lines indicate the switch from protraction to retraction in C. insculpta and from elevation to depression in C. caretta at 51% of the limb cycle. (A) Humeral protraction and retraction (i.e. angle from the transverse plane). An angle of 0 deg indicates that the humerus is perpendicular to the midline of the turtle, while an angle of 90 deg indicates a fully protracted forelimb with the distal end of the humerus directed anteriorly (an angle of –90 deg would indicate a fully retracted forelimb with the distal tip of the humerus directed posteriorly). (B) Humeral elevation and depression (i.e. angle from the horizontal plane). An angle of 0 deg indicates that the humerus is in the horizontal plane. Angles greater than zero indicate elevation above the horizontal (distal end above proximal end) and negative angles indicate depression of the humerus (distal end lower than proximal end). Peak elevation is coincident with peak protraction for T. scripta and C. caretta, meaning that limb protraction happens at the same time as elevation and retraction is concurrent with depression. (C) Elbow flexion and extension. Extension is indicated by larger angles and flexion is indicated by smaller angles. An angle of 0 deg indicates complete flexion, 180 deg indicates a fully extended elbow, and 90 deg indicates that the humerus is perpendicular to the radius and ulna. (D) Forefoot orientation angle is calculated as the angle between a vector pointing forwards along the anteroposterior midline (also the path of travel) and a vector emerging from the palmar surface of a plane defined by the tips of digits 1 and 5 and the elbow; this angle is transformed by subtracting 90 deg from each value. A high-drag orientation of the forefoot paddle with the palmar surface of the paddle directed opposite the direction of travel (and in the same direction as the flow of water) is indicated by a feathering angle of 90 deg, and a perfect low-drag orientation of the forefoot paddle is indicated by a feathering angle of 0 deg.

Fig. 5.

Plot of the first two axes of a principal components analysis of swimming kinematics for eight variables in four species of turtle: Carettochelys insculpta (red squares), rowing Apalone ferox (blue inverted triangles), rowing Trachemys scripta (green triangles) and flapping Caretta caretta (black circles). The first two axes explain 56.9% of the total variation in forelimb swimming kinematics. See Table 2 for axis loadings.

Fig. 6.

Lateral view of the paths taken by the distal-most point of the forelimb (digit 3; tip of the flipper in Carettochelys insculpta and Caretta caretta) for C. insculpta (red squares), Apalone ferox (blue inverted triangles), Trachemys scripta (green triangles) and C. caretta (black circles) showing the amount of anteroposterior and dorsoventral motion relative to the turtle’s body throughout the limb cycle. Coordinate positions of X and Z throughout the swimming cycle were smoothed and interpolated to 101 points. Paths are the average of all trials for each species, and have been scaled to unit size to facilitate comparisons of trajectories. Paths start at the origin. Position of the shoulder relative to the path is indicated for each species with a color-coded cross. Despite greater dorsoventral motion in T. scripta, the trajectories of A. ferox and T. scripta (rowers) are both horizontal. Caretta caretta (flapper) approaches (but does not attain) a vertical trajectory. Finally, in C. insculpta, the trajectory of the tip of the flipper is intermediate between A. ferox/T. scripta and C. caretta. The ratios of dorsoventral to anteroposterior motion of digit 3 designate A. ferox, T. scripta and C. insculpta as rowers (ratios less than 1: DV/AP=0.23±0.01, 0.29±0.01 and 0.58±0.03, respectively) and C. caretta as a flapper with a ratio greater than 1 (DV/AP=1.47±0.13).

Fig. 7.

Comparison of hydrodynamic angle of attack of the forelimb at mid-phase for protraction/elevation (A) and retraction/depression (B) in four species of turtle. For each trial, a representative midstroke protraction/elevation value was calculated as the mean of the five central values during this phase, and a representative midstroke retraction/depression value was calculated as the mean of the five central values during this phase. Box plots are based on the distributions of these representative values: solid lines indicate medians, dashed lines indicate means, box margins represent 50th and 75th percentiles, whiskers show 10th and 90th percentiles, and circles show 5th and 95th percentiles. Angle of attack was calculated as the angle between a vector representing the path of motion of the tip of the forelimb (digit 3) and a vector emerging from the palmar surface of a plane defined by the tips of digits 1 and 5 and the elbow. Small angular values indicate a shallow angle between the path of limb motion and the forefoot; an angle of 0 deg during protraction/elevation indicates the leading edge of the forefoot is oriented perfectly along the path of motion in a low-drag orientation. Maximum drag orientation of the forefoot paddle relative to the path of motion of the forefoot is indicated by an angle of 90 deg during protraction/elevation, and an angle of –90 deg during retraction/depression. Results of post hoc multiple comparison Tukey’s tests are indicated with solid black lines above the boxplots. During protraction/elevation, two groups were identified; rowing Apalone ferox and Trachemys scripta do not differ from one another, and Carettochelys insculpta groups with flapping Caretta caretta. However, during retraction/depression, C. insculpta groups with rowing species.