Integrative and Comparative Biology Integrative and Comparative Biology, Pp

Integrative and Comparative Biology Integrative and Comparative Biology, pp. 1–16 doi:10.1093/icb/icab021 Society for Integrative and Comparative Biology

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The Role of the Tail or Lack Thereof in the Evolution of Tetrapod Aquatic Propulsion Frank E. Fish,1,* Natalia Rybczynski,† George V. Lauder‡ and Christina M. Duff*

*Department of Biology, West Chester University, West Chester, PA 19383, USA; †Department of Palaeobiology, Canadian Museum of Nature, Ottawa, ON, Canada K1P 6P4; ‡Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA From the symposium “An evolutionary tail: Evo-Devo, structure, and function of post-anal appendages” presented at the virtual annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2020.

1E-mail: [email protected]

Synopsis Secondary aquatic vertebrates exhibit a diversity of swimming modes that use paired limbs and/or the tail. Various secondarily aquatic tetrapod clades, including amphibians, reptiles, and mammals use transverse undulations or oscillations of the tail for swimming. These movements have often been classified according to a kinematic gradient that was established for fishes but may not be appropriate to describe the swimming motions of tetrapods. To understand the evolution of movements and design of the tail in aquatic tetrapods, we categorize the types of tails used for swimming and examine swimming kinematics and hydrodynamics. From a foundation of a narrow, elongate ancestral tail, the tails used for swimming by aquatic tetrapods are classified as tapered, keeled, paddle, and lunate. Tail undulations are associated with tapered, keeled, and paddle tails for a diversity of taxa. Propulsive undulatory waves move down the tail with increasing amplitude toward the tail tip, while moving posteriorly at a velocity faster than the anterior motion of the body indicating that the tail is used for thrust generation. Aquatic propulsion is associated with the transfer of momentum to the water from the swimming movements of the tail, particularly at the trailing edge. The addition of transverse extensions and flattening of the tail increases the mass of water accelerated posteriorly and affects vorticity shed into the wake for more aquatically adapted animals. Digital Particle Image Velocimetry reveals that the differences were exhibited in the vortex wake between the morphological and kinematic extremes of the alligator with a tapering undulating tail and the dolphin with oscillating wing-like flukes that generate thrust. In addition to exploring the relationship between the shape of undulating tails and the swimming performance across aquatic tetrapods, the role of tail reduction or loss of a tail in aquatic-tetrapod swimming was also explored. For aquatic tetrapods, the reduction would have been due to factors including locomotor and defensive specializations and phylogenetic and physiological constraints. Possession of a thrust-generating tail for swimming, or lack thereof, guided various lineages of secondarily aquatic vertebrates into different evolutionary trajectories for effective aquatic propulsion (i.e., speed, efficiency, and acceleration).

Introduction 1999), anuran tadpoles (Wassersug and Hoff 1985; Tails are ubiquitous as propulsive organs among ver- Liu et al. 1996), urodele amphibians (Ashley-Ross tebrates for swimming. Animals using the tail to swim and Bechtel 2004), snakes (Jayne 1985; Brischoux are generally classified as undulatory. Undulatory and Shine 2011), lizards (Ringma and Salisbury swimmers pass a series of waves that can be generated 2014), crocodilians (Manter 1940; Fish 1984), dino- in the body and move posteriorly down the tail. saurs (Ibrahim et al. 2020), mosasaurs (Lindgren et al. Undulatory swimming vertebrates include bony and 2010), ichthyosaurs (Riess 1986; Motani et al. 1996; cartilaginous fishes (Lindsey 1978; Sfakiotakis et al. Motani 2000; Buchholtz 2001), various semiaquatic

ß The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 2 F. E. Fish et al. mammals (Howell 1930), sirenians (Hartman 1979; quintessential example of evolutionary convergence Kojeszewski and Fish 2007), and cetaceans (Fish displayed by lamnid sharks, ichthyosaurs of the 1998a). Thunnosauria, and oceanic dolphins of the Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 One of the definitive chordate characteristics is the Delphinidae (Howell 1930; Hildebrand 1995; post-anal tail. The legacy of this caudal appendage Motani 1999; Liem et al. 2001; Kardong 2019; from the early chordates is its use as a propulsive Moon 2019; Fish submitted for publication). All apparatus in many vertebrate clades to move these groups independently developed a high- through the aquatic medium. Swimming by basal performance wing-like, lunate caudal fin. Even semi- chordates originated with serial activation of myo- aquatic mammals (e.g., Castor, Castorocauda, meres to produce a wriggling movement of the body Ornithorhynchus, and Pteronura) display parallelism and tail for swimming (Webb 1973; Stokes 1997; in the flattening of their tails (Howell 1937; Duff and Lacalli 2012). From the basal chordates, movement Fish 2002; Ji et al. 2006). Between terrestrial forms through water by the majority of fishes used body making limited forays into water and these highly and caudal fin (BCF) swimming (Breder 1926; Webb derived aquatic morphologies are a diversity of tail 1975, 1982, 1984; Lindsey 1978; Sfakiotakis et al. designs with varying degrees of performance in re- 1999). Given the importance of speed, long- gard to thrust production and propulsive efficiency. distance swimming, acceleration, and efficiency, the This article examines the evolution of the tail as elaboration of a tail including the development of an aquatic propulsive structure in tetrapods. the caudal fin allowed greater propulsive diversity Although not a comprehensive review, the tails ex- in early vertebrates (Webb 1980). amined are drawn from vertebrate groups that were The majority of research on swimming move- historically terrestrial but became secondarily ments associated with a propulsive tail has focused aquatic. Gutmann (1994) provided a series of illus- on the undulatory-oscillatory gradient displayed by trations indicating the transition of body forms and fishes (see reviews by Breder 1926; Webb 1975, 1978; propulsive modes for secondarily aquatic vertebrates, Lindsey 1978; Blake 1983; Videler 1993; Sfakiotakis but without grounding these alterations in modern et al. 1999). However, the evolution of propulsive hydrodynamic theory. Here, we categorize and ad- tails has occurred independently multiple times in dress the changes in tail morphology in the context a variety of vertebrate clades that went through a of thrust production and propulsive efficiency. The terrestrial phase. interaction of the physical properties of the aqueous In one of the “Great Transformations” in evolu- medium with the hydrodynamics of propulsion most tion, vertebrates moved from an obligate aquatic ex- likely placed high selective pressures on animals istence to terrestrial habits (Dial et al. 2015). The tail attempting to move through the water with speed took on a non-propulsive role with the development and high-energy economy. In addition, we consider of legged locomotion on land (Inger 1962), although lineages with reduced tails and the relationship be- the tail served as the origin for some muscles asso- tween tail reduction/loss and the evolution of limb- ciated with the hind legs. This decreased reliance on based mechanisms for aquatic propulsion. the tail as a propulsive surface by terrestrial species meant that as multiple linages of vertebrates returned Reinventing the water wheel to the water a finned tail would have had to be reinvented. It is the secondary evolution of aquatic Undulatory categories habits by tetrapods that fostered the development of Undulatory propulsive motions are cyclical with tails similar to the earlier fish evolutionary lineages. symmetrically repeating flexion of the body and With the trends to larger body sizes and increased tail, generating a traveling wave during steady swim- need for speed and efficiency in the aquatic realm, ming. In fishes, the traveling wave is generated by the evolution of propulsive tails in secondarily sequential activation of the myomeres that are ar- aquatic tetrapods has culminated in the development ranged serially along the trunk and caudal vertebrae of high performance caudally derived propulsors modified from the original chordate swimming (Flower 1883; Lighthill 1969; Webb and De mechanism. Undulatory swimming has been best de- Buffrenil 1990; Fish 1996). Dealing with the same scribed for BCF swimming in fishes along a kine- physical hurdles and strong selection criteria im- matic gradient that is categorized according to posed by the aquatic environment, secondarily wavelength and proportion of the posterior body aquatic tetrapods converged on similar solutions generating the traveling wave. Propulsive movements with fishes for effective swimming. This “aquatic of wavelengths shorter than an animal’s body length confluence” culminated in what has been the are defined as undulatory; whereas wavelengths Tetrapod tails and aquatic propulsion 3 Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021

Fig. 1 Silhouettes of tetrapods displaying tapering, keeled, paddle, and lunate tails arranged along an undulation–oscillation gradient for tailed propulsion. The animals are (1) salamander, (2) river otter, (3) alligator, (4) muskrat, (5) tadpole, (6) Spinosaurus,(7) giant otter, (8) beaver, (9) manatee, (10) Triassic ichthyosaur, (11) Thunnosauria ichthyosaur, and (12) dolphin. longer than a body length are considered oscillatory swimming for tetrapods and the commonalities of (Breder 1926; Ringma and Salisbury 2014). At its their evolutionary trajectories, the diversity of tail extreme, the oscillatory motions are confined to a morphologies and the associated dynamics of thrust caudal fin that swivels at its base without exhibiting production need to be examined. wave formation (Sfakiotakis et al. 1999). With respect to decreasing proportion of the posterior Diversity of tail morphologies body used to generate propulsive forces for BCF There are four basic tail morphologies for swimming fishes, the classification categories include anguilli- tetrapods. These tail morphologies are associated form (100% of body), subcarangiform (50% of with the degree of thrust production and propulsive body), carangiform (33% of body), and thunniform efficiency (Fig. 1). Tails can be categorized using ba- (caudal fin) (Breder 1926; Webb 1975; Lindsey 1978). sic external anatomical shapes and features as The kinematic classification of BCF fishes has lim- follows. ited utility for tail-swimming tetrapods. In many cases, the tail of tetrapods, which can be half of Tapering tail the total body length, is morphologically distinct An elongate tail that narrows posteriorly to a point. from the rest of the body, and flexing motions of The tail can be round in cross-section or flattened. the body may not produce thrust. In addition, the The tapering tail can be a little modified from the paddling limbs can be used for thrust production. basic tail of terrestrial tetrapods. Examples include Braun and Reif (1982, 1985) produced an extensive crocodilians (Alligator, Crocodylus), monitor lizard listing of swimming modes categorizing all verte- (Varanus), river otters (Lontra, Lutra), salamanders brates, but they still relied upon the classification (Ambystoma, Siren), and water snakes (Natrix). scheme used for fish (Breder 1926; Webb 1975; Lindsey 1978). The only tailed swimming mode Keeled tail that truly groups diverse vertebrates is the thunni- Flattened tail with a prominent continuous fleshy form mode. The thunniform mode has been used to keel along its length. The keel can be located on characterize the analogous and convergent body the dorsal, ventral, or both surfaces of the tail. The form, swimming kinematics, and hydrodynamically keel provides a uniform depth along the majority of derived, lift-based propulsion of scombrid fishes the tail length. The tail tip may be pointed or and lamnid sharks with the addition of rounded. Examples include desmans (Desmana, Thunnosauria ichthyosaurs and cetaceans. For a Galemys), giant otter shrew (Potamogale), muskrat full understanding of the use of the tail for (Ondatra), newts (Ichthyosaura, Notophthalmus), 4 F. E. Fish et al. Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021

Fig. 2 Relationships of posteriorly moving traveling wave with respect to forward movement of swimming beavers (Castor canadensis) on left and giant otter (Pteronura brasiliensis) on the right. The solid lines indicate equivalency of the velocity. Picture inserts show the paddle tails of both species. Image of Pteronura is courtesy of the American Society of Mammalogists. Data are archived at https:// digitalcommons.wcupa.edu/bio_data/6/.

Spinosaurus, tadpoles (Lithobates, Rana), and Triassic than the swimming velocity of the animal (Webb ichthyosaurs (Mixosaurus, Tylosaurus). 1988). Undulatory actions and propulsion by the tail oc- Paddle tail cur even when the animal additionally uses its limbs to paddle (Tarasoff et al. 1972; Fish 1982, 1984). Highly flattened tail with a tail tip broader than the Videos demonstrated that the tail wave moved at a tail base. Examples include beavers (Castor), velocity faster than the forward progression of the Castorocauda, giant otter (Pteronura), manatee beaver (Castor canadensis) and giant river otter (Trichechus), platypus (Ornithorhynchus), and sea (Pteronura brasiliensis)(Supplementary Videos S1 snakes (Laticauda, Pelamis). and S2 and Fig. 2; Duff and Fish 2002; Rybczynski et al. 2005). Both species have a paddle-shaped tail Lunate tail and swim using the tail in combination with simul- Wing-like hydrofoil fins or flukes connected from taneous paddling of the hind feet. Even so, the ve- rest of the body with a narrow caudal peduncle. locity of the tail wave is in-line with other The lunate tail has a sickle-shaped appearance with undulatory tail swimmers (Fig. 3). On average, mea- a broad insertion on the tail that tapers to a point at sured tail-wave speeds for swimming vertebrates are the tips. Typically, the lunate tail displays a swept- 55% greater than the forward velocity of the animal. back design. Examples include cetaceans The evolution of a lunate tail in conjunction with (Balaenoptera, Stenella), dugong (Dugong), a thunniform body design and kinematics can be Thunnosaurian ichthyosaurs (Ichthyosaurus, considered a quantum leap for the generation of Stenopterygius), and mosasaurs (Prognathodon). propulsive thrust in aquatic surroundings. Rather The animals possessing a tapered, keeled, or pad- than undulating the entire length of the tail to pro- dle tail swim by undulation passing traveling waves vide thrust, the relatively stiff lunate tail acts like an down the length of the tail. These waves increase in oscillating hydrofoil to produce the propulsive amplitude to a maximum at the tail tip (Fish 1982, forces. There is a distinct morphological separation 1984, 1994, 1996; Jayne 1985; Wassersug and Hoff of the caudal fin/flukes from the body from the nar- 1985; Frolich and Biewener 1992; Liu et al. 1996; row peduncle region, referred to as “narrow Gillis 1997; Ashley-Ross and Bechtel 2004; necking” (Lighthill 1969). With the propulsor all- Kojeszewski and Fish 2007; Ringma and Salisbury but separated from the body, the lunate tail func- 2014). The traveling waves within the tails create tions as a distinct propeller that is largely indepen- thrust by moving posteriorly at velocities greater dent of the anterior drag-incurring body region Tetrapod tails and aquatic propulsion 5

Added mass effects Undulations of the tail interact with the surrounding Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 water to generate thrust. As each section of the tail is accelerated transversely and longitudinally, the tail section faces caudally at an angle to the mean motion of the body. The water mass adjacent to the accelerated section produces a reaction force with a component in the direction of thrust (Lighthill 1971; Webb 1988; Daniel et al. 1992). For a tail of constant width or depth along its length, the mass of water acted on will be the same for all segments. However, the momentum of the associated mass of water will increase toward the tail tip, where the velocity and amplitude are maximal (Webb 1975). Therefore, undulatory swimming relies on an acceleration reaction for propulsion, resulting from changes in the kinetic energy of the water accelerated by the action of the propulsive body structure (Daniel 1984; Webb 1988). Fig. 3 Comparative tail wave velocities demonstrating thrust The acceleration reaction is dependent on an added production in species swimming by tail undulations. Values above mass (Lighthill 1970; Daniel 1984; Daniel and Webb the line of equivalency (dashed line) indicate thrust production, 1987). whereas equivalent tail wave velocities and swimming velocities indicate no thrust production. Data for fish, alligator, and muskrat Lighthill (1970) calculated the added mass per from Webb (1975) and Fish (1982, 1984). unit length (m) from elongate body theory as

2 (Lighthill 1969, 1970; Fish et al. 1988; Fish and Hui m ¼ krpdT =4; 1991; Fish 1993b, 1998b; Nauen and Lauder 2000, where k is the non-dimensional added mass coeffi- 2001). Joints within the peduncle allow the lunate cient, q is the density of water, and d is the trailing tail to be pitched at angles through the stroke cycle T edge depth. The value of k varies with the eccentric- independent of any body curvature. Control of the ity of cross-sectional geometry of the trailing edge of pitch angle of the hydrofoil permits the lunate tail to the tail (Fig. 4). A flat or elliptical cross-section has manage its angle of attack (Lighthill 1969; Magnuson k ¼ 1, whereas a circular cross-section has k ¼ 0.75, 1978; Fish et al. 1988; Fish 1993b, 1998a). The angle reducing m and the thrust by 25% (Lighthill 1970; of attack is generally small (<20) corresponding to Webb 1978). the deflection of the hydrofoil from the incident A reduction in thrust will also occur due to ta- flow. pering of the tail. A tapered tail comes to a point at its terminus, where dT is effectively zero and so Momentum transfer affects zero mass of water. In such cases, reduced Propulsion through a liquid universe thrust would be derived from more anterior seg- The act of swimming reflects the interaction of a ments on the tail with larger dT but lower ampli- body surface with a fluid environment through an tudes and wave velocities anteriorly compared with exchange of momentum. Propulsion through water the tail tip reduce thrust (Webb 1982). The magni- is the result of the transfer of momentum from the tude of the inertial thrust production is enhanced by motions of the animal to the fluid environment flattening of the undulatory surface and expansion of (Webb 1988). The rate of momentum exchanged be- the caudal tip into a paddle-like shape (Lighthill tween the animal’s propulsor and the water deter- 1969, 1970, 1971; Webb 1978; Sanders et al. 2012). mines the amount of thrust generated (Daniel et al. Certain aquatic mammals exemplify the effects of 1992). Propulsors maximize thrust most efficiently tapering and small dT. The muskrat, Ondatra zibe- by accelerating a large mass of fluid, at a low velocity thicus, undulates its laterally compressed, keeled tail (Alexander 1983). Propulsors, therefore, should be when paddling at the surface of the water. Although large in span and area (Blake 1981; Webb 1988; the tail wave travels faster than the progression of Fish 1993a). A large excursion of the propulsor will the animal (Supplementary Video S3), the tail furthermore accelerate an increased mass of water to accounts for only 1.4% of the total thrust production increase momentum transfer. (Fish 1982, 1984). The muskrat tail stabilizes the 6 F. E. Fish et al.

motions is generated primarily from stiff wing-like extensions at the end of the tail (Webb 1988; Sfakiotakis et al. 1999). The main propulsive force Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 produced by oscillating lunate tails is lift. In lift- based propulsion, the tail is modified as a hydrofoil. Lift arises from asymmetries in the flow around the hydrofoil. The asymmetry generates a pressure difference between the sides of the hydrofoil with a net force normal to the incident flow. Due to both heaving and pitching motions of the hydrofoil-shaped tail, the tail is canted at an angle of attack to the flow (Supplementary Video S4). A lift vector is directed perpendicular to the pathway traversed by the Fig. 4 Added mass coefficient for different tail cross-section hydrofoil that can be resolved into an anteriorly di- configurations and added mass equation, where m is the added rected thrust vector and laterally directed side forces mass, k is the added mass coefficient, q is the density of water, (Weihs and Webb 1983; Fish 1993a). The momen- and dT is the trailing edge depth of the tail with reference to tum imparted to the water by the oscillating hydro- the flat plate with k ¼ 1.0. Cross-sections from left to right are foil takes the form of a wake of a reverse Karman elliptical, flat, elliptical with dorsal and ventral fins, circular with street of thrust-type vortices (see below; Weihs 1972; dorsal and ventral fins, and circular. After Lighthill (1970) and Triantafyllou et al. 2000; Fish et al. 2014; Smits Webb (1978). 2019). body in yaw. Similarly, thrust produced by undula- Comparative hydrodynamics tion of the tail in Lontra would be low compared with its hind foot paddling stroke because the tail Robotic analogs tapers to a narrow tip. The beaver (Castor canaden- The emulation of biological systems by mechanical sis) and the giant otter, Pteronura brasiliensis possess designs to experimentally elucidate performance broad paddle-like tails that when undulated could attributes is facilitated through “robotics-inspired produce large amounts of thrust (Fish 1994, 2001; biology” (Gravish and Lauder 2018). Robotic models Rybczynski et al. 2005). To increase thrust genera- can often be used to test the biological hypothesis tion and acceleration capabilities by expanding dT in that would be very difficult in living animals. By the early evolution of fishes, the caudal fin was en- studying the performance of even highly simplified larged by extension of the trailing-edge fin-flap models of animal anatomy, we can control for inter- (Webb 1980). Similar changes in dT transpired in specific differences and isolate individual traits to the evolution of the caudal propulsor for ichthyo- assess their effect on performance. In addition, using saurs and cetaceans (Motani et al. 1996; Thewissen mechanical systems we can often easily measure 2014). The change in the effective surface and design traits such as thrust and efficiency that can be quite of the propulsive tail from tapered, to keeled to pad- challenging to quantify in moving animals. dle, and finally to lunate is expressed in the embry- To directly examine the effect of different tail onic development of dolphins in a manner similar to shapes on swimming performance two-dimensional the evolutionary transition of cetaceans (see Fig. 7 in plastic tails of the same flexural stiffness and equiv- Fish 1998b and Fig. 11 in Thewissen 2018). alent scale were fashioned from the tail geometry of The magnitude of the acceleration reaction force the dinosaurs Coelophysis bauri, Allosaurus fragilis, is constrained by size (Webb 1988). As animals get and Spinosaurus aegyptiacus, the modern crocodile larger, the ability of the muscles to generate propul- Crocodylus niloticus, and crest newt Triturus dobrogi- sive force relative to inertial forces decreases (Daniel cus (Ibrahim et al. 2020). Coelophysis and Allosaurus and Webb 1987; Webb and Johnsrude 1988). were terrestrial and had strongly tapering tails. The Acceleration reaction is more sensitive to size than aquatic Spinosaurus, Crocodylus, and Triturus had lift-based propulsion (Sfakiotakis et al. 1999). Large keeled tails, although the tail of Crocodylus did animals use lift-based propulsion as used in the have an extended tapered caudal region. thunniform mode (Webb 1988; Webb and De Each tail was tested in a flow tank while attached Buffrenil 1990). to a robotic controller to generate heave and pitch In the thunniform mode with a lunate tail, the motions and produce undulatory movements. A six- momentum imparted from the animal’s oscillatory axis force–torque sensor measured the forces on the Tetrapod tails and aquatic propulsion 7 tail. The tapered tails generated the least thrust and 1999, 2001; Lauder 2000; Videler et al. 1999, 2002) had the lowest efficiencies compared with the keeled and to use this approach to understand the dynamics tails (Ibrahim et al. 2020). Triturus produced the of aquatic propulsion. Since the early use of DPIV, Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 greatest thrust, which was 14.6 times the thrust of the majority of research on tailed propulsion has Coelophysis. With the highest efficiency, Crocodylus been confined to swimming by fishes. This research was 4.0 times greater than Coelophysis. It was how- demonstrated that the broad caudal fin of subcaran- ever surprising that Crocodylus with a tapered aft giform and carangiform fish produces much of the section of its tail had a higher thrust production vorticity that is shed into its wake. The vorticity rolls than Spinosaurus and higher efficiency than both up into a vortex due to the action of the tail as it Spinosaurus and Triturus with their more extensive reaches its maximum sideways deflection (Fish and keels. The implication of this study was that the Lauder 2013). As the vortex moves away from the undulations of a vertically expanded tail shape im- tail, a new vortex forms with an opposite spin direc- part a substantial benefit in thrust production com- tion as the body flexes and the tail reverses direction. pared with tapering tails. This action leads to a thrust-type wake comprised of a staggered array of vortices with clockwise and anti- clockwise spins (Weihs 1972; Triantafyllou et al. DPIV of tapered versus lunate tails 1991; Sfakiotakis et al. 1999; Fish and Lauder Rotation of fluid in the wake generated by the tail, 2006). The alternating vortices are linked three- known as vorticity, can occur as a tail undulates or dimensionally as a series of connected vortex rings oscillates, changing the direction and magnitude of or tori (Vogel 1994; Fish and Lauder 2013). These flow passing first over the body and then along the vortex rings induce a jet flow that is oriented to the tail as momentum is added to the fluid. This in- side and backward and laced through the center of crease in vorticity transfers the kinetic energy of the interconnected rings is a central momentum jet. the swimmer to the water, which is eventually lost To examine the vortex wake of a tetrapod swim- in the formation of eddies and frictional forces in the mer with a tapered tail, we swam juvenile (27.9– water of the distant wake. Force production by an 30.2 cm) alligators (Alligator mississippiensis)ina undulating or oscillating tail is directly associated recirculating flow tank (Fig. 5) with a current veloc- with the shedding of vorticity into the wake ity of one body length/s. The DPIV experiments were (Drucker and Lauder 1999). This shed vorticity conducted according to the procedure of Standen reflects the transfer of momentum from the tail to (2008) using a laser sheet from a Coherent Innova the fluid and thrust production from the propulsive 300 laser to illuminate 10 mm diameter silver- movements of the tail particularly from the trailing coated glass beads. The movement of the alligators edge. If the trailing edge is a defining characteristic and beads was recorded with a Redlake PC1500 cam- responsible for thrust generation, how do swimmers era at 250 frames/s and the videos were processed with tapering tails generate thrust? Furthermore, with DaVis 7.0 (LaVision Inc.). when compared with broad lunate tails, which differ Juvenile alligators swam against the current of wa- considerably from tapered tails, would we expect to ter in the flow tank at the water’s surface with the see different mechanisms of thrust production? tail submerged. The alligators swam by body undu- These questions have been difficult to address by lations as waves were passed down the body and direct experimentation largely due to a lack of data long tapering tail with increasing amplitude toward on tapered tail hydrodynamics. the tail tip. When the flow field of the swimming One technique to visualize and measure wake vor- alligators was visualized using DPIV, a different pat- ticity to address these questions is digital particle tern of vortices in the wake emerged from that of image velocimetry (DPIV). DPIV is a video-based subcarangiform/carangiform fish (Fish and Lauder flow measurement technique (Willert and Gharib 2013). In the two-dimensional plane of the laser 1991). The positions of small, neutrally buoyant par- sheet, a pair of vortex rings was shed from the tail ticles illuminated with a laser sheet are statistically at the end of each half stroke. Each vortex ring was tracked between video frames. The trajectories of the elongated as the water was entrained by the whip- particles’ displacements are resolved into flow fields, like action of the tapering tail. Each vortex ring was where velocity vectors, pressure, and vorticity are not linked to the vortex ring generated from the calculated during post-processing. proceeding half stroke (Figs. 5 and 6). The vortex It has only been within the past 24 years that rings had a jet flow that was canted rearward at a DPIV has been used to study swimming animals mean downstream angle of 32.4 relative to the lon- in vivo (Mu¨ller et al. 1997; Drucker and Lauder gitudinal axis of the alligator. This arrangement of 8 F. E. Fish et al. 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Fig. 5 DPIV of swimming juvenile alligator. The DPIV set up showing position of the alligator and laser sheet in the flow tank (top). The deflection of reflective beads suspended in the water due to the movements of the tail was Average flow field (bottom) in the horizontal plane in the wake of the alligator tail (white) moving to right and left. Vorticity is shown in color (red: counter-clockwise; blue: clockwise) and velocity vectors as yellow arrows, which were calculated from sequential pairs of high-speed video images. paired vortices shed at the end of each half stroke is rising bubbles is subtracted from the flow field, de- categorized as a 2P vortex pattern (Techet et al. flection of the bubbles allowed for direct measure- 1998; Smits 2019), and is generally similar to the ments of the wake and propulsive forces from the wake of swimming eels (Tytell and Lauder 2004). oscillation of the flukes. At the other extreme of tailed swimming by tetra- Oscillations of the caudal flukes are the basis for pods is the lunate tail of the thunniform mode as thrust production by the dolphins, as the flukes are exemplified by dolphins. The size of these cetaceans, pitched at a positive angle of attack to the oncoming their protected status (i.e., Marine Mammal flow. The oscillating trajectory of the flukes and the Protection Act), and the volume of water needed angle of attack imparts a velocity difference around to permit continuous swimming preclude use of the propulsor. According to the Bernoulli theorem, the standard DPIV setup, including the use of lasers the differential velocities produce a net pressure dif- and seeding particles. Therefore, the wake structure ference resulting in a force. The hydrodynamic force of a swimming dolphin was visualized using micro- is resolved into a drag that is tangential to the axis of bubbles (<1 mm) generated in a nominally planar the motion of the flukes, and a lift that is perpen- sheet from a porous hose at the bottom of the test dicular to the axis of motion and canted anteriorly pool (Fish et al. 2014, 2018). After the velocity of the (Webb 1975). Along with leading-edge suction, the Tetrapod tails and aquatic propulsion 9 Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021

Fig. 6 Comparison of vortex wake of an alligator and a dolphin. The alligator sheds paired vortices at the end of each half stroke in a 2P pattern; whereas, the dolphin generates a 2S pattern with a single vortex on each half stroke. The colors of the vortices indicate clockwise (blue) and counterclockwise (red) spins. anteriorly directed lift is resolved into a horizontal vector component, which represents the thrust Fig. 7 Reconstruction (top) and skeleton (bottom) of P. darwini,a (Sfakiotakis et al. 1999). As thrust from the lift is transitional fossil pinniped from the early Miocene High Arctic, produced, momentum is transferred from the flukes showing the thin, elongate tail. Reconstruction credit: A. Tirabasso/Canadian Museum of Nature; Photo credit: M. Lipman/ to the water. Canadian Museum of Nature. Momentum shed into the wake of the swimming dolphin was visualized by the bubble DPIV (Fish et al. 2014). The dorsoventral oscillations of the of oscillation, and U is the mean forward velocity flukes produced a thrust-type wake (Weihs 1972; (Triantafyllou et al. 1991, 2000). The optimum cre- Fish and Lauder 2006; Smits 2019). One vortex ation of thrust-producing jet vortices lies in a narrow was generated on each half stroke. The vortices of range of St. The predicted St range for maximum each upstroke and each downstroke of the flukes had spatial amplification occurs between 0.25 and 0.35, opposite rotations. A central momentum jet flow where swimming efficiency peaks (Triantafyllou et al. opposite to the swimming direction was directed 1991; Triantafyllou and Triantafyllou 1995). The 2S through the center of the staggered array of vortices vortex wake corresponds to St within the “optimal” rings. The vortex wake generated from the pitching range; whereas 2P wakes occur at higher St values and heaving motions of the flukes of the dolphins associated with lower propulsive efficiencies (Dewey was analogous to the vortex wake of subcarangiform/ et al. 2012; Smits 2019). carangiform fishes described above. This vortex wake The 2S vortex wake exhibited by the bottlenose pattern is categorized as 2S (Techet et al. 1998; Smits dolphin with an oscillating lunate tail has a high 2019). propulsive efficiency with a maximum of 0.85 at a The 2S and 2P vortex patterns have distinct ram- mean St of 0.26 (Fish 1998a; Rohr and Fish 2004; ifications in regard to propulsive efficiency (Techet Fish et al. 2014). On the other hand, the undulating et al. 1998; Smits 2019). Optimal thrust propulsion tapering tail of the alligator has an average St of 0.59 and efficiency are achieved by controlling the pattern to generate a 2P vortex wake (Fish and Lauder and periodicity of vortices in the wake. The devel- 2006). This value of St for the alligator is above opment of the 2P wake pattern is due to the bifur- the optimal range indicating a low propulsive effi- cation of the 2S structure as the Strouhal number ciency. Reduced efficiency is further indicated by the (St) increases (Dewey et al. 2012). St is related to ratio of the swimming speed (U) to tail wave speed how fast the vortices are being generated and the (V)(Webb 1975), also known as the propulsive space between them. St is defined as St ¼ Af/U, “slip.” For an alligator swimming at 1.0 BL/s, U/V where A is the width of the wake, taken to be equal is 0.75 (Fish 1984). Webb (1975) indicated that most to the peak-to-peak maximum excursion of the trail- measurements of U/V for anguilliform and subcar- ing edge of the caudal propulsor, f is the frequency angiform swimmers are below 0.7. For animals with 10 F. E. Fish et al. a tapering tail, the propulsive efficiency for undula- between the hind limbs to the axial skeleton as a tory swimming would be less than that calculated for locomotor specialization for hopping (Emerson fishes. The American eel (Anguilla rostrata) with a 1979; Shubin and Jenkins 1995; Peters et al. 1996; Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 keeled, but tapering tail has a propulsive efficiency of Rockoca and Rocek 2005). Hopping is believed to 0.43–0.54, while producing a 2P wake. However, a have originated in a riparian environment and was computational study of the tadpole with a keeled tail used as an escape behavior to rapidly leap from land achieved a calculated efficiency of 0.8 (Liu et al. into water (Inger 1962; Gans and Parsons 1966). 1996). Another locomotor specialization drove the evolu- The components of locomotor forces calculated tion of swimming styles in birds. Before semiaquatic from the wake depend directly upon the orientation birds propelled themselves through the liquid envi- of the central momentum jet of the vortex rings. ronment of water, they flew through the fluid atmo- Whereas the momentum jet for the alligator is sphere of air. The dinosaurian origins of birds came canted at 32.4 downstream, the eel produces a lat- with a long tail. A long reptilian tail like in eral jet that is oriented slightly upstream at 87 Archaeopteryx, however, would be detrimental to (Tytell and Lauder 2004). Therefore, it is expected flight stability and control (Heers and Dial 2012; that the alligator would have a higher propulsive ef- Rashid et al. 2018). For flying, the tail was truncated ficiency compared with the eel. However, drag due and fused into a pygostyle in birds (Gao et al. 2008; to the body (and limbs) must also be taken into Heers and Dial 2012). Taxa returning to aquatic lo- account when considering the comparative propul- comotion without a long tail were consigned to sive efficiencies of eels and alligators. Alligators with winged or foot-based propulsion (Lane 1947; Hui a 2P vortex wake pattern, tapering tail, and undula- 1988; Fish 2016) and the function of the pygostyle tory swimming mode display a notably lower swim- was relegated to no more than rudder in diving birds ming performance relative to dolphins with their 2S (Felice and O’Connor 2014). wake pattern, lunate tail, and oscillatory swimming mode. Defensive specialization The ancestors of turtles possessed long tails (Schoch Beyond the tail and Sues 2015; Li et al. 2018). However, stiffening The gap in aquatic adaptation by vertebrates result- the trunk of the body with a bony shell and with- ing from the foray into terrestriality by tetrapods had drawing the head and appendages within the shell consequences related to the use of the tail. Although for protection would have been facilitated by short- various taxonomic groups of tetrapods returned to ening the limbs and tail. In this case, morphological aquatic habits, not all groups adopted the tail as a specialization associated with defensive armor poten- propulsive organ along an undulatory–oscillatory tially played a part in the reduction in a tail by continuum. Indeed, some groups lost or reduced turtles. A possible exception is the snapping turtle an effective tail as a means to traverse the aqueous (Chelydra serpentine), characterized by a moderate environment (Inger 1962). These tailless tetrapod tail that is too large to be withdrawn within the shell. swimmers arrived at various solutions to the prob- Lateral movement of its tail may be able to assist, to lem posed by the need to swim, using different mor- a small degree, with forward propulsion in underwa- phological designs and modes of propulsion, such as ter walking (Willey and Blob 2004). The resulting flippers, wings, and feet. The evolution of these al- short tail of turtles can also be used as a rudder ternative modes of propulsion was due to various (Mayerl et al. 2018). Similarly, a paddle-like tail fin constraints that selected for a reduction in the tail. was envisioned to function as a rudder for maneuverability and stability by the plesiosaur Locomotor specialization Rhomaleosaurus zetlandicus, which swam with its flippered limbs and possessed a rigid body (Smith Although the larval tadpoles swim by undulating a 2013). keeled tail, the metamorphosis to a more terrestrial adult frog eliminates this caudal structure. What remains of the tail in frogs is an urostyle composed Phylogenetic constraints of a few fused caudal vertebrae (Shubin and Jenkins Phylogenetic constraints on locomotor diversification 1995). The urostyle is hidden within the body as the can occur when a lineage has already reduced or lost ilium elongates. These skeletal modifications are as- the tail in its evolution. The subsequent divergence sociated with iliosacral mobility and the recruitment of new semiaquatic lineages could continue the evo- of the tail musculature for transmission of force lutionary trajectory for increasing swimming Tetrapod tails and aquatic propulsion 11 specialization, while retaining the reduced tail. As an mid-late Oligocene at 30.6–23 million years ago example, the capybara (Hydrochoerus hydrochaeris)is (Repenning 1976; Barnes et al. 1985; Fish 2001; Liu a semi-aquatic South American rodent with a vesti- et al. 2009; Rybczynski et al. 2009; Berta 2017; Poust Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 gial tail that swims and dives with ease (Nowak and Boessenecker 2018). Such climatic conditions 1999). The genus has only been in existence for would select for increased insulation and a shorter the last 3 Ma (Vucetich et al. 2013). Molecular phy- tail to limit heat loss (Mincer and Russo 2020). With logenetic analysis of modern South American thermoregulatory constraints favoring a less substan- rodents shows the capybara nested within tial tail, aquatic pinnipeds would rely on propulsion Caviodea, a group whose fossil history extends into from the limbs, which increased in size and were the Oligocene (34–23 Mya) (Perez and Pol 2012). modified as hydrofoils (Wyss 1989; Berta and Ray Today Caviodea includes eight other genera, and 1990; Bebej 2009). The short tail of the sea otter all of these have diminutive tails (Alvarez et al. Enhydra lutris similarly precludes its use in generat- 2017) and, aside from the capybara, all are terrestrial ing thrust, necessitating the enlargement and use of (Nowak 1999). The appearance of short tails in the the hind feet as propulsors (Kenyon 1969; Williams ancestors of the modern Caviodea lineage (e.g., 1989). Eocardia) suggests that the ancestor of the capybara In contrast, in warm climates, a long tail could be was a terrestrial rodent with a vestigial tail (Scott useful to counteract overheating by dumping excess 1905). With the tail all but gone, there is little op- metabolic heat to the environment (Steen and Steen portunity for natural selection to favor the evolution 1965; Fish 1979; Young and Dawson 1982; Kuhn and of a swimming-specialized tail in the capybara Meyer 2009; Mincer and Russo 2020). The long-tailed lineage. ancestors of cetaceans and sirenians originated in tropical and subtropical climates during the Eocene (Domning 1976; Barnes et al. 1985; Fordyce 1992; Physiological constraints Gingerich et al. 1994; Thewissen et al. 1994). It was On account of their high surface-to-volume ratios during this period that ancestral cetaceans were ex- and vascularization, poorly insulated tails in homeo- posed to the Paleocene–Eocene thermal maximum thermic tetrapods can potentially act as avenues of (PETM), a global greenhouse thermal event heat loss from the body (Scholander et al. 1950; Fish (Gingerich 2015). Whereas Ambulocetus had well- 1979; Hickman 1979). In water temperatures below developed limbs and a prominent tail (Thewissen body temperature, blood flow from the body to the et al. 1994; Thewissen and Fish 1997), the tail became tail can be reduced allowing for regional heterother- more robust as limb size decreased in later fossil mia and curtailing excessive heat loss (Steen and taxa such as Rhodhocetus (Gingerich et al. 1994). Steen 1965; Fish 1979). With increased exposure to Ultimately, propulsion in cetaceans was facilitated by cold water and limited ability to haul out of the the development of caudal flukes with an oscillatory water and re-warm extremities, a reduced tail would motion for high thrust production and propulsive be thermally beneficial to aquatic homeotherms in efficiency (Fish 1996, 1998b, 2001; Fish et al. 2014). cold environments. Given this perspective, it is in- teresting that the otter-like transitional pinniped, Puijila darwini, had a long tail, although shorter Conclusions than modern otters (Fig. 7; Rybczynski et al. 2009; Upon returning to the water after an evolutionary Paterson et al. 2020). In contrast, the archaic flip- terrestrial venture, many secondarily aquatic tetra- pered pinniped, Enaliarctos mealsi, had a short tail as pods relegated their swimming propulsion to thrust do the species within the three extant pinniped fam- generated by an elongate tail. The tail as a propulsive ilies (Berta and Ray 1990). The tail of Puijila appears organ generates thrust by undulation. Morphological to have been more rat-like than the broader tails of changes in the tail accompanying increased use of the beaver and modern river otters (e.g., Castor, aquatic habits likely were associated with enhanced Lontra, and Pteronura), which undulate their tails swimming capability (i.e., thrust production, speed, to aid the paddling strokes of the hind feet (Fish efficiency, maneuverability). The diversity of tail 1996). A possible explanation for the reduction in morphologies among swimming tetrapods can be tails in the pinnipeds would lie in the association categorized as tapered, keeled, paddle, and lunate. of thermoregulation and climatic conditions These tail morphologies fall along a performance (Mincer and Russo 2020). Puijila and the short- and kinematic gradient with increasing thrust gener- tailed pinnipeds originated in temperate or subarctic ation and propulsive efficiency and a shift from un- environments with cold water currents during the dulatory to oscillatory swimming. 12 F. E. Fish et al.

Thrust production results from the interaction of the propulsive movements of the tail with the phys- Acknowledgments ical properties of the aqueous medium. The viscosity The authors are grateful for the assistance of Danielle Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 and density of the water determine how momentum Adams, Annalisa Berta, William Gough, and Ariel is transferred from kinetic tail motion into the Leahy with their assistance on researching the struc- downstream water flow to sustain and propel the ture and swimming performance of highly derived animal. The kinematics and shape of the tail are aquatic vertebrates. We greatly appreciate the coop- important in determining the rate of momentum eration of the Philadelphia Zoo for filming the giant transferred to the water. For an undulating tail, river otters, and thanks for the generosity of Frank thrust is generated by an acceleration reaction that Newell (Newell Farms Wildlife Rehabilitation Center, is dependent on the mass of water that is accelerated Warrenton, NC) for allowing us to film beavers. The into the wake. The mass of water affected by a ta- research on the beavers was approved by the West pering tail is greatly reduced compared with other Chester University Institutional Animal Care and tail shapes because the trailing edge comes to a Use Committee (IACUC) under Fish-06-01 and point. Increased propulsive efficiency and thrust pro- Fish-07-02, and the research on the alligators was duction by an undulating tail therefore necessitates under Fish-03-2005 from West Chester University broadening the tail with a keel and flattened cross- and IACUC 20-03 from Harvard University. sectional geometry. This change from a tapered tail increases the vorticity along its length, and studies Conflict of Interest with simple models of different tail shapes actuated The authors declare no conflict of interest. by a robotic system confirm these predicted patterns of thrust and efficiency. Further augmentation of the tail leads to an expanded paddle-like trailing edge to Funding increase the mass of water affected. Further improve- This work was supported in part with a grant (to ments in thrust and efficiency occur with the evolu- F.E.F) from the Office of Naval Research [grant tion of the lunate tail in concert with a thunniform number N000141410533] and from the Canadian body design and oscillatory swimming mode seen in Museum of Nature (to N.R.). the most highly derived aquatic tetrapods. 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