Amphibious adaptations in a newly recognized amphibious fish: Terrestrial locomotion and the influences of body size and temperature

Amphibious animals are adapted for both aquatic and terrestrial habitats. The conflicting requirements for dual habitats are perhaps most pronounced in the air‐breathing fishes, which represent an intermediate stage between the totally aquatic habitat and terrestrial colonization. A key requirement for amphibious fishes is terrestrial locomotion. The different densities and compositions of air and water impose constraints for efficient terrestrial locomotion that differ from those required for aquatic locomotion. I investigated terrestrial locomotion in a small South African fish, Galaxias ‘nebula’, by exposing 60 individual fish to air in specially designed raceways and quantifying movement type and occurrence as a function of availability of water, fish size and environmental temperature. Nebula showed a sustained undulating form of terrestrial locomotion characteristic of amphibious fishes and also a transient ballistic locomotion (jumps) typical of fully aquatic species. Terrestrial movement was influenced by fish size, with medium‐sized fish undertaking more jumps towards water, and fewer jumps away from water, than their smaller or larger conspecifics. In contrast, axial undulation was mainly influenced by temperature. However, there was no consistent pattern in temperature effects presumably because temperature is just one of a suit of environmental factors that may affect terrestrial locomotion. Nebula's amphibious adaptations allow it to cope with the unpredictability inherent in its natural environment.     

Kinematics of terrestrial locomotion in harbor seals and gray seals: Importance of spinal flexion by amphibious phocids

Pinnipeds are amphibious mammals with flippers, which function for both aquatic and terrestrial locomotion. Evolution of the flippers has placed constraints on the terrestrial locomotion of phocid seals. The detailed kinematics of terrestrial locomotion of gray (Halichoerus grypus) and harbor (Phoca vitulina) seals was studied in captivity and in the wild using video analysis. The seals exhibited dorsoventral undulations with the chest and pelvis serving as the main contact points. An anteriorly directed wave produced by spinal flexion aided in lifting the chest off the ground as the fore flippers were retracted to pull the body forward. The highest length‐specific speeds recorded were 1.02 BL/s for a gray seal in captivity and 1.38 BL/s for a harbor seal in the wild. The frequency and amplitude of spinal movement increased directly with speed, but the duty factor remained constant. Substrate did not influence the kinematics except for differences due to moving up or down slopes. The highly aquatic nature of phocids seals has restricted them to locomote on land primarily using spinal flexion, which can limit performance in speed and duration.     

Jumping sans legs: does elastic energy storage by the vertebral column power terrestrial jumps in bony fishes?

Despite having no obvious anatomical modifications to facilitate movement over land, numerous small fishes from divergent teleost lineages make brief, voluntary terrestrial forays to escape poor aquatic conditions or to pursue terrestrial prey. Once stranded, these fishes produce a coordinated and effective “tail-flip” jumping behavior, wherein lateral flexion of the axial body into a C-shape, followed by contralateral flexion of the body axis, propels the fish into a ballistic flight-path that covers a distance of multiple body lengths. We ask: how do anatomical structures that evolved in one habitat generate effective movement in a novel habitat? Within this context, we hypothesized that the mechanical properties of the axial skeleton play a critical role in producing effective overland movement, and that tail-flip jumping species demonstrate enhanced elastic energy storage through increased body flexural stiffness or increased body curvature, relative to non-jumping species. To test this hypothesis, we derived a model to predict elastic recoil work from the morphology of the vertebral (neural and hemal) spines. From ground reaction force (GRF) measurements and high-speed video, we calculated elastic recoil work, flexural stiffness, and apparent material stiffness of the body for Micropterus salmoides (a non-jumper) and Kryptolebias marmoratus (adept tail-flip jumper). The model predicted no difference between the two species in work stored by the vertebral spines, and GRF data showed that they produce the same magnitude of mass-specific elastic recoil work. Surprisingly, non-jumper M. salmoides has a stiffer body than tail-flip jumper K. marmoratus. Many tail-flip jumping species possess enlarged, fused hypural bones that support the caudal peduncle, which suggests that the localized structures, rather than the entire axial skeleton, may explain differences in terrestrial performance.     

Structural features of neural spines of the caudal vertebrae of protoceratopoids (Ornithischia: Neoceratopsia)

The structure of caudal neural spines of protoceratopoids displays adaptation for aquatic and terrestrial mode of life. The increasing height of caudal neural spines in the series Leptoceratops, Udanoceratops, Protoceratops, Bagaceratops is connected with the extent of adaptation for swimming and changes in inclination of neural spines are connected with the mechanical balance of the lever. Thus, the anterior caudal vertebrae (1cd–15cd) of Protoceratops and Bagaceratops show an anticliny, which promotes extension (rise) of a heavy tail in terrestrial conditions. In the middle part of the tail (16cd–23cd), with the greatest height of neural spines, a decrease in width and increase in thickness counteract transverse loads accompanying movements on land. At the same time, the supraspinal ligament prevents divergence of neural spines caused by curvature of the tail as it is raised above the ground.     

Comparative study of the anatomy and laminar organization in the olfactory bulb of three orders of freshwater teleosts

The anatomy and lamination of the olfactory bulb in Cyprinus carpio, Tinca tinca, Barbus bocagei (Fam. Cyprinidae, Or. Cypriniformes); Salmo gairdneri (Fam. Salmonidae, Or. Salmoniformes); and Gambusia affinis (Fam. Poeciliidae, Or. Cyprinodontiformes), all of them freshwater teleosts, are studied. These species show significative differences on the location, size, morphology, and lamination of their olfactory bulbs. The presence of a new stratum in the olfactory bulb of Salmo gairdneri and a completely different laminar organization in the olfactory bulb of Gambusia affinis are described for the first time. The anatomical and histological peculiarities of this structure in the orders studied could be the basis for different experimental approaches.     

Tail development and regeneration throughout the life cycle of the four-toed salamander Hemidactylium scutatum

The salamander tail displays different functions and morphologies in the aquatic and terrestrial stages of species with complex life cycles. During metamorphosis the function of the tail changes; the larval tail functions in aquatic locomotion while the juvenile and adult tail exhibits tail autotomy and fat storage functions. Because tail injury is common in the aquatic environment, we hypothesized that mechanisms have evolved to prevent altered larval tail morphology from affecting normal juvenile tail morphology. The hypothesis that injury to the larval tail would not affect juvenile tail morphology was investigated by comparing tail development and regeneration in Hemidactylium scutatum (Caudata: Plethodontidae). The experimental design included larvae with uninjured tails and with cut tails to simulate natural predation. The morphological variables analyzed to compare normally developing and regenerating tails were 1) tail length, 2) number of caudal vertebrae, and 3) vertebral centrum length. Control and experimental groups do not differ in time to metamorphosis or snout-vent length. Tails of experimental individuals are shorter than controls, yet they display a significantly higher rate of tail growth and less resorption of tail tissue. Anterior to the site of tail injury, caudal vertebrae in juveniles display greater average centrum lengths. Results suggest that regenerative mechanisms are functioning not only to produce structures, but also to influence growth of existing structures. Further investigation of juvenile and adult stages as well as comparative analyses of tail morphology in salamanders with complex life cycles will enhance our understanding of amphibian development and of the evolution of amphibian life cycles. J Morphol 233:15–29, 1997. © 1997 Wiley-Liss, Inc.     

Patterns of regional variation in the vertebral column of terrestrial salamanders

Regional variation in the vertebral column of several species of salamanders (families Ambystomatidae, Salamandridae and Plethodontidae) is analyzed. Measurements of three dimensions, centrum length, prezygapophyseal width, and transverse process length, provide the data. Ontogenetic, interspecific, intergeneric and interfamilial patterns of positional variation are diagrammed and discussed. Distinctive patterns of variation characterize the families, genera, and to a lesser extent, the species. The patterns of ambystomatid salamanders are the most generalized, and probably reflect derivation from a primitive ancestral stock. The most specialized conditions occur in the fully terrestrial plethodontids, a group generally considered to be highly derived. Data such as those presented here will aid in the identification of fossils. The patterns described have functional significance. For example, species which have an aquatic larval stage and which return to aquatic breeding sites have vertebrae which taper in length and width behind the pelvis. This is a feature associated with production of a traveling wave in the tail which is necessary for propulsion in water. Fully terrestrial species do not have a tapering column. In them, standing waves, such as occur in the trunk region of all species, typically occur in the tail. The caudal vertebrae of terrestrial species are rather uniform in dimensions for some distance, and the tail is cylindrical in form. Other functionally important features include the narrowing and shortening of some anterior vertebrae, associated with the development of a neck in some species with tongue feeding mechanisms. In contrast, species which use their heads as wedges during locomotion have broadened anterior vertebrae which serve as sites of origin for hypertrophied neck muscles.     

Retracted: Evolution and development of the homocercal caudal fin in teleosts

The vertebrate caudal skeleton is one of the most innovative structures in vertebrate evolution and has been regarded as an excellent model for functional morphology, a discipline that relates a structure to its function. Teleosts have an internally‐asymmetrical caudal fin, called the homocercal caudal fin, formed by the upward bending of the caudal‐most portion of the body axis, the ural region. This homocercal type of the caudal fin ensures powerful and complex locomotion and is thought to be one of the most important evolutionary innovations for teleosts during adaptive radiation in an aquatic environment. In this review, we summarize the past and present research of fish caudal skeletons, especially focusing on the homocercal caudal fin seen in teleosts. A series of studies with a medaka spontaneous mutant have provided important insight into the evolution and development of the homocercal caudal skeleton. By comparing developmental processes in various vertebrates, we propose a scenario for acquisition and morphogenesis of the homocercal caudal skeleton during vertebrate evolution.     

Comparative histomorphology of the Mauthner cells in some freshwater teleosts.

The histomorphological observations are made on the Mauthner cells in eight species of teleosts belonging to six different families. The cells are better developed in Channa punctatus, Heteropneustes fossilis, Labeo rohita, Danio, malabaricus and Puntius ticto. They are symmetrically situated in Nandus nandus and are found to be absent in Mastocembalus armatus. Their position, shape and size vary in different species. The axon cap is well developed in Channa punctatus, Heteropneustes fossilis and carps. The cell body sends lateral and ventral dendrites besides several small dendrites. The lateral dendrite emerges through the axon cap, turns dorsolateral and becomes myelinated to form Mauthner axon. The Mauthner axon extends in the spinal region upto the caudal peduncle and forms synapses with the spinal motoneurons of the front column. There are numerous synapses and end bulbs from the vestibular fibres and VIIIth nerve distributed on the perikaryan of the Mauthner cell body. It is suggested that the Mauthner cells are comparatively well developed in those species in which the tail fin is better utilized for swimming.     

Caudal vertebral development and morphology in three salamanders with complex life cycles (Ambystoma jeffersonianum, Hemidactylium scutatum, and Desmognathus ocoee)

We describe caudosacral and caudal vertebral morphology across life history stages in three caudate amphibians: Ambystoma jeffersonianum (Ambystomatidae), Desmognathus ocoee (Plethodontidae: Desmognathinae), and Hemidactylium scutatum (Plethodontidae: Plethodontinae). All three species have aquatic larvae, but adults differ in habitat and predator defense strategy. Predator defense includes tail autotomy in D. ocoee and H. scutatum but not A. jeffersonianum. Of the species that autotomize, H. scutatum has a specialized constriction site at the tail base. We investigated whether aquatic larvae exhibit vertebral features similar to those previously described for aquatic adults and examined the effect of metamorphosis, if any, on vertebral morphology and the ontogeny of specialized vertebral features associated with tail autotomy. Interspecific comparisons of cleared-and-stained specimens indicate that vertebral morphology differs dramatically at hatching and that caudosacral and caudal vertebrae undergo continuous ontogenetic change throughout larval, metamorphic, and juvenile periods. Larvae and juveniles of H. scutatum do not exhibit adult vertebral features associated with constricted-base tail autotomy. The pond-type larvae of A. jeffersonianum and H. scutatum have tapering centrum lengths posterior to the sacrum. This pattern is functionally associated with aquatic locomotion. The stream-type larvae of D. ocoee undergo enhanced regional growth in the anterior tail such that the anterior caudal centra become longer than the preceding caudosacral centra. With the exception of the first two caudal vertebrae, a similar growth pattern occurs in H. scutatum adults. We hypothesize that enhanced growth of the anterior caudal segments is associated with tail elongation and autotomy.     

Lungfish Axial Muscle Function and the Vertebrate Water to Land Transition

The role of axial form and function during the vertebrate water to land transition is poorly understood, in part because patterns of axial movement lack morphological correlates. The few studies available from elongate, semi-aquatic vertebrates suggest that moving on land may be powered simply from modifications of generalized swimming axial motor patterns and kinematics. Lungfish are an ideal group to study the role of axial function in terrestrial locomotion as they are the sister taxon to tetrapods and regularly move on land. Here we use electromyography and high-speed video to test whether lungfish moving on land use axial muscles similar to undulatory swimming or demonstrate novelty. We compared terrestrial lungfish data to data from lungfish swimming in different viscosities as well as to salamander locomotion. The terrestrial locomotion of lungfish involved substantial activity in the trunk muscles but almost no tail activity. Unlike other elongate vertebrates, lungfish moved on land with a standing wave pattern of axial muscle activity that closely resembled the pattern observed in terrestrially locomoting salamanders. The similarity in axial motor pattern in salamanders and lungfish suggests that some aspects of neuromuscular control for the axial movements involved in terrestrial locomotion were present before derived appendicular structures.     

Triturus newts defy the running-swimming dilemma

Conflicts between structural requirements for carrying out different ecologically relevant functions may result in a compromise phenotype that maximizes neither function. Identifying and evaluating functional trade-offs may therefore aid in understanding the evolution of organismal performance. We examined the possibility of an evolutionary trade-off between aquatic and terrestrial locomotion in females of European species of the newt genus Triturus. Biomechanical models suggest a conflict between the requirements for aquatic and terrestrial locomotion. For instance, having an elongate, slender body, a large tail, and reduced limbs should benefit undulatory swimming, but at the cost of reduced running capacity. To test the prediction of an evolutionary trade-off between swimming and running capacity, we investigated relationships between size-corrected morphology and maximum locomotor performance in females of ten species of newts. Phylogenetic comparative analyses revealed that an evolutionary trend of body elongation (increasing axilla-groin distance) is associated with a reduction in head width and forelimb length. Body elongation resulted in reduced maximum running speed, but, surprisingly, also led to a reduction in swimming speed. The evolution of longer tails was associated with an increase in maximal swimming speed. We found no evidence for an evolutionary trade-off between aquatic and terrestrial locomotor performance, probably because of the unexpected negative effect of body elongation on swimming speed. We conclude that the idea of a design conflict between aquatic and terrestrial locomotion, mediated through antagonistic effects of body elongation, does not apply to our model system.     

How muscles accommodate movement in different physical environments: aquatic vs. terrestrial locomotion in vertebrates.

Representatives of nearly all vertebrate classes are capable of coordinated movement through aquatic and terrestrial environments. Though there are good data from a variety of species on basic patterns of muscle recruitment during locomotion in a single environment, we know much less about how vertebrates use the same musculoskeletal structures to accommodate locomotion in physically distinct environments. To address this issue, we have gathered data from a broad range of vertebrates that move successfully through water and across land, including eels, toads, turtles and rats. Using high-speed video in combination with electromyography and sonomicrometry, we have quantified and compared the activity and strain of individual muscles and the movements they generate during aquatic vs. terrestrial locomotion. In each focal species, transitions in environment consistently elicit alterations in motor output by major locomotor muscles, including changes in the intensity and duration of muscle activity and shifts in the timing of activity with respect to muscle length change. In many cases, these alterations likely change the functional roles played by muscles between aquatic and terrestrial locomotion. Thus, a variety of forms of motor plasticity appear to underlie the ability of many species to move successfully through different physical environments and produce diverse behaviors in nature.     

Patterns of axial and appendicular movements during aquatic walking in the salamander Siren lacertina

Most studies of salamander locomotion have focused either on swimming or terrestrial walking, but some salamanders also use limb-based locomotion while submerged under water (aquatic walking). In this study we used video motion analysis to describe the aquatic walking gait of Siren lacertina, an elongate salamander with reduced forelimbs and no hindlimbs. We found that S. lacertina uses a bipedal-undulatory gait, which combines alternating use of the forelimbs with a traveling undulatory wave. Each forelimb is in contact with the substrate for about 50% of the stride cycle and forelimbs have little temporal overlap in contact intervals. We quantified the relative timing and frequency of limb and tail movements and found that, unlike the terrestrial gaits of most salamanders, axial and appendicular movements are decoupled during aquatic walking. We found no significant relationship between stride frequency and aquatic walking velocity, but we did find a statistically significant relationship between tailbeat frequency and aquatic walking velocity, which suggests that aquatic walking speed is mainly modulated by axial movements. By comparing axial wavespeed and distance traveled per tailbeat during swimming (forelimbs not used) and aquatic walking (forelimbs used), we found lower wavespeed and greater distance traveled per tailbeat during aquatic walking. These findings suggest that the reduced forelimbs of S. lacertina contribute to forward propulsion during aquatic walking.     

Emergence behavior of a tide pool fish <Emphasis Type="Italic">Praealticus tanegasimae</Emphasis> (Teleostei; Blenniidae) on subtropical reefs

Praealticus tanegasimae is a rockpool blenny that occurs around the higher edge of the intertidal zone in subtropical waters of the western Pacific. Terrestrial emergence from tide pools was confirmed in the blenny during daytime low tide periods on Kuchierabu-jima Island, southern Japan. They stayed in the pools, putting their heads above the water surface, and then jumped out with a tail flip. The duration for each terrestrial emergence ranged from 4 to 665 s (median 31 s), during which they never showed reproductive-related behaviors or active feeding behavior on land. The emergence behavior was often followed by hopping toward neighboring pools, and suggested that the goal of the behavior was to change pools for escape from unfavorable water conditions.     

Functional significance of intramandibular bending in Poeciliid fishes

Substrate-feeding teleosts show multiple, independent evolutionary acquisitions of intramandibular bending (bending within the lower jaw)—a behavior that likely enhances performance when feeding on attached or encrusting food items. However, intramandibular bending has only been quantified for marine teleosts. Here, we examine substrate feeding in eight species from the order Cyprinodontiformes and quantify movements produced by the anterior jaws of four target species selected from the family Poeciliidae to represent a variety of trophic strategies. Intramandibular bending, defined here as bending between the dentary and angular–articular bones of the lower jaw, is not present in some poeciliids (i.e. Gambusia affinis), nor is it present in outgroup cyprinodontiforms (i.e. Fundulus rubrifrons). However, intramandibular bending is present in certain poeciliids (i.e. Poecilia sphenops), and can exceed 90°. Such jaw bending enables the production of a gape angle that approaches 120°, which likely allows the fish to maximize contact between the toothed tips of the jaws and the substrate during the bite. Intramandibular bending in poeciliid species is associated with specific trophic shifts: the greater the intramandibular bending in a given species, the more attached algae (periphyton) reported in its diet. This result supports the hypothesis that intramandibular bending enhances performance when feeding on encrusting food items. We predict that additional examples of functional convergence are likely to be documented in freshwater teleosts as more herbivorous species are examined, and we propose that intramandibular bending represents an excellent model system in which to examine the functional processes that underlie convergent evolution. An erratum to this article can be found at     

Muscular mechanisms of snake locomotion: an electromyographic study of lateral undulation of the Florida banded water snake (Nerodia fasciata) and the yellow rat snake (Elaphe obsoleta)

Electromyography and cinematography were used to determine the activity of epaxial muscles of colubrid snakes during terrestrial and aquatic lateral undulatory locomotion. In both types of lateral undulation, at a given longitudinal position, segments of three muscles (Mm. semispinalis-spinalis, longissimus dorsi, and iliocostalis) usually show synchronous activity. Muscle activity propagates posteriorly and generally is unilateral. With each muscle, large numbers of adjacent segments (30 to 100) show simultaneous activity. Terrestrial and aquatic undulation differ in two major respects. (1) During terrestrial undulation, muscle activity in a particular region begins when that portion of the body has reached maximal convex flexion and ends when it is maximally concave; this phase relation is uniform along the entire snake. During swimming, however, muscle activity passes posteriorly faster than the wave of vertebral flexion, causing the relation of muscle activity to flexion to change along the length of the snake. (2) In the terrestrial mode, the block of active muscle segments remains approximately constant in size as it passes down the snake, whereas during swimming the number of adjacent active muscle segments increases posteriorly. Despite the fact that Elaphe obsoleta has nearly twice as many body vertebrate as Nerodia fasciata (240 vs. 125), the only difference observed in the swimming of these two species is that a larger number of adjacent muscle segments is simultaneously active in comparable regions of Elaphe obsoleta than in Nerodia fasciata.     

Fiber‐type distribution of the perivertebral musculature in Ambystoma

Many salamanders locomote in aquatic and terrestrial environments. During swimming, body propulsion is solely produced by the axial musculature generating lateral undulations of the trunk and tail. During terrestrial locomotion, the trunk is oscillated laterally in a standing wave, and body propulsion is achieved by concerted trunk and limb muscle action. The goal of this study was to increase our knowledge of the functional morphology of the tetrapod trunk. We investigated the muscle‐fiber‐type distribution and the anatomical cross‐sectional area of all perivertebral muscles in Ambystoma tigrinum and A. maculatum. Muscle‐fiber‐type composition was determined in serial cross‐sections based on m‐ATPase activity. Five different body segments were investigated to test for cranio‐caudal changes along the trunk. The overall fiber‐type distribution was very similar between the species, but A. tigrinum had relatively larger muscles than A. maculatum, which may be related to its digging behavior. None of the perivertebral muscles possessed a homogeneous fiber‐type composition. The M. interspinalis showed a distinct layered organization and may function to ensure the integrity of the spine (local stabilization). The M. dorsalis trunci exhibited the plesiomorphic pattern for notochordates in having a distinct superficial layer of red and intermediate fibers, which covered the central white fibers; therefore, it is suggested to function as a mobilizer and a stabilizer of the trunk, but, may also be involved in modulating body stiffness. Similarly, the M. subvertebralis showed clear regionalizations, implying functional subunits that can stabilize and mobilize the trunk as well as modulate of body stiffness. Cranio‐caudally, neither the fiber‐type composition nor the a‐csa changed dramatically, possibly reflecting the need to perform well in both aquatic and terrestrial habitats. J. Morphol., 2010. © 2009 Wiley‐Liss, Inc.     

Axial allometry in a neutrally buoyant environment: effects of the terrestrial‐aquatic transition on vertebral scaling

Ecological diversification into new environments presents new mechanical challenges for locomotion. An extreme example of this is the transition from a terrestrial to an aquatic lifestyle. Here, we examine the implications of life in a neutrally buoyant environment on adaptations of the axial skeleton to evolutionary increases in body size. On land, mammals must use their thoracolumbar vertebral column for body support against gravity and thus exhibit increasing stabilization of the trunk as body size increases. Conversely, in water, the role of the axial skeleton in body support is reduced, and, in aquatic mammals, the vertebral column functions primarily in locomotion. Therefore, we hypothesize that the allometric stabilization associated with increasing body size in terrestrial mammals will be minimized in secondarily aquatic mammals. We test this by comparing the scaling exponent (slope) of vertebral measures from 57 terrestrial species (23 felids, 34 bovids) to 23 semi‐aquatic species (pinnipeds), using phylogenetically corrected regressions. Terrestrial taxa meet predictions of allometric stabilization, with posterior vertebral column (lumbar region) shortening, increased vertebral height compared to width, and shorter, more disc‐shaped centra. In contrast, pinniped vertebral proportions (e.g. length, width, height) scale with isometry, and in some cases, centra even become more spool‐shaped with increasing size, suggesting increased flexibility. Our results demonstrate that evolution of a secondarily aquatic lifestyle has modified the mechanical constraints associated with evolutionary increases in body size, relative to terrestrial taxa.