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.     

Modular functional organisation of the axial locomotor system in salamanders

Most investigations on tetrapod locomotion have been concerned with limb movements. However, there is compelling evidence that the axial musculoskeletal system contributes to important functions during locomotion. Adult salamanders offer a remarkable opportunity to examine these functions because these amphibians use axial undulations to propel themselves in both aquatic and terrestrial environments. In this article, we review the currently available biological data on axial functions during various locomotor modes in salamanders. We also present data showing the modular organisation of the neural networks that generate axial synergies during locomotion. The functional implication of this modular organisation is discussed.     

From lamprey to salamander: an exploratory modeling study on the architecture of the spinal locomotor networks in the salamander

The evolutionary transition from water to land required new locomotor modes and corresponding adjustments of the spinal “central pattern generators” for locomotion. Salamanders resemble the first terrestrial tetrapods and represent a key animal for the study of these changes. Based on recent physiological data from salamanders, and previous work on the swimming, limbless lamprey, we present a model of the basic oscillatory network in the salamander spinal cord, the spinal segment. Model neurons are of the Hodgkin–Huxley type. Spinal hemisegments contain sparsely connected excitatory and inhibitory neuron populations, and are coupled to a contralateral hemisegment. The model yields a large range of experimental findings, especially the NMDA-induced oscillations observed in isolated axial hemisegments and segments of the salamander Pleurodeles waltlii. The model reproduces most of the effects of the blockade of AMPA synapses, glycinergic synapses, calcium-activated potassium current, persistent sodium current, and $h$ -current. Driving segments with a population of brainstem neurons yields fast oscillations in the in vivo swimming frequency range. A minimal modification to the conductances involved in burst-termination yields the slower stepping frequency range. Slow oscillators can impose their frequency on fast oscillators, as is likely the case during gait transitions from swimming to stepping. Our study shows that a lamprey-like network can potentially serve as a building block of axial and limb oscillators for swimming and stepping in salamanders.     

A distance–performance trade‐off in the phenotypic basis of dispersal

Across taxa, individuals vary in how far they disperse, with most individuals staying close to their origin and fewer dispersing long distances. Costs associated with dispersal (e.g., energy, risk) are widely believed to trade off with benefits (e.g., reduced competition, increased reproductive success) to influence dispersal propensity. However, this framework has not been applied to understand variation in dispersal distance, which is instead generally attributed to extrinsic environmental factors. We alternatively hypothesized that variation in dispersal distances results from trade‐offs associated with other aspects of locomotor performance. We tested this hypothesis in the stream salamander Gyrinophilus porphyriticus and found that salamanders that dispersed farther in the field had longer forelimbs but swam at slower velocities under experimental conditions. The reduced swimming performance of long‐distance dispersers likely results from drag imposed by longer forelimbs. Longer forelimbs may facilitate moving longer distances, but the proximate costs associated with reduced swimming performance may help to explain the rarity of long‐distance dispersal. The historical focus on environmental drivers of dispersal distances misses the importance of individual traits and associated trade‐offs among traits affecting locomotion.     

Sprawling locomotion in the lizard Sceloporus clarkii: the effects of speed on gait, hindlimb kinematics, and axial bending during walking

Although the hindlimb is widely considered to provide the propulsive force in lizard locomotion, no study to date has analysed kinematic patterns of hindlimb movements for more than one stride for a single individual and no study has considered limb and axial kinematics together. In this study, kinematic data from several individuals of the Sceloporus clarkii are used to describe the movement patterns of the axial skeleton and hindlimb at different speeds, to analyse how kinematics change with speed, and to compare and contrast these findings with the inferred effects of speed cited in the literature. Angular limb movements and axial bending patterns (standing wave with nodes on the girdles) did not change with speed. Only the relative speed of retracting the femur and flexing the knee during limb retraction changes with speed. Based on these data and similar results from a recent study of salamanders, it appears that, over a range of speeds involving a walking trot, sprawling vertebrates increase speed by simply retracting the femur relatively faster, thus this simple functional adjustment may be a general mechanism to increase speed in tetrapods. The demonstration that femoral retraction alone is the major speed effector in Sceloporus clarkii lends strong functional support to ecomorphological implications of limb length (and especially femur length and caudifemoralis size) in locomotory ecology and performance in phrynosomatid lizards. It also lends support to inferences about the caudifemoralis muscle as a preadaptation to terrestrial locomotion and as a key innovation in the evolution of bipedalism.     

The Evolution of the Functional Role of Trunk Muscles During Locomotion in Adult Amphibians

SYNOPSIS. The axial musculature of all vertebrates consistsof two principal masses, the epaxial and hypaxial muscles. Theprimitive function of both axial muscle masses is to generatelateral bending of the trunk during swimming, as is seen inmost fishes. Within amphibians we see multiple functional andmorphological elaborations of the axial musculature. These elaborationsappear to be associated not only with movement into terrestrialhabits (salamanders), but also with subsequent locomotor specializationsof two of the three major extant amphibian clades (frogs andcaecilians). Salamanders use both epaxial and hypaxial musclesto produce lateral bending during swimming and terrestrial,quadrupedal locomotion. However during terrestrial locomotionthe hypaxial muscles are thought to perform an added function,resisting long-axis torsion of the trunk. Relative to salamanders,frogs have elaborate epaxial muscles, which function to bothstabilize and extend the iliosacral and coccygeosacral joints.These actions are important in the effective use of the hindlimbsduring terrestrial saltation and swimming. In contrast, caecilianshave relatively elaborate hypaxial musculature that is linkedto a helix of connective tissue embedded in the skin. The helixand associated hypaxial muscles form a hydrostatic skeletonaround the viscera that is continuously used to maintain bodyposture and also contributes to forward force production duringburrowing.     

Aquatic and terrestrial locomotory energetics in a toad and a turtle: a search for generalisations among ectotherms

Murray short-necked turtles were trained to walk on a motorised treadmill and to swim in a recirculating flume. Through filmed records, the frequency of limb movement and the time that thrust was directed against the substrate were measured. The animals wore masks when walking and accessed air when swimming from a ventilated capsule placed on top of the water surface. Measurement of the exhalant O(2) and CO(2) levels from these devices enabled the measurement of metabolic rates. Equivalent data were obtained from swimming and hopping cane toads, although repeatable measures of limb frequency and contact times were not obtained due to the intermittent form of locomotion in this species. Comparing the cost of transport, the energy required to transport a mass of animal over a unit distance, with other animals showed that toads do not have a cheap form of terrestrial locomotion, but turtles do; turtles use half the cost predicted from their body mass. This economy of locomotion is consistent with what is known about turtle muscle, the mechanics of their gait, and the extremely long contact time for a limb with the substrate. Swimming in toads is energetically expensive, whereas turtles, on the basis of mass, use about the same energy to transport a unit mass as an equivalent-size fish. The data were compared with the predictions of the Kram-Taylor hypothesis for locomotory scaling, and walking turtles were found to provide a numerical fit. The data show that both terrestrial and aquatic locomotory energetics in toads are generally higher than predictions on the basis of mass, whereas in turtles they are lower.     

Neither season nor sex affects the cost of terrestrial locomotion in a circumpolar diving duck: the common eider (Somateria mollissima)

Locomotion accounts for a significant proportion of the energy budget in birds, and selection is likely to act on its economy, particularly where energy conservation is essential for survival. Birds are capable of different forms of locomotion, such as walking/running, swimming, diving and flying, and adaptations for these affect the energetic cost [cost of locomotion (CoL)] and kinematics of terrestrial locomotion. Furthermore, seasonal changes in climate and photoperiod elicit physiological and behavioural adaptations for survival and reproduction, which also influence energy budget. However, little is understood about how this might affect the CoL. Birds are also known to exhibit sex differences in size, behaviour and physiology; however, sex differences in terrestrial locomotion have only been studied in two cursorially adapted galliform species in which males achieved higher maximum speeds, and in one case had a lower mass-specific CoL than females. Here, using respirometry and high-speed video recordings, we sought to determine whether season and sex would affect the CoL and kinematics of a principally aquatic diving bird: the circumpolar common eider (Somateria mollissima). We demonstrate that eiders are only capable of a walking gait and exhibit no seasonal or sex differences in mass-specific CoL or maximum speed. Despite sharing identical limb morphometrics, the birds exhibited subtle sex differences in kinematic parameters linked to the greater body mass of the males. We suggest that their principally aquatic lifestyle accounts for the observed patterns in their locomotor performance. Furthermore, sex differences in the CoL may only be found in birds in which terrestrial locomotion directly influences male reproductive success.     

Dynamic plantar pressure distribution during terrestrial locomotion of bonobos (Pan paniscus)

We collected high-resolution plantar pressure distributions of seven bonobos during terrestrial bipedal and quadrupedal locomotion (N = 146). Functional foot length, degree of hallux abduction, and total contact time were determined, and plots, showing pressure as a function of time for six different foot regions, were generated. We also studied five adult humans for comparison (N = 13). Both locomotion types of the bonobo show a large variation in plantar pressure distributions, which could be due to the interference of instantaneous behavior with locomotion and differences in walking speed and body dimensions. The heel and the lateral midfoot typically touch down simultaneously at initial ground contact in bipedal and quadrupedal walking of bonobos, in contrast with the typical heel-strike of human bipedalism. The center of pressure follows a curved course during quadrupedalism, as a consequence of the medial weight transfer during mid-stance. Bipedal locomotion of bonobos is characterized by a more plantar positioning of the feet and by a shorter contact time than during quadrupedal walking, according to a smaller stride and step length at a higher frequency. We observed a varus position of the foot with an abducted hallux, which likely possesses an important sustaining and stabilizing function during terrestrial locomotion.     

From swimming to walking: a single basic network for two different behaviors

 In this paper we consider the hypothesis that the spinal locomotor network controlling trunk movements has remained essentially unchanged during the evolutionary transition from aquatic to terrestrial locomotion. The wider repertoire of axial motor patterns expressed by amphibians would then be explained by the influence from separate limb pattern generators, added during this evolution. This study is based on EMG data recorded in vivo from epaxial musculature in the newt Pleurodeles waltl during unrestrained swimming and walking, and on a simplified model of the lamprey spinal pattern generator for swimming. Using computer simulations, we have examined the output generated by the lamprey model network for different input drives. Two distinct inputs were identified which reproduced the main features of the swimming and walking motor patterns in the newt. The swimming pattern is generated when the network receives tonic excitation with local intensity gradients near the neck and girdle regions. To produce the walking pattern, the network must receive (in addition to a tonic excitation at the girdles) a phasic drive which is out of phase in the neck and tail regions in relation to the middle part of the body. To fit the symmetry of the walking pattern, however, the intersegmental connectivity of the network had to be modified by reversing the direction of the crossed inhibitory pathways in the rostral part of the spinal cord. This study suggests that the input drive required for the generation of the distinct walking pattern could, at least partly, be attributed to mechanosensory feedback received by the network directly from the intraspinal stretch-receptor system. Indeed, the input drive required resembles the pattern of activity of stretch receptors sensing the lateral bending of the trunk, as expressed during walking in urodeles. Moreover, our results indicate that a nonuniform distribution of these stretch receptors along the trunk can explain the discontinuities exhibited in the swimming pattern of the newt. Thus, separate limb pattern generators can influence the original network controlling axial movements not only through a direct coupling at the central level but also via a mechanical coupling between trunk and limbs, which in turn influences the sensory signals sent back to the network. Taken together, our findings support the hypothesis of a phylogenetic conservatism of the spinal locomotor networks generating axial motor patterns from agnathans to amphibians. Received: 12 October 2001 / Accepted in revised form: 16 May 2002 Correspondence to: T. Bem (e-mail: tiaza.bem@ibib.waw.pl)     

Morphology and mechanics of myosepta in a swimming salamander (Siren lacertina)

In contrast to the complex, three-dimensional shape of myomeres in teleost fishes, the lateral hypaxial muscles of salamanders are nearly planar and their myosepta run in a roughly straight line from mid-lateral to mid-ventral. We used this relatively simple system as the basis for a mathematical model of segmented musculature. Model results highlight the importance of the mechanics of myosepta in determining the shortening characteristics of a muscle segment. We used sonomicrometry to measure the longitudinal deformation of myomeres and the dorsoventral deformation of myosepta in a swimming salamander (Siren lacertina). Sonomicrometry results show that the myosepta allow some dorsoventral lengthening, indicating an amplification of myomere shortening that is greater than that produced by muscle fiber angle alone (10% muscle fiber shortening produces 28.7% myomere shortening). Polarized light and DIC microscopy of isolated hypaxial myosepta revealed that the collagen fiber orientation in hypaxial myomeres is primarily mediolateral. The mediolateral collagen fiber orientation, combined with our finding that the hypaxial myosepta lengthen dorsoventrally during swimming, suggests that one possible function of hypaxial myosepta in S. lacertina is to increase the strain amplification of the muscle fibers by reducing the mediolateral bulging of the myomeres and redirecting the bulging toward the dorsoventral direction.     

Swimming performance in semiaquatic and terrestrial Oryzomyine rodents

Semiaquatic and terrestrial mammals frequently have to cross or move along water bodies, both trying to remain on the water surface using one or two pairs of limbs, combining different gaits and stride lengths and frequencies. This is the case of the semiaquatic water rats Nectomys and the cursorial Cerradomys, sister genera of the Oryzomyini tribe, capable of swimming using similar gaits. They provide an opportunity to investigate performance specializations involving the semiaquatic habitat, our objective in this study. Rodents were filmed at 30 frames s⁻¹ in lateral view, swimming in a glass aquarium. Video sequences were analyzed dividing the swimming cycle into power and recovery phases. Differences in swimming performance were detected between species of Nectomys and Cerradomys, but not between species of the same genus. Absolute mean speed did not differ between the semiaquatic and terrestrial groups, but the semiaquatic Nectomys had longer stride lengths with lower stride frequency, whereas the terrestrial Cerradomys had higher stride frequency and relative swimming speed. The widest behavior repertoire of Nectomys allowed more efficient, but not necessarily faster swimming than the terrestrial Cerradomys. Efficient aquatic locomotion in Nectomys is ultimately a result of improved buoyancy by hydrophobic fur and subtle morphological specializations, which allow this genus to perform more efficiently in water than the terrestrial Cerradomys without compromising locomotion in the terrestrial environment.     

Tetrapod-like axial regionalization in an early ray-finned fish

Tetrapods possess up to five morphologically distinct vertebral series: cervical, thoracic, lumbar, sacral and caudal. The evolution of axial regionalization has been linked to derived Hox expression patterns during development and the demands of weight-bearing and walking on land. These evolutionary and functional explanations are supported by an absence of similar traits in fishes, living and extinct. Here, I show that, Tarrasius problematicus, a marine ray-finned fish from the Mississippian (Early Carboniferous; 359-318 Ma) of Scotland, is the first non-tetrapod known to possess tetrapod-like axial regionalization. Tarrasius exhibits five vertebral regions, including a seven-vertebrae 'cervical' series and a reinforced 'sacrum' over the pelvic area. Most vertebrae possess processes for intervertebral contact similar to tetrapod zygapophyses. The fully aquatic Tarrasius evolved these morphologies alongside other traits convergent with early tetrapods, including a naked trunk, and a single median continuous fin. Regional modifications in Tarrasius probably facilitated pelagic swimming, rather than a terrestrial lifestyle or walking gait, presenting an alternative scenario for the evolution of such traits in tetrapods. Axial regionalization in Tarrasius could indicate tetrapod-like Hox expression patterns, possibly representing the primitive state for jawed vertebrates. Alternately, it could signal a weaker relationship, or even a complete disconnect, between Hox expression domains and vertebrate axial plans.     

Locomotion patterns in two South American gymnophthalmid lizards: Vanzosaura rubricauda and Procellosaurinus tetradactylus

We quantified gait and stride characteristics (velocity, frequency, stride length, stance and swing duration, and duty factor) in the bursts of locomotion of two small, intermittently moving, closely related South American gymnophthalmid lizards: Vanzosaura rubricauda and Procellosaurinus tetradactylus. They occur in different environments: V. rubricauda is widely distributed in open areas with various habitats and substrates, while P. tetradactylus is endemic to dunes in the semi-arid Brazilian Caatinga. Both use trot or walking trot characterised by a lateral sequence. For various substrates in a gradient of roughness (perspex, cardboard, sand, gravel), both species have low relative velocities in comparison with those reported for larger continuously moving lizards. To generate velocity, these animals increase stride frequency but decrease relative stride length. For these parameters, P. tetradactylus showed lower values than V. rubricauda. In their relative range of velocities, no significant differences in stride length and frequency were recorded for gravel. However, the slopes of a correlation between velocity and its components were lower in P. tetradactylus on cardboard, whereas on sand this was only observed for velocity and stride length. The data showed that the difference in rhythmic parameters between both species increased with the smoothness of the substrates. Moreover, P. tetradactylus shows a highly specialised locomotor strategy involving lower stride length and frequency for generating lower velocities than in V. rubricauda. This suggests the evolution of a central motor pattern generator to control slower limb movements and to produce fewer and longer pauses in intermittent locomotion.     

Issues for Aquatic Pedestrian Locomotion

Aquatic pedestrian locomotion represents an important mode oflocomotion for many aquatic and amphibious animals, both extantand extinct. Unlike terrestrial locomotion where weight is thedefining force, in aquatic locomotion buoyancy and hydrodynamicforces may be as important as weight. Aquatic pedestrian locomotiondiffers fundamentally from swimming because pedestrians mustmaintain contact with the substratum in order to locomote. Ambientwater motion may constrain or prevent locomotion of aquaticpedestrians by requiring that they actively grip the substratum.A comprehensive biomechanical analysis of aquatic pedestrianlocomotion will require an integration of hydrodynamics withterrestrial locomotor dynamics.     

Comparison between aquatic and terrestrial locomotions of the leatherback sea turle (Dermochelys coriacea)

Kinematic characteristics of the fore- and hindlimb displacements during terrestrial and aquatic locomotions in juvenile marine turtles Dermochelys coriacea are compared. Modulations of the spatial displacements of the limbs and durations of the stance and swing phases are analysed in relationship with the constraints of the aquatic and terrestrial environments. The stance and swing phases used for describing the aquatic locomotion are re-evaluated in the light of the spatial displacements of the forelimbs during complete beating cycles.     

Linking the evolution of habitat choice to ecosystem functioning: direct and indirect effects of pond-reproducing fire salamanders on aquatic-terrestrial subsidies

Shifts in life history traits and in the behaviour of species can potentially alter ecosystem functioning. The reproduction of the central European fire salamander (Salamandra salamandra), which usually deposits its larvae in first-order streams, in small pool and pond-like habitats, is an example of a recent local adaptation in this species. Here we aimed to quantify the direct and indirect effects of the predatory larvae on the aquatic food webs in the ponds and on the flux of matter between the ponds and adjacent terrestrial habitats. Our estimates are based on biomass data of the present pond fauna as well as on the analysis of stomach content data, growth rates and population dynamics of the salamander larvae in pond habitats. By their deposition of larvae in early spring, female fire salamanders import between 0.07 and 2.86 g dry mass m^?2 larval biomass into the ponds. Due to high mortality rates in the larval phase and the relatively small size at metamorphosis of the pond-adapted salamanders compared to stream-adapted ones, the biomass export of the metamorphosed salamanders clearly falls below the initial biomass import. Catastrophic events such as high water temperatures and low oxygen levels may even occasionally result in mass mortalities of salamander larvae and thus in a net 100 % import of the salamander biomass into the pond food webs. Indirect effects further accelerate this net import of matter into the aquatic habitat, e.g. the feeding of salamanders on aquatic insect larvae with the emergence of terrestrial adults—thus preventing export—and on terrestrial organisms that fall on the water surface (supporting import). This study demonstrates that the adaptation of salamanders to pond reproduction can alter food web linkages across ecosystem boundaries by enhancing the flux of materials and energy from terrestrial (i.e. forest) to the aquatic (i.e. pond) habitat.     

Perceived predation risk as a function of predator dietary cues in terrestrial salamanders

Prey often avoid predator chemical cues, and in aquatic systems, prey may even appraise predation risk via cues associated with the predator's diet. However, this relationship has not been shown for terrestrial predator-prey systems, where the proximity of predators and prey, and the intensity of predator chemical cues in the environment, may be less than in aquatic systems. In the laboratory, we tested behavioural responses (avoidance, habituation and activity) of terrestrial red-backed salamanders, Plethodon cinereus, to chemical cues from garter snakes, Thamnophis sirtalis, fed either red-backed salamanders or earthworms (Lumbricus spp.). We placed salamanders in arenas lined with paper towels pretreated with snake chemicals, and monitored salamander movements during 120 min. Salamanders avoided substrates preconditioned by earthworm-fed (avoidanceX+/-SE=91.1+/-2.5%, N=25) and salamander-fed (95.2+/-2.5%, N=25) snakes, when tested against untreated substrate (control). Salamanders avoided cues from salamander-fed snakes more strongly (75.2+/-5.5%, N=25) than earthworm-fed snakes when subjected to both treatments simultaneously, implying that salamanders were sensitive to predator diet. Salamanders tended to avoid snake substrate more strongly during the last 60 min of a trial, but activity patterns were similar between salamanders exposed exclusively to control substrate versus those subject to snake cues. In another experiment, salamanders failed to avoid cues from dead conspecifics, suggesting that the stronger avoidance of salamander-fed snakes in the previous experiment was not directly due to chemical cues emitted by predator-killed salamanders. Salamanders also did not discriminate between cues from a salamander-fed snake versus a salamander-fed snake that was recently switched (i.e. <14 days) to an earthworm diet. Our results imply that terrestrial salamanders are sensitive to perceived predation risk via by-products of predator diet, and that snake predators rather than dead salamanders may be largely responsible for the release of such chemicals. Copyright 1999 The Association for the Study of Animal Behaviour.