Publications by authors named "Richard W Blob"

59 Publications

Bendy to the bone: Links between vertebral morphology and waterfall climbing in amphidromous gobioid fishes.

J Anat 2021 Apr 29. Epub 2021 Apr 29.

Department of Biological Sciences, Clemson University, Clemson, SC, USA.

Locomotor force production imposes strong demands on organismal form. Thus, the evolution of novel locomotor modes is often associated with morphological adaptations that help to meet those demands. In the goby lineage of fishes, most species are marine and use their fused pelvic fins to facilitate station holding in wave-swept environments. However, several groups of gobies have evolved an amphidromous lifecycle, in which larvae develop in the ocean but juveniles migrate to freshwater for their adult phase. In many of these species, the pelvic fins have been co-opted to aid in climbing waterfalls during upstream migrations to adult habitats. During horizontal swimming, forces are produced by axial musculature pulling on the vertebral column. However, during vertical climbing, gravity also exerts forces along the length of the vertebral column. In this study, we searched for novel aspects of vertebral column form that might be associated with the distinctive locomotor strategies of climbing gobies. We predicted that stiffness would vary along the length of the vertebral column due to competing demands for stability of the suction disk anteriorly and flexibility for axial thrust production posteriorly. We also predicted that derived, climbing goby species would require stiffer backbones to aid in vertical thrust production compared to non-climbing species. To test these predictions, we used microcomputed tomography scans to compare vertebral anatomy (centrum length, centrum width, and intervertebral space) along the vertebral column for five gobioid species that differ in climbing ability. Our results support our second prediction, that gobies are more flexible in the posterior portion of the body. However, the main variation in vertebral column form associated with climbing ability was the presence of larger intervertebral spaces in Sicyopterus stimpsoni, a species that uses a distinctive inching behavior to climb. These results build on past kinematic studies of goby climbing performance and lend insights into how the underlying vertebral structure of these fishes may enable their novel locomotion.
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http://dx.doi.org/10.1111/joa.13449DOI Listing
April 2021

Sticking to it: testing passive pull-off forces in waterfall-climbing fishes across challenging substrates.

J Exp Biol 2021 01 21;224(Pt 2). Epub 2021 Jan 21.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

The pelvic sucker of Hawaiian waterfall climbing gobies allows these fishes to attach to substrates while climbing waterfalls tens to hundreds of meters tall. Climbing ability varies by species and may be further modulated by the physical characteristics of the waterfall substrate. In this study, we investigated the influence of surface wettability (hydrophobic versus hydrophilic surface charges) and substrate roughness on the passive adhesive system of four species of gobies with different climbing abilities. Overall, passive adhesive performance varied by species and substrate, with the strongest climbers showing the highest shear pull-off forces, particularly on rough surfaces. Thus, differences in passive adhesive performance may help to explain the ability of some species to migrate further upstream than others and contribute to their ability to invade new habitats.
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http://dx.doi.org/10.1242/jeb.228718DOI Listing
January 2021

Functional correlations of axial muscle fiber type proportions in the waterfall-climbing Hawaiian stream fish Sicyopterus stimpsoni.

J Anat 2020 06 24;236(6):1160-1166. Epub 2020 Feb 24.

Aquatic Toxicology Laboratory, St. Cloud State University, St. Cloud, MN, USA.

Assessing the factors that contribute to successful locomotor performance can provide critical insight into how animals survive in challenging habitats. Locomotion is powered by muscles, so that differences in the relative proportions of red (slow-oxidative) vs. white (fast-glycolytic) fibers can have significant implications for locomotor performance. We compared the relative proportions of axial red muscle fibers between groups of juveniles of the amphidromous gobiid fish, Sicyopterus stimpsoni, from the Hawaiian Islands. Juveniles of this species migrate from the ocean into freshwater streams, navigating through a gauntlet of predators that require rapid escape responses, before reaching waterfalls which must be climbed (using a slow, inching behavior) to reach adult breeding habitats. We found that fish from Kaua'i have a smaller proportion of red fibers in their tail muscles than fish from Hawai'i, matching expectations based on the longer pre-waterfall stream reaches of Kaua'i that could increase exposure to predators, making reduction of red muscle and increases in white muscle advantageous. However, no difference in red muscle proportions was identified between fish that were either successful or unsuccessful in scaling model waterfalls during laboratory climbing trials, suggesting that proportions of red muscle are near a localized fitness peak among Hawaiian individuals.
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http://dx.doi.org/10.1111/joa.13169DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7219618PMC
June 2020

Variation in limb loading magnitude and timing in tetrapods.

J Exp Biol 2020 01 27;223(Pt 2). Epub 2020 Jan 27.

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA.

Comparative analyses of locomotion in tetrapods reveal two patterns of stride cycle variability. Tachymetabolic tetrapods (birds and mammals) have lower inter-cycle variation in stride duration than bradymetabolic tetrapods (amphibians, lizards, turtles and crocodilians). This pattern has been linked to the fact that birds and mammals share enlarged cerebella, relatively enlarged and heavily myelinated Ia afferents, and γ-motoneurons to their muscle spindles. Both tachymetabolic tetrapod lineages also possess an encapsulated Golgi tendon morphology, thought to provide more spatially precise information on muscle tension. The functional consequence of this derived Golgi tendon morphology has never been tested. We hypothesized that one advantage of precise information on muscle tension would be lower and more predictable limb bone stresses, achieved in tachymetabolic tetrapods by having less variable substrate reaction forces than bradymetabolic tetrapods. To test this hypothesis, we analyzed hindlimb substrate reaction forces during locomotion of 55 tetrapod species in a phylogenetic comparative framework. Variation in species means of limb loading magnitude and timing confirm that, for most of the variables analyzed, variance in hindlimb loading and timing is significantly lower in species with encapsulated versus unencapsulated Golgi tendon organs. These findings suggest that maintaining predictable limb loading provides a selective advantage for birds and mammals by allowing energy savings during locomotion, lower limb bone safety factors and quicker recovery from perturbations. The importance of variation in other biomechanical variables in explaining these patterns, such as posture, effective mechanical advantage and center-of-mass mechanics, remains to be clarified.
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http://dx.doi.org/10.1242/jeb.201525DOI Listing
January 2020

Pectoral and pelvic girdle rotations during walking and swimming in a semi-aquatic turtle: testing functional role and constraint.

J Exp Biol 2019 12 12;222(Pt 24). Epub 2019 Dec 12.

Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA.

Pectoral and pelvic girdle rotations play a substantial role in enhancing stride length across diverse tetrapod lineages. However, the pectoral and pelvic girdle attach the limbs to the body in different ways and may exhibit dissimilar functions, especially during locomotion in disparate environments. Here, we tested for functional differences between the forelimb and hindlimb of the freshwater turtle during walking and swimming using X-ray reconstruction of moving morphology (XROMM). In doing so, we also tested the commonly held notion that the shell constrains girdle motion in turtles. We found that the pectoral girdle exhibited greater rotations than the pelvic girdle on land and in water. Additionally, pelvic girdle rotations were greater on land than in water, whereas pectoral girdle rotations were similar in the two environments. These results indicate that although the magnitude of pelvic girdle rotations depends primarily on whether the weight of the body must be supported against gravity, the magnitude of pectoral girdle rotations likely depends primarily on muscular activity associated with locomotion. Furthermore, the pectoral girdle of turtles rotated more than has been observed in other taxa with sprawling postures, showing an excursion similar to that of mammals (∼38 deg). These results suggest that a rigid axial skeleton and internally positioned pectoral girdle have not constrained turtle girdle function, but rather the lack of lateral undulations in turtles and mammals may contribute to a functional convergence whereby the girdle acts as an additional limb segment to increase stride length.
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http://dx.doi.org/10.1242/jeb.212688DOI Listing
December 2019

The Translation of Movement From the Equine to Rider With Relevance for Hippotherapy.

J Equine Vet Sci 2019 06 28;77:125-131. Epub 2019 Feb 28.

Department of Bioengineering, Clemson University, Clemson, SC. Electronic address:

Although horseback riding is a well-established means of rehabilitation therapy for a variety of human patients, there are few data on the biomechanical relationships between horse and rider during such hippotherapy. We simultaneously tracked the movements of a horse with several different novice riders, under conditions similar to hippotherapy, to evaluate whether horses pass the same motion to different riders while being lead at a walk. Riders were outfitted with a goniometric data collection system that recorded the angles of flexion and extension and lateral bending of the thoracic and lumbar spine, as well as the flexion, extension, abduction, and adduction of each hip. We found consistent rhythmic motion in the horse's hock, shoulder, and knee. There were no significant differences in equine movement across six different riders, supporting the conclusion that horses can be used as a reproducible rehabilitation platform for riders. Moreover, although riders demonstrated different baseline postures, there were no significant differences in their ranges of motion in each joint. These results indicate that a horse can reproducibly influence a population of participants in a hippotherapy situation.
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http://dx.doi.org/10.1016/j.jevs.2019.02.017DOI Listing
June 2019

Evidence of local adaptation in a waterfall-climbing Hawaiian goby fish derived from coupled biophysical modeling of larval dispersal and post-settlement selection.

BMC Evol Biol 2019 04 11;19(1):88. Epub 2019 Apr 11.

Department of Biological Sciences, Clemson University, Clemson, SC, 29634, USA.

Background: Local adaptation of marine and diadromous species is thought to be a product of larval dispersal, settlement mortality, and differential reproductive success, particularly in heterogeneous post-settlement habitats. We evaluated this premise with an oceanographic passive larval dispersal model coupled with individual-based models of post-settlement selection and reproduction to infer conditions that underlie local adaptation in Sicyopterus stimpsoni, an amphidromous Hawaiian goby known for its ability to climb waterfalls.

Results: Our model results demonstrated that larval dispersal is spatio-temporally asymmetric, with more larvae dispersed from the southeast (the Big Island) to northwest (Kaua'i) along the archipelago, reflecting prevailing conditions such as El Niño/La Niña oscillations. Yet connectivity is nonetheless sufficient to result in homogenous populations across the archipelago. We also found, however, that ontogenetic shifts in habitat can give rise to adaptive morphological divergence when the strength of predation-driven post-settlement selection crosses a critical threshold. Notably, our simulations showed that larval dispersal is not the only factor determining the likelihood of morphological divergence. We found adaptive potential and evolutionary trajectories of S. stimpsoni were greater on islands with stronger environmental gradients and greater variance in larval cohort morphology due to fluctuating immigration.

Conclusions: Contrary to expectation, these findings indicate that immigration can act in concert with selection to favor local adaptation and divergence in species with marine larval dispersal. Further development of model simulations, parameterized to reflect additional empirical estimates of abiotic and biotic factors, will help advance our understanding of the proximate and ultimate mechanisms driving adaptive evolution, population resilience, and speciation in marine-associated species.
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http://dx.doi.org/10.1186/s12862-019-1413-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6458715PMC
April 2019

Comparative limb bone scaling in turtles: Phylogenetic transitions with changes in functional demands?

J Morphol 2019 04 27;280(4):593-603. Epub 2019 Feb 27.

Department of Biological Sciences, Clemson University, Clemson, South Carolina.

Several terrestrial vertebrate clades include lineages that have evolved nearly exclusive use of aquatic habitats. In many cases, such transitions are associated with the evolution of flattened limbs that are used to swim via dorsoventral flapping. Such changes in shape may have been facilitated by changes in limb bone loading in novel aquatic environments. Studies on limb bone loading in turtles found that torsion is high relative to bending loads on land, but reduced compared to bending during aquatic rowing. Release from torsion among rowers could have facilitated the evolution of hydrodynamically advantageous flattened limbs among aquatic species. Because rowing is regarded as an intermediate locomotor stage between walking and flapping, rowing species might show limb bone flattening intermediate between the tubular shapes of walkers and the flattened shapes of flappers. We collected measurements of humeri and femora from specimens representing four functionally divergent turtle clades: sea turtles (marine flappers), softshells (specialized freshwater rowers), emydids (generalist semiaquatic rowers), and tortoises (terrestrial walkers). Patterns of limb bone scaling with size were compared across lineages using phylogenetic comparative methods. Although rowing taxa did not show the intermediate scaling patterns we predicted, our data provide other functional insights. For example, flattening of sea turtle humeri was associated with positive allometry (relative to body mass) for the limb bone diameter perpendicular to the flexion-extension plane of the elbow. Moreover, softshell limb bones exhibit positive allometry of femoral diameters relative to body mass, potentially helping them maintain their typical benthic position in water by providing additional weight to compensate for shell reduction. Tortoise limb bones showed positive allometry of diameters, as well as long humeri, relative to body mass, potentially reflecting specializations for resisting loads associated with digging. Overall, scaling patterns of many turtle lineages appear to correlate with distinctive behaviors or locomotor habits.
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http://dx.doi.org/10.1002/jmor.20968DOI Listing
April 2019

The impact of keels and tails on turtle swimming performance and their potential as models for biomimetic design.

Bioinspir Biomim 2018 11 7;14(1):016002. Epub 2018 Nov 7.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, United States of America. Author to whom any correspondence should be addressed.

Stability and turning performance are two key metrics of locomotor performance in animals, and performance in both of these metrics can be improved through a variety of morphological structures. Aquatic vehicles are often designed with keels and rudders to improve their stability and turning performance, but how keels and rudders function in rigid-bodied animals is less understood. Aquatic turtles are a lineage of rigid-bodied animals that have the potential to function similarly to engineered vehicles, and also might make use of keels and rudders to improve their stability and turning performance. To test these possibilities, we trained turtles to follow a mechanically controlled prey stimulus under three sets of conditions: with no structural modifications, with different sized and shaped keels, and with restricted tail use. We predicted that keels in turtles would function similarly to those in aquatic vehicles to reduce oscillations, and that turtles would use the tail like a rudder to reduce oscillations and improve turning performance. We found that the keel designs we tested did not reduce oscillations in turtles, but that the tail was used similarly to a rudder, with benefits to both the magnitude of oscillations they experienced and turning performance. These data show how variation in the accessory structures of rigid-bodied animals can impact swimming performance, and suggest that such variation among turtles could serve as a biomimetic model in designing aquatic vehicles that are stable as well as maneuverable and agile.
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http://dx.doi.org/10.1088/1748-3190/aae906DOI Listing
November 2018

Biomechanical factors influencing successful self-righting in the pleurodire turtle .

J Exp Biol 2018 07 17;221(Pt 14). Epub 2018 Jul 17.

Department of Biological Sciences, Clemson University, Clemson, SC 29631, USA

Self-righting performance is a key ability for most terrestrial animals, and has been used as a metric of fitness, exhaustion and thermal limits in a variety of taxa. However, there is little understanding of the underlying mechanisms that drive variation in self-righting performance. To evaluate the mechanical factors that contribute to success versus failure when animals attempt to self-right, we compared force production and kinematic behavior in the rigid-bodied, pleurodire turtle between successful and unsuccessful self-righting efforts. We found that the moment exerted during efforts to roll the body and the velocity of that roll are the primary drivers behind self-righting success. Specifically, turtles that self-righted successfully produced both larger moments and faster rolls than turtles that failed. In contrast, the angle at which the head was directed to lever the body and the extent of yaw that was incorporated in addition to roll had little impact on the likelihood of success. These results show that specific performance metrics can predict the ability of animals to self-right, providing a framework for biomimetic applications as well as future comparisons to test for differences in self-righting performance across animals from different environments, sexes, populations and species.
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http://dx.doi.org/10.1242/jeb.182642DOI Listing
July 2018

Humeral loads during swimming and walking in turtles: implications for morphological change during aquatic reinvasions.

J Exp Biol 2017 11 7;220(Pt 21):3873-3877. Epub 2017 Sep 7.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

During evolutionary reinvasions of water by terrestrial vertebrates, ancestrally tubular limb bones often flatten to form flippers. Differences in skeletal loading between land and water might have facilitated such changes. In turtles, femoral shear strains are significantly lower during swimming than during walking, potentially allowing a release from loads favoring tubular shafts. However, flipper-like morphology in specialized tetrapod swimmers is most accentuated in the forelimbs. To test whether the forelimbs of turtles also experience reduced torsional loading in water, we compared strains on the humerus of river cooters () between swimming and terrestrial walking. We found that humeral shear strains are also lower during swimming than during terrestrial walking; however, this appears to relate to a reduction in overall strain magnitude, rather than a specific reduction in twisting. These results indicate that shear strains show similar reductions between swimming and walking for forelimb and hindlimb, but these reductions are produced through different mechanisms.
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http://dx.doi.org/10.1242/jeb.156836DOI Listing
November 2017

Data Management Rubric for Video Data in Organismal Biology.

Integr Comp Biol 2017 07;57(1):33-47

Department of Biology, California State University Fresno, 2555 E San Ramon Avenue, Fresno, CA 93740, USA.

Synopsis: Standards-based data management facilitates data preservation, discoverability, and access for effective data reuse within research groups and across communities of researchers. Data sharing requires community consensus on standards for data management, such as storage and formats for digital data preservation, metadata (i.e., contextual data about the data) that should be recorded and stored, and data access. Video imaging is a valuable tool for measuring time-varying phenotypes in organismal biology, with particular application for research in functional morphology, comparative biomechanics, and animal behavior. The raw data are the videos, but videos alone are not sufficient for scientific analysis. Nearly endless videos of animals can be found on YouTube and elsewhere on the web, but these videos have little value for scientific analysis because essential metadata such as true frame rate, spatial calibration, genus and species, weight, age, etc. of organisms, are generally unknown. We have embarked on a project to build community consensus on video data management and metadata standards for organismal biology research. We collected input from colleagues at early stages, organized an open workshop, "Establishing Standards for Video Data Management," at the Society for Integrative and Comparative Biology meeting in January 2017, and then collected two more rounds of input on revised versions of the standards. The result we present here is a rubric consisting of nine standards for video data management, with three levels within each standard: good, better, and best practices. The nine standards are: (1) data storage; (2) video file formats; (3) metadata linkage; (4) video data and metadata access; (5) contact information and acceptable use; (6) camera settings; (7) organism(s); (8) recording conditions; and (9) subject matter/topic. The first four standards address data preservation and interoperability for sharing, whereas standards 5-9 establish minimum metadata standards for organismal biology video, and suggest additional metadata that may be useful for some studies. This rubric was developed with substantial input from researchers and students, but still should be viewed as a living document that should be further refined and updated as technology and research practices change. The audience for these standards includes researchers, journals, and granting agencies, and also the developers and curators of databases that may contribute to video data sharing efforts. We offer this project as an example of building community consensus for data management, preservation, and sharing standards, which may be useful for future efforts by the organismal biology research community.
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http://dx.doi.org/10.1093/icb/icx060DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5886321PMC
July 2017

A novel, bounding gait in swimming turtles: implications for aquatic locomotor diversity.

J Exp Biol 2017 10 14;220(Pt 20):3611-3615. Epub 2017 Aug 14.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Turtles are an iconic lineage in studies of animal locomotion, typifying the use of slow, alternating footfalls during walking. Alternating movements of contralateral limbs are also typical during swimming gaits for most freshwater turtles. Here, we report a novel gait in turtles, in which the pleurodire swims using a bounding gait that coordinates bilateral protraction of both forelimbs with bilateral retraction of both hindlimbs. Use of this bounding gait is correlated with increased limb excursion and decreased stride frequency, but not increased velocity when compared with standard swimming strokes. Bounding by provides a second example of a non-mammalian lineage that can use bounding gaits, and may give insight into the evolution of aquatic flapping. Parallels in limb muscle fascicle properties between bounding turtles and crocodylids suggest a possible musculoskeletal mechanism underlying the use of bounding gaits in particular lineages.
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http://dx.doi.org/10.1242/jeb.164103DOI Listing
October 2017

Hindlimb muscle function in turtles: is novel skeletal design correlated with novel muscle function?

J Exp Biol 2017 07 5;220(Pt 14):2554-2562. Epub 2017 May 5.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Variations in musculoskeletal lever systems have formed an important foundation for predictions about the diversity of muscle function and organismal performance. Changes in the structure of lever systems may be coupled with changes in muscle use and give rise to novel muscle functions. The two extant turtle lineages, cryptodires and pleurodires, exhibit differences in hindlimb structure. Cryptodires possess the ancestral musculoskeletal morphology, with most hip muscles originating on the pelvic girdle, which is not fused to the shell. In contrast, pleurodires exhibit a derived morphology, in which fusion of the pelvic girdle to the shell has resulted in shifts in the origin of most hip muscles onto the interior of the shell. To test how variation in muscle arrangement might influence muscle function during different locomotor behaviors, we combined measurements of muscle leverage in five major hindlimb muscles with data on muscle use and hindlimb kinematics during swimming and walking in representative semiaquatic cryptodire () and pleurodire () species. We found substantial differences in muscle leverage between the two species. Additionally, we found that there were extensive differences in muscle use in both species, especially while walking, with some pleurodire muscles exhibiting novel functions associated with their derived musculoskeletal lever system. However, the two species shared similar overall kinematic profiles within each environment. Our results suggest that changes in limb lever systems may relate to changes in limb muscle motor patterns and kinematics, but that other factors must also contribute to differences in muscle activity and limb kinematics between these taxa.
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http://dx.doi.org/10.1242/jeb.157792DOI Listing
July 2017

One foot out the door: limb function during swimming in terrestrial versus aquatic turtles.

Biol Lett 2017 Jan;13(1)

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Specialization for a new habitat often entails a cost to performance in the ancestral habitat. Although aquatic lifestyles are ancestral among extant cryptodiran turtles, multiple lineages, including tortoises (Testudinidae) and emydid box turtles (genus Terrapene), independently specialized for terrestrial habitats. To what extent is swimming function retained in such lineages despite terrestrial specialization? Because tortoises diverged from other turtles over 50 Ma, but box turtles did so only 5 Ma, we hypothesized that swimming kinematics for box turtles would more closely resemble those of aquatic relatives than those of tortoises. To test this prediction, we compared high-speed video of swimming Russian tortoises (Testudo horsfieldii), box turtles (Terrapene carolina) and two semi-aquatic emydid species: sliders (Trachemys scripta) and painted turtles (Chrysemys picta). We identified different kinematic patterns between limbs. In the forelimb, box turtle strokes most resemble those of tortoises; for the hindlimb, box turtles are more similar to semi-aquatic species. Such patterns indicate functional convergence of the forelimb of terrestrial species, whereas the box turtle hindlimb exhibits greater retention of ancestral swimming motions.
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http://dx.doi.org/10.1098/rsbl.2016.0732DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5310579PMC
January 2017

"On the Fence" versus "All in": Insights from Turtles for the Evolution of Aquatic Locomotor Specializations and Habitat Transitions in Tetrapod Vertebrates.

Integr Comp Biol 2016 12 23;56(6):1310-1322. Epub 2016 Oct 23.

*Department of Biological Sciences, Clemson University, Clemson, SC, 29634, USA.

Though ultimately descended from terrestrial amniotes, turtles have deep roots as an aquatic lineage and are quite diverse in the extent of their aquatic specializations. Many taxa can be viewed as "on the fence" between aquatic and terrestrial realms, whereas others have independently hyperspecialized and moved "all in" to aquatic habitats. Such differences in specialization are reflected strongly in the locomotor system. We have conducted several studies to evaluate the performance consequences of such variation in design, as well as the mechanisms through which specialization for aquatic locomotion is facilitated in turtles. One path to aquatic hyperspecialization has involved the evolutionary transformation of the forelimbs from rowing, tubular limbs with distal paddles into flapping, flattened flippers, as in sea turtles. Prior to the advent of any hydrodynamic advantages, the evolution of such flippers may have been enabled by a reduction in twisting loads on proximal limb bones that accompanied swimming in rowing ancestors, facilitating a shift from tubular to flattened limbs. Moreover, the control of flapping movements appears related primarily to shifts in the activity of a single forelimb muscle, the deltoid. Despite some performance advantages, flapping may entail a locomotor cost in terms of decreased locomotor stability. However, other morphological specializations among rowing species may enhance swimming stability. For example, among highly aquatic pleurodiran turtles, fusion of the pelvis to the shell appears to dramatically reduce motions of the pelvis compared to freshwater cryptodiran species. This could contribute to advantageous increases in aquatic stability among predominantly aquatic pleurodires. Thus, even within the potential constraints of a body plan in which the body is encased by a shell, turtles exhibit diverse locomotor capacities that have enabled diversification into a wide range of aquatic habitats.
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http://dx.doi.org/10.1093/icb/icw121DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5146712PMC
December 2016

Flowing water affects fish fast-starts: escape performance of the Hawaiian stream goby, Sicyopterus stimpsoni.

J Exp Biol 2016 10 28;219(Pt 19):3100-3105. Epub 2016 Jul 28.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Experimental measurements of escape performance in fishes have typically been conducted in still water; however, many fishes inhabit environments with flow that could impact escape behavior. We examined the influences of flow and predator attack direction on the escape behavior of fish, using juveniles of the amphidromous Hawaiian goby Sicyopterus stimpsoni In nature, these fish must escape ambush predation while moving through streams with high-velocity flow. We measured the escape performance of juvenile gobies while exposing them to a range of water velocities encountered in natural streams and stimulating fish from three different directions. Frequency of response across treatments indicated strong effects of flow conditions and attack direction. Juvenile S. stimpsoni had uniformly high response rates for attacks from a caudal direction (opposite flow); however, response rates for attacks from a cranial direction (matching flow) decreased dramatically as flow speed increased. Mechanical stimuli produced by predators attacking in the same direction as flow might be masked by the flow environment, impairing the ability of prey to detect attacks. Thus, the likelihood of successful escape performance in fishes can depend critically on environmental context.
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http://dx.doi.org/10.1242/jeb.137554DOI Listing
October 2016

Tail use improves performance on soft substrates in models of early vertebrate land locomotors.

Science 2016 Jul;353(6295):154-8

School of Physics, Georgia Institute of Technology, Atlanta, GA, USA. School of Biology, Georgia Institute of Technology, Atlanta, GA, USA.

In the evolutionary transition from an aquatic to a terrestrial environment, early tetrapods faced the challenges of terrestrial locomotion on flowable substrates, such as sand and mud of variable stiffness and incline. The morphology and range of motion of appendages can be revealed in fossils; however, biological and robophysical studies of modern taxa have shown that movement on such substrates can be sensitive to small changes in appendage use. Using a biological model (the mudskipper), a physical robot model, granular drag measurements, and theoretical tools from geometric mechanics, we demonstrate how tail use can improve robustness to variable limb use and substrate conditions. We hypothesize that properly coordinated tail movements could have provided a substantial benefit for the earliest vertebrates to move on land.
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http://dx.doi.org/10.1126/science.aaf0984DOI Listing
July 2016

Pelvic girdle mobility of cryptodire and pleurodire turtles during walking and swimming.

J Exp Biol 2016 09 23;219(Pt 17):2650-8. Epub 2016 Jun 23.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Movements of the pelvic girdle facilitate terrestrial locomotor performance in a wide range of vertebrates by increasing hind limb excursion and stride length. The extent to which pelvic movements contribute to limb excursion in turtles is unclear because the bony shell surrounding the body presents a major obstacle to their visualization. In the Cryptodira, which are one of the two major lineages of turtles, pelvic anatomy indicates the potential for rotation inside the shell. However, in the Pleurodira, the other major suborder, the pelvis shows a derived fusion to the shell, preventing pelvic motion. In addition, most turtles use their hind limbs for propulsion during swimming as well as walking, and the different locomotor demands between water and land could lead to differences in the contributions of pelvic rotation to limb excursion in each habitat. To test these possibilities, we used X-ray reconstruction of moving morphology (XROMM) to compare pelvic mobility and femoral motion during walking and swimming between representative species of cryptodire (Pseudemys concinna) and pleurodire (Emydura subglobosa) turtles. We found that the pelvis yawed substantially in cryptodires during walking and, to a lesser extent, during swimming. These movements contributed to greater femoral protraction during both walking and swimming in cryptodires when compared with pleurodires. Although factors related to the origin of pelvic-shell fusion in pleurodires are debated, its implications for their locomotor function may contribute to the restriction of this group to primarily aquatic habits.
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http://dx.doi.org/10.1242/jeb.141622DOI Listing
September 2016

Comparative limb bone loading in the humerus and femur of the tiger salamander: testing the 'mixed-chain' hypothesis for skeletal safety factors.

J Exp Biol 2016 Feb 23;219(Pt 3):341-53. Epub 2015 Nov 23.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Locomotion imposes some of the highest loads upon the skeleton, and diverse bone designs have evolved to withstand these demands. Excessive loads can fatally injure organisms; however, bones have a margin of extra protection, called a 'safety factor' (SF), to accommodate loads that are higher than normal. The extent to which SFs might vary amongst an animal's limb bones is unclear. If the limbs are likened to a chain composed of bones as 'links', then similar SFs might be expected for all limb bones because failure of the system would be determined by the weakest link, and extra protection in other links could waste energetic resources. However, Alexander proposed that a 'mixed-chain' of SFs might be found amongst bones if: (1) their energetic costs differ, (2) some elements face variable demands, or (3) SFs are generally high. To test whether such conditions contribute to diversity in limb bone SFs, we compared the biomechanical properties and locomotor loading of the humerus and femur in the tiger salamander (Ambystoma tigrinum). Despite high SFs in salamanders and similar sizes of the humerus and femur that would suggest similar energetic costs, the humerus had lower bone stresses, higher mechanical hardness and larger SFs. SFs were greatest in the anatomical regions where yield stresses were highest in the humerus and lowest in the femur. Such intraspecific variation between and within bones may relate to their different biomechanical functions, providing insight into the emergence of novel locomotor capabilities during the invasion of land by tetrapods.
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http://dx.doi.org/10.1242/jeb.125799DOI Listing
February 2016

Limb bone loading in swimming turtles: changes in loading facilitate transitions from tubular to flipper-shaped limbs during aquatic invasions.

Biol Lett 2015 Jun;11(6):20150110

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Members of several terrestrial vertebrate lineages have returned to nearly exclusive use of aquatic habitats. These transitions were often accompanied by changes in skeletal morphology, such as flattening of limb bone shafts. Such morphological changes might be correlated with the exposure of limb bones to altered loading. Though the environmental forces acting on the skeleton differ substantially between water and land, no empirical data exist to quantify the impact of such differences on the skeleton, either in terms of load magnitude or regime. To test how locomotor loads change between water and land, we compared in vivo strains from femora of turtles (Trachemys scripta) during swimming and terrestrial walking. As expected, strain magnitudes were much lower (by 67.9%) during swimming than during walking. However, the loading regime of the femur also changed between environments: torsional strains are high during walking, but torsion is largely eliminated during swimming. Changes in loading regime between environments may have enabled evolutionary shifts to hydrodynamically advantageous flattened limb bones in highly aquatic species. Although circular cross sections are optimal for resisting torsional loads, the removal of torsion would reduce the advantage of tubular shapes, facilitating the evolution of flattened limbs.
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http://dx.doi.org/10.1098/rsbl.2015.0110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4528462PMC
June 2015

In vivo strains in the femur of the nine-banded armadillo (Dasypus novemcinctus).

J Morphol 2015 Aug 21;276(8):889-99. Epub 2015 Mar 21.

Department of Biological Sciences, Youngstown State University, Youngstown, Ohio.

The capacity of limb bones to resist the locomotor loads they encounter depends on both the pattern of those loads and the material properties of the skeletal elements. Among mammals, understanding of the interplay between these two factors has been based primarily on evidence from locomotor behaviors in upright placentals, which show limb bones that are loaded predominantly in anteroposterior bending with minimal amounts of torsion. However, loading patterns from the femora of opossums, marsupials using crouched limb posture, show appreciable torsion while the bone experiences mediolateral (ML) bending. These data indicated greater loading diversity in mammals than was previously recognized, and suggested the possibility that ancestral loading patterns found in sprawling lineages (e.g., reptilian sauropsids) might have been retained among basal mammals. To further test this hypothesis, we recorded in vivo locomotor strains from the femur of the nine-banded armadillo (Dasypus novemcinctus), a member of the basal xenarthran clade of placental mammals that also uses crouched limb posture. Orientations of principal strains and magnitudes of shear strains indicate that armadillo femora are exposed to only limited torsion; however, bending is essentially ML, placing the medial aspect of the femur in compression and the lateral aspect in tension. This orientation of bending is similar to that found in opossums, but planar strain analyses indicate much more of the armadillo femur experiences tension during bending, potentially due to muscles pulling on the large, laterally positioned third trochanter. Limb bone safety factors were estimated between 3.3 and 4.3 in bending, similar to other placental mammals, but lower than opossums and most sprawling taxa. Thus, femoral loading patterns in armadillos show a mixture of similarities to both opossums (ML bending) and other placentals (limited torsion and low safety factors), along with unique features (high axial tension) that likely relate to their distinctive hindlimb anatomy.
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http://dx.doi.org/10.1002/jmor.20387DOI Listing
August 2015

Terrestrial locomotion-where do we stand, where are we going? An introduction to the symposium.

Integr Comp Biol 2014 Dec 23;54(6):1051-7. Epub 2014 Jul 23.

*Department of Biological Sciences, Clemson University, 132 Long Hall, Clemson, SC 29634, USA; Department of Biology, University of California Riverside, 900 University Avenue, Riverside, CA 92521, USA.

Locomotion is fundamental to the survival of many animal species, and terrestrial environments are one of the primary habitats through which a wide range of animals (including humans) must move. Many recent efforts have been made to broaden the approaches and systems used to understand how terrestrial locomotion is executed and modulated. This symposium highlights these efforts and seeks to identify new directions for the study of this diverse behavior. Studies focusing on the structural and functional foundations of terrestrial locomotion, terrestrial locomotor dynamics, and terrestrial locomotor diversity point toward several promising areas for future work. These include: the development, application, and refinement of computational and robotic models; the integration of approaches to clarify which of multiple layers of selection and biological organization influence locomotor performance; increasing the taxonomic, environmental, and behavioral range of study systems to promote new research syntheses and questions; and expansion of studies from laboratory settings to examinations in the field and in the context of ontogenetic and evolutionary time. With new, integrative data from diverse systems in natural settings, new opportunities will emerge for understanding how locomotion contributes to the survival and fitness of terrestrial animals.
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http://dx.doi.org/10.1093/icb/icu105DOI Listing
December 2014

Diversity of limb-bone safety factors for locomotion in terrestrial vertebrates: evolution and mixed chains.

Integr Comp Biol 2014 Dec 7;54(6):1058-71. Epub 2014 May 7.

*Department of Biological Sciences, Clemson University, Clemson, SC, USA; Department of Biological Sciences, Youngstown State University, Youngstown, OH, USA; Department of Anatomy, Midwestern University, Glendale, AZ, USA; Department of Bioengineering, Clemson University, Clemson, SC, USA; Clemson Libraries, Clemson University, Clemson, SC, USA.

During locomotion over land, vertebrates' limb bones are exposed to loads. Like most biological structures, limb bones have a capacity to withstand greater loads than they usually experience, termed a safety factor (SF). How diverse are limb-bone SFs, and what factors correlate with such variation? We have examined these questions from two perspectives. First, we evaluated locomotor SF for the femur in diverse lineages, including salamanders, frogs, turtles, lizards, crocodilians, and marsupials (opossums). Comparisons with values for hind-limb elements in running birds and eutherian mammals indicate phylogenetic diversity in limb-bone SF. A high SF (∼7) is primitive for tetrapods, but low magnitudes of load and elevated strength of bones contribute to different degrees across lineages; moreover, birds and eutherians appear to have evolved lower SFs independently. Second, we tested the hypothesis that SFs would be similar across limb bones within a taxon by comparing data from the humerus and femur of alligators. Both in bending and in torsion, we found a higher SF for the humerus than for the femur. Such a "mixed chain" of different SFs across elements has been predicted if bones have differing variabilities in load, different costs to maintain, or high SF values in general. Although variability in load is similar for the humerus and femur, a high SF may be less costly for the humerus because it is smaller than the femur. The high SFs of alligators also might facilitate differences in SF among their limb bones. Beyond these specific findings, however, a more general implication of our results is that evaluations of the diversity of limb-bone SFs can provide important perspective to direct future research. In particular, more complete understanding of variation in SF could provide insight into factors that promoted the evolutionary radiation of terrestrial locomotor function in vertebrates.
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http://dx.doi.org/10.1093/icb/icu032DOI Listing
December 2014

Stairway to heaven: evaluating levels of biological organization correlated with the successful ascent of natural waterfalls in the Hawaiian stream goby Sicyopterus stimpsoni.

PLoS One 2013 27;8(12):e84851. Epub 2013 Dec 27.

Department of Food Science and Nutrition, University of Minnesota, Saint Paul, Minnesota, United States of America.

Selective pressures generated by locomotor challenges act at the level of the individual. However, phenotypic variation among individuals that might convey a selective advantage may occur across any of multiple levels of biological organization. In this study, we test for differences in external morphology, muscle mechanical advantage, muscle fiber type and protein expression among individuals of the waterfall climbing Hawaiian fish Sicyopterus stimpsoni collected from sequential pools increasing in elevation within a single freshwater stream. Despite predictions from previous laboratory studies of morphological selection, few directional morphometric changes in body shape were observed at successively higher elevations. Similarly, lever arm ratios associated with the main pelvic sucker, central to climbing ability in this species, did not differ between elevations. However, among climbing muscles, the adductor pelvicus complex (largely responsible for generating pelvic suction during climbing) contained a significantly greater red muscle fiber content at upstream sites. A proteomic analysis of the adductor pelvicus revealed two-fold increases in expression levels for two respiratory chain proteins (NADH:ubiquinone reductase and cytochrome b) that are essential for aerobic respiration among individuals from successively higher elevations. Assessed collectively, these evaluations reveal phenotypic differences at some, but not all levels of biological organization that are likely the result of selective pressures experienced during climbing.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0084851PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3873996PMC
February 2015

Forelimb muscle function in pig-nosed turtles, Carettochelys insculpta: testing neuromotor conservation between rowing and flapping in swimming turtles.

Biol Lett 2013 Oct 21;9(5):20130471. Epub 2013 Aug 21.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

Changes in muscle activation patterns can lead to new locomotor modes; however, neuromotor conservation-the evolution of new forms of locomotion through changes in structure without concurrent changes to underlying motor patterns-has been documented across diverse styles of locomotion. Animals that swim using appendages do so via rowing (anteroposterior oscilations) or flapping (dorsoventral oscilations). Yet few studies have compared motor patterns between these swimming modes. In swimming turtles, propulsion is generated exclusively by limbs. Kinematically, turtles swim using multiple styles of rowing (freshwater species), flapping (sea turtles) and a unique hybrid style with superficial similarity to flapping by sea turtles and characterized by increased dorsoventral motions of synchronously oscillated forelimbs that have been modified into flippers (Carettochelys insculpta). We compared forelimb motor patterns in four species of turtle (two rowers, Apalone ferox and Trachemys scripta; one flapper, Caretta caretta; and Carettochelys) and found that, despite kinematic differences, motor patterns were generally similar among species with a few notable exceptions: specifically, presence of variable bursts for pectoralis and triceps in Trachemys (though timing of the non-variable pectoralis burst was similar), and the timing of deltoideus activity in Carettochelys and Caretta compared with other taxa. The similarities in motor patterns we find for several muscles provide partial support for neuromotor conservation among turtles using diverse locomotor styles, but the differences implicate deltoideus as a prime contributor to flapping limb motions.
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http://dx.doi.org/10.1098/rsbl.2013.0471DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971683PMC
October 2013

Correlation of muscle function and bone strain in the hindlimb of the river cooter turtle (Pseudemys concinna).

J Morphol 2013 Sep 3;274(9):1060-9. Epub 2013 Jun 3.

Department of Biological Sciences, Youngstown State University, Youngstown, OH 44555, USA.

During terrestrial locomotion, limb muscles must generate mechanical work and stabilize joints against the ground reaction force. These demands can require high force production that imposes substantial loads on limb bones. To better understand how muscle contractile function influences patterns of bone loading in terrestrial locomotion, and refine force platform equilibrium models used to estimate limb bone safety factors, we correlated in vivo recordings of femoral strain with muscle activation and strain in a major propulsive hindlimb muscle, flexor tibialis internus (FTI), of a species with a published model of hindlimb force production (river cooter turtles, Pseudemys concinna). Electromyography (EMG) recordings indicate FTI activity prior to footfall that continues through approximately 50% of the stance phase. Large EMG bursts occur just after footfall when the muscle has reached its maximum length and is beginning to actively shorten, concurrent with increasing compressive strain on the anterior femur. The FTI muscle shortens through 35% of stance, with mean fascicle shortening strains reaching 14.0 ± 5.4% resting length (L0 ). At the time of peak compressive strains on the femur, the muscle fascicles remain active, but fascicles typically lengthen until mid-stance as the knee extends. Influenced by the activity of the dorsal knee extensor femorotibialis, the FTI muscle continues to passively lengthen simultaneously with knee extension and a shift to tensile axial strain on the anterior femur at approximately 40% of stance. The near coincidence in timing of peak compressive bone strain and peak muscle shortening (5.4 ± 4.1% stance) indicates a close correlation between the action of the hip extensor/knee flexor, FTI, and femoral loading in the cooter hindlimb. In the context of equilibrium models of limb bone loading, these results may help explain differences in safety factor estimates observed between previous force platform and in vivo strain analyses in cooters.
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http://dx.doi.org/10.1002/jmor.20162DOI Listing
September 2013

Propulsive forces of mudskipper fins and salamander limbs during terrestrial locomotion: implications for the invasion of land.

Integr Comp Biol 2013 Aug 10;53(2):283-94. Epub 2013 May 10.

Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA.

The invasion of land was a pivotal event in vertebrate evolution that was associated with major appendicular modifications. Although fossils indicate that the evolution of fundamentally limb-like appendages likely occurred in aquatic environments, the functional consequences of using early digited limbs, rather than fins, for terrestrial propulsion have had little empirical investigation. Paleontological and experimental analyses both have led to the proposal of an early origin of "hind limb-driven" locomotion among tetrapods or their ancestors. However, the retention of a pectoral appendage that had already developed terrestrial adaptations has been proposed for some taxa, and few data are available from extant functional models that can provide a foundation for evaluating the relative contributions of pectoral and pelvic appendages to terrestrial support among early stem tetrapods. To examine these aspects of vertebrate locomotor evolution during the invasion of land, we measured three-dimensional ground reaction forces (GRFs) produced by isolated pectoral fins of mudskipper fishes (Periophthalmus barbarus) during terrestrial crutching, and compared these to isolated walking footfalls by the forelimbs and hind limbs of tiger salamanders (Ambystoma tigrinum), a species with subequally-sized limbs that facilitate comparisons to early tetrapods. Pectoral appendages of salamanders and mudskippers exhibited numerous differences in GRFs. Compared with salamander forelimbs, isolated fins of mudskippers bear lower vertical magnitudes of GRFs (as a proportion of body weight), and had GRFs that were oriented more medially. Comparing the salamanders' forelimbs and hind limbs, although the peak net GRF occurs later in stance for the forelimb, both limbs experience nearly identical mediolateral and vertical components of GRF, suggesting comparable contributions to support. Thus, forelimbs could also have played a significant locomotor role among basal tetrapods that had limbs of sub-equal size. However, the salamander hind limb and mudskipper pectoral fin had a greater acceleratory role than did the salamander forelimb. Together, data from these extant taxa help to clarify how structural change may have influenced locomotor function through the evolutionary invasion of land by vertebrates.
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http://dx.doi.org/10.1093/icb/ict051DOI Listing
August 2013

Vertebrate land invasions-past, present, and future: an introduction to the symposium.

Integr Comp Biol 2013 Aug 9;53(2):192-6. Epub 2013 May 9.

Department of Biology, Wake Forest University, Winston-Salem, NC 27109, USA.

The transition from aquatic to terrestrial habitats was a seminal event in vertebrate evolution because it precipitated a sudden radiation of species as new land animals diversified in response to novel physical and biological conditions. However, the first stages of this environmental transition presented numerous challenges to ancestrally aquatic organisms, and necessitated changes in the morphological and physiological mechanisms that underlie most life processes, among them movement, feeding, respiration, and reproduction. How did solutions to these functional challenges evolve? One approach to this question is to examine modern vertebrate species that face analogous demands; just as the first tetrapods lived at the margins of bodies of water and likely moved between water and land regularly, many extant fishes and amphibians use their body systems in both aquatic and terrestrial habitats on a daily basis. Thus, studies of amphibious vertebrates elucidate the functional demands of two very different habitats and clarify our understanding of the initial evolutionary challenges of moving onto land. A complementary approach is to use studies of the fossil record and comparative development to gain new perspectives on form and function of modern amphibious and non-amphibious vertebrate taxa. Based on the synthetic approaches presented in the symposium, it is clear that our understanding of aquatic-to-terrestrial transitions is greatly improved by the reciprocal integration of paleontological and neontological perspectives. In addition, common themes and new insights that emerged from this symposium point to the value of innovative approaches, new model species, and cutting-edge research techniques to elucidate the functional challenges and evolutionary changes associated with vertebrates' invasion of the land.
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http://dx.doi.org/10.1093/icb/ict048DOI Listing
August 2013

The evolution of locomotor rhythmicity in tetrapods.

Evolution 2013 Apr 20;67(4):1209-17. Epub 2012 Dec 20.

Organismal Biology & Anatomy, University of Chicago, 1027 East 57th Street, Chicago, Illinois 60637, USA.

Differences in rhythmicity (relative variance in cycle period) among mammal, fish, and lizard feeding systems have been hypothesized to be associated with differences in their sensorimotor control systems. We tested this hypothesis by examining whether the locomotion of tachymetabolic tetrapods (birds and mammals) is more rhythmic than that of bradymetabolic tetrapods (lizards, alligators, turtles, salamanders). Species averages of intraindividual coefficients of variation in cycle period were compared while controlling for gait and substrate. Variance in locomotor cycle periods is significantly lower in tachymetabolic than in bradymetabolic animals for datasets that include treadmill locomotion, non-treadmill locomotion, or both. When phylogenetic relationships are taken into account the pooled analyses remain significant, whereas the non-treadmill and the treadmill analyses become nonsignificant. The co-occurrence of relatively high rhythmicity in both feeding and locomotor systems of tachymetabolic tetrapods suggests that the anatomical substrate of rhythmicity is in the motor control system, not in the musculoskeletal components.
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http://dx.doi.org/10.1111/evo.12015DOI Listing
April 2013