Michael E. Jorgensen

The evolution of jumping in frogs: morphological evidence for the basal anuran locomotor condition and the radiation of locomotor systems in crown group anurans.

Our understanding of the evolution of frog locomotion follows from the work of Emerson in which anurans are proposed to possess one of three different iliosacral configurations: 1) a lateral‐bending system found in walking and hopping frogs; 2) a fore‐aft sliding mechanism found in several locomotor modes; and 3) a sagittal‐hinge‐type pelvis posited to be related to long‐distance jumping performance. The most basal living (Ascaphus) and fossil (Prosalirus) frogs are described as sagittal‐hinge pelvic types, and it has been proposed that long‐distance jumping with a sagittal‐hinge pelvis arose early in frog evolution. We revisited osteological traits of the pelvic region to conduct a phylogenetic analysis of the relationships between pelvic systems and locomotor modes in frogs. Using two of Emersons diagnostic traits from the sacrum and ilium and two new traits from the urostyle, we resampled the taxa originally studied by Emerson and key paleotaxa and conducted an analysis of ancestral‐character state evolution in relation to locomotor mode. We present a new pattern for the evolution of pelvic systems and locomotor modes in frogs. Character analysis shows that the lateral‐bender, walker/hopper condition is both basal and generally conserved across the Anura. Long‐distance jumping frogs do not appear until well within the Neobatrachia. The sagittal‐hinge morphology is correlated with long‐distance jumping in terrestrial frogs; however, it evolved convergently multiple times in crown group anurans with the same four pelvic traits described herein. Arboreal jumping has appeared in multiple crown lineages as well, but with divergent patterns of evolution involving each of the three pelvic types. The fore‐aft slider morph appears independently in three different locomotor modes and, thus, is a more complex system than previously thought. Finally, it appears that the advent of a bicondylar sacro‐urostylic articulation was originally related to providing axial rigidity to lateral‐bending behaviors rather than sagittal bending. J. Morphol., 2011.

Phylogenetic patterns of skeletal morphometrics and pelvic traits in relation to locomotor mode in frogs

Frogs are one of the most speciose groups of vertebrate tetrapods (> 6200sp) with a diverse array of locomotor behaviours. Despite the impressive diversity in frog locomotor behaviours, there remains a paucity of information on the relationship between skeletal variation and locomotor mode in frogs and the evolutionary patterns in which these relationships are framed across the frog phylogeny. Our current understanding of the evolution of frog locomotion shows that hopping transitioned into jumping within the Neobatrachia where a variety of pelvic/hindlimb length patterns and locomotor niches have appeared, but this has yet to be studied over a broad taxonomic sample of frogs. Although limb length remains as the primary predictor of leaping performance, pelvic and sacral morphometrics have not been quantified in relation to limb proportions, body size and locomotor mode and previous studies have not sampled more than 24 families. We present a large‐scale phylogenetic comparison of skeletal morphometrics in relation to locomotor mode in 188 genera from 37 families. Osteological variation in limb/pelvic girdle morphometrics and pelvic traits that are posited to be associated with locomotor mode were analysed to identify which aspects of the frog skeleton are the best descriptors of locomotor mode. Our results, contrary to previous work, reveal that the greatest axis of variation in frogs is represented by the shape of the sacrum with two pelvic morphologies evident in qualitative and quantitative ancestral trait reconstructions. Limb morphology was not significantly different across most locomotor modes, but we identified several outliers in hindlimb phylomorphospace. Patterns of sacral evolution together with hindlimb length outliers reveal how the general bauplan of this successful group of vertebrate tetrapods is constrained, has radiated and has converged on certain phenotypes to fill an array of locomotor modes.

Conquering the world in leaps and bounds: hopping locomotion in toads is actually bounding

Summary While most frogs maximize jump distance as an escape behaviour, toads have traded jump distance for endurance with a strategy of hopping repeatedly. This strategy has enabled toads to expand across the continents as one of the most diverse groups of anurans. Multiple studies have revealed physiological endurance adaptations for sustained hopping in toads, however, the kinematics of their sequential hopping behaviour, per se, has not been studied. We compared kinematics and forces of single hops and multiple hopping sequences and quantified field performance of hopping behaviours in free ranging toads of three species and discovered a novel aspect of locomotion adaptation that adds another facet to their exceptional terrestrial locomotor abilities. We found that bouts of repeated hopping are actually a series of bounding strides where toads rotate on their hands and then land on their extended their feet and jump again without stopping. In addition, free-ranging toads appear to use bounding locomotion more frequently than single hops. Bounding in toads has the advantage of maintaining velocity and producing longer jump distances. In comparison to single hops, cyclic bounding steps reduce energy expenditure and appear to provide limb loading dynamics better suited for potential cycling of elastic energy from stride to stride than would be possible with repeated single hops. This is the first case of the common use of a bounding gait outside of mammals. Bounding adds a key terrestrial locomotor trait to the toads phenotype that may help explain their history of global expansion and the challenges to modern faunas as introduced toads rapidly invade new ecosystems today.

Comparative feeding kinematics of temperate pond-dwelling tadpoles (Anura, Amphibia)

Several studies have explored various components of feeding kinematics in anuran larvae; however, a direct comparison of feeding kinematics among morphologically similar and sympatric taxa has not been undertaken. We used high-speed videography (500 frames/s) to capture feeding kinematics of Anaxyrus fowleri (Hinckley, 1882) (Fowler’s Toad), Hyla chrysoscelis (Cope, 1880) (Grey Treefrog), Scaphiopus holbrookii (Harlan, 1835) (Eastern Spadefoot Toad), and Lithobates sphenocephalus (Cope, 1889) (Southern Leopard Frog) tadpoles as they foraged from an algal-covered substrate. In total, we filmed 120 feeding sequences from 25 feeding bouts and quantified eight kinematic variables that were common among all four species. Despite relatively similar keratinized feeding structures among taxa, our videography data revealed fundamental differences in how the tadpoles used these structures. One specific difference was in the speed of the gape cycle. Among taxa, S. holbrookii tadpoles had the longest gape cycle and longest time to reach maximum gape, whereas A. fowleri and L. sphenocephalus tadpoles had shorter durations for both variables and did not differ between species. We also found species differences in the magnitude that tadpoles narrow their lower jaw sheath. Irrespective of gape size, the lower jaw sheath of S. holbrookii tadpoles narrowed by approximately 26% of its maximum width—a twofold difference from A. fowleri tadpoles, which narrowed only 13%. Our study revealed that tadpoles with similar oral structures feeding on the same substrate can exhibit major differences in feeding kinematics.

Variation in timing of ossification affects inferred heterochrony of cranial bones in Lissamphibia

The evolutionary origin of Lissamphibia likely involved heterochrony, as demonstrated by the biphasic lifestyles of most extant orders, differences between Anura (with tadpole‐to‐froglet metamorphosis) and Urodela (which lack strongly defined metamorphosis), and the appearance of direct development among separate lineages of frogs. Patterns in the timing of appearance of skeletal elements (i.e., ossification sequence data) represent a possible source of information for understanding the origin of Lissamphibia, and with the advent of analytical methods to directly optimize these data onto known phylogenies, there has been a renewed interest in assessing the role of changes in these developmental events. However, little attention has been given to the potential impact of variation in ossification sequence data—this is particularly surprising given that different criteria for collecting these data have been employed. Herein, new and previously published ossification data are compiled and all pairs of data for same‐species comparisons are selected. Analyses are run to assess the impact of using data that were collected by different methodologies: (1) wild‐ versus lab‐raised animals; (2) different criteria for recognizing timing of ossification; and (3) randomly selecting ossification sequences for species from which multiple studies have been published, but for which the data were collected by different criteria. Parsimov‐based genetic inference is utilized to map ossification sequence data onto an existing phylogeny to reconstruct ancestral sequences of ossification and infer instances of heterochrony. All analyses succeeded in optimizing sequence data on internal nodes and instances of heterochrony were identified. However, among all analyses little congruence was found in reconstructed ancestral sequences or among inferred instances of heterochrony. These results indicate a high degree of variation in timing of ossification, and suggest a cautionary note about use of these data, particularly given that in most instances issues associated with the original sources of data (e.g., wild‐ vs. lab‐raised animals; or criteria for identification of earliest ossification) are not addressed. Potential sources of variation in the original data are discussed and may explain the incongruence observed here.

Effects of Temperature Regime Through Premetamorphic Ontogeny on Shape of the Chondrocranium in the American Toad, Anaxyrus americanus

If one considers the substantial amount of information that exists about phenotypic plasticity in amphibians, it is surprising that few studies have examined abiotic factors that influence phenotype through ontogeny. Phenotypic change and stability of morphology are artifacts of organisms that bear significant relevance to evolution within and among taxonomic groups. Here, we examine development as a phenotypically plastic aspect of larval anurans. Fertilized eggs of the American Toad, Anaxyrus (= Bufo) americanus (Holbrook, 1836), were obtained from two pairs of adults, and larvae were reared in four temperature treatments (constant Mean, constant High, constant Low, and Fluctuating regime [Low night–High day]); developmental series were collected from each treatment, representing larvae of this species from Gosner Stages 28–40. Cleared and stained larvae were analyzed with landmark‐based geometric morphometric methods to facilitate examination of differences in overall shape change of the larval chondrocranium through ontogeny, as a result of developmental temperature or temperature regime. Changes in shape of the chondrocranium and in amount and direction of phenotypic change through ontogeny were found in response to temperature treatment and temperature regime. Mean chondrocranial shape of the Fluctuating regime was more similar to the consensus shape of the overall data set than were those of all other treatments. Given that differences in amount and direction of shape change were observed among these treatments and throughout ontogeny, one should consider the affects of abiotic factors (such as temperature) when rearing larval anurans for studies of developmental morphology. Anat Rec, 291:818‐826, 2008.

Bow hunter's syndrome in a patient with vertebral artery atresia, an arcuate foramen, and unilateral deafness: a case report

Bow hunters syndrome (BHS) is a rare cause of vertebrobasilar insufficiency that occurs when the vertebral artery (VA) is occluded on rotation of the head and neck. This dynamic occlusion of the VA can occur anywhere along its course after it arises from the subclavian artery. Although most cases are associated with compression by osteophytes, cervical spondylosis, or lateral disc herniation, BHS has a highly variable clinical course that depends on the patients specific anatomy. Therefore, it may be important for clinicians to be aware of anatomical variants that predispose individuals to BHS. Here, we report on a patient with BHS who was found to have two uncommon anatomical anomalies: an atretic right VA and a left-sided arcuate foramen.

Pelvic function in anuran jumping: Interspecific differences in the kinematics and motor control of the iliosacral articulation during take-off and landing.

Although the anuran pelvis is thought to be adapted for jumping, the function of the iliosacral joint has seen little direct study. Previous work has contrasted the basal “lateral‐bender” pelvis from the “rod‐like” pelvis of crown taxa hypothesized to function as a sagittal hinge to align the trunk with take‐off forces. We compared iliosacral movements and pelvic motor patterns during jumping in the two pelvic types. Pelvic muscle activity patterns, iliosacral anteroposterior (AP) movements and sagittal bending of the pelvis during the take‐off and landing phases were quantified in lateral bender taxa Ascaphus (Leiopelmatidae) and Rhinella (Bufonidae) and the rod‐like Lithobates (Ranidae). All three species exhibit sagittal extension during take‐off, therefore, both pelvic types employ a sagittal hinge. However, trunk elevation occurs significantly earlier in the anuran rod‐like pelvis. Motor patterns confirm that the piriformis muscles depress the urostyle while the longissimus dorsi muscles elevate the trunk during take‐off. However, the coccygeoiliacus muscles also produce anterior translation of the sacrum on the ilia. A new model illustrates how AP translation facilitates trunk extension in the lateral‐bender anurans that have long been thought to have limited sagittal bending. During landing, AP translation patterns are similar because impact forces slide the sacrum from its posterior to anterior limits. Sagittal flexion during landing differs among the three taxa depending on the way the species land. AP translation during landing may dampen impact forces especially in Rhinella in which pelvic function is tuned to forelimb‐landing dynamics. The flexibility of the lateral‐bender pelvis to function in sagittal bending and AP translation helps to explain the retention of this basal configuration in many anurans. The novel function of the rod‐like pelvis may be to increase the rate of trunk elevation relative to faster rates of energy release from the hindlimbs enabling them to jump farther. J. Morphol. 277:1539–1558, 2016.

Treatment-refractory vulvodynia from nutcracker syndrome: A case report

Background Pelvic venous disorders are often undiagnosed due to the symptom variability and similarity to other disease presentations. ‘Pelvic congestion syndrome’ is a term often used as a diagnosis of exclusion, since there is currently no standardized diagnostic approach for pelvic venous disorders, which further delays treatment. Case A 25-year-old woman with treatment-refractory vulvodynia presented with symptoms that included left-sided vaginal wall pain, pruritis, dysmenorrhea, dyspareunia, muscle tension, and a chronic vaginal ulceration. Abnormal pelvic varices were discovered, and she was referred to vascular surgery for treatment of nutcracker syndrome causing ovarian vein reflux and abnormal engorgement of pelvic varices. Conclusion Patients presenting with signs of pelvic venous insufficiency such as vaginal pruritis, irritation, pain, recurrent vaginitis, or chronic ulcerations should be examined for pelvic venous disorders.

Envenomated-invertebrate prey preference of the viperid Agkistrodon contortrix during strike-induced chemosensory searching

Many crotaline snakes exhibit envenomated-prey preference in laboratory experiments. We examined the ability of copperheads (Agkistrodon contortrix) to distinguish between envenomated and nonenvenomated tobacco hornworm larvae (Manduca sexta). Snakes directed significantly more tongue flicks at envenomated hornworms than at nonenvenomated hornworms, and snakes consumed envenomated hornworms more frequently than nonenvenomated prey. These results support the hypothesis that envenomated tissue is an important stimulus to copperheads during strike-induced chemosensory searching. Copperheads preferred hornworms envenomated by conspecifics in the relative order: Louisiana > Texas > Kansas; this preference matches the relative order of preference and venom potency documented in a previous study of copperheads for envenomated mice. We conclude that the venom protein-prey tissue interaction responsible for the observed behaviour is similar in both invertebrate and rodent prey items.