Publications

2017

Thompson, Cynthia L, Brianna L Powell, Susan H Williams, Goro Hanya, Kenneth E Glander, and Christopher J Vinyard. (2024) 2017. “Thyroid Hormone Fluctuations Indicate a Thermoregulatory Function in Both a Tropical (Alouatta Palliata) and Seasonally Cold-Habitat (Macaca Fuscata) Primate”. American Journal of Primatology 79 (11). https://doi.org/10.1002/ajp.22714.
Thyroid hormones boost animals basal metabolic rate and represent an important thermoregulatory pathway for mammals that face cold temperatures. Whereas the cold thermal pressures experienced by primates in seasonal habitats at high latitudes and elevations are often apparent, tropical habitats also display distinct wet and dry seasons with modest changes in thermal environment. We assessed seasonal and temperature-related changes in thyroid hormone levels for two primate species in disparate thermal environments, tropical mantled howlers (Alouatta palliata), and seasonally cold-habitat Japanese macaques (Macaca fuscata). We collected urine and feces from animals and used ELISA to quantify levels of the thyroid hormone triiodothyronine (fT3 ). For both species, fT3 levels were significantly higher during the cooler season (wet/winter), consistent with a thermoregulatory role. Likewise, both species displayed greater temperature deficits (i.e., the degree to which animals warm their body temperature relative to ambient) during the cooler season, indicating greater thermoregulatory pressures during this time. Independently of season, Japanese macaques displayed increasing fT3 levels with decreasing recently experienced maximum temperatures, but no relationship between fT3 and recently experienced minimum temperatures. Howlers increased fT3 levels as recently experienced minimum temperatures decreased, although demonstrated the opposite relationship with maximum temperatures. This may reflect natural thermal variation in howlers habitat: wet seasons had cooler minimum and mean temperatures than the dry season, but similar maximum temperatures. Overall, our findings support the hypothesis that both tropical howlers and seasonally cold-habitat Japanese macaques utilize thyroid hormones as a mechanism to boost metabolism in response to thermoregulatory pressures. This implies that cool thermal pressures faced by tropical primates are sufficient to invoke an energetically costly and relatively longer-term thermoregulatory pathway. The well-established relationship between thyroid hormones and energetics suggests that the seasonal hormonal changes we observed could influence many commonly studied behaviors including food choice, range use, and activity patterns.
Stover, Kristin K, JoAnna Sidote, and Susan H Williams. (2024) 2017. “An Ontogenetic Perspective on Symphyseal Fusion, Occlusion and Mandibular Loading in Alpacas (Vicugna Pacos)”. Zoology (Jena, Germany) 124: 95—105. https://doi.org/10.1016/j.zool.2017.06.006.
A primary hypothesis for the evolution of mandibular symphyseal fusion in some mammals is that it functions to resist loads incurred during routine mastication. Anecdotal support for this hypothesis is based on the fact that when the symphysis fuses, it typically does so early during postnatal ontogeny prior to or around the time of weaning. However, little is known about the process of fusion, particularly relative to feeding behaviors and the dynamics of mastication, including occlusion and masticatory loading. In the present study, we investigate the timing and process of symphyseal fusion in alpacas (Vicugna pacos) in the context of maturation of the oral apparatus and oral behavior. We also report on in vivo strains from the symphysis and corpus in young alpacas prior to and following full fusion and M1 occlusion. Results show that fusion begins rostrally by 1 month and is complete by 6-7 months whereas all deciduous premolars and M1 come into occlusion by 6 months. Although symphyseal loading patterns are maintained throughout ontogeny, in young alpacas symphyseal strain magnitudes are low compared with adults but corpus strain magnitudes are comparable to those found in adults. Reduced symphyseal loading in young individuals is contrary to what might be predicted given that the symphysis is still fusing. When considered in light of the development of occlusion and rumination, strain magnitudes may be necessarily low and reflect an overall delay in the maturation of masticatory dynamics.
Thompson, Cynthia L, Caleb Scheidel, Kenneth E Glander, Susan H Williams, and Christopher J Vinyard. (2024) 2017. “An Assessment of Skin Temperature Gradients in a Tropical Primate Using Infrared Thermography and Subcutaneous Implants”. Journal of Thermal Biology 63: 49—57. https://doi.org/10.1016/j.jtherbio.2016.11.005.
Infrared thermography has become a useful tool to assess surface temperatures of animals for thermoregulatory research. However, surface temperatures are an endpoint along the body s core-shell temperature gradient. Skin and fur are the peripheral tissues most exposed to ambient thermal conditions and are known to serve as thermosensors that initiate thermoregulatory responses. Yet relatively little is known about how surface temperatures of wild mammals measured by infrared thermography relate to subcutaneous temperatures. Moreover, this relationship may differ with the degree that fur covers the body. To assess the relationship between temperatures and temperature gradients in peripheral tissues between furred and bare areas, we collected data from wild mantled howling monkeys (Alouatta palliata) in Costa Rica. We used infrared thermography to measure surface temperatures of the furred dorsum and bare facial areas of the body, recorded concurrent subcutaneous temperatures in the dorsum, and measured ambient thermal conditions via a weather station. Temperature gradients through cutaneous tissues (subcutaneous-surface temperature) and surface temperature gradients (surface-ambient temperature) were calculated. Our results indicate that there are differences in temperatures and temperature gradients in furred versus bare areas of mantled howlers. Under natural thermal conditions experienced by wild animals, the bare facial areas were warmer than temperatures in the furred dorsum, and cutaneous temperature gradients in the face were more variable than the dorsum, consistent with these bare areas acting as thermal windows. Cutaneous temperature gradients in the dorsum were more closely linked to subcutaneous temperatures, while facial temperature gradients were more heavily influenced by ambient conditions. These findings indicate that despite the insulative properties of fur, for mantled howling monkeys surface temperatures of furred areas still demonstrate a relationship with subcutaneous temperatures. Given that most mammals possess dense fur, this provides insight for using infrared imaging in thermoregulatory studies of wild animals lacking bare skin.
Davis, Jillian S, and Susan H Williams. (2024) 2017. “The Influence of Diet on Masticatory Motor Patterns in Musteloid Carnivorans: An Analysis of Jaw Adductor Activity in Ferrets (Mustela Putorius Furo) and Kinkajous (Potos Flavus)”. Journal of Experimental Zoology. Part A, Ecological and Integrative Physiology 327 (9): 551—561. https://doi.org/10.1002/jez.2141.
Broad similarities in the timing of jaw adductor activity driving jaw movements across distantly related and morphologically disparate species have led to the hypothesis that mammalian masticatory motor patterns are conserved. However, some quantitative analyses also suggest that masticatory motor patterns have evolved in concert with dietary and/or morphological specialization. Here, we assess this relationship in two closely related carnivoran species with divergent diets and morphology: carnivorous ferrets and frugivorous kinkajous. Using electromyography to characterize jaw adductor activity during rhythmic mastication, we test the hypotheses that (1) carnivoran masticatory motor patterns differ from those of non-carnivorans based on previously published data, and (2) differences between ferret and kinkajou motor patterns are associated with dietary and morphological differences. We find that both species exhibit highly synchronous jaw adductor activity that is likely typical of most carnivorans. Kinkajous differ from ferrets, however, in having a balancing-side zygomaticomandibularis that is active later than all other adductors. The significance of these different masticatory motor patterns may relate to morphological differences in the dentition of ferrets and kinkajous. Whereas ferret cheek teeth have vertical occlusal surfaces that limit jaw closing to a primarily dorsally directed movement, kinkajous have relatively flat occlusal surfaces that allow more transverse movement, which may be essential for processing fruits. Our results suggest that some aspects of masticatory motor patterns are highly conserved yet some components are modified in concert with functional and morphological evolution of the masticatory apparatus.
Mahato, Niladri K, Stephane Montuelle, Craig Goubeaux, John Cotton, Susan Williams, James Thomas, and Brian C Clark. (2017) 2017. “Quantification of Intervertebral Displacement With a Novel MRI-Based Modeling Technique: Assessing Measurement Bias and Reliability With a Porcine Spine Model.”. Magnetic Resonance Imaging 38: 77-86. https://doi.org/10.1016/j.mri.2016.12.022.

The purpose of this study was to develop a novel magnetic resonance imaging (MRI)-based modeling technique for measuring intervertebral displacements. Here, we present the measurement bias and reliability of the developmental work using a porcine spine model. Porcine lumbar vertebral segments were fitted in a custom-built apparatus placed within an externally calibrated imaging volume of an open-MRI scanner. The apparatus allowed movement of the vertebrae through pre-assigned magnitudes of sagittal and coronal translation and rotation. The induced displacements were imaged with static (T1) and fast dynamic (2D HYCE S) pulse sequences. These images were imported into animation software, in which these images formed a background 'scene'. Three-dimensional models of vertebrae were created using static axial scans from the specimen and then transferred into the animation environment. In the animation environment, the user manually moved the models (rotoscoping) to perform model-to-'scene' matching to fit the models to their image silhouettes and assigned anatomical joint axes to the motion-segments. The animation protocol quantified the experimental translation and rotation displacements between the vertebral models. Accuracy of the technique was calculated as 'bias' using a linear mixed effects model, average percentage error and root mean square errors. Between-session reliability was examined by computing intra-class correlation coefficients (ICC) and the coefficient of variations (CV). For translation trials, a constant bias (β0) of 0.35 (±0.11) mm was detected for the 2D HYCE S sequence (p=0.01). The model did not demonstrate significant additional bias with each mm increase in experimental translation (β1Displacement=0.01mm; p=0.69). Using the T1 sequence for the same assessments did not significantly change the bias (p>0.05). ICC values for the T1 and 2D HYCE S pulse sequences were 0.98 and 0.97, respectively. For rotation trials, a constant bias (β0) of 0.62 (±0.12)° was detected for the 2D HYCE S sequence (p<0.01). The model also demonstrated an additional bias (β1Displacement) of 0.05° with each degree increase in the experimental rotation (p<0.01). Using T1 sequence for the same assessments did not significantly change the bias (p>0.05). ICC values for the T1 and 2D HYCE S pulse sequences were recorded 0.97 and 0.91, respectively. This novel quasi-static approach to quantifying intervertebral relationship demonstrates a reasonable degree of accuracy and reliability using the model-to-image matching technique with both static and dynamic sequences in a porcine model. Future work is required to explore multi-planar assessment of real-time spine motion and to examine the reliability of our approach in humans.

Thompson, Cynthia L, Brianna L Powell, Susan H Williams, Goro Hanya, Kenneth E Glander, and Christopher J Vinyard. (2017) 2017. “Thyroid Hormone Fluctuations Indicate a Thermoregulatory Function in Both a Tropical (Alouatta Palliata) and Seasonally Cold-Habitat (Macaca Fuscata) Primate.”. American Journal of Primatology 79 (11). https://doi.org/10.1002/ajp.22714.

Thyroid hormones boost animals' basal metabolic rate and represent an important thermoregulatory pathway for mammals that face cold temperatures. Whereas the cold thermal pressures experienced by primates in seasonal habitats at high latitudes and elevations are often apparent, tropical habitats also display distinct wet and dry seasons with modest changes in thermal environment. We assessed seasonal and temperature-related changes in thyroid hormone levels for two primate species in disparate thermal environments, tropical mantled howlers (Alouatta palliata), and seasonally cold-habitat Japanese macaques (Macaca fuscata). We collected urine and feces from animals and used ELISA to quantify levels of the thyroid hormone triiodothyronine (fT3 ). For both species, fT3 levels were significantly higher during the cooler season (wet/winter), consistent with a thermoregulatory role. Likewise, both species displayed greater temperature deficits (i.e., the degree to which animals warm their body temperature relative to ambient) during the cooler season, indicating greater thermoregulatory pressures during this time. Independently of season, Japanese macaques displayed increasing fT3 levels with decreasing recently experienced maximum temperatures, but no relationship between fT3 and recently experienced minimum temperatures. Howlers increased fT3 levels as recently experienced minimum temperatures decreased, although demonstrated the opposite relationship with maximum temperatures. This may reflect natural thermal variation in howlers' habitat: wet seasons had cooler minimum and mean temperatures than the dry season, but similar maximum temperatures. Overall, our findings support the hypothesis that both tropical howlers and seasonally cold-habitat Japanese macaques utilize thyroid hormones as a mechanism to boost metabolism in response to thermoregulatory pressures. This implies that cool thermal pressures faced by tropical primates are sufficient to invoke an energetically costly and relatively longer-term thermoregulatory pathway. The well-established relationship between thyroid hormones and energetics suggests that the seasonal hormonal changes we observed could influence many commonly studied behaviors including food choice, range use, and activity patterns.

2016

Druzinsky, Robert E, James P Balhoff, Alfred W Crompton, James Done, Rebecca Z German, Melissa A Haendel, Anthony Herrel, et al. 2016. “Muscle Logic: New Knowledge Resource for Anatomy Enables Comprehensive Searches of the Literature on the Feeding Muscles of Mammals”. PloS One 11 (2): e0149102. https://doi.org/10.1371/journal.pone.0149102.

Background

In recent years large bibliographic databases have made much of the published literature of biology available for searches. However, the capabilities of the search engines integrated into these databases for text-based bibliographic searches are limited. To enable searches that deliver the results expected by comparative anatomists, an underlying logical structure known as an ontology is required.

Development and testing of the ontology

Here we present the Mammalian Feeding Muscle Ontology (MFMO), a multi-species ontology focused on anatomical structures that participate in feeding and other oral/pharyngeal behaviors. A unique feature of the MFMO is that a simple, computable, definition of each muscle, which includes its attachments and innervation, is true across mammals. This construction mirrors the logical foundation of comparative anatomy and permits searches using language familiar to biologists. Further, it provides a template for muscles that will be useful in extending any anatomy ontology. The MFMO is developed to support the Feeding Experiments End-User Database Project (FEED, https://feedexp.org/), a publicly-available, online repository for physiological data collected from in vivo studies of feeding (e.g., mastication, biting, swallowing) in mammals. Currently the MFMO is integrated into FEED and also into two literature-specific implementations of Textpresso, a text-mining system that facilitates powerful searches of a corpus of scientific publications. We evaluate the MFMO by asking questions that test the ability of the ontology to return appropriate answers (competency questions). We compare the results of queries of the MFMO to results from similar searches in PubMed and Google Scholar.

Results and significance

Our tests demonstrate that the MFMO is competent to answer queries formed in the common language of comparative anatomy, but PubMed and Google Scholar are not. Overall, our results show that by incorporating anatomical ontologies into searches, an expanded and anatomically comprehensive set of results can be obtained. The broader scientific and publishing communities should consider taking up the challenge of semantically enabled search capabilities.
Mahato, Niladri K, Stephane Montuelle, John Cotton, Susan Williams, James Thomas, and Brian Clark. (2016) 2016. “Development of a Morphology-Based Modeling Technique for Tracking Solid-Body Displacements: Examining the Reliability of a Potential MRI-only Approach for Joint Kinematics Assessment.”. BMC Medical Imaging 16 (1): 38. https://doi.org/10.1186/s12880-016-0140-1.

BACKGROUND: Single or biplanar video radiography and Roentgen stereophotogrammetry (RSA) techniques used for the assessment of in-vivo joint kinematics involves application of ionizing radiation, which is a limitation for clinical research involving human subjects. To overcome this limitation, our long-term goal is to develop a magnetic resonance imaging (MRI)-only, three dimensional (3-D) modeling technique that permits dynamic imaging of joint motion in humans. Here, we present our initial findings, as well as reliability data, for an MRI-only protocol and modeling technique.

METHODS: We developed a morphology-based motion-analysis technique that uses MRI of custom-built solid-body objects to animate and quantify experimental displacements between them. The technique involved four major steps. First, the imaging volume was calibrated using a custom-built grid. Second, 3-D models were segmented from axial scans of two custom-built solid-body cubes. Third, these cubes were positioned at pre-determined relative displacements (translation and rotation) in the magnetic resonance coil and scanned with a T1 and a fast contrast-enhanced pulse sequences. The digital imaging and communications in medicine (DICOM) images were then processed for animation. The fourth step involved importing these processed images into an animation software, where they were displayed as background scenes. In the same step, 3-D models of the cubes were imported into the animation software, where the user manipulated the models to match their outlines in the scene (rotoscoping) and registered the models into an anatomical joint system. Measurements of displacements obtained from two different rotoscoping sessions were tested for reliability using coefficient of variations (CV), intraclass correlation coefficients (ICC), Bland-Altman plots, and Limits of Agreement analyses.

RESULTS: Between-session reliability was high for both the T1 and the contrast-enhanced sequences. Specifically, the average CVs for translation were 4.31 % and 5.26 % for the two pulse sequences, respectively, while the ICCs were 0.99 for both. For rotation measures, the CVs were 3.19 % and 2.44 % for the two pulse sequences with the ICCs being 0.98 and 0.97, respectively. A novel biplanar imaging approach also yielded high reliability with mean CVs of 2.66 % and 3.39 % for translation in the x- and z-planes, respectively, and ICCs of 0.97 in both planes.

CONCLUSIONS: This work provides basic proof-of-concept for a reliable marker-less non-ionizing-radiation-based quasi-dynamic motion quantification technique that can potentially be developed into a tool for real-time joint kinematics analysis.

2015

Montuelle, Stephane J, and Susan H Williams. 2015. “In Vivo Measurement of Mesokinesis in Gekko Gecko: The Role of Cranial Kinesis During Gape Display, Feeding and Biting”. PloS One 10 (7): e0134710. https://doi.org/10.1371/journal.pone.0134710.
Cranial kinesis refers to movements of skeletal sub-units relative to one another at mobile sutures within the skull. The presence and functional significance of cranial kinesis has been investigated in various vertebrates, with much of our understanding coming from comparative studies and manipulation of ligamentous specimens. Drawing on these studies, cranial kinesis in lizards has been modeled as a four-bar linkage system involving streptostyly (rotation of the quadrate), hypokinesis (dorsoventral flexion and extension of the palato-maxillary sub-unit), mesokinesis (dorsoventral flexion and extension of the snout at the fronto-parietal suture) and metakinesis (sliding movements between parietal and supraocciptal bones). In vivo studies, although limited, suggest that cranial kinesis serves an important role during routine behaviors such as feeding. Here, we use X-ray Reconstruction Of Moving Morphology to further quantify mesokinesis in vivo in Gekko gecko during three routine behaviors: gape display, biting and post-ingestion feeding. During gape display, the snout rotates dorsally above rest position, with mesokinesis accounting for a 10% increase in maximum gape over that achieved solely by the depression of the lower jaw. During defensive biting, the snout rotates ventrally below rest position to participate in gape closure. Finally, ventroflexion of the snout also occurs during post-ingestion feeding, accounting for 42% of gape closure during intra-oral transport, 86% during puncture-crushing, and 61% during pharyngeal packing. Mesokinesis thus appears to facilitate prey puncturing by allowing the snout to rotate ventrally so that the upper teeth pierce the prey item, thus limiting the need for large movements of the lower jaw. This is suggested to maintain a firm grip on the prey and reduce the possibility of prey escape. More generally, this study demonstrates that mesokinesis is a key component of defensive biting and gape display behaviors, as well as post-ingestion feeding, all of which are linked to organismal fitness.
Williams, Susan H, Nicholas R Lozier, Stephane J Montuelle, and Sonsoles De Lacalle. (2015) 2015. “Effect of Postnatal Myostatin Inhibition on Bite Mechanics in Mice.”. PloS One 10 (8): e0134854. https://doi.org/10.1371/journal.pone.0134854.

As a negative regulator of muscle size, myostatin (Mstn) impacts the force-production capabilities of skeletal muscles. In the masticatory system, measures of temporalis-stimulated bite forces in constitutive myostatin KOs suggest an absolute, but not relative, increase in jaw-muscle force. Here, we assess the phenotypic and physiologic impact of postnatal myostatin inhibition on bite mechanics using an inducible conditional KO mouse in which myostatin is inhibited with doxycycline (DOX). Given the increased control over the timing of gene inactivation in this model, it may be more clinically-relevant for developing interventions for age-associated changes in the musculoskeletal system. DOX was administered for 12 weeks starting at age 4 months, during which time food intake was monitored. Sex, age and strain-matched controls were given the same food without DOX. Bite forces were recorded just prior to euthanasia after which muscle and skeletal data were collected. Food intake did not differ between control or DOX animals within each sex. DOX males were significantly larger and had significantly larger masseters than controls, but DOX and control females did not differ. Although there was a tendency towards higher absolute bite forces in DOX animals, this was not significant, and bite forces normalized to masseter mass did not differ. Mechanical advantage for incisor biting increased in the DOX group due to longer masseter moment arms, likely due to a more anteriorly-placed masseter insertion. Despite only a moderate increase in bite force in DOX males and none in DOX females, the increase in masseter mass in males indicates a potentially positive impact on jaw muscles. Our data suggest a sexual dimorphism in the role of mstn, and as such investigations into the sex-specific outcomes is warranted.