Publications by authors named "Natalie M Warburton"

11 Publications

  • Page 1 of 1

The skeleton of , a semiarboreal kangaroo from the Pleistocene of southern Australia.

R Soc Open Sci 2021 Mar 24;8(3):202216. Epub 2021 Mar 24.

College of Science and Engineering, Flinders University, South Australia 5042, Australia.

The macropodine kangaroo, , was first described in 1989 from a Pleistocene deposit within Mammoth Cave, southwestern Australia, on the basis of a few partial dentaries and maxilla fragments. Here, we recognize within the Pleistocene assemblages of the Thylacoleo Caves, south-central Australia, where it is represented by several cranial specimens and two near-complete skeletons, a probable male and female. We reallocate this species to the hitherto monotypic genus . differs from all other macropodid species by having a highly unusual pocket within the wall of the nasal cavity. It is distinguished from by having a longer, narrower rostrum, a taller occiput and a deeper jugal. is closest to in overall cranial morphology but is smaller and less robust. In most postcranial attributes, also resembles , including general limb robustness and the atypical ratio of 14 thoracic to five lumbar vertebrae. It is distinguished by the high mobility of its glenohumeral joints, the development of muscle attachment sites for strong adduction and mobility of the forelimb, and large, robust manual and pedal digits with strongly recurved distal phalanges. These adaptations resemble those of tree-kangaroos more than ground-dwelling macropodines. We interpret this to imply that was semiarboreal, with a propensity to climb and move slowly through trees. This is the first evidence for the secondary adoption of a climbing habit within crown macropodines.
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http://dx.doi.org/10.1098/rsos.202216DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8074921PMC
March 2021

Ontogenetic growth and the development of a unique fibrocartilage entheses in Macropus fuliginosus.

Zoology (Jena) 2021 Feb 25;144:125860. Epub 2020 Oct 25.

College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA, 6150, Australia.

Here we examine the bone histology of the femora and humeri of the Western Grey Kangaroo, Macropus fuliginosus. Our results reveal that bone modelling in response to ontogenetic growth and the development of tuberosities on the femur, and especially in the humerus, lead to a highly complex histology. We propose that the alternating fast and slow rates of bone deposition are seasonal, and are likely correlated with heterothermy related to ecological constraints during the summer months. In females, after the fourth growth mark in the femur, there is a distinctive change to a more lamellar textured bone deposition with sparse vascularisation, directly indicating a slowdown in growth. However, in males, the zones remain woven textured and well vascularised, which is indicative of continued fast growth. Here we also report the novel occurrence of a fibrocartilaginous entheses for the attachment of the m. quadratus femoris to the caudal femoral tuberosity. Using a combination of methodologies, we show that perimeter measurements of growth marks provide a reasonable estimation of the age of kangaroos. Additionally, we observed large individuals that have ceased diaphyseal appositional growth of the femur and the humerus, as well as fusion of the distal epiphyses of both bones, though the proximal epiphyses may remain unfused.
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http://dx.doi.org/10.1016/j.zool.2020.125860DOI Listing
February 2021

Extreme bilateral polydactyly in a wild-caught western grey kangaroo.

Anat Rec (Hoboken) 2020 Oct 9. Epub 2020 Oct 9.

School of Veterinary Medicine, Murdoch University, Murdoch, Western Australia, Australia.

Polydactyly is a congenital malformation resulting from an autosomal dominant mutation manifesting as supernumerary digits of the hands or feet. It is most commonly reported in humans and domestic mammals, though there have also been isolated examples across a range of wild vertebrate species. Here we report a case of extremely unusual bilateral preaxial polydactyly on the pectoral limbs of a male western grey kangaroo (Macropus fuliginosus) from the South West region of Western Australia, in which two supernumerary digits were present on each manus. A supernumerary digit I on each manus was rudimentary in morphology without extrinsic muscular connections. However, supernumerary digit II present on each manus had fully developed extrinsic and intrinsic muscular connections, suggesting that these digits possessed normal function in flexion and extension. An alternative hypothesis is that the two supernumerary digits are both representatives of the most radial digit I, though this would then require the true digit I to have taken on the appearance of digit II by acquiring an additional phalanx and modified muscular attachments. The carpal bones exhibited a number of subtle differences in morphology when compared to normal pentadactyl individuals. The presence of a distal, rather than proximal, epiphysis on the first metacarpal was unexpected but further investigation suggested that this characteristic is perhaps more variable (in this species at least) than has been previously recognized. This case provides an unusual example to be considered within the broader context of limb development.
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http://dx.doi.org/10.1002/ar.24530DOI Listing
October 2020

Review of the methods used for calculating physiological cross-sectional area (PCSA) for ecological questions.

J Morphol 2020 07 6;281(7):778-789. Epub 2020 May 6.

Medical, Molecular and Forensic Sciences, Murdoch University, Murdoch, Australia.

This review examines literature that used physiological cross-sectional area (PCSA) as a representative measure of an individual muscle's maximal isometric force production. PCSA is used to understand the muscle architecture and how a trade-off between muscle force and muscle contractile velocity reflect adaptations of the musculoskeletal system as a reflection of functional demands. Over the decades, methods have been developed to measure muscle volume, fascicle lengths, and pennation angle to calculate PCSA. The advantages and limitations of these methods (especially the inclusion/elimination of pennation angle) are discussed frequently; however, these method descriptions are scattered throughout the literature. Here, we reviewed and summarised the different approaches to collecting and recording muscle architectural properties to subsequently calculate PCSA. By critically discussing the advantages and limitations of each methodology, we aim to provide readers with an overview of repeatable methods to assess muscle architecture. This review may serve as a guide to facilitate readers searching for the appropriate techniques to calculate PCSA and measure muscle architecture to be applied in ecomorphology research. RESEARCH HIGHLIGHTS: Discuss the theories behind PCSA in a synthesised review to inform researchers about PCSA methodology.
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http://dx.doi.org/10.1002/jmor.21139DOI Listing
July 2020

Covariation between forelimb muscle anatomy and bone shape in an Australian scratch-digging marsupial: Comparison of morphometric methods.

J Morphol 2019 12 22;280(12):1900-1915. Epub 2019 Oct 22.

Medical, Molecular, and Forensic Sciences, Murdoch University, Murdoch, Western Australia, Australia.

The close association between muscle and bone is broadly intuitive; however, details of the covariation between the two has not been comprehensively studied. Without quantitative understanding of how muscle anatomy influences bone shape, it is difficult to draw conclusions of the significance of many morphological traits of the skeleton. In this study, we investigated these relationships in the Quenda (Isoodon fusciventer), a scratch-digging marsupial. We quantified the relationships between forelimb muscle anatomy and bone shape for animals representing a range of body masses (124-1,952 g) using two-block partial least square analyses. Muscle anatomy was quantified as muscle mass and physiological cross-sectional area (PCSA), and we used two morphometric methods to characterize bone shape: seven indices of linear bone proportions, and landmarks analysis. Bone shape was significantly correlated with body mass, reflecting allometric bone growth. Of the seven bone indices, only shoulder moment index (SMI) and ulna robustness index (URI) showed a significant covariation with muscle anatomy. Stronger relationships between muscle anatomy and forelimb bone shape were found using the landmark coordinates: muscle mass and PCSA were correlated with the geometric shape of the scapula, humerus, and third metacarpal, but to a lesser extent with shape of the ulna. Overall, our data show that landmark coordinates are more sensitive than bone indices to capturing shape changes evident throughout ontogeny, and is therefore a more appropriate method to investigate covariation with forelimb muscle anatomy. Single-species studies investigating ontogeny require refined methods to accurately develop understanding of the important relationships between muscle force generation and bone shape remodeling. Landmark analyses provide such a method.
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http://dx.doi.org/10.1002/jmor.21074DOI Listing
December 2019

Mechanical similarity across ontogeny of digging muscles in an Australian marsupial (Isoodon fusciventer).

J Morphol 2019 03 1;280(3):423-435. Epub 2019 Feb 1.

School of Veterinary and Life Sciences, Murdoch University, Murdoch, Western Australia, Australia.

Many mammals dig, either during foraging to access subsurface food resources, or in creating burrows for shelter. Digging requires large forces produced by muscles and transmitted to the soil via the skeletal system; thus fossorial mammals tend to have characteristic modifications of the musculoskeletal system that reflect their digging ability. Bandicoots (Marsupialia: Peramelidae) scratch-dig mainly to source food, searching for subterranean food items including invertebrates, seeds, and fungi. They have musculoskeletal features for digging, including shortened, robust forelimb bones, large muscles, and enlarged muscle attachment areas. Here, we compared changes in the ontogenetic development of muscles associated with digging in the Quenda (Isoodon fusciventer). We measured muscle mass (m ), pennation angle, and fiber length (FL) to calculate physiological cross-sectional area (PCSA; a proxy of maximum isometric force) as well as estimate the maximum isometric force (Fmax) for 34 individuals ranging in body size from 124 to 2,390 g. Males grow larger than females in this bandicoot species, however, we found negligible sex differences in mass-specific m , PCSA or FL for our sample. Majority of the forelimb muscles PCSA showed a positive allometric relationship with total body mass, while m and FL in the majority of forelimb muscles showed isometry. Mechanical similarity was tested, and two thirds of forelimb muscles maximum isometric forces (Fmax) scaled with isometry; therefore the forelimb is primarily mechanical similar throughout ontogeny. PCSA showed a significant difference between scaling slopes between main movers in the power stroke, and main movers of the recovery stroke of scratch-digging. This suggests that some forelimb muscles grow with positive allometry, specially these associated with the power stroke of digging. Intraspecific variation in PCSA is rarely considered in the literature, and thus this is an important study quantifying changes in muscle architectural properties with growth in a mammalian model of scratch-digging.
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http://dx.doi.org/10.1002/jmor.20954DOI Listing
March 2019

Anatomy of the cavernous muscles of the kangaroo penis highlights marsupial-placental dichotomy.

J Anat 2019 03 6;234(3):306-315. Epub 2019 Jan 6.

School of Veterinary and Life Sciences, Murdoch University, Murdoch, Western Australia, Australia.

The mammalian penis is a complex hydraulic organ of cavernous (spongy) tissue supported by both smooth and skeletal muscle structures. In placental mammals, the paired ‎Musculus ischiocavernosi anchor the corpora cavernosa to the pelvis (at the ischium), and the paired M. bulbospongiosi converge as they envelop the base of the corpus spongiosum. Male marsupials have a dramatically different anatomy, however, in which both sets of paired muscles remain separate, have a bulbous, globular shape and do not have any direct connection to the pelvis. Here we provide the first detailed anatomical investigation of the muscles of the penis in the western grey kangaroo (Macropus fuliginosus) incorporating dissection, histology, vascular casting and computed tomography. The M. ischiocavernosus and M. bulbospongiosus form massive, multipennate bodies of skeletal muscle surrounding the paired roots of the corpus cavernosum and corpus spongiosum, respectively. Bilateral vascular supply is via both the artery of the penis and the ventral perineal artery. Histological examination reveals cavernous tissues with substantial smooth muscle supported by fibroelastic trabeculae, surrounded by the thick collagenous tunica albuginea. The M. ischiocavernosus and M. bulbospongiosus are known to function during erection of the penis and ejaculation via muscular contraction increasing blood pressure within cavernous vascular tissues. The thick muscular anatomy of the kangaroo would be well suited to this function. The absence of any connection to the bony pelvis in marsupials suggests the possibility of different mechanisms of action of these muscles with regard to reduction of venous return, eversion from the cloaca, or movements such as penile flips, which have been described in some placental mammals. This highlights a greater diversity in form and function in the evolution of the mammalian penis than has been previously considered.
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http://dx.doi.org/10.1111/joa.12930DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6365618PMC
March 2019

The fibular meniscus of the kangaroo as an adaptation against external tibial rotation during saltatorial locomotion.

J Anat 2017 Dec 19;231(6):931-938. Epub 2017 Sep 19.

School of Veterinary and Life Sciences, Murdoch University, Murdoch, WA, Australia.

The kangaroo knee is, as in other species, a complex diarthrodial joint dependent on interacting osseous, cartilaginous and ligamentous components for its stability. While principal load bearing occurs through the femorotibial articulation, additional lateral articulations involving the fibula and lateral fabella also contribute to the functional arrangement. Several fibrocartilage and ligamentous structures in this joint remain unexplained or have been misunderstood in previous studies. In this study, we review the existing literature on the structure of the kangaroo 'knee' before providing a new description of the gross anatomical and histological structures. In particular, we present strong evidence that the previously described 'femorofibular disc' is best described as a fibular meniscus on the basis of its gross and histological anatomy. Further, we found it to be joined by a distinct tendinous tract connecting one belly of the m. gastrocnemius with the lateral meniscus, via a hyaline cartilage cornu of the enlarged lateral fabella. The complex of ligaments connecting the fibular meniscus to the surrounding connective tissues and muscles appears to provide a strong resistance to external rotation of the tibia, via the restriction of independent movement of the proximal fibula. We suggest this may be an adaptation to resist the rotational torque applied across the joint during bipedal saltatory locomotion in kangaroos.
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http://dx.doi.org/10.1111/joa.12683DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5696135PMC
December 2017

Forelimb Myology of Carnivorous Marsupials (Marsupialia: Dasyuridae): Implications for the Ancestral Body Plan of the Australidelphia.

Anat Rec (Hoboken) 2017 Sep 27;300(9):1589-1608. Epub 2017 May 27.

L'Ecole Nationale Veterinaire de Toulouse, France.

Carnivorous marsupials of the family Dasyuridae represent a more generalized anatomical condition of both craniodental and postcranial features in comparison to other groups of Australidelphian marsupials. Plesiomorphic characters include polyprotodont dentition, didactylous (rather than syndactylous) pedal morphology, the retention of clavicles and epipubic bones, and an unossified patelloid. In light of the anatomy of the postcranial skeleton, we hypothesized that the muscular anatomy of the Dasyuridae would likely display a range of plesiomorphic traits. We performed gross anatomical dissection on the forelimbs of four species of dasyurid marsupials to produce anatomical descriptions and muscle origin and insertion maps for Dasyurus geoffroii, D. hallucatus, and Phascogale tapoatafa, together with comparative notes for Antechinus flavipes. These new descriptions were then compared with those of other marsupials from the published literature in order to establish the principal patterns in forelimb muscular anatomy. In nearly all aspects of anatomy, we found that the arrangement of the muscular origins and insertions, and the relative degree of separation between muscle bellies among dasyurids, provide a natural starting point from which the anatomies of other Australidelphian marsupial groups can be derived. Anat Rec, 300:1589-1608, 2017. © 2017 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/ar.23612DOI Listing
September 2017

Functional morphology of the forelimb of living and extinct tree-kangaroos (Marsupialia: Macropodidae).

J Morphol 2011 Oct 31;272(10):1230-44. Epub 2011 May 31.

School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch, Western Australia 6150, Australia.

Tree-kangaroos are a unique group of arboreal marsupials that evolved from terrestrial ancestors. The recent discovery of well-preserved specimens of extinct tree-kangaroo species (genus Bohra) within Pleistocene cave deposits of south-central Australia provides a unique opportunity to examine adaptive evolution of tree-kangaroos. Here, we provide the first detailed description of the functional anatomy of the forelimb, a central component of the locomotor complex, in the extant Dendrolagus lumholtzi, and compare its structure and function with representatives of other extant marsupial families. Several features were interpreted as adaptations for coping with a discontinuous, uneven and three-dimensional arboreal substrate through enhanced muscular strength and dexterity for propulsion, grasping, and gripping with the forelimbs. The forelimb musculoskeletal anatomy of Dendrolagus differed from terrestrial kangaroos in the following principal ways: a stronger emphasis on the development of muscles groups responsible for adduction, grasping, and gripping; the enlargement of muscles that retract the humerus; and modified shape of the scapula and bony articulations of the forelimb bones to allow improved mobility. Many of these attributes are convergent with other arboreal marsupials. Tree-kangaroos, however, still retain the characteristic bauplan of their terrestrial ancestors, particularly with regard to skeletal morphology, and the muscular anatomy of the forelimb highlights a basic conservatism within the group. In many instances, the skeletal remains of Bohra have similar features to Dendrolagus that suggest adaptations to an arboreal habit. Despite the irony of their retrieval from deposits of the Nullarbor "Treeless" Plain, forelimb morphology clearly shows that the species of Bohra were well adapted to an arboreal habitat.
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http://dx.doi.org/10.1002/jmor.10979DOI Listing
October 2011

An arid-adapted middle Pleistocene vertebrate fauna from south-central Australia.

Nature 2007 Jan;445(7126):422-5

Department of Earth and Planetary Sciences, Western Australian Museum, Perth, Western Australia 6000, Australia.

How well the ecology, zoogeography and evolution of modern biotas is understood depends substantially on knowledge of the Pleistocene. Australia has one of the most distinctive, but least understood, Pleistocene faunas. Records from the western half of the continent are especially rare. Here we report on a diverse and exceptionally well preserved middle Pleistocene vertebrate assemblage from caves beneath the arid, treeless Nullarbor plain of south-central Australia. Many taxa are represented by whole skeletons, which together serve as a template for identifying fragmentary, hitherto indeterminate, remains collected previously from Pleistocene sites across southern Australia. A remarkable eight of the 23 Nullarbor kangaroos are new, including two tree-kangaroos. The diverse herbivore assemblage implies substantially greater floristic diversity than that of the modern shrub steppe, but all other faunal and stable-isotope data indicate that the climate was very similar to today. Because the 21 Nullarbor species that did not survive the Pleistocene were well adapted to dry conditions, climate change (specifically, increased aridity) is unlikely to have been significant in their extinction.
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http://dx.doi.org/10.1038/nature05471DOI Listing
January 2007