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Pectoral girdle movements and the role of the glenohumeral joint during landing in the toad, Rhinella marina (Linnaeus, 1758)

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Abstract

Compared to anurans from other families, landings of toads (Bufonidae) during saltation appear well coordinated and the initial landing impact is absorbed exclusively by the forelimbs. Although the forelimbs and particularly the pectoral girdle have been suggested to be important for shock absorption, the functional roles of its various elements have not been evaluated in detail. This study addresses open questions regarding the kinematics of the forelimbs during landing in Rhinella marina using X-ray reconstruction of moving morphology and scientific rotoscoping. The kinematic analysis clearly showed that in addition to motions in the shoulder and elbow joints, substantial movements of the pectoral girdle in toto as well as of its elements relative to each other do occur during landing. The pectoral girdle showed first and foremost rotations about its latero-lateral axis as well as dorso-ventral translations relative to the spine. Our results quantify the extent of flexion and extension in the suprascapula-scapular synchondrosis during landing. Forelimb kinematics in R. marina differed from that of other anurans in starting elbow extension relatively early during the landing process, which likely prevents the chest from contacting the ground. Furthermore, the animal regains an upright and ready-to-hop-again position quickly and the recovery phase is short compared to other anurans. Humeral kinematics and anatomy confirm that the glenohumeral interlocking mechanism guides the humerus during the initial landing phase. Cranio-ventral ridges on the humeral head and the paraglenoid cartilage interlock in anteverted and slightly retroverted humeral positions. This occurs at the beginning of the landing. When interlocked, adduction/abduction as well as long-axis rotation of the humerus are restricted. During the course of landing, the humerus retroverts and is gradually freed from interlocking restrictions due to a smoother relief at the caudal aspect of the humeral head.

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Abbreviations

ASD:

Averaged standard deviation

3D:

Three-dimensional

CT:

Computer tomography

DOF:

Degree of freedom

EMG:

Electromyography

GCS:

Global coordinate system

SD:

Standard deviation

XROMM:

X-ray reconstruction of moving morphology

ROM:

Range of motion

GRF:

Ground reaction force

Fps:

Frames per second

SVL:

Snout vent length

M:

Mean

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Acknowledgments

The authors would like to thank M.S. Fischer, F. Friedrich, J. Nyakatura, D. McLeod and R. Schulz-Schaefer for valuable discussions. Technical help was provided by A. Adikfar, B. Hesse, D. Kühne, M. A. Kuppe, R. Petersohn, A. Taebel-Hellwig, A. Vogt and K. Wachs. A.D. Teege and S. Düwel were taking care of the animals. This study was financially supported by Körperschaftsvermögen der Universität Hamburg.

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Authors and Affiliations

  1. Biozentrum Grindel und Zoologisches Museum Hamburg, Martin-Luther-King-Platz 3, 20146, Hamburg, Germany

    Stine Griep, Lisa M. Hahne & Alexander Haas

  2. Institut für Spezielle Zoologie und Evolutionsbiologie, Erbertstr. 1, 07743, Jena, Germany

    Nadja Schilling

  3. UKE Athleticum, Martinistr. 52, 20246, Hamburg, Germany

    Percy Marshall

  4. Institut für Osteologie und Biomechanik, Lottestr. 59, 22529, Hamburg, Germany

    Michael Amling

Authors
  1. Stine Griep
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  2. Nadja Schilling
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  3. Percy Marshall
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  4. Michael Amling
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  5. Lisa M. Hahne
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  6. Alexander Haas
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Corresponding author

Correspondence to Alexander Haas.

Additional information

Communicated by A. Schmidt-Rhaesa.

Electronic supplementary material

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S1: Movie of landing Rhinalla marina. The skeleton was obtained from CT scans of the same animals that was recorded in high-speed X-ray videography (1.000 fps) in dorso-ventral (left) and lateral (right) views. The skeleton was superimposed onto the X-ray videos by XROMM rotoscoping. Skeletal reconstruction from CT does not show cartilaginous parts (e.g. dorso-caudal rim or suprascapula, epicoracoid cartilages or sternal process). (MOV 306 kb)

435_2013_189_MOESM2_ESM.tiff

S2. Supplement to Fig. 3 with definitions and origins of local coordinate systems (color dots). Bone position colored in beige shows the bone’s zero position, and the same bone colored red visualizes, in these cases, purely hypothetical rotation of the bone, as the measured rotation was 0 in these three axes. Red: x-axis, green: y-axis, blue: z-axis. The skeleton represents adult Rhinella marina (RmA) rendered by computer tomography; cartilaginous parts not rendered in CT. (TIFF 4720 kb)

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Griep, S., Schilling, N., Marshall, P. et al. Pectoral girdle movements and the role of the glenohumeral joint during landing in the toad, Rhinella marina (Linnaeus, 1758). Zoomorphology 132, 325–338 (2013). https://doi.org/10.1007/s00435-013-0189-0

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  • DOI: https://doi.org/10.1007/s00435-013-0189-0

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