Advertisement

Zoomorphology

, Volume 132, Issue 3, pp 325–338 | Cite as

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

  • Stine Griep
  • Nadja Schilling
  • Percy Marshall
  • Michael Amling
  • Lisa M. Hahne
  • Alexander HaasEmail author
Original Paper

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.

Keywords

Lissamphibia Anura Three-dimensional Locomotion Animation High-speed Jumping 

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

Notes

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.

Supplementary material

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 (4.6 mb)
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)

References

  1. Akella T, Gillis G (2011) Hopping isn’t always about the legs: forelimb muscle activity patterns during toad locomotion. J Exp Zool Part A: Ecol Gen Physiol 315A:1–11CrossRefGoogle Scholar
  2. Barclay O (1946) The mechanics of amphibian locomotion. J Exp Biol 23:177–203PubMedGoogle Scholar
  3. Bigalke R (1926) Zur Myologie der Erdkröte. Z Anat Entwicklungsgesch 83:286–353Google Scholar
  4. Brainerd E, Baier D, Gatesy S, Hedrick T, Metzger K, Gilbert S, Crisco J (2010) X-ray Reconstruction of Moving Morphology (XROMM): precision, accuracy and applications in comparative biomechanics research. J Exp Zool Part A: Ecol Genet Physiol 313:262–279Google Scholar
  5. Cope E (1864) On the limits and relations of the raniformes. Proc Acad Nat Sci Philadelphia 16:181–183Google Scholar
  6. Dietrich HF, Fontaine AR (1975) A decalcification method for ultrastructure of echinoderm tissues. Stain Tech 50:351–354Google Scholar
  7. Emerson S (1983) Functional analysis of frog pectoral girdles. The epicoracoid cartilages. J Zool 201:293–308CrossRefGoogle Scholar
  8. Emerson S (1984) Morphological variation in frog pectoral girdles: testing alternatives to a traditional adaptive explanation. Evolution 38:376–388CrossRefGoogle Scholar
  9. Essner R, Suffian D, Bishop PJ, Reilly S (2010) Landing in basal frogs: evidence of saltatorial patterns in the evolution of anuran locomotion. Naturwissenschaften 97:935–939PubMedCrossRefGoogle Scholar
  10. Gans C, Parsons T (1966) On the origin of the jumping mechanism in frogs. Evolution 20:92–99CrossRefGoogle Scholar
  11. Gatesy S, Baier D, Jenkins F, Dial K (2010) Scientific rotoscoping: a morphology-based method of 3-D motion analysis and visualization. J Exp Zool Part A: Ecol Gen Physiol 313:244–261Google Scholar
  12. Gaupp E (1896) Anatomie des Frosches. Erste Abtheilung. Lehre vom Skelet und vom Muskelsystem. Braunschweig, Friedrich Vieweg und SohnGoogle Scholar
  13. Gillis G, Akella T, Gunaratne R (2010) Do toads have a jump on how far they hop? Pre-landing activity timing and intensity in forelimb muscles of hopping Bufo marinus. Biol Lett 6:486–489PubMedCrossRefGoogle Scholar
  14. Marsh RL, John-Alder H (1994) Jumping performance of hylid frogs measured with high-speed cine film. J Exp Biol 188:131–141PubMedGoogle Scholar
  15. Mulisch M, Welsch U (2010) Romeis-mikroskopische Technik. Spektrum Akademischer Verlag 2010Google Scholar
  16. Nauwelaerts S, Aerts P (2006) Take-off and landing forces in jumping frogs. J Exp Biol 209:66–77PubMedCrossRefGoogle Scholar
  17. Noble GK (1931) The Biology of the Amphibia. McGraw-Hill Book Co., New YorkGoogle Scholar
  18. Peters S, Kamel L, Bashor D (1996) Hopping and swimming in the leopard frog, Rana pipiens: I. step cycles and kinematics. J Morph 230:1–16PubMedCrossRefGoogle Scholar
  19. Phillips B, Brown G, Webb J, Shine R (2006) Invasion and the evolution of speed in toads. Nature 439(7078):803PubMedCrossRefGoogle Scholar
  20. Rand A (1952) Jumping ability of certain anurans, with notes on endurance. Copeia 1952:15–20CrossRefGoogle Scholar
  21. Weninger WJ, Meng S, Streicher J, Müller GB (1998) A new episcopic method for rapid 3-D reconstruction: applications in anatomy and embryology. Anat Embryol 197:341–348PubMedCrossRefGoogle Scholar
  22. Zug GR, Altig R (1978) Anuran locomotion structure and function: the jumping forces of frogs. J Wash Acad Sci 68:144–147Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Stine Griep
    • 1
  • Nadja Schilling
    • 2
  • Percy Marshall
    • 3
  • Michael Amling
    • 4
  • Lisa M. Hahne
    • 1
  • Alexander Haas
    • 1
    Email author
  1. 1.Biozentrum Grindel und Zoologisches Museum HamburgHamburgGermany
  2. 2.Institut für Spezielle Zoologie und EvolutionsbiologieJenaGermany
  3. 3.UKE AthleticumHamburgGermany
  4. 4.Institut für Osteologie und BiomechanikHamburgGermany

Personalised recommendations