Motor control of jaw movements in placental and marsupial grazers and browsers

Adapted from a presentation given in Greifswald, Germany in August, 2008 by AW Crompton.\

A ubiquitous feature of both placental and marsupial grazers and folivores, such as the goat and koala, is that during the power stroke of mastication the working side jaw is drawn transversely in a medial direction. The masticatory motor pattern or the firing pattern of adductor muscles responsible for this transverse movement in several placental herbivores is now relatively well-known. This is not the case for marsupials. The purpose of this project was to test whether the activity pattern of the adductor muscles  in selected marsupial herbivores is similar to or fundamentally different from that of typical placental herbivores.

Before describing the motor pattern in marsupials a very brief review of placental control is helpful.

EMG patterns of adductor muscles in the goat vs opossum

In a typical grazer such as the goat, jaw movements are controlled by a combination of working and balancing side muscles. For example, as the jaw closes it is drawn upwards and laterally until the the molars are brought into contact by one set of working and balancing side muscles.  These are referred to as "Triplet I muscles" and indicated in the figure above by red arrows. The graphs to the right show the order and duration when each of these Triplet I muscles reach peak amplitude in a single chewing cycle, circled in pink.(Time is shown on the X axis, the balancing side muscles in green and the working in black.)  During the power stroke the jaw is drawn medially by Triplet II muscles, also a combination of balancing and working side muscles (blue arrows). The firing pattern of these muscles shown in the graph are encircled within violet overlays. The orientation of jaw movement during the power stroke is indicated by the bold red arrow. In primitive mammals

such as the opossum, in marked contrast to herbivores jaw movement during the power stroke  is essentially vertical, lacking a transverse component. Their activity pattern of their adductors is shown in the graph above and can also be divided into two triplets of working and balancing side muscles. However the duration of the overall activity is shorter and there is a broad overlap of the two triplets.. The increased transverse jaw movements of herbivores involves an increase in the duration of adductor activity  and a temporal  separation of the activity periods of Triplets I and II muscles .

Is this also true for  marsupial herbivores?

Marsupials

For this study we monitored the EMGs of the main jaw adductors in three of the larger extant Australian marsupial herbivores:  red kangaroos, koalas and wombats. This work was carried out with the assistance of Prof. Russ Baudinette in his lab at the University of Adelaide. His untimely death in 2004 was a major loss to the future of environmental physiology research in Australia.

Transverse movement during chewing in the kangaroo, koala and wombat

The outline of one half of each of the lower jaws is shaded in these palatal views of the three mammals of this study. As indicated by the length of the arrows above the outlines, koalas and wombats have extensive transverse jaw movement during the power stroke. In macropods like the kangaroo transverse movements are greatly reduced. Their narrow upper incisor arcade (indicated in red) greatly limits transverse jaw movement.  Now let us look at the masticatory motor patterns of these three animals.

masticatory motor patterns of kangaroo vs opossum

Macropod molars, seen above, bottom left section, top left drawing in occlusal view, consist of high transverse lophs (red diamonds) and ridges or links between the lophs (yellow triangles). As the jaws close, the lophs shear food as they pass one another, and in occlusion meet ridges or links to crush the trapped food. During the limited transverse jaw movement, the molar links are dragged across the apices of the lophs to further grind food. Consequently the power stroke is divided into two distinct phases: a vertical Phase I (shearing and crushing) and a horizontal Phase II (Grinding. The two bold red arrows above indicate this double phase). This double phase involves a major change of the motor pattern. During the vertical phase I of the power stroke, high levels of activity occur in both working and balancing side muscles; whereas in the the horizontal Phase II only working side muscles are involved. This is best illustrated in the graph of adductor activity. Only a single Triplet I muscle moves the active side jaw laterally; whereas during Phase I of the power stroke (here on the graphs at right indicated by the purple overlay), balancing side muscles that are normally part of Triplet I fire later (indicated by the black arrows pointing to the right) and those that are normally part of Triplet II fire earlier (black arrows pointing the the left).  A reduced number of working side muscles draw the jaw medially during Phase II. Note the lack of balancing side muscles.

Masticatory muscle patterns in the koala

The molars of koalas consist of high shearing crests, here shown in occlusal view (bottom left drawing) and in posterior view (bottom right drawing). Eucalyptus leaves are shredded by these crests as the as the jaw is drawn dorsomedially (bold red arrow). The masticatory pattern is similar to that of placental herbivores in that both working and balancing side muscles are involved in drawing the working side jaw laterally Triplet I); and a complimentary set of muscles, Triplet II (blue arrows), draws the jaw medially. The masticatory pattern is best illustrated in the graph, with a clear temporal separation of Triplet I & II muscles. As in placental herbivores, increased transverse jaw movement is accompanied by a wide separation in the timing of the two triplets and an increase in the duration of adductor activity.

Mandibular angles in the wombat (inflected), koala and goat

A motor pattern similar to that of placental herbivores is not the only parallel feature that koalas share with  placentals like goats. Above are posterior views of the lower jaws of two marsupials and one placental. Placental herbivores have a deep mandibular angle whereas almost all marsupials have an inflected angle. The only exception are koalas, that have de-inflected or reversed the angle, and in this aspect are similar to placental herbivores. There may be a relationship between this and the placental-like masticatory motor  pattern.

Wombat masticatory motor pattern

Wombats have a bizarre and unique masticatory motor pattern. High occlusal forces rapidly obliterate the original cusp pattern as the working side jaw is drawn across the uppers, shown above in occlusal view. During the power stroke, the jaw moves horizontally toward the midline (bold red arrow). Only one balancing side muscle is involved in drawing the working side jaw laterally (red arrow) and only working side muscles (blue arrows) are active as the jaw is drawn medially. This is best illustrated in the graph. Only a single Triplet I muscle draws the jaw laterally (pink overlay). During the power stroke (blue overlay) all the balancing side muscles are silent (indicated by the four red cancel signs) and working side muscles that are normally associated with Triplet I (indicated by the three black arrows) shift their peak activity to become Triplet II muscles.

Three distinct masticatory motor patterns

In conclusion, Australian herbivores have modified a primitive pattern in different ways and have come up with three distinct masticatory motor patterns. This was accomplished by altering the timing of activity in the adductor muscles seen in primitive mammals. Macropods have altered the timing of Triplets I and II muscles to achieve a powerful vertically orientated power stroke, followed by a weaker transversely orientated power stroke.  Wombats have developed a powerful transversely orientated power generated only by working side muscles. To my knowledge there is no parallel to the macropod and wombat motor patterns within placental herbivores. Koalas on the other hand evolved a masticatory pattern that is analogous to that of some large placental ungulates.

These three patterns represent independent adaptations for the mastication of tough fibrous plant material. The entire radiation of marsupial occurred on an isolated  Australia continent. These three animals are the paltry remnants of a massive fauna of Australian herbivores that disappeared about 49,000 years ago.