William P. Wall and Sherri J. Hayes
Department of Biology
Milledgeville, GA 31061
A biomechanical analysis of mastication in the protrogomorphous Oligocene rodent, Ischyromys is presented. Ischyromys jaw muscles are reconstructed based on comparison with various modern rodents, particularly Sciurus. Detailed dissections of the temporalis, masseter lateralis, masseter medialis, and masseter superificialis in Sciurus, Rattus, and Cavia provided baseline data for the sciuromorph, myomorph, and hystricomorph jaw muscle patterns. Analysis of muscle vectors and dental wear patterns indicate Ischyromys had a single phase chewing cycle centered around grinding at the cheek teeth. This information is compared to mastication in modern rodents which exhibit an anterior shift of some parts of the masseter muscle and a more posterior orientation for the temporalis. This muscle arrangement allows advanced rodents to utilize a two phase chewing cycle, an ingestive phase when the incisors are in proper occlusion and a grinding phase when the cheek teeth line up. We believe the reason for the expansion of the masseter muscle onto the rostrum is for increased efficiency in gnawing. The posterior orientation of the temporalis is interpreted as an adaptation to resist extrinsic forces at the incisors and for positioning the jaw properly for the grinding phase. Increased efficiency of gnawing is viewed as the major reason for the success of rodents by opening up additional feeding niches, i.e. nuts and other hard shelled vegetation.
Rodents are the most successful, diverse group of mammals alive today. There are 29 families, 426 living genera, and 1,814 living species of rodents (Nowak, 1991). They are found in a wide variety of habitats: deserts, tundra, mountains; some are burrowers and some are aquatic. They are a remarkably complicated group with respect to morphological diversity, lines of descent, and parallel evolution of similar features in different groups (Vaughan, 1986).
Three jaw muscle patterns, sciuromorph, myomorph, and hystricomorph are often used to designate major taxonomic divisions of the rodents. Not every rodent can readily be placed into one of these groups, however, nor do experts agree on how the morphologic types evolved (Eisenberg, 1981). Specifically these groups represent important differences in the structure of the skull and masseter muscles. Sciuromorphs typically do not have an enlarged infraorbital foramen and the lateral masseter attaches to both the zygomatic arch and rostrum via the zygomatic plate. Myomorphs have a slightly enlarged infraorbital foramen and the medial masseter attaches to the zygomatic arch and rostrum via the infraorbital foramen. Myomorphs also have a zygomatic plate which allows the lateral masseter to expand onto the rostrum. Hystricomorphs have a greatly enlarged infraorbital foramen and the medial masseter attaches to the zygomatic arch and the rostrum via the infraorbital foramen. The most primitive rodents were protrogomorphous, a masseter condition lacking the specializations described above.
The oldest rodent, Acritoparamys, appeared in the late Paleocene. By the late Eocene some rodents had abandoned the primitive arrangement of jaw musculature in which all three parts of the masseter were attached to the zygomatic arch. The time between the late Eocene and middle Oligocene was a period of important diversification (Wilson, 1972).
The phylogenetic relationships between rodent groups are complex. Different rodent lineages may have evolved similar jaw muscle patterns independently. Since rodent evolution is so equivocal, we decided to avoid this massive complexity and look at the radiation of rodents not from an ancestor-descendant viewpoint, but from a biomechanical or functional viewpoint. A particular focus of our research was to determine what morphological changes gave rise to sciuromorphs and why these changes occurred.
MATERIALS AND METHODS
The jaw musculature from a typical example of each of the major rodent groups was examined in detail. All recent specimens used in this study are housed in the Georgia College Mammal Collection (GCM). A tree squirrel, Sciurus carolinensis, was chosen for the sciuromorph; GCM 594, 595, 596, 597, 598, 850, 851, and 852; a laboratory rat, Rattus norvegicus, was selected for the myomorph; GCM 599, 600, and 853; and a guinea pig, Cavia porcellus, provided the hystricomorph, GCM 601, 602, and 854.
Each rodent was preserved in 10% formalin and then dissected. The points of origin and insertion for the temporalis and each component of the masseter muscle: the masseter superficialis, masseter medialis, and masseter lateralis were identified. The fiber pattern for each muscle was described in order to determine the line of action of the muscle. We arbitrarily decided not to include the pterygoideus in this study to simplify our analysis.
Individual muscles from both the right and left side were removed and weighed on an Ainsworth balance to the nearest 0.01 gram in order to determine the relative mass of each muscle. Based on these muscle weights we determined the relative percent of the total muscle mass for each muscle to use in a vector analysis (see Hiiemae, 1971 for technique).
We chose Ischyromys, a common fossil protrogomorph from the Oligocene of Badlands National Park, South Dakota, to represent the ancestral rodent jaw muscle pattern. The origin and insertion for each jaw muscle was determined by comparing muscle scars on the recent rodents to the corresponding muscle scars on Ischyromys. All of the Ischyromys specimens used in this study are housed in the Georgia College Vertebrate Paleontology Collection (GCVP). Cranial material included GCVP 275, 276, 277, 279, 290, and 295. We estimated the mass for each muscle in Ischyromys by determining its surface area and comparing that to Sciurus.
To eliminate size differences we measured the diameter of the foramen magnum of each species, then standardized the size of each rodent to the taxon with the largest foramen magnum. A vector length of 10cm=100% was chosen for Sciurus, the largest rodent. Individual vector length was based on its percentage of the total muscle mass. Vector direction was a line drawn from the point of insertion through the center of mass of the muscle. Individual lever arms were measured for each muscle using the jaw joint, cheek teeth, and incisors as alternate fulcra (Bramble, 1978). To test the accuracy of our biomechanical analysis of Ischyromys we examined cheek teeth using a Bausch and Lomb dissecting scope at 30X magnification to determine wear facet patterns. Dental wear patterns are a good indicator of the relative importance of each part of the chewing cycle which ultimately is dictated by muscle activity (Butler, 1972). The following specimens were examined: GCVP 28, 45, 47, 49, 50, 60, 79, 80, 81, 86, 276, 279, 289, 291, 292, 293, 522, 766, 1133, 1138, and 1793.
Masticatory Musculature of Recent Rodents (Table 1)
M. Masseter Lateralis.--In Rattus norvegicus this muscle originates on the anterior zygomatic arch and on the rostrum via the zygomatic plate; it inserts on the border of the masseteric fossa and the edge of the jaw. The lateralis was the largest component of the masseter muscle. In Sciurus carolinensis the muscle originates on all of the zygomatic arch and onto the rostrum via the zygomatic plate; it inserts on the jaw from the anterior border of the cheek teeth through to the posterior border of the masseteric fossa and edge of jaw. The lateralis is the largest jaw muscle in the squirrel. In Cavia porcellus the lateralis originates only on the zygomatic arch; it inserts on the posterior region of the jaw and angle of the jaw. The lateralis is the smallest of the masseter muscles in the guinea pig.
M. Masseter Medialis.--In Rattus norvegicus the medial masseter originates on the anterior portion of the zygomatic arch and onto the rostrum via the infraorbital foramen; it inserts onto the masseteric fossa. The medial masseter is the smallest component of the masseter muscle in the myomorph. In Sciurus carolinensis the medial masseter originates on the ventral surface of the zygomatic arch via the zygomatic plate and inserts onto the masseteric fossa. It is larger than the superficial masseter but smaller than the lateral masseter. In Cavia porcellus the medial masseter originates on the rostrum via the enlarged infraorbital foramen; it inserts onto the masseteric fossa. It is larger than the lateralis but smaller than the superficialis.
M. Masseter Superficialis.--In Rattus norvegicus the masseter superficialis originates on the pit on the rostrum; it inserts on the angle of the jaw. It is the second largest of the masseter muscles in the rat. In Sciurus carolinensis the masseter superficialis originates on the anterior base of the zygomatic arch; it inserts on the angle of the jaw. It is the smallest of the masseter muscles in the squirrel. In Cavia porcellus the masseter superficialis originates on the anterior portion of the zygomatic arch and it inserts on the angle of the jaw. It is the largest jaw muscle in the guinea pig.
Temporalis.--In Rattus norvegicus the temporalis originates on the temporal fossa; it inserts on the coronoid process. It is the largest jaw muscle in the rat. In Sciurus carolinensis the temporalis originates on the temporal fossa and inserts on the coronoid process. It constitutes next to the smallest amount of the skull musculature in the squirrel. In Cavia porcellus the temporalis is the smallest of the jaw muscles studied and originates in a small temporal fossa; it inserts on the coronoid process.
Our reconstruction of the jaw musculature of Ischyromys is shown in Figure 1. The masseter lateralis originated only on the zygomatic arch and inserted on the edge of the jaw. The masseter medialis originated on the zygomatic arch and inserted onto the masseteric fossa. The masseter superficialis originated on a pit on the rostrum and inserted along the angle of the jaw. The temporalis originated on the temporal fossa and inserted on the coronoid process. Ischyromys is advanced compared to other protrogomorphous rodents (such as Ischyrotomus reconstructed by Wood, 1965) in having the origin of the superficial masseter on the rostrum instead of on the zygomatic arch.
Figure 2 illustrates our vector analysis of jaw muscles in Cavia, Rattus, Ischyromys, and Sciurus. Note in particular the dominance of the temporalis and medial masseter in Ischyromys , and the more vertical orientation of these muscles compared to the other rodents. Our analysis of jaw muscle action implies that the lingual phase has become more important than the buccal phase in modern rodent mastication.
Examination of dental wear patterns supports our findings. Primitive rodent occlusion was ectental with the lingual phase possessing a more anterior component than the buccal phase which approaches the horizontal (Butler, 1972). The hypocone and protocone are similar in size and shape in Ischyromys. The hypocone occludes with the protoconid and the protocone occludes with the hypoconid. On the lower molars, the entoconid is high and connects with the hypoconid via a transverse ridge. Here a facet is present resulting from occlusion with the protocone; similarly, there is a facet on the metaconid resulting from its occlusion with the hypocone and a facet on the entoconid also resulting from occlusion with the hypocone. In Ischyromys, lingual phase wear facets cover a larger area of the tooth, but distinct buccal phase wear facets are present. In Sciurus, lingual and buccal phase facets are almost continuous forming a single oblique grinding surface. Note for example, that the path of the hypoconid, during the buccal and lingual phase, develops a more anterior and longitudinal orientation in Sciurus than in Ischyromys. This wear pattern is almost certainly due to the anterior shift in orientation of the masseter in sciuromorphs..
Rodent classification is based primarily on the structure of the jaw muscles, infraorbital foramen, characteristics of the lower jaw, and the cheek teeth (Weijs, 1980). These characters are all part of the food acquisition system, and when traced through time, their observed modifications reveal a complex phylogeny. Gaps in the sequence, however, cannot always be filled. Whole families of rodents stand in uncertain relations to proposed phylogenies. This situation is not surprising; in a phase of rapid evolution a gap of a few million years is enough to permit a discrete group to appear full-blown in the fossil record. The ancestry of such a group is often unclear because of parallelism among the earlier lineages from which it could have descended (Wahlert, 1974). Since definitive ancestor-descendant relations are difficult to determine, questions regarding the origin of modern groups are still problematic. Functional analysis of the feeding mechanism should add to our knowledge of rodent evolution. Woods and Howland (1979) examined the radiation of recent capromyid rodents in a similar way with moderate success.
The aim of this study was to construct a biomechanical model which could explain what changes took place in the evolution of sciuromorphs from protrogomorphs. Modern rodents have a two phase chewing cycle, one when the cheek teeth are in occlusion, the masticatory cycle, and the other when the incisors are in occlusion, the ingestive cycle (Hiiemae, 1971). The masseter and pterygoideus are responsible for side to side movement during mastication. The anterior segments of the masseter are responsible for rapid jaw closing, which is demonstrated when the incisors are in occlusion.
The evolution of sciurid mastication from a protrogomorph like Ischyromys is due primarily to a shift in the orientation and relative importance of the jaw muscles. Ischyromys had a more vertical orientation for all of the jaw musculature and the vector lengths for each muscle were not significantly different. In Sciurus, all components of the masseter have a noticeable anterior orientation with the masseter lateralis being greatly enlarged. The temporalis is also enlarged and displays a posterior orientation. A similar dichotomy between the masseter and temporalis is seen in myomorphs and hystricomorphs. The vertical orientation of the jaw muscles in Ischyromys implies that protrogomorphs had only a single phase chewing cycle centered around the cheek teeth. We believe the anterior migration of the masseter muscle in advanced rodents increased efficiency in the ingestive phase of the chewing cycle. Expanding the masseter onto the rostrum adds a second phase to the chewing cycle, resulting in increased speed of jaw closure while the incisors are in occlusion. The posterior orientation of the temporalis allows it to act as a stabilizer during the ingestive phase, resisting extrinsic forces at the incisors and as a jaw retractor to correctly align the cheek teeth during the grinding phase.
Our interpretation of the importance of incisor gnawing in the evolution of sciuromorphs is supported by a comparison of the lever systems for each muscle using the jaw joint, bite point, and incisors as possible fulcra. Sciurus exhibits increased efficiency compared to Ischyromys when viewing the incisors or jaw joint as the fulcrum but the two genera are similar when the cheek teeth are interpreted as the fulcrum.
Increased efficiency in the ingestive phase allowed the advanced rodents to occupy additional niches by making available a new food source: nuts and other hard shelled vegetation, a food source that protrogomorphs were probably unable to take advantage of. The success of modern rodents therefore seems to be due to their highly efficient two phase chewing cycle which takes full advantage of the chisel-like, ever-growing incisors.
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Bramble, D.M., 1978. Origin of the Mammalian Feeding Complex: Models and Mechanisms: Paleobiology, v. 4(3), p. 271-301.
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Figure 1. Muscle reconstruction of Ischyromys. Abbreviations: Ml, masseter lateralis; Mm, masseter medialis; Ms, masseter superficialis; and T, temporalis.
Figure 2. Vector diagrams illustrating relative magnitude and direction of Ml, masseter lateralis; Mm, masseter medialis; Ms masseter superficialis; and T, temporalis. A, Cavia porcellus; B, Rattus norvegicus; C, Ischyromys sp.; and D, Sciurus carolinensis.
Table 1. Wet Weights and Percentages of Rodent Jaw MusclesRODENT WEIGHT PERCENTAGERattus norvegicus (Myomorphous) M. Masseter Lateralis 1.68g 29.7% M. Masseter Medialis 0.99g 17.5% M. Masseter Superficialis 1.23g 21.7% Sum of Masseter 3.90g 68.9% Temporalis 1.76g 31.1% Sum of Masseter + Temporalis 5.66g 100%Sciurus carolinensis (Sciuromorphous) M. Masseter Lateralis 2.66g 40.8% M. Masseter Medialis 1.49g 22.9% M. Masseter Superficialis 0.96g 14.7% Sum of Masseter 5.11g 78.4% Temporalis 1.41g 21.6% Sum of Masseter + Temporalis 6.52g 100%Cavia porcellus (Hystricomorphous) M. Masseter Lateralis 0.16g 7.5% M. Masseter Medialis 0.66g 30.8% M. Masseter Superficialis 1.25g 58.4% Sum of Masseter 2.07g 96.7% Temporalis 0.07g 3.3% Sum of Masseter + Temporalis 2.14g 100%Back to Table of Contents
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