Comparative functional morphological study of masticatory system in Carnivora

概要

Carnivora is an ecologically diverse group with various lifestyles, such as terrestrial, aquatic, and arboreal. They show a wide range of body size and external morphology. Contrary to the name of the taxon, the actual diet of Carnivora is diverse, including carnivorous, piscivorous, herbivorous, and omnivorous food habit. In vertebrates, systems that assist in various functions such as eyes, nose, ears and brain concentrate in the head part. The masticatory system is one of the most essential systems within the head. The mastication in mammals allowed them to efficiently extract energy from food. Several masticatory organs such as teeth, skull, and the temporomandibular joint comprise the masticatory system in the head. When these masticatory organs work as one system, it produces bite force. There are three aims in this thesis. The first purpose of this study is to understand the functional morphological strategies of masticatory system among lineages of a diverse mammalian group: Carnivora. Secondly, I investigated the relationships between the organs that contribute to mastication, and to confirm the functional morphological strategies that produce bite force. Lastly, I established a new bite force estimation method that is supported by the anatomical data. I carried out anatomical validations using thirty-two species of Carnivora belonging to ten families. In Chapter 1, I examined the morphological changes in the masticatory muscles in Carnivora to clarify their variation in masticatory muscle among families. In addition, I investigated the relationship of the masticatory muscle with other morphological features such as teeth, skull and ecology. I measured the physiological cross-sectional area (PCSA) of the masticatory muscles as an indicator of muscle force from all thirty-two species. As a result, PCSA of all masticatory muscles correlated to the body size of the species. Carnivora species with smaller body size have the larger PCSA values in the masticatory muscle compared to the species with larger body size. Because of the metabolism, smaller carnivorans spend more time eating compared to larger carnivorans. Thus, smaller species have a need to have large masticatory muscle. In addition, PCSA of the masticatory muscle was also determined by the phylogenetic factor in Carnivora. Felidae showed significantly higher ratio of PCSA of the whole masseter and superficial masseter muscle layer against PCSA of total muscles. Also, the residuals of PCSA of the medial pterygoid, whole masseter and superficial masseter muscle layer in Felidae were much larger compared with those of the other families. I suggest that these large muscles in Felidae may facilitate the carnassial biting. Mustelidae have the highest ratio of PCSA of the temporalis muscles per PCSA of total muscles. Since the mandibular condyle of Mustelidae deeply fits into the glenoid fossa, temporomandibular dislocation does not usually occur, and thus members of Mustelidae can recruit their large temporalis for biting without the danger of temporomandibular dislocation. Furthermore, Canidae have high ratio of the medial pterygoid muscle and the superficial masseter muscle layer PCSA, and Ursidae have high ratio of the deep masseter muscle layer PCSA. My results suggest that by using these muscles, both Canidae and Ursidae shift the mandible horizontally. In Chapter 2, my purpose is to investigate the presence of phylogenetic constraint in Carnivora regarding gape. In addition, I aimed to understand which masticatory muscle is utilized for wide gape. Gape, which is the mouth opening, is also important to understand the functional morphological pattern of skull in Carnivora. Fiber architecture of masticatory muscle is interrelated with gape, especially fascicle length of the masticatory muscle. Also, it is known that the fascicle length influence not only excursion, which is the range of motion, and velocity but also production of force. My study reveals that among the masticatory muscles, the excursion of the superficial masseter muscle determines the size of gape. Also, the size of gape has a phylogenetic constraint. Felidae and Mustelidae can perform large gape angle. The gape distance measured between canines, in Felidae exceeds that in Canidae. Felidae have large gape angle and distance as a result of the long fascicle length of the superficial masseter muscle layer. Felidae prevents the decrease in PCSA, due to long fascicle length by increasing the mass. The strategy of the Felidae allows them to increase both fascicle length and PCSA. As a result, it permits them to perform wide gape and large force exerted by the superficial masseter muscle layer. In Chapter 3, I compared the temporomandibular joint structure between species and investigated the traits among family lineages. Also, the effect of the masticatory muscle PCSA on the structure of the temporomandibular joint was examined. Each masticatory muscle contract in different directions and put pressure at the temporomandibular joint. I studied the effect of the ratio of each masticatory muscle PCSA and each muscle size relative to body size on the structure of the temporomandibular joint. The size of the temporalis muscle relative to body size showed the highest correlation with the temporomandibular joint structure. When the temporalis muscle is large relative to the body size, the preglenoid projects caudally, the postglenoid projects rostrally, and the pre-postglenoid angle interval is small, meaning that the condyle is locked in the fossa to reinforce the temporomandibular joint. Carnivorans use developed blade-like carnassial teeth during mastication. Dislocation occurs when the carnassial teeth are used with the temporalis muscle. My results suggest that the temporomandibular joint is reinforced to prevent dislocation caused by the temporalis muscle. In Mustelidae, the temporomandibular joint with rostrally projected postglenoid is suitable for carnassial biting using the temporalis muscle. In Felidae, the force of the masseter muscle for carnassial teeth is diverted for the canine teeth by tightening the temporomandibular joint with caudally projected preglenoid. In Canidae, the masticatory muscle arrangement is well-balanced in terms of the combination action of the temporalis and the masseter muscle. Hence, enforcement of the temporomandibular joint by bone structure is unnecessary. In Chapter 4, I investigated the relationship between each masticatory muscle PCSA and the muscle attachment area of skull. I established a new method that reconstructs the masticatory muscle PCSA from skull specimen. Specimens in which masticatory muscle PCSA can be measured are rare. However, skull collections are preserved in many institutions all over the world including rare or extinct species. Thus, if masticatory muscle PCSA could be measured from skull specimens, analyses using a range of species will be possible. For this reason, I proposed the use of selected measurement area (SMA), which is based on the ridges and scars of masticatory muscle attachment area on skulls. I show that SMA highly correlates with PCSA. However, the SMA of the superficial masseter muscle layer and its PCSA has weaker correlation compared to that of other muscles and their PCSAs. Felidae, which has a small attachment area relative to PCSA, presumably causes this result as the superficial masseter muscle layer of felids protrudes from the skull to use the developed carnassial teeth. In Chapter 5, I estimated the bite force of Carnivora using the 3D morphometrical estimation method. The bite force estimated using my method in Neovison vison was compared with the direct in vivo measurement data of the bite force in Mustela putorius furo, which is close to N. vision both in terms of phylogeny and body size. The estimated bite force was within the range of values obtained in in vivo experiment. The bite force of both canine and molar teeth at the working side was compared among thirty-two carnivoran species. As a result, Felidae, Cuon alpinus, Paguma larvata, Helarctos malayanus, and Procyon lotor marked large canine and molar bite forces, and Ailurus fulgens marked large molar bite force. In addition, N. vison, M. itatsi, Potos flavus and pinnipeds marked small canine and molar bite forces. In large predators such as Felidae and C. alpinus, the bite force at canine teeth is necessary to capture large prey and also the bite force at carnassial teeth is necessary to slice meat. Paguma larvata, Helarctos malayanus, and Procyon lotor performs large bite force, which is used to destruct a variety of prey. Thus, these species increases the range of prey that can be used as food. The reason that A. fulgens performs large bite force only at the molar teeth is presumably a specialization to grinding bamboo. Small carnivorans feed on prey with small body size. It is most likely that N. vison and M. itatsi do not require large bite force. P. flavus feed on ripe fruits. Thus, they do not demand large bite force. Pinnipeds such as Phoca largha and Odobenus rosmarus swallow fish and shellfish. Thus, large bite force is unnecessary in these species. My study suggests that Carnivorans produce bite force using a strategy suitable for their diet. There are three essential morphometrical factors to produce large bite force including 1) reduction of the distances between the temporomandibular joint and working teeth, 2) elongation of the distance from the temporomandibular joint to the line of action of each masticatory muscle, and 3) enlargement of PCSA. Most carnivroans use the second and the third strategies to increase bite force. However, only the third strategy is utilized in Felidae and C. alpinus. Performing large bite force by the enlargement of PCSA enables the felids and C. alpinus to chew using large consistent force. This is important during prey capture and slicing meat. A. fulgens performs large bite force through the second strategy such as the elongation of the distances from the temporomandibular joint to the line of action of masticatory muscles. Masticatory morphology does not rely on the muscles and prevents muscle fatigue, which is advantageous during the mastication of bamboo that lasts for a long time. My study suggests that Felidae, C. alpinus, and A. fulgens have distinctive masticatory strategies.