Jpn. J. Oral Biol., 43: 43-59, 2001.

ORIGINAL

Relative Growth of Molar Sizes in Three Species of Arvicolinae,

Eothenomys andersoni , Eothenomys smithii and Microtus montebelli

Eiichi Sakai and Yasushi Uematsu

Department of Second Anatomy, School of Dentistry, Aichi-Gakuin University (Chief: Prof. Hajime Hanamura) 1-100 Kusumoto-cho, Chikusa-ku, Nagoya 464-8650 , Japan 〔Received on June 16,2000; Accepted on September 25,2000〕

Key words: Arvicolinae species/continuously growing molar/molar size/relative growth/eating habit

Abstract: In this paper, the mesiodistal and buccolingual crown diameters of the upper and lower molars in three Arvicolinae species , Eothenomys andersoni, Eothenomys smithii and Microtus montebelli were measured and their relative growth patterns relative to each condylobasal length were studied from the perspective of infraspecific relative growth and compared among the three species. The mesiodistal and buccolingual crown diameters of each upper and lower molar in all three species continue growing with the growth of condylobasal length. Comparing the growth potentials among molars, in each upper and lower molar relative to the condylobasal length the growth potential of the third molar was higher than that of the first and second molars except for the buccolingual crown diameters of the upper and lower molars in E . smithii. The growth potentials of mesiodistal crown diameters were higher than those of buccolingual crown diameters of all molars in E. andersoni, of the upper and lower third molars in E . smithii and of the upper third molar in M. montebelli. Therefore, the forms of these molars became relatively more slender as their condylobasal lengths increased. It can be surmised that the characteristics in relative growth of the upper and lower molars correspond to the characteristics in eating habits (herbivore) and the mandibular movement of the three Arvicolinae species. Comparing growth potentials among the three species , there was no fixed tendency among the relative growth coefficients (a).

抄 録:ハ タ ネ ズ ミ亜 科 に属 す ヤ チ ネ ズ ミ,ス ミス ネ ズ ミお よ び ハ タ ネ ズ ミの 上 ・下顎 大 臼 歯 の 近 遠 心 径 お よ び 頬 舌 径 を計 測 し,頭 蓋 骨 基 底 全 長 に対 す る 相 対 成 長 様 相 を種 内 相 対 成 長 の 立 場 か ら検 討 し,さ ら に そ れ ら を種 間 で 比 較 し た 。3種 の上 ・下顎 各 大 臼 歯 の 近 遠 心 径 お よ び 頬 舌 径 は,頭 蓋 骨 基 底 全 長 の成 長 に 伴 っ て 成 長 を続 け る 。 歯 種 別 に成 長 能 を比 較 す る と,ス ミス ネ ズ ミの 上 ・下顎 大 臼 歯 の頬 舌 径 を除 き,第3大 臼 歯 で 第1,第2大 臼 歯 よ り成 長 能 が 高 い。 近 遠 心 径 の 成 長 能 は,ヤ チ ネ ズ ミの全 大 臼 歯,ス ミス ネ ズ ミの 上 ・下顎 第3大 臼 歯 お よ び ハ タ ネ ズ ミの 上 顎 第3大 臼 歯 で 頬 舌 径 の そ れ よ り大 きい 。 した が っ て,こ れ らの 大 臼 歯 は 頭 蓋 骨 基 底 全 長 の 成 長 が 進 む に 従 い,相 対 的 に よ り細 長 い形 態 を と る。 これ らの 結 果 は,3種 の 食 性(食 植 性)お よ び下 顎 運 動 と強 く結 び つ い て い る こ と を示 唆 して い る 。種 間 で成 長 能 を比 較 す る と,相 対 成 長 係 数 α の 値 に一 定 の 傾 向 は認 め られ な い 。

differences are remarkable. The specific differences Introduction of the cranium in Muridae are found at the locations directly connected with the molars or masticatory The teeth are a part of the digestive systems and muscles, and these differences correspond to differ- play a direct role in the preservation and metabolism ences in eating habits1). of the living body. The teeth of the mammal, espe- The dental formula of Muridae is 1・0・0・3/1・ cially the molars located in the rear, have forms and 0・0・3=16, and the second and third incisors , canines structures peculiar to the species and their specific and all premolars in the upper and lower jaws degen - 44 Jpn. J. Oral Biol., 43: 43-59, 2001.

erate and disappear compared with the basic dental molars between the mesiodistal and buccolingual formula of a mammal. The incisors are rootless and crown diameters and among the three species are continue growing throughout their life. This charac- connected with the characteristics of eating habits teristic is common to all species of Muridae. However, and masticatory movement in Arvicolinae. there is a difference in the growth patterns of molars Although the eating habits of all three species stud- between Murinae and Arvicolinae. That is, in Murinae ied are basically herbivorous, there are also specific the molars form roots while the tooth crowns continue differences in detail1). to abrade after completion of the tooth bodies, but in Arvicolinae the pulp cavities do not close and the Materials and Methods molars go on growing throughout their life or roots are formed in old age. The materials used in this study were as follows: The most important points at the level of individual 429 (217 males, 200 females and 12 unidentified) E. preservation in mice are the differences in quality and andersoni caught in Mt. Yatsugatake, Nagano Prefec- quantity of food, in other words the kind of food and ture, 107 (59 males, 40 females and 8 unidentified) E. the amount eaten are directly connected with differ- smithii caught in Mt. Daisen, Tottori Prefecture and ences of quantity and steps of growth, and also bring 190 (101 males, 68 females and 21 unidentified) M. acceleration or lag in their developmental rate1). For montebelli caught in Mt. Yatsugatake and Kiso Val- this paper, we measured the mesiodistal and buccolin- ley, Nagano Prefecture2-4). These mice were of vari- gual crown diameters of each upper and lower molar ous sizes from subadults just starting independent life, in the three Arvicolinae species, the Anderson's red- which were caught in field traps, up to old specimens . backed vole, Eothenomvs andersoni, the Smith's red- The mesiodistal and buccolingual crown diameter backed vole, Eothenomvs smithii and the Japanese on each molar and condylobasal length (dimension field vole, Microtus montebelli, and studied their rela- from the most projective point of the premaxilla tive growth patterns relative to each condylobasal (prosthion) to the extreme end point of the occipital length. In this process, we wanted to clarify the condyle) were measured with an optical microscope growth directions of each upper and lower molar and for measurement with a printer (MS 113; Fusoh Co ., how the differences of growth potentials among Ltd., Tokyo, Japan) reading to 0 .001mm (Fig. 1). The

Fig. 1 The skull and right upper and lower molars of Eothenomys

andersoni showing the cranial and crown measurements . CBL: condylobasal length, MD : mesiodistal crown diameter , BL: buccolingual crown diameter, M1: upper 1 st molar , M2: upper 2 nd molar, M3: upper 3 rd molar, M1: lower 1 st molar , M2 lower 2 nd molar, M3: lower 3 rd molar , Same abbreviations are used Tables 2-10 and Figs. 2-7 . E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 45

cranium and mandible were fixed to a micro slide ences among relative growth coefficients (α) were glass with wax so that the occlusal surface of their tested using covariance analysis. molars was set in a horizontal plane. The mesiodistal Generally, there was no gender difference in the crown diameter of the upper and lower molars was molar size of Muridae5-7). Therefore, male, female measured in parallel with the long axis of each molar . and unidentified data were combined for the statisti- The buccolingual crown diameter of the upper and cal analysis in this study. lower molars was measured at right angles to the longitudinal axis of the mesiodistal crown diameter . Results The measurements were done on the right side (Fig . 1). 1. Mesiodistal crown diameter Next, the dimension of the upper and lower molars The sample means (Mean) and standard deviations (y) against the condylobasal length (x) was plotted (SD) of the condylobasal length (CBL) and the on double logarithmic grids for each specimen . By the mesiodistal crown diameters were calculated for each least squares method, the relative growth coefficients skull and molar of the three Arvicolinae species, the (α) and initial growth indices (log b) relative to the result and the greatest and least values (Max, Min) condylobasal length were calculated with the al- are shown in Tables 1, 2. lometric formula y=bxα(log y=α log x+log b) and The allometric formula y=bxα(log y=α log x+ then the growth patterns were examined. The differ- log b) could be applied (p<0.01), when the mesiodistal crown diameters of each upper and lower molar against the condylobasal length in E. andersoni, E. Table 1 Descriptive statistics for measurements smithii and M. montebelli were plotted on double (mm) of CBL (condylobasal length) in logarithmic grids (Fig. 2). The mesiodistal crown three species of Arvicolinae diameter of each upper and lower molar relative to the condylobasal length in the three Arvicolinae species shows a monophasic allometry. The relative

growth coefficients (α) and initial growth indices (log b) of the mesiodistal crown diameters relative to the condylobasal length in the three species are shown in Table 3. The α values of the mesiodistal crown diameters in each upper and lower molar relative to the con-

Table 2 Descriptive statistics for measurements (mm) of mesiodistal crown diameters in three species of Arvicolinae 46 Jpn. J. Oral Biol., 43: 43-59, 2001.

Fig. 2 Allometric growth of mesiodistal crown diameters of each molar against condylobasal l ength for three species of Arvicolinae, shown by regression lines on double logarithic grids .

dylobasal length were smaller than 1.00 (p<0 .01) ues of the upper third molars in three species and the except for those of the upper third molar in three lower third molars in two Eothenomys species did not species and the lower third molar in two Eothenomys show any significant differences to 1 .00 (p<0.01), so species. Therefore, the mesiodistal crown diameters the mesiodistal crown diameters of these molars grow of these molars became relatively smaller as the at the same speed as the condylobasal length . condylobasal lengths increased. However, the α val- Comparing the growth potentials among molars E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 47

(Fig. 3, Table 4), an overall mesio-distal (anterior- diameters of each lower molar, those of the first posterior) gradient was observed, and the α values of molars were clearly bigger than those of the second the upper and lower third molars were largest in all and third molars throughout the growth process, but three species. The smallest were the upper second for those of the second and third molars, whose molar in three species, the first molar in two Eoth- measurements almost overlapped, the relationship of enomys species and the lower second molar in M . sizes differed according to age. Thus as shown in Fig. montebelli . There were significant differences in the α 2(b), the mesiodistal crown diameters of second values between the third and first or between the third molars at the weaning period or just after that were and second molars in three species except for the first slightly bigger than those of the third molars, while

and third molars in M. montebelli. So the growth the α values of the third molars in the three species potentials of molars located more posteriorly were were clearly bigger than those of the second molars, higher than those in the anterior . so the difference in mesiodistal crown diameters On the mesiodistal crown diameters of each upper between the second and third molars decreased with molar, those of the first molars were the biggest and advancing age. Then as age advanced further, the those of the second molars were the smallest through- relationship of sizes between the second and third out the growth process in the three species, but in the molars in two Eothenomys species reversed, that is, differences between the first and third molars, the the size of the third molar became bigger than the significant differences in α values among these de- second molar. The mesiodistal crown diameters of the creased, while those between the second and third second and third molars in M. montebelli became molars increased as the condylobasal lengths in- creased (Fig. 2(a)). Among the mesiodistal crown

Table 3 Allometric growth constants of mesiodistal crown diameters of first molar (M 1), second molar (M 2) and third molar (M 3) against condylobasal length in three species of Arvicolinae

Fig. 3 Growth gradients by the values of α in mesiodistal crown diameters of upper and lower molar against condylobasal length for three species of Arvicolinae.

Table 4 Comparison of values of α of mesiodistal crown diameters among upper and lower three molars 48 Jpn. J. Oral Biol., 43: 43-59, 2001.

almost identical in old specimens. are shown in Table 6. Comparing the growth pattern among the three In the buccolingual crown diameter of each upper studied species (Figs. 3 and 4, Table 5), there was a and lower molar relative to the condylobasal length, tendency for the α values of the upper molars, except E. andersoni, E. smithii and M. montebelli showed a the third molar in E. andersoni, to be bigger than monophasic allometry when plotted on double logar- those in E. smithii and M. montebelli, and there was a ithmic grids (Fig. 5). The relative growth coefficients

significant specific difference on the upper first molar (α) and initial growth indices (log b) of the buccolin- between E. andersoni and M. montebelli. The α value gual crown diameters relative to the condylobasal of the upper third molar in E. smithii was bigger than length are shown in Table 7.

those of E. andersoni or M. montebelli, but there were The α values of the buccolingual crown diameters no significant specific differences among these. The in each upper and lower molar relative to the con- regression lines of each upper molar in the three dylobasal length were smaller than 1.00 (p<0.01) species almost overlapped, so there was no fixed except for the lower third molar in M. montebelli, so tendency in the relative lengths of each upper molar. the buccolingual crown diameters of these molars With regard to the lower molars, there were no decreased relatively as the condylobasal lengths grow.

significant specific differences in the α values in the There were no significant differences between the α lower first molar among the three species (Table 5), values only on the lower third molar in M. montebelli but the regression line of the lower first molar in M. and 1.00 (p <0.01), where the buccolingual crown montebelli was clearly located higher than those of diameter grew at the same tempo as the condylobasal two Eothenomvs species throughout their growth proc- length. ess as shown in Fig. 4. So the mesiodistal crown Comparing the growth potential among molars (Fig. diameter on the lower first molar in M. montebelli 6, Table 8), a mesio-distal gradient can be seen in the was relatively bigger than those of the two Eoth- α values of the upper and lower molars in M. cnomys species. For the lower second and third montebelli and the lower molars in E. andersoni, and molars, the α values in E. andersoni were the biggest there were significant differences between the lower and those in M. montebelli the smallest, and there first and third molars in E. andersoni and M . were significant specific differences in the lower sec- montebelli and between the lower second and third ond molars between E. andersoni and M. montebelli, molars in M. montebelli. On the upper molar in two

and in the third molars between the two Eothenomys Eothenomys species, the α value of the upper second species and M. montebelli. molar was bigger than those of the first and third As shown in Fig. 4, there were no specific differ- molars, and there were significant differences

ences in the relative sizes of the lower second and between the second molar and the first or third molar . third molars in specimens immediately after the The α values for each lower molar in E . smithii were weaning period, but as indicated previously, there was almost the same and there were no differences among a difference in growth potential among these molars, them. so the mesiodistal crown diameters of the lower sec- Among the buccolingual crown diameters of the ond molar in E. andersoni or of the third molars in the upper and lower molars, that of the first molar was two Eothenomys species became larger than that in M. the biggest and that of the third molar was the smal - montebelli as their condylobasal lengths grew . lest throughout their growth process in the three species, but in E. andersoni there were significant

2. Buccolingual crown diameter differences in the α values among the upper molars; Sample means (Mean) and standard deviations (SD) the size difference between the upper first and second of the buccolingual crown diameters were calculated molar increased with the condylobasal length , where for each molar of the three Arvicolinae species , the as the difference between the upper second and third result and the greatest and least values (Max, Min) molar decreased (Fig . 5(a)). As shown in Fig . 5(b), E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 49

Fig. 4 Allometric growth of mesiodistal and bucccolingual crown diameters of upper and lower molar against condylobasal length for three species of Arvicolinae , shown by regression lines on double logarithic grids. 50 Jpn. J. Oral Biol., 43: 43-59, 2001.

Table 5 Comparison of values of α of mesiodistal crown diameters among three species of Arvicolinae

Table 6 Descriptive statistics for measurements (mm) of bucccolingual crown diameters in three species of Arvicolinae

the size differences between the lower first and third lower molar in the two Eothenomys species , except the molars in E. andersoni and between the lower third lower first molar in E. smithii, were bigger than those

and first or second molars in M. montebelli decrease of the buccolingual crown diameters , and there were as their condylobasal lengths grew. significant differences in all molars in E . andersoni Comparing growth patterns among the three stud- and in the upper and lower third molars in E. smithii . ied species (Figs. 4 and 6, Table 9), a tendency was Therefore each upper and lower molar in two Eoth- found for the α values of the upper and lower molars enomys species, except for the lower first and second in M. montebelli to be bigger than those in the two molars in E. smithii, took a form in which their Eothenomys species, but there were significant spe- mesiodistal crown diameter was longer than their cific differences only in the lower third molars buccolingual crown diameter as their condylobasal between M. montebelli and the two Eothenomys length grew, that is to say, they had a slender shape

species. The regression lines of the buccolingual mesiodistally. In M. montebelli , there were no signifi- crown diameters of each upper and lower molar rela- cant differences in the a values between the mesiodis - tive to their condylobasal lengths in M. montebelli tal and buccolingual crown diameters on the upper were located higher than those of the two Eothenomys and lower first and second molars , but on the upper species as shown in Fig. 4, so there was a tendency for third molar the α value of the mesiodistal crown the relative sizes of buccolingual crown diameters of diameter was bigger than that of the buccolingual , each upper and lower molar in M. montebelli to be while on the lower third molar , the buccolingual larger than those in the two Eothenomys species . crown diameter α value was bigger than that of the Comparing the growth potentials between the mesiodistal, and these differences were significant . mesiodistal crown diameters and buccolingual crown Therefore, the form of the upper third molars became diameters (Figs. 3, 6 and Table 10), the α values of more slender, while that of the lower third molars the mesiodistal crown diameters of each upper and became more square as their condylobasal lengths E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 51

Fig. 5 Allometric growth of buccolingual crown diameters of each molar against condylobasal length for three species of Arvicolinae, shown by regression lines on double logarithic grids.

grew. on the third molar in M. montebelli and the buccolin- Comparing the growth potentials in corresponding gual crown diameter on the second molar in E. ander- molars between upper and lower (Fig. 7), there were soni (p<0.01), but there were no significant differ- significant differences in the α values of the mesiodis- ences on other molars and no fixed tendency in α tal crown diameter and buccolingual crown diameter values. 52 Jpn. J. Oral Biol., 43: 43-59, 2001.

Table 7 Allometric growth constants of buc- colingual crown diameters of first molar (M 1) , second molar (M 2) and third molar (M 3) against condylobasal length in three species of Arvicolinae

Fig. 6 Growth gradients by the values of α in buccolin. gual crown diameters of upper and lower molar against condylobasal length for three species of Arvicolinae.

Table 8 Comparison of values of α of buccolingual crown diameters among upper and lower molars

Table 9 Comparison of values of α of buccolingual crown diameters among three species of Arvicolina e

Table 10 Comparison of values of α among mesiodistal and buccolingual crown diameters. MD> BL indicates values of α of mesiodistal crown diameter is significantly larger than that of buccolingual crown diamete r E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 53

Arvicolinae, which are herbivores, are hypsodont molars continuously growing without forming roots throughout the animal's life or forming roots in old age. The forms of the occlusal surface of the former are bunodont and those of the latter are lophodont. In this way, the basic form of molars in Muridae are regulated by their eating habits. The specific differences of absolute sizes of the upper and lower molars and among each molar in the three species of Arvicolinae examined in this study were previously reported by Hanamura, et al.6), but Fig. 7 Growth gradients by the values of α in mesiodistal and buccolingual crown diameters of upper and these molars in the three species are continuously lower molar against condylobasal length for three growing teeth, and if there are differences in growth species of Arvicolinae. potentials of the upper and lower molars among each molar or species, the relation of molar sizes will differ according to age. Therefore, comparisons of absolute Discussion sizes of molars must be made among populations of the same age. So for this study, from the perspective Animals have varied eating habits, and necessarily of infraspecific relative growth, we compared the have differing anatomical and physiological mecha- growth potentials of each molar, then investigated nisms to heighten efficiency in consuming these foods. how their characteristic growth patterns connected The difference in these mechanisms will appear in the with the characteristics of their eating habits, and still digestive organs first. Therefore, the tooth form in further compared these among the three species. mammals has an aspect that is exceedingly conserva- The mesiodistal crown diameters and buccolingual tive and also has remarkable variation corresponding crown diameters of the upper and lower molars in the to environmental factors, especially differences in three species grew as their condylobasal lengths grew, eating habits. The molar form in particular shows but there were differences in relative growth patterns peculiarities according to the species, as reflected by for each molar : only relative growth patterns of the the animal's eating habits. For example, the biological mesiodistal crown diameters of the upper and lower distances based on molar size in seven species of third molars in the two Eothenomys species and the Muridae are more closely connected with their eating buccolingual crown diameter of the lower third molar habits and environmental factors of their habitat than in M. montebelli showed isometry, while the others to the phyletic classification of each species8,9). In showed a negative allometric growth pattern. Thus, it primates, it has been also reported that the connection can be said that the molar sizes on the whole become between tooth size and body size differs according to relatively smaller with advancing age. eating habits10-12). In E. smithii, the relative weight of the masticatory In Muridae, there are large differences in the and suprahyoid muscles that are connected with growth patterns and forms of molars between the masticatory movement directly or the relative weight Arvicolinae species and Murinae species, and these of the mandible that makes these muscles a functional differences have a large adaptive significance corre- matrix showed a negative allometric growth pattern sponding to differences in eating habits. Therefore, relative to the body weight13). This means that the the molars of Murinae, which are omnivores and quantity of ingestion per unit body weight gradually seed-insectivores, form roots and are brachyodont diminishes with growth, that is, the body size becomes molars which continue to abrade after the teeth have large. There may be a connection between the facts formed completely. However, the molars of that the smaller the body the larger the body surface 54 Jpn. J. Oral Biol., 43: 43-59, 2001.

area per body weight is and the bigger the standard than masticating seeds and insects. As for the diges- metabolic quantity is. tive efficiency of foods in the Muridae, that of the Furthermore, the relative weight of each lower herbivorous species is the lowest, and that of the molar in E. smithii showed a negative allometric seed-insectivorous species is the highest19), the food of growth pattern relative to the mandible weight4), and the herbivorous species is inferior in quality, so they this agrees with the result of this report. This may be need much more food. The continuously growing due to the fact that the size of the mandible is more molars in the three species have great meaning in that plastic than that of the molars14,15). These growth their mass and occlusal surface areas enlarge and patterns will be the same in E. andersoni and M. their durability for attrition becomes strong, and also montebelli. That is, food consumption in the their masticatory ability improves20). The relative Arvicolinae species decreases with advancing age and weight of masseter and temporal muscles relative to body enlargement, so the development of their mas- the body weight is heavier in E. smithii than in ticatory organs gets relatively weak especially in the Apodemus speciosus and Apodemus argenteus which molars. are seed-insectivorous species. This indicates the The mesiodistal crown diameters and buccolingual greater amount of mandibular movement and power- crown diameters of the upper and lower molars in the ful forces between the rows of upper and lower molars three species showed a monophasic allometry to the these muscles are able to provide for E. smithii". condylobasal length. On the relative growth of each At the time that the crowns complete their forma- part of the cranial bone relative to the condylobasal tion and eruptions reach the occlusal plane, the oc- length in M. montebelli, most parts of the cranial bone clusal relationship between the upper and lower showed a biphasic allometry, and the critical points of molars is established, so it can be thought that molars relative growth coefficients (α) were located from which not only keep on growing but also have a around 10 days old to 30 days old which represents the difference in growth potential among the molars weaning period or just entering the active period soon would lose their normal relationship in the position of after the weaning period16). The upper and lower adjoining each molar and also in occlusion among molar series length to the condylobasal length in E. upper and lower molars. As the molars have complex andersoni, which are formed between 0 and 200 days, forms and occlusion, they have to suppress variability also showed a biphasic allometry17). However, this to function normally, and having little variability has report did not note the period of the critical points of a high value in natural selection21,22). Such continuous- the α values. All specimens in the three species ly growing molars can be thought to be a disadvan- examined in this study were those whose stages were tage for occlusal function, but the molar forms of the after the weaning period and caught in the field, so the three Arvicolinae species are almost square and have results would show a monophasic allometry. The no interproximal space, their occlusal surfaces are relative weight of masticatory muscles, suprahyoid flat and they are lophodont molars that have many muscles, mandible and each lower molar relative to loops in the buccolingual direction . Therefore, the the body weight in E. smithii, which were in the stage occlusal surfaces of the three molars are effectively a after the weaning period, or the mesiodistal and buc- single functional area which is long and slender , and colingual crown diameters of each lower molar rela- the upper and lower molars can make a stable occlu- tive to the mandibular length also showed monophasic sion anywhere within limits . On such molars whose allometries4,13,18). occlusal relationship is loose , the growth in mesiodis- The eating habits of the three Arvicolinae species tal and buccolingual directions creates no disharmony studied are herbivorous. Masticating vegetable fibers in the occlusal relationship. In this way , the molar such as leaves, stalks and roots, requires a greater forms, growth patterns and occlusal relationship have amount of mandibular movement and more powerful a strong connections with each other. forces between the upper and lower raws of molars Obtaining normal masticatory pressure helps E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 55 molars grow normally. For example, the molars in the molars in M. montebelli and two Eothenomys E. andersoni specimens which have difficulty in feed- species29), forms of the mandibular condyle and fossa ing because of incisors growing too long have signs of in E. smithii30) and masticatory muscles in E. smith- root-closure17), and continuously growing hypsodont ii13), and these do not allow no lateral movements in molars are being simultaneously abraded and Murinae. The relative growth coefficients (α) of rebuilt23). However, for the molars in E. smithii, the relative weight on each part of the masseter and impeded eruption rate is greater than the attrition temporal muscle relative to the body weight in E. rate, so attrition alone can not compensate for the smithii are larger for the parts that have muscle fibers impeded eruption rate. As a consequence, the height of running horizontally (anterior-posterior) than for any the molars increases with advancing age18). part that has fibers running vertically, so it was In the case of human molars, in general, the effects suggested that propalinal (anterior-posterior) man- of environmental factors are apparent on buccolingual dibular movements during mastication progressively crown diameters, while on the mesiodistal crown increased with advancing age13). The anterior- diameters, there is a compensatory interaction among posterior movements of the mandible on the power adjacent molars for the jaw which is restricted stroke for food crushing and grinding31), and the larger mesiodistally and the place for growing24). On buc- movements made, the more effective the crushing and colingual crown diameters, the restriction of place, grinding of food because the enamel protuberances of that is the jaw, is clearly weak. These findings were the occlusal surfaces are grinding against each other also seen in the mouse25), so it could be expected that more. When the mandibular movements are too big, the growth potential of the molars is higher in the however, the number of enamel protuberances grind- buccolingual crown diameters than in the mesiodistal ing against each other decrease again, and the greater crown diameters. However, there was a tendency for part of the movement becomes useless. So, the species the α values of the mesiodistal crown diameters to be with relatively longer upper and lower molar series greater than those of the buccolingual crown diame- make food grinding and crushing more effective by ters, especially in the two Eothenomys species. There- anterior-posterior movements of the mandible. That fore, the upper and lower molars in two Eothenomys is, for food mastication in Arvicolinae species, whose species had forms in which the mesiodistal crown horizontal movements of the mandible are limited to diameters were longer than the buccolingual crown anterior-posterior movements, these horizontal move- diameters, that is, increasingly slender forms ments increase with advancing age, and along with the mesiodistally with advancing age. Although in Mur- increasingly slender shape of the molars with aging, idae, especially in Arvicolinae (E. andersoni, E. the efficiency of the grinding function improves, smithii, M. montebelli) , the correlation among buc- which is indispensable for the digestion of vegetable colingual crown diameters was remarkably stronger fibers. than that among mesiodistal crown diameters9,26,27), it Comparing α values among molars, generally a is thought that one reason for this result is the differ- mesio-distal gradient was seen in the mesiodistal and ence in growth potential between the mesiodistal buccolingual crown diameters, and the α value of the crown diameter and buccolingual crown diameter as third molars was greater than that of the first and described above. second molars. The mesiodistal crown diameters of It was supposed that the mandibular movements in the upper and lower third molars in the three species, the three Arvicolinae species studied were mainly except for that of the lower third molar in M. limited to propalinal (anterior-posterior) movements montebelli, especially showed isometry, although by the study of comparative anatomy of the mas- other measurements of the molars showed a negative ticatory organization such as the forms of the occlusal allometric growth pattern. The absolute molar size surface, occlusion and wear patterns of the upper and sequence of the mesiodistal crown diameters of the lower molars in M. montebelli28), wear striations of molars in Arvicolinae (E. smithii, E. andersoni and 56 Jpn. J. Oral Biol., 43: 43-59, 2001.

M. montebelli) was M1>M3>M2 in both upper and variation of the third molar to be bigger than that of lower molars6), but because there were differences the first and second molarem, and one of the reasons among the growth potentials as described above, the for these differences is the difference in the growth size relation between the second and third molars potential described above. This conforms to the case differed with age. Especially in the mesiodistal crown of the mouse34). Of the molars in Mus musculus, the diameters of the lower second and third molars, whose anterior molars (the first and second molars) can be size differences were small, the second molar was a clearly distinguished from the posterior molar (the little bigger than the third molar in the specimens at third molar) by an analysis of variations and correla- the weaning period or just after the weaning period. tion in molars35). As described above, the characteris- However, the size differences decreased with age, and tics of the growth pattern of the molars can be under- with further aging, the size relationship between the stood as adaptive systems. It is thought that the lower second and third molars in the two Eothenomys difference in growth potentials for each molar differs species reversed, that is, the third molar became according to its development, size, degree of mor- bigger than the second molar; moreover the mesiodis- phological and functional demand and occlusal rela- tal crown diameters of the second and third molars in tionship. M. montebelli were almost the same in aged speci- Although the morphology of the molars was not mens. In the upper molars, the difference between the observed on this study, the morphology of the enamel upper first and third molars became smaller, while the pattern of the distal part of the occlusal surface of the difference between the upper second and third molars upper third molar in Arvicolinae had an age variation increased with growth. such as a simple form, intermediate form and complex It is indicated that the critical period in the mor- form, and most of the young specimens showed a phologic formation of the molars lies in the period complex form, while the simple form became more between the formation of the enamel organ and the prevalent with advancing age17,36-39).The α values of commencement of calcification on the crown, and the the mesiodistal crown diameters of the upper third variability of molar sizes and shapes is due to a large molar in the three Arvicolinae species studied were extent to the degree of karyokinesis nuclear division significantly bigger than those of the buccolingual activity in this critical period32). The period of enamel crown diameters in all species, and the third molar organ formation will differ with the kind of teeth, and showed the highest tendency to become slender. It can the growth patterns may expose strong characteris- be assumed that the curved loop becomes straighter tics with the kind of teeth. For example in Microtus and the morphology shifts to a simple form through an arvalis, in the first and second molars, the formation intermediate form at the time that the molar showing

of predentin, dentin and enamel is observed before a complex form magnifies in a mesiodistal direction , birth, while the formation of the third molar epithelial but not in a buccolingual direction. The difference in bud and enamel organ are not observed, so the devel- growth potential between the mesiodistal crown diam- opment of the third molar is obviously after birth33). eter and buccolingual crown diameter is possibly one This result will be the same in the three Arvicolinae reason for the age variation in the morphology of the species studied. In general, it can be assumed that the upper third molars. The shape of the upper third lateness of development makes molars bigger or smal- molar is used as a standard of classification in ler, and in connection with this, the third molar has a Arvicolinae40) and is also seen in the geographical high growth potential because it is apt to be influenced variation41-43) and chrono-variation44) , but to examine by environmental factors and abounds with plastic- these, the age stage must be the same . We will report ity15). In the three Arvicolinae species, the correlation on this point on another occasion . between the mesiodistal crown diameter of the third The three Arvicolinae species are all herbivorous , molar and that of the other molar is exceedingly but there are fine specific differences between the weak9,27), or there is a tendency for the coefficient of eating habits of the two Eothenomys species and M . E. Sakai, et al.: Relative Growth of Molar in Arvicolinae 57

montebelli. Thus, the ratio of the lengths on the upper than in M. montebelli, with significant differences in and lower molar series and zygomatic width7) relative four molars. On the other hand, the α values of the to the total skull length, the frequency of the appear- buccolingual crown diameters were bigger in M. ance of the complex form on the upper third molar36), montebelli than in the two Eothenomys species, and the relative length of the mandible, relative weight of the relative sizes were bigger in the former than in the the masseter muscle to the cranial bone weight45), the latter. ratio of length between the large and small intestines, In this way, the eating habits conjectured by charac- the length of the caecum and its ratio to the length of teristics of the molar shapes do not always correspond the small intestine46), all of these are bigger in M. with conjectured characteristics of other digestive montebelli than in two Eothenomys species, and it is systems. The significance and cause of this are supposed that specialized herbivority is more remark- obscure at present. It will be exceedingly difficult to able in the former than in the latter two. Also, the clarify the quality and quantity of food on the field in result of the principal component analysis on the M. montebelli by investigation of the growth patterns molar size shows more adaptive specialization to of masticatory muscles, but we want to clarify their herbivority in M. montebelli than in the two Eoth- eating habits and consider these problems further. enomys species47). Moreover, it is also necessary to clarify the growth There were no significant differences in the α pattern of molars in Japanese Arvicolinae to compare values of the upper and lower molars among the two these three species that have no molar roots through- Eothenomys species ; the measurements showing sig- out their life with the Clethrionomys species that form nificant differences were specifically between M. molar roots as they age. montebelli and the two Eothenomys species. The regression line of the mesiodistal crown diame- Acknowledgment ter of the lower first molar in M. montebelli was clearly located higher than that in the two Eothenomys Most of materials of M. montebelli and E. ander- species throughout all growth stages, and the relative soni used in this study were collected by Dr. Takeo length of the mesiodistal crown diameter of the lower Miyao. We wish to express our deep appreciation to first molar relative to the condylobasal length was the Dr. Takeo Miyao. largest in M. montebelli, so the specialization of the herbivority was remarkable. Miyao (1964) also report- References ed on this point based on morphologic difference on the lower first molar; that is, five salient angles are 1) Miyao, T.: Dobutsu seitaigaku nyumon [Introduc- present on the lingual side and four on the buccal side tion to animal ecology].pp. 145-178, Chiiki bunka in the two Eothenomys species, and six on the lingual kenkyujo, Saitama, 1970. side and five on the buccal side in M. montebelli7). 2) Miyao, T., Morozumi, T., Morozumi, M., Hanamu- However, the tendency toward slenderlization of the ra, H., Sato, N., Akahane, H. and Sakai, A.: The molars thought to be effective for mastication in the small mammals on Mt. Yatsugatake in Honshu. II. herbivorous species (that is based on the result that Seasonal differences of sex ratio, body weight and the growth potential of mesiodistal crown diameter is reproduction in Apodemus argenteus and Cleth- rionomys andersoni in the subalpine forest zone on higher than that of buccolingual one) was found on Mt. Yatsugatake. Zool. Mag. 72: 187-193, 1963. all molars in two Eothenomys species except for the 3) Miyao, T., Morozumi, M. and Morozumi, T.: Small lower first molar in E. smithii, otherwise it was found mammals of Mt. Yatsugatake in Honshu. VI. Sea- only in half of the molars in M. montebelli, but the sonal variation in sex ratio, body weight and repro- lower third molar was square. There was also a duction in the vole, Microtus montebelli. Zool. Mag . tendency for the α values of the mesiodistal crown 75: 98-102, 1966. diameters to be bigger in the two Eothenomys species 4) Sakai, E., Uematsu, Y. and Miyao, T.: Relative 58 Jpn. J. Oral Biol., 43: 43-59, 2001.

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