Tooth Development and Replacement in the Japanese Greater Horseshoe Bat, Rhinolophus ferrumequinum nippon(COMMUNICATION)(Developmental Biology)

6 Pages·1992·5.1 MB·English

by  Kimitake Funakoshi

ZOOLOGICAL SCIENCE 9: 445-450 (1992) © 1992 Zoological SocietyofJapan
[COMMUNICATION]
Tooth Development and Replacement in the Japanese Greater
Horseshoe Bat, Rhinolophus ferrumequinum nippon
Kimitake Funakoshi1 Yuko Fukue2 and Shoji Tabata3
,
lBiological Laboratory, Kagoshima Keizai University, Kagoshima 891-01,
2Department of Biology, Faculty of Science, Kagoshima University 890, and
^Department of Oral Anatomy, Kagoshima University Dental
School, Kagoshima 890, Japan
ABSTRACT—The dental formula of the deciduous Triaenops (Hipposideridae), all the deciduous
teeth in Rhinolophus ferrumequinum nippon was il/2 teeth are resorbed or exfoliated prior to birth [12-
cl/1p2/3x2=20. Allthegermsofdeciduousteethwere 14], and in Tadarida (Molossidae) some of them
presentinthefetusesof7-8weeks. Thedeciduousteeth,
wexecelkuss,ivaendofthtehenopd3o,nattotcaliansetdstahpepieramraedxiimnatlhesidzeentaatl9p-u1l0p adirfefaelrseoncreessoarrebendotprcelneaatra,lblyut[1i5t]h.asRebaeseonnssufgogressutcehd
and began to resorb the dentin. The resorption and that the youngin suchgenera are forsome reasons
exfoliation of the teeth have completed at birth. The in less need of the deciduous teeth after birth [3].
typicalsequenceofresorptionofthedeciduousteethwas From an evolutionary or phylogenetic point of
iaip,pie2a,rcel5dcl1a,tep,2,dpev2e,li2o,ppe4d,spl4o.wlOyn, atnhedowtahserrehmaanidn,etdheinpa3 view, suchdeciduousdentition anditsreplacement
small size, while the tooth germ of the P3 was degener- would be of interest to study. However, there
ating. The permanent teeth began to erupt atbirth, and have been few reports which dealt with the
Pth4e, Pus4u,a(lP2s,eMqule3nMce2,oMf\theMir2e),ruMpt3i,oMn3w,a(sI2I,1?P2I,2,p3C).1,TChle3 tsheequdeenctiiadluoruessotrepettihoinn baantdsh[i14s]t.olToghiecaplrecsheanntgesstudoyf
incidenceoflackofthep3was 13.2,5.3and5.3%forthe was therefore carried out to examine histological
left, right andbothsidesofthejaw, respectively. Such a
congenital abnormality suggests that the p3is genetically changes of the deciduous teeth in the Japanese
undergoing a process ofdegeneration. greater horseshoe bat, Rhinolophus ferrum-
equinum nippon.
INTRODUCTION
MATERIALS AND METHODS
Unlike deciduous teeth ofmost mammals, those
A
in the Chiroptera are not functional in feeding. In total of34 (14pregnant females and 20young
mostbatspecies, however, the deciduousteeth are males) were collected at the tuffaceous cave of
highly specialized, strikingly different from the Katano-do in Kagoshima Prefecture during the
permanentones, andusedbythe youngin clinging periodfrom May to August in 1988. Onthe dayof
to the maternal nipple [1-11]. On the other hand, capture, the fetuses were taken out from the
in at least four genera, Rhinolophus (Rhinolophi- mothers under ether anesthesia, weighed, meas-
dae), Lavia (Megadermatidae), Hipposideros and uredofthelengths ofskull andforearm, andsexed
(see Table 1). The age ofeach fetus or young was
determined on the basis ofthe assumptions that in
Accepted December 26, 1991
Received October 11, 1991 R. f nippon, fertilization would have occurred on
2 Present address: Department of Biology, Faculty of ~3 April [16], and the greatest length ofthe skull
mm
Science, Kanazawa University, Kanazawa 920, Japan. would have increased at a rate of0.32 per day
446 K. FUNAKOSHI, Y. FUKUE AND S. TABATA
Table 1. External measurements, body weights and estimated age of fetus in R. f. nippon.
Date captured Fetus Sex Gorfeastkeusltl (lemnmg)th lenFgotrhea(rmmm) weiBgohdty(g) ofEfsettuismaitnewdeeakgse*
29 May 5PE d* 10.1 7.7 0.89 7
29 May 5PY d* 11.1 7.4 1.03 8
29 May 5JJ d* 11.5 8.5 1.18 8
29 May 5PB J 11.5 8.8 1.25 8
29 May 5PC £ 11.6 8.3 1.26 8
11 June 6PD £ 14.3 11.3 2.40 9
11 June 6PZ S 14.5 12.2 2.66 9
11 June 6PU S 15.5 13.7 3.16 10
11 June 6PL d* 15.8 14.6 3.61 10
11 June 6PW d* 16.2 14.5 3.90 10
26 June 6PT ? 18.5 18.0 4.75 11
26 June 6PC * 18.6 20.7 5.52 11
26 June 6PB d* 19.5 24.2 6.72 11
26 June 6PH* d* 21.0 28.5 7.58 12
* Newborn young shortly after birth.
* Estimated from the presumed day (~3 April) of fertilization [16].
on and after the 3rd week [17]. RESULTS
Of 14 fetuses, 8 were fixed in 10% formalin and
their skulls were decalcified in Plank-Rychlo's
fluid, embedded in Sorvall embeddingmedium PN Development and resorption ofdeciduous teeth
45582 (DuPont Comapny, Connecticut). Trans- Thedentalformulaofthe deciduous dentitionin
verse serial sections (3 jum) for light microscopy the Japanese greater horseshoe bat was found as,
were stained with Mayer's hematoxylin and eosin. il/2cl/1 p2/3x2=20. In the fetusesofthe7th or
Six fetuses were fixed in 80% ethanol and their 8th week, all the germs of the deciduous teeth
skulls were stained with alucian blue 8GS and were observed in the upper and lower jaws (Figs
alizarin red S. Cartilaginous tissues are stained 1A, B and2A-E). Inthese deciduoustoothgerms,
deeply blue with the former, while bone and teeth predentin or dentin has been formed with the
are stained deeply red with the latter. The exception of p3. The p3 appeared later in the
deciduous teeth were observed using a binocular developmentandwasstillinthecaporbellstage at
microscope. Adult females or young males rang- the 8th week (Fig. 2E). The dental laminas of
ingfromnewborntovolant sizeswerefixedin 10% permanent teeth were already present in the
formalin and transferred to 70% ethanol; their alveoli lingually to the deciduous teeth. Espe-
teeth were observed in situ using a binocular cially, the P2 developed just below the p2 and was
microscope. The tooth nomenclature used here in the cap stage at the 8th week (Fig. 2D).
was followed by that of Miller [2]. Uppercase At the 9-10th week, the deciduous teeth,
letters signify permanent teeth and lowercase exclusive of the p3, attained their greatest size
letters, deciduous ones; numbers indicate tooth (0.05-0.34mm long), moved upward, and located
positions in the upper or lower jaw (e.g. P2 or P2 in the tissue just over the permanent teeth. The
respectively). The dental formula of permanent deciduous incisors (i2, ii and i2) were simple in
teeth in R. f. nippon has been known as follows shape, that is, ovoid in the longitudinal section of
[18]: 11/2 Cl/1 P2/3 M3/3x2=32. the teeth (Figs 1C, D and 2F). The deciduous
canines (c1 and Ci) were relatively small, with the
Dental Ontogeny in Greater Horseshoe Bat 447
crowns being only slightly larger than those ofthe D and2H-J). The p3 (0.19 mmlong) wasrooted at
deciduous incisors (Figs 1C, D and 2G). The the upper-labial edge of the alveolus, and many
deciduous premolars (p2, p4, p2, p3 and p4) had odontoblasts were observed along the margin of
roughly triangular and recurved crowns (Figs 1C, the dental pulp (Fig. 21). Calcification of the
B
mm
Fig. 1. Diagrams showing the occlusal view of deciduous and permanent teeth in R. f. nippon after staining with
alucianblue8GSandalizarinredS. A-B,C-DandE-F,basedonspecimenNo. 5PY,6PDand6PT,respectively.
A,C, E,lowerjaws;B, D,F,upperjaws. AbbreviationsinFigs 1and2: i,candp,deciduousincisor,canineand
premolar, respectively. I, C, P and M, permanent incisor, canine, premolar and molar, respectively.
448 K. FUNAKOSHI, Y. FUKUE AND S. TABATA
'oc-
K
5* T
ST* L^-v
M
t' 0/ .
Dental Ontogeny in Greater Horseshoe Bat 449
bdeenctaiunseanodf tehneairmedlariknerthsetapi3niwnagswiatlhsoheinmaptrooxgyrleisns tMan2e),ouMsl3y,):Ml3u, (II22,,CP21,, Qp3,).P4, P4, (P2, Ml5 M2, M\
and eosin. On the other hand, the tooth-germ of Congenital abnormalities in the dentition ofthe
the P3 became degenerated. In other deciduous bat were found. Of 38 specimens, five (13.2%)
teeth, calcification did not occur at this stage. lacked the left p3, two (5.3%) lacked the right p3,
Larger and deeply-staining odontoclasts, having and two (5.3%) had no p3 on both sides.
several nuclei, appeared in the dental pulp and
destroyed and resorbed the root dentin when the
DISCUSSION
permanent tooth germ began to develop (Fig.
2F-H, J). Degrees ofthe resorption were variable The present study revealed that complete num-
in different individuals. For example, in fetuses ber of the deciduous teeth in R. f. nippon
6PD and 6PZ (9th week), the left iu i2 and right ij (Rhinolophidae) is expressed by the dental for-
had been resorbed in the former, while ii, i2 on mula of il/2 cl/1 p2/3x2=20. These teeth are
both sides and left Ci had been resorbed in the greatly reduced in size and less complex in form as
latter. All the upper deciduous teeth, however, compared with those ofthe Vespertilionidae [2,5,
were still intact at this stage (Fig. ID). 6, 8, 12, 19, 20] and Phyllostomidae [2, 11].
At the 11th week, only the deciduous lower Furhter, in R. f. nippon, the deciduous teeth,
premolars (p2 or p4) were located at the alveolar exclusive of p3, are resorbed and exfoliated prior
crest on the labial side. Resorptions ofthese teeth to birth.
progressed in considerable part ofthe dentin (Fig. The development of deciduous teeth in R. f.
2K, M). On the other hand, the p3 grew and nippon is similar to that in Hipposideros ruber or
located in the upper, labial and slightly posterior Triaenops persicus (Hipposideridae) [14], though
region of the alveoli in the developing permanent in the latter two species, the resorption process in
plemolar (P4) (Fig. 2L). No deciduous teeth were each deciduous tooth is as yet unknown. In a
observed in the newborn young (6PH) at birth newborn young of H. ruber, two small deciduous
(12th week) and other young males. Namely, all teeth are still retained [14]. Thus, it is assumed
the deciduous teeth, except the p3, were resorbed that the degeneration of deciduous teeth in R. f.
and exfoliated prior to birth. nippon is more marked as compared with that in
H. ruber.
Tooth replacement The formation ofp3 begins later and it develops
The sequence of resorption of the deciduous slowlyin comparisonwith otherdeciduousteethin
teeth was usually as follows: ils i2, c1? c1, p2, p2, i2, R. f. nippon. The p3 is not replaced by the
p4, p4. However, the third deciduous premolar permanent premolar (P3) which is degrading, and
(p3) was not resorbed but remained. Parturition the p3 erupts last. The congenital abnormality,
occurred from late June to early July. At birth, that is, loss ofp3 is found inR.f. nippon. The rate
permanent teeth began to erupt. I1? I2, C1 and Q of loss (23.7%) is similar to that (20.4%) in the
appeared within 1-2 weeks after birth, and P4 and same species examined in Nagano Prefecture [21].
aPn4dfoMll2oweerdu.ptAetd3s-i4muwleteaknesouofslayg,e,aPnd2, MMi3,aMnd2,MM31 Tisheusnedefragcotsinsgeeamrteogrpersosviiodne, afreovimdetnhceeetvhoaltuttihoenapl3
followed. I2, P2 and p3 appeared simultaneously point of view. In Hipposideros the p3 or P3 is
during the weanlingperiod of5 weeksofage. The missing [2]. Hipposideros seems to be genetically
usual sequence oferuption ofthe permanent teeth more advanced and specialized form than Rhino-
was shown as follows (groups ofteeth shown here lophus [22, 23].
in parentheses were considered to erupt simul- Similarly, the small P2 inR. nippon developed
f.
Fig. 2. Cross sections through the lower jaw in R. f. nippon, showing deciduous and developing permanent teeth
afterstainingwithMayer's haematoxylin andeosin. A-E, F-J and K-M, obtainedfrom specimensNo. 5JJ, 6PU
and 6PB, respectively, d, dentin; e, enamel; ob, odontoblast; oc, odontoclast; pg, permanent tooth germ; pi,
permanent dental lamina. Scale bar, 0.1 mm.
450 K. FUNAKOSHI, Y. FUKUE AND S. TABATA
slowlyanderuptedlate, andwasmissingin5outof 10: 113-114.
54 specimens (9.3%) [21], while none of the 2 Miller, G. S. (1907) Bull. U. S. Nat. Mus., 57: 1-
specimens examined here lost the P2 282.
.
The deciduous teeth of the Phyllostomidae are 3 Allen, G. M. (1939) Bats. Harvard Univ. Press,
Cambridge, pp. 1-368.
generally smaller in size and morphologically less
4 Matthews, L. H. (1950) Mammalia, 14: 11-13.
complex than those of the Vespertilionidae and 5 Reeder,W. G. (1953) Mus. Zool. Univ. Mich.,545:
Molossidae [2, 11, 24]. The size and shape of 1-3.
deciduous teeth seem to correlate with the mater- 6 Stegman, L. C. (1956) J. Mamm., 37: 58-63.
nal care pattern in the bat. It has been suggested 7 Friant, M. (1963) Acta Anat., 52: 90-101.
that the increased complexity in the deciduous 8 Fenton, M. B. (1970) Can. J. Zool., 48: 817-820.
dentition of vespertilionids may facilitate for the 9 Orr, R. T. (1970) In"BiologyofBats,I". Ed. byW.
young to grasp the mother rather than to maintain A. Wimsatt, Academic Press, New York, pp. 217-
231.
a hold on the nipple after clinging to the mother
10 Slaughter, B. H. (1970) In "AboutBats". Ed. byB.
[25]. On the other hand, in rhinolophids and H. Slaughterand D. W. Walton, SouthernMethod-
hipposiderids, the young are not left alone but are ist Univ. Prss, Dallas, pp. 51-83.
attachingto the mother atthe roost allthroughthe 11 Phillips, C. J. (1971) Misc. Publ. Mus. Nat. Hist.,
day. Such young behavior and parental care in Univ. Kansas, 54: 1-138.
rhinolophidsandhipposideridsmaynotsostrongly 12 Spillmann, Fr. (1927) Abhandl. Senckenbergischen
Naturforschenden Gesellschaft, Frankfurt A. M.,
require the deciduous teeth for the young to grasp
40: 249-255.
the mother as do those in vespertilionids and 13 Dorst, J. (1953) Mammalia, 17: 83-84.
molossids. 14 Hermanson, J. W., Woods, C. A. and Howell, K.
Eruption ofthe permanent teeth in R. f. nippon M. (1982) J. Mamm., 63: 527-529.
begins after the exfoliation of the deciduous teeth 15 Dorst, J. (1957) Mammalia, 21: 133-135.
excluding the p3 has ended. The eruption, how- 16 Oh, Y. K., Mori, T. and Uchida, T. A. (1985) J.
ever, is not necessarily associatedwith the exfolia- Reprod. Fert., 73: 121-126.
tion oftheir deciduouscounterparts, though this is 17 Fukue, Y. (1989) Unpublished graduation thesis.
true for the lower incisors. The development of Fac. Sci. Kagoshima Univ., pp. 1-39 (inJapanese).
18 Imaizumi, Y. (1970) The Handbook of Japanese
the permanent teeth in R. f. nippon, particularly Land Mammals. Shin-shicho-sha, Tokyo, pp. 1-350
Ii, I2, C1 andCi, israpidaswellasinH. ruber[14], (in Japanese with English description).
and they erupt earlier than those in most bat 19 Dorst, J. (1949) Mammalia, 13: 45-48.
families. Therefore, the erupted permanent teeth 20 Morii, R. (1976) J. Mamm. Soc. Japan, 6: 248-258
may permit, to some extent, for the young to hold (in Japanese with English abstract).
on their mother's nipples or on the false ones 21 Miyao, T. (1973) J. Mamm. Soc. Japan, 5: 230-233
(in Japanese with English abstract).
existingonthelowerpartofthe abdomen, inplace
22 Ando, K. (1982) Unpublished Ph. D. thesis. Fac.
of the deciduous teeth. Agr. Kyushu Univ., pp. 1-359 (in Japanese with
English summary).
ACKNOWLEDGMENTS 23 Yoon,M. H. andUchida,T. A. (1983) J. Fac. Agr.,
Kyushu Univ., 28: 135-146.
We wish to thank Prof. T. Semba of Kagoshima 24 Phillips, C. J., Grimes, G. W. and Forman, G. L.
UniversityDentalSchool, andProf. M. HottaandDr. S. (1977) In"BiologyofBatsoftheNewWorldFamily
Yamane of Kagoshima University for their warm en- Phyllostomatidae. Part II". Ed. by R. J. Baker, J.
couragement and the use of their facilities, and to Drs. K. Jones, Jr. and D. C. Carter, Spec. Publ. Mus.
K. wada and T. Nakama of Kagoshima University Texas Tech Univ., Lubbock, pp. 121-246.
Dental School for their valuable advice and discussions 25 Kleiman, D. G. and Davis, T. M. (1979) In
during the course ofthis study. "Biology of Bats of the New World Family Phyllo-
stomatidae. Part III." Ed. by R. J. Baker, J. K.
Jones,Jr. andD. C. Carter, Spec. Publ. Mus. Texas
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1 Miller, G. S. (1896) Proc. Biol. Soc. Washington,