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MALACOLOGIA,1990,31(2):297-312
COMPARA丁 IVE MORPHOLOGY OF LIViNG Nハ t/Tlと υS(CttPHALOPODA)
FROM ttHE PHILIPPINES,Fl」 IAND PALAU
Kazushige ttanabel,」 yunzo丁sukahara2&shozo Hayasaka3
ABSTRAC丁
Morphological features of rVaυ rllυ s frOm the Philippines,Fり i and Palau are compared from a
taxonomic viewpOint on the basis of live― caught animals ln spite of their widely separated
distributions,animals from the three pOpulations share qu te sln∩ ￨lar overa‖ she‖ morphology,
ontogenetic she‖ variation,and radular and iaW Structures SheH coloration and sculpture,and
the shape of radularteeth,a‖ of which have been used in previous taxonomic studies,are also
markedly variable even in specimens of individual pOpulations, and their ranges of var ation
overiap among the three samples The three samples can be distinguished malnly by adut
features,such as the dimensions ofthe she‖ s and totai number of septa,which are probably
attributed to the difference in their pre― reproductive ages 」udging from these observatlons and
avallable genetic data,itis suggested that the Palau population,previously distinguished as N
beraυ θ
η
sls and the other two populations belong to the same,wide ranging species,N ρ
Om―
ρ
j/1υ S, Or otherwise they are closely related sib ing species, 7V belat7θ nsls and 7V ρ
ο
mpr/1υ s
respectively
Key wOrdsi rVaυ rllυs ρ
ο
mpllrtys,7Vaurllυs belat/θ ηsls,SOuthwest Pacric,mOrphology,taxon―
omy
INttROD∪ CT10N
The superfamily Naullaceae (Ceph―
alopoda,Nautiloidea)first appeared in the ttri‐
assic,and fiourished rnainly during the Meso―
zoic and ヽ4iddle ttertiary tthey suddenly
declined afterthe Miocene,and atthe present
tirne only a few species ofthe genus Naυ ″′υs
survive, in the reiatively deep waters of the
tropical southwestern Pacific
Although ll species and seven variants of
rvatrr′′
υs have hitherto been proposed (See
Saunders,1987,table l),theirtaxonomic va‐
‖
dity has long been obscured because ofthe
seemingly rnorphological conservatism of the
genus,extreme splitting Of phenotypes based
on sma‖ co‖ ections, and the lack of knowl―
edge of the morphological and genetic varia‐
tlon within individual populations. Recently,
Saunders(1987)reviSed these``species''and
variants into five or pOssibly six recognized
species(Araυ rf/yS ρ
ο
npr17L/s Linnaeus, 1758;
rv macrOmpわ aノυ
s Sowerby,1849;ヽ たscrobrc‐
υlarυs ILightfoot, 1786]; rV sゎη
ο
η
phaノυs
Sowerby, 1849; Ar わθ
laυθ
17sた Saunders,
1981:and possibly rV rθ ρ
θFfLIS:redale,1944),
but some malacologists(eg Habe,1980:Ab‐
bott& pance, 1983)regard the latter three
species as geographic variants of′ V ρ
Omρ〃
―
′υ
S
丁he species‐level taxonomy of Araυ ノlJs
should,therefore,be re― exanlined in view of
recent biometric and electrophoretic analyses
of large live‐ caught co‖ ections(Ward et al,
1977;丁anabe et al,1983,1985;Saunders&
Davis,1985;丁anabe&丁sukahara,1987;Ma―
suda & Shinomiya, 1983; Woodruff et al.,
1983, 1987: Swan & Saunders, 1987), for
these works detected marked morphological
and genetic variation even within individual
populations
丁his paper considers the taxonomic rela‐
tionships oftwo closely a‖ ied morphospecies,
Ar bθlat/θnsls and N ρ
ο
mp″υS,On the basis
of the comparative morphologic examination
of large co‖ections from several populations
MAttERIAL AND MEttHODS
Material
The fo‖ owing three samples of rVaυ rr/υ s
populations from vvide:y separated areas
were used in this study:(1)34 specimens(10
l Geologlcal lnsttute, UnlverS ty of Tokyo,Tokyo l13,」 apan
21nSttute of Blology, Facu ty of Sclence,Kagoshima Unlvers ty, KagOsh rna 890,」 apan
31nSttute of Earth Sciё nces,Faculty of Science,Kagoshlma Unlversity,KagOshlma 890,」 apan
297
298
males and 24 females)ofrV ρ
ο
mρ′″lyS Cap‐
tured with baited traps from off Bindoy Vi‖ age
(depth Of 120-310m),丁 anon Stralt,the Phil―
ippines,in September 1981(speCimens Bl一
B32,B41 and B52 among 52 anirnals listed in
Hayasaka et al,1982,table 1 0);(2)A total of
280 specimens(245 maies,34 females and
one unsexed iuvenile)Of Ar ρ
O177p′″υs cap‐
tured alive from off Suva(Kandavu Passage;
depth of 290-450m),∨ li Lebu,FJi,on tWO
occasions (August‐ September 1983 and
1986: see ttanabe, 1985, fig 5, tables l-3,
and ttanabe,1988,fig.3,tables l-4,for their
iocations and biological data), and (3)94
specimens(57 males, 36 females and one
unsexed luvenile)of Ar わθ
laυθr7Sた Captured
live from eastern Mutremdiu Bay(=Mutrem―
diu Point of Saunders,1981a,19ure l);depth
of 190-400m,off Augulpelu ReeF,Palau,in
August‐September 1988 and in 」
anuary
1989 1n addition to the above three ‖ve‐
caught samples,two specimens caughtfrom
off Siqulor iSland, Bohol Strait, the Philip―
pines(provided by the courtesy of native fish‐
errnen;sp nos SQ l-2 in Hayasaka et al,
1982)were uSed for comparison of ontoge―
netic septal growth and mature she‖ size
The specimens i‖ ustrated are kept at the
Universty Museum, Universly of Tokyo
(UMUT), and the remaining ones used for
measurements are deposited at the Geology
and Biology lnstitutes,KagOshima∪ niversity
Of three(Habe,1980)or pOSSibly six(Saun―
ders, 1987)currently recognized Araυ rrlyS
species, IV ρ
οmp〃′
υs has the widest 9eo‐
graphic range,extending from the Philippines
in the northwest to Amerlcan Samoa in the
southeast(Saunders, 1987)丁 he two sam‐
ples from the Philippines(丁anon Strait)and
Fli thuS represent the western and eastern
marginal populations of this species tthe two
specimens from Bohol Stral(Philippines)are
compared wlth the rnorphotype distinguished
as IV.ροmprlJus str′ υθ
nsた by Habe&Okutani
(1988,lgs l-4).IV.bθlaυ θ
r7sls is known only
from Palauan waters,about 800 km from the
range of r吼 ρ
ο
mpr1/υs.
Methods
Fo‖ owing the methods described in ttan‐
abe&Tsukahara(1987),a‖ animals captured
were weighed,sexed,and measured(See
Hayasaka et a:, 1982,table 1 0,and the re‐
vised version in Tanabe et al,1983,table l:
丁
anabe,1988,table 3;丁 anabe&Tsukahara,
1989, table 2) Some Were tagged and re‐
丁ANABE,丁S∪ KAHARA&HAYASAKA
leased nearthe samp‖ ng locations for long‐
ternl growth analysis,and most ofthe remain一
ing animals were dissected, and their fresh
soft tissues and gonads were weighed by
means of a dial scale(acCuracy± 10 mg)for
biometry ln addition, the buccal mass was
removed from the body of selected speci―
mens it was soaked in a 20%KOH solulon
for 20 minutes, and thereafter the mandib!e
and radular ribbon were carefu‖ y removed.
丁he radular and iaw mOrphologies of each
specirnen were observed under the optica!
and scanning electron microscopes
We further anOlyzed the ontogenetic she‖
gr6wth patterns in several specimens se‐
lected from each sampie. For this purpose,
radius vector(Rl,breadth(3),height(1つ and
flank length(o ofa WhOn,and har length Of
umbi!icus(C),diSregarding secondary umbil‐
ical deposls(callus),WhiCh were measured in
each dorso― ventra‖y sectioned she‖ at inter‐
va:s of180° using a prolle prolectOr(NIKON,
V16),attaChed to a dignal micrOmeter(aCCu―
racy± l μ
m)(magnrica10n ×20:see ttan‐
abe & 丁sukahara, 1987, figure l, for mea―
surements)Based on these measurements,
four geometric parameters:ie whorl expan‐
sion rate[(Rn/Rη _1)2;n>1宙],flank poslion
(FD),whOn infla10n(3/→ and invo:ution(C
Rl at different growth stages were calculated
for each specirnen.
SHELL MORPHOLOGY
Gross Morphology and Coloration
丁he shells ofthe Palau,Philippine(TanOn)
and Fり i Araυ r〃υs essentia‖ y resemble one an‐
otherin overa‖ morphology and she‖ colora―
tion.Their whorls are tightly co‖ ed with a nar‐
row umbilicus,rnostly filled with a ca‖ us in the
middle‐late growth stages The she‖ colora‐
tion consists of two elements, i e irregu:ar
reddish brown to brown serrate radiai stripes
extending from the inner flank to venter and
branching across the mid‐f!ank, and a longi‐
tudinal stripe of the same color around the
umbilical area(Fig l)ln mature and almost
mature she‖ s, the former element tends to
disappear toward the aperture,retaining only
its trace on the inner flank tthe mode of dis―
tribution,strength and hue ofthe she‖ color‐
ation is fairly variable even in the specimens
from the same area,butthe Ftti sample con‐
sists mostly of the phenotype with relatively
short and broad radial stripes(Fig l)
COMPARAttiVE MORPHOLOGY OF A/4υ TILυ S
￨￨￨￨￨￨￨￨■￨￨￨￨￨￨￨‐■
￨￨￨￨￨￨￨￨￨￨￨■￨￨￨￨￨￨‐ ￨￨
FIG l Mature shelis of Nat7111t/s belatrθ ηsrs(A-3)and Nat7″ ′υS ρ
Ompllrus(C― G),shoWing the simi anty in
overall morphology and coloralon A― B Male(A:T3‐ 2:UMUT RM 18708-3)and female(B:T9-3;UMUT RM
18708-9)frOm Palau C― D Male(C:B21;∪ MUT RM 18705-3)and fema e(B30:UMUT RM 18705-7)from
TanOn strat,the Phllippines E― F Male(E:SV6-1:UM∪T RM 18707-2)and female(Fi SV5‐3;UMUtt RM
18707-1)frOm Off Suva,Vli Lebu lsland,Fl G Sex― unknown specimen(SQ3;UMUT RM 18706-2)from
Bohol Stran near siquり or lSiand,the Philppines Scale bar represents 5 cm
二
==■￨￨‐
300 丁
ANABE,丁S∪ KAHARA&HAYASAKA
FIG 2 0plcal micrographs ofthe ventral she‖ surface of rvaυ rllus belaυθ,slS(A)and rvaυrrlυ s ρ
ο
mprlrus
(B― D),shoWing ongludinally crenulated sculpture A UMUT RM 18708-2(T2-4;female)frOm Palau B
UMUT RM 18707-7(S∨ 13‐ 8;female)frOm Fりi C UMUT RM 18707-8(SV13-13;male)from FJi D UMUT
RM 18705-8(B31;female)frOm the Ph lippines(TanOn stran)Scale bars indicate 500 μ
m
丁he whorls of every specimen exhibit
dense sinuous growth lines.ln addition,we‖ ―
marked, longitudina‖y crenulated ridges
showing a reticulate pattern are developed in
every specirnen from Palau tthis sculpture
was assigned by Saunders(1981a)as One Of
the diagnoses for dlstinguishing the Palauan
IVわθ
/aυ θ
nsrs from N ρ
ο
177pr/Jυs However,1
also occurs on the ventral side of rnany spec‐
imens of Ar ρ
O177p′″
υs from Fり i and the Phiト
ippines,although it is especia‖ y conspicuous
in the Palau specimens(Fig 2).
Ontogenetlc She‖ VanatiOn
BIometric analysis of selected specimens in
dorso‐ventral section reveals that the three
samples exhibit sinnilar ontogenetic patterns
of she‖ geometric parameters, as repre‐
sented by the gradual decrease of whorl in‐
flalon(3/→ Wth increase of who‖ number,
sudden decline of flank pos1lon(FD)near
the end ofthe first whorl,and abruptincrease
and subsequent decline of distance of the
who‖s to the coiling axis(CR)in the second―
third who‖ s(Fig 3)!n every sample,the
ranges of variation of geometric Parameters
are!arger in the early stage than in the later
stage tthe observed ranges of each param‐
eter at a given whorl stage in FJi and Palau
specimens rnostly overlap each other,except
forthe larger C R ratio in the later stage ofthe
Palau specirnens tthe umbilicus of every
specimen is initia‖ y free from a ca‖us The
ca‖ us begins to appear during the develop‐
ment ofthe second whorl,increasing its thick―
COMPARA丁IVE MORPHOLOGY OF A1lυ TILυS
◆Pa:au(N=7)
O Fili (N=21)
*Phi:ippineS(N二 4)
(鷺f
3
301
F◆ ν
%
Q5 1.5 25 3.5 4.5 5.5 6.5π 2.5 4.5
3.5 5.5 6.5ル
0.5 1.5 2.5 3.5 4.5 5.5 6.5ι 0
TOTAL ROTAT:ON ANGLE
FIG 3 0ntogenelc changes of whon expansion rate[(ヽ Rヽ、
_1)21,frank poslion(馬 イD),WhO‖ inlalon rate
(34り ,and who‖ involuJon rate(C Rl versus total rota‖ on angle of spiralfor specimens of Naυfllys bθ rat7θ n_
sls from Palau and Naurllυ s ρ
ο
mplrrυ s frOm the Philippines(Tanon stral)and Fli VertiCal bars indicate the
range of one standard deviation
ness as the she‖ grows(Fig.4)A complete
seal ofthe umbilicus by the ca‖ us occurs dur‐ ing the formation of the second whorlforthe
F,i and Philippine specimens,while n is de―
302 丁ANABE,TSUKAHARA&HAYASAKA
10mm
FIG 4 Drawings of cross―sectioned specirnens of
Naυrrlυ s belaυ θ77SIS from Palau(A― C)and 7Vaυ rllυs
ρ
Oη
plllus from the Philippines(TanOn strait)(D―F)
and Fり i(G―H)A UMUT RM 18708‐ 7(T9‐ 1,ma―
ture male),B UMUT RM 18708-8(T9-2,mature
male), C UMUT RM 18708‐2(T2-4, mature
female), D UMUT RM 18705-5(B27, mature
male),E UM∪T RM 18705-6(B29,mature male),
F UMUT RM 18705-4(B22,submature female),G
UMUT RM 18707-3(SV12-1,submature female),
H UMUT RM 18707-5(SV13-1,submature male)
b ci body chamber,ci ca‖ us
layed afterthe formation ofthe second whorl
for the Palau specimens tthis obseⅣ ation
correlates we‖ with the description of Saun‐
derS(1987,pp 43-44)
The scatter plot of f3ィ H ratios of a‖ captured
anirnals exhibits wide ranging intra‐ and inter―
populational variation of this parameter at
least for premature and mature specimens
(Fig 5).Atthe same she‖ size(D=150-160
mm)mOSt Fli speCimens have a more com‐
pressed she‖ than the Philippine specirnens
丁he Palau specimens display remarkably
wide variation in gリ イH ratio both in the imrna―
ture and mature stages, and the values of
irnmature and submature specimens partly
Ovenap those of mature specimens from Fll
and the Philippines
丁he ontogenetic pattern of chamberlength
(=diStance between contlguous septa)in the
early to middle stages is fairly anke amOng
specirnens ofthe three samples and the one
Siqu10r specimen(Fig 6)
vana10n Of Mature Shelis
As demonstrated by previous authors
(HaVen,1977;Ward et al,1977;Saunders&
Spinosa, 1978; Ward & Martin, 1980, Ha―
yasaka et al., 1982, 1987; Tanabe et al,
1983i Tanabe&丁 sukahara,1987),speCies of
‖ving Naυ rflυ s show distinct sexual dimor‐
phism in the size and weight of anirnals and
she‖ proportions at maturity Namely,mature
males are genera‖y larger and possess
broader she‖ s than mature females
By examining the gonad development in
‖ve‐ caught anirnals, Tanabe & 丁sukahara
(1987)discuSSed the sexual dimorphism in JV.
ρ
οmpllfys from the Philippines(丁 anon Stralt)
and Fり i The difference in she‖ size at maturity
among the Palau,Fli and Philippine(丁 anon)
populations is rnade clear by summarizing the
gonad and tissue weight data on live‐ caught
anirnals(TSukahara,1985;Tanabe&丁suka‐
hara, 1987)(Fig 7)in eaCh Sample,abrupt
increase of 9onad Weightinitiates atthe same
she‖ size for both sexes.Fu‖ development of
the gonad is we‖ marked in the male speci‐
mensfrom Palau and Fり i,and this causes the
relatively larger she‖ size in males than in fe‐
males at the same gonad index[= gonad
weight/1ssue weight(%)](Fig.7).
Figure 7 also shows the difference in she‖
diameter at maturity among the three sam‐
ples The average diameters of rnale and fe‐
male specimensin the Palau sample(Ca 210
mm and 190 mm respeclvely)are much
!arger than those in the Fli sample(ca 150
mm and140 mm,respectively)丁hose in the
Philippine(Tanon)sample(ca 170 mm and
160 mm:see also Tanabe et al, 1983,table
3)are intermediate between the Fり i and
Palau samples Thus,the above differences
in mature she‖ size among the three samp!es
are much larger than that between sexes
wnhin the same sample
Recognition of maturity is also shown by
such characteristic she‖ features as approxi‐
mation ofthe finaltwo orthree septa,a thick‐
ened last septunl, and blackened and thick‐
ened aperture(e g Stenzel, 1964;Collins&
COMPARATiVE MORPHOLOGY OF ArAυTrと υs303
250
■
PALAU(N=94)
▲
PHiL:PP:NES(N=34)
(N=179)
0.9
、0.8 ま
▲
j・ イ
・
150 200
SHELL D:AMETER(mm)
FIG 5 Scatter plot of she‖ breadth/height ralo(3イ Fう Versus she‖ diameter for specimens of rVaυ llrtys
belatrensls from Palau and 7Vaυ rrlυ s ρ
ο
mplrrtrs frOm the Philippines(Tanon stral)and Fl Measurements of
1 79 anirnals captured in 1 986(Tanabe,1987,table 3)are uSed for the FJi sample
Ward, 1987), because these features com‐
mon:y occurin specimens with a large gonad
index. in accordance with these criteria,the
two specimens from Bohol Stral near Siqu10r
lsland(the Philippines)are regarded as ma‐
ture or submature she‖ s tthey are much
smaller in shell diameter(ca 130 mm;Fig
lG)than the mature specimens from TanOn
Stral Totai number of septa at rnaturlty ap―
pears to be different among the three sam‐
ples(33-39,32-35,and 28-32 septa in the
Palau,Philippine(丁anon)and Fり i samples re―
spectively)(Fig 8)
RADULAR AND」 AVV MORPHOLOGIES
Radula
丁he radula ofrVaυr′′
υsis secreted by colum‐
nar epithelial ce‖ s, named odontoblasts, in
the posterior part of the radular sac, and is
generated anteriorly in a series of rows
(丁anabe&Fukuda,1987)Each row consists
of nine primary teeth(one central rachidian,
and two pairs of laterals and marginals on
each side)and tWO pairs of rnarginal support
plates(丁hiele,1893:Vayssiё re,1896;Griffin,
1900; Naef, 1923; Solem & Richardson,
1975; Lehmann, 1976; Mikanli et al, 1980;
Saunders, 1981a, 1987;Tanabe & Fukuda,
1987) 丁his arrangement is clea‖ y distln―
guished from that in modern coleoids,which
in general havё seven primary teeth and a
pair of marginal plates(Solem&Richardson,
1975)
Morphologicalfeatures of each radular ele‐
ment are essentia‖ y identical among the Phil‐
ippine(丁anon),Fり i and Palau rVatr″υs(Figs
9-10)Namely,the central rachidian tooth is
triangular in shape, being more than two or
three tirnes as high as the two laterals(Fig 9)
丁he two rnarginalteeth are much longerthan
the central and laterals: they are gently
304 TANABE,丁S∪KAHARA&HAYASAKA
20
。
A T2-1(male), Palau
OB T5-3《 female), Palau
▲
C B-5(male), Ta3on st., PhHippines
▲
D B-3(female), TanOn st., Phi‖ ppines
●
E SQ-1(sex unknown), Boh。 l st.,Ph‖ ip
☆
F SV13-2(ma:o), suva,Flii
ノ
ロ
｀
｀
☆
/
10 20 30 40
CHAMBER NUMBER
FIG 6 0ntogenelc change ofchamberlength(=septalinterval)for Selected rnature specimens of JVa″ frlυ s
bθlaυ θ
η
s/s frOm Palau and Natrrrlys ρ
οη
pl17ys from the Ph‖ ippines(TanOn and BOhol Strans)and Fli A
UMUtt RM 18708-1,B UMUT RM 18708-5,C UMUT RM 18705-2,D UMUT RM 18705-1,E UMUT RM
18706-1,F UMUT RM 18707-6
15
0
curved and acutely proleCted anteriorly,vvith
two strong grooves along their longitudinal
axis(Fig lo)ln the anterior portion,the teeth
are subcircular in cross section with a round
tlp, but they become rapidly broaden and
compressed tovvard the base A characteristic
spatula‐ like anterior expansion is present at
the base ofthe rnarginalteeth of every spec‐
imen from Palau and Fui(Fig loA― C&E),
but this feature is nOt so pronlinent in many
specimens from the Philippines(Fi9 10D;
see also Saunders, 1981a, figure 2) The
marginal support plates are rectangular in
outline;the inner one is largerthan the outer
A marked depression is developed in the an‐
terior portion of the outer plate
丁he shape of each radular elementis rnark―
edly variable even in the specimens from the
same area,and the range of variation of the
height/width ratio of the central tooth in the
Palau sample apparently overlaps those in
the Fli and the Philippine samples(Fig ll).
」
aws
丁he law apparatus of Naυ rrlυ s differs from
those of modern coleoids by the presence of
conspicuous anterior calcareous coverings
Number of septa
FIG 8 Variation in the total number of septa at
maturity for Naυrrrys bθ ノ
aυ er7srs from Palau and
Naυflrys ρ
ο
mp1/1ys from the Philippines(Tanon
Stral)and Fui
on the chitinous plates ofthe upper and lower
iaWS and by the shorterinnerlame‖ ae ofthe
loweriaw(Okutani&Mikami,1977;Saunders
et al, 1978; 丁anabe & Fukuda, 1987) :ts
overa‖ morphology, composition and struc‐
turalrelalonship wth the iaw muscles are the
same among the species ofrVaυr〃 υs,and are
we‖ designed for a cutting and shearing func‐
305
190 200 210 220 230
10n (Saunders et al, 1978; 丁
anabe &
Fukuda,1987)
丁he loweriawS Ofthe Fり i and Palau spec‐
irnens are both characterized by a distinct an‐
terior depression in the antero‐dorsal rnargin
of the outer lame‖ a, fo‖owed by a rather
straight shoulder(Fi9 12A― B&E一 F)in con―
trast,the loweriaWS Ofthe Philippine(丁anon)
specimens mostly lack such a depression,
and their outer lame‖a has gently concave
antero‐ dorsal margin and roundly convex
shoulder(Fig 12C― D)
D!SCUSS10N
丁axonomic Re!ationships
丁he present study shows thatthe Philippine
(丁anon Stran), Fり i and Palau rvaυ ″υ
s popu―
lations have strong affinities in overa‖ she‖
morpholo9y and radular and iaW Structures
Furtherrnore, the large co‖ ections from the
populations dispiay similar ontogenetic pat‐
terns for the she‖ shape parameters and
chamber length, and they can be distin‐
COMPARA丁!∨ E MORPHOLOGY OFrV4υT/ι υs
140 150 160 170 180
SHELL DIAMETER(mm)
0
100 130
FiG 7 Scatter plot of 9onad index[90nad weight/1ssue weight(%)]VersuS She l diameterfor specimens of
rvaυ″
υs belaυ θ
η
sys from Palau and Naυ ″′υ
s ρ
Omρrllus from the Philippines(TanOn stral)and Fり i
(N=14)
:ド=綸ale PALAU
:書=Lle PHILIPPiNES
:Ygれle Fi」 ￨
027282930313233343536373839
306 丁ANABE,丁SUKAHARA&HAYASAKA
F:G 9 Scanning electron micrographs of central rachidian and lateral(in part)radular teeth in /Vat7tilus
belat/er7Sた frOm Palau(A― B)and rvaurrlυs ρ
ο′η
ρ
lll1/s from the Philippines(TanOn stral)(C― D)and Fり i(E― F)
A UMUT RM 18708-6(T5-4,mature female),B UMUT RM 18708-8(T9‐ 2,mature male),C UM∪ T RM
18705-7(B30;mature female),D UMUT RM 18705-5(B27:mature male),E UMUT RM 18707-4(SV12-3;
immature female),F UMUT RM 18707-9(SV13-14:immature female)Scale bars indicate 200 μ
m
COMPARA丁lVE MORPHOLOGY OF IVAυ TILυ S307
議
靱∬
鸞
博
鷺鸞
鮒
構
腫
曹
￨』
蒻嶽蒻
mnσ and o帆∝
はσtt bdL鴫 and Mが い
n∝ and:∬ 鰊
tttti「肥
鮒
喘
躍
l需じ
蹴:吼暑
marginal support plates
II樅脚
鷺
1苛:憾淵
IWttζ蔽
et al, 1978; Saunders & Spinosa, 1978,
ing the Palauan population as a separate spe―
α
tte PJauan Naυ″υs was de雨 led by l:アき
pt:農￨ヤ畿λ
llぎ鼎
品
T府∬
』
308 丁ANABE,丁 S∪ KAHARA&HAYASAKA
H/W=20 of she‖s,and the trends of the allometric re―
lationships of several characters of the she‖ s
and soft tissues, not only among the geo‐
graphica‖ y separated populations (Ward et
al, 1977:Hayasaka et al, 1982, 1987;丁 an‐
abe&丁sukahara, 1987;Saunders, 1987:K.
Tanabe's observations on specirnens from
various ioca!ities housed in the∪ S.National
Museum of Natural History),but also among
neighboring populations (Hayasaka et al,
1982; Saunders, 1987; Swan & Saunders,
1987;Habe&Okutani,1988).丁 he minor dif‐
ference in the loweriaw mOrphology between
the Philippine anl Fり i Specimens can proba‐
bly be attributed to conspecific variation.
:n addition to the above results at morpho―
logicallevel,recent examinations ofiarge coト
lections using electropheretic techniques pro‐
vided interesting data relevant to taxonomic
relationships of rVaυ rf/yS populations from a
genelc viewpoint(Masuda & shinomiya,
1983; Woodruff et al., 1983, 1987) 丁hese
works have rnade clear that Araυ rf/υs exhibits
normal or s‖ghtly high levels of genetic vari‐
ation and that the isolated populations are
we‖ differentiated genetica‖y Relying upon
Nei's (1978)genetiC distance coefficients,
Woodruff et al (1987)suggeSted that the
Palau population(rV.bθ /aυθns′s)and possibly
the Fli pOpula10n(N.ρ ο
mpttυs)are C10Sely
related to,but we‖ differentiated at a species
level from the populalons ofノV ρ
OmprlJys in
the waters around New Guinea and Queen‐
sland tthe genetic distance coefficients be―
tween the samples of Ar.bθ laυθnsls from
Palau and Ⅳ.ροmpilius from eight locali‖ es in
the southwestern Pacific excluding the Ph‖ ip―
pines(<o2)are, hOWever, much smaller
than those between paired samples of Ar.
scЮbrcυ larυs,7v macro177pゎ aルS and′吼ρ
ο
″ト
ρ
J/fυ S(>0・5)(see W00druff et al,1987,table
:V&19 2)As Woodruff et al.(1987)docu―
mented,there is no simple basis to translate a
genetic distance into a taxonomic decision,
because the processes of speciation are not
closely coupled to the changes of structural
genes tto Sum up the above― rnentioned mor‐
phological and genetic data,two different in―
terpretations can be considered for the taxo‐
nomic relationship among the three
populations tthe one is thatthe populations in
the Phi:ippine, Fりi and Palauan waters are
summarized into the amphimictica‖ y out―
breeding species,ノ V ρ
Ompilitys,with high lev‐
els of genetic and morphological differentia―
tion,and the other is that Ar.わ θraυ θηsls is a
distinct species reproductively isolated from
■PALAU(♂ )
▲
PHILlPPINES(♂ )
△
(9)
●
Fl」 ￨
12
:lo
.09
Ш08
o7
06
05
04
■
H/W‐ 15
0301 03 04 05 06 07 0B
BASAL WIDTH(mm)
FIG ll Scatter plot of central rachidian tooth
height(H)and basal width(W)fOr specimens of
Naυ″lt/s bθ /aυθ
′
sls from Palau and Araυfrlυ s ρ
οm―
ρ
1/1tys from the Philippines(Tanon stral)and Fli
examination of more than l,00o live caught
anirnals According to Saunders(1981a, b,
1987),Ar bθlaυ θns/s is dislnguished from Ar
ρ
OmρJ/fυ S by ls larger mature size and wider
central rachidian radular tooth, and by the
presence of longitudina‖ y crenulated growth
lines on the she‖ The present work,however,
confirms the presence of crenulated she‖ or‐
namentalon in many specimens of rV ρ
ο
m_
ρ
′〃
υS from Fli and the Ph‖ ippines Further‐
more, the width/height ratios of radular
elements are highly variable even in the spec―
irnens fronl the same area, suggesting that
the shape of radular teeth appears to be of
little significance at!eastforthe species― level
systematics of living rvaυ r′ ′υs The remaining
diagnosis of the Palau population, unusua‖ y
large mature she‖ size, should not be rened
on for distinguishing species for the fo‖ owing
reasons lndeed,the widespread species,Ar
ρ
OttρJ/fυ S displays well― marked morphologi‐
cal differentiation regarding overa‖ weight
and size at rnaturity,proportion and coloration
FIG 12 Drawings of upper(nght s de)and OWer(lefl Side)iaws fOr specimens of Naυ rlltys ρ
ο
mp′″
υS from
Fり i(A―B)and the Philippines(Tanon stral)(C― D),and 7Vatrrllυs belat7θ η
SIS frOm Palau(E― F)(lateral views)
A UMUT RM 18707-9(SV13-14;mature female),B UMUT RM 18707-10(SV28-4‐ 2;mature male),C
UMUT RM 18705-7(B30;mature female),D UMUT RM 18705-2(B5,mature ma e),E UMUT RM 18708-5
(T5-3;mature female),F ∪
M∪T RM 18708-4(T5-1;mature male)SCale bars indlcate l cm
the populations ofrV ρ
Oηp〃′
υs.in this paper,
we refrain from choosing between the two be―
cause of the insufficient data for the genetic
variation of rV ρ
ο
■
p〃′
υs throughout its wide
geographic range, especia‖ y of the popula―
tions in the Ph‖ ippine waters
lnterpretation on Mature She‖ Size Variation
!n his discussion of Naυrrltls systematics,
Saunders(1987)suggeSted that the drfer_
encein mature she‖ size between Ar bθ laυθn_
sls and Ar ρ
Oηp″υs dOes not resu‖ from the
difference in the period of growth,on the basis
of counting of septal number and the stage of
the umbilical ca‖ us appearance Although the
absolute growth and longevity of Araυ fr′υ
s in
their natural habitats are not fu‖ y understood,
previous direct and indirect growth rate mea―
surements by release‐ recapture experiments
of tagged specirnens, radiographic obsen/a―
tion of aquarium specimens,and radiometric
dating of septa have shown thatthe period of
chamber(septal)fOrmalon increases expo‐
nentia‖ y with increasing chamber number
(COChran et al,1981;Saunders,1983,1984;
COMPARATI∨E MORPHOLOGY OF 7V4υTILυ S309
Ward,1985i Cochran&Landman,1984;see
comp‖ ation in Landman&Cochran,1987,fig―
ure 4,table V)丁 he marked difference in the
totalnumber of septa among the mature spec‐
imensfrom Fり i,the Philippines and Palau can
be,therefore,interpreted as refiecting the dif―
ference in the pre― reproductive age among
them tthis interpretation is in accord vvith
Landman & Cochran's(1987)age eStimate
from septal growth equalons(109 y and 5 9
y for N わθ
laυθ
nsys and rV ρ
οη
p′″
υS respec―
tively)The Palau population may attain sexual
matunty at siower rates than the FJi and Phiト
ippine populations,although its rate of septal
formation in earlier stages may not differ
greaJy from those in the Ph‖ ippine and Fli
populations tthe rate of shell growth and the
tirne required to attain sexual maturity rnay be
contro‖ed by both ecology(foOd Supply,tem―
perature, water depth etc)and genetic fac―
tors,and the degrees of dependence ofthese
factors on growth apparently differ among in―
dividual populations Based on the data from
genetic analysis,Woodruff et al(1987)sug‐
gestedthatthePalauandFlipOpulationshave
distinctly diverged from the ancestral form of
310 TANABE,丁SUKAHARA&HAYASAKA
Ar ρ
Ottρノ″
υs by peripheralisolation for about
l million years VVe have no available data on
the fossil record of Naυ ′
〃
υs to verify this hy‐
pothesis,but if it is correct,the adult size in―
crease or decrease in relation to the length of
pre‐ reproductive age in the history of Al ρ
Om‐
ρ
′″
υS StOCk can be expressed by hypermor‐
phosis and progenesis in terms of McNama―
ra'S(1986)definitiOn of heterochrony
Conclusion
The Araυrrノυ
s pOpulations in Palau,the Ph‖ ―
ippines and Fli are eSSentia‖ y similarin over‐
a‖ she‖ morphology,ontogenetic she‖ varia―
lon,and iaw and radular structures tthey are
distinguished mainly by the dirnensions of
adult animals From these morphological ev―
idence and the avallable genetic data, the
Palau and the other two populations are re―
garded as either summarizing into the wide‐
spread species, Aratyrr′ tls ρ
OηpllJus, or be―
longing to the closely related sib‖ ng species,
N わθ
laυθ
17srS and Ar ρ
O177pl17υs respectlvely
丁he size difference among the adult anirnals
from the three populations probably results
from the difference in their pre― reproductive
ages
ACKNOVVLEDGMENttS
llVe acknowiedge Yoshiko Kakinuma for her
facilities and encouragement,both in the field
and laboratory Ourthanks to Angel C AIcala,
Uday Ral,and David K !dip for providing fa―
c‖ ities to operate our field research, other
members ofthe prolectin the Philippines,Fり i
and Palau for their assistance in co‖ ecting
live rvaυ rlltJs and for hetpful discussions,and
Clyde F Roperfor a‖ owing one of us(K丁 )to
observe the co‖ ectlons of AraL/fflυ s atthe∪ S
Natlonal Museum of Natural History in his
care 1/V Bruce Saunders and Neil H Land‐
man read the manuscript critica‖y and gave
useful comments forimprovement of this pa―
per Supported by the Scientific Research
Fund from the」 apanese Ministry of Educa―
lon, Science and Cunure(MOmbυ Sわο
)(No
57043059 for 1982;No 58041055 for 1983;
No 59043050 for 1984; No 62043064 for
1986;No 63041103 for 1987;No 63540622
for 1 988-89;No 01460062 for 1989)
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