Contributions to Zoology, 72 (4) 195-209 (2003)
SPB Academic Publishing bv, The Hague
Variation in number of trunk vertebrae and in of costal in count grooves
salamanders of the family Hynobiidae
S.N. Litvinchuk¹ & L.J. Borkin²
Institute Russian 194064 St. 1 of Cytology, Academy of Sciences, Tikhoretsky pr. 4, Petersburg, Russia, e-
2 mail: [email protected]; Zoological Institute, Russian Academy of Sciences, Universitetskaya nab. 1,
199034 St. Petersburg, Russia, e-mail: [email protected]
Keywords: Hynobiidae, trunk vertebrae, costal grooves
Abstract Introduction
Ten from five of the Hynobiidae were modem tailed species genera family Among amphibians, the family Hyno- studied. The number of trunk vertebrae varied between 14 and biidae (about 40 species), distributed predominantly and the of costal from 10 15. Both 21, count grooves ranged to in temperate Asia, is an early diverged branch, which the within-species variation and the within-population varia- retains characters Duellman tion the values of many primitive (e.g., were recorded in some species. In both kinds
the coefficient of low. Salamandrella & Larson Based variation were quite In Trueb, 1986; & Dimmick, 1993).
the south-eastern differed from keyserlingii, samples markedly on recent studies (Fei & Ye, 2000a; Fu et al., 2001),
remaining ones. the the genus Onychodactylus Among hynobiids, ten of the approximately genera hynobiids could number (both species) and Batrachuperus mustersi have higher be The genus is the richest ofvertebrae in the anterior oftrunk and recognized. Hynobius part (5 4, respectively, one and consists of about 22 which versus 3), and, thus, demonstrated a distinct position. The rela- species, may
tion between the number of trunk vertebrae and the count of be arranged in three subgenera (Matsui et al., 1992;
costal studied. The variation in number of trunk grooves was Borkin, 1999), namely Hynobius (about 14 species),
vertebrae across urodelan families was discussed. Pseudosalamandra and Satohius (7 species) (1 spe-
cies). The family also includes the genera Liua Content (1 species), Onychodactylus (2 species), Pachy-
hynobius (1 species), Protohynobius (1 species), Introduction 195 Pseudohynobius (1 species), Ranodon (2 species), Materials and methods 196 Salamandrella (1 species, which penetrates to east- Results 196 ern Europe), and Batrachuperus sensu lato (about Number of trunk vertebrae 196 9 The taxonomic Patterns of trunk vertebrae composition 199 species). positions of Ranodon,
Count of costal 200 and grooves Liua, Pseudohynobius, Batrachuperus were Discussion 201 discussed in recent papers (Fei & Ye, 2000b; Fu et Number oftrunk vertebrae 201 al., 2001; Kuzmin & Thiesmeier, 2001). Within-population variation 201 Based on mitochondrial DNA (Fu et Sexual dimorphisms 202 study al., it found that the Geographic variation 202 2001), was genus Batrachuperus
Comparison between the hynobiids and other families 204 be into distinct could split two geographic groups, Patterns of trunk vertebrae composition 204 probably, of generic level. The eastern (Chinese) Count of 205 costal grooves to stricto group belongs Batrachuperus sensu and Correlating number of trunk vertebraewith count of
205 consists of six & Ye, 2000b; et costal grooves species (Fei Song
Taxonomic 205 The value al., 2001). western (Middle East) group con-
Concluding remarks 206 of three sists two or species. They may be allo- Acknowledgements 206 cated to Paradactylodon. References 206
Hynobiids were and are a favorite model for the Appendix 209
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lower study on evolutionary morphology and tetra- Materials and methods pod phytogeny (e.g., Schmalhausen, 1964; Voro- byeva, 1994). Special attention was paid to the study A total of 635 adult and subadult specimens be- of the morphogenesis of vertebral column (Schmal- longing to ten hynobiid species were studied. The hausen, 1957, 1958a, 1958b, 1964; Borchwardt, materials studied are kept at the collections of the
1974). However, as yet, the data about the number Department of Herpetology, Zoological Institute, of in of trunk vertebrae hynobiids are quite scarce. In Russian Academy Sciences, St. Petersburg his comprehensive description of osteology of the (n=265), Department of Vertebrate Zoology, St. Pe-
Japanese clawed salamander, Onychodactylus ja- tersburg State University, St. Petersburg (n=171), ponicus, Okajima (1908) mentioned the position and Zoological Museum, Moscow State University, of the sacral vertebra in vertebral column. Later, Moscow (n=199).
Hilton (1948) & Teege (1957) provided the infor- The number of trunk vertebrae (or “dorsal ver- mation about vertebral morphology for four and tebrae” according to Mivart, 1870) was accounted three of the number of of species hynobiid salamanders, respec- by the spinal processes by means
data of muscles. The tively, including O. japonicus. However, even dissection dorsal position of the based on the same (latter) species were conflict- sacrum was identified by feeling of sacral ribs on ing. Antipcnkova (1994) published a short review the left side of the body.
in on number and morphology of vertebrae the Unfortunately, various authors used different tech-
Siberian Salamandrella of costal under salamander, keyserlingii. niques grooves counting. Moreover,
Some other data were also published by Deynegi the same name they understood different cases. So,
(1917), Antipcnkova (1982), Zhang (1985), Nambu Dunn (1923) has applied the name “costal grooves”
& Fei & Ye all lateral situated between the (1991), (2000a). to body grooves
since the late number of fore- and the Nevertheless, 1950s, hindlimb, probably, including grooves, trunk vertebrae has been using in systematics of which touched the posterior margin of the base of urodelans. devoted hindlimbs. the Some papers were to study geo- According to Highton (1957), cos-
in graphic variation various salamanders, mostly tal grooves are such grooves, which are situated plethodontids, proteids and salamandrids (Brodie, between the posterior margin of the head and the
1961; Highton, 1962; Worthington & Wake, 1972; anterior margin of the hindlimb. Misawa (1989)
Sket & Arntzen, 1994; Arntzen & Wallis, 1999; has proposed to recognize under the name “costal
Litvinchuk lateral & Borkin, 2000). grooves” only grooves between the fore- and
As is known, urodelans, at least, at the larval hindlimbs, which didnot touch limb’sposterior and stage, have external body segmentation expressed anteriormargins, respectively. We followed Misawa.
the classic by so-called costal grooves. Since mono- However, we counted the number of costal grooves graph about the family Hynobiidae (Dunn, on the left on the body side only (Misawa counted count of such became taxo- both grooves an important on sides). According to Cope (1889), the nomic character used for identification of species grooves contacting the base of forelimbs should
(e.g., Chang, 1936; Thorn, 1969; Thorn & Raffaelli, be named “axillary”, whereas that contacting the
2001). The question arises whether a correlation base of hind limbs “inguinal”, respectively. between the number of trunk vertebrae and count ofcostal grooves exists. Some authors have analysed the problem based on plethodontids and Results ambystomatids (e.g., Highton, 1957; Jockusch,
1997). However, hynobiids are still markedly less Number of trunk vertebrae studied.
of the is to evaluate the The goal present paper The number of trunk vertebrae in the family Hyno- in of both trunk vertebraeand costal variation amount biidae varied between 14 and 21 (Table 1). The of the grooves among representatives family Hyno- lowest number was recorded in Ranodon sibiricus, biidae. whereas the in highest count was Onychodactylus
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Table I. Variation in number of trunk vertebrae and in ofcostal in count grooves ten hynobiid species
Trunk vertebrae Costal grooves
Species n mean SD min max mean SDSD min max
Batrachuperus mustersi 6 17.3 0.50.5 17 18 11.811.8 0.40.4 IIii 1212
- - Batrachuperus pinchoniipinchonii 2 15.5 - 15 1616 10.5 - 10 II11
HynobiusHynohius leechii 2 16.0 -- 16 16 11.5 - 111! 1212
- - Hynobius nigrescens 2 15.0 - 15 1515 11.0 - 11 1111
Hynobius nebulosus 1 16.0 -- 16 1616 12.0 -- 12 12
Hynobius naevis 3 16.7 0.6 16 1717 12.0 0 12 12
Onychodactylus fischeri 33 20.2 0.6 19 21 14.2 0.6 13 15
Onychodactylus japonicus 5 17.8 0.4 1717 1818 11.8 0.4 II 12
Ranodon sibiricus 77 15.1 0.3 14 16 10.9 0.4 10 12
Salamandrellakeyserlingiikeyserlingii 504 16.9 0.5 1515 19 12.0 0.5 10 14
“n” is number of specimens examined; “SD” is the standard deviation.
ofcostal Table 2. Distribution ofnumber of trunk vertebrae and count grooves in nine hynobiid species
Trunk vertebrae Costal (%)(%) grooves (%)
Species n 14 15 16 17 18 19 20 , 21 10 11 12 13 14 15
- Batrachuperus mustersi 6 67 33 ' 17 83
Batrachuperus pinchonii 2 50 50 50 50
Hynobius leechii 2 100 50 50
Hynobius nigrescens 2 100 100
Hynobius nebulosus 1 100 100100
Hynobius naevis 3 33 67 100100
Onychodactylus fischeriflscheri 33 9 6767 24 9 67 24
Onychodactylus japonicus 5 20 80 20 80
Ranodon sibiricus 77 1 89 10 13 84 3
Salamandrella keyserlingii 504 2 13 78 6 0.2 1 11 75 13 0.2
The modal classes are in bold.
of trunk vertebrae as well. The of fischeri. The modal number was majority species displayed sym-
15 in Ranodon sibiricus (and, probably, Hynobius metrical distributionof numbers of trunk vertebrae,
i.e. less and than nigrescens), 16 in Hynobius leechii (and, probably, more the modal class (Table 2).
Hynobius nebulosus), 17 in Salamandrella keyser- Geographic variation was studied in two species,
lingii, Hynobius naevis and Batrachuperus mustersi, namely Salamandrella keyserlingii and Ranodon
Within and 18 in Onychodactylus japonicus. Onychodac- sibiricus. the formerspecies, the salamanders
the tylus fischeri was characterized by the higher modal from majority of samples had, as a rule, 17 trunk
with the between number, which was equal to 20. vertebrae, averages 16.9 and 17.4
In the majority of species, the differences be- (Table 3). However, populations distributed in the
tween of trunk south-eastern of the had minimum and maximum numbers part species’ range less
vertebrae less How- 16.5 vertebrae in were equal to two or (Table 2). than trunk (16.2-16.4 average).
Such ever, in Salamandrellakeyserlingii, such differences samples were recorded in the Primorsky Terri-
in reached four vertebrae. In three most studied spe- tory, the southernmost part of Khabarovsk Ter-
cies (Salamandrella Ranodon Ussuri River as well in the ( keyserlingii, sibiricus, ritory (the Valley), as,
and Onychodactylus fischeri) the coefficient of varia- southeast of Manchuria (north-eastern China).
tion (CV%) ranged between 2.2 percent and 3.0 Unlike Salamandrella keyserlingii with the vast dis-
percent. Within these species, at the level of indi- tribution from eastern Europe to Kamchatka Pen-
insula Ranodon vidual populations, the variability was quite small (Fig. 1), sibiricus is characterized
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Table 3. variation in number oftrunk vertebrae and in ofcostal in eleven of Geographic (TV) count grooves (CG) samples Salamandrella keyserlingii and two samples of.Ranodon sibiricus.
Mean ± SD TV (%) CG (%)
Samples n TV CG 14 15 16 17 18 19 10 11 12 13 14
Salamandrella keyserlingii
1 Udmurt Republic 7 16.9 ±0.4 12.1 ±0.7 14 86 14 57 29
22 Sverdlovsk Province 175 17.0 ±0.3 12.1 ±0.4 3 92 5 2 86 11
33 TomskTomsk Province 5 17.4 ±0.5 12.4 ±0.5 75 25 63 37
4 Buryatia Republic 19 16.9 ±0.2 12.1 ±0.3 5 95 89 11
5 Mongolia 13 17.0 ±0 12.2 ±0.4 100100 85 15
6 Amur Province 24 17.1 ±0.6 12.2 ±0.6 17 63 1717 4 13 63 21 4
7 Yakutia Republic 73 17.0 ±0.2 12.1 ±0.3 I1 95 44 11 92 77
8 Magadan Province 16 17.3 ±0,5 12.4 ±0.5 69 31 63 37
9 Kamchatka Province 76 17.1 ±0.3 12.3 ±0.5 1 87 12 71 29
10 Khabarovsk Territory 8 16.4 ±±0.70.7 11.5 ±0.5 11 38 51 50 50
11 Primorsky Territory 83 16.2 ±0.6 11.4 ±0.6 13 57 30 6 49 42 2
12 China (north-east) 3 16.3 ±0.6 11.7 ±0,6 67 33 33 67
Ranodon sibiricus
Tekeli and Kopal towns 60 15.1 ±0.4 10.9 ±0.4 2 86 12 10 87 33
Jukentas Pass 17 15.1 ±0.2 10.8 ±0.4 94 6 24 76
The modal classes are bold.
Fig. I. The distribution of Salamandrella keyserlingii (grayish area) and Ranodon sibiricus (square) with localities studied. Black
circles of S. with number of trunk vertebrae more than circles - than 16.5. designate samples keyserlingii average 16.5, open less
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small in Central which three The first by a relatively range Asia, groups. group (with 5 vertebrae)
consists of two semi-isolated parts in the Dzhun- consists oftwo species of the genus Onychodactylus,
includes garsky Alatau Mountains (Brushko et al., 1988; the second group (4 vertebrae) Batrachu-
Kuzmin our The of and the third et al., 1998; data). comparison perus mustersi only, group (3 verte-
samples from these parts did not reveal any sig- brae) contains of Batrachuperus pinchonii, Hynobius
nificant differences in number of trunk vertebrae leechii, H. nigrescens, H. nebulosus, H. naevis,
(Table 3). Ranodonsibiricus. and Salamandrellakeyserlingii.
Sexual dimorphism was studied in the Tekeli The composition of the middle part of trunk de-
Ranodon sample of sibiricus only (20 males and monstrated markedly more variation (Table 4). Num-
Both 11 females). sexes had almost equal number ber of vertebrae in this part ranged between 11 and
of trunk vertebrae. 16, whereas that in the posterior part had no or one
vertebra only. Based on the compositions of the
trunk Patterns of vertebrae composition middle and posterior trunk parts, theoretically,
twelve combinations would be possible. However,
The trunk portion of the vertebral column may be we recorded only eleven patterns. Unlike the ante-
separated in three segments (Fig. 2). The anterior rior part, the variation in number of vertebrae was
part consists of vertebrae, which are situated be- found both between species and within some spe-
tween the atlas and the posterior margin of the cies. In this aspect, Salamandrella keyserlingii
forelimb base. The middle part includes vertebrae, showed the maximum variability, with eight pat-
which are situated between the posterior margin of terns, whereas Ranodonsibiricus had five ones, and
the forelimb base and anteriormargin of the hindlimb Onychodactylus fischeri three ones. Unfortunately,
base. The of the trunk the other two posterior part covers species (with one or patterns) were rep-
vertebrae lying between the anterior margin of the resented by too small samples.
hindlimb base and the sacral vertebra. Five hynobiid species (Table 4) displayed the
In these three parts, the composition of trunk in variation in absence/presence of the vertebra in the
ofnumber ofvertebrae but with terms was variable, posterior part of the trunk. The most specimens of
some limitations.We recognized 17 patterns (Table Ranodon sibiricus (80%, the patterns 3/11/0, 3/12/
4). The anterior part of the trunk was less variable, 0 and 3/13/0) had no vertebrae in this part of trunk,
and failed find of Salamandrella we to any case within-species whereas keyserlingii, probably, to-
Based numberof vertebraein this with small variation. on part, gether Hynobius naevis (too sample),
all species examined could be arranged between had one vertebra. Inboth geographic entities of S.
2. The scheme of distribution oftrunk vertebrae and costal in “A” is the and Fig. grooves Salamandrellakeyserlingii. axillary, “1” is
the inguinal grooves.
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Table 4. The frequency of trunk patterns (percent) expressed by number of vertebrae in anterior/middle/posterior parts of trunk in
hynobiids.
2 Pattern B.m. B.p. H.l. H.ni. H.ne. H.na. H.t. O.f. o.j. R.s. S.k. 1 S.k.
(6) (2) (2) (2) (1) (3) (18) (33) (5) (77) (410) (94)
3/1 I/O 1
3/11/1 50 12 5
3/12/0 100 76 7
3/12/1 50 50 8 2 41
3/13/0 50 100 33 72 3 1 14
3/13/1 67 6 81 30
3/14/0 22 8 2
3/14/1 8
3/15/1 0.2
4/12/1 17
4/13/0 50
4/13/1 33
5/12/0 20
5/13/0 80
5/14/0 9
5/15/0 67
5/16/0 24
B.m. is Batrachuperus mustersi (see Appendix); B.p. is B. pinchonii; H.l. is Hynobius leechii; H.ni. is H. nigrescens; H. ne. is H. is is Ranodon is nebulosus; H. na. is H. naevis; O.f. is Onychodactylus fischeri; O.j. O. japonicus; R. s. sibiricus; S.k. 1 samples 1-9 of
2 Salamandrella keyserlingii; S.k. is samples 10-12 of the same species; and H.t. is Hynobius tenuis (Nambu, 1991). Sample sizes are
given in brackets.
with trunk numbers of costal keyserlingii, specimens one posterior mum grooves were equal to two
Batra- in vertebraewere predominant (76% and 91%). or less in the majority of species. However,
chuperus mustersi (and, probably, Hynobius leechii) Salamandrella keyserlingii, again, such differences
characterized of reached four The variation was by equal amount specimens grooves. within-species
with absence of trunk verte- in numberof costal between or presence posterior (C V%) grooves ranged
bra. Unlike these five species, other hynobiids show- 4.2 percent and 4.6 percent, i.e. this was slightly
in ed no within-species variation in the posterior part higher than number of trunk vertebrae. The dis-
of trunk. could be in tribution of ofcostal around the modal They separated two groups: count grooves
both species of the genus Onychodactylus as well class was symmetrical in all species examined(Table
and H. nebulosus as, probably, Hynobius nigrescens 2).
The of were characterized by lacking of posterior trunk pattern geographic variation in number ( whereas vertebrae, Batrachuperus pinchonii had one of costal grooves in Salamandrella keyserlingii was
vertebra. similar to that in number of trunk vertebrae. In the
majority of samples, the modal class of 12 costal
Count costal was recorded, whereas in the south-east- of grooves grooves
ern corner of the the salamanders species range,
with 11 or 12 costal had almost oc- Among hynobiids, number ofcostal grooves ranged grooves equal
from with the modal class of 12 currence In Ranodon we failed 10 to 15, grooves (Table 3). sibiricus,
find differences between (Tables 1 and 2). The minimum count of costal to any significant two
grooves was found in Salamandrella keyserlingii, geographic samples (Table 3).
Ranodon sibiricus, and Batrachuperus pinchonii, in all hynobiids under the study, the count of the number of whereas Onychodactylus fischeri provided the maxi- costal grooves was always equal to
vertebrae in middle of trunk one mum amount (Table 1). Parallel to trunk vertebrae, the part minus
the differences between the minimum and maxi- (Fig. 2).
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in three Discussion are agreement, except cases (Table 5).
According to Deynegi (1917), Ranodon sibiricus
Number of trunk vertebrae had 17 trunk vertebrae (instead of 14-16 in our
study). A similar case was with Batrachuperus
Hilton considered that this The literature provided quite scarce information in pinchonii. (1948) spe- total about eleven species ofthe hynobiids (Okajima, cies had 17 trunk vertebrae. However, we observed
1908; Deynegi, 1917; Hilton, 1948; Teege, 1957; only 15-16 ones. Such differences might be ex-
Antipenkova, 1982, 1994; Zhang, 1985; Nambu, plained by geographic variation or by impact of
1991; Fei & Ye, 2000a). Our and published data small sample size. Probably, both authors studied
only a few specimens or even one specimen (they
data about size and Table 5. Number of trunk vertebrae (TV) and count of costal provided no sample locality). in various hynobiids. grooves (CG) For Batrachuperus pinchonii, the problem with
species identification may also be not excluded (see Species TV CO References Fu et ah, 2001). Teege (1957) mentioned 15 trunk
Batrachuperus mustersi 17-1817-18 11-12 Present paperpaper vertebrae for Onychodactylus japonicus, whereas Batrachuperus pinchonii 17 nd Hilton (1948) other authors, including ours, calculated 17-18 verte- 15-1615-16 10-11 Present -II--//- paperpaper brae (Table 5). Batrachuperus persicus nd 11-12 Stock (1999)
Batrachuperus gorganensisgorganensis nd 11-121 M2 -II--//- Unlike other authors, we studied the within-spe-
abeiabet nd 11 Misawa HynohiusHynobius (1989) cies variation for three hynobiid species, which were Hynobius dunni nd 11-1211-12 -//--II- 33 represented by relatively good samples with or HynohiusHynobius kimurae nd 1313 -//- more specimens (Table 1). This variation includes Hynobius leechii 16 nd Hilton (1948)
two and -II- 16 11-12 Present categories: within-population geographic paper Hynobius lichenatus nd 10-12 Misawa (1989) (between-population) variations.
16-17 12 Hynobius naevis 16-17 12 Present paper
Hynobius nebulosus nd 12-13 Misawa (1989) Within-population variation -//- 16 12 PresentPresent paper
Hynobius nigrescens nd 10-12 Misawa (1989) In of in- -//- 15 II11 PresentPresent paper our opinion, this term is not a synonym
15 nd Hynobius sp. [peropus][peropus] Teege(1957)Teege (1957) dividual variation although the latter should be Hynobius retardatus 15 nd -//--//- in included. For instance, case of a structured popula- -//--II- nd 11 Misawa (1989) tion, samples from different subpopulations might Hynobius steinegeri nd 13 -//- demonstrate some variation as well. sex- Hynobius tenuis 17-18 12-13 Nambu (1991) Moreover, ual could be Hynobius tokyoensistokyoensis ndnd 11-13 Misawa(1989)Misawa (1989) dimorphisms recognized as a special
tsuensistsuensis nd 13 -II--//- Hynobius case of within-population variation. LiuaLiua shihi 16-16-17 nd Zhang (1985) The first case of the within-species variability Onychodactylus fischeri 20 nd Antipenkova in hynobiids may be ascribed to Okajima (1908), (1982)
19-21 13-15 Present who has mentioned 18 vertebrae in 12 -//--II- paper presacral
nd 19 in Onychodactylus japonicus 17-17-18 nd OkajimaOkajima(1908)(1908) specimens, and ones 3 specimens of Ony- -II--//- 17 nd Hilton (1948) chodactylus japonicus. According to Nambu (1991), -II--//- 15 nd Teege (1957) among 18 specimens ofthe Japanese species Hyno- 17-18 11-12 Present -II- paper bius tenuis, 14 individuals had 17 trunk vertebrae Protohynobius puxiongensis 17 nd Fei, Ye (2000a) 4 Ranodon sibiricussibiricus 17, nd DeynegiDeynegi(1917)(1917) and individuals had 18 ones. Finally, Antipenkova
-//- 15 nd Antipenkova (1994) studied 102 specimens of Salamandrella (1982) keyserlingii. She revealed that 99 individuals had -//--II- 14-14-16 10-12 Present paper 17 trunk vertebrae, and three specimens had asym- Salamandrella keyserlingii 17 nd Hilton (1948) metrical sacra and 16.5 vertebrae. -//- 16,5-1716.5-17 nd Antipenkova Unfortunately,
(1994) these authors did not mention localities. However,
-//- 15-15-19 10-14 Present paperpaper we know that Antipenkova worked with the sample
from the Ekaterinburg [former Sverdlovsk] area, “nd” means no data.
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Middle and this is classic Ural Mountains, a local- Geographic variation
ity for the long-term study of the species by Rus-
sian researchers. The within-population variability Among hynobiids, we found geographic variation
should be not a rare phenomenon because we found only in a case of Salamandrella keyserlingii (Table
it for seven of ten hynobiid species (other species 3). However, the differences between samples from
were represented by one or two specimens only). the south-east and other parts of the species’ dis-
& Borkin Apart from hynobiids, a true within-population tribution are not surprising. Bassarukin
in For variation has been recorded other families. (1984) pointed out some peculiarities of popula-
instance, Highton (1960) & Jockusch (1997) de- tions from Primorsky Territory. For instance, local
varia- scribed such variability (“intrapopulational salamanders have an unusual shape of egg-sacks
tion”), with the largest differences in number of (Korotkov, 1977) and shorter larval development
trunk vertebrae (up to four vertebrae), for some (Korotkov, 1977; Sapozhnikov, 1990; Vorobyeva
samples of the plethodontid salamandersPlethodon et ah, 1999). The Primorsky salamanders also dif-
cinereus and Batrachoseps attenuatus, respectively. fer by thereproduction habitat (Kuzmin, 1990) and
Numerous other cases associated with the size et as well as family genome (Litvinchuk ah, 2001b)
Salamandridae were published by Gerecht (1929) by allozymes (our unpublished data). Therefore,
for European newts, Triturus [“Triton”] cristatus geographic peculiarities in Salamandrella keyser-
Cmo- and T. vulgaris [“taeniatus”] as well as by lingii be explained by distinct taxonomic posi- , may
brnja-lsailovic et al. (1997), Arntzen & Wallis tion of the Primorsky samples.
(1999), and by us (Litvinchuk, 1998; Litvinchuk Geographic variation has also been described for
& Borkin, 2000; Litvinchuk et al., 2001a) for the salamanders from other families. The differences
Triturus cristatus complex. in number of trunk vertebrae have been used for
Based on published data provided by various discrimination of subspecies, for instance, in Pletho-
authors, we calculated values of the coefficient of don cinereus (Highton & Grobman, 1956), in Pro-
well-studied in variation (CVs) for some species from teus anguinus (Sket & Arntzen, 1994), and
six families, namely dicamptodontids, hynobiids, Triturus dobrogicus (Litvinchuk & Borkin, 2000).
and sala- for vari- rhyacotritonids, plethodontids, proteids, Geographic variation estimated by us
mandrids (Table 6). Across species of these fami- ous species of urodelans was low (Table 6), with
lies, the level of within-population variation proved the minimum value in Triturus cristatus (CV=1.0%)
to be quite similar and low, and the CVs ranged and with the maximum value in Triturus vittatus between 0% and 4.3%. The CVs for hynobiids were (CV=5.1%). In five species of hynobiids, the CVs
within these limits (0-4.3%). ranged between 2.2% and 3.0%.
Therefore, the levels of variation in number of
Sexual dimorphisms trunk vertebrae, expressed by CVs, both within and
between populations, were quite similar in species
Such a kind of variation has been found in the from various urodelan families. The low values of
Californian plethodontid salamander Batrachoseps CVs reflect the relatively high stability in this char-
in acter Caudata. the situation attenuatus (Jockusch, 1997) and the European among However, may
be different in various for the same newts of the Triturus cristatus complex (Cmobrnja- genera even
Isailovic et al., 1997). Unfortunately, in the hyno- family. For instance, in plethodontids, the modal biids examined sexual differences are not number of trunk vertebrae is variable in by us, (19-22)
expressed in external characters, except the breeding Batrachoseps whereas, by contrast, the number is
time. Our study was based mostly on the museum fixed (14) for numerous species of Bolitoglossa
the & collections, and we failed to identify reliably (Jockusch, 1997; Parra-Olea Wake, 2001).
sex of the most individuals, without dissections (in As a rule, the differences between the lowest and
of the exception one sample of Ranodon sibiricus). highest numbers of trunk vertebrae within a
vertebrae. species are equal to 1-3 This was found
in various urodelan families, with both lower and
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Table variation for several and of variation in 6. Within-species (WSV; overall, samples) range within-population (WPV) some urodelans, estimated by the coefficient ofvariation (percent). All CV’s were calculated by us on the base of referenced data.
Species N i. N , WSV WPV References ‘ samples specimens
Dicamptodontidae
Dicamptodon aterrimus 4 107 2.9 0-2.3 Nussbaum (1976)
D. copeicopei 7 183 3.2 0-3.0 -II-
D. ensalusensalus 2 24 0 0 -II-
D. tenebrosus 12 307 1.4 0-2.2 -II-
Hynobiidae
Hynobius tenuis ? 18 2.5 - Nambu (1991)
11 33 - 3.0 Present Onychodactylus fischerifischeri paper
Onychodactylus japonicus ? 18 2.2 - Okajima (1908)(1908)
Ranodon sibiricus 22 7777 2.2 1.6-2.3 PresentPresent Ranodon sibiricus paper
Salamandrella keyserlingii 1 102 - 0.5 Antipenkova (1994)
504 0-4,3 -II- 11It 504 3.0 0-4,3 PresentPresent paper
Plcthodontidae
Aneides flavipunctatusflavipunctatus 41 1213 3.3 0-3.2 Lynch (1981)
EnsalinaEnsatina eschscholtzii 7? 431431 1.2 - Frolich (1991)
PlelhodonPlethodon cinereus 8 3399 3.3 2.2-2.622-2.6 Highton (1960)
ProteidacProteidae
Necturus maculosus 1 2727 - 2.72.1 Parker (1896)
-II- 1 30 - 4.0 Waite (1897)
‘ -II- ?? 127 1.41.4 - Smallwood (1908)
ProteusProteus anguinus 4 78 - 1.7-2.41.7-2.4 Sket, Arntzen (1994)
Rhyacotritonidae
Rhyacotriton cascadae 2 55 2.8 1.0-3.0 Good, Wake (1992)(1992)
R. variegatus 33 81 2.9 0-3.10-3.1 -II-
SalamandridaeSalamandridac
NothophlhalmusNothophthalmus viridescens 11 30 - 2.32.3 Moment (1949)
TritumsTriturus cristatuscrislatus 1 162 - 1.6 Gerecht (1929)
9 -II- ? 44 1.0 -- Lanza et al. (1994)
-II--II- 33 54 2.0 1.4-2.2 Cmobmja-IsailovicCmobrnja-Isailovic etet al. (1997)
-II--II- 4 165 1.81.8 0.9-3.0 Litvinchuk (1998)
T. carnifex ? 148 2.1 - Lanza et al.al. (1994)(1994)
-//--II- 2323 421 2.12.1 0-3.2 Cmobmja-IsailovicCmobrnja-Isailovic et al.al. (1997)
T.T. dobrogicusdobrogicus ? 14 3.1 - Lanza et al. (1994)
-II- 6 95 3.6 2.3-4.3 Cmobmja-IsailovicCmobrnja-Isailovic et al. (1997)
-//--II- 3 142 3.6 2.4-3.8 Litvinchuk, Borkin (2000)
T.T. kareliniikarelinii ? 40 2.3 - Lanza etet al. (1994)
-II- 5 110 3.6 2.1-3.5 Cmobmja-IsailovicCmobrnja-Isailovic et al. (1997)
-II--//- 3 73 2.5 2.2-2.72.2-2.1 Litvinchuk (1998)
T. montandoni ? 33 3.6 -- Amtzen,Arntzen, Olgun (2000)
T. vittatus ?? 78 5.15,1 - -II-
T. vulgaris i1 176 - 3,73.7 Gerecht (1929)
higher vertebral count. However, in Proteus an- four vertebrae. However, at the level of individual
guinus some individuals can differ by eight trunk samples, differences between individuals did not
vertebrae (Estes, 1981; Sket & Arntzen, 1997). excess three vertebrae (e.g., 16-19 trunk vertebrae
Among hynobiids, the majority of species also show- in Chernyaevo sample, Amur Province).
ed small within-species differences estimated by The variation in number of trunk vertebrae can
1-2 trunk vertebrae. Nevertheless, as a whole spe- be influenced by various internal and external fac-
cies, Salamandrella keyserlingii demonstratedhigher tors. Parallel to fishes, some authors provided evi-
because such differences reach dences that plasticity can up to the temperature of development affects
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the numberof vertebrae in urodelans as well (Orska Indeed, the former newt has higher numberof trunk
& Imiolek, 1962; Lindsey, 1966; Peabody & Brodie, vertebrae rather than others, namely 15-18 versus
in 13-15 1975; Jockusch, 1997). Curiously, Ambystoma 12-14 or (Crnobrnja-Isailovic et al., 1997;
maculatum, the numberofvertebrae increased with Litvinchuk, 1998; Arntzen & Wallis, 1999; Litvin-
increasing salinity, and there was no effect of photo- chuk & Borkin, 2000; our unpublished data).
period (Peabody & Brodie, 1975). However, Highton Although terrestrial mode of life tends to lead to
& Jockusch that the robust with lower number oftrunk (I960) (1997) suggested geo- more body ver-
variation is resulted from be associated with graphic largely genetic tebrae, fossoriality may elon-
variation. and such be achieved gated body, an elongation may
via an increase in number of trunk vertebrae. Joc-
Comparison between the hynobiids and other kusch (1997) discussed such possibilities for evo-
lution families in some plethodontids.
number Patterns We summarized published and our data on of trunk vertebrae composition
of trunk vertebrae in various families (Table 7).
As mentioned above, in hynobiids (Table 4), the
Table 7. The number oftrunk vertebrae in various families of base of forelimb is fixed by its posterior margin to
urodelans. the third trunk vertebrae, except the genus Onycho-
dactylus (the fifth vertebrae) and Batrachuperus Family Range References mustersi (the fourth vertebrae). Interestingly, such
Sirenidae about 32-42* Lucas, 1886; Hilton, 1948 a 3rd-vertebral position is also characteristic of Cryptobranchidae 18-22 Chang, 1936; Hilton, 1948 ambystomatids and ofthe majority ofplethodontids 14-21 Hynobiidae Present paper (Highton, 1957). However, in larvae of the Triturus Proteidae 16-36 Estes, 1981 cristatus the base is fixed to the second, Plethodontidae 13-23 Jockusch, 1997 complex, third Amphiumidae 60-64 Lucas, 1886; Teege, 1957 rarely (1.6 %), vertebra (Litvinchuk, 1998).
14-17 Good, Wake, 1992 Based Rhyacotritonidae on pictures published by Cope (1889), Rabb Dicamptodontidae 14-15 Nussbaum, 1976 (1965), Meyer-Rochow & Asashima (1988), Sket Ambystomatidae 13-15 Teege, 1957 & Arntzen (1994), Parra-Olea & Wake (2001), and Salamandridae 11-18 Teege, 1957; Litvinchuk, al. Chan et (2001), we concluded that the fixation Borkin, 2000 of the forelimbs in ambystomatids ((Ambystoma
* Hoffmann (1878) erroneously mentioned that Siren lacertina maculatum), cryptobranchids (Cryptobranchus alle- has 63 trunk vertebrae. ghiensis), dicamptodontids (Dicamptodon tenebro-
sus), plethodontids ((Chiropterotriton magnipes,
Among Caudata, vertebral count ranged from 11 Lineatritonlineolus, Pseudoeurycea leprosa, Oedi-
to 64 The and some of the (Salamandridae) (Amphiumidae). ma- pina stenopodia species genus jority of families have the number of trunk verte- Batrachoseps), proteids (Neeturns maculatus and
less than 23. brae, which are The Hynobiidae also Proteus anguinus), salamandrids ((Paramesotriton
to this numbers belong group. Considerably higher hongkongensis, Pachytriton labiatus, Cynops pyr-
of trunk vertebrae are characteristic of proteids rhogaster and Cynops cyanurus) and sirenids (Si-
(Proteus), sirenids, and amphiumids. Remarkably, ren lacertina) is also shifted to the second or third
these water inhabitants are obligatory neotenics with trunk vertebra (perhaps, in Amphiuma tridactylum
the eel-like body and reduced limbs. Interestingly, it is shifted to the first vertebra). Therefore, the
number of trunk vertebrae is associated with mode genus Onychodactylus and Batrachuperus mustersi
of life ofthe have urodelans. in the European newts Triturus cristatus a unique position among Thus,
The Danube has number of vertebrae in the anterior of group. newt, T. dobrogicus more higher part
elongated body, relatively reduced limbs and more trunk should be recognized as an advanced (apo-
aquatic mode of life in comparison with other spe- morphic) character.
cies (for instance, T. marmoratus or T. karelinii). Unlike the anterior part, number of vertebrae in
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the of trunk can be more variable The posterior part Borchwardt, 1974). segmental borders (or myo- within the of varia- between the fore- and a population. However, range septs) lying hindlimbs are tion is not wide because ofshortedness of the pos- externally expressed by costal grooves. Therefore, terior of trunk 2 vertebrae in urodelans in the number of these should be correlated part (0 to grooves
Number general). of vertebrae is equal to 0 or 1 in with the number of trunk vertebrae.
0 in and The variation in hynobiids (Table 4), ambystomatids pletho- number of costal grooves is
and 0 in the dontids (Highton, 1957), 1, rarely or 2, influenced by both account of trunk vertebrae salamandrids (Litvinchuk, 1998). and the position of limb bases. The former factor
was discussed above. The position ofbases of limbs
Count costal varies of grooves markedly in various families, genera, spe-
cies and, sometimes, individuals. Curiously, as far
number of costal as we could the Although grooves was (and is) conclude, taxonomically, position traditionally applied to the taxonomy of the hyno- of forelimbs seems to be more conservative in com- biids, nevertheless, approaches of various authors parison with that of hindlimbs.
count these different. Misawa Based on our with could to grooves were quite experience hynobiids, we
the the (1989) has elaborated a unified method to count of propose following formula to describe re-
which with the lation between of and grooves, did not contact bases of count costal grooves (CG)
vertebrae in limbs. He has also pointed out possible differences number of the middle part of trunk
in the number of costal the left and TV CG= TV L We 6St that tMs grooves on right ( midJ : SU88 middle
sides of the same individuals. Later, similar method formula may be applied to other families ofurodelans
has been accepted by Nambu (1991), Stock (1999) as well, except some rare cases with appearance of
and reliable additional costal by us (this paper). Currently, counts (secondary) grooves.
taken by this method are provided for twenty hyno-
biid species (Table 5). Taxonomic value
Among hynobiids, number of costal grooves va-
ried between 10and 15. The modal number for the Various authors suggested several configurations
12. As the be family is a whole, family seems to of evolutionary relationships between hynobiids.
char- quite homogeneous, except Onychodactylus fischeri, For instance, based on reproductive biology
which has 13-15 costal Thorn grooves (Table 5). acters, (1969) proposed to recognize sepa-
variation revealed Significant geographic was in rate family Ranodontidae, with the genus Ranodon
Os- Salamandrella keyserlingii. So, according to only. Using a set of morphological and biological
& Zhao tashko (1981) Borkin (1994), the samples from data, and based on Chinese species, & Hu
Yakutia, & Sverdlovsk Province differed also the into “natural” Buryatia, (1984) split family two groups:
from the the of the Primorsky sample by amount cos- Hynobius group with predominantly terrestrial
tal grooves. Our data confirmed these results (Table species (Hynobius and Salamandrella) and the Ra-
3). Like Misawa (1989), we also failed to discover nodon group with predominantly water inhabitants
geographic variation in other species. (Ranodon, Onychodactylus, Batrachuperus and
Lina). Later, Zhao & Zhang (1985) separated the
number trunk vertebrae with the Correlating of count genusPachyhynobius to third group. Combining
costal of characters and mitochondrial of grooves morphological DNA
data, Larson & Dimmick (1993) have found the
has out the relations be- closest between the Salaman- Highton (1957) pointed relationships genera
tween external body segmentation and countof trunk drella and Hynobius, thus, confirming traditional
vertebrae in urodelans. Briefly, since early stages acceptance of the similarity of these taxa. How-
of development, the body segmentation (the so- ever, the genus Onychodactylus was more closely
called somites) results both in vertebralcolumn and related to the lineage, whereas Batrachuperus (the
in muscles (Schmalhausen, 1957, 1958a, 1958b, eastern group) proved to be more distant. Recently,
& Ye 1964; Mauger, 1962; Wake & Lawson, 1973; Fei (2000a) have erected a new subfamily
Downloaded from Brill.com10/01/2021 08:55:57AM via free access 206 S.N. Litvinchuk & LJ. Borkin — Variation in Hynobiid salamanders
former the for the newly discovered Protohynobius puxion- at field or museum conditions by means
whereas all other were allocated of of external costal the gensis, hynobiids accounting grooves (if
to another subfamily. number of vertebrae in anterior part of trunk is
Our data in with all present are not agreement known) and, thus, to avoid any dissections, x-ray
the and and these suggestions, which did not recognize genus analysis other damaging relatively com-
Onychodactylus as a separate lineage. The distinct- plicated techniques.
of the ness genus was supported by karyologicall
and genome size data (Morescalchi et al., 1979;
Olmo, 1983; Kohno et al., 1991; lizuka, Yazawa, Acknowledgements
1994; Vinogradov, 1998; Kuro-o et al., 2000; our
unpublished data). We thank to V.G. Borchwardt (St. Petersburg), A.E. Dunaev &
V.F. Orlova (Moscow) who kindly offered the museum The genusHynobius may be split into three groups collections, T.N. Platonova (St. Petersburg) for correcting the of the subgeneric level (Matsui et al., 1992; Borkin, and two English, anonymous reviewers for their valuable com- failed 1999). However, we to find the differences ments on the manuscript. The St. Petersburg Association of between the of representatives subgenera Hynobius Scientists and Scholars provided the facilities for preparation
H. H. and Pseudo- ofthe The research funded (H. nebulosus, leechi, nigrescens) manuscript. was by the INTAS (grant
the Russian Foundation for Basic Research salamandra(H. naevis) in terms ofnumbers of trunk no97-11909), (grants
02-04-49631 and and the Federal State Pro- vertebrae and costal no 02-04-63157), grooves. No. gram “Integration” (the grant E-0121). However, we have found obvious differences in
anterior trunk vertebrae number between Batra-
chuperus pinchonii from the eastern (Chinese) group References and B. mustersi from the western (Middle East)
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4. Kyakhta Town, Buryatia Republic, Russia; 5. Ulan Bator
Accepted: 29 October 2002 City, Dzun Buren and Shamar villages, Mongolia; 6. Yakutsk
Town, Russia; 7. Ust Srednekan Town, Magadan Province,
Russia; 8. Kamaki Village, Kamchatka Province, Russia; 9.
Chemyaevo Village, Amur Province, Russia; 10. Vyazemsky
and Lesopilnoe villages, Khabarovsk Territory, Russia; 11.
Shmakovka, Chernikovka and Troitskoe villages, Dalner-
echensk, Kamen-Rybolov and Vladivostok towns, Ussuriysk
and Kedrovaya Pad reserves, Primorsky Territory, Russia;
12. Dachuan Village, China.
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