Vol. 8, pp. 38-42

Asiatic Heij>etological Research

1999

The Hemipenes of Chinese Species of Deinagkistrodon and Gloydius(Serpentes: Crotaiinae)

Peng Guo1,Fu-ji Zhang, and Yue-ying Chen

Chengdu Institute of Biology: the Chinese Academy of Sciences, Chengdu 610041, ChinaAbstract.- The hemipenes of eight species of two genera, Gloydius and Deinagkistrodon are described in detailand illustrated. The results indicate that ( 1 ) the structures of hemipenes of Gloydius markedly different from thatof Deinagkistrodon, (2) more similarities are present among species of Gloydius. At the end of the paper, thetaxonomic relationships among species revealed by hemipenial structures are discussed.

Key words.- Serpentes, Crotaiinae, Deinagkistrodon, Gloydius, Hemipenes.

'Present address: Sichuan Yibin Teachers College. Yibin, Sichuan 644007. China.

Introduction

ficially.

Since Cope has firstly implied the characters of reptilian

hemipenes

tothe classification

in1893, theirimportant value in the classification and phylogeny
was realized by more and more researchers aroundworld (Pope, 1935; Smith, 1943: Dowling et al., 1960;

Zhang et al., 1984; Zhang, 1986; Branch, 1988; Mao,1989; Gloyd et al., 1990; Malnate, 1990). Althoughsome of hemipenes of Chinese Deinagkistrodon andGloydius were described (Pope, 1935; Smith, 1943;

The drawings were done under the binocular-dissecting microscope.

Results
Gloydius

ussuriensis(Emelianov).

The

dividedhemipenis (Fig.l) extends to eighth subcaudal plateand is forked opposite the third. While the Russia(Kebrovka, Primorskiy Kray) specimens described by

Gloyd et al. (1990) and Malnate (1990) extend to theeleventh subcaudal and are forked for eight subcau-Mao, 1989; Gloyd et al., 1990; Malnate, 1990) previously, the authors didn't illustrate them except Gloy-dals. It is spinous proximally, calyculate distally. The

dius brevicaudus and Deinagkistrodon acutus.

The calyculate area is about equal to that of spinous
one. The calyculate edges are spinous. Over sixty

anatomy on
two genera was done (in press.), we

Prior to this paper, a comparativeskull of these

confirm that there are eight valid species of Deinagkistrodon and Gloydius in China. At the present work,

hemipenes of these eight species
will be described in detail, and the taxonomic rela-

the feathers of thetionships indicated by their structures will also be discussed, they will provide additional and further datatransition

from spines

to calyces isinconspicuous.

spines, they reduce in size distally and away from sul-cus. Base of organ, proximal to the large spinous,

isbeset with very minute spines. Centripetal sulcus distinct,

forking near the crotch which is about the sec-

ond subcaudal, it ends at the tips of the organ. The lips
of sulcus are spinous and calyculate in the respective
areas of ornamentation.

The M. retractor penis magnus ends in the twenty-for the classification and systematic of these species.

third to twenty-fifth subcaudal, it is forked at the level

Material and Methodsof the eleventh subcaudal before its insertion the dororgan. The dorsal lobe is one subcaudal longer
than the ventral lobe (in situ).
sal

The materials used in this study are based up formalin-preserved adult specimens; all of them are deposited

inof Biology, the Chineseof Sciences. The number and locality ofChengdu

AcademyInstituteexamined and figured specimens are listed in Table

1 .

G. brevicaudus (Stejneger). The hemipenes (Fig. 2)of the specimens from Anhui and Zhejiang extend tothe fifth to eighth subcaudal plate and are forked at thelevel

In this paper, the descriptive terminology gener-

followed literature (Dowling et al., 1960; Zhang
et al., 1984: Branch, 1986). In a majority of cases, theallyeverted hemipenes were illustrated. In a fewcases, the partly everted hemipenes were everted artifullyof the third to fourth subcaudal. Base of theorgan nude. The proximally half of the organisspinous and the other half calyculate. The calyculate

Gloyd et al. (1990) also
fromdescribed the hemipenes
Anhui, they were suresmooth. The demarof
werethat the lips
top calyces
ridges bears tiny spines.

1999

Asiatic Herpetological Research

Table 1 Material used in this study.
.

SpeciesVol. 8, p. 39

Asiatic Herpetological ResearchVol. 8, p. 40

1999

ttgl

(CIB785185, Panshi, Jilin)

Figure 2. The right everted hemipenis of G. brevicaudus(CIB 726108, Taiping, Anhui)

Figure 3. The right everted hemipenis of G. intermedius (CIB 8010015, Xingyuan, Xinjiang)(CIB 79I0090, R. Zhuang, Liaoning)covered with tiny spines. Spinouse proximally, calyculate distally. The margins of calyces are

G. strauchii (Bedriaga). The hemipenis (Fig. 6)
examined extends to the seventh to eleventh subcau-Figure 1 The right everted hemipenis of G. ussuriensis
.

organ

Figure 4. The right everted hemipenis of G. saxatilis

istiny spines.

The extent of calyces is about half ofdal andis

forked for four to five subcaudals.

Itisisspinous proximally half, and the distally half is caly-inconspicuous. There are ninety to one hundred spines

culate. The line of changing from spines to calyces isin the spinous area, and six especially larger spines ininconspicuous. The calyces are small adjacent to thesulcus but larger away from it, their lips bearing tinyspines. Line of changing

from spine to calyces

each lobe. The sulcus prominent, forked at the level ofthe third subcaudal, and extends to the tips of theorgan rami. Sulcus lips are spinous or calyculate in
the respective areas of ornamentation. The M. retrac-spines. About sixty spines are present in the spinous
area, they reduced in size distally and near the sulcus.

One or two strongly enlarged spines are adjacent totor penis magnus originates at the level of the twenty-the sulcus at the crotch level. Small spines are present

fourth to twenty-seventh subcaudal and is bifid for thein the base of the organ. The sulcus forks at the level

length of two to three subcaudals before its insertionof the second to fifth subcaudal, and continues to theat the organ tips.

tipsof the lobes. The lips of the sulcus prominent,
they are spinous or calyculate in the respective areasof ornamentation. M. retractor penis magnus origi-

Asiatic Herpetological Research

1999

Vol. 8, p. 41

nates al the level of the twenty-seventh to twenty-Figure 6. The right everted hemipenis of G. strauchii(CIB 755127, Hongyuan, Sichuan)

Figure 5. The right everted hemipenis of G. shedaoensis(CIB 79110006, Shedao, Liaonong)

ninth subcaudal, and is forked for the length of two toFigure 7. The right everted hemipenis ofG qinlingensis

Figure 8. The right everted hemipenis of D. acutus (CIB

(840050, Qinling, Shaanxi)

6416190, Fujian)four subcaudals before its insertion at the organ tips.

qinlingensis (Song). The hemipenis

G.

(Fig.

7)

extends to the eleventh subcaudal plate in length andisforked at the level of thefifthsubcaudal. Minutecalyces in the calyculate one. The length of M. rectractor penis niagnus extending is 14 subcaudals andit isforked for the length of two subcaudals before its

insertion at the organ tips.

spines are present in the base of the organ. It isspinous proximally, calyculate distally, the spinous

Deinagkistrodon acutus (Gunther). The hemipenis

about twice to third times as the calyculate
one. The line of demarcation between two areas is

and is forked opposite the fourth subcaudal, base ofarea

isinconspicuous. The

arecalyculate edges
spinous,
there are approximately thirty to forty spines in thespinous region. The sulcus bifurcates the(Fig. 8) extends to the eleventh to thirteenth subcaudalorgan nude. The proximally half of the organ is spinouse, the distally half calyculate, the demarcation

between these two areas is distinct. The calyces withfourth tosmooth margins reduce in size distally and near theof the organ.

sulcus. The spines are about sixth to seventy, they are

Sulcus is distinct, bearing spines in spinous area andlarger on the lateral surface of each lobe than those

fifthsubcaudal, terminates

at the tips

Vol. 8, p. 42

Asiatic Herpetological Research

1999

near the sulcus. The sulcus forks at the level of theChinese Academy of Sciences, for providing literatureof the eachand reviewing the manuscript. We also thank the fol-lobe. The lips of sulcus prominent, they bearing calyarea. M. retractor penis magnus originates at the level

lowing people for presenting with studying specimens: Prof. M. H. Huang. Zhejiang Medical
University: Prof. M. T Song, Shaanxi Institute ofof the twenty-sixth subcaudal and is bifid for thelength of two to four subcaudals before its insertion atZoology; Prof. Y. H. Zhou, Xinjiang Normal University; Prof. K. C. Huang, Dalian Museum of Natural

the tips of the organ.

History.

Discussion

Literature Cited

The hemipenes are deeply forked in eight Chinese

Branch, W. R. 1986. Hemipenial morphology of Afri-species of pitvipers, the shape of the everted hemipe-

can snakes: a taxonomic review, part I: Scolecophidia

nes are "Y". It is spinous proximal ly and calyculate

and Boidae. Journal of Herpetology 20(3): 285-299.

distally. The centripetal sulcus is consistently bifur-

cated on the basal part of the organ in all of the spe-Dowling, H. G. and J. M. Savage. 1960. A guide to thesnake hemipenis: a survey of basic structure and sys-cies examined, and it extends to the tips of the lobes.

tematic characters. Zoologica 45: 2, 17-28.

fourth subcaudal,

itextends to thetips

ces in the calyculate region and smooth in the spinous

These similarities reveal the taxonomic relationships
between genus Gloydius and Deinagkistrodon. The
deeply forking of the hemipenis and the bifurcation ofthe sulcus in the basal region of the organ are exactly
like those of the other pitvipers (Pope, 1935; Smith,Gloyd, H. K. and R. Conant. 1990. Snakes of Agkistrodon Complex: A Monographic Review. Oxford(Ohio), USA. 614pp.

Malnate, E. V.

1990.

A review and comparison ofhemipenial structure in the genus Agkistrodon (sensu1943).

D. acutus can be characterized by presence of thefowling hemipenial structures: (1) the margins of thecalyces are smooth: (2) transition from spines to caly-lato). pp.

583-588. //;: H. K. Gloyd and R. Conant(eds.), Snakes of Agkistrodon Complex:
graphic Review. Oxford (Ohio), USA.

A Mono-smooth in the spinous area: (4) the base of the organ is

Mao, S. H., FY. Yin, and Y W. Guo. 1984. The hemipenes of common Taiwanese venomous snakes. Her-naked. These conditions further confirmed the validity

petologica 40(4): 406-410.

of the independent generic status of Deinagkistrodon.

Pope, C. H. 1935. The Reptiles of China, Natural History of Central Asia, X. American Museum Natural

ces is abrupt and conspicuous: (3) the sulcus lips are

The seven species of Gloydius exhibit rather conservative and stable hemipenial structures, the inter-History, New York. 604pp.

specific variation is only limited to: ( 1 the length of
the hemipenes and the depth of their forking: (2) theand Burma, including the whole of the Indo-Chinese

extent of the calyculate area on the lobes; (3) thelength of the retractor muscle and the depth of their

Taylor and Francis, London. 583pp.

)

forking; (4) the manner of insertion of the retractor

muscle onto the organ; (5) the number of enlarge
spines. The results above indicated that the differentiation of the hemipenial structures in Gloydius is little.

Smith, M. A. 1943. The fauna of British India, Ceylon
sub-region. Reptilia and Amphibia, vol. III-Serpentes.

Zhang, F J.. S. Q. Hu. and E. M. Zhao. 1984. [Comparative studies and phylogenetic discussions on
hemipenial morphology of the Chinese Colubrinae(Colubridae)]. Acta Herpetologica Sinica, new series
3(3): 23-44. (in Chinese).

Acknowledgments
This project was supported by the Special Fund forClassification& Fauna, the Chinese Academy of Sci-Zhang, F J. 1986. [Comparative studies on hemipenial morphology of the Chinese Opisthoglyph genera(Reptilia:Colubridae)]. Acta Herpetologica Sinica,

ences (950633), and by Chengdu Diao Science Fund,new series 5(4): 166-170. (in Chinese).

the Chinese Academy of Sciences.

Zhao, E. M. andThe authors express their grateful appreciation toProf. E. M. Zhao, Chengdu Institute of Biology, theChina. Oxford (Ohio), USA. 522pp.

K Adler.

1993.

Herpetology of