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ZOOLOGICAL SERIES UNIVERSITY OF ILLINOIS

OF

FIELD MUSEUM OF NATURAL HISTORY

Volume 24 CHICAGO, AUGUST 30, 1941 No. 22

COPULATORY ADJUSTMENT IN SNAKES

BY CLIFFORD H. POPE

CURATOR OF REPTILES AND AMPHIBIANS

The reproductive habits of snakes, though long neglected, are
at last receiving considerable attention from a variety of angles.
Sex recognition, courtship patterns, and viability of the sperm have
been investigated recently with surprising results.

The literature is, however, silent on one aspect of reproduction,
namely, the actual position of the hemipenis in the cloaca during
copulation. Just how is the seminal fluid conducted to the oviducts?
The older literature, Boulenger's "Snakes of Europe" (1913), for
example, states that one hemipenis is pressed against the other so
that the two sulci form a canal through which the semen is conducted
"into the oviduct." Such a statement is obviously erroneous,
since recent observations, as cited in two excellent summaries
of snake courtship (Davis, 1936; Noble, 1937), prove that only one
hemipenis is used at a time. Therefore, the sulcus of one organ
must alone convey the semen.

This separate use of the hemipenes is fully confirmed by a pair
of colubrid snakes (Liophis poecilogyrus Wied, F.M.N.H. Nos.
35697-8 from Bolivia) killed while copulating and preserved without
dislodging the hemipenis. Dissection shows that each branch of the
sulcus ends in a lip surrounded by a ridge which is firmly pressed
against an area of the cloaca, in the center of which an oviduct opens.
Thus each sulcus makes a direct connection with an oviduct, as
shown in the accompanying figure. Moreover, the numerous
hemipenial spines grip the cloacal walls so firmly that no shifting is
possible. The turgid male organ greatly distends the cloaca, as
also noted by Noble (op. cit., p. 677) and others in various species
of snakes during copulation.

Hans Beuchelt's study of penial erection in the aquatic European
colubrid snake, Natrix natrix, led him to conclude that the organ
is inserted in a half-tumescent condition and that full and complete
evagination is accomplished only after the basal spines have become

No. 500 249

250 FIELD MUSEUM OF NATURAL HISTORY — ZOOLOGY, VOL. 24

anchored. Obviously, then, these spines serve a dual purpose:
they keep the hemipenis from being pulled out and they hold the
basal part firmly in place as a support for the distal section, which
in turn can, quite independently of the male's movements, attain
its ultimate position. The independent adjustment and firm grip
must be of considerable advantage, since the male often loses his posi-
tion and is dragged along by the female (Noble, op. cit., p. 678, etc.).

One unfamiliar with snake genitalia might conclude that this
observation on Liophis poedlogyrus virtually closes the problem of
hemipenial adjustment, whereas actually the problem is barely
opened, for the hemipenes in snakes vary greatly in structure.
They may be simple, with either a divided or an undivided sulcus;
or shallowly bifid, as in L. poedlogyrus; or deeply bifid, as in the
king cobra (Hamadryas hannah). The bifid section in this cobra
is seven times as long as the simple one. Many other types are
known and each one must have its own special adjustment.

There is, moreover, close correlation between penial and cloacal
structure. Cope (1900, p. 700) states that the vaginal part of the
cloaca may be deeply bilobate. Apparently, he did not connect
this condition with bifid hemipenes, since he wrote: "It [the hemi-
penis] enters the vagina of the female and its extremity occupies
the corresponding anterior lobe of the latter." In the few species
that I have dissected, the cloaca is bilobed and the hemipenis bifid
to about the same extent. It is reasonable to conclude that each
branch of the male organ fits into a lobe of the cloaca. Liophis
poedlogyrus illustrates an intermediate condition in which the
hemipenis is only slightly bifid and the cloaca shallowly bilobate.
Distortion by the turgid hemipenis has obscured the latter condition
in the female figured.

Cope (loc. cit.) also noted that when the hemipenis is spiny the
cloacal walls are thick, but when the male organ is unarmed the
cloaca is thin- walled. I have been able to confirm this point nicely
in two species of Asiatic pit-vipers, Trimeresurus albolabris Gray
and T. stejnegeri Schmidt, known to be astonishingly alike in color
and all other external characters. They were, in fact, long considered
identical and the females cannot yet be distinguished by external
characters alone. In 1933 my wife and I demonstrated that the
two species could be recognized by their strikingly different hemi-
penes, that of the former being long, slender, devoid of spines and
deeply bifid, whereas that of the latter is shorter, thicker, not as
deeply forked, and spinous. Dissection of a female of the former

r

I xx

1941

COPULATORY ADJUSTMENT IN SNAKES — POPE

251

(F.M.N.H. No. 6711) shows that the cloaca is long, deeply bilobed,
and thin-walled. In contrast to this a specimen of the latter
(F.M.N.H. No. 25201) has a shorter cloaca with shorter lobes and
thick walls. The correlation is obvious enough.

The question at once arises whether such a marked difference in
penial structure is an efficient isolating mechanism making cross-
breeding of these two strikingly similar species physically impossible.

Ridge.

Orifice of
sufcus branch

Small spine
Fork of sulcu:

Basal spines
Sulcu s

Intestine

Orifice of
oviduct

Impression of
ridge

Impressipns of
small spines

Impressions of
basal spines

Orifice of
intestine

FIG. 23. Anal region of a male (left) and of a female of the colubrid snake
Liophis poecilogynis seen from below. The ventral body wall of the female has
been bisected and its halves spread apart to expose the interior of the cloaca, from
which the turgid hemipenis was removed. The exposed side of the latter lay against
the dorsal wall of the cloaca so that each sulcus spermaticus opened at the orifice
of an oviduct. X 3. Drawing by H. Elizabeth Story.

The long spines of T. stejnegeri would probably do considerable
damage to the delicate walls of the T. albolabris cloaca. Moreover,
the differences in form and proportion of the two organs would
present other difficulties. Noble (op. cit.) has summarized the
few authentic cases of cross-mating in snakes, but too few details
are known about them to permit the drawing of conclusions as to
the frequency of their occurrence in nature or its results under any
conditions. Very careful experiments would have to be devised to
investigate this matter, since evidence that sperm remain viable

252 FIELD MUSEUM OF NATURAL HISTORY — ZOOLOGY, VOL. 24

in females for months if not years is rapidly accumulating (see
Rahn, 1940, and Haines, 1940, and their bibliographies).

SUMMARY

During copulation the raised terminal lip of each branch of the
bifid sulcus spermaticus in a colubrid snake, Liophis poecilogyrus,
fits snugly against the orifice of an oviduct. It is reasonable to
conclude that a similar adjustment occurs in other snakes with
divided sulci.

Close correlation between penial and cloacal structure occurs in
two Asiatic pit-vipers and a South American colubrid snake. Such a
correlation is probably of common occurrence among snakes.

It is suggested that penial structure may be an important isolating
mechanism in certain snakes. Therefore, penial adjustment is a
subject worthy of further investigation because of its bearing on the
important problem of speciation.

REFERENCES
BEUCHELT, HANS

1936. Bau, Funktion und Entwicklung der Begattungsorgane der mannlichen
Ringelnatter (Natrix natrix L.) und Kreuzotter (Vipera berus L.). Morph.
Jahrb., 78, pp. 445-516.

BOULENGER, G. A.

1913. The Snakes of Europe. London, Methuen & Co., Ltd. xi+269 pp., 42
figs., 14 pis.

COPE, E. D.

1900. The Crocodilians, Lizards, and Snakes of North America. Kept. U. S.
Nat. Mus., 1898, pp. 153-1270, figs. 1-347, pis. 1-36.

DAVIS, D. D.

1936. Courtship and Mating Behavior in Snakes. Field Mus. Nat. Hist.,
Zool. Ser., 20, pp. 257-290, figs. 28-34.

HAINES, T. P.

1940. Delayed Fertilization in Leptodeira annvlata polysticta. Copeia, 1940,
pp. 116-118, fig. 1.

NOBLE, G. K.

1937. The Sense Organs Involved in the Courtship of Storeria, Thamnophis
and Other Snakes. Bull. Amer. Mus. Nat. Hist., 73, pp. 673-725, figs. 1-8,
pis. 8-10.

POPE, C. H. and S. H.

1933. A Study of the Green Pit-Vipers of Southeastern Asia and Malaysia,
Commonly Identified as Trimeresurus gramineus (Shaw), with Description
of a New Species from Peninsular India. Amer. Mus. Nov., 620, pp. 1-12.

RAHN, HERMANN

1940. Sperm Viability in the Uterus of the Garter Snake, Thamnophis. Copeia,
1940, pp. 109-115, figs. 1-4.

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