Abstract.--Reproductive tissue was examined from 109 sexually
mature Hypsiglena torquata museum specimens from Arizona. Males follow a
seasonal testicular cycle with sperm produced April to September. The
prolonged period of sperm production suggests a similarity to testicular
cycles of some tropical snakes. Sperm was present in the vasa deferentia
from April to September indicating H. torquata has the potential for
breeding throughout this period. Male H. torquata reach sexual maturity
at a smaller size than females. Females with enlarged follicles
([greater than] 12 mm length) or oviductal eggs were found April to
August. There was no evidence that more than one clutch of eggs is
produced during the same breeding season. Mean clutch size for nine
females was 3.2 [+ or -] 1.5 SD, range = 2-6.
The night snake, Hypsiglena torquata ranges from northern
California, central Washington, northern Utah, southwest Kansas, south
to the tip of Baja California and through mainland Mexico from sea level
to around 2650 m (Stebbins 1985). It is a nocturnal and crepuscular
prowler that frequents a variety of habitats including grassland,
chaparral, sagebrush, deserts, woodland, mountain meadows, thornscrub
and thorn forest (Stebbins 1985). There are many anecdotal reports of
reproduction in this species (Hibbard 1937; Tanner 1944; Dundee 1950;
Werler 1951; Stebbins 1954; Gates 1957; Clark & Lieb 1973; Vitt
1975; Tanner & Ottley 1981; Tennant 1984; Lowe et al. 1986;
Degenhardt et al. 1996; Hammerson 1999). Diller & Wallace (1986)
published an account of reproduction in H. torquata from southwestern
Idaho. Fitch (1970) reported H. torquata has an extended breeding
season. The purpose of this paper is to provide information on the
ovarian and testicular cycles of H. torquata from Arizona from a
histological examina tion of preserved gonads from museum specimens. A
comparison is made with reproductive data on H. torquata from Idaho
(Diller & Wallace 1986). Studying the reproductive cycle in
different parts of a snake's range allows one to see the extent of
geographic variation in reproduction within a species.
MATERIALS AND METHODS
A sample of 109 sexually mature specimens of H. torquata (42
females, mean snout-vent length, SVL = 360 mm [+ or -] 45.4 SD, range =
310-503 mm; 67 males, SVL = 300 mm [+ or -] 27.2 SD, range = 237-368 mm)
from Arizona was examined from the herpetology collections of Arizona
State University, Tempe (ASU), The Natural History Museum of Los Angeles
County, Los Angeles (LACM) and The University of Arizona, Tucson (UAZ).
Snakes were collected 1947-1998. Most of the snakes 66/109 (61%) came
from Pima County. Counts were made of enlarged ovarian follicles
([greater than] 12 mm length) or oviductal eggs. The left testis, vas
deferens and a portion of the kidney were removed from males; the left
ovary was removed from females for histological examination. Tissues
were embedded in paraffin and sectioned at 5 [micro]m. Slides with
tissue sections were stained with Harris' hematoxylin followed by
eosin counterstain. Testis slides were examined to determine the stage
of the testicular cycle; ovary slides were examined f or the presence of
yolk deposition (secondary yolk deposition sensu Aldridge 1979). Because
some of the specimens were road kills, not all tissues were available
for histological examination due to damage or autolysis. Number of
specimens examined by reproductive tissue were: testis = 67, vas
deferens = 45, kidney = 55, ovary = 42.
Material examined.-- The following adult specimens of Hypsiglena
torquata from Arizona were examined: COCUISE COUNTY, (ASU 30138, 30183,
30252, 31380, UAZ 24967, 24981, 37878, 39745, 44326); GILA COUNTY, (ASU
675, UAZ 32527, 39736); GRAHAM COUNTY,(ASU 7007); GREENLEE COUNTY, (UAZ
42682); LAPAZ COUNTY,(LACM 138304, UAZ 5000); MARICOPA COUNTY, (ASU 252,
894, 895, 1228, 1595, 1597, 1599, 2256, 2263, 2280, 2292, 2316, 2676,
3655, 10244, 27451, LACM 125260, 125261, UAZ 24997, 44604, 46497);
MOHAVE COUNTY, (LACM 145172, UAZ 33965, 44864); PIMA COUNTY, (ASU 24025,
24026, 28055, 28413, LACM 2367, 27752, 34920-34923, 63455, 64311, 76373,
101827- 101829, 101832, 101833, 107338, 115799, 115801, 115802, 123769,
UAZ 24956-24958, 24961, 24964, 24975, 24985, 24989, 24991, 24998, 24999,
25003, 25021, 25027, 28063, 28501, 28600, 30621, 32526, 34517, 40386,
41205, 41210, 41220, 41227, 42473, 42474, 42595,44245, 44309, 47167,
50317, 50799-50801, 51095, 51096, 51628); PINAL COUNTY, (ASU 13907, UAZ
24292, 25022); SANTA CRUZ COUNTY,(UAZ 48598); YAVAPAI COUNTY (UAZ
50802); YIJMA COUNTY, (LACM 9131, UAZ 35708, 39742).
RESULTS AND DISCUSSION
Testicular histology was similar to that reported by Goldberg &
Parker (1975) for two colubrid snakes, Masticophis taeniatus and
Pituophis catenifer (= P. melanoleucus). In the regressed testes,
seminiferous tubules contained spermatogonia and Sertoli cells. In
recrudescence, there was renewal of spermatogenic cells characterized by
spermatogonial divisions; primary and secondary spermatocytes were
typically present. A few spermatids were occasionally seen. In
spermiogenesis, metamorphosing spermatids and mature sperm were present.
Males undergoing spermiogenesis were found April-September; one male
with a regressed testis was from March. Testes in recrudescence were
found in February (one), April (two) and May (two) (Table 1). The
smallest spermiogenic male measured 237 mm SVL, other males close to
this size that were undergoing spermiogenesis measured 246, 253, 262,
270, 272, 273, 274, 275, 279 mm. Two males smaller than 237 mm SVL were
examined. One male measured 231 mm SVL (UAZ 48182, Mojave County, 8 Ap
ril) and had no sperm in the vas deferens; testes were not available.
Another measured 230 mm SVL (UAZ 36794, Pinal County, 25 June) and had
very small testes that were not sectioned. These were not included in
the study to avoid including immature males in analysis of the
testicular cycle. There is likely some variation between different
geographic locations in the minimum sizes at which males begin
reproductive activity. Vasa deferentia of 45/45 (100%) of the following
H. torquata males contained sperm: April (3); May (9); June (14); July
(7); August (8); September (4). The kidney sexual segments were enlarged
and contained secretory granules in 53/55 (96%) of the following H.
torquata males: February 1/1 (100%); April 6/6 (100%); May 11/12 (92%);
June 12/12 (100%); July 6/6 (100%); August 14/15 (93%); September 3/3
(100%). Enlarged kidney sexual segments typically coincide with breeding
(Saint Girons 1982).
Because sample sizes from February-March consisted of only two
males (Table 1) it is not possible to characterize the H. torquata
testicular cycle early in the year. However, since the only male with a
regressed testis was from March and males with testes in recrudescence
were from February, April and May, it is possible that regression occurs
in winter and recrudescence occurs in early spring in the H. torquata
testicular cycle. Examination of additional H. torquata males will be
needed to verify this. Nevertheless, the continuous period of
spermiogenesis (sperm production) lasting six months (April-September)
and encompassing spring, summer and autumn is indeed striking. The
prolonged, continuous testicular cycle of H. torquata appears to fit the
testicular portion of the "polyestrous with seasonal
reproduction" B pattern of Saint Girons (1982) which is found in
snakes from tropical regions (Saint Girons 1982). Since Hypsiglena is
thought to have arisen within a neotropical clade of snakes (see
Rodriguez-R obles et al. 1999), it is not surprising to see aspects of
its reproductive cycle consistent with that of a 'tropical"
In the only other examination of the H. torquata testicular cycle,
Diller & Wallace (1986) reported sperm in the vasa deferentia of
Idaho males from April to September (similar to Arizona). However, since
a histological analysis of the testes was not done, the duration of H.
torquata spermiogenesis in Idaho is not known. Diller & Wallace
(1986) reported that enlarged testes in summer suggested spermiogenesis
occurred in mid-summer which would mean H. torquata has an aestival
testicular cycle in Idaho (sensu Saint Girons 1982). Sexual segments of
the kidneys were largest in males collected in spring and decreased
during summer (Diller & Wallace 1986). The extent of geographic
variation in the testicular cycle of H. torquata remains to be
Body sizes of females were significantly larger than males, t =
8.7, 107 df, P [less than] 0.0001. This was also found to be the case
for H. tcrquata in Idaho (Diller & Wallace 1986). Females with
enlarged follicles or oviductal eggs were found April-August in Arizona
(Table 2). The smallest reproductively active H. torquata female
(enlarged follicles [greater than] 12 mm length) measured 310 mm SVL.
Two females examined from the period of reproductive activity
(March-August, Table 2) were smaller than 310 mm SVL and showed no
evidence of yolk deposition. These were not included in the study to
avoid including immature females in analysis of the female reproductive
cycle (ASU 28412, SVL = 256 mm, Pima County, 9 June; LACM 64312, SVL =
235, Pima County, 4 August). As was the case for males, the minimum size
at which females begin reproductive activity likely varies between
different locations. Their was no suggestion that H. torquata produces
more than one clutch of eggs in a reproductive season (oviductal eg gs
and secondary yolk deposition in progress) although Vitt (1975)
suggested this might be possible in Arizona if conditions were
favorable. Since the smallest reproductively active male H. torquata
measured 237 mm SVL, it is possible males reach sexual maturity at an
earlier age than females. Similarly, in Idaho, H. torquata males reach
sexual maturity at a smaller size (29 cm SVL), than females which
approximated 40 cm SVL at sexual maturity (Diller & Wallace 1986).
Mean clutch size for nine H. torquata females from Arizona was 3.2
[+ or -] 1.5 SD, range = 2-6 (Table 3). This is within the range of 2-9
reported by Stebbins (1985) and Lowe et al. (1986). There are a variety
of individual clutch sizes for H. torquata in the literature from
different parts of its extensive geographic range. These include: four
from Kansas (Hibbard 1937); nine from Utah (Tanner 1944); six from
Oklahoma (Dundee 1950); four from Texas (Werler 1951); four from Kansas,
six from Oklahoma and four from Texas (Stebbins 1954); four from Arizona
(Gates 1957); three from Arizona (Clark & Lieb 1973); three from
Arizona (Vitt 1975); nine from Sonora, Mexico (Tanner & Ottley
1981); three, four, seven from Idaho (Diller & Wallace 1986).
Clark & Lieb (1973) used the single values of Hibbard (1937),
Dundee (1950), Werler (1950) and Gates (1957), added seven of their own
values and reported a mean clutch value of 3.6 [+ or -] 0.3 SE, range
2-6 for eleven H. torquata clutches from various localities.
The amount of geographic variation in clutch sizes over the range
of H. torquata remains to be determined. Regression analysis revealed
the correlation between log body size (snout-vent length) and log clutch
size for the nine females in Table 3 was not significant (r = 0.49, P =
0.10). This may reflect the snakes being collected in different years
(with varying food supplies) and at different times in the reproductive
season [in lizards, larger clutches are produced earlier in the season
(Goldberg 1975)]. There are reports of H. torquata mating in May in
Texas and Colorado (Tennant 1984; Hammerson 1999). Whether the sperm
used in these matings was produced in the spring or the fall and stored
over winter in the vasa deferentia is not known. The production of sperm
and the presence of sperm in the vas deferens during autumn indicate
that H. torquata has the potential of autumn mating. However, there are
no known reports of this occurring. Werler & Dixon (2000) discussed
the possibility of H. torquata mating i n either fall or very early
spring which might be needed because of the early deposition of eggs in
Thirty-six percent (10/28) H. torquata females were reproductively
active (yolk deposition or oviductal eggs) during the reproductive
period (April-August) (Table 2). It is unlikely the one August female
with early yolk deposition (secondary yolk deposition sensu Aldridge
1979) would have produced an egg clutch during the current reproductive
season. It is possible that yolk deposition may have been completed the
following spring or the follicles may have undergone atresia. In view of
the presence of a female from 2 April with oviductal eggs (Table 3), it
is conceivable that yolk deposition may need to commence the previous
summer for it to be completed in early April. Examination of additional
females will be needed to determine if this occurs in H. torquata.
While some information on snake reproduction can be obtained by
examination of museum specimens, field studies will be needed to
elucidate other aspects of H. torquata reproductive biology.
I thank Michael E. Douglas (Arizona State University), David A.
Kizirian (Natural History Museum of Los Angeles County), and Charles H.
Lowe (University of Arizona) for permission to examine H. torquata.
Aldridge, R. D. 1979. Female reproductive cycles of the snakes
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Clark, D. R. Jr. & C. S. Lieb. 1973. Notes on reproduction in
the night snake (Hypsiglena torquata). Southwest. Nat., l8(2):248-252.
Degenhardt, W. G., C. W. Painter & A. H. Price. 1996.
Amphibians and reptiles of New Mexico. University of New Mexico Press,
Albuquerque, xix + 431 pp.
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history and ecology of the desert night snake, Hypsiglena torquata
deserticola: Colubridae, in southwestern Idaho. Southwest. Nat.,
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Table 1. Monthly distribution of conditions in seasonal
testicular cycle of Hypsiglena torquata. Values shown are
the numbers of males exhibiting each of the three conditions.
Month n Regressed Recrudescence Spermiogenesis
February 1 0 1 0
March 1 1 0 0
April 7 0 2 5
May 16 0 2 14
June 15 0 0 15
July 7 0 0 7
August 15 0 0 15
September 5 0 0 5
Table 2. Monthly distribution of conditions in
seasonal ovarian cycle of Hypsiglena torquata
from examination of museum specimens. Values shown
are the numbers of females exhibiting each of the
Month n No yolk Early yolk Enlarged follicles
deposition deposition [greater than] 12 mm length
February 3 3 0 0
March 4 3 1 0
April 7 6 0 0
May 5 * 1 0 3
June 2 1 0 0
July 6 4 0 2
August 8 6 1 1
September 6 6 0 0
October 1 1 0 0
(*)Includes one damaged road-killed female
(UAZ 50799) with yolk in ovaries; distinguishing
between enlarged follicles or oviductal eggs
was not possible.
Table 3. Clutch sizes for 9 Hypsiglena torquata
from Arizona (estimated from counts of yolked
follicles [greater than] 12 mm length or
Date SVL Clutch size County Source
2 April 342 2 * LaPaz LACM 138304
2 May 323 4 Maricopa ASU 27451
23 May 310 3 Pima UAZ 50800
30 May 395 5 Pima UAZ 25003
13 June 411 6 * Pima LACM 63455
4 July 362 2 Maricopa ASU 895
10 July 332 2 Cochise ASU 30252
9 August 315 2 Pima UAZ 25021
15 August 391 3 Maricopa Vitt (1975)
(*)Oviductal eggs, others are enlarged
follicles except Vitt (1975) cikkected 15
August laid 3 eggs 1 September