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REPRODUCTION IN THE NIGHT SNAKE, HYPSIGLENA TORQUATA (SERPENTES: COLUBRIDAE), FROM ARIZONA.
Article Type:
Statistical Data Included
Subject:
Snakes (Physiological aspects)
Reproduction (Physiological aspects)
Reproductive organs (Physiological aspects)
Author:
Goldberg, Stephen R.
Pub Date:
05/01/2001
Publication:
Name: The Texas Journal of Science Publisher: Texas Academy of Science Audience: Academic; General Format: Magazine/Journal Subject: Science and technology Copyright: COPYRIGHT 2001 Texas Academy of Science ISSN: 0040-4403
Issue:
Date: May, 2001 Source Volume: 53 Source Issue: 2
Geographic:
Geographic Scope: Arizona Geographic Code: 1U8AZ Arizona

Accession Number:
78359396
Full Text:
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" snake.

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 determined.

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 April.

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.

ACKNOWLEDGMENTS

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.

LITERATURE CITED

Aldridge, R. D. 1979. Female reproductive cycles of the snakes Arizona elegans and Crotalus viridis. Herpetologica, 35(3):256-261.

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.

Diller, L. V. & R. L. Wallace. 1986. Aspects of the life history and ecology of the desert night snake, Hypsiglena torquata deserticola: Colubridae, in southwestern Idaho. Southwest. Nat., 31(1):55-64.

Dundee, H. A. 1950. Additional records of Hypsiglena from Oklahoma, with notes on the behavior and the eggs. Herpetologica, 6(2):28-30.

Fitch, H. S. 1970. Reproductive cycles of lizards and snakes. Misc. Publ. Mus. Nat. Hist., Univ. Kansas, 52:1-247.

Gates, G. O. 1957. A study of the herpetofauna in the vicinity of Wickenburg, Maricopa County, Arizona. Trans. Kansas Acad. Sci., 60(4):403-418.

Goldberg, S. R. 1975. Reproduction in the sagebrush lizard, Sceloporus graciosus. Amer. Midl. Nat., 93(l):177-187.

Goldberg, S. R. & W. S. Parker. 1975. Seasonal testicular histology of the colubrid snakes, Masticophis taeniatus and Pituophis melanoleucus. Herpetologica, 31(3):317-322.

Hammerson, G. A. 1999. Amphibians and reptiles in Colorado, 2nd edit., University Press of Colorado & Colorado Division of Wildlfe, xxvi + 484 pp.

Hibbard, C. W. 1937. Hypsiglena ochrorhynchus in Kansas and additional notes on Leptotyphiops dulcis. Copeia, 1937(l):74.

Lowe, C. H., C. R. Schwalbe & T. B. Johnson. 1986. The venomous reptiles of Arizona. Arizona Game & Fish Department, Phoenix, ix + 115 pp.

Rodriguez-Robles, 3. A., D. G. Mulcahy & H. W. Greene. 1999. Feeding ecology of the desert nightsnake, Hypsiglena torquata (Colubridae). Copeia, 1999(1):93-100.

Saint Girons, H. 1982. Reproductive cycles of male snakes and their relationships with climate and female reproductive cycles. Herpetologica, 38(1):5-16.

Stebbins, R. C. 1954. Amphibians and reptiles of western North America. McGraw-Hill Book Company, Inc., New York, xxii + 536 pp.

Stebbins, R. C. 1985. A field guide to western reptiles and amphibians. Houghton Mifflin Company, Boston, Massachusetts, xiv + 336 pp.

Tanner, W. W. 1944. A taxonomic study of the genus Hypsiglena. Gt. Bas. Nat., 5(3&4):25-92.

Tanner, W. W. & J. R. Ottley. 1981. Reproduction in Hypsiglena. Gt. Bas. Nat., 41(3):310.

Tennant, A. 1984. The snakes of Texas. Texas Monthly Press, Inc., Austin, 561 pp.

Vitt, L. J. 1975. Observations on reproduction in five species of Arizona snakes. Herpetologica, 31(1):83-84.

Werler, J. E. 1951. Miscellaneous notes on the eggs and young of Texan and Mexican reptiles. Zoologica, 36(1):37-48.

Werler, 3. E. & J. R. Dixon. 2000. Texas snakes: identification, distribution, and natural history. University of Texas Press, Austin, xv + 437 pp.
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
four conditions.
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
Month      Oviductal
             eggs
February       0
March          0
April          1
May            0
June           1
July           0
August         0
September      0
October        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
oviductal eggs).
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
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