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Reproduction in the Speckled Rattlesnake, Crotalus mitchellii (Serpentes: Viperidae).

The speckled rattlesnake, Crotalus mitchellii (Cope, 1861) occurs from southern Nevada to the tip of Baja California and southern California to northwest and west central Arizona from sea level to around 2440 m (Stebbins 1985). It is one of 6 rattlesnake species to occur in southern California (Stebbins 1985). There are only anecdotal reports on reproduction in this species (Klauber 1936; Cunningham 1959; Brattstrom 1965; Lowe et al. 1986). Klauber (1972) provided information on sizes of egg-sets and broods. The purpose of this paper is to provide information on the seasonal ovarian and testicular cycles of C. mitchellii and to provide additional litter sizes.

A sample of 99 specimens of C. mitchellii (42 females, Mean Snout-Vent Length, SVL = 673 mm [+ or -] 82 SD, range = 520--825 mm); (57 Males, Mean SVL = 708 mm [+ or -] 137 SD, range 512--1047 mm) from Arizona, California and Nevada was examined from the herpetology collections of Arizona State University, Tempe, (ASU), the Natural History Museum of Los Angeles County (LACM) and The University of Arizona, Tucson (UAZ) (Appendix). Snakes were collected 1951-1990. Counts were made of enlarged follicles ([greater than] 10 mm length). The left testis, vas deferens and part of the left kidney were removed from males; the left ovary was removed from females for histological examination. Tissues were embedded in paraffin and cut into sections at 5 [micro]m. Slides were stained with Harris' hematoxylin followed by eosin counterstain. Testes slides were examined to determine the stage of the male cycle; ovary slides were examined for the presence of yolk deposition. Vasa deferentia were examined for sperm. Slides of k idney sexual segments were examined for secretory activity. Because some of the specimens were road-kills, not all tissues were available for histological examination due to damage or autolysis. In road-killed males, the kidneys typically underwent autolysis before the reproductive organs. Number of specimens examined by reproductive tissue were: testis = 57, vas deferens 38, kidney = 50, ovary = 42.

Testicular histology was similar to that reported by Goldberg and Parker (1975) for the colubrid snakes, Masticophis taeniatus and Pitupophis catenifer (= P. melanoleucus) and the viperid snake, Agkistrodon piscivorus reported by Johnson et al. (1982). 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 and spermatids were occasionally present. In spermiogenesis, metamorphosing spermatids and mature sperm were present.

Males undergoing spermiogenesis were found April--September; regressed testes were found March-June; testes in recrudescence were found March--August (Table 1). The smallest spermiogenic male measured 512 mm SVL. This was the smallest male included in the study. Sperm were present in the vasa deferentia of the following males: March 2/2 (100%); April 8/8 (100%); May 15/15 (100%); June 7/8 (88%); July 2/3 (67%); August 1/1 (100%); September 1/1 (100%) suggesting C. mitchellii has the capacity to breed March-September. Kidney sexual segments were enlarged and contained secretory granules in 16/17 (94%) of males undergoing spermiogenesis; 11/11 (100%) of males with regressed testes and 14/20 (70%) of males with recrudescent testes. On a monthly basis enlarged sexual segments with secretory granules were found in males in the following proportions: March 3/3 (100%); April 8/9 (89%); May 19/23 (83%); June 6/7 (86%); July 2/ 3 (67%); August 3/4 (75%); September 1/1 (100%). Mating coincides with hypertrophy of the kidney sexual segment (Saint Girons 1982).

Because of insufficient sample sizes from summer and autumn, it is difficult to compare the testicular cycle of C. mitchellii with that of other crotalids. The observation of 44% of May males undergoing spermiogenesis may suggest that spermiogenesis occurs primarily in the spring in C. mitcheliji. This is in contrast to the western rattlesnake, Crotalus viridis, the western diamondback rattlesnake, Crotalus atrox, the Mojave rattlesnake, Crotalus scutulatus and the tiger rattlesnake, Crotalus tigris in which the major period of spermiogenesis occurs in summer-autnumn (Aldridge 1979a, Jacob et al. 1987; Goldberg 1999). Since the peak of C. mitchellii activity occurs in May-June in southern California (Klauber 1931) collections of summer-autumn samples to describe the testicular cycle would be difficult.

One male (LACM 28018) was found in copulation by G. Ahern near Cabazon on the west slope of the San Jacinto Mountains, Riverside County, California at 1800 hours on 11 June 1964. J. W. Wanen (c.f. Brattstrom 1965) found a pair of C. mitchellii mating in the afternoon at Afton, San Bernardino County on 18 April 1953. Mating in Arizona occurs in April-May (Lowe et al. 1986). Additional field observations are needed before the period in which mating occurs under natural conditions is known.

During the months of female reproductive activity (April-June) (Table 2)15/34 (44%) C. mitchellii showed evidence of reproductive activity (early yolk deposition, enlarged follicles or oviductal eggs). This is slightly higher than the value (35%) reported for C. tigris females (Goldberg 1999).

Females with enlarged follicles ([greater than] 10 mm length) were found April-June (Table 2). Females in early yolk deposition (i.e., secondary vitellogenesis sensu Aldridge 1979b) were found in April-May. The "small eggs" reported 10 June in a female C. mitchellii by Cunningham (1959) were likely undergoing early yolk deposition. The smallest reproductively active female (follicles [greater than] 10 mm length) measured 552 mm SVL. Mean litter size for 9 females from Table 3 was 5.78 [+ or -] 1.79 SD (3-8 range). This value is close to the mean litter size 5.77 [+ or -] 2.47 SD (1-10 range) calculated for 22 C. mitchellii listed in Klauber (1972). According to Fitch (1985) C. mitchellii litter sizes are largest in the north and decrease in southern (Mexican) populations.

Crotalus mitchellii appears to follow a biennial reproductive cycle in which yolk deposition (secondary vitellogenesis sensu Aldridge 1979b) commences in summer followed by ovulation the next year which is similar to that reported in other North American rattlesnakes (see Goldberg, 1999). However, Crotalus atrox females are believed to bear litters each year in Oklahoma (Fitch and Pisani 1993) as do southern populations of the western rattlesnakes, Crotalus viridis (c.f. Fitch 1985). Furthermore, there are reports of different populations of the timber rattlesnake, Crotalus horridus following biennial, triennial or quadrennial reproductive cycles (Ernst 1992). Additional reproductive data on C. mitcheliji from different parts of its range will be needed before the timing of the female reproductive cycle can be ascertained for this species.

I thank Robert L. Bezy (Natural History Museum of Los Angeles County), Michael E. Douglas (Arizona State University) and Charles H. Lowe (The University of Arizona) for permission to examine C. mitchellii. Michelle Zamora assisted with histology.

Department of Biology. Whittier College, Whittier, California 90608, U.S.A.

Literature Cited

Aldridge, R. D. l979a. Seasonal spermatogenesis in sympatric Crotalus viridis and Arizona elegans in New Mexico. J. Herpetol., 13:187-192.

-----. 1979b. Female reproductive cycles of the snakes Arizona elegans and Crotalus viridis. Herpetologica, 35:256-261.

Brattstrom. B. H. 1965. Body temperatures of reptiles. Amer. Midl. Nat., 73:376-422.

Cunningham, J. D. 1959. Reproduction and food of some California snakes. Herpetologica, 15:17-19.

Fitch, H. S. 1985. Variation in clutch and litter size in New World reptiles. Misc. Pub. Mus. Nat. Hist., Univ. Kansas, 76:1-76.

Ernst, C. H. 1992. Venomous reptiles of North America. Smithsonian Institution Press, Washington, D.C., ix + 236 pp.

-----. and G. R. Pisani. 1993. Life history traits of the western diamondback rattlesnake (Crotalus atrox) studied from roundup samples in Oklahoma. Occas. Pap. Mus. Nat. Hist., Univ. Kansas, 156:1-24.

Goldberg, S. R. 1999. Reproduction in the tiger rattlesnake, Crotalus tigris (Serpentes: Viperidae). Texas J. Sci., 51:31-36.

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

Jacob, J. S., S. R. Williams and R. P. Reynolds. 1987. Reproductive activity of male Crotalus atrox and C. scutulatus (Reptilia: Viperidae) in northeastern Chihuahua, Mexico. Southwest. Nat., 32:273-276.

Johnson, L. F., J. S. Jacob and P. Torrance. 1982. Annual testicular and androgenic cycles of the cottonmouth (Agkistrodon piscivorus) in Alabama. Herpetologica, 38:16-25.

Klauber, L. M. 1931. A statistical survey of the snakes of the southern border of California. Bull. Zool. Soc. San Diego, No. 8, 93 pp.

-----. 1936. Crotalus mitchellii, the speckled rattlesnake. Trans. San Diego Soc. Nat. Hist., 8:149-184.

-----. 1972. Rattlesnakes. Their habits, life histories, and influence on mankind. 2nd ed. Vol. 1, Univ. California Press, Berkeley, x1vi + 740 pp.

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

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

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

Accepted for publication 15 June 1999.
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Author:Goldberg, Stephen R.
Publication:Bulletin (Southern California Academy of Sciences)
Geographic Code:1U9CA
Date:Aug 1, 2000
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