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Reproduction in the Baja California rattlesnake, Crotalus enyo.

The Baja California rattlesnake, Crotalus enyc occurs over most of the Baja peninsula from the vicinity of Cabo Colonet in the northwest, south to Cabo San Lucas, Baja California Sur and on associated islands in the Gulf of California (Beaman and Grismer 1994). Aside from data on captive breeding in C. enyo (Tryon and Radcliffe 1977; Armstrong and Murphy 1979), a report of "eggs" in a female collected 22 March (Klauber 1931), two clutch sizes in Klauber (1972) and time of appearance of neonates (Grismer 2002), information on reproduction in this species is unknown. The purpose of this paper is to provide information on the reproductive cycle of C. enyc from a histological examination of gonads from museum specimens. The reproductive cycle of this species is compared with that of other North American rattlesnakes.

Materials and Methods

A sample of 44 C. enyo (13 females, Mean snout-vent length, SVL = 549 mm [+ or -] 47 SD, range = 487-667 mm); 31 males, Mean SVL = 583 mm [+ or -] 79 SD, range = 470-730 mm) from Baja California was examined from the herpetology collections of the California Academy of Sciences, San Francisco, California (CAS), Natural History Museum of Los Angeles County, Los Angeles, California (LACM), Museum of Vertebrate Zoology, Berkeley, California (MVZ), San Diego Museum of Natural History, San Diego, California (SDSNH), and University of Arizona, Tucson (UAZ) (Appendix). All snakes were collected between 1919 and 1986. The left testis and vas deferens (when available) were removed from males and the left ovary was removed from females for histological examination. Tissues were embedded in paraffin, cut into 5 [micro]m sections and stained with Harris' hematoxylin followed by eosin counterstain. Slides were then examined to determine the stage of the male cycle and for the presence of yolk deposition (secondary vitell ogenesis sensu Aldridge 1979) in females. Histological examination was not performed on two females containing enlarged follicles (> 10 mm length), a female containing oviductal eggs and a female containing a full-term embryo. The number of specimens histologically examined were, testis (= 31), vas deferens (= 22), and ovary (= 9).

Testicular histology was similar to that reported by Goldberg and Parker (1975) for the colubrid snakes, Masticophis taeniatus and Pituophis catenifer (= P. melanoleucus) and the viperid snake, Agkistrodon piscivorus (Johnson et al. 1982). In the regressed testis, seminiferous tubules contained spermatogonia and Sertoli cells. In recrudescence, there was renewal of spermatogenic cells characterized by spermatogonial divisions and primary and secondary spermatocytes were occasionally present. In spermiogenesis, metamorphosing spermatids and mature sperm were present.

Males undergoing spermiogenesis were collected from June through October, with regressed testes present in specimens collected from March through May and testes in recrudescence (recovery) present in specimens collected from March through June (Table 1). The smallest reproductively active male (regressed testes but sperm in the vasa deferentia from a previous spermiogenesis) measured 470 mm SVL. Sperm were present in the vasa deferentia of the following males: March 1/1 (100%); April 2/2 (100%); May 2/2 (100%); June 2/2 (100%); July 1/1 (100%); August 1/1 (100%); September 11/11 (100%); October 2/2 (100%).

The presence of males with regressed testes in spring (March-May) and spermiogenic males from June through October indicate that the timing of the testicular cycle of C. enyo is similar to that of other North American rattlesnakes in which sperm formation occurs summer-autumn and is stored over winter in the vasa deferentia (see Goldberg 1999a,b,c, 2000a,b,c; Goldberg and Holycross 1999; Goldberg and Rosen 2000; Holycross and Goldberg 2001). Field observations are needed to determine when mating occurs in C. enyc.

The seasonal ovarian cycle is summarized in Table 2. The presence of one female collected in March (SYL = 543 mm; GAS 87372) with oviductal eggs (N = 7) suggests that ovulation occurs in spring. We examined the March female (SVL = 545 mm; SDSNH 3003) described by Klauber (1931) as containing "eggs" and found it to contain four enlarged ovarian follicles (> 15 mm length) which would have ovulated. One female collected in August (SVL = 563 mm; GAS 101612) with a full-term embryo (SVL = 220 mm) suggests an ovarian cycle similar to that of other North American rattlesnakes in which ovulation occurs in spring with young being born in late summer (Armstrong and Murphy 1979). Grismer (2002) found newborn C. enyo from late July to mid-October. One female collected 26 September (SVL = 582; MVZ 189971) contained five enlarged ovarian follicles > 10 mm length. This indicates that yolk deposition begins the summer prior to ovulation. The presence of reproductively inactive females suggests that only part of the female p opulation breeds in a particular year. This coincides with the ovarian cycle of other North American rattlesnakes (Goldberg 1999a,c; Goldberg and Holycross 1999; Holycross and Goldberg 2001).

Klauber (1972) reported litter sizes of six and nine for Crotalus enyo. Our finding of one female with seven oviductal eggs is within the range cited by Klauber (1972) although the March female from Klauber (1931) that would have ovulated four eggs is outside this range. It is impossible to know if the five enlarged follicles (> 10 mm length) in the September female (SVL = 582 mm; MVZ 189971) would have ovulated. The one female collected in August with a single full-term embryo indicates the minimum litter size for C. enyc. Small litter sizes are indicated for C. enyo by a female (LACM 134435) collected 12 October 1974 which gave birth in captivity to two neonates on 17 September 1977 (LACM 134431, 134432) and two more on 29 August 1979 (LACM 134433, 134434) respectively. This C. enyo female exhibited a biennial reproductive cycle. However, other rattlesnake species may have an annual, biennial or triennial reproductive cycle in different parts of their range: Crotalus atrox (Tinkle 1962; Fitch and Pisani 19 93; Price 1998; Werler and Dixon 2000); Crotalus viridis (Rahn 1942; Diller and Wallace 1988; Macartney and Gregory 1988). Goldberg and Rosen (2000) reported that yearly percentages of gravid Crotalus scutulatus appeared to be related to an increase in nutritional resources. Therefore it seems plausible that during periods of prey abundance C. enyo could reproduce annually whereas it would reproduce less frequently when these resources are scarce.

Appendix: Specimens of Crotalus enyo examined from the herpetology collections of the California Academy of Sciences (CAS), Museum of Vertebrate Zoology (MVZ), Natural History Museum of Los Angeles County (LACM), San Diego Society of Natural History (SDSNH), and University of Arizona (UAZ).

Baja California: CAS 87372, 143987, 204090, 204094; LACM 20023, 74024, 134431-134435; MVZ 189963, 189967, 189968, 189970, 189971; SDSNH 18778, 44355, 46196, 46198.

Baja California Sur: CAS 14022, 15630, 45885, 90317, 101612, 110997, 135229, 143844, 143853, 143982, 146748, 160223, 160229; LACM 107220, 132135; MVZ 176061, 176062, 189998, 190000, 190042, 190043, 190129; SDSNH 3003, 46102, 46197; UAZ 23295, 23521, 31692, 31693.
Table 1. Monthly distribution of reproductive conditions in seasonal
testicular cycle of Crotalus enyo. Values are the number of males
exhibiting each of the three conditions.

Month N Regressed Recrudescence Spermiogenesis

March 2 1 1 0
April 4 2 2 0
May 2 1 1 0
June 3 0 1 2
July 3 0 0 3
August 2 0 0 2
September 13 0 0 13
October 2 0 0 2

Table 2. Monthly distribution of reproductive conditions in seasonal
ovarian cycle of Crotalus enyo. Values are the number of females
exhibiting each of the four conditions.

 Enlarged
 follicles Oviductal Full-term
Month N Inactive (> 10 mm width) eggs embryo

March 4 2 1 1 0
April 1 1 0 0 0
May 1 1 0 0 0
June 1 1 0 0 0
July 1 1 0 0 0
August 4 3 0 0 1
September 1 0 1 0 0


Acknowledgments

We thank: G. Bradley (UAZ), B. Hollingsworth (SDSNH), D. Kizirian (LACM), J. Vindum (GAS) and D. Wake (MVZ) for permission to examine specimens.

Accepted for publication 5 August 2002.

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Grismer, L. L. 2002. Amphibians and reptiles of Baja California, including its Pacific islands and the islands in the Sea of Cortes. University of California Press, Berkeley, 399 pp.

Holycross, A. T., and S. R. Goldberg. 2001. Reproduction in northern populations of the ridgenose rattlesnake, Crotalus willardi (Serpentes: Viperidac). Copeia, 2001:473-481.

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. Crotalus tigris and Crotalus enyo, two little known rattlesnakes of the Southwest. Trans. San Diego Soc. Nat Hist., 6:353-370.

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

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Tryon. B. W., and C. W Radcliffe. 1977. Reproduction in captive Lower California rattlesnakes, Crotalus enyo enyo (Cope). Herpetol. Rev., 8:34-36.

Werler, J. E., and J. R. Dixon. 2000. Texas snakes. Identification, distribution and natural history. University of Texas Press, Austin, xv + 437 pp.

Stephen R. Goldberg (1) and Kent R. Beaman (2)

(1.) Department of Biology, Whittier College, Whittier, California 90608

(2.) Section of Herpetology, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007
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Author:Goldberg, Stephen R.; Beaman, Kent R.
Publication:Bulletin (Southern California Academy of Sciences)
Date:Apr 1, 2003
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