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Reproduction in the Baja California collared lizard, Crotaphytus vestigium (squamata: Crotaphytidae).

Crotaphytus vestigium, a rock-dwelling species of the peninsular ranges of Baja California, occurs along the northern slope of the San Jacinto Mountains, Riverside County, California, south to the southern margin of the volcanic Magdalena Plain in Baja California Sur (McGuire 1996). Published information on the reproduction of C. vestigium consists of brief accounts by Lemm (2006), Ivanyi, (2009) and field observations by McGuire (1996), Grismer (2002) and Stebbins (2003). The purpose of this paper is to examine the reproductive biology of C vestigium from a histological analysis of gonadal material from museum specimens, an often used method, see for example, Goldberg (1974). Information on the reproductive cycle such as timing of spermiogenesis, number of egg clutches produced and period of vitellogenesis may not only be helpful in determining phylogenetic affinities, but also provides essential lire history data for implementing conservation management strategies of lizard species.

We examined 61 C. vestigium consisting of 33 males (mean snout-vent length, SVL = 96.5 mm [+ or -] 12.3 SD, range: 72-116 mm and 28 females (mean SVL = 80.4 mm [+ or -] 8.6 SD, range: 54-93 mm) from Imperial, Riverside and San Diego Counties, California and Baja California and Baja California Sur, Mexico. Specimens were examined from the herpetology collections of the Natural History Museum of Los Angeles County (LACM), Museum of Vertebrate Zoology (MVZ), and San Diego Society of Natural History (SDSNH) (Appendix I). Lizards were collected 1934-1997. Histology slides were deposited at LACM, MVZ and SDSNH.

The left testis was removed from males and the left ovary was removed from females for histological examination (Presnell and Schreibman 1997). Enlarged ovarian follicles (> 5 mm) and/or oviductal eggs were counted. Tissues were embedded in paraffin, sectioned at 5 [micro]m and stained with hematoxylin followed by eosin counterstain. Ovary slides were examined for yolk deposition or corpora lutea. Testis slides were examined to ascertain the stage of the testicular cycle present. Mean SVL of maie and female C. vestigium were compared using an unpaired t-test (Instat vers. 3.0b, Graphpad Software, San Diego, CA).

The mean male SVL of C. vestigium significantly exceeded that of females (unpaired t test, t = 5.82, df = 59, P < 0.0001). Monthly stages in the testicular cycle of C. vestigium were shown in Table 1. Three stages were present: (1) Regression, the germinal epithelium was reduced to 1-3 cell layers in thickness and consists of spermatogonia and Sertoli cells; (2) Recrudescence, a proliferation of germ cells for the next period of sperm formation was underway. In early recrudescence, primary spermatocytes predominate, whereas in late recrudescence, secondary spermatocytes and spermatids were most abundant; (3) Spermiogenesis, lumina of the seminiferous tubules were lined by clusters of sperm or clusters of metamorphosing spermatids. The smallest reproductively active male (LACM 63168) with spermiogenesis in progress measured 73 mm SVL and occurred in July. One male collected in April (LACM 138523) measured 72 mm SVL and exhibited testicular recrudescence. It was not known when this individual would have commenced spermiogenesis.

The testicular cycle of C. vestigium was typical of other lizards from western North America that undergo spermiogenesis beginning in spring and terminate in summer (see Goldberg 1974, 1975, 1977, 1983). The congener Crotaphytus collaris follows a testicular cycle similar to that of C. vestigium. However, in west-central Texas, reproductive activity in C. collaris was observed from April into July (Ballinger and Hipp 1985). The onset of sperm production was delayed until early May in Arkansas (Trauth 1979). This suggests some geographic variation in the reproductive cycle of C. collaris. It was not known whether there was geographic variation in the reproductive cycle of C. vestigium, although one individual (Table 1) in spermiogenesis (MVZ 73568) in March was from the southern part of its range in Baja California Sur, Mexico. Lemm (2006) reported breeding of C. vestigium in May and June, although data were lacking to support this claim. However, out results suggested breeding may commence in April. This was corroborated by McGuire (1996), Grismer (2002) and Stebbins (2003), who reported C. vestigium from Baja California Sur with breeding coloration in April.

Four stages were present in the ovarian cycle of C. vestigium: (1) no yolk deposition (quiescent); (2) early yolk deposition with basophilic granules present; (3) enlarged preovulatory follicles; (4) oviductal eggs. Monthly changes in the ovarian cycle were presented in Table 2. The smallest reproductively active C. vestigium female (LACM 63169) measured 75 mm SVL and was undergoing yolk deposition. The maturity of two females (LACM 4000, SVL = 67 mm and SDSNH 17667, SVL = 54 mm) was doubtful, and were excluded from Table 2. Mean clutch size (enlarged ovarian follicles > 5 mm or oviductal eggs) for three females was 2.67 [+ or -] 1.2 SD, range: 2-4. One clutch from June (SDSNH 60111) was damaged and could not be counted (Table 2). Lemm (2006) reported 1-2 clutches of 8 or more eggs, although we know of no report in the literature documenting multiple clutching for C. vestigium. Ivanyi (2009) reported clutches of 3-8 eggs with breeding lasting until late summer. Our observation of two eggs was an unreported minimum clutch size for C. vestigium.

It appeared that the period of female reproductive activity encompasses spring and summer (Table 2). Since all seven females from May had quiescent ovaries (Table 2) it was possible yolk deposition was delayed in some females or not all females reproduced each year. Two females from Baja California (LACM 16993) and Riverside County (LACM 52889) contained vitellogenic follicles in April. Thus, there was no indication of yolk deposition commencing earlier in the south, although our female sample size was too small to clarify this issue. Four females from July undergoing early yolk deposition (Table 2) also raised questions. We had no females from the month of August, soit was not possible to conclude if late season egg clutches were produced. As in other North American lizards (Goldberg 1973, 1975), vitellogenic follicles occurring late in the breeding season might typically undergo atresia and yolk reabsorption. On the other hand, Grismer (2002) reported a female with gravid coloration in early October, just east of Canipole, Baja California Sur which suggests eggs were produced late in the year.

Considering the ovarian cycle of the congener C. collaris, females from Arkansas and Utah ceased reproduction at the end of June (Trauth 1978, Andre and MacMahon 1980). In the arid regions of southern California and Baja California, the ovarian cycle of C. vestigium, was of longer duration and extends into August and perhaps October (Grismer 2002). This difference tended to support the separation of C. collaris and C. vestigium into separate species.

Appendix I

Crotaphytus vestigium examined from the Natural History Museum of Los Angeles County (LACM), Museum of Vertebrate Zoology (MVZ), and San Diego Society of Natural History (SDSNH).

LACM Baja California 4000, 16993, 16995, 16996, 63176, 94681, 138523, Baja California Sur, 16994, 63167-63171, 63173-63175, 63177, 63178, California, Imperial County, 146603, Riverside County 16873-16875, 52889, 52890, 94625, 94627-94629, 122043; MVZ Baja California, 50016, 51140, 140754, 140755, Baja California Sur 73568; SDSNH Baja California, 17052, 17667, 19788-19792, 26754, 37815, 41612, Baja California Sur, California, 30107-30111, Imperial County, 60110, 60111, 60216, 62822, 62823, Riverside County 20699, San Diego County 11088, 11951, 13250, 29698, 40353, 58391.

Acknowledgments

We thank Christine Thacker (LACM), Carol Spencer (MVZ) and Bradford Hollingsworth and Melissa Stepek (SDSNH) for permission to examine specimens.

Literature Cited

Andre, J.B. and J.A. MacMahon. 1980. Reproduction in three sympatric lizard species from west-central Utah. Great Basin Naturalist, 40:68-72.

Ballinger, R.E. and T.G. Hipp. 1985. Reproduction in the collared lizard, Crotaphytus collaris, in west central Texas. Copeia, 1985:976-980.

Goldberg, S.R. 1973. Ovarian cycle of the western fence lizard, Sceloporus occidentalis. Herpetologica, 29: 284-289.

--. 1974. Reproduction in mountain and lowland populations of the lizard Sceloporus occidentalis. Copeia, 1974:176-182.

--. 1975. Reproduction in the sagebrush lizard, Sceloporus graciosus. Amer. Midl. Nat., 93:177-187.

--. 1977. Reproduction in a mountain population of the side-blotched lizard, Uta stansburiana (Reptilia, Lacertilia, Iguanidae). J. Herpetol., 11:31-35.

--. 1983. Reproduction of the coast horned lizard, Phrynosoma coronatum, in southern California. Southwest. Nat., 28:478-479.

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.

Ivanyi, C.S. 2009. Baja California Collared Lizard Crotaphytus vestigium Smith and Tanner, 1972. Pp. 112-115, In: Lizards of the American Southwest, A Photographic Field Guide. (L.L.C. Jones and R.E. Lovich, eds.) Rio Nuevo Publishers, Tucson, Arizona. 567 pp.

Lemm, J.M. 2006. Field Guide to Amphibians and Reptiles of the San Diego Region. University of California Press, Berkeley. 326 pp.

McGuire, J.A. 1996. Phylogenetic systematics of crotaphytid lizards (Reptilia: Iguania: Crotaphytidae). Bulletin of the Carnegie Museum of Natural History, 32:1-143.

Presnell, J.K. and M.P. Schreibman. 1997. Humason's Animal Tissue Techniques, 5th Ed. The Johns Hopkins University Press, Baltimore. 572 pp.

Stebbins, R.C. 2003. A Field Guide to Western Amphibians and Reptiles, 3rd Ed. Houghton Mifflin Co., Boston. 533 pp.

Trauth, S.E. 1978. Ovarian cycle of Crotaphytus collaris (Reptilia, Lacertilia, Iguanidae) from Arkansas with emphasis on corpora albicantia, follicular atresia, and reproductive potential. Journal of Herpetology, 12:461-470.

--. 1979. Testicular cycle and timing of reproduction in the collared lizard (Crotaphytus collaris) in Arkansas. Herpetologica, 35:184-192.

Stephen R. Goldberg (1) and Clark R. Mahrdt (2)

(1) Whittier College, Department of Biology, P.O. Box 634, Whittier, California 90608, USA, sgoldberg@whittier.edu

(2) Department of Herpetology, San Diego Natural History Museum, P.O. Box 121390, San Diego, California 92112-1390, USA, leopardlizard@cox.net
Table 1. Monthly stages in the testicular cycle of Crotaphytus
vestigium.

Month       n    Regression   Recrudescence   Spermiogenesis

March       6        1              4               1
April       6        0              2               4
May         8        0              2               6
June        2        0              0               2
July        6        0              0               6
August      4        4              0               0
November    1        1              0               0

Table 2. Monthly stages in the ovarian cycle of Crotaphytus
vestigium. A female in June contained  damaged oviductal eggs which
were not counted.

                                          Enlarged
                             Early yolk   follicles   Oviductal
Month       n    Quiescent   deposition    > 5 mm       eggs

March        1       1           0            0           0
April        2       0           2            0           0
May          7       7           0            0           0
June         2       0           0            1          1 *
July        11       5           4            1           1
September    2       2           0            0           0
December     1       1           0            0           0
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Title Annotation:Research Note
Author:Goldberg, Stephen R.; Mahrdt, Clark R.
Publication:Bulletin (Southern California Academy of Sciences)
Article Type:Report
Geographic Code:1USA
Date:Dec 1, 2010
Words:1728
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