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Reproductive cycle of the spotted sand lizard, Pedioplanis lineoocellata (Squamata: Lacertidae) from southern Africa.

Abstract. -- The reproductive cycle of the spotted sand lizard, Pedioplanis lineoocellata, is described from histological examination of gonadal material. Reproduction is seasonal and mainly confined to summer. Males have a testicular cycle in which spermiogenesis occurred primarily in December-February. Females with enlarged ovarian follicles (> 4 mm length) occurred January-February and October. The presence of females with corpora lutea from a previous clutch and yolk deposition for a subsequent clutch suggests more than one clutch can be produced in the same reproductive season. Mean clutch size for 22 females with enlarged ovarian follicles was 6.8 [+ or -] 2.0 SD, range: 2-11. Two eggs is a new minimum clutch size and 11 is a new maximum clutch size for P. lineoocellata. The smallest reproductively active male measured 42 mm SVL and the smallest reproductively active female measured 50 mm SVL.

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The spotted sand lizard, Pedioplanis lineoocellata, occurs in the western half of the African subcontinent including parts of Namibia, Botswana and Republic of South Africa, but is absent from regions of deep sand like the Namib and central Kalahari deserts (Branch 1998). It occurs in varied habitats including karroid veld, mesic thicket and arid and mesic savannah (Branch 1998); it is a sit and wait predator (Pianka 1971). Anecdotal information on its reproduction appeared in Fitzsimons (1943); Pianka (1971; 1986); De Waal (1978); Auerbach (1985); Baard (1987); Rogner (1997) and Branch (1998). The purpose of this paper is to present additional information on the reproductive cycle of P. lineoocellata from a histological examination of gonadal material from museum specimens. Information on the reproductive cycle of an organism is needed to understand the evolution of life-history strategies. Such data are also useful in formulating conservation policies.

MATERIALS AND METHODS

One-hundred twelve female (mean snout-vent length, SVL = 56.0 mm [+ or -] 3.1 SD, range = 48-63 mm) and 167 male (mean SVL = 57.2 mm [+ or -] 4.5 SD, range = 42-67 mm) P. lineoocellata were examined from the herpetology collection of the Natural History Museum of Los Angeles County, Los Angeles, CA. Lizards were collected during 1969-1970. The left testis and epididymides were removed from males and the left ovary was removed from females for histological examination. Enlarged follicles (> 4 mm length) were counted but not examined histologically. Oviductal eggs were previously removed for an ecological study (Pianka 1986). Tissues were embedded in paraffin, sectioned at 5 [micro]m and stained with Harris' hematoxylin followed by eosin counterstain. Testes slides were examined to determine the stage of the spermatogenic cycle and epididymides were examined for the presence of sperm. Ovary slides were examined for the presence of yolk deposition or corpora lutea. The relationship between body size (snout vent length, SVL) and clutch size was examined by linear regression analysis and male and female P. lineoocellata mean body sizes and mean egg clutch sizes from Botswana and the Republic of South Africa were compared with unpaired t tests using Instat (vers. 3.0b, Graphpad Software, San Diego, CA).

Material examined. -- Specimens of Pedioplanis lineoocellata from the Republic of South Africa (Northern Cape Province) and Botswana (Kgalagadi Province) examined from the herpetology collection of the Natural History Museum of Los Angeles County, Los Angeles (LACM).

REPUBLIC OF SOUTH AFRICA

31 km N, 100 km E Upington (28[degrees]13'S, 22[degrees]16'E). LACM 79158, 79159, 79160, 79161, 79164, 79166, 79170-79173, 79178, 79179, 79184, 79187, 79190, 79192-79194, 79196, 79200, 79207, 79210, 79211, 79231, 79234, 79256, 79297, 79302, 79305, 79314-79316, 79321.

120 km N, 54 km W Upington (27[degrees]22'S, 20[degrees]43'E). 78740-78742, 78745-78749, 78752-78771, 78773-78777, 78779, 78780, 78782, 78784-78788, 78790-78792, 78794-78797, 78799, 78801-78803, 78809, 78810, 78820, 78874, 78904, 79019.

24 km N, 53 km E. Upington (28[degrees]17'S, 22[degrees]05'E). 84085, 84086.

Kalahari-Gemsbok National Park (25[degrees]45'S, 20[degrees]44'E). 138978-138980, 138983.

29 km S, 40 km E Rietfontein (27[degrees]00'S, 20[degrees]27'E). 78923, 78924, 78926-78949, 78951, 78952, 78954-78958, 78960-78965, 78968-78970, 78972, 78973, 78974, 78975, 78977, 78978, 78979, 78980, 78981, 78982, 78985, 79428.

Kalahari-Gemsbok National Park, 1 km W Kameel Sleep (23[degrees]45'S. 20[degrees]44'E). 79324-79328, 79330-79333, 79335, 79337, 79342, 79344-79354, 79356, 79358, 79369.

121 km N, 16 km E Upington (27[degrees]22'S, 21[degrees]25'E).79446-79450, 79459, 79597.

129 km N, 65 km W Upington (27[degrees]17'S, 21[degrees]54'E). 79020-79024, 79026, 79027, 79029-79034, 79036-79040, 79042-79044, 79047, 79049, 79050, 79055-79057, 79059, 79060, 79062, 79064, 79066, 79067, 79069, 79079, 79084-79086, 79135, 79138, 79139, 79142, 79146, 79147.

BOTSWANA

11 km S. Tsabong (26[degrees]08'S, 22[degrees]28'E). 79712-79714, 79718-79722, 79725-79738, 79740, 79741, 79743-79750, 79755, 79756, 79759, 79761, 79763-79766, 79768-79770, 79773, 79774, 79816, 79817, 79829, 79834, 79845, 79846, 79848, 79851, 79852.

RESULTS

The mean of the male P. lineoocellata sample was significantly larger than that of the female sample (t = 2.44, df = 277, P = 0.0151). Seasonal changes in the testicular cycle are presented in Table 1. In the regressed testis, the germinal epithelium is exhausted and the predominant cells are Sertoli cells and spermatogonia. In testes undergoing recrudescence there is a renewal of the germinal epithelium for the next period of spermiogenesis. Primary and secondary spermatocytes are the predominant cells; some spermatids, but no spermatozoa may be present. During spermiogenesis the seminiferous tubules are lined by clusters of spermatozoa and metamorphosing spermatids and the epididymides are packed with sperm.

The main period of spermiogenesis (sperm formation) occurs from December-February (summer) (Table 1). During this time 123/126 (98%) of males were undergoing spermiogenesis and sperm was present in the epididymides. Males with regressed testis were present in February-April and September. Testes in recrudescence (recovery) were present in September-November (spring). The smallest reproductively active male (spermiogenesis in progress) was from September. It measured 42 mm SVL (LACM 79816). Another male measuring 43 mm SVL from October was also undergoing spermiogenesis.

Data on the seasonal ovarian cycle is presented in Table 2. The primary period of ovarian activity occurred during summer (January-February) when 82/97 (85%) females were reproductively active (i.e., early yolk deposition, enlarged follicles or corpora lutea). The period of ovarian activity apparently occurs from October-February as one female with enlarged follicles (> 4 mm length) was collected in October (Table 2). The presence of early yolk deposition for a subsequent clutch and corpora lutea from a previous clutch in the same female suggests that female P. lineoocellata may produce two clutches in a reproductive season. The smallest reproductively active female (corpora lutea present) measured 50 mm SVL (LACM 79234). Mean clutch size for 22 sets of enlarging ovarian follicles (> 4 mm diameter) from P. lineoocellata females from South Africa and Botswana was 6.8 [+ or -] 2.0 SD, range 2-11 (Table 3). There was no statistical difference between clutch sizes from these two areas (t = 0.010, df = 20, P = 0.99). The clutch size of two from LACM 79726 collected in January represents a new minimum clutch size for P. lineoocellata. The clutch size of 11 (LACM 78975) from February is a new maximum clutch size for P. lineoocellata. Linear regression analysis for 22 gravid females revealed that the relation between body size (SVL) and clutch size was not significant (r = 0.36, P = 0.100). Clutch sizes are presented in Table 3.

DISCUSSION

Pedioplanis lineoocellata males have a seasonal testicular cycle in which spermiogenesis occurs primarily during summer. Recrudescence (recovery and renewal of germinal epithelium) occurs in spring. The ovarian cycle of P. lineoocellata was also seasonal with ovarian activity occurring in October-February (spring-summer). More than one egg clutch may be produced in the same reproductive season. Nkosi et al. (2004) reported that reproduction in the congener Pedioplanis burchelli similarly occurred in spring-summer and that some females may produce two clutches per reproductive season. As with P. lineoocellata, clutch size was not correlated with snout-vent length. Similarly, reproduction in Pedioplanis namaquensis occured mainly in summer, clutch size was also not correlated with snout-vent length and multiple egg clutches were possible (Goldberg 2006).

Baard (1987) reported that mating in captivity for P. lineoocellata occurred in October. Attempts to deposit eggs were made in November which concurs with that reported by Rogner (1997) and Branch (1998) that females lay 4-8 eggs in that month; De Waal (1978) reported 4-8 eggs being deposited in February. Presumably eggs may be deposited from November-February. Fitzsimons (1943) reported that P. lineoocellata laid about six eggs in early summer; Auerbach (1985) reported about six eggs are laid. Pianka (1986) reported an average clutch size (n = 123) of 6.9 [+ or -] 2.0 SD eggs which compares to the value presented herein (6.8 [+ or -] 2.0 SD).

The lacertid lizard, Meroles cuenirostris from Namibia, exhibited a testis cycle similar to P. lineoocellata wherein spermiogenesis occurred in spring-summer followed by autumn regression (Goldberg & Robinson 1979). Females of M. cuneirostris contained oviductal eggs over a five month period (September-March) and may produce two clutches per year (Goldberg & Robinson 1979). In contrast, male Meroles anchietae exhibited continuous spermiogenesis throughout the year, while females were capable of year-round reproductive activity (Goldberg & Robinson 1979). This continuous reproductive activity may be the result of M. anchietae eating seeds as well as insects thus having access to a continuous supply of food (Goldberg & Robinson 1979). Further histological examination of seasonal gonad samples from other lacertid species from southern Africa would be required to ascertain variations in reproductive cycles of these species.

ACKNOWLEDGMENTS

I thank Christine R. Thacker (LACM) for permission to examine specimens. Jessica Carlson and Dustin Goto (Whittier College) assisted with histology.

LITERATURE CITED

Auerbach, R. D. 1985. The Reptiles of Gaborone. A Guide to the Reptiles of the South-Eastern Hardveld of Botswana. The Botswana Book Centre, Gaborone. 48 pp.

Baard, E. H. W. 1987. Pedioplanis lineoocellata (Ocellated Sand Lizard): Reproduction. J. Herp. Assoc. Afr., 33:34-35.

Branch, B. 1998. Field Guide to Snakes and other Reptiles of Southern Africa. 3rd ed., Ralph Curtis Books Publishing, Sanibel Island, Florida, 399 pp.

De Waal, S. W. P. 1978. The squamata (Reptilia) of the Orange Free State, South Africa. Mem. Van Die Nasionale Museum, Bloemfontein, Repub. Suid-Afrika 11:1-160

Fitzsimons, V. F. 1943. The Lizards of South Africa. Transvaal Museum Memoir, Pretoria, South Africa, Memoir No. 1, 528 pp.

Goldberg, S. R. 2006. Reproductive cycle of the Namaqua sand lizard, Pedioplanis namaquensis (Squamata: Lacertidae) from southern Africa. Afr. Zool., 41:147-149.

Goldberg, S. R., & M. D. Robinson. 1979. Reproduction in two Namib Desert lacertid lizards (Aporosaura anchietae and Meroles cuneirostris). Herpetologica, 35:169-175.

Nkosi, W. T., N. J. L. Heidman & J. H. Van Wyk. 2004. Reproduction and sexual size dimorphism in the lacertid lizard Pedioplanis burchelli (Sauria: Lacertidae) in South Africa. J. Herpetol., 38:473-480.

Pianka, E. R. 1971. Lizard species density in the Kalahari Desert. Ecology, 52:1024-1029.

Pianka, E. R. 1986. Ecology and Natural History of Desert Lizards. Princeton University Press, Princeton, New Jersey, x + 208 pp.

Rogner, M. 1997. Lizards. Vol. 2. Monitors, Skinks, and Other Lizards Including Tuataras and Crocodilians. Krieger Pub. Co., Malabar, Florida, 308 pp.

SRG at: sgoldberg@whittier.edu

Stephen R. Goldberg

Department of Biology, Whittier College

Whittier, California 90608
Table 1. Monthly distribution of reproductive conditions in seasonal
testicular cycle of 167 Pedioplanis lineoocellata. Values are the
numbers of males exhibiting each of the three conditions.

Month n Regressed Recrudescence Spermiogenesis

January 64 0 0 64
February 42 3 0 39
March 2 1 0 1
April 5 5 0 5
September 6 1 4 1
October 19 0 10 9
November 9 0 5 4
December 20 0 0 20

Table 2. Monthly distribution of reproductive conditions in seasonal
ovarian cycle of 112 Pedioplanis lineoocellata. Values shown are the
numbers of females exhibiting each of the four conditions.

 Enlarged Corpora
 Early yolk follicles Corpora lutea yolk
Month n Inactive deposition (>4 mm length) lutea deposition

January 50 9 28 10 3 0
February 47 6 25 11 3 2
April 1 1 0 0 0 0
October 3 2 0 1 0 0
November 4 4 0 0 0 0
December 7 5 2 0 0 0

Table 3. Clutch sizes for 22 Pedioplanis linoocellata estimated from
counts of enlarged follicles > 4 mm length from southern Africa;
Kgalagadi Province (Botswana), Northern Cape Province (Republic of South
Africa).

Month SVL (mm) Clutch size Province LACM #

January 55 4 N. Cape 79170
January 52 4 N. Cape 79184
January 60 7 N. Cape 79022
January 58 7 N. Cape 79030
January 59 8 Kgalagadi 79736
January 57 9 Kgalagadi 79730
January 58 7 Kgalagadi 79735
January 54 2 Kgalagadi 79726
January 59 7 Kgalagadi 79765
January 52 9 Kgalagadi 79738
February 59 7 N. Cape 79447
February 58 7 N. Cape 78802
February 60 9 N. Cape 78981
February 58 7 N. Cape 78973
February 55 5 N. Cape 78982
February 58 11 N. Cape 78975
February 60 8 N. Cape 78965
February 58 7 N. Cape 78961
February 58 6 Kgalagadi 79774
February 59 7 Kgalagadi 79765
February 63 6 Kgalagadi 79747
October 58 5 N. Cape 84086
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Author:Goldberg, Stephen R.
Publication:The Texas Journal of Science
Geographic Code:60AFR
Date:Feb 1, 2006
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