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Reproductive cycle of the Kalahari tree skink, Trachylepis spilogaster (Squamata: Scincidae) from southern Africa.

Abstract. -- The reproductive cycle of the viviparous Kalahari tree skink, Trachylepis spilogaster, was studied from a histological examination of gonadal material. Males follow a seasonal testicular cycle in which spermiogenesis occurred in spring and early summer. Regression followed by recrudescence took place during summer and autumn. Females began to deposit yolk the previous summer from which young were born. Not all females reproduce annually. Female litter size was positively correlated with body size. Mean litter size for 29 T. spilogaster females was 4.93 [+ or -] 1.6 SD; range 2-9. Litter sizes of 2 and 9 are new minimum and maximum sizes for T. spilogaster.

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The Kalahari tree skink, Trachylepis spilogaster, (formerly Mabuya spilogaster), is an arboreal species that frequents Acacia trees along dry river beds in arid savannah from Kimberley and the Lower Orange River in Northern Cape Province, Republic of South Africa through Botswana and Namibia to southern Angola (Branch 1998). There is little information on its reproduction. Branch (1998) reported T. spilogaster gave birth to 3-5 offspring. Pianka (1986) reported a mean litter size of 4.4 [+ or -] 1.3 SD for 74 females. The purpose of this paper is to supplement known information on T. spilogaster reproduction from a histological examination of museum specimens.

MATERIALS AND METHODS

One-hundred twenty-five female (mean snout-vent length, SVL = 66.1 mm [+ or -] 6.5 SD, range = 53-85 mm), 102 male (mean SVL= 63.5 mm [+ or -] 7.0 SD, range = 47-76 mm) and seven neonates (mean SVL = 25.3 mm [+ or -] 2.3 SD, range = 23-28 mm) T. spilogaster were examined from the herpetology collection of the Natural History Museum of Los Angeles County (LACM), Los Angeles, CA. Lizards were collected during 1969-1970, 1972. The left testis and epididymis 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 or embryos were previously removed (Pianka, 1986). Tissues were embedded in paraffin, sectioned at 5 [micro]m and stained with hematoxylin followed by eosin counterstain. Testicular 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 (secondary vitellogenesis sensu Aldridge 1979) or corpora lutea. Trachylepis spilogaster adult male versus adult female mean body sizes were compared using an unpaired t test. The relationship between body size (snout-vent length, SVL), and clutch size was examined by linear regression analysis. Statistical tests were performed using Instat (vers. 3.0b, Graphpad Software, San Diego, CA).

The following specimens of Trachylepis spilogaster from Botswana (Kgalagadi Province), the Republic of South Africa (Northern Cape Province) and Namibia were examined from the herpetology collection of the LACM.

BOTSWANA

59 km N Tsabong (25[degrees]32'S, 22[degrees]18'E) LACM 81245; 131 km N Tsabong (24[degrees]55'S, 22[degrees]05'E) LACM 81247, 81249, 81251, 81253-81257; 14 km W Middleputs (26[degrees]51'S, 21[degrees]38'E) 81230-81239; 1 km W Tsabong (26[degrees]03'S, 22[degrees]25'E) 81240-81242; 59 km N Tsabong (25[degrees]32'S, 22[degrees]18'E) 81244, 81246; 31 km S Tsabong (26[degrees]20'S, 22[degrees]27'E) LACM 81000; 11 km S Tsabong (26[degrees]08'S, 22[degrees]28'E) LACM 81002-81005, 81009-81013, 81017, 81019, 81021, 81023, 81024, 81026, 81029, 81031, 81034, 81035, 81039-81042, 81047, 81050, 81051, 81053, 81057, 81058, 81066-81068, 81073, 81074, 81076, 81077, 81081, 81082, 81085, 81091, 81104, 81105, 81120, 81122, 81124, 81129, 81130, 81132-81134, 81136, 81140-81142, 81144-81146, 81151, 81155, 81156, 81158, 81163-81167, 81172, 81175, 81176, 81178, 81186, 81187, 81190, 81192, 81195-81201, 81203-81205, 81210, 81212, 81214-81216, 81219-81228.

REPUBLIC OF SOUTH AFRICA

129 km N, 65 km W Upington LACM 80868; 4 mi SE Aansluit, Kurumar River (26[degrees]45'S, 22[degrees]32'E) LACM 80990-80995, 80998; 3 mi W, 4 mi S. Vanzylsrus (27[degrees]04'S, 21[degrees]48'E) LACM 80973-80976, 80978, 80980-80982, 80986, 80988; 8 mi E, 1 mi N Vanzylsrus (26[degrees]55'S, 21[degrees]52'E) LACM 80986, 80987; Kalahari Gemsbok National Park (27[degrees]17'S, 21[degrees]54'E) LACM 80870-80872, 80874-80877, 80879-80881, 80883-80890, 80892-80894, 80896-80904, 80906, 80908, 80909, 80912, 80915, 80920-80924, 80926, 80928-80930, 80934, 80937, 80939-80944, 80947-80949, 80953-80957, 80960, 80964-80967, 80970, 80979, 139057.

NAMIBIA

Karas Region, 89 km ENE Koes (26[degrees]00'S, 19[degrees]15'E) LACM 77243; Karas Region, 25 km WNW Helmeringhausen (24[degrees]80'S, 15[degrees]05'E) LACM 77012, 77013, 77015; Karas Region, 77 km W Helmeringhausen (25[degrees]88'S, 16[degrees]81'E) LACM 77078-77081; Erongo Region, 47 km S Wilhelmstal (22[degrees]21'S, 16[degrees]21'E) LACM 77618-77622; Khomas Region, 110 km E. Windhoek (22[degrees]41'S, 18[degrees]08'E) LACM 77419-77421, 77423-77425, 77427-77429.

RESULTS

Males followed a seasonal testicular cycle (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 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 period of spermiogenesis (Table 1) encompassed July through January (winter-summer); epididymides contained sperm. Since 98% (65/66) males were undergoing spermiogenesis during this time, breeding most likely occurs during this period. There was a period of regression in February-March (summer) followed by recrudescence which occurred in summer and autumn. The smallest reproductively active male (spermiogenesis) measured 47 mm SVL (LACM 81176) and was from August.

The mean body size of the female T. spilogaster sample was significantly larger than that of the male sample (t = 2.84, df = 225, P = 0.01). Monthly changes in the ovarian cycle are in Table 2. Oviductal eggs and/or embryos were previously removed and their mean value appears in Pianka (1986). In a few cases they were not removed or lizards were collected by other individuals; these data are in Table 2. Females with enlarged follicles (> 4 mm length), oviductal eggs, embryos or corpora lutea only were present September to April (spring-summer). There was no evidence (corpora lutea and early yolk deposition) in the same female to suggest more than one brood is produced during the same reproductive season. The presence of 40/96 (42%) of mature females with inactive ovaries during the period when other females were reproductively active (Table 2) suggests that not all females in the population produce young each year. Four females (Table 2) were undergoing early yolk deposition in January-February (summer) when it would not have been possible to complete it during the current reproductive season. Assuming the follicles continued development without undergoing atresia, they would have resulted in embryos which would have completed development during the next reproductive season. The smallest reproductively active female (corpus luteum present) measured 53 mm SVL (LACM 80998) and was from December. Linear regression analysis revealed a significant positive correlation between female body size (SVL) in mm and clutch = litter size for 29 T. spilogaster females (Fig. 1): Y = -5.26 + 0.15X, r = 0.61, P = 0.0004. Mean clutch = litter size was 4.93 [+ or -] 1.6 SD, range: 2-9. Two eggs is a new minimum litter size and nine is a new maximum litter size for T. spilogaster. Young < 30 mm SVL (presumably neonates) were collected (November, n = 1; February, n = 4; April, n = 2).

DISCUSSION

The sequence of events in the testicular cycle of T. spilogaster is similar to that which occurs in the African lacertids Meroles cuneirostris (cf. Goldberg & Robinson 1979), Pedioplanis namaquensis (cf. Goldberg 2006a) and Pedioplanis lineoocellata (cf. Goldberg 2006b). All undergo spring spermiogenesis followed by summer regression and subsequent recrudescence. Males of the scincid lizard, Mabuya capensis, from South Africa followed a testicular cycle similar to T. spilogaster as peak spermiogenesis occurred during late winter to early summer followed by summer regression (Flemming 1994). The timing of the testicular cycle of T. spilogaster with spring spermiogenesis followed by summer regression is similar to that of the North American skinks, Eumeces skiltonianus (cf. Goldberg 2005); Eumeces anthracinus and Eumeces fasciatus (cf. Trauth 1994). In contrast, two other African skinks, Mabuya quinquetaeniata and Mabuya striata from Zambia exhibited cycles in which spermiogenesis was continuous (Simbotwe 1980).

[FIGURE 1 OMITTED]

The timing of the T. spilogaster female reproductive cycle was similar to that of the African skink Mabuya capensis reported by Flemming (1994) as ovulation occurred during mid-spring to midsummer and gravid females were collected from October to February. It was indicated by Van Wyk (1991) that Cordylus giganteus females exhibited a biennial reproductive strategy with females reproducing once every two years. This may be the case for T. spilogaster females as almost half of the female population was not reproductively active during the reproductive season and there were no regressing corpora lutea in these lizards to indicate recent reproduction. Goldberg & Bezy (1974) similarly reported that only about half of the population of live-bearing Xantusia riversiana females from California were reproductively active in a given year. It appears that some T. spilogaster females start yolk deposition during summer for next year's litter.

As was the case for M. capensis (cf. Flemming 1994), there was no evidence that T. spilogaster females produce more than one litter per year. In contrast, Patterson (1990) reported the viviparous Mabuya striata might be multi-clutched. Trachylepis spilogaster females apparently mated at different times during the reproductive period as evidenced by the eight month span (September to April) in which females were found in different stages of the ovarian cycle (oviductal eggs, embryos or corpora lutea).

As occurred in M. capensis (cf. Flemming 1994). female body sizes and clutch sizes in T. spilogaster were positively correlated. Male and female reproductive cycles of T. spilogaster appear synchronized as males undergo spermiogenesis during spring at which time females are close to ovulation. The appearance of T. spilogaster neonates during November, February and April is consistent with the period during which females were reproductively active. Pianka (1986) reported a mean clutch/litter size of 4.4 [+ or -] 1.3 SD for T. spilogaster which is close to the value of 4.9 [+ or -] 1.6 SD reported herein.

Skinks are the second most diverse group of lizards in southern Africa with 69 species in 11 genera (Branch 1998). Subsequent studies on the reproductive cycles of additional scincid species from southern Africa are needed to ascertain whether the reproductive pattern exhibited by T. spilogaster is common to other members of the Scincidae from this region.

ACKNOWLEDGMENTS

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

LITERATURE CITED

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

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

Flemming, A. F. 1994. Male and female reproductive cycles of the viviparous lizard, Mabuya capensis (Sauria: Scincidae) from South Africa. J. Herpetol., 28:334-341.

Goldberg, S. R. 2005. Reproductive cycle of the western skink, Eumeces skiltonianus (Sauria: Scincidae), in southern California. Tex. J. Sci., 57(3):295-301.

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

Goldberg, S. R. 2006b. Reproductive cycle of the spotted sand lizard, Pedioplanis lineoocellata (Squamata: Lacertidae) from southern Africa. Texas J. Sci., 58(1):65-72.

Goldberg, S. R., & R. L. Bezy. 1974. Reproduction in the island night lizard, Xantusia riversiana. Herpetologica, 30:350-360.

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

Patterson, J. W. 1990. Female reproductive cycles in two subspecies of the tropical lizard Mabuya striata. Oecologia, 84:232-237.

Pianka, E. R. 1986. Ecology and Natural History of Desert Lizards. Analyses of the Ecological Niche and Community Structure. Princeton University Press, Princeton, New Jersey, x + 208 pp.

Simbotwe, M. P. 1980. Reproductive biology of the skinks Mabuya striata and Mabuya quinquetaeniata in Zambia. Herpetologica, 36:99-104.

Trauth, S. E. 1994. Reproductive cycles in two Arkansas skinks in the genus Eumeces (Sauria: Scincidae). Proc. Arkansas Acad. Sci., 48:210-218.

Van Wyk, J. H. 1991. Biennial reproduction in the female viviparous lizard Cordylus giganteus. Amphib.-Reptil., 12:329-342.

SRG at: sgoldberg@whittier.edu

Stephen R. Goldberg

Department of Biology, Whittier College Whittier, California 90608
Table 1. Monthly distribution of reproductive conditions in the seasonal
testicular cycle of 102 Trachylepis spilogaster. Sequence of months
begin with austral spring. Values are the numbers of males exhibiting
each of the conditions.

Month n Regressed Recrudescence Spermiogenesis

September 15 0 0 15
October 11 0 0 11
November 5 0 0 5
December 12 0 0 12
January 5 0 0 5
February 14 1 5 8
March 3 1 2 0
April 2 0 2 0
May 12 1 6 5
June 5 1 2 2
July 10 0 0 10
August 8 0 1 7

Table 2. Monthly distribution of reproductive conditions in the seasonal
ovarian cycle of 125 Trachylepis spilogaster from southern Africa.
Sequence of months begin with austral spring. Values shown are the
numbers of females exhibiting each condition.

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

September 17 10 0 3
October 20 6 0 2
November 9 6 0 0
December 21 7 1 7
January 7 2 3 0
February 14 4 1 1
March 3 1 0 0
April 5 4 0 0
May 6 6 0 0
June 9 9 0 0
July 10 10 0 0
August 4 4 0 0

Month Oviductal eggs Embryos Corpora lutea

September 1 0 3
October 4* 7 1
November 2 1 0
December 1 0 5
January 1 0 1
February 0 1 7
March 1* 0 1
April 0 0 1
May 0 0 0
June 0 0 0
July 0 0 0
August 0 0 0

*One female contained squashed oviductal eggs that could not be counted.
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Author:Goldberg, Stephen R.
Publication:The Texas Journal of Science
Geographic Code:6BOTS
Date:Nov 1, 2006
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