Reproductive Cycles of the Grass Lizard, Takydromus ...

Reproductive Cycles of the Grass Lizard, Takydromus hsuehshanensis, with Comments on Reproductive Patterns of Lizards from the Central High Elevation Area of Taiwan Wen-San Huang Copeia, Vol. 1998, No. 4. (Dec. 30, 1998), pp. 866-873. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819981230%293%3A1998%3A4%3C866%3ARCOTGL%3E2.0.CO%3B2-6 Copeia is currently published by American Society of Ichthyologists and Herpetologists.

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Copna, 1998(4), pp. 866873

Reproductive Cycles of the Grass Lizard, Takydromus hsuehshanensis, with

Comments on Reproductive Patterns of Lizards from the Central High

Elevation Area of Taiwan

In this study, I describe seasonal variations in the male and female reproductive cycles of Takydromus hsuehshanensis, an oviparous grass lizard endemic to the high altitude areas of Taiwan. Mean snout-vent length (SVL) of adult males (n = 78) and females (n = 105) were 60.5 mm (range = 47-72 mm) and 61.2 mm (range = 54-72 mm), respectively. Females exhibited a spring vitelloge~cperiod with parturition occurring in May to July. The onset of vitellogenesis showed a negative correlation with the mass of the female fat body. Females produced two to four eggs per clutch, and clutch size was positively correlated with SVL: only females with SVLs equal to or larger than 61 mm produced a clutch consisting of four eggs. Two clutches were recorded during a single year in some individuals. Males exhibited a continuous spermatoge~cpattern, but testis mass, accessory sexual organ mass, and seminiferous tubule diameter showed cyclical changes with a peak before the dormant months from September to December. The tubules of the epididymides were full of sperm from December to the following March, indicating that sperm were stored in the epididymides until the occurrence of ovulation in the spring. Male fat bodies exhibited the lowest mass from March to June, coincident with the period of reproductive activity. Male seminiferous tubule diameter exhibited a positive correlation with liver, fat body, and testis masses. However, seminiferoustubule diameter, as well as testes mass, had a negative correlation with precipitation. Timing of reproduction in four other sympatric lizards and clutch size variation in other Takydromus species are compared with those in Z hsuehshand.

It is generally considered that the reproducN most temperate oviparous lizards, both males and females seem to exhibit spring tive cycle of a given lizard species reflects an gonadogenesis, with subsequent courtship, mat- adaptation to the environmental regimes of its ing, and oviposition (Fitch, 1970; Duvall et a]., habitats (e.g., ambient temperature,-photoperi1982; Mendez De La Cruz et a]., 1988). Al- od, precipitation, resource dynamics; Ota, though Taiwan is generally categorized as a sub- 1994),a simple phenotypic response to their entropical area, it does have high elevation moun- vironments (Duvall et a]., 1982), effects of phytains reaching to about 4060 m. Climatic pat- logenetic constraints (James and Shine, 1985; terns on such mountains are similar to those of Vitt, 1986; Ota, 1994), or a mixture of these factemperate regions. Recently, I demonstrated tors. Comparative studies of reproductive cycles that annual reproductive patterns in two Tai- in several species have often attempted to identify the underlying causes responsible for o b wanese high elevation lizards, Eumeces ekgans served reproductive patterns (e.g., Vitt, 1986). and Sphenomorphus taiwanensis, resemble those However, up to now, no such attempts have in temperate lizards (Huang, 1996a, 1997b). been made for the Taiwanese lizards, although The genus Takydromus consists of some 15 a number of species there have been studied species of slender, long-tailed lizards occurring (e.g., Cheng and Lin, 1977, 1978; Kato and Ota, in grassy habitats in south to east Asia (Welch 1994). This study examines reproductive cycles et a]., 1990; Ota, 1991a; Takeda and Ota, 1996). in male and female grass lizards, ir: hsuehshanenThe Snow Mountain (Hsuehshan) grass lizard, sis, and compares them with other species of Takydromus hsuehshanensis, is a poorly known Takydromus, sympatric species of different famispecies endemic to the central high altitudes lies, and ir: hsuehshanensis from different locali(2400-2950 m) of Taiwan (Lin and Cheng, ties, on the basis of data provided in previous 1990; Zhao and Adler, 1993). Except for a brief literature. description of the clutch size and incubation MATERIALS AND METHODS duration of eggs (Lin and Cheng, 1990), no information is available regarding of aspects of The study was conducted in a high elevation the reproductive biology of ir: hsuehshakensis. area at Hohuan Mountain, Hualien County

I

0 1998 by the American Society of Ichthyologistsand Herpetologists

HUANG--GRASS LIZARD REPRODUCTION

Fig. 1. Mean monthly temperature, daily photoperiod, and total monthly precipitation at Hohuan Mountain. Data are from the Hohuan weather station, Central Weather Bureau, Republic of China.

(24"101N,12"1201E),from July 1993 to December 1994. The elevation of this area is approximately 2600 m. Mean maximum air temperature, occurring from June to August, ranged from 7.9-10.1 C, and the minimum ranged from -0.7-3.3 C during December to March. Total precipitation in the study area was about 3614.5 mm in 1994, of which 1063 mm was brought by a typhoon in August. The longest sunshine duration occurred in November 1994 and the shortest in May 1994 (Fig. 1). The vegetation of the study area is mostly composed of Polygonurn cuspidaturn and Yushania niitakayamnsis. Additionally, some mosses cover rocks. Lizards were hand collected in each month. In each time period, attempts were made to collect five males and five females, but some monthly samples were smaller due to the difficultly of finding lizards in the rainy weather. Each specimen was weighed to the nearest 0.01 gram, measured for snout-vent length (SVL) to the nearest 0.1 mm, and dissected to remove the liver, fat body, and gonads and associated organs. All organs were weighed wet to the nearest 0.01 g. Stage of maturity for males was assessed by spermatogenic activity; the appearance of sperm bundles and/or free sperm in seminiferous tubules in a given specimen was regarded as indicative of its being mature. The reproductive state of adult females was determined on the basis of the presence or absence of larger vitellogenic ovarian follicles and oviductal eggs. Follicles longer than 3 mm were considered vitellogenic. Females having large vitellogenic follicles or eggs and those having neither of them were defined as reproductively active and inactive, respectively. Clutch size was estimated on the basis of the number of larger vitellogenic follicles or oviductal eggs. The time necessary for producing a clutch of eggs was estimated from the period between dates when

867

the first females with larger vitellogenic follicles and first females with oviductal eggs were collected. Clutch frequency was calculated from the estimated dates of first and last ovipositions and the estimated time necessary to produce a clutch. Females having regressed ovaries with follicles less than 3 mm in diameter were considered to be postparturient. Reproductive states of males were determined by testis mass, sexual accessory organ mass, and spermatogenic activity. The right testis and epididyrnis from each adult male were fixed in Bouin's solution, embedded in paraffin, serially sectioned at 6 pm, and stained with hematoxylin and eosin. Spermatogenetic activity was assessed qualitatively by use of Licht's (1967) system as follow: (1) seminiferous tubules involuted but filled with spermatogonia only; (2) primary spermatocytes appearing; (3) secondary spermatocytes and early spermatids abundant; (4) transforming spermatids into a few spermatozoa; (5) spermatids and spermatozoa abundant; (6) spermatozoa abundant (maximal level of spermiogenesis); and (7) spermatozoa abundant, but spermatids and spermatocytes greatly reduced. Voucher specimens are deposited at the National Museum of Natural Science, Taichung, Taiwan. The relationship between clutch size and female body size was examined using a Pearson's correlation analysis. Statistical differences were assessed by ANCOVA using SVL as the covariate. Regression analysis was performed between masses of male liver, fat body, left testis, and sexual accessory organ, as well as seminiferous tubule diameter and environmental variables. In the analyses, masses of left testis and sexual accessory organs, and seminiferous tubule diameter for each monthly sample were treated as dependent variables, whereas the climatic factors (i.e., monthly air temperature, photoperiod, and precipitation) were treated as independent variables. A probability of 0.05 or less was used to indicate statistical significance.

Takydrornus hsuehshanensis in this study were active-from March to December. ~ e c a u s ethe study site was covered with snow from January to mid-March and hit by a typhoon that closed the road in August 1994, specimen collection was severely limited during these months. A total of 183 specimens were collected [National Museum of Natural Science (NMNS) 2351, 2394, 2398, 2408-2409, 2434, 2436,2459-2460, 2466, 2529,2532,2536,2538-25391. Mean SVLs of adult males and females, 60.5 and 61.2 mm,

868

COPEIA, 1998, NO. 4

OF SNOUT-VENT LENGTH (SVL; ? SE) AND BODY MASS (BM; -C SE) OF FEMALE AND

TABLE 1. MEANVALUES MALEGRASS LIZARDS Takydromus hsuehshanensis IN CENTRAL TAIWAN.

BM (g)

SVL (mm) Sex

n

Female Male

105 78

mean

+ SE

61.2 i 0.5 60.5 i 0.6

range

54-72 47-72

respectively, did not differ from each other significantly (P > 0.05), whereas the mean body mass of adult males (5.06 g; range = 2.10-8.74 g) was significantly greater than that of adult females (4.44 g; range = 2.06-7.28 g; Table 1). Female reproductive cycle.-The smallest reproductively active female 17: hsuehshanensis measured 54 mm SVL; therefore, only females with SVL 54 mm were considered as adults. All adult females were reproductively active between April and May, 91% in June 1994, and 67% in July (Table 2). All adult females captured in August showed postparturient characteristics (Table 2). Females were nonreproductive from September to March (Table 2). The first vitellogenic females were found on 20 April and the first females with oviductal eggs b n 30 May. The interval between dates when the first females with larger vitellogenic follicles and those with oviductal eggs were 40 days: I interpret this as the approximate period -

-

mean

+ SE

4.44 ? 0.07 5.06 i 0.09

range

2.06-7.28 2.10-8.74

required for female's production of a clutch. here are two sources of evidence that females produce two clutches per reproductive season: (1) three of the 12 females collected in May 1994 still had enlarged vitellogenic follicles after having laid three eggs; and (2)the reproductive season lasts approximately 90 days, double the period of a clutch production by a female estimated above. Vitellogenesis seems to be associated with a r a ~ i dincrease in environmental temperatures (Fig. 1) and is negatively correlated with female fat body mass. Clutch size averaged 3.23 +- 0.47 (X +- SD; range = 2-4) and positively correlated with female SVL (Y = 0.0836 X - 1.8733; r = 0.45; n = 39; P = 0.005; Fig. 2). Female fat body and liver masses showedsignificant monthly "ariation (F,,,,, = 8.39, P < 0.0001 in fat body; F,,,,, = 13.54, P < 0.0001 in liver). Fat body mass was smaller during the reproductive season from April to July but increased before the dormant season from September to December (Fig. 3A). Liver mass did not fluctuate as clearlv as those of fat body mass but did show an increase before the dormant season (Fig. 3B).

OF FEMALE TABLE 2. PERCENT Takydromus hsuehshaREPRODUCTIVE STATES DURlNG DIFnensis IN DISTINCT FERENT MONTHS. n = sample size; NVF = nonvitellogenic follicles; EVF = enlarged vitellogenic follicles; Male reproductive cyck-Left testis mass showed a significant monthly variation (F,,,,, = 12.23, P OE = oviductal eggs; PP = postparturient. < 0.0001; Fig. 4A), with an increase commencing in September and a peak being reached Percent occurrence from September to December. Testicular mass Month n NVF EVF OE PP

1993 July

August

September

October

November

1994 March

April

May

June

July

September

October

November

December

Snout-vent length (rnrn)

Fig. 2. Correlation between female body size (SVL),and the number of large vitellogenic follicles (open circles) and oviductal eggs (solid circles) in Takydromus hsuehshanensis (Y = 0.0836 X - 1.8733; n = 39, r = 45; P = 0.005).

HUANG--GRASS LIZARD REPRODUCTION

J

A

S

O

1993

N

M

A

M

J

J

S

O

N

D

1994

Fig. 3. Monthly variation (mean i SE) in (A) fat body mass and (B) liver mass during the female reproductive cycle of Takydromus hsuehshanensis. Numbers above or below the values indicate sample sizes. showed a significant positive correlation with fat body mass ( r = 0.66, P < 0.05) and seminiferous tubule diameter ( r = 0.87, P < 0.05) and a significant negative cbrrelation with rainfall ( r = -0.56, P < 0.05; Table 3). The total mass of male sexual accessory organs showed a significant monthly variation (Fig. 4B), with a decrease to the lowest value from July to September and an increase to the highest value from ~ mass October to December. ~ c c e s i o rorgan showed a significant negative correlation with ambient temperatures ( r = -0.71, P < 0.05; Table 3). Male seminiferous tubule diameter = 3.50, P < showed monthly variation (F 0.001) with a high peak in September (Fig. 4C). There was a significant positive correlation between this parameter and liver mass ( r = 0.68, P < 0.05), fat body mass ( r = 0.85, P < 0.05), and photoperiod ( r = 0.61, P < 0.05). A significant negative correlation was observed between male seminiferous tubule diameter and the rainfall ( r = -0.57, P < 0.05). Male fat body mass showed significant monthly variation (F,',,,,, = 8.60, P < 0.0001; Fig. 5A), with a decrease to the lowest value from March to June and an increase to a peak in September. Male liver mass also showed significant monthly variation (F,,,,, = 10.36, P < 0.0001; Fig. 5B), with a distinct peak before the dormant month, December 1994. Histological examinations indicated that tes-

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Fig. 4. Monthly variation (mean i SE) in (A) left testis mass,(B) accessory sexual organ mass, and (C) seminiferous tubule diameter during the male reproductive cycle of Takydromus hsuehshanensis. Numbers above the values indicate sample sizes. tes were at stage 6 in all males but one in March and all but three in July 1994. These four specimens possessed testes at stage 5. The tubules of the epididymis were filled with sperm from September to the following March. This suggests that males accumulate spermatozoa in the epididymides during the winter until spring.

Temperate-zone lizards have a consistent seasonal pattern of reproduction, with oviposition in the late spring or summer months (James and Shine, 1985); and this generalization holds true for all scincid, pygopodid, gekkonid, agamid, and varanid taxa studied to date (Shine, 1985), except for some viviparous lizards which ovulate in autumn (Fitch, 1970; Guillette, 1983;

COPEIA, 1998, NO. 4

870

3. CORRELATION COEFFICIENTS (r) OF MALE LIVER MASS (MLM), MALEFATBODYm s (MFBM),MALE TABLE TESTIS WSS(MTM),MALE SEMINIFEROUS TUBULE DIAMETER (MSTD),MALEACCESSORY SEXUAL ORGAN hlASs (TEM), RAINFALL (RF), AND PHOTOPERIOD (MASO),TEMPERATURE (PHO) OF Takydromus hsuehshanasis IN CENTRAL TAIWAN. Correlation coefficients (r) were analyzed from the monthly means of those parameters. * = P < 0.05.

MLM MFBM MTM MSTD MAS0

MLM

MFBM

MTM

MSTD

MAS0

-

0.60* -

0.47 0.66* -

0.68* 0.85* 0.87* -

0.50 0.08 0.30 0.28 -

Guillette and Cruz, 1993). Present results indicate that, in female T hsuehshanensis, the reproductive period commences in spring (April) and lasts until early summer (July). This seems to fit the reproductive pattern in many temperate-zone lizards. The reproductive timing of a sympatric oviparous scincid lizard, Sphenomorphus taiwanensis, in which large vitellogenic follicles and oviductal eggs appear in late spring and early summer (May and June; Huang, 1997b), also fits the temperate-zone pattern. Similar patterns have also been reported for a viviparous scincid, S. indicus (Huang, 1996b), and an oviparous agamid, Japalura brevipes (Huang, 1997a), both occurring in high altitude areas of Taiwan.

A

S

O

N

1993

M

A

M

J

J

S

O

N

D

1994

Fig. 5. Monthly variation (mean t SE) in (A) fat body mass and (B) liver mass during the male reproductive cycle of Takydromus hsuehshanasis. Numbers above the values indicate sample sizes.

TEM

0.23 0.12 -0.71*

RF

-0.56* -0.57* 0.50

PHO

0.50 0.61* 0.13

Various studies have revealed that phylogenetic constraints have a strong influence on seasonal timing of quiescence and recrudescence of gonadal activity in a few species (e.g., Fitch, 1982; Vitt, 1986; but see Guillette and Cruz, 1993). However, the reproductive pattern in high altitude lizards in Taiwan mentioned above dies not seem to be explained on the phylogenetic grounds but is more likely to reflect the ~rimary~physiological response to environmental stimuli as in some temperate-zone lizards. In the study of relationships between absolute body size, variance in maternal size, and mean clutch size in Australian lizards, Shine and Greer (1991) made four predictions: (1) evolutionary changes in mean clutch size tend to occur concurrently with evolutionary changes in the coefficient of variation of clutch size; (2) female body size is correlated with clutch size; (3) smaller species have less variation and low mean in clutch size; and (4) invariant, low clutch size is more common in tropical species than among their temperate relatives. Clutch sizes of nine species of Takydromus (Table 4) suggest that species of the genus distributed in the tropical and subtropical regions seemingly have smaller clutches than do the temperate species. In a study of the clutch size variation in 20 populations of four Takydromus species in Japan, Takenaka (1981) also reported the presence of a positive correlation between clutch size and latitude. These results indicate that clutch size of Takydromus might be affected by environmental factors that differ in accordance with latitudinal differences. However, the primary differences among geographically s e p arated species of Takydromus appear to be associated with clutch frequency per season and perhaps time interval between clutches. For example, the clutch size of T stgnega' (2.2; Cheng, 1987) is smaller than that of T. hsuehshanensis (3.2), but clutch frequency per season is higher in the former (2-3) than in the latter (1-2).

HUANG--GRASS LIZARD REPRODUCTION TABLE4. CLUTCHSIZE(CS) OF THE CONGENER SPECIES OF Takydromus. 7: smaragdinus (TSM), 'T: sexlineatus (TSE), 7: stqnega' (TST), 'T: fmosanus (TFO), 7: hsuehshanensis (THS), 'T: septentrionalis (TSEP), 'T: tachydre moides (TTA), 7: amurensis (TAM), and 7: wolta' (TWO). n

Locally

Mean CS

Range

Sources

6 43 39 23 332 5 -

Okinawa, Japan Malaysia Lowland, Taiwan Lowland, Taiwan High Mt., Taiwan Fukien, China Saitama, Japan Tsushima, Japan Liaoning, China

2.0 2.2 2.2 3.2 3.2 3.4 5.0 5.5

2-3 1-4 2-3 2-4 1-6 1-7 4-9

Takenaka, 1989 Kopstein, 1938 Cheng, 1987 Liang and Wang, 1975 This study Pope, 1929 Telford, 1969 Takenaka, 1989 Ji et al., 1987

Species

TSM TSE TST TFO THS TSEP TTA TAM TWO

Clutch sizes of the four sympatric lizards in the central high elevation area of Taiwan show significant variations (F,,,, = 19.4, P < 0.001; ANCOVA, SVL as the covariate; Table 5). In Japalura brevipes, clutch size ( X = 5.2) is not correlated with the maternal SVL and is greater than J. swinhonis from the subtropical environment in Taiwan (mean = 4.6; previously referred as J. mitsukurii mitsukurii: see Ota, 1991b; Lin and Cheng, 1986). Likewise, clutch size of the temperate 7: hsuehshanensis (mean = 3.2) is greater than that of its subtropical congener 7: stgnegeri (mean = 2.2; Cheng and Lin, 1987). In S. taiwanensis, female SVL was the smallest (Table 5); however, the clutch size (mean = 5.22) was larger than another sympatric 7: hsuehshanensis. As such, my results suggest that the clutch size of temperate lizards tends to be larger than those of tropical and subtropical lizards (fit fourth prediction) but that the second and third predictions were not true with Taiwanese lizards. Factors affecting the clutch size of closely related species of Takydromus and sympatric high altitude Taiwanese lizards may be complex. Vitt (1981) in the study of lizard Platynotus semitaeniatus, revealed that the reproductive adaptations in animals should be understood in light of not only the competitive environments but also of the fecundity and lifetime reproductive success

of specific reproductive strategies. Furthermore, annual clutch number may also be an important fecundity parameter to be considered, since the combined number of eggs in two clutches in one species or population may be greater than the egg number in a single clutch in another one having a greater clutch size. Clutch mass is also an important factor in the analysis of investment of maternal lizard (Huang, 1996b). The present study indicates that the environments may be the major factors that regulate the clutch size of Takydromus. Nevertheless, effects of phylogenetic constraints and other factors, such as clutch frequency and clutch mass, should also be considered. Lin and Cheng (1990) described the clutch size of 7: hsuehshanensis and indicated there were two or three eggs in a clutch, which is smaller than that reported in this study of a clutch size between two and four eggs. Three kinds of explanations may be possible for such inconsistencies: (1) Lin and Cheng (1990) examined female lizards with SVLs largely smaller than those of females examined in this study; (2) populations investigated by those authors have reproductively adapted to environments that are different from those of the present p o p ulation; or (3) sample sizes vary between the two studies. The continuous spermatogenetic cycles

TABLE5. CLUTCHSIZEOF THE FOURSWPATRIC LIZARDS, Takydromus hsuehshanensis (TH), Sphenomwphus taizuanensis (ST),Japalura brevipes (JB), A N D S. indicus (SI) IN THE CENTRAL HIGHELEVATION AREA OF TAIM~AN. Clutch size

Species

TH ST

JB SI

n

mean SVL

mean 2 SE

39 9 13 24

61.3 i 3.2 57.8 ? 3.2 66.9 i 3.1 81.8 i 4.9

3.23 i 0.47 5.22 t 1.10 5.40 ? 0.43 7.27 t 1.62

range

2-4 4-8 3-7 4-1 1

Sources

This study Huang, 1997b Huang, 1997a Huang, 1996b

872

COPEIA, 1998, NO. 4

shown by T. hsuehshanensis seems to fit the pattern of most tropical lizards (Cheng, 1987), whereas the masses of testis and accessory sexual organs and seminiferous tubule diameter of this species exhibited cyclical patterns. This inclusive pattern in ?: hsuehshanensis is different from that in other high altitude lizards in Taiwan [e.g., Eumeces elegans (see Huang, 1996a), Sphenomorphus indicus (see Huang, 1996b), and S. taiwanensis (see Huang, 1997b)l. Although the female reproductive cycles are similar among most temperate-zone oviparous lizards, males exhibit a diversity of reproductively active seasons, and copulation can occur in late summer and autumn (postpartum) or in spring (preovulatory; Fitch, 1970; James and Shine, 1985). The large testicular mass of ?: hsuehshanensis before the dormant months (Sept. to Dec.) has been shown to correlate with seminiferous tubule diameter and high intensity of spermiogenesis. Such phenomena were also o b served in the temperate lizard, Eumeces elegans (Huang, 1996a) and some tropical lizards [e.g., Sceloporus orcutti (see Mayhew, 1963), Amphibolurus isolepis (see Pianka, 1971)l. Thus, it is possible that testicular size correlates with spermiogenesis in most temperate and tropical lizards. Sperm storage is a common phenomenon in temperate-zone reptiles (Cuellar, 1966; James and Shine, 1985). The enlargement of the testes and accessory organ of T hsuehshanensis correlates with the presence of sperm in the epididymes from September to the following March. Successful reproduction seems to be ensured by storage of spermatozoa in the epididymes until the occurrence of ovulation in females in the following spring. Stored lipids may be used for winter dormancy and/or reproduction (Derickson, 1976). In T hsuehshanensis females, fat body and liver masses are large from September to December. This suggests that energy is accumulated during this period for use in the inactive months. Small fat body mass in the reproductive season from April to July indicates that the energy was used for reproductive activities, such as vitellogenesis and/or egg laying. A similar pattern of fat body and liver fluctuations were also observed in males in which low values occurred in the reproductive season and high values occurred before the dormant months.

I thank H. Ota for valuable discussion; R. G. Bowker, W. E. Cooper, H. Ota, R. Shine, S. Takenaka, L. Vitt, and two anonymous reviewers for critical reading of the manuscript and helpful

comments; and C. S. Chang for assistance with fieldwork. I am also indebted to Taroko National Park for permission to sample within the park. Sincere thanks also go to Y. B. Huang for assistance with graphics. Thanks go to S. J. Wei, L. M. Huang, S. Y. Chen, K. H. Chuang, and Y. F. Huan for their assistance in the laboratory. Financial support was provided by the National Museum of Natural Science, Taichung, Taiwan, Republic of China.

CHENG, H. Y. 1987. A review on annual reproductive and energetic patterns of five taxa of lizards in Taiwan for ten years. Proc. Nat. Sci. Counc. Pt. B: Life Sci. 11:313-321. , AND J. Y. LIN. 1977. Comparative reproductive biology of the lizard, ,\apalura swinhonis form* sensis, ~akjdromus septentnonalis and ~emidactylus frenatus in Taiwan. I . Male reproductive cycles. Bull. Inst. Zool., Acad. Sin. (Taipei) 16:107-120. , AND . 1978. Comparative reproductive biology of the lizard, Japalura swinhonis fmosensis, Takydromus septentnonalis and Hemidactylus frenatus in Taiwan. 11. Fat body and liver cycles of the males. Ibid. 17:67-74. , AND . 1987. Annual ovarian, fat body and liver cycles of the grass lizard Takydromus stgnega' in Taiwan. Zool. Sci. 4:557-561. CUELLAR, 0. 1966. Oviductal anatomy and sperm storage structures in lizards.J. Morph. 119:7-19. W. K. 1976. Lipid storage and utilization DERICKSON, in reptiles. Am. Zool. 16:711-723. D., L. J. GUILLETTE 1982. DL'VALL, JR.,AND R. E. JONES. Environmental control of reptilian reproductive cycles, p. 201-231. In: Biology of the Reptilia. C. Gans and F. H. Pough (eds.).Academic Press, London. FITCH, H. S. 1970. Reproductive cycles in lizards and snakes. Univ. Kans. Mus. Nat. Hist. Misc. Publ. 52: 1-247. . 1982. Reproductive cycles in tropical reptiles. Occ. Pap. Mus. Nat. Hist. Univ. Kans. 96:l-53. L. J., JR. 1983. Notes concerning reproGUILLETTE, duction of the montane skink, Eumeces cop; J. Herpetol. 14:143-147. , AND F. R. MUNDEZDE LA CRUZ.1993. The reproductive cycle of the viviparous Mexican lizard Sceloporus torquatus. Ibid. 27:168-1 74. W. S. 1996a. The male reproductive cycle of HUANG, the skink Eumeces elegans (Squamata: Scincidae) from the central high altitude area of Taiwan. Bull. Natl. Mus. Nat. Sci. 7:99-106. . 1996b. Reproductive cycles and sexual dimorphism in the viviparous skink, Sphenomo?phusindicus (Sauria: Scincidae) from Wushe, central Taiwan. Zool. Stud. 35:55-61. . 1997a. Reproductive cycle of the oviparous lizard Japalura hmipes (Agamidae: Reptilia) in Taiwan, Republic of China. J. Herpetol. 31:22-29. . 1997b. Reproductive cycle of the skink,

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mail: [email protected]. Submitted: 28 July 1997. Accepted: 14 May 1998.

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You have printed the following article: Reproductive Cycles of the Grass Lizard, Takydromus hsuehshanensis, with Comments on Reproductive Patterns of Lizards from the Central High Elevation Area of Taiwan Wen-San Huang Copeia, Vol. 1998, No. 4. (Dec. 30, 1998), pp. 866-873. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819981230%293%3A1998%3A4%3C866%3ARCOTGL%3E2.0.CO%3B2-6

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Literature Cited Reproduction in the Granite Spiny Lizard, Sceloporus orcutti Wilbur W. Mayhew Copeia, Vol. 1963, No. 1. (Mar. 30, 1963), pp. 144-152. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819630330%293%3A1963%3A1%3C144%3ARITGSL%3E2.0.CO%3B2-L

Ecology of the Agamid Lizard Amphibolurus isolepis in Western Australia Eric R. Pianka Copeia, Vol. 1971, No. 3. (Sep. 3, 1971), pp. 527-536. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819710903%293%3A1971%3A3%3C527%3AEOTALA%3E2.0.CO%3B2-E

Why are Clutch Sizes More Variable in Some Species than in Others? Richard Shine; Allen E. Greer Evolution, Vol. 45, No. 7. (Nov., 1991), pp. 1696-1706. Stable URL: http://links.jstor.org/sici?sici=0014-3820%28199111%2945%3A7%3C1696%3AWACSMV%3E2.0.CO%3B2-%23

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The Ovarian Cycle, Reproductive Potential, and Structure in a Population of the Japanese Lacertid Takydromus tachydromoides Sam R. Telford, Jr. Copeia, Vol. 1969, No. 3. (Aug. 29, 1969), pp. 548-567. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819690829%293%3A1969%3A3%3C548%3ATOCRPA%3E2.0.CO%3B2-K

Reproductive Tactics of Sympatric Gekkonid Lizards with a Comment on the Evolutionary and Ecological Consequences of Invariant Clutch Size Laurie J. Vitt Copeia, Vol. 1986, No. 3. (Aug. 4, 1986), pp. 773-786. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819860804%293%3A1986%3A3%3C773%3ARTOSGL%3E2.0.CO%3B2-K