Southwestern Association of Naturalists

Reproductive Biology of the Lizard "Eumeces Copei" (Lacertilia: Scincidae) from the Eje Neovolcanico, Mexico Author(s): Aurelio Ramirez-Bautista, Louis J. Guillette Jr., Guadalupe Gutierrez-Mayen and Zeferino Uribe-Pea Reviewed work(s): Source: The Southwestern Naturalist, Vol. 41, No. 2 (Jun., 1996), pp. 103-110 Published by: Southwestern Association of Naturalists Stable URL: http://www.jstor.org/stable/30055091 . Accessed: 08/05/2012 22:35
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.

Southwestern Association of Naturalists is collaborating with JSTOR to digitize, preserve and extend access to The Southwestern Naturalist.

http://www.jstor.org

41(2):103-110 THESOUTHWESTERN NATURALIST

JUNE 1996

REPRODUCTIVE BIOLOGY OF THE LIZARD EUMECES COPEI (LACERTILIA: SCINCIDAE) FROM THE EJE NEOVOLCANICO, MEXICO
AURELIO RAMIREZ-BAUTISTA,
GUADALUPE GUTIERREZ-MAYEN

Louis

J.

GUILLETTE, JR.,

AND ZEFERINO URIBE-PEJA

Laboratoriode Herpetologia, Departamento de Zoologia, Instituto de Biologia, UNAM A.P. 70-153 C.U., 04510, Mexico 20, Distrito Federal, Mexico, (AR-B and ZU-P) Department of Zoology, University of Florida, Gainesville, Florida 32611, USA (LJG) Escuela de Biologia, Universidad Autonoma de Puebla, 4 sur # 104, Edificio Carolino, 72000, Puebla, Pue (GG-M) ABSTRACT-The reproductive biology of the viviparous Scincid lizard, Eumeces copei, from high elevation sites in the Eje Neovolcinico was studied. The species exhibits a pattern of asynchronous gonadal activity, with males showing maximal testicular volume during the spring and summer, and females beginning vitellogenesis in August and ovulating in late autumn. Courtship and mating occur in the summer. The development of embryos occurs during the winter with births in late spring. This reproductive pattern is common in other montane Mexican lizards. Individuals reach sexual maturity after a year. Clutch size, as determined from counts of vitellogenic follicles, was significantly different from the clutch size obtained by counting embryos in utero. A correlation between actual clutch size and snout-vent length (SVL) of females was found. Males exhibited a significantly smaller SVL than females. RESUMEN-Se estudi6 la biologia reproductive de la especie escincida vivipara Eumeces copei de sitios de elevaciones altas para el Eje Neovolcanico. Esta especie presenta un patr6n de actividad gonadal asincr6nica, con el desarrollo maximo de volumen testicular de los machos durante la primavera y el verano, y la vitelog6nesis de las hembras empezando en agosto, con la ovulaci6n al final del otofio. El cortejo y apareamiento ocurren en el verano. El desarrollo de los embriones sucede durante el invierno con nacimientos tardios en la primavera. Este patr6n de actividad es comun en las especies de Mexico que habitan las montafias. El periodo en el que los individuos alcanzaron la madurez sexual fue mayor de un afio. El tamafio de la camada, determinado por el conteo de los foliculos vitelog6nicos fue significativamente diferente del tamaio de la camada obtenido por el conteo de los embriones en el itero. Se encontr6 una correlaci6n entre el tamafio de su camada y la longitud hocicocloaca (LHC) de la hembra. Los machos presentaron una LHC significativamente menor que la de las hembras.

Even though our knowledge of the reproductive patterns of tropical and temperate lizards has increased notably in recent years (Fitch, 1982; Licht, 1984; Ramirez-Bautista et al., 1995), information for many reptilian species is still anecdotal. Fitch's (1970) monumental review synthesized the majority of the data available at that time and established the foundation for future work on the reproductive biology of lizards. Most detailed studies on reproduction in tropical and temperate lizards have been done on oviparous iguanids, anguids, teiids, scincids and agamids

(Fitch, 1970, 1982). Among scincids, Eumeces is a diverse genus, inhabiting the temperate regions of the Northern Hemisphere of both the New and Old World (Taylor, 1935). Of the 16 species examined by Fitch (1970), most are oviparous. However, several montane species, Eumeces dicei (Axtell, 1960), E. lynxe (Werler, 1949), and E. copei (Guillette, 1983), are viviparous. The reproductive cycles of several oviparous Eumeces species are well known. In general, reproductive activity occurs in spring (Fitch, 1970; Hall, 1971; Vitt and Cooper, 1986). That is,

104

The Southwestern

Naturalist

vol. 41, no. 2

gonadogenesis, courtship, ovulation, fertilization and oviposition all occur during spring and early summer. Many of these oviparous females remain with the eggs in the nest throughout the incubation period (Shine, 1988; Somma, 1990). In contrast to the above pattern, the red-tailed skink (E. egregius) of the southeastern United States exhibits fall mating (Mount, 1963). The onset of gonadal activity, ovulation and fertilization occurs during September and October; oviposition is initiated during April, followed by a 31- to 51day incubation period. Relatively little is known of the reproductive biology of the viviparous species of Eumeces, although some observations on reproduction have been reported for all three species: E. dicei (Axtell, 1960), E. lynxe (Werler, 1949, 1951) and E. copei (Guillette, 1983). Axtell (1960) observed that E. dicei females contained large, well-developed embryos in early July, whereas Werler (1951) captured two gravid female E. lynxe in January which gave birth in March; these data suggest the possibility of fall or very early spring gestation and birthing. A preliminary report on the reproduction of E. copei, a Mexican species of montane habitats (Guillette, 1983), indicated that this is a viviparous species with fall mating and gestation. We describe in detail the female and male reproductive cycle of the montane lizard Eumeces copei. In particular, we examine the relationship between clutch size and snout-vent length of females, growth of neonates after hatching, and sexual dimorphism in adults.

varies between 11C and 19C, with a range in mean annual precipitation from 800 mm to 1,200 mm (Garcia, 1981). Animals collected during our field work were killed and preserved in 10% neutral buffered formalin. Initial data obtained from each animal consisted of snout-vent length (SVL) and date of capture. Following fixation, females were examined to determine the stage of follicular development (nonvitellogenic, vitellogenic, or luteal) and the presence or absence of eggs in utero. The following, if present, were recorded: diameter and number of follicles in the ovary, number of eggs in each oviduct, and presence and number of corpora lutea. For males, length and width of testes were recorded. Length and width of testes and follicles were used to obtain testicular and follicular volume (V) as calculated using the formula for the volume of an ellipsoid: V = 4/37ra2b where "a" is 1/2 the shortest diameter and "b" is 1/2 the longest diameter. These counts and measurements were tabulated to obtain monthly means and standard errors. One-way ANOVA was performed to determine significant overall differences among monthly values and Scheffe's pairwise post-hoc tests were used to identify homogeneous subgroups of months. Pearson's product-moment correlation coefficients were calculated for the relationship between litter size and SVL of females, and between gonadal activity and environmental conditions in both sexes. The smallest female containing enlarged vitellogenic follicles or oviductal eggs was used to indicate the minimum SVL at maturity; enlarged testes were used in males. We used a probability equal to or less than 0.05 to indicate statistical significance. RESULTS-The reproductive cycle of males (n = 100) and females (n = 110) of Eumeces copei is shown in Fig. 1. Males exhibited significant increases in testicular activity in early April, with peak testicular volume occurring from May to August (F = 8.30, d.f. = 8,99, P < 0.001; Fig. 1). Lack of data for September and October did not allow a determination of the exact onset of testicular regression, but by November males had regressed testes. Testicular growth was positively correlated with increasing precipitation (r = 0.86, P < 0.05), but not photoperiod (r = 0.35, P > 0.05) or temperature (r = 0.22, P > 0.05). Of 100 adult male E. copei, 81 specimens collected between April and August showed evidence of reproductive activity. Mean SVL (1 SE) for the adult male population was 58.62 0.63 mm (45.0 to 73.0 mm). The reproductive cycle and changes in follic-

AND METHODS-The majority of the MATERIALS specimens analyzed were obtained on loan from the Museum of Zoology, University of Michigan, USA, and Museum of Natural History, University of Illinois, USA, through the courtesy of the curators of herpetology. The remaining lizards were collected from several sites in the transvolcanic mountains (Eje Neovolcanico) of the Mexican states of Mexico and Distrito Federal. Specific localities were: (1) Zoquiapan (19* 12'30"N, 98* 42'30"W), (2) Cahuacan (19037'7"N, 99*24'6"W), and (3) Ajusco (1917'10"N, 98013'40"W) between elevations of 2,600 and 3,100 m. Two hundred and sixty one lizards were examined of which 110 were females, 100 males, 36 juveniles and 15 neonates. In the mountains of the Eje Neovolcanico, the prevailing climate is humid temperate with rain in summer. However, some localities are classified as subhumid temperate. Zoquiapan is the most humid whereas Cahuacan is the least; mean annual temperature

June 1996

Ramirez-Bautista et al.-Reproductive

biology of Eumeces copei

105

ular volume of females are shown also in Fig. 1. Female E. copei did not exhibit a spring period of gonadal activity as occurs in oviparous species of this genus (Fitch, 1970). Follicular volume did not begin to increase until August, with a maximal follicular volume between September and
April (F = 24.14, df = 9,92, P < 0.001). Vitel-

350 300 VOLUME FOLLICULAR mm3

50 mm3 VOLUME TESTICULAR 40

250 200 150 100 10 30

logenesis and follicular growth were negatively correlated with decreasing ambient photoperiod (r = -0.793, P < 0.05); no relationship between ovarian activity and temperature (r = -0.54, P
> 0.05) or rainfall (r = 0.36, P > 0.05) was

20

50 0 J F M A M J J A MONTHS S O N D
0

noted. Mating and courtship behavior was observed in the field from June to August; no mating or courtship behavior was noted after this period. Ovulation occurred during early September, with pregnancy throughout the fall, winter and spring. Vitellogenic follicles were observed in the ovaries during August, September, October, November, maybe December, January, March, and April, whereas nonvitellogenic follicles and/or embryos were present during the rest of the year (Fig. 2). The fertilization of ovulated eggs in the autumn was apparently by sperm stored in the female reproductive tract. Embryonic development occurred throughout the winter and early spring with the majority of births occurring from late May to July. Neonates were collected frequently between 28 May and 30 July, with only two young collected in August. Of the females examined which were collected between September and November, the majority had vitellogenic follicles and a mean (1 SE) SVL of 63.0 1.98 mm (55.0 to 72.2 mm; n = 14). The females that were pregnant between September and January had a mean SVL of 65.2 2.02 mm (56.0-72.0 mm; n = 21). These data suggest that reproductive maturity was reached at a SVL of approximately 55.0 mm. ClutchSize-Estimates were made from counts of yolked follicles, oviductal eggs and embryos in the uterus. Mean clutch size determined by counts of yolked ovarian follicles was 4.35 0.51 (3 to 6; n = 14), which was significantly higher (t-test:
t = 1.82, d.f. = 33, P < 0.05) than the mean

FEMALES

MALES

FIG. 1-Monthly

changes in testicular and ovarian

activitythroughoutthe reproductive cycle of Eumeces copei.Data are presented mean 1 SE; within each as sex, values having different superscriptsare significantly different. in utero embryos on SVL (Fig. 3B) produced a significant positive correlation (r = 0.67, d.f. = 20; P < 0.001). Growth-Mean SVL of young at birth in May was 23.43 1.11 mm (19.5 to 26.3 mm; n = 15), whereas in August, mean length of these now juvenile lizards had increased to 31.53 1.75 mm (26.6 to 39.2 mm; n = 36; Fig. 4). Young born during the spring grew 8.1 mm in 89 days (0.091 mm/day). A third sample, obtained during November, had mean SVLs of 45.5 1.69 mm (44 to 48 mm; n = 4), or growth of 13.97 mm in 82 days (0.170 mm/day). A sample of juveniles collected in May of the following year had SVLs averaging 52.59 1.04 mm (50.3 to 55.0 mm; n = 10), that represented a gain of only 7.09 mm in 188 days (0.038 mm/day). Growth was rapid in summer, maximal in fall and suppressed during winter. Furthermore, these data support the hypothesis (Guillette, 1983) that for individuals of this species, reproductive maturity is reached after a year or more. Body Size and Sexual Dimorphism-The distribution of body size (SVL) of adults is shown in Fig. 5. The female population exhibited a mean length of 62.18 0.51 mm (55.0 to 72.2 mm; n = 110), which was larger than the mean SVL of males (58.62 0.63 mm [45.0 to 73.0 mm; n = 100]). A t-test demonstrated a significant difference (t = 4.37, d.f. = 208, P < 0.001) in size

clutch size (3.71 0.73 [2 to 6; n = 21]) obtained by counting in utero embryos. Counts of nonvitellogenic follicles, 9.88 0.69 (4 to 19; n = 75), indicate a standing reserve in the ovary of three times the number of follicles ovulated per clutch. Further, no correlation existed between the number of vitellogenic follicles and female SVL (Fig. 3A). Analysis of clutch size using the number of

between males and females, supporting the hy-

106

The Southwestern

Naturalist

vol. 41, no. 2

NON-VITELLOGENIC

VITELLOGENIC

GRAVID

100 90 80 70
PERCENT 60

50 40 30 20 10 0

MONTHS
FIG. 2-Seasonal distribution (percent) of female Eumeces copei in each of three reproductive states.

pothesis of reversed sexual size dimorphism in this species. DISCUSSION-Eumeces copei shows a reproductive cycle in which males and females exhibit asynchronous gonadal activity. Testicular recrudescence occurs in spring with maximal activity during the summer months. This pattern is similar to that observed for many temperate zone male squamates (Fitch, 1970; Duvall et al., 1982; Licht, 1984). In contrast, ovarian activity of females did not begin until late summer with ovulation, fertilization and pregnancy in fall and winter. Fall ovarian activity is common for many Mexican viviparous lizards and occurs in representatives of three squamate families: Phry-

nosomatidae (Guillette and Casas-Andreu, 1980; Ortega and Barbault, 1984; Guillette and Sullivan, 1985; Feria, 1986; Guillette and Bearce, 1986; Mendez de la Cruz et al., 1988), Scincidae (Guillette, 1983), and Anguidae (Guillette and Casas-Andreu, 1987). This reproductive pattern may be due to the phylogenetic inheritance of an ancestral pattern as fall gonadal activity may be associated with the evolution of viviparity (Guillette, 1982). Although possible advantages and disadvantages of such a reproductive strategy have been discussed (Goldberg, 1971; Ballinger, 1973, 1977; Guillette and Casas-Andreu, 1980), most have not been tested in depth. Asynchrony in the onset of reproductive activity between males and females (as in E. copei),

June 1996

Ramirez-Bautista et al.-Reproductive

biology of Eumeces copei

107

Field Specimens
12 Follicles Vitellogenic 10 Museum Specimens

80

70

8 6 4 2 40 0
50 55 60 65 70 male (mm) SVL

60
female

50

75

80 30

SVL (mm)

Field Specimens Museum Specimens

20

6
Size Clutch

10

5 4 3 2 1
50 55 60 65 70

89

171

359

DAYS FIG. 4-Mean (1 SE) size of Eumeces copei

75

80

throughoutthe first year of life. Mean 1 SE (box) or range (bar) are given for adult femalesand males. gins to increase approximately two months before the onset of male testicular activity, and precipitation that increases in May leads to an increase in the availability (quality and quantity) of insects (Gutierrez and Sanchez, 1986) by the time males show gonadal recrudescence. These factors could permit males to find the thermal and nutritional condition necessary to start testicular activity. Thus, reproductive activity in males may be linked to a permissive environmental temperature and availability of an adequate food supply due to the onset of spring precipitation. Females cannot initiate the reproductive activity at the same time as males because they are pregnant at this time. Births occur between May and July, coincident with the heightened insect productivity. Thus, the offspring find an abundance of food in the environment and grow fast. The females also use this period to feed and gain energy in a short time (2 or 3 months) such that they can respond to a second cue of photoperiod during August and September, when reproductive activity starts again. Like males, reproductive activity in females has been associated with adequate nu-" trition and environmental temperature (Hahn and

SVL (mm)
FIG. 3-Correlation between (A) number of vitel-

logenic folliclesand (B) in utero embryosand female

body size (SVL) in Eumeces copei.

has been observed previously in several Mexican sceloporine lizards (Sceloporusgrammicus: Guillette and Casas-Andreu, 1980; S. t. torquatus: Feria, 1986; S. m. mucronatus:Mendez de la Cruz et al., 1988). The disparity in the onset of reproductive activity in males and females suggests that the sexes use different environment cues. Testicular activity in E. copei was positively correlated with precipitation, but not with photoperiod or ambient temperature. Female gonadal activity was correlated with decreasing ambient temperature and photoperiod. These data suggest different stimulatory agents in the sexes, but such an implication appears to run counter to experimental studies that have clearly shown that lizards cannot initiate reproductive activity without an appropriate thermal and nutritive environment (Licht, 1984, for review). At our study site ambient temperature be-

108

The SouthwesternNaturalist

vol. 41, no. 2

50

Males Females
40

Frequency 30

20

10

50

55

60

65

70

75

SVL (mm)
FIG.5-Size distribution copei. (SVL) for female and male adult Eumeces Tinkle, 1965; Licht, 1972; Greenberg and Gist, 1985). Several studies have shown that viviparous female lizards end pregnancy with minimal fat stores (Goldberg, 1972; Guillette and Casas-Andreu, 1981). This may explain why postpartum females do not respond reproductively when males do in late spring but does not account for the lack of a response in young primaparous females. Moreover, females exhibit maximal vitellogenesis between September and October when none of the environmental features we examined changed in any significant way. Thus, although our data suggested a correlation, they were not conclusive. The disparity in reproductive cyclicity implies that males and females "read" the environmental stimuli associated with reproductive activity differently, but experimental studies are needed to test this hypothesis. Species exhibiting fall reproductive activity, as well as those exhibiting asynchrony between sexes, provide important models for future work examining the mechanisms controlling seasonal cyclicity in reptiles. Sexual dimorphism is an important atribute of the reproductive strategy of some species (Trivers, 1972, 1976; Vitt and Cooper, 1986). If a correlation exists between clutch size and female body size, then body size can have a direct effect on reproductive success, suggesting that sometimes selection should favor continued growth of fe-

June 1996

Ramirez-Bautista et al.-Reproductive

biology of Eumeces copei

109

males. However, such selection for further female growth is tempered by survival probabilities at that age and males also may have selection pressures to grow larger (competition against other males). Consequently, even in many lizards species that show a positive relation between clutch size and female body size, adult males are larger. In our study we found a relationship between female clutch size and SVL as observed in many lizards species, including oviparous skinks (Fitch, 1954; Vitt and Cooper, 1985). Additionally, females had a tendency to be larger than males and reach sexual maturity at a larger size. Rapid growth of the neonates occurred during late spring and early summer, but maximal growth was in late summer and early autumn, when insect productivity is high (Gutierrez and Sanchez, 1986). During the winter months, growth rate declines, presumably due to the onset of cool winter weather. A year after birth (May), juveniles were approximately the size of males entering sexual maturation; neonates averaged 52.59 mm SVL, whereas the smallest reproductively active males were 45.0 mm SVL. Males exhibited the onset of reproductive activity in May, whereas females began reproduction in August-September. Conservatively using the smallest rate (0.038 mm/ day), derived from the growth data (Fig. 4) and applied over the interval May-August, females reaching sexual maturity in August should be 56.0 mm SVL, approximately the same size as the smallest sexually mature female (55.0 mm SVL). These data suggest that males require approximately only one year to reach sexual maturity, whereas females require a year and three months. The delay in onset of sexual maturity by three months gives the juvenile females an extra summer of growth. Fall reproductive activity allows the extra months of growth while still insuring that a reproductive season is not lost to the female. An extra summer season helps explain the observed sexual size dimorphism. The factors controlling the onset of sexual maturation in reptiles are still poorly understood, but several studies, including one examining the skink Eumeces obsoletus(Masson and Guillette, 1985), suggested that the onset of sexual maturation was due to development of the central nervous system, as the gonads of juvenile lizards were responsive to gonadotropin stimulation. We thank R. Sanchezfor his help in the field, S. F. Fox, M. Feria, and E. Naranjofor their commentson

this manuscript, F. Villegas for his help with graphics, O. Flores (MZUNAM), and the curators of herpetology from MZUM and MNHUI for allowing us to specimens examine under their care, and C.O.N.A.C.Y.T. of Mexico for financial support of A.R.B. during his study at the University of Florida (U.S.A) in 1987. LITERATURECITED AXTELL, W. 1960. A new subspecies of Eumeces R. dicei from Sierra Madre of Northeastern Mexico. Copeia 1960:19-26. BALLINGER, 1973. Comparative demography of R. two viviparous lizards (Sceloporusjarrovi and Sceloporuspoinsetti). Ecology 54:269-283. BALLINGER, 1977. Reproductive strategies: food R. availability as a source of proximal variation in a lizard. Ecology 58:628-645. DUVALL, D., L. J. GUILLETTE, JR., AND R. E. JONES. 1982. Environmental control of reptilian reproductive cycle. Pp. 201-231, in Biology of the Reptilia, Vol. 13. (C. Gans and F. H. Pough, eds.). Academic Press, New York. FERIA,O. M. 1986. Contribuci6n al conocimiento del ciclo de vida de Sceloporus torquatus torquatus (Lacertilia: Iguanidae) al sur del Valle de Mexico. Unpubl. tesis de Licenciatura. Escuela Nacional de Estudios Profesionales, Zaragoza, Universidad Nacional Aut6noma de Mexico, Mexico, 54 pp. FITCH, H. S. 1954. Life history and ecology of the five-linked skink, Eumeces fasciatus. University of Kansas Publications, Museum of Natural History 8:1-156. FITCH, H. S. 1970. Reproductive cycles of lizards and snakes. University of Kansas Museum of Natural History Miscellaneous Publications 52:1-247. FITCH,H. S. 1982. Reproductive cycles in tropical reptiles. University of Kansas Museum of Natural History Occasional Papers 96:1-53. E. GARCIA, 1981. Modificaciones al sistema de clasificaci6n de Kippen. Third ed. Instituto de Geografia, Universidad Nacional Aut6noma de M6xico, Mexico. S. GOLDBERG, R. 1971. Reproductive cycle of the ovoviviparous iguanid lizard Sceloporus jarrovi Cope. Herpetologica 27:123-131. GOLDBERG, R. 1972. Seasonal weight and cytoS. logical changes in the fat bodies and liver of the iguanid lizard SceloporusjarroviCope. Copeia 1972: 227-232. GREENBERG, S., ANDD. H. GIST. 1985. Fat bodies D. and reproduction in female Anolis carolinensis. Journal of Experimental Zoology 223:277-283. L. GUILLETTE, J., JR. 1982. The evolution of viviparity and placentation in the high elevation Mexican lizard Sceloporusaeneus. Herpetologica 38:94103.

110

The Southwestern Naturalist

vol. 41, no. 2

L. GUILLETTE, J., JR. 1983. Notes concerning reproduction of the montane skink, Eumeces copei. Journal of Herpetology 17:144-148. L. GUILLETTE, J. JR., ANDD. A. BEARCE.1986. Reproductive and fatbody cycle in the lizard, Sceloporus grammicus disparilis. Transactions of the Kansas Academy of Science 89:31-39.
GUILLETTE, L.

MENDEZ-DELA CRUZ,F. R., L. J. GUILLETTE, JR.,

M. VILLAGRAN, AND G. CASAS-ANDREU. 1988.

J.

JR., AND CASAS-ANDREU.

1980.

Reproductive and fat body cycles of the viviparous lizard, Sceloporus mucronatus (Sauria: Iguanidae). Journal of Herpetology 22:1-22. MOUNT,R. H. 1963. The natural history of the redtailed skink, Eumeces egregius Baird. American Midland Naturalist 70:356-385.
ORTEGA, A., AND R. BARBAULT. 1984. Reproductive

Fall reproductive activity in the high altitude Mexican lizard, Sceloporus grammicus microlepidotus. Journal of Herpetology 14:143-147. GUILLETTE, J. JR., AND CASAS-ANDREU.1981. L. Seasonal variation in fat body weights of the Mexican high elevation lizards Sceloporusgrammicus microlepidotus. Journal of Herpetology 15:366-371. GUILLETTE, J. JR., AND CASAS-ANDREU.1987. L. The reproductive biology of the high elevation Mexican lizard, Barisia imbricata.Herpetologica 43: 229-38. L. GUILLETTE, J. JR., AND W. P. SULLIVAN. 1985. Reproductive and fatbody cycles of the lizard, Sceloporusformosus. Journal of Herpetology 19:474480. M. GUTIERREZ MA. G., ANDR. SANCHEZ.1986. Repartici6n de los recursos alimenticios en la comunidad de lacertilios de Cahuacin, Edo. de Mexico. Unpubl. tesis Licenciatura, Escuela Nacional de Estudios Profesionales, Iztacala, Universidad Nacional Aut6noma de Mexico, Mexico, 177 pp. HAHN, W. E., AND D. W. TINKLE. 1965. Fat body cycling and experimental evidence for its adaptive significance to ovarian follicle development in the lizard Uta stansburiana. Journal of Experimental Zoology 158:79-86. HALL, R. J. 1971. Ecology of a population of the great plains skink (Eumeces obsoletus). University of Kansas Science Bulletin 49:359-387. LIGHT,P. 1972. Environmental physiology of reptilian breeding cycles: roles of temperature. General Comparative Endocrinology Supplement 3:477-488. P. LIGHT, 1984. Reptiles. Pp. 206-282, in Marshall's physiology of reproduction. Fourth ed., Vol. 1. (G. E. Lamming, ed.). Churchill Livingstone, Edinburgh. MASSON,G. R., AND L. J. GUILLETTE, JR. 1985. FSH-induced gonadal development in juvenile lizards, Eumeces oboletus. Journal of Experimental Zoology 236:343-351.

cycles in the mesquite lizard, Sceloporusgrammicus. Journal of Herpetology 18:168-175. RAMIREZ-BAUTISTA, Z. URIBE-PE A, AND L. J. A., GUILLETTE, JR. 1995. Reproductive biology of the lizard Urosaurusbicarinatus bicarinatus (Reptilia: Phrynosomatidae) from Rio Balsas Basin, Mexico. Herpetologica 51:24-33. SHINE,R. 1988. Parental care in reptiles. Pp. 275329, in Biology of the Reptilia, Vol. 16. (C. Gans and R. Huey, eds.). Alan R. Liss, New York. L. SOMMA, A. 1990. A. categorizaction and bibliographic survey of parental behavior in lepidosaurian reptiles. Smithsonian Herpetological Information Service 81:1-53. E. TAYLOR, H. 1935. A taxonomic study of the cosmopolitan scincoid lizards of the genus Eumeces. University of Kansas Science Bulletin 23:1-643. TRIVERS, L. 1972. Parental investment and sexual R. selection. Pp. 136-175, in Sexual selection and the descent of man (B. G. Campbell, ed.). Aldine, Chicago. TRIVERS, L. 1976. Sexual selection and resourceR. accruing abilities in Anolis garmani. Evolution 30: 253-269. VITT, L. J., AND W. E. COOPER. 1985. The relationship between reproduction and lipid cycling in the skink Eumeces laticeps with comments on brooding ecology. Herpetologica 4:419-432. VITT, L. J., AND W. E. COOPER. 1986. Skink reproduction and sexual dimorphism: Eumecesfasciatus in the southeastern United State, with notes on Eumeces inexpectatus. Journal of Herpetology 20: 65-76. J. WERLER, E. 1949. Reproduction of captive Texas and Mexican lizards. Herpetologica 5:67-70. WERLER, E. 1951. Miscellaneous notes on the eggs J. and young of Texan and Mexican reptiles. Zoologica 36:37-55.