reproductive biology of the lizard eumeces copei

7/31/2019 Reproductive Biology of the Lizard Eumeces Copei

1/9

Southwestern Association of Naturalists

Reproductive Biology of the Lizard "Eumeces Copei" (Lacertilia: Scincidae) from the EjeNeovolcanico, MexicoAuthor(s): Aurelio Ramirez-Bautista, Louis J. Guillette Jr., Guadalupe Gutierrez-Mayen andZeferino Uribe-PeaReviewed work(s):Source: The Southwestern Naturalist, Vol. 41, No. 2 (Jun., 1996), pp. 103-110Published by: Southwestern Association of NaturalistsStable 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 [email protected].

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

The Southwestern Naturalist.

http://www.jstor.org
http://www.jstor.org/action/showPublisher?publisherCode=swanhttp://www.jstor.org/stable/30055091?origin=JSTOR-pdfhttp://www.jstor.org/page/info/about/policies/terms.jsphttp://www.jstor.org/page/info/about/policies/terms.jsphttp://www.jstor.org/stable/30055091?origin=JSTOR-pdfhttp://www.jstor.org/action/showPublisher?publisherCode=swan


2/9

REPRODUCTIVE BIOLOGY OF THE LIZARDEUMECES COPEI (LACERTILIA: SCINCIDAE)FROM THE EJE NEOVOLCANICO, MEXICOAURELIO RAMIREZ-BAUTISTA, Louis J. GUILLETTE, JR.,

GUADALUPE GUTIERREZ-MAYEN AND ZEFERINO URIBE-PEJA

Laboratoriode Herpetologia, Departamentode Zoologia, Instituto de Biologia,UNAM A.P. 70-153 C.U., 04510, Mexico 20, Distrito Federal, Mexico, (AR-B and ZU-P)

Departmentof Zoology, Universityof Florida, Gainesville, Florida 32611, USA (LJG)Escuela de Biologia, UniversidadAutonomade Puebla, 4 sur # 104,Edificio Carolino, 72000, Puebla, Pue (GG-M)

ABSTRACT-The reproductive biology of the viviparous Scincid lizard, Eumeces copei, from highelevation sites in the Eje Neovolcinico was studied. The species exhibits a pattern of asynchronousgonadal activity, with males showing maximal testicular volume during the spring and summer, andfemales beginning vitellogenesis in August and ovulating in late autumn. Courtship and mating occurin the summer. The development of embryos occurs during the winter with births in late spring. Thisreproductive pattern is common in other montane Mexican lizards. Individuals reach sexual maturityafter a year. Clutch size, as determined from counts of vitellogenic follicles, was significantly differentfrom the clutch size obtained by counting embryos in utero. A correlation between actual clutch sizeand snout-vent length (SVL) of females was found. Males exhibited a significantly smaller SVL thanfemales.

RESUMEN-Se estudi6 la biologia reproductive de la especie escincida vivipara Eumeces copei desitios de elevaciones altas para el Eje Neovolcanico. Esta especie presenta un patr6n de actividadgonadal asincr6nica, con el desarrollo maximo de volumen testicular de los machos durante la primaveray 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 elinvierno con nacimientos tardios en la primavera. Este patr6n de actividad es comun en las especiesde Mexico que habitan las montafias. El periodo en el que los individuos alcanzaron la madurezsexual fue mayor de un afio. El tamafio de la camada, determinado por el conteo de los foliculosvitelog6nicos fue significativamente diferente del tamaio de la camada obtenido por el conteo de losembriones en el itero. Se encontr6 una correlaci6n entre el tamafio de su camada y la longitud hocico-cloaca (LHC) de la hembra. Los machos presentaron una LHC significativamente menor que la delas hembras.

Even though our knowledge of the reproductivepatterns of tropical and temperate lizards hasincreased notably in recent years (Fitch, 1982;Licht, 1984; Ramirez-Bautista et al., 1995), in-formation for many reptilian species is still an-ecdotal. Fitch's (1970) monumental review syn-thesized the majority of the data available at thattime and established the foundation for futurework on the reproductive biology of lizards. Mostdetailed studies on reproduction in tropical andtemperate lizards have been done on oviparousiguanids, anguids, teiids, scincids and agamids

(Fitch, 1970, 1982). Among scincids, Eumeces isa diverse genus, inhabiting the temperate regionsof the Northern Hemisphere of both the Newand Old World (Taylor, 1935). Of the 16 speciesexamined by Fitch (1970), most are oviparous.However, several montane species, Eumecesdicei(Axtell, 1960), E. lynxe (Werler, 1949), and E.copei (Guillette, 1983), are viviparous.

The reproductive cycles of several oviparousEumeces species are well known. In general, re-productive activity occurs in spring (Fitch, 1970;Hall, 1971; Vitt and Cooper, 1986). That is,

THESOUTHWESTERNATURALIST1(2):103-110 JUNE 1996


3/9

The Southwestern Naturalist

gonadogenesis, courtship, ovulation, fertilizationand oviposition all occur during spring and earlysummer. Many of these oviparous females remainwith the eggs in the nest throughout the incu-bation period (Shine, 1988; Somma, 1990). Incontrast to the above pattern, the red-tailed skink(E. egregius) of the southeastern United Statesexhibits fall mating (Mount, 1963). The onset ofgonadal activity, ovulation and fertilization oc-curs during September and October; ovipositionis initiated during April, followed by a 31- to 51-day incubation period.

Relatively little is known of the reproductivebiology of the viviparous species of Eumeces, al-though some observations on reproduction havebeen reported for all three species: E. dicei (Ax-tell, 1960), E. lynxe (Werler, 1949, 1951) and E.copei (Guillette, 1983). Axtell (1960) observedthat E. dicei females contained large, well-devel-oped embryos in early July, whereas Werler(1951) captured two gravid female E. lynxe inJanuary which gave birth in March; these datasuggest the possibility of fall or very early springgestation and birthing. A preliminary report onthe reproduction of E. copei, a Mexican speciesof montane habitats (Guillette, 1983), indicatedthat this is a viviparous species with fall matingand gestation.

We describe in detail the female and male re-productive cycle of the montane lizard Eumecescopei. In particular, we examine the relationshipbetween clutch size and snout-vent length of fe-males, growth of neonates after hatching, andsexual dimorphism in adults.

MATERIALS ND METHODS-The majority of thespecimens analyzed were obtained on loan from theMuseum of Zoology, University of Michigan, USA,and Museum of Natural History, University of Illinois,USA, through the courtesy of the curators of herpe-tology. The remaining lizards were collected from sev-eral sites in the transvolcanic mountains (Eje Neovol-canico) of the Mexican states of Mexico and DistritoFederal. 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 hundredand sixty one lizards were examined of which 110 werefemales, 100 males, 36 juveniles and 15 neonates.In the mountains of the Eje Neovolcanico, the pre-vailing climate is humid temperate with rain in sum-mer. However, some localities are classified as sub-humid temperate. Zoquiapan is the most humid where-as Cahuacan is the least; mean annual temperature

varies between 11C and 19C, with a range in meanannual precipitation from 800 mm to 1,200 mm (Gar-cia, 1981).

Animals collected during our field work were killedand preserved in 10%neutral buffered formalin. Initialdata obtained from each animal consisted of snout-ventlength (SVL) and date of capture. Following fixation,females were examined to determine the stage of fol-licular development (nonvitellogenic, vitellogenic, orluteal) and the presence or absence of eggs in utero.The following, if present, were recorded:diameter andnumber of follicles in the ovary, number of eggs ineach oviduct, and presence and number of corpora lu-tea. For males, length and width of testes were re-corded. Length and width of testes and follicles wereused to obtain testicular and follicular volume (V) ascalculated using the formula for the volume of an el-lipsoid:

V = 4/37ra2bwhere "a" is 1/2 the shortest diameter and "b" is 1/2the longest diameter.

These counts and measurements were tabulated toobtain monthly means and standard errors. One-wayANOVA was performed to determine significant over-all differences among monthly values and Scheffe'spairwise post-hoc tests were used to identify homo-geneous subgroups of months. Pearson's product-mo-ment correlation coefficients were calculated for therelationship between litter size and SVL of females,and between gonadal activity and environmental con-ditions in both sexes. The smallest female containingenlarged vitellogenic follicles or oviductal eggs was usedto indicate the minimum SVL at maturity; enlargedtestes were used in males. We used a probability equalto or less than 0.05 to indicate statistical significance.

RESULTS-The reproductive cycle of males (n= 100) and females (n = 110) of Eumeces copeiis shown in Fig. 1. Males exhibited significantincreases in testicular activity in early April, withpeak testicular volume occurring from May toAugust (F = 8.30, d.f. = 8,99, P < 0.001; Fig.1). Lack of data for September and October didnot allow a determination of the exact onset oftesticular regression, but by November males hadregressed testes. Testicular growth was positivelycorrelated 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). Of100 adult male E. copei, 81 specimens collectedbetween April and August showed evidence ofreproductive activity. Mean SVL (1 SE) for theadult male population was 58.62 0.63 mm(45.0 to 73.0 mm).

The reproductive cycle and changes in follic-

104 vol. 41, no. 2


4/9

Ramirez-Bautista et al.-Reproductive biology of Eumeces copei

ular volume of females are shown also in Fig. 1.Female E. copei did not exhibit a spring periodof gonadal activity as occurs in oviparous speciesof this genus (Fitch, 1970). Follicular volume didnot begin to increase until August, with a max-imal follicular volume between September andApril (F = 24.14, df = 9,92, P < 0.001). Vitel-logenesis and follicular growth were negativelycorrelated with decreasing ambient photoperiod(r = -0.793, P < 0.05); no relationship betweenovarian activity and temperature (r = -0.54, P> 0.05) or rainfall (r = 0.36, P > 0.05) wasnoted. Mating and courtship behavior was ob-servedin the field fromJune to August; no matingor courtship behavior was noted after this period.Ovulation occurredduring early September, withpregnancy throughout the fall, winter and spring.Vitellogenic follicles were observed in the ovariesduring August, September, October, November,maybe December, January, March, and April,whereas nonvitellogenic follicles and/or embryoswere present during the rest of the year (Fig. 2).The fertilization of ovulated eggs in the autumnwas apparently by sperm stored in the femalereproductive tract. Embryonic development oc-curred throughout the winter and early springwith the majority of births occurring from lateMay to July. Neonates were collected frequentlybetween 28 May and 30 July, with only twoyoung collected in August.Of the females examined which were collectedbetween September and November, the majorityhad 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 betweenSeptember and January had a mean SVL of 65.2 2.02 mm (56.0-72.0 mm; n = 21). These datasuggest that reproductive maturity was reachedat a SVL of approximately 55.0 mm.ClutchSize-Estimates were made from countsof yolked follicles, oviductal eggs and embryos inthe uterus. Mean clutch size determined by countsof yolked ovarian follicles was 4.35 0.51 (3 to6; n = 14), which was significantly higher (t-test:t = 1.82, d.f. = 33, P < 0.05) than the meanclutch size (3.71 0.73 [2 to 6; n = 21]) obtainedby counting in utero embryos. Counts of nonvi-tellogenic follicles, 9.88 0.69 (4 to 19; n = 75),indicate a standing reserve in the ovary of threetimes the number of follicles ovulated per clutch.Further, no correlation existed between the num-ber of vitellogenic follicles and female SVL (Fig.3A). Analysis of clutch size using the number of

350300

250200150100

500

FOLLICULAROLUMEm350

40

30

20

10

0

TESTICULAROLUMEm3

J F M A M J J A S O N DMONTHS

FEMALES MALESFIG. 1-Monthly changes in testicular and ovarianactivity hroughout he reproductiveycleof Eumecescopei.Data are presented s mean 1 SE; withineachsex, values having differentsuperscriptsare signifi-cantlydifferent.

in utero embryos on SVL (Fig. 3B) produced asignificant positive correlation (r = 0.67, d.f. =20; P < 0.001).Growth-Mean SVL of young at birth in Maywas 23.43 1.11 mm (19.5 to 26.3 mm; n =15), whereas in August, mean length of these nowjuvenile lizards had increased to 31.53 1.75mm (26.6 to 39.2 mm; n = 36; Fig. 4). Youngborn during the spring grew 8.1 mm in 89 days(0.091 mm/day). A third sample, obtained duringNovember, had mean SVLs of 45.5 1.69 mm(44 to 48 mm; n = 4), or growth of 13.97 mm in82 days (0.170 mm/day). A sample of juvenilescollected in May of the following year had SVLsaveraging 52.59 1.04 mm (50.3 to 55.0 mm;n = 10), that represented a gain of only 7.09 mmin 188 days (0.038 mm/day). Growth was rapidin summer, maximal in fall and suppressed dur-ing winter. Furthermore, these data support thehypothesis (Guillette, 1983) that for individualsof this species, reproductive maturity is reachedafter a year or more.Body Size and Sexual Dimorphism-The dis-tribution of body size (SVL) of adults is shownin Fig. 5. The female population exhibited a meanlength of 62.18 0.51 mm (55.0 to 72.2 mm; n= 110), which was larger than the mean SVL ofmales (58.62 0.63 mm [45.0 to 73.0 mm; n =100]). A t-test demonstrated a significant differ-ence (t = 4.37, d.f. = 208, P < 0.001) in sizebetween males and females, supporting the hy-

June 1996 105


5/9

The Southwestern Naturalist

NON-VITELLOGENIC

PERCENT

VITELLOGENIC

J F M A M J J A S O N DMONTHS

1009080706050403020100

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

pothesis of reversed sexual size dimorphism inthis species.DISCUSSION-Eumecescopei shows a repro-ductive cycle in which males and females exhibitasynchronous gonadal activity. Testicular recru-descence occurs in spring with maximal activityduring the summer months. This pattern is sim-ilar to that observed for many temperate zone

male squamates (Fitch, 1970; Duvall et al., 1982;Licht, 1984). In contrast, ovarian activity of fe-males did not begin until late summer with ovu-lation, fertilization and pregnancy in fall andwinter. Fall ovarian activity is common for manyMexican viviparous lizards and occurs in rep-resentatives of three squamate families: Phry-

nosomatidae (Guillette and Casas-Andreu, 1980;Ortega and Barbault, 1984; Guillette and Sul-livan, 1985; Feria, 1986; Guillette and Bearce,1986; Mendez de la Cruz et al., 1988), Scincidae(Guillette, 1983), and Anguidae (Guillette andCasas-Andreu, 1987). This reproductive patternmay be due to the phylogenetic inheritance of anancestral pattern as fall gonadal activity may beassociated with the evolution of viviparity (Guil-lette, 1982). Although possible advantages anddisadvantages of such a reproductive strategy havebeen discussed (Goldberg, 1971; Ballinger, 1973,1977; Guillette and Casas-Andreu, 1980), mosthave not been tested in depth.Asynchrony in the onset of reproductive activ-ity between males and females (as in E. copei),

GRAVID

vol. 41, no. 206


6/9


FieldSpecimens12 Museum Specimens10

86420

50 55 60 65 70SVL (mm)

7 Field SpecimensMuseum Specimens6

54321 50 55 60 65 70 75 80

SVL (mm)FIG. 3-Correlation between (A) number of vitel-logenicfollicles and (B) in uteroembryosand femalebody size (SVL) in Eumeces copei.

has been observed previously in several Mexicansceloporine lizards (Sceloporusgrammicus: Guil-lette and Casas-Andreu, 1980; S. t. torquatus:Feria, 1986; S. m. mucronatus:Mendez de la Cruzet al., 1988). The disparity in the onset of re-productive activity in males and females suggeststhat the sexes use different environment cues.Testicular activity in E. copei was positively cor-related with precipitation, but not with photo-period or ambient temperature. Female gonadalactivity was correlated with decreasing ambienttemperature and photoperiod.

These data suggest different stimulatory agentsin the sexes, but such an implication appears torun counter to experimental studies that haveclearly shown that lizards cannot initiate repro-ductive activity without an appropriate thermaland nutritive environment (Licht, 1984, for re-view). At our study site ambient temperature be-

0 89 171 359DAYS

FIG. 4-Mean (1 SE) size of Eumeces copeithroughout he firstyear of life. Mean 1 SE (box)or range(bar) are givenfor adultfemalesandmales.gins to increase approximately two months beforethe onset of male testicular activity, and precip-itation that increases in May leads to an increasein the availability (quality and quantity) of in-sects (Gutierrez and Sanchez, 1986) by the timemales show gonadal recrudescence. These factorscould permit males to find the thermal and nu-tritional condition necessary to start testicular ac-tivity. Thus, reproductive activity in males maybe linked to a permissive environmental temper-ature and availability of an adequate food supplydue to the onset of spring precipitation. Femalescannot initiate the reproductive activity at thesame time as males because they are pregnant atthis time. Births occur between May and July,coincident with the heightened insect productiv-ity. Thus, the offspring find an abundance of foodin the environment and grow fast. The femalesalso use this period to feed and gain energy in ashort time (2 or 3 months) such that they canrespond to a second cue of photoperiod duringAugust and September, when reproductive activ-ity starts again. Like males, reproductive activityin females has been associated with adequate nu-"trition and environmental temperature (Hahn and

A

75 80

B

80

70

60

50

40

30

20

10

June 1996 107

male

female

Clutchize

Vitellogenicollicles

SVLmm)


7/9

The SouthwesternNaturalist

50

MalesFemales

40

30

20

10

0 50 55 60 65 70 75

SVL (mm)FIG.5-Size distribution SVL) for femaleandmale adult Eumeces opei.

Tinkle, 1965; Licht, 1972; Greenberg and Gist,1985).Several studies have shown that viviparous fe-male lizardsend pregnancywith minimal fat stores(Goldberg, 1972; Guillette and Casas-Andreu,1981). This may explain why postpartum fe-males do not respond reproductively when malesdo in late spring but does not account for the lackof a response in young primaparous females.Moreover, females exhibit maximal vitellogenesisbetween September and October when none ofthe environmental features we examined changedin any significant way. Thus, although our datasuggested a correlation, they were not conclusive.The disparity in reproductive cyclicity implies

that males and females "read"the environmentalstimuli associated with reproductive activity dif-ferently, but experimental studies are needed totest this hypothesis. Species exhibiting fall re-productive activity, as well as those exhibitingasynchrony between sexes, provide importantmodels for future work examining the mecha-nisms controlling seasonal cyclicity in reptiles.Sexual dimorphism is an important atribute ofthe reproductivestrategy of some species (Trivers,1972, 1976; Vitt and Cooper, 1986). If a corre-lation exists between clutch size and female bodysize, then body size can have a direct effect onreproductive success, suggesting that sometimesselection should favor continued growth of fe-

108 vol. 41, no. 2

Frequency


8/9


males. However, such selection for further femalegrowth is tempered by survival probabilities atthat age and males also may have selection pres-sures to grow larger (competition against othermales). Consequently, even in many lizards spe-cies that show a positive relation between clutchsize and female body size, adult males are larger.In our study we found a relationship betweenfemale clutch size and SVL as observed in manylizards species, including oviparous skinks (Fitch,1954; Vitt and Cooper, 1985). Additionally, fe-males had a tendency to be larger than males andreach sexual maturity at a larger size. Rapidgrowth of the neonates occurredduring late springand early summer, but maximal growth was inlate summer and early autumn, when insect pro-ductivity is high (Gutierrez and Sanchez, 1986).During the winter months, growth rate declines,presumably due to the onset of cool winter weath-er. A year after birth (May), juveniles were ap-proximately the size of males entering sexualmaturation; neonates averaged 52.59 mm SVL,whereas the smallest reproductively active maleswere 45.0 mm SVL. Males exhibited the onsetof reproductive activity in May, whereas femalesbegan reproduction in August-September. Con-servatively using the smallest rate (0.038 mm/day), derived from the growth data (Fig. 4) andapplied over the interval May-August, femalesreaching sexual maturity in August should be56.0 mm SVL, approximately the same size asthe smallest sexually mature female (55.0 mmSVL). These data suggest that males require ap-proximately only one year to reach sexual ma-turity, whereas females require a year and threemonths. The delay in onset of sexual maturity bythree months gives the juvenile females an extrasummer of growth. Fall reproductive activity al-lows the extra months of growth while still in-suring that a reproductive season is not lost tothe female. An extra summer season helps explainthe observed sexual size dimorphism. The factorscontrolling the onset of sexual maturation in rep-tiles are still poorly understood, but several stud-ies, including one examining the skink Eumecesobsoletus Masson and Guillette, 1985), suggestedthat the onset of sexual maturation was due todevelopment of the central nervous system, as thegonads of juvenile lizards were responsive to go-nadotropin stimulation.

We thank R. Sanchez orhis help in the field,S. F.Fox, M. Feria, andE. Naranjo ortheircommentson

this manuscript, F. Villegas for his help with graphics,O. Flores (MZUNAM), and the curators of herpe-tology from MZUM and MNHUI for allowing us toexamine specimens under their care, andC.O.N.A.C.Y.T. of Mexico for financial support ofA.R.B. during his study at the University of Florida(U.S.A) in 1987.

LITERATURECITEDAXTELL,R. W. 1960. A new subspecies of Eumeces

dicei from Sierra Madre of Northeastern Mexico.Copeia 1960:19-26.

BALLINGER, . 1973. Comparative demography oftwo viviparous lizards (Sceloporus arrovi and Sce-loporuspoinsetti). Ecology 54:269-283.BALLINGER, . 1977. Reproductive strategies: foodavailability as a source of proximal variation in alizard. Ecology 58:628-645.

DUVALL, D., L. J.GUILLETTE, JR., AND R. E. JONES.1982. Environmental control of reptilian repro-ductive cycle. Pp. 201-231, in Biology of the Rep-tilia, Vol. 13. (C. Gans and F. H. Pough, eds.).Academic Press, New York.

FERIA,O. M. 1986. Contribuci6n al conocimientodel ciclo de vida de Sceloporustorquatus torquatus(Lacertilia: Iguanidae) al sur del Valle de Mexico.Unpubl. tesis de Licenciatura. Escuela Nacional deEstudios Profesionales, Zaragoza, Universidad Na-cional Aut6noma de Mexico, Mexico, 54 pp.FITCH, H. S. 1954. Life history and ecology of thefive-linked skink, Eumeces fasciatus. University ofKansas Publications, Museum of Natural History8:1-156.

FITCH,H. S. 1970. Reproductive cycles of lizardsand snakes. University of Kansas Museum of Nat-ural History Miscellaneous Publications 52:1-247.

FITCH,H. S. 1982. Reproductive cycles in tropicalreptiles. University of Kansas Museum of NaturalHistory Occasional Papers 96:1-53.GARCIA,E. 1981. Modificaciones al sistema de clas-ificaci6n de Kippen. Third ed. Instituto de Geo-grafia, Universidad Nacional Aut6noma de M6x-ico, Mexico.

GOLDBERG,. R. 1971. Reproductive cycle of theovoviviparous iguanid lizard Sceloporusarrovi Cope.Herpetologica 27:123-131.GOLDBERG,. R. 1972. Seasonal weight and cyto-

logical changes in the fat bodies and liver of theiguanid lizard SceloporusjarroviCope. Copeia 1972:227-232.

GREENBERG,. S., ANDD. H. GIST. 1985. Fat bodiesand reproduction in female Anolis carolinensis.Journal of Experimental Zoology 223:277-283.GUILLETTE, . J., JR. 1982. The evolution of vivi-

parity and placentation in the high elevation Mex-ican lizard Sceloporusaeneus. Herpetologica 38:94-103.

June 1996 109


9/9

The SouthwesternNaturalist

GUILLETTE, . J., JR. 1983. Notes concerning re-production of the montane skink, Eumeces copei.Journal of Herpetology 17:144-148.

GUILLETTE,. J. JR., ANDD. A. BEARCE.1986. Re-productive and fatbody cycle in the lizard, Scelop-orusgrammicus disparilis. Transactions of the Kan-sas Academy of Science 89:31-39.

GUILLETTE, L. J. JR., AND CASAS-ANDREU. 1980.Fall reproductive activity in the high altitude Mex-ican lizard, Sceloporus grammicus microlepidotus.Journal of Herpetology 14:143-147.

GUILLETTE,L. J. JR., AND CASAS-ANDREU.1981.Seasonal variation in fat body weights of the Mex-ican high elevation lizards Sceloporusgrammicusmi-crolepidotus. Journal of Herpetology 15:366-371.

GUILLETTE,L. J. JR., AND CASAS-ANDREU.1987.The reproductive biology of the high elevationMexican lizard, Barisiaimbricata.Herpetologica 43:229-38.

GUILLETTE, . J. JR., ANDW. P. SULLIVAN.1985.Reproductive and fatbody cycles of the lizard, Sce-loporusformosus. Journal of Herpetology 19:474-480.

GUTIERREZ . MA. G., ANDR. SANCHEZ.1986. Re-partici6n de los recursos alimenticios en la comu-nidad de lacertilios de Cahuacin, Edo. de Mexico.Unpubl. tesis Licenciatura, Escuela Nacional deEstudios Profesionales, Iztacala, Universidad Na-cional Aut6noma de Mexico, Mexico, 177 pp.

HAHN, W. E., ANDD. W. TINKLE. 1965. Fat bodycycling and experimental evidence for its adaptivesignificance to ovarian follicle development in thelizard Uta stansburiana. Journal of ExperimentalZoology 158:79-86.HALL,R. J. 1971. Ecology of a population of thegreat plains skink (Eumeces obsoletus). Universityof Kansas Science Bulletin 49:359-387.LIGHT,P. 1972. Environmental physiology of rep-tilian breeding cycles: roles of temperature. GeneralComparative Endocrinology Supplement 3:477-488.LIGHT,P. 1984. Reptiles. Pp. 206-282, in Marshall'sphysiology of reproduction. Fourth ed., Vol. 1. (G.E. Lamming, ed.). Churchill Livingstone, Edin-burgh.MASSON,G. R., AND L. J. GUILLETTE,R. 1985.FSH-induced gonadal development in juvenile liz-ards, Eumeces oboletus. Journal of ExperimentalZoology 236:343-351.

MENDEZ-DELA CRUZ,F. R., L. J. GUILLETTE,R.,M. VILLAGRAN, AND G. CASAS-ANDREU. 1988.Reproductive and fat body cycles of the viviparouslizard, Sceloporusmucronatus(Sauria: Iguanidae).Journal of Herpetology 22:1-22.MOUNT,R. H. 1963. The natural history of the red-tailed skink, Eumeces egregius Baird. AmericanMidland Naturalist 70:356-385.

ORTEGA, A., AND R. BARBAULT. 1984. Reproductivecycles in the mesquite lizard, Sceloporusgrammicus.Journal of Herpetology 18:168-175.

RAMIREZ-BAUTISTA,., Z. URIBE-PE A, AND L. J.GUILLETTE,R. 1995. Reproductive biology ofthe lizard Urosaurusbicarinatus bicarinatus (Repti-lia: Phrynosomatidae) from Rio Balsas Basin,Mexico. Herpetologica 51:24-33.SHINE,R. 1988. Parental care in reptiles. Pp. 275-329, in Biology of the Reptilia, Vol. 16. (C. Gansand R. Huey, eds.). Alan R. Liss, New York.

SOMMA,L. A. 1990. A. categorizaction and biblio-graphic survey of parental behavior in lepidosau-rian reptiles. Smithsonian Herpetological Infor-mation Service 81:1-53.

TAYLOR, . H. 1935. A taxonomic study of the cos-mopolitan scincoid lizards of the genus Eumeces.University of Kansas Science Bulletin 23:1-643.TRIVERS, . L. 1972. Parental investment and sexualselection. Pp. 136-175, in Sexual selection and thedescent of man (B. G. Campbell, ed.). Aldine, Chi-

cago.TRIVERS,R. L. 1976. Sexual selection and resource-accruing abilities in Anolis garmani. Evolution 30:253-269.VITT, L. J., ANDW. E. COOPER. 1985. The rela-tionship between reproduction and lipid cycling in

the skink Eumeceslaticepswith comments on brood-ing ecology. Herpetologica 4:419-432.

VITT, L. J., ANDW. E. COOPER. 1986. Skink re-production and sexual dimorphism: Eumecesfascia-tus in the southeastern United State, with notes onEumeces inexpectatus. Journal of Herpetology 20:65-76.

WERLER, . E. 1949. Reproduction of captive Texasand Mexican lizards. Herpetologica 5:67-70.

WERLER,. E. 1951. Miscellaneous notes on the eggsand young of Texan and Mexican reptiles. Zool-ogica 36:37-55.

vol. 41, no. 210

reproductive biology of the lizard eumeces copei

Documents