reproductive cycle of a high-elevation, oviparous lizard ( sceloporus spinosus ...

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Reproductive Cycle of a High-Elevation, Oviparous Lizard (Sceloporus spinosus:Reptilia: Phrynosomatidae)Author(s): Fausto R. Méndez-de la Cruz , Maricela Villagrán-Santa Cruz , María Leticia López-Ortíz ,and Oswaldo Hernández-GallegosSource: The Southwestern Naturalist, 58(1):54-63. 2013.Published By: Southwestern Association of NaturalistsDOI: http://dx.doi.org/10.1894/0038-4909-58.1.54URL: http://www.bioone.org/doi/full/10.1894/0038-4909-58.1.54

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THE SOUTHWESTERN NATURALIST 58(1): 54–63 MARCH 2013

REPRODUCTIVE CYCLE OF A HIGH-ELEVATION, OVIPAROUSLIZARD (SCELOPORUS SPINOSUS: REPTILIA: PHRYNOSOMATIDAE)

FAUSTO R. MENDEZ-DE LA CRUZ,* MARICELA VILLAGRAN-SANTA CRUZ, MARIA LETICIA LOPEZ-ORTIZ, AND OSWALDO

HERNANDEZ-GALLEGOS

Laboratorio de Herpetologıa, Departamento de Zoologıa, Instituto de Biologıa, Universidad Nacional Autonoma de Mexico,C.P. 04510, Apartado Postal 70–153, Distrito Federal, Mexico (FMC, MLL)

Laboratorio de Biologıa de la Reproduccion Animal, Departamento de Biologıa Comparada, Facultad de Ciencias,Universidad Nacional Autonoma de Mexico, C.P. 04510, Distrito Federal, Mexico (MVS, MLL)

Centro de Investigacion en Recursos Bioticos, Carretera Toluca-Ixtlahuaca Km 14.5, San Cayetano Toluca,Estado de Mexico, Mexico (OHG)

*Correspondent: [email protected]

ABSTRACT—We studied the reproductive cycle of Sceloporus spinosus from Laguna La Preciosa, Puebla,Mexico, elevation 2,400 m. There was no sexual dimorphism in snout–vent length (males, 87.5 mm; females,88.8 mm). Gonadal mass varied monthly and was related to snout–vent length; both sexes had a synchronousreproductive cycle that peaked in late winter and early spring. In males, recrudescence occurred November–January with abundant primary and secondary spermatocytes. Maximum testicular mass was in February whenseminiferous tubules showed spermiogenesis and spermatozoa were in the lumen and epididymis. Regressionwas evident in April, when testicular mass decreased, and it continued in May, although spermatozoa were inseminiferous tubules and lumen of epididymal ducts. In July–September, testicular mass was less, and onlyspermatogonias, Sertoli cells, and remains of sperm were in seminiferous tubules. In females, vitellogenesisbegan in late autumn, maximum deposition of yolk was in March, and ovulation was in April. Oviductal eggswere present in April–June and oviposition was in June–July. In August–September, only previtellogenic andatretic follicles were present; hatchlings were present in September. Size of clutch was 6–17 eggs andcorrelated with snout–vent length. One clutch is produced per reproductive season. Reproductive activity inboth sexes was distinct from spring-summer activity in tropical sceloporines from high elevations, but wassimilar to other lizards in northern temperate areas.

RESUMEN—Estudiamos el ciclo reproductor de Sceloporus spinosus de la laguna La Preciosa, Puebla, Mexico, auna elevacion de 2,400 m. No hubo dimorfismo sexual en la longitud hocico cloaca de machos (87.5 mm) yhembras (88.8 mm). La masa gonadal vario mensualmente y se correlaciono con la longitud hocico cloaca;ambos sexos tuvieron un ciclo reproductor sincronico con una maxima actividad a fines del invierno y principiosde la primavera. En los machos, la recrudescencia ocurrio de noviembre a enero con abundantes espermatocitosprimarios y secundarios. La maxima masa testicular fue en febrero cuando los tubulos seminıferos mostraronespermiogenesis y espermatozoides se encontraron en la luz y en los conductos del epidıdimo. La regresion fueevidente en abril, cuando decrecio la masa testicular y se continuo en mayo, aunque espermatozoides estuvieronpresentes en la luz de los tubulos seminıferos y en los conductos del epidıdimo. De julio a septiembre la masatesticular se redujo y solo espermatogonias, celulas de Sertoli y restos de espermatozoides permanecieron en lostubulos seminıferos. En las hembras la vitelogenesis inicio a fines del otono, el maximo deposito de vitelo fue enmarzo y la ovulacion en abril. Los huevos en el oviducto estuvieron presentes de abril a junio y la ovoposicion fueen junio-julio. De agosto a septiembre solo folıculos previtelogenicos y atresicos estuvieron presentes; los recieneclosionados aparecieron en septiembre. El tamano de la puesta fue de 6 a 17 huevos y se correlaciono con lalongitud hocico cloaca. Solo una puesta es producida por estacion reproductora. La actividad reproductora enambos sexos fue diferente de la actividad de primavera–verano de sceloporinos tropicales de elevaciones altas,pero fue similar a la de otros lacertilios de areas templadas nortenas.

The reproductive cycle is an important aspect of lifehistory and is determined by intrinsic and extrinsic factors(Duvall et al., 1982; Licht, 1984; Ramırez-Pinilla et al.,2009). Lizards of the genus Sceloporus occur in a variety of

environments and include oviparous and viviparous forms(Guillette et al., 1980). Continuous reproduction occursin both oviparous (S. variabilis; Garcıa-Collazo et al.,1993) and viviparous (S. bicanthalis; Hernandez-Gallegos

et al., 2002) species, while seasonal cycles are representedby reproduction in viviparous lizards in autumn (Guilletteand Mendez-de la Cruz, 1993; Mendez-de la Cruz et al.,1998) and in most oviparous species in spring-summer(Villagran-Santa Cruz et al., 2009).

Oviparous Sceloporus are more abundant than theirviviparous counterparts at elevations <1,500 m (Guilletteet al., 1980), and few oviparous species reach higherelevations. Reproductive cycles have been documented inseveral species of oviparous Sceloporus that occur atelevations >1,500 m: S. orcutti at 2,100 m (Mayhew,1963), S. occidentalis at 1,584 m (Goldberg, 1974), S.scalaris at 2,600 m (Newlin, 1976), S. aeneus at 2,600–3,000m (Guillette, 1981; Hernandez-Gallegos, 1995; Manrıquez-Moran, 1995), and S. graciosus at 1,950–2,040 m (Tinkle etal., 1993). Reproductive cycles of most oviparous Sceloporusfrom high elevations present maximum testicular activityduring spring, regression during early summer, andtesticular recrudescence during early autumn (Goldberg,1974; Newlin, 1976; Hernandez-Gallegos, 1995), whereasvitellogenesis occurs during spring, ovulation during latespring or summer (Newlin, 1976; Guillette, 1982), andhatching by late summer (Goldberg, 1974; Guillette 1982;Manrıquez-Moran, 1995).

Another species that occurs at elevations >1,500 m is S.spinosus (Calderon-Espinosa et al., 2006). The reproduc-tive cycle of S. spinosus was described previously by Valdez-Gonzalez and Ramırez-Bautista (2002), who detecteddifferences from the reproductive cycles of high-elevationSceloporus previously mentioned. However, this studycombined populations from different locations, eleva-tions, and years (Acajete, Puebla, at 2,254 m, and LasMinas, Puebla, at 537 m, during 1973–1983). Thereproductive cycles they described may differ becausesome reproductive characteristics may vary geographically(Grant and Dunham, 1990). Furthermore, S. spinosus is awidely distributed lizard that occurs from Durango andwestern Tamaulipas to northern Jalisco, Michoacan,Hidalgo, and Puebla on the Mexican Plateau (Smithand Taylor, 1950). Recent studies have shown that S.spinosus includes several different clades (Calderon-Espinosa et al., 2006) and each one may exhibit differentreproductive cycles. Our study describes the reproductivecycle of a population of S. spinosus at Laguna La Preciosa,Puebla, Mexico, and makes a comparison with previouslydescribed cycles of high-elevation, oviparous Sceloporus.

MATERIALS AND METHODS—We collected S. spinosus at LagunaLa Preciosa or Las Minas, Puebla, Mexico (198220N, 978230W;2,400 m elevation). During spring 1993–spring 1994, 2–16individuals were collected monthly (except October for bothsexes and March for males). The study area had a dry climatewith rain in summer (Garcıa, 1981). These lizards are terrestrialand associated with cacti that they use for perches and shelter.Lizards were captured by hand or by using a noose.

We measured snout–vent length (mm) and weighed ovariesand testes (g). Because mass of reproductive organs vary with

size of body, we used analysis of covariance (ANCOVA) withgonadal mass as the dependent variable, snout–vent length asthe covariate, and month as the factor as described byHernandez-Gallegos et al. (2002), followed by a LSD multiple-comparison test to determine differences among averages.Females were classified as previtellogenic (without vitellogenicfollicles), vitellogenic (with yellow follicles ‡2 mm in diameter),and gravid (with oviductal eggs). To characterize reproductiveactivity of females, we calculated percentage in each stage permonth. We estimated size of clutch by counting oviductal eggs.We also performed a correlation analysis to determine therelationship between size of clutch and snout–vent length.

Gonads were prepared for a conventional histological study(dehydrated in a gradual alcohol series, cleared in xylene, andembedded in paraplast). Tissues were sectioned at 7 lm andstained with hematoxilin-eosin and Masson’s Tricrome (Presnelland Schreibman, 1997). Cells of the male germinal line wereclassified according to Villagran-Santa Cruz et al. (1994). Thesmallest female with eggs in the oviduct was used to estimateminimum snout–vent length at sexual maturity. Among males,presence of convoluted epididymides (Goldberg and Lowe,1966) and spermatozoa in seminiferous tubules and epididymi-des were used to define minimum size at sexual maturity.Specimens were fixed in 10% formalin, preserved in 70%alcohol, and deposited in the Coleccion Nacional de Anfibios yReptiles, Instituto de Biologıa, Universidad Nacional Autonomade Mexico.

RESULTS—We collected 43 males and 52 females. Thesmallest male with convoluted epididymides andspermatozoa in seminiferous tubules and epididymideswas 72 mm snout–vent length. Snout–vent length of 39adult males was 72–104 mm (average, 87.5 – 1.53 mm).The smallest female with oviductal eggs was 70 mmsnout–vent length. Snout–vent length of 52 adult femaleswas 70–102 mm (average, 88.8 – 1.03 mm). There was nodifference between snout–vent lengths of adult males andfemales (t = 0.75, P = 0.456).

Snout–vent lengths of males and females, and size ofclutch were distributed normally (P ‡ 0.10 for overallmodels). Mass of testes and ovaries were not distributednormally (P < 0.01 in both models). Therefore, we log10-transformed gonadal data to achieve normality (Zar,1999).

Mass of testes varied monthly (F8, 25 = 96.8, P < 0.001)and was related to snout–vent length (F1, 25 = 77.3, P <0.001). Only samples with ‡2 males were included. Adultmales exhibited a seasonal reproductive cycle (Fig. 1a).Five homogenous groups were identified. Testes enlargedNovember–December through January, when primaryand secondary spermatocytes were abundant and earlystages of spermiogenesis were observed (Figs. 1a and 2a–b). Maximum testicular mass was in February whenseminiferous tubules exhibited spermiogenesis and pres-ence of spermatozoa in the lumen and epididymides(Figs. 1a and 2c–d). Regression was evident in April, whentesticular mass decreased, and continued in May, whengerminal epithelium in seminiferous tubules was re-duced, although spermatozoa were present in the lumen

March 2013 Mendez-de la Cruz et al.—Reproductive cycle of lizards 55

and epididymides (Figs. 1a and 2e–f). In July–September,testicular mass had lower values (Fig. 1a), and weobserved spermatogonia, Sertoli cells, and remains ofcells in seminiferous tubules but no spermatozoan inepididymides (Figs. 2g–h). By late September, evidence ofearly testicular recrudescence was observed in 20% ofmales, which was verified by primary spermatocytes inseminiferous tubules.

Mass of ovaries varied monthly (F10, 39 = 10.72, P <

0.001) and was related to snout–vent length (F1, 39 = 20.6,P < 0.001). Females had a seasonal reproductive cycle,with maximum ovarian activity in late winter (Fig. 1b).There was no important difference in reproductivecondition of females within each monthly sample (i.e.,females in the population were synchronous duringvitellogenesis, but differed during gestation and periodof oviposition; Fig. 3). LSD multiple-range tests identifiedfour homogenous groups (Fig. 1b). A small amount ofyolk was deposited in November–January (Figs. 1b and4a–b). Follicles began to enlarge significantly in February(Figs. 1b and 4c) and some atretic follicles were evident.Maximum deposition of yolk was in March (Figs. 1b and4d). Ovulation occurred in April; therefore, during April–June, the ovaries presented atretic and previtellogenicfollicles and corpora lutea. Oviductal eggs also wereobserved during this period (Figs. 1b, 3, 4e, and 4f). Noprevitellogenic female in April–June showed evidence of asecond clutch or early vitellogenesis. In June–July,oviposition occurred, and females collected in Julyshowed only previtellogenic and atretic follicles, whereascorpora lutea had been reabsorbed (Fig. 4g). In August–September, only females with previtellogenic and atreticfollicles were present (Figs.1b and 4h). Atretic follicleswere present February–September, i.e., during vitellogen-esis, ovulation, and after oviposition. First hatchlings wereobserved in September, and the incubation period was ca.60 days. Size of clutch was estimated based on number ofoviductal eggs, which was 6–17, and was correlated withsnout–vent length (r2 = 0.46, P = 0.001, n = 19). Averagesize of clutch was 11.5 – 0.68.

DISCUSSION—The reproductive season in oviparousreptiles generally occurs during spring or summer, andin most of these reproductive cycles, gametogenesisoccurs shortly before reproduction (Fitch, 1970;Villagran-Santa Cruz et al., 2009). Also, reproductiveactivity of oviparous Sceloporus in temperate or high-elevation tropical areas occur in spring and summer, suchas in S. graciosus (Fitch, 1970; Tinkle et al., 1993), S. orcutti(Mayhew, 1963), and S. aeneus (Manrıquez-Moran, 1995).However, some sceloporines from temperate areas haveearlier reproductive activity, including S. scalaris (Newlin,1976), S. occidentalis (Goldberg, 1974), and S. woodi(Jackson and Telford, 1974). In these species, testicularrecrudescence commences as early as September,vitellogenesis occurs in late winter, and maximum

FIG. 1—Average (–SE) log10-transformed mass of a) testesand b) ovaries of Sceloporus spinosus at Laguna La Preciosa,Puebla, Mexico. Averages with different letters are significantlydifferent (P < 0.001).

�FIG. 2—Gonadal and epididymal changes throughout the reproductive cycle of male Sceloporus spinosus: a–b) recrudescence

(November–January); a) increased number of primary (Ps) and secondary spermatocytes (Ss) in the seminiferous tubules, and earlystages of spermatogenesis (�); b) note in the epididymal ducts the presence of primary spermatocytes (Ps) in the lumen; c–d)maximal testicular activity (February); c) spermatogenetic activity in seminiferous tubules and sperm in the lumen (�); d) epididymalducts showing increased epithelial height and secretory activity and the lumen filled with sperm; e–f) regression (May); e)seminiferous tubules with germinal epithelium reduced but with sperm in the lumen (�); f) epididymal ducts also with sperm; g–h)quiescence (July–September); g) seminiferous tubules only with spermatogonias (G) and Sertoli cells (S) present; h) epididymispresent evident small ducts and the lumen is empty (hematoxylin-eosin stain, 40·).

56 vol. 58, no. 1The Southwestern Naturalist

activity of both sexes occurs until April–May. Also, otherreptiles, such as the southern alligator lizard Gerronotusmulticarinatus (Goldberg, 1972), the wall-lizard Lacertavivipara (Joly and Saint Girons, 1975), and some snakes(Saint Girons, 1982), present recrudescence in lateSeptember and early October. The reproductive cycle ofS. spinosus, although it is from a high-elevation tropicalarea, is more similar to reproductive cycles of thesespecies than to those of most other oviparoussceloporines. Both sexes initiate reproduction in lateautumn, maximum activity occurs in late winter and earlyspring, and ovulation and fertilization occur in earlyspring, with hatching in September.

Testicular recrudescence and early vitellogenesis dur-ing autumn were reported for temperate sceloporines (S.scalaris, S. occidentalis, and S. woodi). Whereas tropicalsceloporine lizards begin reproduction in late winter inhigh (i.e., S. aeneus; Hernandez-Gallegos, 1995; Man-rıquez-Moran, 1995) or low elevations (i.e., S. gadovae;Lemos-Espinal et al., 1999; S. ochoterenae; Bustos-Zagal etal., 2011). Therefore, early reproductive events (testicularrecrudescence and early vitellogenesis) in S. spinosus

during autumn are unusual within tropical, high-eleva-tion lizards. Early reproductive activity in S. spinosusoccurs during the dry season and months with lowtemperatures.

The reproductive cycle of S. spinosus is a seasonal cycle,as evidenced by macroscopical (variation in gonadalmass) and microscopical (histological) data. In contrast,the reproductive cycle of S. spinosus described by Valdez-Gonzalez and Ramırez-Bautista (2002), indicated thatmales present two reproductive peaks, during spring andautumn. In fact, our study determined that recrudescenceoccurred during autumn, as a phase preceding theunique maximum testicular activity that occurs untilFebruary. Also, Valdez-Gonzalez and Ramırez-Bautista(2002) determined that females have a longer reproduc-tive season (January–October), where gonadal mass offemales increased in January–July and decreased inAugust–October. Unfortunately, gonadal mass was calcu-lated considering ovaries and oviductal eggs, which was amistake. Valdez-Gonzalez and Ramırez-Bautista (2002:37)stated ‘‘The largest egg (oviductal, vitellogenic follicle, ornonvitellogenic follicle) on each side of the body wasweighed to – 0.0001 g and multiplied by the number ofeggs on that side. The calculated total weight for bothsides was used as an estimate of female gonadal mass.’’Their study did not consider that after ovulation,

fertilization takes place and initiates embryonic develop-

ment in the oviduct. Therefore, considering that gameto-

genesis and embryogenesis represent different processes of

the reproductive cycle, oviductal eggs must not be mixed

with gonads to describe the gonadal cycle. This inaccurate

method results in comparisons that are incompatible with

reproductive cycles that are described properly, considering

that different structures were used to describe the gonadal

cycle, as Villagran-Santa Cruz et al. (2009) pointed out

previously.

Our study demonstrated that the population of S.spinosus at Laguna Las Minas laid eggs in June–July, andhatchlings were present in September. We determinedthat only one clutch was laid each reproductive season.We found no evidence of females that had ovulated (withcorpora lutea) initiating a second clutch; post-layingfemales only presented atretic follicles. Moreover, femalesin the population were synchronous during vitellogenesis,but differed in time of ovipositioning. One clutch perseason is a common phenomenon in several species oflizards (Fitch, 1985). Nesting areas may promote variation

FIG. 3—Monthly changes in reproductive stages of femaleSceloporus spinosus at Laguna La Preciosa, Puebla, Mexico: whitebars, previtellogenic; gray bars, vitellogenic; black bars, gravid.

�FIG. 4—Gonadal changes throughout the reproductive cycle of female Sceloporus spinosus: a–c) recrudescence (vitellogenesis in

November, Januarys and February, respectively); previtellogenic (Pf) and vitellogenic (Vf) follicles in ovary; d) maximal activity(March), the increased size of vitellogenic follicles (Vf) was correlated with deposition of yolk (y) within the cytoplasm; e–g) gonadalregression; e) luteogenesis (April) after ovulation, the postovulatory follicles initiate formation of corpora lutea (Cl), and there areprevitellogenic follicles (Pf); f) luteolysis (June) of corpora lutea (Cl) and there are previtellogenic (Pf) and atretic follicles (Af)evident; g) in July, corpora lutea disappear and only previtellogenic and atretic follicles are evident in the ovary; h) quiescence(September); the ovary presents only previtellogenic (Pf) and atretic follicles (Af); (hematoxylin-eosin stain, 40·).


throughout the nesting microenvironment, which maypromote phenotypic variability in offspring (Overall,1994; Andrews et al., 2000) that allows hatchlings to copewith environmental conditions to which they are exposedat time of hatching.

Results from our study differ from the reproductivecycle previously described by Valdez-Gonzalez andRamırez-Bautista (2002:39) because they reported that22.2% of females were capable of laying ‡2 clutchesduring the reproductive season, arguing that from‘‘January to October females of S. spinosus were foundwith all three classes of eggs (oviductal eggs, vitellogenicand non vitellogenic ovarian follicles).’’ They determined

that average diameter of vitellogenic follicles (20.5 – 2.2;range, 8–31 mm) appeared bigger than that of oviductaleggs (15.3 – 1.2; range, 12–22 mm). In contrast, our studyrevealed that vitellogenic follicles were only 5.8 – 0.33 mm

(range, 3.1–9.7 mm). In lizards, vitellogenic follicles aresmaller than oviductal eggs. After ovulation, eggs gainwater and became larger and heavier; consequently,exhibiting an increase of 179% in weight (Cuellar, 1970,

1984). Size of vitellogenic follicles (average, 20.5 mm;maximum, 31 mm) reported by Valdez-Gonzalez andRamırez-Bautista (2002) seems improbable, as in mostlizards with snout–vent length similar to that of S. spinosus,vitellogenic follicles barely reach 10 mm (Cuellar, 1970;Estrada-Flores et al., 1990). Inappropriate measurementsby Valdez-Gonzalez and Ramırez-Bautista (2002) give riseto estimated volumes of oviductal eggs of 679.2 – 73.4mm3 (range, 384.0–928.9 mm3), which is impossible inmedium-sized lizards.

Valdez-Gonzalez and Ramırez-Bautista (2002) suggest-ed that reproductive traits of S. spinosus (period ofreproductive activity, snout–vent length at adulthood, sizeof clutch, and volume of oviductal eggs) could beresponses to environmental conditions and availabilityof resources. The population they studied inhabited atropical rainforest with 3,908.9 mm of rain. However, S.spinosus occurs only in arid areas, such as desert scrub orthorn forests (average annual rainfall is 419.9 mm atLaguna La Preciosa), and barely reaches surroundingareas of oak forest. No population has been reported intropical rainforest (Frost, 1973; Sites et al., 1992;Calderon-Espinosa et al., 2006). Moreover, lizards studiedby Valdez-Gonzalez and Ramırez-Bautista (2002) weredeposited in the Coleccion Nacional de Anfibios yReptiles, Instituto de Biologıa, Universidad NacionalAutonoma de Mexico, and while the only lizards fromLas Minas Puebla were listed as from a tropical forest, thelatitude was incorrect (198580N instead of 198220N). Thisis the same locality as our study.

Variation in size of clutch is an important trait inreproductive effort and has been documented in manyspecies (Fitch, 1978, 1985). In addition, intrapopulationvariation in size of clutch has been attributed toenvironmental factors (Rodrıguez-Romero and Mendez-

de la Cruz, 2004). Lizards that produce one clutch usuallyproduce larger clutches than those that produce multipleclutches (Mattison, 1989). Tinkle et al. (1970) deter-mined that temperate species produce one large clutchper reproductive season. Tinkle and Hadley (1975)considered that large clutches may be because onechance to reproduce favors females with larger clutches.Our study demonstrates that size of clutch, obtained fromnumber of oviductal eggs of S. spinosus, was 6–17 eggs(average, 11.5 – 0.68 eggs) and was correlated withsnout–vent length. Previous studies of S. spinosus deter-mined that size of clutch was 9–11 (average, 10 eggs) inthe same locality as our study, and 11–23 (average, 16.5eggs) in Cerro Gordo (2,000 m). In addition, variationhas been documented in other species from lowerelevations within the spinosus group and size of clutchaverages 9.20 in Chamela, Jalisco (30–70 m), 16.43 in ElRodeo, Morelos (1,100 m), 13.16 in Huahutla, Morelos(1,040 m), 12.88 in Oaxaca (1,665 m), and 15.62 inXalitla, Guerrero (538 m; Calderon-Espinoza et al., 2006).These results differ from those of Valdez-Gonzalez andRamırez-Bautista (2002), as they reported size of clutchesalmost twice those previously reported for S. spinosus(average, 18.5 – 1.54; range, 8–31; n = 18). Differencesmay be because they determined size of clutch bycounting eggs in the oviduct or vitellogenic follicles ofadult females during the reproductive season. Maturefemales may present previtellogenic, vitellogenic andatretic follicles, and corpora lutea. Follicular atresia mayoccur at any stage of ovogenesis (previtellogenic orvitellogenic follicles; Saidapur, 1978; Guraya, 1989).During our study, we observed 30% follicular atresia invitellogenic follicles of S. spinosus that evidently reducesize of clutch, as has been detected in other species oflizards (Mendez-de la Cruz et al., 1993; Jones and Swain,2000). Some of the S. spinosus studied by Valdez-Gonzalezand Ramırez-Bautista (2002) were from Las Minas,Puebla, 537 m, and others were from Acajete, 2,254 m.Lizards of the spinosus group differ in size of clutch byelevation (Calderon-Espinosa et al., 2006). Therefore,differences between our research and the study by Valdez-Gonzalez and Ramırez-Bautista (2002) may be attributedto their combining lizards from localities whose elevationsdiffered by >1,700 m. However, considering that thelatitudinal location of Las Minas was not accurate, theactual difference was only 146 m. Therefore, differencesmay only be attributed to summation of vitellogenicfollicles and oviductal eggs to determine size of clutch.

The incubation period, determined by our observa-tions of oviposition (June–July) and the date when firsthatchlings were observed (September), lasted ca. 60 days.This differs from the incubation period observed fromherpetological collections by Valdez-Gonzalez andRamırez-Bautista (2002). They reported that productionof eggs occurred in late June, although hatchlings were


caught in July–September, and they calculated anincubation period of ca. 30 days.

Reproductive cycles represent important traits in lifehistory of lizards (Fitch, 1970) and appropriate methodsshould be used to describe them correctly. Previousstudies revealed considerable differences in gonadalactivity due to problems associated with methods of study(Villagran-Santa Cruz et al., 2009). Unfortunately, severalstudies erroneously considered oviductal eggs or embryosas part of gonads to determine variation in ovarian activityin oviparous (e.g., Ramırez-Bautista and Gutierrez-Mayen,2003) and viviparous lizards (e.g., Hernandez-Salinas etal., 2010). In oviparous lizards, ovulation and ovipositionoccur within a short time (differing by 1–3 months) andthe discrepancy in reproductive cycles may not be soevident. Conversely, in viviparous lizards that present ‡5months of pregnancy, differences between ovulation andbirth are substantial. In both instances, results shouldallow appropriate comparison with reproductive cyclespreviously described.

Reproductive cycles are influenced strongly by envi-ronmental conditions (Licht, 1984; Grant and Dunham,1990; Borrelli et al., 2000). In general, peripheralpopulations must face harsh environments (Hardie andHutchings, 2010). Lizards that survive at the limit of theirdistribution present variation in several traits of lifehistory, such as behavior, thermoregulation, and repro-ductive phenology (Boretto and Ibarguengoytıa, 2006;Sinervo et al., 2010). Our study demonstrates thatreproductive phenology of oviparous lizards that inhabitthe limit of their distribution have a longer reproductiveseason, i.e., spermatogenesis and vitellogenesis occursearlier than sceloporine lizards that are in low-elevationand tropical environments. Apparently, lizards that faceadverse cold environments start gametogenesis earlierand lay eggs when time of hatching favors survival ofnewborns (Goldberg, 1971; Ballinger, 1973).

We thank M. Y. Mendez and F. D. Mendez for assistance in thefield and for preparing figures, E. Bastiaans for comments andcorrections, and M. Aguilar and E. Mendoza for assistance inhistological assessments. This research was supported byConsejo Nacional de Ciencia y Tecnologıa 171N and Programade Apoyo a Proyectos de Investigacion e Innovacion Tecnologica213405, 215011–3. Lizards were collected under permit Secre-tarıa de Medio Ambiente y Recursos Naturales FAUT 0074.

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Submitted 3 August 2010. Accepted 9 November 2012.

Associate Editor was Rocky Ward.


reproductive cycle of a high-elevation, oviparous lizard ( sceloporus spinosus ...

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