Reproductive Ecology of the Whiptail Lizard Cnemidophorus ... - BioOne

Copeia, 2000(3), pp. 712–722

Reproductive Ecology of the Whiptail Lizard Cnemidophorus lineatissimus (Squamata: Teiidae) in a Tropical Dry Forest AURELIO RAMI´REZ-BAUTISTA, CARLOS BALDERAS-VALDIVIA,

AND

LAURIE J. VITT

We studied the reproductive ecology of the teiid lizard Cnemidophorus lineatissimus during 1993 and 1994 near Chamela, Jalisco, Me´xico. We estimate that males reached sexual maturity at a snout–vent length (SVL) of 51 mm and an age of five months, and females reached sexual maturity at a SVL of 62 mm and an age of seven months. Testicular mass increased from April to July, reaching maximal size between August and December, and decreased in January of the next year. Gonads of females began to increase in mass during June when vitellogenesis occurred. They reached maximum mass from July to November when most egg production occurred. Some egg production occurred in January as well. The reproductive season for males and females is extended, similar to many other tropical lizards. Mean clutch size was 4.1 ⴞ 0.2 eggs. Clutch size was correlated with female size, but egg size and relative clutch mass remained constant among females and between years. Mean clutch size and female body condition were lower in 1993 compared to 1994, presumably reflecting the effects of annual variation in resource availability on females. Proximal climatic factors influence the timing and intensity of reproduction in C. lineatissimus, but the historical effect of foraging mode on teiid lizard morphology constrains relative clutch mass. Sexual dimorphism is evident with males reaching larger size than females, and seasonal variation in mean SVL in both sexes suggests that much of the population is replaced annually. Estudiamos la ecologıá reproductiva de la lagartija teıída, Cnemidophorus lineatissimus, durante 1993 y 1994 cerca de Chamela, Jalisco, Me´xico. Estimamos que los machos alcanzaron la madurez sexual a la longitud hocico-cloaca (LHC) de 51 mm y a una edad de 5 meses, y las hembras alcanzaron la madurez sexual a una LHC de 62 mm y a una edad de 7 meses. La masa testicular aumento´ de abril a julio, llegando a su tamanõ ma´ximo entre agosto y diciembre, y disminuyo´ en enero del anõ siguiente. Las gońadas de las hembras empezaron a aumentar en masa durante junio cuando la vitelogeńesis sucedio´. Alcanzararon su masa ma´xima de julio a noviembre cuando ocurrio la mayo produccioń de los huevos. Una parte de la produccioń de los huevos tambień ocurrio´ en enero. La e´poca reproductiva para los machos y las hembras es prolongada, parecida a muchas otras lagartijas tropicales. El promedio de la puesta fue de 4.1 ⴞ 0.2 huevos. El tamanõ de la puesta estuvo correlacionado con el tamanõ de la hembra, pero el tamanõ del huevo y la masa relativa de la puesta se mantuvieron constantes entre hembras y entre anõs. El promedio de la puesta y la condicioń corporal de las hembras fueron ma´s bajos en 1993 que en 1994, presumiblemente reflejando los efectos de la variacioń de la disponibilidad anual de recursos para las hembras. Factores clima´ticos inmediatos influyen el patroń temporal y la intensidad de reproduccioń en C. lineatissimus, pero en el efecto histo´rico del modo de alimentar en la morfologıá de las lagartijas teıídas restringe la masa relativa de la puesta. Se nota el dimorfismo sexual, en que los machos alcanzan un tamanõ mayor que las hembras, y la variacioń estacional en el promedio LHC de ambos sexos sugiere que mucho de la poblacioń cambia anualmente.

ESCRIPTIVE studies on reproduction of reptiles have provided data necessary to formulate and test hypotheses on the evolution of life histories. For example, by analyzing a large database on lizard reproduction, Tinkle (1969) was able to show that lizard species investing heavily in reproduction at any given

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time tended to be short-lived compared to those that spread their investment over long time periods. With coworkers (Tinkle et al., 1970), he identified discrete reproductive ‘‘strategies,’’ combinations of life-history traits that balanced energy invested in reproduction with potential survivorship. More extensive analyses show that

䉷 2000 by the American Society of Ichthyologists and Herpetologists

RAMI´REZ-BAUTISTA ET AL.—CNEMIDOPHORUS REPRODUCTION at least a portion of the variation among species in life-history traits has a historical basis (Dunham and Miles, 1985; Dunham et al., 1988); closely related species tend to have more similar life histories than distantly related species. Data used for the above analyses represent a very small portion of global lizard species, and, as a result, conclusions could change as more data become available. We add to the existing data on lizard reproduction by describing the reproductive cycle of the Mexican Whiptail Lizard, Cnemidophorus lineatissimus. The few Mexican lizard species studied vary considerably in reproduction (e.g., Sceloporus aeneus, Guillette, 1981a,b; Anolis nebulosus, Ramı´rez-Bautista, 1995; Eumeces copei, Ramı´rez-Bautista et al., 1996; Eumeces lynxe, Ramı´rez-Bautista et al., 1998; Sceloporus variabilis, Benabib, 1994). This variation is not surprising considering the wide range of habitats in Me´xico. Me´xico spans a latitudinal range from the southern temperate-zone to near the tropics and contains deserts, montane forest, tropical dry forest, and rain forest. It also contains a great diversity of lizards (e.g., Smith and Taylor, 1950). The whiptails (genus Cnemidophorus) are among the most conspicuous lizards in tropical dry forest. Four of the five species groups of Cnemidophorus recognized by Wright (1993) are represented in Me´xico. Although many reproductive studies of temperate-zone whiptail species exist (e.g., Ballinger and Schrank, 1972; Hulse, 1981; Schall, 1978), there have been no detailed reproductive studies on Mexican species of Cnemidophorus (see Vitt and Breitenbach, 1993). Reproductive studies on tropical species of Cnemidophorus indicate that the reproductive season is extended in response to the extended activity season (e.g., Leon and Cova, 1973; Vitt, 1983; Vitt et al., 1997) when compared with temperate-zone species. To date, only anecdotal descriptions of reproduction of C. lineatissimus have appeared (e.g., Walker, 1970; Ramı´rez-Bautista and Uribe-Pena, 1989; Ramı´rez-Bautista, 1994). Reproduction of other species inhabiting this tropical dry forest, such as Anolis nebulosus (Ramı´rez-Bautista, 1995; Ramı´rez-Bautista and Vitt, 1997) and Urosaurus bicarinatus (Ramı´rez-Bautista et al., 1995; Ramı´rez-Bautista and Vitt, 1998), occurs as rainfall, temperature, and photoperiod increase. In this study, we address the following general questions with respect to the reproductive cycle of C. lineatissimus: (1) Are sexually mature males and females the same size? (2) What is the reproductive cycle of females and males? (3) Is peak reproductive activity associated with environmental factors (temperature, precipitation,

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or photoperiod)? (4) Does clutch size vary with female SVL (snout–vent length) or among years? and (5) Are reproductive characteristics of C. lineatissimus similar to those of other whiptail lizards? MATERIALS

AND

METHODS

This study was conducted at Chamela, near the Estacioń de Biologıá ‘‘Chamela’’ (EBCH), 5 km east and 15 km south of the Pacific coast at approximately 19⬚30⬘N latitude and 105⬚03⬘W longitude, at an elevation varying from 10–584 m in Jalisco, Me´xico. The dominant vegetation type is tropical dry forest with rains occurring in late spring and summer. Mean annual temperature is 24.9 C with an average annual rainfall of 748 ⫾ 119 mm, varying from 585–961 mm (Bullock, 1986). Monthly mean temperatures and precipitation over a 10-yr period that encompassed the study were recorded at the Estacioń Meteoreolo´gica in the region. Data on photoperiod were taken from the Astronomical Almanac (1984). A total of 264 (148 females and 116 males) lizards were collected from August to December 1993 and from January to November 1994. Because samples were often small for individual months and varied considerably between years, data were pooled to describe the general annual reproductive cycle. Lizards were humanely killed and fixed in 10% formalin in the laboratory where gonadal analyses were performed. SVL was measured on necropsied lizards to 1.0 mm. The SVL of the smallest female with enlarged vitellogenic follicles or oviductal eggs was used to estimate minimum SVL at maturity. Males were considered sexually mature if they contained enlarged testes and convoluted epididymides typically associated with sperm production (Goldberg and Lowe, 1966). Testes of males and livers and fat bodies of both sexes were removed and weighed (0.0001 g) so that seasonal cycles in mass of organs related to reproduction could be described. Past studies have shown that fat bodies generally are reduced during the reproductive season and liver mass appears to cycle with fat body mass although its role in reproduction remains unknown (van Loben Sels and Vitt, 1984). In reproductive females, the largest egg (oviductal, vitellogenic follicle, or nonvitellogenic follicle) on each side of the body was weighed to 0.0001 g and multiplied by the number of eggs on that side to estimate total gonadal mass on each side of the body. The sum of both gonads estimated female gonadal mass. Data on lizard SVL and organ masses were transformed to logs (base

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10) which linearized the regressions. Because organ mass usually varies with SVL, we first calculated regressions of log10-transformed organ mass data with log10 of female SVL. For those regressions that were significant (indicating a body size effect), we calculated residuals from the relationship of organ mass to SVL (all variables log10-transformed) to produce SVL-adjusted variables. We used these residuals to describe the organ and/or reproductive cycle of both sexes. This technique maintains variation because of extrinsic factors (e.g., season) while minimizing the compounding effect of size-related individual variation in SVL. We performed ANOVAs on the residuals of the organ mass regressions with month as the factor to determine whether significant monthly variation exists, including only those months for which n ⱖ 3. Games-Howell posthoc tests were used to determine which months differed. To estimate the volume of oviductal eggs, we measured length and width of the largest egg in each oviduct, calculated a mean for the two eggs, and calculated volume as V ⫽ · LW2 (3c2 ⫹ 14c ⫹ 35)/210 where L is egg length, W is egg width, and c ⫽ ␥ (兹E ⫺ 1). E was estimated as 1.8 and ␥ as 0.25 by comparing the shape of C. lineatissimus eggs with models in Maritz and Douglas (1994). Clutch size was determined by counting eggs in the oviduct or vitellogenic follicles in the ovaries of adult females during the reproductive season. Mean clutch size was determined based on counts of oviductal eggs and counts of vitellogenic follicles separately. We then tested to determine whether these produced different estimates of clutch size prior to combining data for both. Incubation period was estimated as the interval between the date on which individual females had their first oviductal eggs of the season (late July) and the date on which first hatchlings appeared in the field (early October). This provides only an approximation because we cannot be certain when females first deposited eggs or whether the first hatchlings resulted from clutches deposited when we observed females with oviductal eggs. We calculated relative clutch mass (RCM; Vitt and Congdon, 1978) as mass of the oviductal eggs/(female mass ⫺ clutch weight). Morphological descriptions were restricted to sexually mature males and females. To examine sexual size differences between males and females, we restricted the dataset to the upper 50% of the sample of sexually mature lizards to reduce bias resulting from sampling error. Means are presented ⫾ 1 SE unless otherwise

Fig. 1. Seasonal variation in temperature and rainfall near the study site at Chamala, Me´xico.

indicated. Standard parametric statistical tests were used when possible. Otherwise, appropriate nonparametric tests were substituted. Statistical analyses were performed with the Macintosh version of Statview 4.5. Specimens are deposited at the Coleccioń Nacional de Anfibios y Reptiles, Departamento de Zoologıá, Instituto de Biologıá, UNAM in Me´xico City. RESULTS Seasonal variation in climate.—Because of its latitude and elevation, Chamela experiences very little seasonal variation in photoperiod. Minimum photoperiod was 11.0 h, whereas maximum photoperiod was 13.3 h. Mean monthly temperatures varied from 23.05–28.05 C, and mean monthly rainfall varied from 0–222.8 mm (Fig. 1). Chamela can be considered highly seasonal with respect to rainfall, moderately seasonal with respect to temperature, and relatively aseasonal with respect to photoperiod. Size and sexual dimorphism.—Sampled C. lineatissimus varied in SVL from 42–112 mm. Sexually mature males varied from 51–112 mm SVL (x¯ ⫽ 77.6 ⫾ 1.6, n ⫽ 115). Sexually mature females ranged in size from 62–99 mm SVL (x¯ ⫽ 78.6 ⫾ 0.9, n ⫽ 109). Based on the time at which hatchlings appeared and the seasonal size distribution of males and females, we estimate that males reached sexual maturity at an age of five months, and females reached sexual maturity at an age of seven months. Based on our comparison of the largest 50% of sexually mature males and females, males were larger (SVL ⫽ 89.5 ⫾ 1.27 mm, n ⫽ 65) than females (SVL ⫽ 84.8 ⫾ 0.77 mm, n ⫽ 66, Z ⫽ ⫺2.57, P ⫽ 0.0102; Fig. 2) and weighed more (males ⫽ 21.8 ⫾ 1.05 g, females ⫽ 16.04 ⫾ 0.49 g, Z ⫽ ⫺4.14, P ⬍ 0.0001). Male reproductive and organ cycle.—The annual reproductive cycle of males is based on 115 sexually mature lizards collected in 1993 and 1994.

RAMI´REZ-BAUTISTA ET AL.—CNEMIDOPHORUS REPRODUCTION

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Fig. 2. Size (SVL) distribution of sexually mature males and females and unsexed juveniles (open bars) of Cnemidophorus lineatissimus from Chamela. Arrows indicate size at sexual maturity.

There was a significant relationship between log10 body mass and log10 testes mass (R2 ⫽ 0.62, F1,113 ⫽ 58.6, P ⬍ 0.001), log10 liver mass (R2 ⫽ 0.7, F1,113 ⫽ 275.3, P ⬍ 0.001), and log10 fat body mass (R2 ⫽ 0.34, F1,113 ⫽ 59.5, P ⬍ 0.001). ANOVAs on residuals of the regressions (Dec. excluded because of small sample size) revealed significant effects of month on testes mass (F10,102 ⫽ 3.68, P ⬍ 0.0003), liver mass (F10,102 ⫽ 2.57, P ⬍ 0.0081), and fat body mass (F10,102 ⫽ 2.55, P ⬍ 0.0085; Fig. 3). Based on a GamesHowell posthoc test, adjusted testes mass differed significantly (P ⬍ 0.05) between the following months: March differed from January; and June differed from August through November. Testicular mass increased from April to July and reached maximum size from August to January of the following year. Based on a GamesHowell posthoc test, adjusted fat body mass differed significantly (P ⬍ 0.05) between the following months: May differed from January, July, and October; and July differed from August. The fat body mass cycle was irregular, but fat bodies were smallest when testes began to increase in size. When testes were largest (Aug.– Dec.), fat body mass was generally low but beginning to increase; fat bodies reached maximum size at the end of the breeding season ( Jan.). In contrast, liver mass increased significantly from July to December, decreased in February and March of the next year, and reached minimum mass as testes began to increase in mass (April–June; Fig. 3). Based on a GamesHowell posthoc test, adjusted liver body mass differed significantly (P ⬍ 0.05) between the following months: January differed from April through June; March differed from April and May; April differed from July, October, and November; and May differed from June, October, and November. The period of maximal testicular growth of C. lineatissimus was positively cor-

Fig. 3. Seasonal cycle in testes, fat bodies, and livers for male Cnemidophorus lineatissimus. Organ cycles are depicted as residuals from the log total mass versus log organ mass regressions (see text).

related with increasing temperature (r ⫽ 0.79, P ⬍ 0.001) and precipitation (r ⫽ 0.78, P ⬍ 0.005) but not with photoperiod (P ⬎ 0.05). Female reproductive and organ cycle.—A total of 109 females sampled were sexually mature. Significant linear relationships existed between log10 female body mass and log10 gonad mass (R2 ⫽ 0.70, F1,107 ⫽ 9.1, P ⫽ 0.0031), log10 liver mass (R2 ⫽ 0.26, F1,107 ⫽ 39.6, P ⬍ 0.001), and log10 fat body mass (R2 ⫽ 0.30, F1,107 ⫽ 47.0, P ⬍ 0.001). ANOVAs on residuals of the regressions (Feb., March, and Dec. excluded because of small sample sizes) revealed significant effects of month on gonad mass (F8,95 ⫽ 6.2, P ⬍ 0.001) and liver mass (F8,95 ⫽ 4.1, P ⫽ 0.0003) but no effect on fat body mass (F8,95 ⫽ 0.9, P ⫽ 0.5295; Fig. 4). Power for the ANOVA on fat body mass was low (lambda ⫽ 7.1, Power ⫽ 0.386). Based on a Games-Howell posthoc test, adjusted gonadal mass differed significantly (P ⬍ 0.05) between the following months: January differed from May and June; May differed from July

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Fig. 5. Relationship between female snout–vent length (SVL) and clutch size for Cnemidophorus lineatissimus. Dotted lines indicate the 95% confidence intervals for the mean.

confirming the production of January clutches by some females. Vitellogenesis and follicular growth of female C. lineatissimus were correlated with temperature (r ⫽ 0. 51, P ⬍ 0.05) and precipitation (r ⫽ 0.57, P ⬍ 0.05) but not with photoperiod (P ⬎ 0.05). Fig. 4. Seasonal cycle in gonads, fat bodies, and livers for females of Cnemidophorus lineatissimus. Parameters are the same as for Figure 3.

through November; and June differed from August and November. Adjusted liver mass differed only between October and November (P ⬍ 0.05). Average female gonadal mass increased from June when vitellogenesis occurred and reached maximum size from July to November when females began to ovulate. Females likely produced more than a single clutch during this period. A significant decline in gonadal mass occurred in December, but another peak appeared in January of the next year, suggesting the production of yet another clutch by at least some females (Fig. 4). Females with vitellogenic follicles were observed between early summer ( July) and midwinter ( Jan.). Vitellogenic ovarian follicles or oviductal eggs were present in females from July, (83.3%; n ⫽ 6), August (88.9%; n ⫽ 18), September (65.0%; n ⫽ 20), October (48.0%; n ⫽ 25), and November (63.6%; n ⫽ 11). Females (n ⫽ 4) from December had nonvitellogenic follicles; however, in a sample (n ⫽ 8) from January, five (62.5%) females had oviductal eggs

Clutch and egg size.—Females containing oviductal eggs were similar in size to females containing enlarged vitellogenic follicles (SVL ⫽ 78.8 ⫾ 2.1 and 80.6 ⫾ 1.3 mm, respectively; F1,58 ⫽ 0.6, P ⫽ 0.456). Mean clutch size based on counts of vitellogenic follicles was 4.2 ⫾ 0.3 (1– 9, n ⫽ 41); mean clutch size based on counts of oviductal eggs was 3.8 ⫾ 0.4 (1–9, n ⫽ 19). These were not significantly different (MannWhitney U-test, Z ⫽ ⫺1.45, P ⫽ 0.147). This comparison does not take into consideration the effect of body size on clutch size. An ANCOVA comparing clutch size between females with oviductal eggs and those with enlarged vitellogenic follicles yielded similar results. Clutch size was correlated with female SVL (R2 ⫽ 0.52, F1,57 ⫽ 63.6, P ⬍ 0.0001; Fig. 5), and both slopes (F1,56 ⫽ 0.55, P ⫽ 0.548) and intercepts (F1,56 ⫽ 0.44, P ⫽ 0.510) were the same. Pooling data on counts of vitellogenic follicles and oviductal eggs produced an overall mean clutch size of 4.1 ⫾ 0.2 (1–9, n ⫽ 60). Oviductal egg mass was not determined by female SVL (log10-transformed, R2 ⫽ 0.08, F1,18 ⫽ 2.5, P ⫽ 0.136), and there was no relationship between the number of eggs produced and their mass (log10-transformed, rs ⫽ 0.33, Z ⫽ 1.24, P ⫽ 0.214). Most females from July and August had vitellogenic

RAMI´REZ-BAUTISTA ET AL.—CNEMIDOPHORUS REPRODUCTION follicles or oviductal eggs (83% and 89%, respectively). Mean clutch size based on oviductal eggs and enlarged vitellogenic follicles was lower for females during 1993 than for females during 1994 (4.1 ⫾ 0.7,yn ⫽ 29 and 4.8 ⫾ 0.3, respectively, n ⫽ 31; Mann-Whitney U-test, Z ⫽ ⫺3.32, P ⫽ 0.0009). Among females with oviductal eggs, mean clutch mass for 1993 was lower (1.57 ⫾ 0.15 g, n ⫽ 12) than 1994 (3.2 ⫾ 0.43 g, n ⫽ 7; Mann-Whitney U-test, tied Z ⫽ ⫺3.04, P ⫽ 0.0023). An ANCOVA on clutch mass with SVL as the covariate revealed significant differences in slopes (F1,15 ⫽ 5.4, P ⫽ 0.0342) and intercepts (F1,15 ⫽ 5.8, P ⫽ 0.0437); the relationship between clutch mass and body size was different in the two years. Mean egg mass was similar between years (0.54 ⫾ 0.02 and 0.61 ⫾ 0.03, 1993 and 1994, respectively; MannWhitney U-test, tied Z ⫽ ⫺1.69, P ⫽ 0.091), and there was no effect of body size on egg mass (ANCOVA, all P-values ⬎ 0.61). Because we found some reproductive differences in females from the two years, we conducted separate ANCOVAs on body mass for each sex (all individuals included) with SVL as the covariate to compare physical condition of lizards between years. These analyses determined whether lizards weighed more at any given SVL in one year or the other. In males, there was no difference in slopes (P ⫽ 0.514) or intercepts (P ⫽ 0.454) of the annual regressions of log10 body mass on log10 SVL. However, in females, both the slopes (P ⫽ 0.022) and intercepts (P ⫽ 0.017) were different. When the female analysis was limited to just sexually mature females, the difference in slopes was only marginally significant (P ⫽ 0.0504), but the difference in intercepts remained significant (P ⫽ 0.445). Sexually mature females were in better condition during 1994 than in 1993. Oviductal eggs from 25 females averaged 14.4 ⫾ 0.51 mm in length (9.0–17.5 mm), 9.72 ⫾ 0.31 mm in width (4.7–11.9 mm), and 679.8 ⫾ 46.7 mm3 in volume (107.7–1212 mm3). Relative clutch mass averaged 0.160 ⫾ 0.015 in 1993 and 0.212 ⫾ 0.033 in 1994. Because there was no difference between years in RCM (MannWhitney U-test, Z ⫽ ⫺1.352, P ⫽ 0.176), we estimated RCM as the mean based on females from both years, 0.179 ⫾ 0.016. RCM was not correlated with female SVL (both variables log10-transformed, Rs ⫽ 0.16, tied Z ⫽ 0.68, P ⫽ 0.499). Egg production and seasonal and yearly variation in size.—Females began to lay their eggs during mid-July, and the first hatchlings occurred in early October. Mean SVL at hatching was 32.1

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Fig. 6. Seasonal changes in average body size of sexually mature Cnemidophorus lineatissimus.

⫾ 2.1 mm (31–34, n ⫽ 3). During July, August, and September, small juveniles were not observed, suggesting that all had moved into larger size classes. Relatively small juveniles were present in all other months suggesting that hatching occurs over an extended time period. It is unlikely that hatchlings occurred after April because the last eggs were deposited in January. Considering sexually mature males and females separately, significant variation in mean monthly SVL existed in both sexes (males, ANOVA, F10,105 ⫽ 12.4, P ⬍ 0.0001; females, ANOVA, F8,95 ⫽ 3.5, P ⫽ 0.0013; Fig. 6). Mean male SVL was significantly different among the following months based on a Games-Howell posthoc test (P ⬍ 0.05): January differed from July and August; February differed from July through October; March differed from July through November; April differed from July through October; and May differed from July through October. Mean female SVL was significantly different among the following months: January differed from July; May differed from July through October; and July differed from November. DISCUSSION Cnemidophorus lineatissimus inhabits the tropical dry forest on the Pacific coast of Me´xico from Nayarit to Guerrero (Smith and Taylor, 1950). The habitat is highly seasonal with respect to rainfall and less seasonal with respect to temperature and day length (photoperiod). Reproduction in C. lineatissimus in this habitat can be characterized as seasonal, but the reproductive season is long compared with reproductive seasons of lizards in temperate-zone habitats. Reproduction in C. lineatissimus differs from reproduction in nonwhiptail lizards from the same locality. For example, females of A. nebulosus produce clutches of a single egg with

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their reproductive cycle more similar to that of other anoles (Ramı´rez-Bautista and Vitt, 1997). Reproductive cycle.—Reproductive activity in male C. lineatissimus is seasonal with an activity peak from August through December. Reproductive behavior, such as courtship and mating, began in June and July, coincident with the wet season. Testes mass increased as soon as precipitation and temperature increased. Consequently precipitation and temperature, or a combination of the two factors, appear to stimulate gonadal activity in males (e.g., Licht and Gorman, 1970; Marion, 1982). To date, several studies on lizards inhabiting tropical dry forest have shown that precipitation, temperature, and photoperiod or a combination of the three factors play an important role in reproduction (Ramı´rezBautista, 1995; Ramı´rez-Bautista and Vitt, 1997, 1998). However, in this environment, reproductive activity of each species may be influenced by different proximal factors. For example, in A. nebulosus (Ramı´rez-Bautista, 1995; Ramı´rezBautista and Vitt, 1997) and Urosaurus bicarinatus (Ramı´rez-Bautista and Vitt, 1998), gonadal activity is correlated with temperature and photoperiod. In contrast, temperature and precipitation appear to be most important in Sceloporus utiformis (AR-B, unpubl. data). Data presented in this study suggest that proximal climatic factors either directly (e.g., the initiation of reproduction) or indirectly (e.g., through their effect on resources) influence reproduction in C. lineatissimus. Ultimate factors including the effect of foraging mode on morphology and clutch mass (Vitt and Congdon, 1978) likely define the limits within which reproductive investment per episode can vary. Male reproductive activity was also extended, as in other tropical and subtropical whiptail lizards (Vitt and Breitenbach, 1993). Males of temperate-zone whiptail lizards have relatively short reproductive seasons (e.g., C. inornatus; Christiansen, 1971). Fat body mass of males was highly variable during the dry and wet seasons, but lower levels occurred during the peak of the reproductive season, whereas liver mass increased. This pattern is different from that of sit-and-wait foraging species that occur in the same habitat (Ramı´rez-Bautista, 1995; Ramı´rez-Bautista and Vitt, 1997, 1998). Because Cnemidophorus use an active or widely foraging mode (Pianka, 1969, 1970) and do not expend energy defending territories, they not only can use energy searching for and courting females (Anderson and Vitt, 1990; Censky, 1995) but can continue to replenish energy spent in reproductive behavior by continuing to forage because they are not con-

strained by territory defense. This likely accounts for the large amount of variation in fat storage and the relative lack of a seasonal fat body cycle. A consistent decline in fat body mass during the breeding season is typical in territorial species that use the energy stores for reproduction, such as acquisition and maintenance of territories, displays, and mating (Ramı´rez-Bautista and Vitt, 1997, 1998). The female reproductive season was also extended. Follicles began to increase in size during June 1993. Most egg production occurred from August through November, coinciding with rainfall, but oviductal eggs were found as late as January 1994 indicating that females can reproduce over a period of six to seven months. Female reproduction is typically extended in other tropical or subtropical teiids, including Ameiva ameiva (Vitt, 1982; Magnusson, 1987; Colli, 1991), Cnemidophorus communis (Pardo-De la Rosa, 1997), C. ocellifer (Colli, 1991; Vitt, 1983), and Kentropyx striata (Magnusson, 1987) but is highly seasonal in temperate-zone teiids (e.g., Cnemidophorus tigris, Goldberg and Lowe, 1966; C. inornatus and C. neomexicanus, Christiansen, 1971). Tropical and subtropical lizards in the sister taxon Gymnophthalmidae typically have extended breeding seasons as well (e.g., Leposoma rugiceps, Telford, 1971; Neusticurus ecpleopus, Sherbrooke, 1975). Female reproduction in teiids and gymnophthalmids tends to be reduced or not occur at all in the dry season in tropical habitats with distinct wet–dry seasonality (e.g., Gymnophthalmus speciosus, Telford, 1971; C. ocellifer, Vitt, 1983). In C. lineatissimus, the reduction in fat bodies associated with the period of egg production suggests females cannot harvest enough resources to support egg production and thus mobilize some of the energy contained in fat bodies for reproduction as occurs in other lizard species (Hahn and Tinkle, 1965). Vitellogenesis in females began coincident with increases in rainfall and temperature and, although the correlation with photoperiod was not significant, a combination of the three factors likely play an important role initiating reproduction (Marion, 1982; Licht, 1984; Ramı´rez-Bautista and Vitt, 1998). Detecting a photoperiod effect at Chamala may be difficult because photoperiod varies relatively little throughout the year. Although temperature and possibly photoperiod influence or initiate reproduction, the timing of rainfall may be the ultimate cue for reproduction through its effect on egg and offspring survival (Andrews and Sexton, 1981). In June of 1994 the weather was cool and dry, and only one female had vitellogenic follicles. In July, when temperature and

RAMI´REZ-BAUTISTA ET AL.—CNEMIDOPHORUS REPRODUCTION precipitation increased, most females had vitellogenic follicles or oviductal eggs. Clutch size of C. lineatissimus varied with the size of females and between years, but egg size and RCM were consistent among females and between years. Because the overall condition of females was poorer (reduced mass at any given SVL) in 1993 and clutch size was also lower, energy availability may have been reduced during the 1993 breeding season. Females sampled in 1993 contained fewer prey than did females sampled in 1994 (Balderas-Valdivia, 1996), further suggesting that resource availability accounts for the difference in clutch size and physical condition of the lizards. The effect of food availability on growth rate and reproductive characteristics of lizards is well known (e.g., Ballinger, 1977; Dunham, 1978). It is interesting and paradoxical that body condition did not appear to be affected in males, which may suggest that important behavioral differences exist between males and females. The peak of hatchling emergence occurred between December and January, just at the beginning of the dry season when the abundance of litter insects increases (Ramı´rez-Bautista, 1995). The RCM of C. lineatissimus is similar to that of other species of Cnemidophorus (Vitt and Breitenbach, 1993). Low RCM likely reflects the influence of foraging mode on the evolution of morphology within the entire clade Teiidae and likely has its origins in a distant ancestor (see Dunham and Miles, 1985; Dunham et al., 1988). The streamlined morphology and foraging mode of teiids have constrained life-history characteristics such as total clutch mass and RCM (Vitt and Congdon, 1978; Vitt and Price, 1982). In summary, the reproductive cycle of C. lineatissimus in dry forest of Me´xico is similar to that of other species of Cnemidophorus living in wet–dry seasonal environments with an extended growing season (Vitt, 1983, Vitt and Breitenbach, 1993). Males are reproductively active for an extended period during the year, and females produce eggs during an extended time period. In this case, egg production was tied, at least to some degree, to wetter and warmer periods during the year. As in most species of Cnemidophorus, clutch size is correlated with SVL (but for an exception, see Schall, 1983). Like most other Cnemidophorus species, clutch size, clutch mass, and RCM are low (Anderson and Vitt, 1990, Vitt and Breitenbach, 1993; Pardo-De la Rosa, 1997), especially when compared with lizards in the Iguania that have variable clutch sizes (Vitt and Price, 1982). Finally, differences in available resources appear to determine the

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amount of energy invested in reproduction by females. Sexual dimorphism and seasonal variation in size.— Sexual dimorphism in body size and mass is well documented among lizard species. Males are often larger in SVL than females (Stamps, 1983; Fitch, 1981) and have larger heads than females of the same size (e.g., Anderson and Vitt, 1990; Vitt and Cooper, 1985; Censky, 1996). Male C. lineatissimus reached sexual maturity at a smaller size and attained larger maximum size and mass than females, a pattern similar to many other species of Cnemidophorus (e.g., Anderson and Vitt, 1990; Pardo-De la Rosa, 1997). At least three nonexclusive hypotheses may account for sexual dimorphism in this species: sexual selection; differential energy allocation causing different growth trajectories between the sexes; or differential survivorship. Sexual size dimorphism in C. lineatissimus may result from sexual selection in which larger males are at an advantage over smaller males in acquiring mates. Sexual selection can maintain large body size in male lizards when large males mate more frequently than smaller ones, such as in C. tigris (Anderson, 1986), Anolis garmani (Trivers, 1976), A. carolinensis (Ruby, 1984), Sceloporus jarrovi (Ruby, 1981), and Iguana iguana (Dugan, 1982), or when larger males win in intrasexual agonistic encounters (Ruby, 1984; Vitt and Cooper, 1985; Cooper and Vitt, 1987). We have no direct evidence for this in C. lineatissimus, but observations on other teiid lizards suggest that this may occur in most or all species (e.g., Anderson and Vitt, 1990; Censky, 1996). Data on relative head size between sexes would add support to this hypothesis. Differences in growth rates between sexes are suggested by the seasonal distributions of mean body size with female growth appearing to slow down relative to that of males during the reproductive season (Fig. 6). Sexual dimorphism in body size resulting from reduction of growth in females coincident with reproduction has been reported in the Bonaire Island Whiptail Lizard, Cnemidophorus murinus (Dearing and Schall, 1994) and likely occurs in other teiids as well. Whether sexual differences in survival account for apparent sexual dimorphism in the population cannot be determined with our data (e.g., Dunham, 1978). Based on the seasonal variation in mean SVL within males and females, most of the population could turn over during a single season. Although not evident in Figure 6, a few large individuals were present in each month suggesting that at least some individuals live for more than one season.

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(AR-B, CB-V) LABORATORIO DE ECOLOG´ıA, UNIDAD DE BIOLOG´ıA, TECNOLOG´ıA Y PROTOTIPOS (UBIPRO), ESCUELA NACIONAL DE ESTUDIOS PROFESIONALES IZTACALA, UNAM. AV. DE LOS BARRIOS S/N, LOS REYES IZTACALA, TLALNEPAN´ XICO, C.P. 54090, A.P. 314, TLA, EDO. DE ME ME´XICO; AND (LJV) SAM NOBLE OKLAHOMA

MUSEUM

OF NATURAL HISTORY AND DEPARTZOOLOGY, UNIVERSITY OF OKLAHOMA, 2401 CHAUTAUQUA, NORMAN, OKLAHOMA 73072-7029. E-mail: (LJV) [email protected]. Send reprint requests to LJV. Submitted: 17 Dec. 1999. Accepted: 9 Feb. 2000. Section editor: A. H. Price. MENT OF