Diet and Reproductive Biology of the Viviparous Lizard Sceloporus

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Diet and Reproductive Biology of the Viviparous Lizard Sceloporus torquatus torquatus (Squamata: Phrynosomatidae) Author(s): Manuel Feria Ortiz, Adrián Nieto-Montes de Oca and Isaías H. Salgado Ugarte Reviewed work(s): Source: Journal of Herpetology, Vol. 35, No. 1 (Mar., 2001), pp. 104-112 Published by: Society for the Study of Amphibians and Reptiles Stable URL: http://www.jstor.org/stable/1566029 . Accessed: 10/12/2012 13:41

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This content downloaded by the authorized user from 192.168.52.76 on Mon, 10 Dec 2012 13:41:45 PM All use subject to JSTOR Terms and Conditions Journalof Herpetology,Vol. 35, No. 1, pp. 104-112,2001 Copyright2001 Society for the Studyof Amphibiansand Reptiles

Diet and Reproductive Biology of the Viviparous Lizard Sceloporus torquatus torquatus (Squamata:Phrynosomatidae)

MANUEL FERIAORTIZ,1 ADRIAN NIETO-MONTESDE OCA,2 AND ISAIASH. SALGADOUGARTE1

'Museo de Zoologia,Facultad de Estudios SuperioresZaragoza, Unizersidad Nacional Aut6nomade Mdxico,Batalla de 5 de mayos/n, Col. Ejercitode Oriente,Mexico 09230, D. F, Mdxico,2Museo de Zoologia,Facultad de Ciencias, Universidad Nacional Autdnoma de Mexico, Apartado Postal 70-399, Mexico 04510, D. F, Mexico; E-mail:[email protected]

ABSTRACT.-Thereproductive cycle and diet of a population of the viviparous lizard Sceloporus torquatus torquatusfrom the Pedregalde San Angel, Distrito Federal,Mexico, were studied. Ovarianactivity began in June,and by October,one to five preovulatoryfollicles per ovary were present Ovulation took place in Novemberand December,and parturitionoccurred in late April or early May.Relative litter and egg masses were higher at the end of development than at the beginning. Testes increasedin size from June through September,when they reachedtheir maximumvolume and weight Testicularregression began at this point and was particularlyaccentuated in Octoberand November. The diet of both sexes was composedprimarily of insects; however, plant material(small flowers and fruits),spiders, isopods, and occasionallyearthworms were also consumed. Both sexes consumed plant material throughoutthe year. In the dry season, males ingested twice as much food as females.

RESUMEN.-Seestudiaron el ciclo reproductory la dieta de una poblacion de la lagartijavivipara Sceloporus torquatustorquatus que habita en el Pedregalde San Angel, Distrito Federal,Mexico. La actividadovarica comenz6 en junio, y para octubre se encontraronde uno a cinco foliculos preovulatoriospor ovario. La ovulaci6n ocurri6 entre noviembrey diciembre,y el parto a fines de abril o principios de mayo. La masas relativasde la camaday de los huevos fueronmayores a finales del desarrolloembrionario que al principio. Los testlculos aumentaronde tamafnodesde junio hasta septiembre,cuando alcanzaronsu volumen y peso maximos. Posteriormentecomenzo la regresi6ntesticular, la cual fue particularmenteacentuada en octubre y noviembre.La dieta de ambos sexos consisti6 principalmentede insectos; sin embargo,tambien se consumieron,ademais de materiavegetal (floresy frutos pequefios),arafias, is6podos y ocasionalmentelombrices de tierra. Ambos sexos consumieron materia vegetal durantetodo el afo. En la epoca seca, las hembras consumieronalrededor de la mitad del alimento consumido por los machos.

Fitch (1970) stated that the reproductive sea- predator escape behavior (Vitt and Condgon, son in temperate lizards usually occurs during 1978), and individual morphology (Vitt, 1981) the spring and summer. However, reproductive can be important in molding the reproductive patterns in which gametogenesis, courting, cop- biology of lizards. It has been suggested that ulation, and fertilization occur in the fall have differences in life history within a species may been reported since the early 1970s (Goldberg, be the result of physiological or developmental 1971; Ballinger, 1973). Guillette and Casas-An- responses to environmental conditions, rather dreu (1980) pointed out that fall reproductive than phylogenetic effects or genetic sources activity is common in viviparous lizards inhab- (e.g., Steams, 1980). Thus, a better understand- iting high elevations in temperate zones. More ing of the influence of envionmental conditions recent papers have reported this reproductive in molding life-history traits requires knowl- modality in additional species and have at- edge of their variation among populations of the tempted to explain its advantages (Guillette and same species. Bearce, 1986; Guillette and Casas-Andreu, 1987; Sceloporustorquatus torquatus is a viviparous Ramfrez, 1991; Guillette and Mendez de la lizard occurring in central Mexico (Smith, 1936). Cruz, 1993; Ramfrez-Bautista et al., 1996, 1998). It is usually confined to rocky habitats, although Intra- and interspecific variation in reproduc- it is entirely arboreal in some areas (Smith, 1936; tion and life-history traits of lizards is partially Duellman, 1961). Werler (1951), Fitch (1970), and explained by the physical environment (Bena- Feria-Ortiz (1989) provided some data on its re- bib, 1994). However, it has been shown that fac- productive biology. Uribe-Alcocer et al. (1995) tors such as phylogenetic inertia (Ballinger, described the histological changes exhibited by 1983), foraging behavior (Vitt and Price, 1982), the ovaries in the female reproductive cycle.

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20 Fourteen to 17 adults were sampled each month from November 1984 to November 1985. 16 Lizards were killed with ether and the following data taken: sex, snout-vent length (SVL; ?+ 0.1 E 12 mm), and body mass (BM; ?+ 0.1 g). Specimens -- Photoperiod were dissected and their stomach, gonads, and O- - 240 , a) 8 Temperature E (in the case of gravid females) oviductal eggs E C Rain -__ 160 - (developing embryos and yolk) extracted. Testes 0) were with an balance (+ - O3 weighed analytical 80 0.01 mg). The length and width of each testis (? 0 0.01 mm) were used to obtain the testicular vol- J FMAMJ JASOND ume (V), calculated using the volume of an el- lipsoid: V = (4/3)-r(L/2)(W/2)2. Ovaries were 0.01 and num- 20 weighed (? mg) ber of follicles and diameter of the largest fol- 0 16 licle recorded. In the case of gravid females, o both the number of corpora lutea and the di- '- 12 - ameter of the largest corpus (+ 0.01 mm) were Ca Temperature 2 also recorded. In addition, the entire comple- 8 = Rain 240 ----- ment of oviductal eggs was extracted. The em- E ------160 4 . bryos were weighed (? 0.01 mg) and their diameter measured (+ 0.01 mm). The develop- 0 F MAMnJ F 80 mental stage of the embryos was determined by J F M A M J JASOND comparison with the table of embryonic devel- Month opment for the viviparous lizard, Lacertavivipara FIG.1. Temperature,precipitation, and photoperi- (Defaure and Hubert, 1961). Embryos and yolk od; mean monthly values for the lower part of the were then dried to constant mass at 60?C. Rel- Pedregal de San Angel, Distrito Federal.Top: Means ative clutch (litter) mass (RCM) was calculated for 30 years of records. Bottom: Means for the sur- by dividing the total litter mass by the body a veyed year. Data obtained from meteorologicalsta- mass without the litter. Relative oviductal egg tion in the area. study mass (REM) was calculated by dividing the average oviductal egg mass by the body mass Guillette and Mendez-de la Cruz (1993) report- without the litter. ed on the reproductive cycle of a population For each specimen, stomach volume was mea- from Cerro Gordo, near San Juan Teotihuacain, sured with and without its food contents by vol- in the state of Mexico. We describe the repro- umetric displacement, and the difference be- ductive cycle of a population of S. t. torquatus tween these two volumes was used to estimate from the Pedregal de San Angel, Distrito Fed- the volume of stomach contents. Stomach con- eral, Mexico. In addition, nutritional depen- tents were identified to the order level whenever dence of the embryos is analyzed, and diets for possible. The number of items of each prey tax- the dry and wet seasons are provided. on was recorded. A Petri dish containing the stomach contents was placed over a paper sheet MATERIALS AND METHODS with a millimetric scale on it, and the area cov- Study Area.-The study was carried out in the ered by each prey taxon on the paper, as well as lower part of the Pedregal de San Angel, Dis- those areas covered by unidentified material trito Federal, Mexico (99?13'-99?08'W longitude, (parasites, inorganic, plant, and organic but 19?14'-19?18'N latitude), at an elevation of 2250- very digested matter) was estimated. Finally, the 2300 m. The area is covered with solidified lava volume of each item (SVO, for item i) was cal- flows from the Xitle volcano; the crevices in culated by the equation: SVOi = (AOi/ASC) these volcanic rocks serve as shelters for the liz- SCV, where AOi is the area covered by the item ards. Vegetation consists of microphilous scrub, i, ASC is the total area covered by the stomach dominated by Senecio praecox and Schinus molle contents, and SCV the stomach contents volume. (Rzedowski, 1954). The climate is temperate The volume, incidence (number of stomachs in subhumid with rainfall occurring mainly from which a given prey item was found) and num- May to October (wet season) and a dry winter ber of organisms (density) of each prey taxon (Fig. 1). Precipitation and temperature data for were recorded for both the dry and wet seasons. the surveyed year were similar to the average Relative volume, density, and incidence values values of 30 years of climatic records, suggest- were obtained by dividing the value for a given ing that climatic conditions during the survey taxon by the corresponding total sum for all the were typical for the study area (Fig. 1). taxa. An importance value for each taxon was

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l4UU E E 1 8 a) 1000 2(U E 6 v 0 o9 600 0U U 4 E

0 200_- 1 2 0

-L4V E F M A M J J A S ON D 0)

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-a 0.9 07 -( , 12 E_ --I- m 0.5 s- Ovaries - Testes E 03

O 3 < U o -0.1 J F M A M J J A S O N D J F M A M J J A S ON D Month Month FIG.2. Monthlychanges in (top) the mean diam- FIG.3. Monthlychanges in (top) the mean testic- eter of the largestfollicle and (bottom)the mean num- ular volume and (bottom)the mean ovarianand tes- ber of follicles per ovary.Values presented represent ticular wet masses. Values presented representthe the mean + 1 standarderror. mean ? 1 standard error. calculated the relative by adding volume, den- The SVL of the smallest female containing and incidence. sity, oviductal eggs was 73 mm. The SVL of the next results Unless otherwise indicated, are ex- three smallest females with enlarged vitellogen- pressed as mean ? 1 SE. To detect the existence ic follicles were 76 mm, 77 mm, and 78 mm. in the of significant changes adjusted, mean Thus, females attain sexual maturity at a mini- monthly values for the gonad (ovaries or testes) mum SVL of about 73 mm. The SVL of the three ANCOVA were mass, analyses performed using smallest males with enlarged testes were 70.5 SVL as a covariate and gonad mass as the re- mm, 77.0 mm, and 79.0 mm. This indicates that variable. The mean sponse adjusted monthly males reach sexual maturity at approximately values were then compared with a Bonferroni the same size as females. test. In statistical general, standard, parametric Mean SVL of oviductal embryos close to par- tests were when the data performed (whether turition (development stage 40) from four fe- transformation or they required not) fulfilled as- males collected in April was 27.4 ? 0.9 mm, sumptions. Otherwise, nonparametric tests whereas in a sample of 11 juvenile lizards col- (Mann-Whitney or Kruskall-Wallis) were per- lected in November, mean SVL was 65.2 ?_ 0.1 formed. All the statistical were analyses per- mm. The mean SVL of four immature speci- formed with the SPSS statistical package (SPSS mens collected in March and April was 74 mm Inc., 1997). (73-76 mm). RESULTS Ovarian Cycle Size and ApproximateGrowth From January to June, ovaries remained small, Mean SVL of adult males and females were and there were no significant changes in their 92.2 ? 1.1 mm and 90.6 ? 6.5 mm, respectively. mass. Mean diameter of the largest follicles was These means were not significantly different 1.25 ? 0.03 mm (0.6-2.0 mm; N = 66). Also, (t1,6 = 0.59, P > 0.05). Mean BM of adult males during these months the average number of fol- and females were 30.74 ? 1.13 g and 29.09 ? licles per ovary was relatively low (Fig. 2). From 0.62 g, respectively. The difference between June to October, ovary mass increased signifi- these means was not significant (t,;, = 1.38, P cantly (F1,,09 = 27.17; P < 0.01; Fig. 3). Also, > 0.05). from May to September, the number and di-

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I.4 ameter of follicles increased significantly (Krus- 1.3 kall-Wallis H, = 123.7 and 104.4, N = 187 and P < In m 1.1 111, respectively; 0.001; Fig. 2). August, 0) some of the follicles were dull yellow and slight- a) than the rest; the difference in size was CO ly larger 0 larger in September. In this month, each ovary had from three to seven follicles distinctly larger 0.7 than the rest (mean diameter of largest follicles 0) = 4.94 ? 0.31 In the c, 0.5 mm). following months, (0 vitellogenic follicles continued to increase in the numberof follicles decreased < 0.3 size. However, N D J F M A markedly(Fig. 2), which suggests high follicular atresia. Ovulation took from late November to E place E 20 0 early December.Mean diameter of freshly ovu- 0o lated follicles was 10.22 + 0.16 mm. Corpora D16 E lutea resulting from the ovulation were relative- 01 ly large at the beginning of pregnancy (Novem- O 12 ber and December) but decreased rapidly in size (median diameter = 4.15 mm, N = 7, vs. E 1.92 mm, N = 8, in January; Mann-Whitney Z .T 0) = -3.24; P < 0.01). From January to April (i.e., 0 during gestation), the corpora lutea decreased , N D J F M A slightly in size. However, there were no signifi- Month cant changes in their diameter (Kruskall-Wallis H3 = 7.69, N = 40, P > 0.05). After parturition, FIG.4. Monthlyvariation in (top) the averageegg wet mass and the diameter of em- the size reduction was faster, and by June cor- (bottom) average Values the + 1 were almost even bryos. presented represent average pora lutea indistinguishable, standarderror. with the aid of a microscope.

Gestationand Parturition Litter Size The number of oviductal female var- Pregnancy lasted approximately five months, eggs per ied from three to 10 ? N = Mean from late November/early December to late (6.48 0.25; 50). RCM and REM were 0.2 ? 0.011 and 0.033 ? April/early May. Embryonic development was 0.003, RCM and relatively slow during the first gestational respectively. Nevertheless, REM values increased over months (December to February, when ambient significantly gestation = -2.46 + 0.43 (month), r2 = temperature is at its lowest). In February, the [log(RCM) N = 50, P < and = 0.09 mean diameterof embryosfrom 10 females (one 0.60, 0.0001; (REM)1/2 + 0.04 r2 = 0.73, N = 50, P < 0.0001, embryo per female) was only 7.7 ? 0.54 mm. In (month), Table 1]. Litter size was this month, the embryos reachedthe embryonic respectively, (LS) posi- tively correlated with body mass (LS = 0.171 + stage number 31, 32, 33, or 35 (in one, two, six, 1.42 BM, r2 = 0.42, N = 50, P < 0.01) and size and one females, respectively). From February of pregnant females (LS = -7.83 + 1.60SVL, r2 to March, continued to embryos develop slowly, = 0.40; N = 50, P < 0.01). Likewise, litter mass whereas from March to their mean di- April (LM) increased with female size (LM = 0.16 + doubled and em- ameter nearly (Fig. 4), April 8.14 SVL, r2 = 0.26, N = 50, P < 0.01) and fe- bryos close to parturition(embryonic stage 40) male body mass (LM = 1.65 + 21.11BM, r2 = weighed four times as much as the March em- 0.30, N = 50, P < 0.01). The average mass of bryos (embryonic stage 36). Parturition occurred oviductal eggs was not correlated with LS, SVL, between late April and early May. or BM (P > 0.05). Relative litter mass was not During gestation, a significant increase in the correlated with any of these variables either (P average wet mass of oviductal eggs was evident > 0.05). However, REM was negatively correlat- = (F4,45 36.7, P < 0.0001; Fig. 4). In contrast, the ed with LS (RCM = -0.004LS + 0.058, r2 = average dry mass of the eggs decreased consid- 0.21, P < 0.05) and SVL (RCM = 0.007SVL + erably during the gestation. At the onset of de- 0.096, r2 = 0.11, P < 0.05). velopment, mean dry egg mass was 0.26 ? 0.01 g, whereas at the end of development mean dry TesticularCycle egg mass was only 0.18 ? 0.01 g. This difference Testicular mass changed significantly during = = was highly significant (t2 5.64; P < 0.001). the year (F 158 36.5, P < 0.001; Fig. 3). From

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TABLE1. Relative litter mass (RCM) and relative egg mass (REM) values for different time intervals in embryonic development (and throughout gestation) of Sceloporustorquatus torquatus.

RCM REM LS x _ SEEx + SE Month N x + SE (range) (range) November-January 18 7.0 + 0.6 0.13 + 0.007 0.019 _ 0.001 (0.09-0.19) (0.012-0.037) February-March 22 6.7 + 0.3 0.21 ? 0.009 0.034 + 0.001 (0.12-0.27) (0.028-0.043) April-May 9 6.0 + 0.4 0.33 ? 0.025 0.052 + 0.003 (0.24-0.48) (0.037-0.073) November-May 50 6.5 + 0.25 0.20 ? 0.011 0.033 ? 0.003 (0.09-0.48) (0.012-0.073)

December to May, testes remained small, show- terial ingested showed no significant differences ing their minimum size and mass in February. between months in either sex (Kruskall-Wallis Testicular growth was most evident from June H, = 12.8 and 14.5 for males and females, re- to September, being faster in July and August. spectively; P > 0.05; Fig. 5). During the wet sea- In these months, testicular mass increased sig- son, the average volume of the stomach contents nificantly. Testicular regression began in Octo- for males and females was 1.22 ? 0.13 ml and ber, after the testes had reached their maximum 1.08 ? 0.08 ml, respectively. These averages size in September. In October and November, were not significantly different (t92 = -0.99; P reductions in testicular mass were significant, > 0.05). Similarly, in this period the amount of and it was actually in these months that essen- plant material consumed by males and females tially all of the decrease in testicular mass took were not significantly different (median = 10.8 place, even though from December to February, and 9.7, respectively; Mann-Whitney Z = -0.90, the testes suffered a slight, further decrease in P > 0.05). With regard to incidence, 18 of 42 mass. In the latter month, the testes size was males (42.8%) and 30 of 58 females (55.1%) con- only about 3.33% of their size in September. sumed plant material. In the dry season, male stomach content volume was greater than fe- Food Consumption male stomach content volume (0.59 ? 0.07 ml There were no noticeable differences in the vs. 0.27 + 0.03 ml; t, = -4.9; P < 0.001). The type of prey consumed by male and female S. amount of plant material consumed was signif- torquatus (Table 2). In both sexes, the stomach icantly greater in males than in females (median = contained mainly insects and to a lesser extent 11.6 and 10.7, respectively; Mann-Whitney Z = spiders, isopods, centipedes, and plant material -2.3, P > 0.05). Fourteen of 21 males (66%) (mainly small flowers and fruits). However, in and 34 of 61 females (55.7%) consumed plant October the remains of a S. torquatuswere found material. in the stomach of a male. the wet During season, DISCUSSION the most important prey items were coleopterans, hymenopterans, homopterans, lepidopter- Ovarian Cycle ans (larvae), and hemipterans, in that order. The reproductive pattern of the females of S. During the dry season, the types of prey con- t. torquatusfrom the Pedregal de San Angel is sumed were essentially the same, although the similar to that exhibited by the population of S. most important prey items were hymenopter- torquatusin Teotihuacan, state of Mexico (Guil- ans, hemipterans, orthopterans, homopterans, lette and Mendez-de la Cruz, 1993), in other and coleopterans, in that order. Thus, lepidop- species of the torquatus group (Crisp, 1964; teran larvae were less important in the dry sea- Goldberg, 1971; Ballinger, 1973; M6ndez-de la son, whereas the importance value for the or- Cruz et al., 1988), and all viviparous species of thopterans increased. Also, if the immature Sceloporussurveyed to date, except for S. bican- stages are taken into account, the consumed thalis (Guillette and Casas-Andreu, 1980; Guil- prey diversity was larger in the wet than in the lette and Sullivan, 1985; Guillette and Bearce, dry season. 1986; Guillette and Mendez-de la Cruz, 1993). The average volume of food ingested per in- Furthermore, fall breeding followed by gestation dividual was significantly larger in the wet than in winter and parturition in spring is exhibited in the dry season both in male and females (t65 by other, more distantly related, viviparous liz- = 3.89, P < 0.001, and to10= 9.55, P < 0.001, ards, such as Barisia imbricata(Guillette and Ca- respectively). However, the volume of plant masas-Andreu, 1987), Liolaemushuacahuasicus (Ra-

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TABLE2. Volume,incidence, density, and importancevalues for the prey taxa found in the stomachcontents of Sceloporustorquatus torquatus during the wet and dry seasons.

Prey taxon Volume(ml) Incidence Numberof individuals Importancevalue Wet season (N: = 98) Coleoptera adults 16.217 82 373 0.721 Larvae 2.205 13 80 0.123 Pupae 0.031 1 1 0.004 Hymenoptera adults 16.175 52 590 0.760 Larvae 0.633 3 3 0.020 Homoptera adults 9.232 56 357 0.528 Nymphs 0.297 3 9 0.018 Lepidoptera (larvae) 15.276 35 69 0.375 Hemiptera adults 1.96 22 62 0.135 Nymphs 0.312 2 18 0.022 Diptera adults 0.706 9 16 0.048 Larvae 0.277 6 2 0.024 Pupae 0.117 6 5 0.022 Orthoptera 1.915 5 10 0.050 Dermaptera 0.233 6 6 0.026 Neuroptera 0.212 3 4 0.015 Aranae 0.587 10 15 0.049 Oligochaeta 0.759 4 10 0.030 Isopoda 0.381 6 7 0.027 TOTAL 67.525 324 1637 Dry season (N 61) Hymenoptera 4.432 66 113 0.805 Hemiptera 3.816 27 58 0.439 Ortoptera 7.928 12 17 0.411 Homoptera 4.124 26 45 0.411 Coleoptera adults 1.6 26 31 0.274 Larvae 0.465 5 7 0.062 Diptera adults 1.108 13 43 0.225 Larvae 0.072 1 1 0.010 Lepidoptera (larvae) 0.906 11 12 0.121 Neuroptera 0.034 1 1 0.009 Aranae 0.361 10 14 0.101 Isopoda 0.753 8 10 0.096 Chilopoda 0.298 3 2 0.031 TOTAL 25.897 209 354

mirez, 1991), and Eumecescopei and E. lynxe (Ra- mirez-Bautista et al., 1996, 1998). However, other viviparous lizards showing fall ovarian activity ovulate in late winter to early spring, and give birth in summer (e.g., Cordylus p. polyzonus, C. lo 1.2 giganteus, and Pseudocordylusm. melanotus;Flem- ming and Van Wyk, 1992; Flemming, 1993; Van -0 Wyk, 1994) or early spring to midsummer, after approximately 14 months of gestation (e.g., Ho- 0 plodactylusmaculatus; Cree and Guillette, 1995). Gestationand Parturition Oviductal eggs lost about 30% of their dry mass during embryonic development, whereas J F M A M J J A S N D their wet mass increased by more than 100%. Month This pattern of change in the egg dry and wet FIG. 5. Mean volumes for the stomach masses is typical of oviparous species, in which monthly the mother no material to the contents of Sceloporustorquatus torquatusat the Pedre- provides organic gal de San Angel, Distrito Federal. Hatched and stip- developing embryos (Blackburn, 1994). In vivip- pled areas represent animal and plant material, re- arous species, egg wet mass increases markedly spectively. during embryonic development, because the

This content downloaded by the authorized user from 192.168.52.76 on Mon, 10 Dec 2012 13:41:45 PM All use subject to JSTOR Terms and Conditions 110 M. FERIA ORTIZ ET AL. mother usually provides water to the embryos TesticularCycle the direction and (Blackburn,1994). However, The testicular in the of S. t. extent of in mass varies cycle population change egg dry among from the de San is sim- In bistriataand M. essen- torquatus Pedregal Angel species. Mabuya heathi, ilar to that exhibited the of the all neonate mass is by population tially dry acquiredduring same near Teotihuacan, in the state of and Blackburn, species embryonic development (Vitt Mexico (Guillette and Mendez-de la Cruz, 1983, 1991), whereas in Barisia imbricata(Guil- 1993). It is also similar to those in other species lette and Casas-Andreu, 1987) and Lacertavivi- of the S. group (Goldberg, 1971; Ballin- para (Avery, 1975), the dry mass of the torquatus freshly ger, 1973; Garrick, 1974; Mendez-de la Cruz et ovulated is similar to that of the neonate. In egg al., 1994). As in the case of the ovarian cycle, the most S. t. surveyed species, including torquatus, similarity between the testicular cycles in the mass decreases to some extent, indicat- egg dry species of the S. group could be a re- that of the is used in catabolic re- torquatus ing part yolk sult of their phylogenetic relationship. However, actions to sustain and of development growth a population of S. mucronatus from the Stewart and Cas- Ajusco embryos (Thompson, 1981; Mountain exhibits a testicular cycle that differs tillo, 1984). For instance, in Sphenomorphusquoyii, from that found in S. in that testicular lose 10% of their mass torquatus eggs dry during embry- mass is largest in spring-summer, long before onic and there is no need to development, sup- ovulation takes place (M6ndez-de la Cruz et al., the receive ma- pose that embryos any organic 1988). The testicular cycle exhibited by S. mu- from mother terial the (Thompson, 1981, 1982). cronatusalso occurs in viviparous groups of Sce- t. mother It is possible that, in S. torquatus,the loporus (e.g., Guillette and Casas-Andreu, 1980; provides water and inorganic ions to the embry- Guillette and Sullivan, 1985). However, a fall os, and lipids and proteins in the yolk represent testicular cycle also is exhibited by other, more the main source of energy to sustain and nour- distantly related viviparous lizards such as the ish embryonic development. However, it is still tropidurid Liolaemus huacahuasicus (Ramfrez, necessary to analyze the chemical composition 1991), the cordylid Cordylusgiganteus (Van Wyk, of the freshly ovulated eggs and neonates to de- 1995), and the scincid Eumeceslynxe (Ramirez- termine the degree of lecithotrophy in this spe- Bautista et al., 1998). This suggests that environ- cies (Blackburn, 1994). mental conditions may affect male and female reproductive activity in different ways. Litter Size In S. mucronatus and S. jarrovi, testes have from December, Mean litter size of S. t. torquatusin the Ped- sperm August through early a regal de San Angel was smaller than that re- which suggests reproductive activity period of about four and a half ported by Guillette and Mendez-de la Cruz months (Goldberg, 1971; Cruz et al., Given the re- (1993) for the population of S. torquatusat Teo- Villagran-Santa 1994). semblance between the testicular of these tihuacan, Mexico. In a prior paper, Mendez-de cycles and that of S. it is that la Cruz et al. (1992b) compared the litter sizes species torquatus, possible in this takes the fall of these populations and suggested that the species mating place during months. a was observed smaller litter size in the population at the Ped- Indeed, mating attempt in October. regal de San Angel was because of the relatively low primary productivity in this area, a result Diet of poor soil accumulation. Olsson and Shine (1997) demonstrated that, in Diet of male and female S. t. torquatuswere Lacertaagilis, clutch and hatchling sizes are in- similar, consisting mainly of terrestrial inverte- versely correlated. In S. t. torquatus, litter size brates (mostly insects) and, to a lesser extent, and average oviductal egg mass were not cor- plant material (small flowers and fruits). These related. In addition, REM decreased with snout- results are similar to those reported by Burquez vent length and litter size, whereas RCM and et al. (1986) for this population. An omnivorous SVL were not correlated. In S. t. torquatus,like diet also has been reported in several species many other species surveyed, litter size increas- with small body size (Banta, 1961; Smith and es with female size; however, in this species, un- Milstead, 1971; Mendez-de la Cruz et al., 1992a). like other species of lizards (Stewart, 1979; Ols- However, the advantage represented by the in- son and Shine, 1997), egg mass is similar in fe- gestion of plant food is still unclear. As expect- males of different sizes. This suggests that a ed, food consumption was lower in the dry than particular neonate size could be favored by nat- in the wet season. However, the fact that in the ural selection. A similar situation was found in dry season food consumption in females was the oviparous lizards Uta stansburiana(Ferguson about half of that in males indicates there are et al., 1990) and Sceloporusvirgatus (Smith et al., other factors that influence food consumption in 1995). females. In the dry months of the year, females

This content downloaded by the authorized user from 192.168.52.76 on Mon, 10 Dec 2012 13:41:45 PM All use subject to JSTOR Terms and Conditions DIET AND REPRODUCTION OF SCELOPORUS TORQUATUS 111 are pregnant, and the volume occupied by the 1990. Proximate control of variation of clutch, egg, embryos in their bodies may limit food inges- and body size in a West-Texas population of Uta tion (Mendez-de la Cruz et al., 1992a). Also, re- stansburiana stejnegeri (Sauria: Iguanidae). Herpe- duced food ingestion could be caused by a di- tologica 46:227-238. FERIA-ORTIZ,M. 1989. Contribuci6n al conocimiento minished appetite in pregnant females brought del ciclo de vida de Sceloporus torquatus about by (Crews and Garrick, torquatus progesterone (Lacertilia: Iguanidae) al sur del Valle de Mexico. 1980). Bol. Soc. Herpetol. Mex. 1:31-33. Acknowledgments.-We thank G. Casas-Andreu FITCH,H. S. 1970. Reproductive cycles of lizard and for his support and for making available the fa- snakes. Univ. Kans. Publ. Mus. Nat. Hist., Misc. cilities at the herpetological collection of the In- Publ. 52:1-124. FLEMMING, A. F 1993. The female stituto de Biolologia, Universidad Nacional Au- reproductive cycle of the lizard m. melanotus tonoma de Mexico, for the of this Pseudocordylus (Sauria: completion J. 27:103-107. E Mendez-de la Cruz and W. Cordylidae). Herpetol. study. Hodges FLEMMING,A. F, AND H. J. VAN WYK. 1992. The fe- useful comments on the provided manuscript. male reproductive cycle of the lizard Cordylus p. Financial support for this study was received polysonus (Sauria: Cordylidae) in the southwestern from the Direccion General de Asuntos del Per- Cape Province, South Africa. J. Herpetol. 26:121- sonal Academico, Universidad Nacional Auton- 127. oma de Mexico (DGAPA grant IN206695), while GARRICK, D. L. 1974. Reproductive influences on be- this paper was being written. havioral thermoregulation in the lizard, Sceloporus cyanogenys.Physiol. Behav. 12:85-91. LITERATURECITED GOLDBERG,S. R. 1971. Reproductive cycle of the ovo- AVERY,R. A. 1975. Clutch size and reproductive ef- viviparous iguanid lizard Sceloporusjarrovi Cope. fort in the lizard Lacertavivipara (Jacquin). Oecol- Copeia 1972:227-232. ogia 19:165-170. GUILLETTEJR., L. J., AND D. A. BEARCE.1986. The re- BALLINGER,R. E. 1973. Comparative demography of productive and fat body cycles of the lizard, Sce- two viviparous iguanid lizard (Sceloporusjarrovi loporus grammicus disparilis. Trans. Kansas Acad. and Sceloporuspoinsetti). Ecology 54:269-283. Sci. 89:31-39. . 1983. Life-history variations. In R. B. Huey, E. GUILLETTEJR., L. J., AND G. CASAS-ANDREU.1980. Fall R. Pianka, and T. W. Schoener (eds.), Lizard Ecol- reproductive activity in the high altitude Mexican ogy: Studies of Model Organism, pp. 241-259. lizard, Sceloporusgrammicus microlepidotus.J. Her- Harvard Univ. Press, Cambridge, Massachusetts. petol. 14:143-147. BANTA, B. H. 1961. Herbivorous feeding of Phryno- . 1987. The reproductive biology of the high soma platyrhinosin southern Nevada. Herpetologica elevation Mexican lizard, Barisia imbricataimbricata, 17:136-137. with notes on the other imbricatasubspecies. Her- BENABIB, M. 1994. Reproduction and lipid utilization petologica 43:29-38. of tropical populations of Sceloporusvariabilis. Her- GUILLETTEJR., J. L., AND F R. MENDEZ-DE LA CRUZ. petol. Monogr. 8:160-180. 1993. The reproductive cycle of the viviparous BLACKBURN,D. G. 1994. Standardized criteria for the Mexican lizard Sceloporustorquatus. J. Herpetol. 27: recognition of embryonic nutritional patterns in 168-174. squamate reptiles. Copeia 1994:925-935. GUILLETTEJR., L. J., AND W. P. SULLIVAN. 1985. The 0. AND A. BURQUEZ, A., FLORES-VILLELA, HERNANDEZ. reproductive and fat body cycles of the lizard, Sce- 1986. in a small Scelo- Herbivory Iguanid lizard, loporusformosus. J. Herpetol. 19:474-480. porus J. 20:262-264. torquatus torquatus. Herpetol. MENDEZ-DE LA CRUZ, F R., L. J. GUILLETTE JR., M. VIL- CREE,A., AND L. GUILLETTE 1995. Biennial re- J. JR. LAGRAN-SANTA CRUZ, AND G. CASAS-ANDREU. production with a fourteen-month pregnancy in 1988. Reproductive and fat body cycles of the vi- the gecko Hoplodactylus maculatus form Southern viparous lizard, Sceloporus mucronatus (Sauria: Ig- New Zeland. J. Herpetol. 29:163-173. J. 22:1-12. CREWS,D., AND L. D. GARRICK.1980. Methods of in- uanidae). Herpetol. MENDEZ-DE LA CRUZ, F R., G. CASAS-ANDREU, AND ducing reproduction in captive reptiles. In J. B. M. VILLAGRAN-SANTA CRUZ. 1992a. Variaci6n an- Murphy and J. T. Collins (eds.), Reproductive Bi- ual en la alimentaci6n condici6n ffsica de Scelo- ology and Diseases of Captive Reptiles, pp. 49-70. y mucronatus en la Sierra Society for the Study of Amphibians and Reptiles. porus (Sauria: Iguanidae) Lawrence, Kansas. del Ajusco, Distrito Federal, M6xico. Southwest. CRISP,T. 1964. 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