Ecology of the Gecko Gymnodactylus geckoides amarali in a Neotropical Savanna

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———, H. M. A. MENDES, V. B. ASSIS, AND M. C. KIEFER.2002. Reproduction of Tropidurus montanus Ro-drigues, 1987 (Tropiduridae), a lizard from a sea-sonal habitat of southeastern Brazil, anda comparison with other Tropidurus species. Her-petological Journal 12:89–97.

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———. 1990. The influence of foraging mode andphylogeny on seasonality of tropical lizardreproduction. Papeis Avulsos de Zoologia 37:107–123.

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Accepted: 11 August 2003.

Journal of Herpetology, Vol. 37, No. 4, pp. 694–706, 2003Copyright 2003 Society for the Study of Amphibians and Reptiles

Ecology of the Gecko Gymnodactylus geckoides amaraliin a Neotropical Savanna

GUARINO R. COLLI,1 DANIEL O. MESQUITA, PAULO V. V. RODRIGUES, AND KINITI KITAYAMA

Departamento de Zoologia, Universidade de Brasılia, 70910-900 Brasılia,Distrito Federal, Brazil, tel/fax: þ55-61-307-2092

ABSTRACT.—We describe the ecology of the gecko Gymnodactylus geckoides amarali in the Cerrado of central

Brazil and using published data, compare it with the conspecific Gymnodactylus geckoides geckoides from the

Caatinga of northeastern Brazil. Gymnodactylus geckoides amarali is rupicolous, living primarily in rockcrevices in ‘‘campos rupestres’’ (rocky fields), which are highly patchy in Cerrado. Field body temperatures

were low and associated with environmental temperatures, suggesting thermoconformity. Termites were the

most important food item, and consumption was greatest during the dry season. We suggest that access totermites is facilitated by the shallow soils used by G. g. amarali and by its well-developed chemosensory

apparatus. Reproduction was concentrated in the dry season, a pattern known for very few Cerrado

squamates, possibly because of the higher availability of termites during that period. Clutch size was

significantly correlated with female size, a pattern unknown in any other gecko, and there was no associationbetween egg size and female size. Gymnodactylus geckoides amarali produced larger clutches of smaller eggs

relative to G. g. geckoides, presumably because of the high climatic unpredictability of the Caatinga. We

detected a significant sexual dimorphism in both body size and shape: females were larger and had smaller

heads than males. We suggest that large female size is likely a plesiomorphic character of gekkonids and thatlarge head size in males results from sexual selection theory.

Covering an area of approximately 2,000,000km2, the Cerrado is the second largest Brazilianbiome (Oliveira and Marquis, 2002). This Neo-

tropical savanna is currently one of the mostthreatened biomes of South America because ofthe expansion of agriculture. Among the approx-imately 50 lizard species that inhabit the Cerrado,five are members of the Gekkonidae: the gek-

1 Corresponding Author. E-mail: [email protected]

694 C. A. B. GALDINO ET AL.

konines Gymnodactylus geckoides, Hemidactylusmabouia, and Phyllopezus pollicaris, and thesphaerodactylines Coleodactylus brachystoma andColeodactylus meridionalis (Colli et al., 2002). Withthe exception of H. mabouia, an introducedspecies that is abundant in anthropical areas(Vanzolini, 1968, 1978), Cerrado geckos areinconspicuous and relatively uncommon inscientific collections. For example, Vitt (1991)noted a lack of gekkonids at Alto Araguaia inBrazil, attributing this result to the absence ofappropriate microhabitats. If, as put by Doughtyand Shine (1995), natural history studies ongeckos are rare, detailed works on the ecologyof Cerrado gekkonids are simply nonexistent.The few ecological studies on Brazilian geckoswere carried out in Amazonia (e.g., Ramos, 1981;Nunes, 1984; Avila-Pires, 1995; Vitt and Zani,1997; Vitt et al., 1997, 2000), Caatinga (Vitt, 1986,1995), and Restinga (Araujo, 1991; Zamprognoand Teixeira, 1998).

Lizards have contributed significantly to eco-logical theory, including population and commu-nity ecology, foraging and life-history theory, andthe growing field of comparative biology (Hueyet al., 1983; Vitt and Pianka, 1994; Pianka and Vitt,2003). However, most studies were performedeither in the temperate zone or on tropical anoles.The generality of such theoretical advances to thediverse tropical lizard fauna remains to bedetermined. For example, both historic (phylo-genetic) and present-day (ecological) factors in-fluence lizard life histories (e.g., Dunham et al.,1988). Therefore, synapomorphies of lineagesrestricted to the Neotropical region and under-represented in life-history studies, such as Gym-nophthalmidae,Hoplocercidae,Leiosauridae,andSphaerodactylini, might affect life-history theory.In addition, tropical regions are characterizedby unique ecogeographic features and conditionsthat may influence lizard ecologies in ways thatchallenge the generality of life-history models.Most studies on tropical lizards come fromrelatively aseasonal forested biomes, whereasthose from strongly seasonal, open vegetationbiomes are still poorly known (Colli et al., 2002).

Gymnodactylus geckoides contains two re-cognized subspecies: G. g. geckoides from theCaatinga and G. g. amarali from the Cerrado(Vanzolini, 1953, 1968). The only detailed workson the ecology of the genus were carried out onG. g. geckoides in the Caatinga (Vitt, 1986, 1995).Herein we present new data on the ecology ofG. g. amarali from the Cerrado of central Brazil.We report on habitat use, thermal biology,sexual dimorphism, diet, and reproduction andmake comparisons with published accounts onG. g. geckoides from the Caatinga and otherNeotropical geckos, when appropriate. Becausethe Cerrado and Caatinga biomes differ con-

siderably in several features, such as climatepredictability (Nimer, 1989), we attempt toidentify effects of environmental conditions uponthe ecology of G. geckoides, by comparing twovery closely related taxa from different regions.

MATERIALS AND METHODS

Study Sites and Specimens.—We collected spe-cimens at three localities in central Brazil: AltoParaıso de Goias (148079S, 4783’W; N 5 19),Minacu (13849’S, 48820’W; N 5 288), and Pir-enopolis (15851’S, 48857’W; N 5 60), all in thestate of Goias. All specimens were deposited atthe ‘‘Colecao Herpetologica da Universidade deBrasılia’’ (CHUNB). Climate is strongly predict-able and seasonal, with a wet season fromOctober to April receiving almost all of the1500–2000 mm of annual precipitation, anda dry season from May to September (Nimer,1989). Annual temperatures average 20–228C,and minimum and maximum daily temperaturesdrop noticeably during the dry months (Nimer,1989). The phytophysiognomy varies from ex-tensive grasslands with few trees to grasslandswith dense stands of stunted trees, forminga nearly closed canopy in some areas. Trees aretortuous, with thick bark, xeromorphic leaves,and deep root systems, apparently adapted tonatural sporadic fires and soils that are poor innutrients and rich in aluminum. See Oliveira andMarquis (2002) for a review on the Cerrado.

Habitat, Microhabitat, and Temperatures.—Ap-proximately two-thirds (N 5 220) of the speci-mens were collected by third parties during theflooding of the Serra da Mesa hydroelectric damat Minacu, from November 1996 to August 1997.We hand collected the remaining one-third (N 5147) of specimens, recording habitat and micro-habitat at the capture site. We used the followingmicrohabitat categories: rock crevice, termitenest, rock, and ground. All individuals werecollected during the day. Immediately aftercapture, we took cloacal, air, and substratetemperature of 28 individuals using a Millerand Weber� cloacal thermometer. In the lab,geckos were killed by injection with Tiopental�,measured, and fixed with 10% formalin.

Sexual Dimorphism.—From each individual, werecorded the following morphometric variables:snout–vent length (SVL), body width (at broad-est point), body height (at highest point), headwidth (at broadest point), head height (at highestpoint), head length (from tip of snout to anteriormargin of ear opening), and tail length (fromcloaca to tip of tail). We took all measurementswith Mitutoyo� electronic calipers, to the nearest0.01 mm. Since the majority of the individualshad broken tails, we excluded tail length from theanalyses. We also log-transformed (base 10) allmorphometric variables prior to analyses. To

ECOLOGY OF GYMNODACTYLUS GECKOIDES AMARALI 695

partition the total morphometric variation be-tween size and shape variation, we defined bodysize as an isometric size variable (Rohlf andBookstein, 1987) following the procedure de-scribed by Somers (1986): we calculated anisometric eigenvector, defined a priori withvalues equal to p�0.5, where p is the number ofvariables (Jolicoeur, 1963), and obtained scoresfrom this eigenvector, hereafter called body size,by postmultiplying the n 3 p matrix of log10

transformed data, where n is the number ofobservations, by the p 3 1 isometric eigenvector.To remove the effects of body size from thelog10-transformed variables we used Burnaby’smethod (Burnaby, 1966): we postmultiplied then 3 p matrix of the log10-transformed data by ap 3 p symmetric matrix, L, defined as:

L ¼ Ip � VðVTVÞ�1VT ;

where Ip is a p3p identity matrix, V is the isometricsize eigenvector defined above, and VT is thetranspose of matrix V (Rohlf and Bookstein, 1987).Hereafter we refer to the resulting size-adjustedvariables as shape variables. To test the null hy-pothesis of no difference between sexes, we con-ducted separate analyses of variance on body size(ANOVA) and the shape variables (MANOVA).

Diet Composition.—We removed stomachs bydissection and examined their contents undera stereomicroscope. We identified prey itemsusually to the ordinal level, recorded the lengthand width (60.01 mm) of intact items witha micrometric ocular, and estimated prey volume(V) as an ellipsoid:

V ¼ 4

3p

w

2

� �2 l

2

� �;

where w 5 prey width and l 5 prey length. Wecalculated numeric and volumetric percentagesof each prey category for each lizard, to obtainmean values per stomach. We also obtainednumeric and volumetric percentages frompooled stomachs. From these percentages, wecomputed niche breadths (B) for each individualand for pooled stomachs, using the inverse ofSimpson’s diversity index (Simpson, 1949):

B ¼ 1Pn

i¼1

p2i

;

where i stands for prey category, n for number ofcategories, and p for the numeric or volumetricproportion of prey category i. We also calculatedpercentage of occurrence of each prey category(number of stomachs containing prey category i,divided by total number of stomachs). Weexcluded from analyses of volumetric represen-tation prey items that were too fragmented toallow a reliable estimation of their volumes.

To investigate the relationship between preydimensions and head dimensions, we conducteda canonical correlation analysis between two setsof variables: maximum prey length and maxi-mum prey width versus lizard head width,height, and length. Canonical correlation analy-sis finds a linear function from each set ofvariables, termed the first canonical variables,maximizing the correlation between them. Next,successive pairs of canonical variables are calcu-lated, such that the correlation between twocanonical variables of each pair is also maxi-mized and each successive pair is uncorrelatedwith all the preceding canonical variables(Tabachnick and Fidell, 2001). The first canonicalcorrelation is at least as large as the multiplecorrelations between any variable and the oppo-site set of variables. To determine how well preydimensions can be predicted from the canonicalvariables of head dimensions, we also performeda canonical redundancy analysis.

Reproduction.—We determined the sex of eachindividual by dissection and direct examinationof the gonads. We considered females as re-productively active by the presence of vitello-genic follicles or oviductal eggs and males asreproductively active by the presence of enlargedtestes and convoluted epididymides. For repro-ductively active females, we counted and mea-sured width and length (to the nearest 0.01 mm)of vitellogenic follicles and oviductal eggs. Weconsidered presence of enlarged vitellogenicfollicles and either oviductal eggs or corporalutea as evidence of sequential production ofmore than one clutch of eggs. Further, weestimated size at maturity for females based onthe smallest individual containing vitellogenicfollicles or oviductal eggs and, for males, basedon the smallest individual bearing enlargedtestes and convoluted epididymides.

We analyzed monthly distributions of adultsaccording to reproductive condition to determinetiming of reproduction. By pooling individualscollected during different years, we recognizethat some error was introduced in estimating re-productive cycle, presumably caused by annualvariations in amount and distribution of pre-cipitation. However, we assumed that this errorwas small, because (1) average annual deviationsin precipitation from the normal are less than15% in the Cerrado (Nimer, 1989) and (2) abouttwo-thirds of the individuals were collected ina single year.

Statistical Analyses.—We carried out statisticalanalyses using SYSTAT 5.2.1 (SYSTAT, Inc., Cary,North Carolina, 1992) and SAS 6.12 (SAS In-stitute, Inc., Cary, North Carolina, 1988), both forMacintosh, and used a significance level of 5% toreject null hypotheses. Data are expressed asmeans 6 1 SD.

696 G. R. COLLI ET AL.

RESULTS

Habitat, Microhabitat, and Temperatures.—Inthe localities sampled, G. g. amarali was foundexclusively in rocky habitats (‘‘campos ru-pestres’’). In these areas, soils were often lessthan 1 m deep over a solid bedrock (lithosols),and the vegetation was low and sparse (Fig. 1,top). Twenty-eight (89%) individuals collectedwere in rock crevices, whereas remaining indi-viduals were on rocks (7%) or on the ground(4%). All individuals were motionless at firstsight; 68% remained still after approachedwhereas the remaining individuals fled into rockcrevices. When cornered, G. g. amarali oftenexhibited a display in which the tail, usuallybearing transverse white bands, was lifted andheld still (Fig. 1, bottom). We also made un-quantified observations of individuals active inlate afternoon on rock piles.

Body temperatures averaged 30.262.68C (N 528, range 5 26.2–34.08C); substrate temperaturesaveraged 26.8 6 2.58C (range 5 24.0–34.08C); airtemperatures at 5 cm from the substrate averaged26.5 6 2.18C (range 5 23.0–32.08C); and shadedair temperatures averaged 25.76 2.28C (range 522.2–29.68C). A stepwise multiple regressionanalysis indicated that body temperature wasmost strongly associated with air temperature at5 cm from the substrate (model selected: bodytemperature 5 0.8 3 air temperature þ 8.9; r 50.65; P , 0.001). The Caatinga G. g. geckoides (Vitt,1995) exhibits a significantly higher body tem-perature than G. g. amarali (33.5 6 0.5, N 5 10,t36 5 6.3, P , 0.001).

Sexual Dimorphism.—The smallest individualexamined was a female measuring 20.04 mmSVL, whereas the largest individual was a femalemeasuring 54.70 mm SVL. The largest malemeasured 52.48 mm SVL. Sexes differed signif-icantly in body size (ANOVA F1,368 5 4.72, P 5

0.03), with females larger than males (Table 1). Inaddition, there was a significant differencebetween the sexes in shape variables (MANOVAWilk’s Lambda 5 0.93, P , 0.001). To determinewhich of the shape variables contributed most tosexual dimorphism, we performed a stepwisediscriminant analysis using the stepwise methodof variable selection and Wilk’s Lambda as theindicator of discriminatory power (SAS Institute,Inc., Cary, North Carolina, 1988). Three shapevariables were selected as the most powerful dis-criminators of the two sexes (Table 2). Adjustedhead width was the first to be selected, correctlyclassifying 59.7% of the individuals. The discrim-inant function based on both adjusted headwidth and adjusted body width classified 63.2%of the lizards correctly. The addition of adjustedSVL to the model did not improve its classifica-tion power (Table 2). Analyses indicate that

adjusted head width and adjusted body widthwere the most powerful discriminators of thesexes, with males having larger heads, whereasfemales were stockier (Fig. 2, Table 1).

Diet Composition.—A relatively small propor-tion (17.6%) of individuals examined had emptystomachs. We recorded 24 prey categories, by farthe most frequent of which was termites (40%),followed by nonidentified arthropods (20.8%),and ants (18%) (Table 3). Based on the meannumber of prey items per stomach, the dietconsisted mainly of termites (39%), nonidentifiedarthropods (19.3%), and ants (14.5%), whereastermites (68%) and ants (12.9%) dominatedvolumetrically (Table 3). The mean diversityindexes, calculated for numeric and volumetricpercentages of prey, were 1.39 6 0.62 (N 5 204)and 1.04 6 0.16 (N 5 40), respectively.

Results based on data from pooled stomachswere similar to results on a per stomach basis.Numerically, the diet consisted mainly of ter-mites (59%) and ants (17%), while termites (81%)dominated volumetrically (Table 3). The diversityindex calculated from numeric percentages ofprey was 2.61, whereas using volumetric per-centages of prey it was 1.50. Overall, dietarydiversity was low and the diet consisted largelyof termites, followed by ants. Importance oftermites (mean percentage of termite number inthe diet plus mean percentage of termite volumein the diet, divided by two) in the diet was higherin the dry season than in the rainy season (dryseason: mean 5 33.23 6 30.41; rainy season: 5mean 5 12.13 6 22.39; ANOVA of arcsine-transformed data: F1,221 5 25.98, P , 0.0001).

Correlations between prey and head measure-ments were low. The lowest correlation was 0.16,between prey width and head width. The largestcorrelation was 0.33, between prey length andhead length. The first canonical variable for headmeasurements was a contrast between headheight and head length, with more emphasis onhead length, whereas the second was a contrastbetween head width and head height. The firstcanonical variable for the prey measurementswas a contrast between maximum prey widthand maximum prey length, with more emphasison the latter, whereas the second canonicalvariable put more emphasis on the former. Thefirst canonical correlation was 0.44, but thehypothesis that all canonical correlations werezero was not rejected (P 5 0.21); thus, no firmassociation between body dimensions and preydimensions could be established. Indeed, thecanonical redundancy analysis indicated thatneither of the two canonical variables for headmeasurements were good predictors of preymeasurements, with only 10% of the variance inthe latter being explained by the former.


FIG. 1. (Top) Typical habitat of Gymnodactylus geckoides amarali. Locality shown is Pirenopolis, Goias state,Brazil. (Bottom) Adult individual of G. g. amarali showing defensive tail display.


Reproduction.—The smallest reproductive fe-male measured 38.57 mm SVL, whereas thesmallest reproductive male measured 28.94 mmSVL (Fig. 3). Clutch size, based on presence ofeggs or vitellogenic follicles, averaged 1.6560.48(range 5 1–2, N 5 32). When females had twofollicles (N 5 6) or two oviductal eggs (N 5 13),both follicles or eggs were at the same stage ofdevelopment. Females with a clutch size of twowere significantly larger than those with a clutchsize of one (mean 5 45.54 6 2.83 vs. mean 541.60 6 1.89, respectively; F1,31 5 18.45, P ,0.001). Mean egg length was 8.77 6 0.64 mm,mean egg width was 5.72 6 0.47 mm, and meanegg volume was 151.92630.15 mm3 (based on 22oviductal eggs). Apparently, oviductal eggs areelongated, becoming more spherical after de-position. Egg volume was not correlated withfemale SVL (r 5 0.25, N 5 22, P 5 0.26) and therewas no difference in mean egg volume betweenclutches of one egg (mean 5 157.91638.41 mm3,N 5 4) and clutches of two eggs (mean 5 150.596 29.19 mm3, N 5 18, t21 5�0.36, P 5 0.74). Weincubated a clutch of two eggs in the lab (in moist

vermiculite at ambient temperature); upon hatch-ing, lizards measured 21.50 and 23.24 mm SVL,and both weighed 0.2 g. No gravid femalesimultaneously contained enlarged vitellogenicfollicles and either oviductal eggs or corporalutea. Hence, if multiple clutches were producedduring the breeding season, they were relativelywell spaced in time or corpora lutea degeneratedrapidly in time.

Reproductive males occurred throughout theyear, but mating was concentrated during thedry season, from May to September (Fig. 4). InNovember, at the onset of the rainy season, threeadult males examined were all reproductive.Reproductive condition was significantly associ-ated with season in males (v2

1 5 10.34, P 50.001), indicating higher frequency of repro-ductive males during the dry season than inthe wet season. Likewise, a larger proportionof reproductive females were observed duringthe dry season (Fig. 4), with a significant associ-ation between reproductive condition and season

TABLE 1. Mean and standard deviation of morpho-metric characters of Gymnodactylus geckoides amarali.Size-adjusted values (see text) are in parentheses. Bodysize is a linear function with equal contributions ofeach measurement (see text). All measurements inmillimeters.

CharacterMales

(N 5 200)Females

(N 5170)

Body size 2.90 6 0.22 2.95 6 0.24Snout–vent

length38.60 6 6.79(0.56 6 0.02)

40.50 6 7.13(0.56 6 0.02)

Body width 10.20 6 2.25(�0.03 6 0.04)

11.03 6 2.55(�0.01 6 0.05)

Body height 6.05 6 1.33(�0.25 6 0.04)

6.50 6 1.55(�0.24 6 0.05)

Head width 7.85 6 1.31(�0.14 6 0.02)

8.04 6 1.35(�0.15 6 0.02)

Head height 4.93 6 0.85(�0.34 6 0.03)

5.09 6 0.88(�0.34 6 0.03)

Head length 9.23 6 1.37(�0.06 6 0.02)

9.50 6 1.33(�0.07 6 0.02)

Forelimblength

12.30 6 2.09(0.06 6 0.03)

12.75 6 2.15(0.06 6 0.03)

Hind-limblength

17.31 6 2.96(0.21 6 0.03)

18.00 6 3.05(0.21 6 0.03)

TABLE 2. Stepwise discriminant analysis of shape variables of Gymnodactylus geckoides amarali. Error-rateindicates posterior probability error-rate estimates based on cross-validation.

Step Variable entered R2 Wilk’s Lambda P Error-rate

1 Adjusted head width 0.044 0.956 ,0.001 0.4032 Adjusted body width 0.013 0.944 ,0.001 0.3683 Adjusted snout–vent length 0.008 0.936 ,0.001 0.370

FIG. 2. Canonical discriminant scores for males andfemales of Gymnodactylus geckoides amarali using size-adjusted values of snout–vent length, head width andbody width. The first canonical variate was a contrastbetween head width (þ) versus body width andsnout–vent length (�), with males averaging 0.24 andfemales averaging �0.28. The second canonical variatewas largely influenced by snout–vent length, with bothsexes averaging 0.


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(v21 5 39.80, P , 0.001). Therefore, although

reproductive individuals can be found through-out the year, reproductive activity is seasonal,being concentrated during the dry season. Incontrast to G. g. amarali, G. g. geckoides in theCaatinga breeds continuously and lays smallerclutches of larger eggs, even though adultfemales are similarly sized (Table 4).

DISCUSSION

Habitat, Microhabitat, and Temperatures.—Gym-nodactylus geckoides amarali is rupicolous, as hasbeen previously reported for G. g. geckoides (Vitt,1995) and G. guttulatus (Vanzolini, 1982). Con-versely, the congeneric G. darwinii lives inforests and ‘‘restingas’’ (Araujo, 1991; Freire,

1998). Based on a lizard assemblage from AltoAraguaia, Brazil, Vitt (1991) stated that the Cer-rado is depauperate in terms of gekkonid species,relative to other Brazilian biomes. However, thisconclusion likely stems from the lack of rockoutcrops in Alto Araguaia. Geckos are oftenmore diverse in rocky habitats (Bauer, 1993) andthese habitats have a patchy distribution in theCerrado (e.g., Giullietti and Pirani, 1988; Harley,1988). Biological reserves in the Cerrado thatexclude rocky areas may fail to preserve a signif-icant portion of the lizard fauna.

The low body temperatures of G. g. amaraliseem to be characteristic of gekkonids (e.g.,Pianka, 1986; Dial and Grismer, 1992; Werneret al., 1996). The significant association between

FIG. 4. Monthly distribution of male (bottom) andfemale (top) Gymnodactylus geckoides amarali accordingto reproductive condition. Sample sizes are indicatedon top of bars.

FIG. 3. Frequency distribution of male (bottom) andfemale (top) Gymnodactylus geckoides amarali accordingto snout–vent length and reproductive condition.

TABLE 4. Reproductive characteristics of Gymnodactylus geckoides from the Cerrado and Caatinga of Brazil.

Species Clutch size Egg length (mm) Egg width (mm) Adult female SVL (mm)

G. g. geckoidesa 1.00 6 0.00 9.33 6 0.83 6.05 6 0.75 42.80 6 1.94(Caatinga) (N 5 47) (N 5 47) (N 5 47) (N 5 104)

G. g. amarali 1.65 6 0.48 8.77 6 0.64 5.72 6 0.47 43.77 6 4.43(Cerrado) (N 5 32) (N 5 22) (N 5 22) (N 5 38)

t 7.66 3.07 2.43 1.30P ,0.001 0.003 0.018 0.201

a Data from Vitt (1986).


body temperature and environmental temper-atures suggests that this species is a thermocon-former. However, since body temperatures werehigher than substrate temperatures, lizardsgained additional heat and were not thermocon-formers in the strict sense. The higher bodytemperature of G. g. geckoides in Caatinga likelyresults from higher environmental temperaturesin that biome (Vitt, 1995). Our observations onactivity are rare, but they suggest that G. g.amarali is predominantly a nocturnal species ormost activity occurs under rocks (dark places)and that crypsis is used to evade predators. Someanecdotal information indicates that these lizardsmay be active during the day (L. J. Vitt, pers.comm.).

Sexual Dimorphism.—Our results revealed sig-nificant sexual dimorphism in body size andshape in G. g. amarali: females are larger, stockier,and have significantly smaller heads than males.In most geckos studied to date, females are largerthan males (e.g., Fitch, 1981; Vitt, 1986; Doughtyand Shine, 1995), but reasons for this sexual sizedimorphism are unclear. Selection should favorlarge size in females if this is associated withincreased clutch or offspring size, whereas largemale size is usually driven by sexual selection(Trivers, 1976; Cooper and Vitt, 1989; Andersonand Vitt, 1990). When clutch size is fixed, pelvicgirdles are often tightly associated with eggdiameter, and if selection favors large offspring,females will tend to be larger (Doughty, 1996; butsee Vitt, 1986). Hence, large female size in geckosshould be favored by increased offspring size,independent of males. In G. g. amarali, however, itis clutch size that varies with female size. Twoexplanations seem plausible in this situation.First, females of G. g. amarali are larger thanmales because of increased reproductive successassociated with the production of larger clutches.Second, large female size (in relation to male size)is the ancestral condition of Gymnodactylus ora larger subset of Gekkonidae including thatgenus and is present in G. g. amarali because ofphylogenetic inertia. Given that G. g. geckoidesfemales from the Caatinga are larger than malesand there is no correlation between reproductiveoutput and female size (Vitt, 1986), the secondhypothesis is more parsimonious.

In G. g. amarali, males have larger heads thanfemales, independent of body size. This kind ofsexual dimorphism in squamate reptiles has beenattributed to two main causes: intraspecific nichedivergence and sexual selection. The first ex-plains intersexual differences as a mechanism toreduce competition for food resources (e.g.,Schoener, 1967; Perry, 1996), whereas the latterinvokes intrasexual competition among males foraccess to females (e.g., Trivers, 1976; Vitt andCooper, 1985). Our results do not support the

intraspecific niche divergence hypothesis, sincewe observed no association between headdimensions and prey dimensions and no trophicdifferences between the sexes. In addition, thishypothesis assumes that food is a limiting re-source, and apparently this is not true for lizardsin the Cerrado (Colli et al., 1997). The sexualselection hypothesis predicts that males withlarge heads will have increased reproductivesuccess by winning intrasexual aggressive en-counters for access to mates. However, detailedinformation on these aspects is currently lackingfor G. g. amarali. Vitt (1986) indicated that G. g.geckoides is territorial, without presenting quan-titative data, but found no sexual dimorphism inhead shape. It is conceivable that, because of theshorter breeding season of G. g. amarali in theCerrado, the potential for males to monopolizemultiple females increases, in contrast to G. g.geckoides in the Caatinga, where continuousreproduction would render the efforts to monop-olize females energetically impractical (Emlemand Oring, 1977). Hence, sexual selection forlarger head size in males would be stronger in theCerrado. Clearly, additional comparative work,including other species of Gymnodactylus, isnecessary to determine the potential role ofsexual selection in producing sexual size di-morphism.

Diet Composition.—The diet of G. g. amarali inthe Cerrado consists largely of termites. Based onpooled stomachs, termites comprised a remark-able 81% of the prey volume and 59% of the preynumber. Simply taking the average values forindividual geckos, termites comprised approxi-mately 39% of the prey number and 68% of theprey volume of G. g. amarali. These figures are fargreater than those described for any otherCerrado lizard or amphisbaenian studied to date(Vitt and Colli, 1994; Colli et al., 1998; Colli andZamboni, 1999), resembling some Australiangeckos which are termite specialists, such asDiplodactylus conspicillatus, Diplodactylus pulcher,and Rhynchoedura ornata (Pianka, 1986). Thedisproportional representation of termites in thediet is clearly reflected in the reduced values ofdietary diversity. For instance, the syntopic teiidAmeiva ameiva has a diet that is approximatelyfive times as diverse as the diet of G. g. amarali(Vitt and Colli, 1994). The diversity of prey usedby G. g. amarali is comparable to that reported fora syntopic and highly fossorial squamate, Am-phisbaena alba (Colli and Zamboni, 1999). Inaddition, the large numbers of termites and antsin the diet seem to be responsible for the lack ofcorrelation between prey size and lizard headmeasurements.

Termites are a diverse and prominent group inthe Cerrado. The termitaria of some species, suchas the mound building termite Cornitermes


cumulans, can reach impressive densities and ithas been suggested it may act as a keystonespecies (Redford, 1984). Termitaria densitiesrange from 336–776/ha (Redford, 1984; Gontijoand Domingos, 1991), and local diversity can beas high as 46 termite species per 0.25 ha(Mathews, 1977; Gontijo and Domingos, 1991).Given diversity and abundance of Cerradotermites, it is not surprising that G. g. amaralimight include large numbers and volumes oftermites in their diet. Less clear, however, is whytermites are a much less important dietary itemamong syntopic, actively foraging species, suchas Ameiva ameiva (Vitt and Colli, 1994) andCnemidophorus ocellifer (Mesquita and Colli,2003). Termites are regarded as a food itemtypical of actively foraging lizards (Huey andPianka, 1981), and like most gekkonids (Cooper,1994), G. geckoides is best classified as a sit-and-wait or ambush forager (Vitt, 1995).

The preferred diurnal microhabitats of G. g.amarali are spaces underneath rocks and rockcrevices in large outcrops. They are moist, evenduring the dry season, and rich in organic matterin the form of dead leaves, branches, and roots,being intensively used by termites (pers. obs.).Because the soil is very shallow, termite galleriesare built next to the surface (R. Constantino,pers. comm.). Geckos in general are highlychemosensory (Schwenk, 1993a,b); therefore G.g. amarali likely has no problem uncovering andeating large numbers of termites. Gymnodactylusgeckoides geckoides from Caatinga uses similarmicrohabitats and consumes a remarkably sim-ilar volume of termites (82.7% for the pooleddata; Vitt, 1995).

Reproduction.—Although reproductive indi-viduals of G. g. amarali were found throughoutthe year, female reproduction was concentratedduring the dry months (May to September). Allof the Cerrado squamates studied to date havea well-defined reproductive cycle, such as Ameivaameiva (Colli, 1991), Amphisbaena alba (Colli andZamboni, 1999), Tropidurus itambere (Van Sluys,1993), and Tropidurus torquatus (Wiederheckeret al., 2002). However, among these species,only A. alba reproduces primarily during thedry season. In strongly seasonal, Neotropicalhabitats, such as the Cerrado, reproduction isoften tightly correlated with rainfall (Fitch, 1970,1982; Licht and Gorman, 1970), presumablybecause of the influence of rainfall upon arthro-pod abundance (Levings and Windsor, 1982;Smythe, 1982) and/or microenvironments foregg deposition (Andrews and Sexton, 1981;Andrews and Wright, 1994; Overall, 1994).Foraging activity of termites increases duringthe dry season (Pinheiro et al., 2002) to supportthe production of alates that swarm at the onsetof the rainy season. Some Cerrado animals that

feed largely on termites, such as the Hoary Fox,Lycalopex vetulus, ingest termites more frequentlyduring the dry season (Dalponte, 1997). Becausethe consumption of termites is higher during thedry season, individuals of G. g. amarali mayconcentrate breeding in the dry season becauseaccess to termites is maximized.

Contrary to its Cerrado relative, G. g. geckoidesin the Caatinga breeds continuously and layssmaller clutches of larger eggs. A similar situa-tion exists for A. ameiva: the Cerrado populationbreeds primarily during the rainy season andlays larger clutches of smaller eggs (Colli, 1991),whereas the Caatinga population breeds year-round and lays smaller clutches of larger eggs(Vitt, 1982). An analogous variation was reportedbetween Mediterranean populations of Lacertalepida (Mateo and Castanet, 1994). This patternmay reflect ecotypic adaptations produced byenvironmental differences between the tworegions: Climate is predictable in the Cerrado,but unpredictable in the Caatinga (Colli, 1991).Our results are consistent with the notion that, inunpredictable environments, selection may favoran optimal clutch size that is smaller than whata female could produce, because of the effectof high mortality in ‘‘bad’’ years (Roff, 1992).Alternatively, selection favors larger clutches inthe Cerrado because the reproductive seasonis shorter than in the Caatinga. However, if aclutch of two eggs is the ancestral condition forGymnodactylus, then single egg clutches of G. g.geckoides are derived, thus favoring the hypoth-esis of reduced clutch size caused by climateunpredictability. In this case, the larger clutchesof G. g. geckoides would simply be a product ofphylogenetic conservatism (Harvey and Pagel,1991). However, a phylogenetic analysis of thegenus is necessary before adaptation can beinferred (Garland and Adolph, 1994). The smallereggs of G. g. amarali in the Cerrado may simplyreflect the trade-off between egg size and clutchsize (e.g., Abell, 1999), given that there existsno significant difference in SVL of reproductivefemales between the two regions. More compar-isons between the two biomes, involving taxa ofdifferent lineages and sizes, will help resolvehow much environmental differences have influ-enced the evolution and shaped the character ofthe Cerrado and Caatinga faunas.

The correlation we observed between clutchsize and female SVL is, to the best of ourknowledge, the first to be reported for any gecko.Most gekkonids studied to date have a fixedclutch size of one or two eggs, and females areunable to increase clutch size by increasing bodysize (Fitch, 1970; Selcer, 1986; Vitt, 1986; Marquetet al., 1990; Vitt and Zani, 1997). Instead, in fixedclutch species, it is egg size that varies withfemale body size (e.g., Andrews and Rand, 1974;


Doughty, 1996). In G. g. amarali there was nocorrelation between egg size and female SVL andno difference in mean egg volume betweenclutches of one egg and clutches of two eggs.Why is there a correlation between clutch sizeand female SVL in G. g amarali? One possibleexplanation is that since clutch size cannotincrease beyond two eggs with increasing bodysize, selection should favor early production ofeggs, as long as egg size is large enough toproduce viable offspring (Vitt, 1986; Doughty,1996). Thus, with approximately 38 mm SVL,females are able to start producing eggs, butmorphological constraints (Congdon and Gib-bons, 1987; Shine, 1992) or selection againstincreased physical burden, such as reducedmobility and increased visibility to predators(Vitt and Congdon, 1978; Shine, 1980; Vitt andPrice, 1982; Sinervo et al., 1989), may prevent theproduction of clutches of two eggs. With in-creasing body size, females start producingclutches of two eggs.

Acknowledgments.—We thank N. J. da SilvaJr. for donating specimens and L. J. Vitt andtwo anonymous reviewers for insightful criti-cisms on the manuscript. This work was partiallysupported by a master’s fellowship from CAPESto DOM and by a research fellowship fromCNPq (302343/88-1) to GRC.

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Accepted: 13 August 2003.


Ecology of the Gecko Gymnodactylus geckoides amarali in a Neotropical Savanna

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