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Journal of Herpetology, Vol. 36, No. 1, pp. 6975, 2002Copyright 2002 Society for the Study of Amphibians and Reptiles

Shelter Microhabitats Determine Body Temperature and Dehydration

Rates of a Terrestrial Amphibian (Bufo marinus)

FRANK SEEBACHER1 AND ROSS A. ALFORD

Department of Zoology and Tropical Ecology, James Cook University of North Queensland, Douglas,Queensland 4811, Australia

ABSTRACT.Selection of diurnal shelter sites varies significantly with season in the cane toad ( Bufo mar-inus), and the aim of this paper is to determine how hydric and thermal conditions of shelter microhabitatschanged with season and whether those changes explained seasonal differences in toad behavior. Body

temperatures of cane toads were measured by telemetry, and dehydration rates and thermal conditions of

shelter microhabitats were measured by using preserved toads as environmental probes. Live toads and

preserved toad models were monitored monthly over a 18-month period. Laboratory experiments showed

that toad models dehydrated at the same rate as live toads. In the field, dehydration rates varied significantlybetween seasons and shelter microhabitats, but dehydration rates were always significantly less in shelters

compared to a nonshelter control. Daily average body temperature of toads was 16-30C, and it changed

seasonally in proportion to model temperature. Diurnal model temperature was significantly lower in shel-

ters compared to the nonshelter control, but there were significant seasonal differences between shelter sites.

It appears that access to suitable diurnal shelter sites is essential for survival of cane toads outside the wet

season and that seasonal changes in environmental conditions influence shelter microhabitat selection.

Terrestriality in amphibians is often associat-ed with thermal and osmotic stress that mayseverely limit physiological performance (Mooreand Gatten, 1989; Preest and Pough, 1989).There are few terrestrial amphibians that can

tolerate elevated plasma osmolarity (Sinsch etal., 1992), although thermal acclimation of phys-iological functions is more widespread (Rome etal., 1992). Many terrestrial amphibians are noc-turnally active and retreat into shelters duringthe day to avoid extremes of temperature anddehydration (Zug and Zug, 1979; Cohen and Al-ford, 1996; Spieler and Linsenmair, 1998; See-

bacher and Alford, 1999). Among the amphibia,the availability of suitable shelters may be ofparticular importance for toads, because, unlikesome frog species (Wygoda, 1988), they are notable to control rates of evaporative water loss,

and their skin acts as an open water surface(Tracy, 1976; Wygoda, 1988). Also, rates of evap-orative water loss are temperature dependent(Tracy, 1976; Buttemer, 1990) so that thermaland hydric conditions are intrinsically linked(Preest and Pough, 1989), and some amphibiansmay even select lower body temperatures (Tb)in drier environments (Malvin and Wood, 1991)despite optimal performance at higher Tb (Tracyet al., 1993).

Toads, like other terrestrial amphibians, arenocturnally active and remain inactive in shel-

1 Corresponding Author. Present address: School of

Biological Sciences, Heydon Lawrence Building A08,University of Sydney, New South Wales 2006, Austra-lia; E-mail: [email protected].

ters, such as rock crevices, hollow tree trunks,and dense vegetation, during the day (Dentonand Beebee, 1993, 1994; Schwarzkopf and Al-ford, 1996; Seebacher and Alford, 1999). We havereported previously (Seebacher and Alford,

1999) that the choice of diurnal shelter sites bycane toads (Bufo marinus) varies significantlywith season on a tropical island in Australia.This observation led to the question of how suit-able different microhabitats are as shelter siteswith respect to seasonally changing environ-mental conditions. Hence, it was the aim of thisstudy to determine seasonal changes in dehy-dration rates and body temperature (Tb) of canetoads and to discover whether seasonal changesin shelter site use are related to rates of dehy-dration and to temperature profiles characteris-tic of different microhabitats at different sea-

sons. Alternatively, it may be that seasonal var-iation in shelter-site use simply reflects randompatterns. For example, Seebacher and Alford(1999) showed that the return of cane toads tothe same shelter site on consecutive nights wasprobably a result of random movement patternsrather than of a homing response.

Discovering whether environmental condi-tions determine microhabitat use by amphibiansin the wild is important for management andconservation. For example, it has been suggestedthat dry environmental conditions and the lackof suitable diurnal retreat sites are major sourc-es of mortality for adult cane toads (Zug and

Zug, 1979). Hence, knowledge of seasonal vari-ation in microhabitat quality may help the de-sign of management practices aimed either at


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70 F. SEEBACHER AND R. A. ALFORD

protecting habitats of endangered terrestrialamphibians (Lemckert and Brassil, 2000) or at

eradicating noxious species such as the canetoad, which was introduced to Australia fromSouth America (Slade and Moritz, 1998).

MATERIALS AND METHODS

The study was conducted on Orpheus Islandwhich, is located 810 km off the tropical eastcoast of Australia (1839.50S, 14630.00E).There is no permanent water on the island, butstanding water collected in a natural depressionafter heavy rain between January and June 1996.Data were collected monthly from September1995 to December 1996, and the total samplesizes were 11 and 12 months for dehydration

rates and model temperatures, respectively(some data were lost as a result of technicalproblems).

Dehydration rates and toad temperatureswere determined in live toads, as well as indead toads preserved in formalin, which wereused as environmental probes (toad models).The choice of environmental model may seemsomewhat unusual; however, cane toads are amajor pest in Australia so that it was possibleto sacrifice toads for this study. Moreover, deadtoads are the best mimic of live animals and are,therefore, as good or better than alternativessuch as agar models (Navas and Araujo, 2000).

Preservation of the toad models was necessaryto prevent fast deterioration of the models in thetropical climate of Orpheus Island and to re-duce the risk of attack by insects and other in-vertebrates. However, the formalin solutionused for preservation was very weak (7% inaqueous solution), so that it is unlikely that theformalin had an affect on internal temperaturesor dehydration rates of the models (see also be-low).

The temperature of toad models (Tm) wasmeasured every 30 min by temperature sensors(LM335 semiconductor) connected to datalog-

gers (HOBO, Onset Computer Corporation, De-partment of Physics, James Cook University),and the sensors were inserted into the body cav-ity of the models via the cloaca. During sam-pling periods, three replicate models were de-ployed into each of five microhabitats for 45days. Each month, fresh models were distrib-uted randomly within each of the following mi-crohabitats, which were used commonly as shel-ters by cane toads (Seebacher and Alford 1999):in crevices between rocks (Rocks), in hollowsunder large, live trees (Under Tree), buried inloose leaf litter (Leaf Litter), and on the groundamong dense vegetation (Vegetation). As a no-

shelter comparison, models were also placed inthe open (Open) on short grass where they wereexposed to sun for most of the day and where

toads were commonly observed at night (See- bacher and Alford, 1999). Before deployment,

models were patted dry on the surface, and theposture of the models resembled the waterconserving posture typical of anuran amphib-ians, whereby the toad is in a crouching po-sition with the ventral body surface contactingthe ground (Jorgensen, 1994).

Water loss was measured as mass loss of themodels, and models were weighed every morn-ing and every evening. To ascertain that pre-served toads dehydrated at the same rate as livetoads, dehydration rates were also measured inan air flow chamber in the laboratory followingthe experimental protocol of Buttemer (1990).Dehydration experiments were conducted at

room temperature (2325C) with an air flowrate of 12 l/min and a relative humidity of 30%.Seven live toads and eight toad models wereused in the experiment.

Body temperature (Tb) of live toads in thefield was measured by temperature sensitive ra-dio transmitters (Holohill, Canada), which weresurgically implanted into the peritoneal bodycavities of toads at the study site (for proce-dures, see Seebacher and Alford, 1999). Tb wasdetermined in each of 12 (wet), 10 (cool), and15 (dry) toads per season by timing pulse inter-vals every 30 min with a stop watch during theday, and recording transmitter signals by a re-

mote sampling system at night (Grigg et al.,1992). Sample sizes varied between individualtoads [mean 3.27 days 0.20 (SE)], becausemany of the transmitters failed prematurely.

Daily average Tb and Tm were calculated asthe integral of the continuous temperature mea-surements from 06001800 h divided by the in-terval of integration (Seebacher et al., 1999). Thismethod was preferred to taking means, becauseit overcomes the problem of dependence of se-quential measurements, and integrals do nothave a variance attached so that they can beused in statistical analyses.

Data (rates of water loss and Tm) weregrouped into seasons and analyzed by analysesof variance. Datasets for each season were ran-domly subsampled to give equal sample sizes,which was necessary because data from somemonths were lost (see above). Hence, six ran-dom replicates were selected per microhabitatper month. Seasons were defined as in Seebach-er and Alford (1999) according to measurementsof air temperature and soil moisture: Wet

January to April, Cool May to August andDry September to December. Hence, theanalysis included two factors, Season andMicrohabitat and the degrees of freedom

were two for season, four for microhabitat and75 for the error term. Sampling units were day-time dehydration rates and Tm measured during


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71TOAD SHELTER SITES

FIG. 1. Seasonal changes in shelter microhabitatuse of cane toads (data redrawn from Seebacher andAlford, 1999). Cane toads most commonly shelteredunder rocks, under large trees, in dense vegetation, orthey buried in leaf litter, but their use of shelter mi-crohabitats varied significantly between seasons.Toads were rarely observed in the open outside shel-ters at any time of year.

FIG. 2. Rates of water loss of live toads and pre-served toad Models determined in a laboratory air flowchamber. Rates of water loss did not differ significantlybetween live toads and toad models. The non-linear re-gression line is shown (y 140.4827x0.5786, R2 0.86).

FIG. 3. Seasonal changes in the mean ( SE) rateof water loss at the different shelter-site microhabitats.Rates of water loss differed significantly between sea-

sons and between microhabitats, but models in theOpen always dehydrated significantly faster thanmodels in shelters.

the day (06001800 h) on the first day after thedeployment of the models, and Tukey tests wereused to compare means. Dehydration ratesmeasured in the field were corrected for meantoad mass (131 g) to compare seasons and mi-crohabitats. The level of confidence was set at0.05, and details of additional statistical tests aregiven in the Results.

RESULTS

Seebacher and Alford (1999) found that shel-ter site use of cane toads on Orpheus Island var-

ied significantly between seasons (data sum-marized in Fig. 1). In particular, toads remainedin the Open during the day, albeit rarely, andused vegetation as shelters during the wet sea-son only. Rocks were used as shelters to thesame extent throughout the year, while Treeswere used primarily in the dry season (Fig. 1).

In the laboratory air flow chamber, toad mod-els dehydrated at rates similar to live toads (Fig.2). Rate of water loss of both live and preservedtoads decreased with body mass, described by thefollowing power equation: y 140.4827x0.5786 (R2

0.86, F2,13 351.0, P 0.01).Dehydration rates of toad models in the field

varied significantly between season (F2,75 6.72,P 0.01) and shelter microhabitats (F4,75 52.38, P 0.0001; Fig. 3). Toads dehydrated sig-

nificantly faster in the Dry season compared tothe Wet and Cool seasons, and there were nosignificant differences between the latter twoseasons. Dehydration rates in the Open were

significantly greater than in any other micro-habitat. The second most dehydrating micro-


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FIG. 4. Seasonal changes in mean ( SE) toadmodel temperature (Tm) at the different shelter-site mi-crohabitats. There were significant differences in Tmbetween seasons and microhabitats, but Tm was great-est in the Open at any season.

habitat was Vegetation, and the least dehydrat-

ing was Leaf Litter. There were no significantdifferences between Rocks and Tree, but Rockswas also not significantly different from LeafLitter, whereas Tree was. The interaction be-tween Season and Microhabitat was not signif-icant (F8,75 1.73, P 0.11) indicating that rel-ative microhabitat dehydration rates did notvary with season.

Tm also varied between seasons and micro-habitats (Fig. 4), and models were warmest inthe Wet season, followed by the Dry season andTm was lowest in the Cool season (F2,75 85.06,P 0.0001). Microhabitats differed significantly

from each other (F4,75

7.40, P

0.0001), andthe interaction between Season and Microhabi-tat was significant (F8,75 2.21, P 0.05), indi-cating that thermal conditions of microhabitatsrelative to each other changed with season. Tmwas hottest in the Open at any season, and Veg-etation was hotter than the other microhabitats(except Open) during the Wet season. Rockswere warmer than Tree in the Dry season, butthese two microhabitats did not differ at anyother season. Leaf Litter was hotter than Rocksand Tree in the wet season, but there were nodifferences at the other seasons.

Tb of live toads varied proportionally to Tm in

all microhabitats (Fig. 5), although Tb was sig-nificantly warmer than corresponding Tm inRocks (t-test: t 4.41, df 144, P 0.0001)

and Under Trees (t 4.76, df 42, P 0.0001)but not in Leaf Litter (t 0.11, df 14, P

0.91) or in Dense Vegetation (t 0.18, df 16,P 0.86; Fig. 5).

DISCUSSION

Unlike many frog species in which rates ofcutaneous evaporation are reduced by the pres-ence of a dried mucus, or waxy layer on theirskin (Wygoda, 1988), toad skin acts as an openwater surface so that toads are not able to con-trol rates of evaporative water loss via their skin(Tracy, 1976; Wygoda, 1988). Hence, the mosteffective way for terrestrial toads to minimizeevaporation is by microhabitat selection (Zugand Zug, 1979; Schwarzkopf and Alford, 1996),

and our data showed that access to suitable di-urnal retreat sites is an essential factor for sur-vival of adult cane toads. Diurnal shelters sig-nificantly reduced dehydration and temperaturestress in cane toads, and in the driest monthsduring our study cane toads would have lostmore than 25% of their body water, their lethallimit is 50% dehydration (Krakauer, 1970), with-in a day without access to shelters. In contrast,Schwarzkopf and Alfords (1996) concluded thatB. marinus could remain in the open for as longas three days without seeking shelter during thedry season on Cape York Peninsula in NorthernAustralia. The availability of permanent water at

Schwarzkopf and Alfords (1996) study site mayexplain this.

Seebacher and Alford (1999) showed thatthere are significant seasonal differences in shel-ter microhabitat use at our study site, and it may

be that seasonal changes in environmental con-ditions account for these changes in behavior.The types of shelter microhabitats used by canetoads on Orpheus Island are similar to thoseused by cane toads elsewhere, as well as by oth-er toad species (Zug and Zug, 1979; Denton andBeebee, 1993; Schwarzkopf and Alford, 1996),

but environmental conditions of shelter micro-

habitats varied seasonally. Overall, Vegetationwas the most dehydrating microhabitat, whichmay explain why toads used it as shelter in thewet season only, although dehydration rates inVegetation were similar to Tree in the dry sea-son, but Tree, which was used frequently in thedry season, was somewhat cooler. Moreover, theuse of Tree as shelter site increased in the dryseason, whereas that of Rocks decreased despitethe fact that dehydration rates did not differ, al-though Tree was significantly cooler. It may bethat toads selected cooler microhabitats at thedriest time of year, and it has previously beenreported that some amphibians may select low-

er Tb in drier environments (Malvin and Wood,1991).In an environment that has no standing water


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FIG. 5. Daily average Tb of live toads changed proportionally to Tm measured at the same time and in thesame microhabitat. Lines of equality are shown.

for most of the year, behavioral control of de-hydration via microhabitat selection seems to beextremely important for survival in cane toads.Part of their success in colonizing new environ-ments may be the versatility of cane toads touse a variety of microhabitats as shelters. Thisis in contrast to the more specialized Europeantoads, Bufo bufo and Bufo calamita, which showincreased physiological stress and mortalitywhen transferred to foreign habitats without ac-cess to their customary shelter microhabitats(Denton and Beebee, 1994).

Temperatures experienced by toads on Or-pheus island were well within their range of tol-

erance in all shelter microhabitats at any time ofyear, and Tm did not exceed lethal temperatures(Krakauer, 1970) even in the Open. Tb of toads

conformed to the Tm of their microhabitat, andalthough Tb was significantly higher than Tm insome shelters, it nonetheless varied in propor-tion to fluctuations in Tm. The differences be-tween Tb and Tm may have been caused by toadsseeking warmer shelters than those randomlyselected for our models, or they could simplyreflect variation in temperature among similarshelter sites. In any case, the observed patternsof Tb and behavioral observations (Seebacherand Alford, 1999) indicate that regulation of Tbin the sense of decoupling Tb from fluctuationsin Tm by shuttling between thermally differentmicrohabitats (Christian and Weavers, 1996;

Seebacher and Grigg, 1997) did not occur.The physiological consequences of water andtemperature stress, such as a decrease in oxygen


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consumption and metabolic scope (Lillywhite etal., 1973; Gatten et al., 1992), could be particu-

larly disadvantageous when high levels of activ-ity and growth are required, for example inpreparation for and during reproduction (Tai-gen and Pough, 1985; Mitchell and Seymour,2000). Tm increased as the wet breeding seasonapproached in summer, confirming that tem-perature stress would not be severe. In contrast,the period leading up to the reproductive sea-son is the driest time of year, potentially limit-ing growth and activity. It is during this timeof year that the availability of shelter sites would

be of paramount importance, not only for sur-vival but also by providing a more benign hab-itat for toads to be metabolically able to prepare

for reproduction.

Acknowledgments.All procedures were con-ducted with the approval of the James CookUniversity Animal Experimentation EthicsCommittee and the Queensland National Parksand Wildlife Service. We thank G. C. Grigg forthe loan of telemetry equipment and S. Fickling,L. Pope, and S. Craven for help with fieldwork.

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JORGENSEN, C. B. 1994. Water economy in a terrestrialtoad (Bufo bufo), with special reference to cutane-ous drinking and urinary bladder function. Com-

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marinus, in south Florida. Comparative Biochem-istry and Physiology. 33:1526.

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LILLYWHITE, H. B., P. LICHT, AND P. CHELGREN. 1973.The role of behavioral thermoregulation in thegrowth energetics of the toad, Bufo boreas. Ecology54:375383.

MALVIN, G. M., AND S. C. WOODS. 1991. Behavioralthermoregulation in the toad, Bufo marinus: effectsof air humidity. Journal of Experimental Zoology258:322326.

MITCHELL, N. J., AND R. S. SEYMOUR. 2000. Effects oftemperature on energy and timing of embryonicand larval development of the terrestrially breed-ing mass frog, Bryobatrachus nimbus. Physiologicaland Biochemical Zoology 73:829840.

MOORE, F. R., AND R. E. GATTEN JR. 1989. Locomotorperformance of hydrated, dehydrated, and osmot-ically stressed anuran amphibians. Herpetologica45:101110.

NAVAS, C. A., AND C. ARAUJO. 2000. The use of agarmodels to study amphibian thermal ecology. Jour-nal of Herpetology 34:330334.

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acclimation on physiological function. In M. E.Feder and W. W. Burggren (eds.), EnvironmentalPhysiology of the Amphibians, pp. 183205. Uni-versity of Chicago Press, Chicago.

SCHWARZKOPF, L., AND R. A. ALFORD. 1996. Desic-cation and shelter-site use in a tropical amphibian:comparing toads with physical models. FunctionalEcology 10:193200.

SEEBACHER, F., AND R. A. ALFORD. 1999. Movementand microhabitat use of a terrestrial amphibian(Bufo marinus) on a tropical island: seasonal vari-ation and environmental correlates. Journal of Her-petology 33:208214.

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Accepted: 14 June 2001.


Evaluation of Coverboards for Sampling Terrestrial Salamanders inSouth Georgia

C. MICHAEL HOUZE JR. AND C. RAY CHANDLER1

Department of Biology, Georgia Southern University, Statesboro, Georgia 30460, USA

ABSTRACT.We conducted a field study to evaluate whether coverboards are as effective for sampling

terrestrial salamanders as searching natural cover objects such as fallen logs and branches. At each of five

sites in Jenkins County, Georgia, we paired a grid of 100 wooden coverboards (30.4 30.4 2 cm) placed

10 m apart with an adjacent grid containing only natural debris. Searches under coverboards detected most

of the same species (Plethodon ocmulgee, Eurycea cirrigera, Eurycea quadridigitata, and Eurycea guttolineata)as found under natural cover (same four species plus Ambystoma opacum). However, salamanders wereencountered at lower average rates under coverboards (0.8 salamanders per grid search) than under natural

cover (2.3 salamanders per grid search), and this pattern was consistent across seasons. The number of

salamanders encountered was more variable within coverboard grids than within grids of natural cover;

mean encounter rates were equally variable among grids for the two techniques. For the most commonly

encountered species (P. ocmulgee), individuals from coverboards were similar in size to those found undernatural cover. There was no tendency for coverboards to accumulate more salamanders through time. Tem-

peratures were more variable under coverboards than under natural cover.

Because of their small size and fossorial hab-its, terrestrial salamanders can be difficult tomonitor. One common technique, use of pitfalltraps in association with drift fences (Gibbonsand Semlitsch, 1982), is especially suitable formonitoring breeding migrations of salamanders(Dodd and Scott, 1994). However, not all sala-manders breed in groups at discrete sites. Main-taining pitfall traps also is time and labor inten-sive, and captured salamanders can be killed bydrowning, overheating, or depredation (Gib-

bons and Semlitsch, 1982). Another popularmonitoring technique, time-constrained search-ing (Campbell and Christman, 1982; Crump andScott, 1994), attempts to overcome these prob-lems by using a trained collector or team to con-

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

duct timed searches of refugia (logs, rocks, orother debris) where terrestrial salamandersmight hide. However, because of variation in ob-server effort or efficiency, it may be difficult tocompare the results of time-constrained search-es among studies, and repeated lifting of coverobjects can destroy microhabitats used by sala-manders. Because of the problems associatedwith these methods, Fellers and Drost (1994)proposed using artificial cover objects (usuallysmall boards called coverboards) to study andmonitor salamander populations.

Coverboards are designed to provide a cool,moist refuge for terrestrial salamanders that areactive at the surface of the ground. Coverboardsoffer a number of potential advantages as a

sampling technique (Fellers and Drost, 1994;Davis, 1997). They can be placed in standardarrays for sampling or monitoring salamanders


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76 C. M. HOUZE JR. AND C. R. CHANDLER

with known effort over a known area, facilitat-ing a variety of experimental designs. There

should be less between-observer variation com-pared to the time-constrained method becausea fixed number of discrete objects must besearched. Coverboards limit the damage done

by repeatedly lifting logs or other natural de-bris.

Coverboards have been used to estimate di-versity and relative abundance of salamanders(DeGraaf and Yamasaki, 1992; Grant et al., 1992;Bonin and Bachand, 1997; Davis, 1997). For ex-ample, Grant et al. (1992) used coverboards(0.66 1.33 m) to compare salamander popu-lations in bottomland hardwood forests, uplandpine stands, old-field habitats, and along the

borders of wetlands in South Carolina. Howev-er, compared to 3390 salamanders caught withdrift fences, only 242 (less than 7%) were ob-served under coverboards (Grant et al., 1992).Of the two species encountered under cover-

boards (compared to five species detected withdrift fences), the slimy salamander (Plethodon oc-mulgee) accounted for over 97% of the individualsalamanders. DeGraaf and Yamasaki (1992)placed coverboards (1.0 0.2 m) along 270-mtransects through 12 northern hardwood standsof different ages in New Hampshire. Signifi-cantly more salamanders occurred in olderstands than in young stands, and the authors

concluded that coverboards were useful forevaluating changes in the abundance and sur-face activity of terrestrial salamanders in man-aged forests.

Despite studies such as these, several impor-tant questions remain concerning the use of cov-erboards as a sampling technique. For example,do coverboards produce data comparable tothose gathered by searching natural cover ob-

jects? Salamanders that occupy coverboardsmay or may not be similar (in terms of species,size, age, etc.) to those that occupy natural coverobjects. It also is unknown how fast coverboards

accumulate salamanders. Can they be used as ashort-term sampling technique, or do they re-quire a substantial waiting period before at-tracting a sample of the surface-active salaman-ders in a given area? Finally, no studies docu-ment whether coverboards provide the samephysical environment (e.g., temperature, mois-ture) as do natural cover objects. If not, cover-

boards may produce a poor or biased sample ofsalamanders. Answering these questions willhelp characterize the advantages and limitationsof coverboards as a monitoring technique.

The objective of our study was to evaluatecoverboards as a method for sampling the spe-

cies composition and relative abundance of ter-restrial salamanders. To meet this objective, weconducted a field study in which we quantified

the salamander community sampled by an ar-ray of coverboards and by an adjacent, paired

grid of natural cover objects. We addressed fivespecific questions. Do coverboards detect thesame number of salamanders as found search-ing a similar number of natural cover objects?Do coverboards detect the same species of sal-amanders as those found by searching naturalcover? Are salamanders found under cover-

boards the same size, on average, as those foundunder natural cover objects? How rapidly dosalamanders occupy coverboards? Do cover-

boards maintain the same thermal environmentas natural debris?


Study Sites.We conducted this study at fivesites in Jenkins County, on the coastal plain ofsoutheastern Georgia (Houze, 1998). Three ofthe five study sites were located in MagnoliaSprings State Park, a 379.2-ha area located ap-proximately 8 km north of Millen, Georgia(3252N, 8156W). The fourth study site, Elam,was located off of U.S. Highway 25 and ElamRoad, 16 km south of Millen, Georgia (3238N,8157W). The final site, Four Points, was locatedoff of Georgia Highway 121 and Elam Road 20km south-southwest of Millen, Georgia(3237N, 8200W).

The three sites at Magnolia Springs (MS1,

MS2, and MS3) were similar in habitat structureand composition. These forests contained ma-ture pines Pinus elliotii and P. taeda (some greaterthan 80 cm in diameter) and a diversity of oakspecies (including Quercus falcata, Q. laevis, Q.laurifolia, Q. margarretta, Q. marilandica, Q. nigra,and Q. virginiana). The sites at Magnolia SpringsState Park were prescribe-burned 2.5 yr prior tothis study. Elam and Four Points were predom-inantly second-growth forest of P. elliotii, P. pal-ustris, P. taeda, Q. nigra, Q. laurifolia, Nyssa syl-vatica, and Liquidambar styraciflua.

Coverboards at MS1 were set out on 18 Oc-

tober 1996. This site was on a slight slope thatincreased in elevation from west to east. Theclosest body of water, a sinkhole fed by an ad-

jacent spring, was 1 km to the west. Cover-boards at MS2 were set out on 24 January 1997.This site was relatively flat and located about 2km east of the sinkhole. MS2 was generallymore xeric than MS1 and MS3, and it containedabundant lichens in some areas. The cover-

boards at MS3 were set out on 15 April 1997.This site slightly increased in elevation fromeast to west and was immediately adjacent tothe sinkhole. The three sites at Magnolia Springswere separated by 12 km. A dirt road separat-

ed sites 1 and 3, and several fire breaks sepa-rated sites 1 and 2. The coverboards at Elamwere set out on 11 April 1997. This site was a


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77EVALUATION OF COVERBOARDS

flat, low-lying area adjacent to a small, seasonalcreek. Coverboards at Four Points were set out

on 21 April 1997. This site sloped east to westinto a seasonal wetland dominated by fernssuch as Osmunda cinnamomea, O. regalis, andWoodwardia areolata.

Study Grids and Coverboards.Each site con-sisted of two 1-ha grids separated by 20 m. Onegrid (determined randomly) contained only un-manipulated natural debris (logs, limbs, etc.);the other grid contained natural debris and 100individually numbered coverboards placed 10m apart in a 10 10 grid. Coverboards wereplaced on top on the leaf litter. We used non-treated sheets of CDX plywood measuring 30.4 30.4 2 cm (1 ft 1 ft 0.75 in) as cover-

boards. Grids were approximately 40120 mfrom any forest edge.

Between April and November of 1997, wechecked the paired grids (coverboards and nat-ural cover) every 12 weeks (every 45 weeksduring the hottest summer months) at each sitefor any salamander species. Although samplingdates varied among sites, paired coverboardand natural grids were always checked sequen-tially on the same day, and the total number ofsalamanders on each grid was recorded. Whenchecking the coverboard grids for salamanders,all boards were lifted and the area beneath wasexamined. All salamanders seen were identified

and measured (snoutvent length, SVL). We didnot mark individual salamanders; our analyseswere based on the paired comparison of thenumber of salamanders encountered per searchon adjacent grids.

It took one person approximately 1 h to checkthe 100 coverboards on a grid. No natural ob-

jects were searched on coverboard grids. On theadjoining grids, we searched natural cover ob-

jects in the same manner as the coverboards bywalking parallel transects separated by about 10m. When any limb or log was encountered itwas lifted, and the area beneath was examined

for salamanders. To make searches of the natu-ral grids comparable to the coverboard grids,we paced the searches to result in approximate-ly 100 natural objects being searched in 1 h. Wesampled each study site 11 times except for MS3(N 10) and Elam (N 9). Thus, we conducteda total of 52 searches of paired grids, duringeach of which 100 coverboards and 100 naturalobjects were lifted.

Abiotic Characteristics.Weekly rainfall andtemperature (minimum and maximum) for thestudy period were compiled through the Geor-gia Forestry Commission for Millen, Georgia.The study sites were located 1035 km west of

the Millen District Office. We used these data toquantify the relationship between weekly rain-fall and temperature and the mean number of

salamanders found under coverboards and nat-ural cover. To compare the thermal microcli-

mates of coverboards and natural cover, weplaced temperature data loggers (Hobo TempData Loggers) under two coverboards and twonatural cover objects (covering the same surfacearea as the coverboards) at MS2 (Mueller andRakestraw 1995). In each case, the coverboardand natural object were no more than 1 m apart.Data were recorded every 4 h for one monthduring August 1997.

Statistical Analysis.For each grid, we aver-aged the number of salamanders encounteredper search for each of four seasons: spring(AprilMay), early summer (JuneJuly), latesummer (AugustSeptember), and fall (Octo-

berNovember). We analyzed these mean en-counter rates using a repeated measuresANOVA with site as a block, cover type as amain effect, and season as the repeated measure(mean encounter rates for the same grid acrossfour seasons). We also calculated the coefficientof variation (CV) in encounter rates, both amongsearches within grids and between mean en-counter rates among grids. Following Zar (1999:105), we determined how many searches of agrid would be needed to estimate mean en-counter rates with 95% confidence limits nogreater than 50% of the mean. A t-test test wasused to test the difference in size of slimy sal-amanders under different cover types, andSpearmans rank correlations were used toquantify the association between salamandernumbers and weekly rainfall and temperature,as well as salamander numbers and time (weekof study). All statistical analyses were conduct-ed using JMP Statistical Discovery Software(vers. 3.1, SAS Institute, Inc., Cary, NC, 1995,unpubl.).

RESULTS

Species Composition.We encountered foursalamander species from two genera under cov-erboards and five species from three genera un-der natural cover (Table 1). Plethodon ocmulgeewas the most common species (over 89% of in-dividuals encountered). The three species of Eu-rycea were encountered infrequently under bothcoverboards and natural cover (Table 1). Ambys-toma opacum was encountered once under nat-ural cover (Table 1).

The number of salamander species variedamong sites. Only one species (P. ocmulgee undercoverboards and natural cover) was observed atMS1, MS2, and Elam. Two species were record-ed at MS3 (P. ocmulgee and E. guttolineata under

coverboards and natural cover). Four specieswere observed at Four Points (P. ocmulgee, E. cir-rigera, and E. quadridigitata under coverboards


10/23


TABLE 1. Distribution of salamanders under cov-erboards and natural cover, Jenkins County, Georgia,

1997.

Species

Number of encounters

Coverboards Natural Total

Plethodon ocmulgeeEurycea cirrigeraEurycea guttolineataEurycea

quadridigitataAmbystoma opacum

32 (20.5%)9 (64.3%)1

10

124 (79.5%)5 (35.7%)1

11

15614

2

21

TOTAL 43 (24.6%) 132 (75.4%) 175

FIG. 1. Frequency distribution of number of sala-manders encountered per grid search for coverboardsand natural cover, Jenkins County, Georgia, 1997.

FIG. 2. Mean ( 1 SE) number of salamanders en-countered per grid search for coverboards and naturalcover at five sites in Jenkins County, Georgia, 1997.

and natural cover, and Ambystoma opacum undernatural cover).

Encounter Rates.Salamanders belonging tothe five species were encountered 175 times,mostly under natural cover (Table 1). We en-countered no more than one salamander underany cover object. A mean of 2.3 ( 0.34 SE; me-dian 0) salamanders was encountered persearch under natural cover, while a mean of 0.8( 0.15 SE; median 2) salamanders per searchwas encountered under coverboards (Fig. 1).There was no difference in mean encounter ratesamong sites (F 1.46, df 4,4, P 0.36), but

significantly more salamanders were encoun-tered under natural cover than under coverboards (F 8.8, df 1,4, P 0.041). We wereunable to test an interaction effect between siteand cover type (each cover type was represent-ed only once at each site), but the tendency ofnatural cover to harbor more salamanders var-ied among sites (Fig. 2). At one site, Four Points,the mean number of encounters was higher un-der coverboards.

The number of salamanders encountered persearch within grids tended to be less variableunder natural cover (mean within-grid CV 86%) than under coverboards (mean within-

grid CV 147%) (paired t-test; t 2.5, df 4,P 0.06). Based on the observed variability be-tween sampling methods, it would take approx-imately 17 searches to estimate (with 95% con-fidence) the observed mean encounter rate oncoverboard grids to within 50%; it would re-quire only 10 searches of natural cover objectsto gain a similar precision. Interestingly, how-ever, the two techniques showed similar vari-ability in mean encounter rates among the fivegrids (69% for coverboards and 74% for naturalcover).

Effect of Season.The tendency of natural cov-

er to harbor more salamanders was consistentamong seasons (season cover type interaction,F 1.9, df 3,12, P 0.19), but there was a

tendency for encounter rates to vary with season(effect of season, F 3.4, df 3, 12, P 0.053).

Size of Salamanders.Because it was possiblethat salamanders of different ages/sizes mightoccupy coverboards, we measured SVL of 109Plethodon ocmulgee from 28 different coverboardsand 81 different natural cover objects. There wasno difference in mean SVL between salaman-ders encountered under coverboards (4.32

0.22 cm SE) and those encountered under nat-ural cover (4.34 0.33 cm SE; t 0.07, df 107; P 0.50).

Colonization of Coverboards.We observed sal-amanders under coverboards the first time wesearched grids at each site (127 weeks after weset out coverboards). The number of salaman-ders encountered under coverboards was notcorrelated with the number of weeks since theywere placed in the field (rs 0.11, P 0.46;Fig. 3).


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FIG. 3. Number of salamanders encountered ver-

sus number of weeks since coverboards were placedin the field, Jenkins County, Georgia, 1997.

FIG. 4. Example of daily temperature fluctuations(815 August 1997) under coverboards and adjacentnatural cover objects at Magnolia Springs State Park, Jenkins County, Georgia, 1997. Lines represent themean of temperatures recorded under two cover-

boards and two natural cover objects.

Physical Environment.Number of salaman-ders encountered under coverboards (rs 0.26,P 0.009) and natural cover (rs 0.38, P 0.006) were both correlated with weekly rainfall.There were no correlations between daily max-imum (rs 0.14, P 0.59) or minimum (rs 0.06, P 0.82) temperature and the numberof salamanders encountered under coverboards.However, there was a negative correlation be-tween daily maximum temperature and the

number of salamanders encountered under nat-ural cover (rs 0.66, P 0.004). There was nocorrelation between daily minimum tempera-ture and the mean number of salamanders en-countered under natural cover (rs 0.31, P 0.15).

Daily temperature fluctuations were greaterunder coverboards than under natural cover inAugust (Fig. 4). Temperature under coverboardsfluctuated over a 10C range (19.529C), where-as temperature fluctuated under adjacent natu-ral cover by approximately 3C (2224.9C) andhad a lag time (i.e., natural objects were slowerto heat and cool). The mean temperature undercoverboards (23.4 2.1C SD) was similar tothe mean temperature under natural cover (23.2 0.9C SD).

DISCUSSION

Our first objective was to determine whethercoverboards sampled the same salamander spe-cies as natural cover objects. Coverboards at-tracted four species of salamanders (from twogenera) compared to the five species (from threegenera) encountered under natural cover. At ourstudy sites, coverboards did a good job of de-tecting most of the species that we found under

nearby natural cover. Thus, coverboards detect-ed most salamander species normally encoun-tered under natural surface objects in southeast

Georgia. Although coverboards require timeand effort to place, if disturbance of cover ob-

jects is undesirable, coverboards probably are agood tool for assessment of salamander speciescomposition. Only Ambystoma opacum wasfound under natural cover but undetected bycoverboards. However, only one individual wasfound under natural cover, and the well-knownfossorial habits of this species make both cov-erboards and natural cover inefficient at sam-pling these salamanders at most times of the

year. For example, Grant et al. (1992) showedthat drift fences captured 548 individual Am-bystoma (including A. talpoideum and A. opacum),compared to only seven Ambystoma found un-der coverboards.

Although coverboards effectively sampled thesame species as natural cover, encounter ratesunder coverboards were significantly lower thanunder natural cover on an adjacent grid. Thispattern did not vary among seasons. Dependingon the site, coverboards usually detected fewersalamanders than natural cover, but they coulddetect as many. This seemed to happen at sites

where natural cover objects were less available.At Four Points and Elam, the number of sala-manders encountered under coverboards andnatural cover was similar, but both of these siteswere covered by relatively young forest withless natural ground debris adequate for wood-land salamanders. Future studies should evalu-ate whether salamander encounter rates undercoverboards vary with the amount, size, and de-cay of adjoining natural cover objects. Cover-

boards may prove most useful in habitats withlittle natural cover such as pine plantations orsecond-growth habitats.

Searches of coverboards not only produced

fewer salamanders, on average, they were morevariable as well. To achieve the same level ofprecision, coverboard grids would need to be


12/23


searched more often than grids of natural ob-jects (17 vs. 10 times to estimatewith 95% con-

fidencemean encounter rate on a grid to with-in 50%). However, variability in average encoun-ter rates among grids was equally variable be-tween techniques. Thus, the two samplingtechniques should be similar in the number ofgrids they require for given sampling require-ments. Although our study is based on datafrom a single year, we believe these results will

be useful in designing appropriate monitoringprograms using coverboards.

Regardless of encounter rates, it was possiblethat coverboards produced a different sample ofthe local salamander community than found un-der natural cover. For example, adult Plethodon

ocmulgee establish territories (Highton, 1956),but juveniles must disperse. Thus, it is possiblethat juvenile salamanders would be especiallyprone to be encountered under coverboards.However, the size distribution of P. ocmulgee didnot differ between coverboards and natural cov-er in our study. There was no evidence that cov-erboards produced a biased sample with re-spect to size, at least for the most common spe-cies at our sites.

The generally poorer performance of cover-boards in terms of encounter rates might be at-tributable to differences in physical characteris-tics between coverboards and natural cover. The

design of our studypaired grids sampled onthe same daycontrolled for variation in theambient environment. Ambient environmentalcharacteristics were important, because thenumber of salamanders encountered during thisstudy increased with rainfall (Grover, 1998).During rains, salamanders are more active atthe surface, which probably increases the chanceof an encounter under coverboards (as well asnatural cover). Although encounter rates wererelated to rainfall, they were not strongly relatedto air temperature. What relationship there was

between temperature and encounter rates was

consistent with the tendency (season effect inANOVA, P 0.053) to encounter fewer sala-manders in the hottest summer months.

The temperature under cover objects probablywas important to salamanders; data loggersshowed that coverboards were poor at main-taining steady temperatures, at least in latesummer. Compared to natural cover, Augusttemperatures under coverboards were more var-iable. Thus, 30.4 30.4 2 cm coverboards donot provide the same thermal microclimates asnatural cover objects. Thicker boards or alter-native materials might provide greater insula-tion and create microclimates more similar to

natural cover. For example, Fellars and Drost(1994) found that 5-cm-thick boards attractedthe most salamanders. These thicker boards

may mimic natural microclimates (i.e., minimizevariation in temperature) better than the 2-cm

boards used in this study. Natural cover suchas sticks and logs also are rounded, which al-lows rain to saturate the soil under the naturalcover objects. Unlike natural cover, the moistureunder coverboards was minimal. Even after sev-eral inches of rain, the soil beneath coverboardswas usually dry. This may be attributable to ourchoice of plywood as a cover object. Naturalwoods may allow moisture to reach the under-side of the board more readily.

Salamanders colonized coverboards quickly.Coverboards that were set out 27 weeks (MS1)and 14 weeks (MS2) prior to the first search hadno more salamanders than coverboards set out

three weeks (MS3 and Elam) and one week(Four Points) before the first search. This impliesthat coverboards are an adequate short-termmonitoring tool, but it remains possible that sal-amander numbers under coverboards may in-crease over the very long term. As coverboards

begin to decay, they may more effectively repro-duce the microclimate of natural cover and at-tract more salamanders. Future studies shouldaddress this possibility.

Acknowledgments.We thank C. Gregory andR. Newton for permitting this research to beconducted at Magnolia Springs State Park and

at Elam and Four Points, respectively. We alsothank the Georgia Forestry Commission in Mil-len and in Statesboro for providing weatherdata. S. Vives, L. Wolfe, and the evolution andecology discussion group at Georgia SouthernUniversity provided helpful comments on ear-lier drafts. S. Droege, J. Fauth, and an anony-mous reviewer provided constructive com-ments. Special thanks to B. Booth, J. Lloyd, andB. Tate for their assistance in the field. This re-search was funded by the Georgia SouthernUniversity Graduate Student Professional De-velopment Fund and met Georgia Southern Uni-versity animal care guidelines.

LITERATURE CITED

BONIN, J., AND Y. BACHAND. 1997. The use of artificialcovers to survey terrestrial salamanders in Quebec.Herpetological Conservation 1:175179.

CAMPBELL, G. S., AND S. P. CHRISTMAN. 1982. Fieldtechniques for herpetofaunal community analysis.In N. J. Scott Jr. (ed.), Herpetological Communities,pp.193200. U.S. Department of the Interior, Fishand Wildlife Research Report No. 13, Washington,DC.

CRUMP, M. L., AND N. J. SCOTT JR. 1994. Visual en-counter surveys. In W. R. Heyer, M. A. Donnelly,R. W. McDiarmid, L. C. Hayek, and M. S. Foster(eds.), Measuring and Monitoring Biological Di-

versity: Standard Methods for Amphibians, pp.8492. Smithsonian Institute Press, Washington,DC.


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DAVIS, T. M. 1997. Nondisruptive monitoring of ter-restrial salamanders with artificial cover objects onsouthern Vancouver Island, British Columbia. Her-petological Conservation 1:161174.

DEGRAAF, R. M., AND M. YAMASAKI. 1992. A non-destructive technique to monitor the relative abun-dance of terrestrial salamanders. Wildlife SocietyBulletin 20:260264.

DODD JR., C. K., AND D. E. SCOTT. 1994. Drift fencesencircling breeding sites. In W. R. Heyer, M. A.Donnelly, R. W. McDiarmid, L. C. Hayek, and M.S. Foster (eds.), Measuring and Monitoring Biolog-ical Diversity: Standard Methods for Amphibians,pp. 125130. Smithsonian Institute Press, Washing-ton, DC.

FELLERS, G. M., AND C. A. DROST. 1994. Samplingwith artificial cover. In W. R. Heyer, M. A. Don-nelly, R. W. McDiarmid, L. C. Hayek, and M. S.

Foster (eds.), Measuring and Monitoring BiologicalDiversity: Standard Methods for Amphibians, pp.146150. Smithsonian Institute Press, Washington,DC.

GIBBONS, J. W., AND R. D. SEMLITSCH. 1982. Terrestrialdrift fences with pitfall traps: an effective tech-

nique for quantitative sampling of animal popu-lations. Brimleyana 7:116.

GRANT, W. G., D. T. ANTON, J. E. LOVICH, A. E. MILLS,P. M. PHILIP, AND J. W. GIBBONS. 1992. The use ofcoverboards in estimating patterns of biodiversity.In Wildlife 2001, pp. 379403. Elsevier, London.

GROVER, M. C. 1998. Influence of cover and moistureon abundance of the terrestrial salamanders Pleth-odon cinereus and Plethodon glutinosus. Journal ofHerpetology 32:489497.

HIGHTON, R. 1956. The life history of the slimy sal-amander, Plethodon glutinosus, in Florida. Copeia 2:7593.

HOUZE JR., C. M. 1998. Evaluation of the use of cov-erboards for sampling salamanders in south Geor-gia. Unpubl. masters thesis, Georgia Southern Uni-versity, Statesboro.

MUELLER, J. M., AND D. L. RAKESTRAW. 1995. Evalu-

ation of a new miniature temperature logger. Her-petological Review 26:2223.

ZAR, J. H. 1999. Biostatistical Analysis. Prentice Hall.Saddle River, NJ.

Accepted: 18 June 2001.


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Reproductive Ecology of Tropidurus torquatus (Squamata:

Tropiduridae) in the Highly Seasonal Cerrado Biome ofCentral Brazil

HELGA C. WIEDERHECKER,1,2 ADRIANA C. S. PINTO,1 AND GUARINO R. COLLI3

1Departamento de Ecologia, Universidade de Braslia, Braslia-Distrito Federal, 70910-900 Brazil3Departamento de Zoologia, Universidade de Braslia, Braslia-Distrito Federal, 70910-900 Brazil

ABSTRACT.We studied the reproductive cycle of Tropidurus torquatus in the Cerrado biome of centralBrazil from October 1997 to September 1998. Females reached sexual maturity at about 65 mm snoutvent

length (SVL), whereas males became sexually mature at 70 mm SVL. Females were reproductively active

between August and February, although males contained spermatozoa in the epididymides year-round.

Frequency of reproductive females was inversely correlated with precipitation and air humidity and posi-

tively correlated with day length. Reproductive activity of males was inversely correlated with air humidity

and positively correlated with day length. Females laid six eggs on average and may have produced up to

three clutches per reproductive season. With the advancement of the reproductive season, clutches tended

to be smaller, whereas egg size remained constant. Fat body mass varied inversely with reproductive activity

in both sexes, but females had significantly larger values than males. After an incubation period of approx-

imately 5 months, young emerged at a SVL around 31 mm. Juveniles began to accumulate energy in fat

bodies after reaching 47 mm SVL. The fat body cycle and the recruitment pattern of T. torquatus suggestthat food resources are not limiting and that the length of the reproductive season is most likely constrained

by the availability of microhabitats suitable for egg development.

A broad spectrum of reproductive strategiesexists among squamates (Fitch, 1970; 1982; Tin-

kle et al., 1970). Variation in such strategieswithin and between lineages has been attribut-ed to phylogenetic inertia, adaptive responses toenvironmental factors, or a combination of both(Ballinger, 1983; Vitt, 1992). The occurrence ofdifferent reproductive tactics among sympatricspecies under the same environmental condi-tions suggests the prevalence of phylogenetic ef-fects (Vitt, 1990, 1991). Several life-history traits,such as clutch size (Dunham et al., 1988), areconservative within families of squamates, ren-dering closely related taxa similar regardless ofenvironmental conditions (Dunham and Miles,1985). However, the influence of environmental

factors becomes evident when distinct repro-ductive tactics occur between populations of thesame species inhabiting different regions (How-land, 1992; Benabib, 1994; Vitt and Colli, 1994).Many field studies have indicated the influenceof temperature, precipitation, and day lengthupon life-history traits of squamates (Ballingerand Congdon, 1981; Adolph and Porter, 1993;Smith, 1996; Ramirez-Bautista et al., 1998). Ex-perimental approaches, moreover, have corrob-orated the influence of environmental factorsupon reproduction (Whittier and Tokarz, 1992),as in the effects of temperature and photoperiod

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

on the development of testes in Anolis carolinen-sis (Licht, 1967).

The temporal pattern of reproductive activi-ties in squamates is often associated with lim-iting environmental factors. In temperate re-gions, reproduction is seasonal and dictated bytemperature and day length (Fitch, 1970; Duvallet al., 1982). In tropical areas, however, squa-mates exhibit a broad variety of reproductivepatterns, ranging from continuous to stronglyseasonal reproduction, making it difficult toidentify the environmental factors that may belimiting (Vitt, 1992; Clerke and Alford, 1993).Two main hypotheses have been advanced toexplain the reproductive seasonality in tropicalareas: (1) the lack of microhabitats with ade-

quate moisture for the development of eggs(Sexton et al., 1971; Andrews, 1988); and (2) thelack of food resources for reproduction or thedevelopment of young or both (Rocha, 1992; VanSluys, 1993b; Vrcibradic and Rocha, 1998) dur-ing the unfavorable season.

Among its congeneric species, Tropidurus tor-quatus (Wied, 1820) has the broadest geographicdistribution, ranging throughout the Cerradoand Atlantic Forest biomes of Brazil (Rodrigues,1987). Several aspects of the biology of T. tor-quatus have been studied, such as diet compo-sition (Bergallo and Rocha, 1994; Rocha and

Bergallo, 1994), thermal ecology (Bergallo andRocha, 1993), and spacing patterns (Giaretta,1996). Nevertheless, little is known about its re-


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83REPRODUCTION OF TROPIDURUS TORQUATUS IN THE CERRADO

productive biology. A variety of reproductivepatterns have been documented in the genus

Tropidurus, from continuous reproduction in T.hispidus in the Caatinga of northeastern Brazil(Vitt, 1993), under highly unpredictable envi-ronmental conditions, to a well-delimited repro-ductive season that lasts for seven months in T.itambere, in the Atlantic Forest domain in south-eastern Brazil (Van Sluys, 1993b), and sixmonths in T. etheridgei in the Argentinian Chaco(Cruz, 1997), both living under predictable, sea-sonal conditions. The paucity of studies includ-ing a large number of localities hampers a betterunderstanding of the association between repro-ductive activity and environmental factors with-in Tropidurus lizards. However, apparently there

is a tendency toward concentration of reproduc-tive activities during the rainy season, underseasonal and predictable climates.

In the central Brazilian Cerrado, precipitationis strongly seasonal and predictable (Nimer,1989); hence it is expected that reproductive ac-tivity in T. torquatus is seasonal, coinciding withthe rainy period. Herein, we describe, for thefirst time, the reproductive biology of T. torqua-tus in the Cerrado of central Brazil, character-izing male and female reproductive cycles andtheir association with environmental variables.Further, we make comparisons with congenericspecies from other regions and less closely re-

lated lizard species from the Cerrado.


We carried out the study in Distrito Federaland surroundings (1547S, 4755W), in thecore region of the Cerrado, the second largest ofthe Brazilian biomes, covering approximately2,000,000 km2 in the central plateaus (Rizzini,1976). The vegetation is formed by a mosaic ofphysiognomies, ranging from open grass fields(campo limpo) to forested formations such ascerradao and gallery forests (Eiten, 1993). Theclimate is the seasonal Aw in Koppen classifi-

cation (Haffer, 1987), with pronounced dry(winter) and wet (summer) seasons. The annualprecipitation varies from 1500 to 1700 mm, be-ing highly predictable and almost entirely re-stricted to the wet season (Nimer, 1989).

We collected lizards with a noose, from Octo-ber 1997 to September 1998. Within 24 h aftercapture, we measured, weighed, humanely killedwith Tiopental, dissected, and fixed lizards in10% formalin. We measured snoutvent length(SVL) with a ruler to the nearest 1 mm, and bodymass with a spring scale (0.5 g). We removed fat

bodies, placed them in 10% formalin, rolled themdry in absorbent paper, and later weighed them

(0.005 g). Whenever fat bodies weighed less than0.005 g, the limit of precision of our scale, weregarded their weight as 0.001 g. To obtain the

caloric content of fat bodies, we considered theaverage composition of 90% of lipids (Brian et

al., 1972) and an equivalence of 37.656 kJ (9 kcal)to 1 g of lipids (Berne and Levy, 1993).To describe the reproductive activity of fe-

males, we recorded the presence and number ofvitellogenic follicles, oviductal eggs, and cor-pora lutea. We measured the diameter of vitel-logenic follicles and the width and length of ovi-ductal eggs with Mitutoyo electronic calipers(0.1 mm). We regarded the SVL of the smallestreproductive female as the minimum SVL forsexual maturity and all females larger than orequal to that size as adults. We considered thesimultaneous occurrence of vitellogenic folliclesand oviductal eggs or corpora lutea as indicative

of more than one clutch per reproductive sea-son. We removed oviductal eggs, placed themin 10% formalin, weighed (0.005 g), lyophilized,and reweighed them. We estimated the caloriccontent of eggs using the formula: caloric con-tent ash-free dry mass of eggs (g) 27.351(J/g) (Vitt and Congdon, 1978). Because we didnot calculate the ash content of eggs, we em-ployed the average ash content of 7% recordedfor iguanian lizards by Vitt (1978).

To describe the reproductive activity of males,we removed the left testis and epididymis andmeasured testis length and width with calipers.

We fixed testes and epididymides in Bouins fix-ative, dehydrated in ascending series of alcohol,and embedded them in paraffin. From each in-dividual, we obtained 10 longitudinal sectionsof 7 m that we stained with hematoxylin-eosin.We obtained 10 measurements for each individ-ual of the seminiferous tubule diameter and ger-minative epithelium height, using a staged mi-crometer. Later, we calculated mean seminifer-ous tubule diameter (STD) and mean germina-tive epithelium height (GEH) for eachindividual. We recorded the most advanced celltype from the spermatogenic lineage in testes,and presence of spermatozoa in testes and epi-didymides. The minimum size at sexual matu-rity was determined as the SVL of the smallestmale with spermatozoa, and all males with SVLequal or greater than the minimum were re-garded as adults. We obtained the testis volumeusing the ellipsoid formula,

2w l

v 6

where v testis volume, w testis width andl testis length.

To meet the requirements of normality (Zar,1984), we transformed some variables (Tabachn-

ick and Fidell, 1996): square root of testis vol-ume (TV), logarithm (base 10) of fat body mass(FBM), and square root of the arcsine of the


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84 H. C. WIEDERHECKER ET AL.

FIG. 1. Monthly values of climatic variables1 and

day length2 in Distrito Federal between October 1997and September 1998. (A) Maximum absolute temper-ature (1), average maximum (2), average (3), averageminimum (4) and minimum absolute (5) in C; (B),total precipitation in mm3 ( ) and relativeair humidity in % ( ); and (C), insolation1

( ) and day length2 ( ) in hours.Sources: 1Instituto Nacional de Meteorologia and 2Ob-servatorio Nacional.

monthly frequency of reproductive females. Tocompare monthly means of some variables in-

dependently of SVL we used an analysis of co-variance. Both STD and TV were significantlycorrelated with SVL (r 0.286, N 115, P 0.002 and r 0.410, N 119, P 0.001, re-spectively). Therefore, we calculated adjustedmeans (Sokal and Rohlf, 1981) to evaluate themonthly variation of these parameters, indepen-dently of SVL.

We obtained additional data on the length ofthe reproductive season and the timing of emer-gence from eggs from a mark-recapture study,using a population from the Santuario de VidaSilvestre do Riacho Fundo, Distrito Federal,from March 1996 to December 1998.

We obtained records of average air tempera-ture (AT), minimum air temperature (MINT),maximum air temperature (MAXT), absoluteminimum air temperature (AMINT), absolutemaximum air temperature (AMAXT), insola-tion, relative air humidity, and precipitationfrom the Instituto Nacional de Meteorologia,and day length from the Observatorio Nacional(Fig. 1). To evaluate the association between cli-matic variables and reproductive activity, weused a stepwise multiple regression analysis foreach sex. Given that the air temperature vari-ables were highly and significantly intercorre-

lated, we performed a principal componentsanalysis on the correlation matrix of the tem-perature variables (the first principal componentexplained 83% of the total variation; eigenvec-tor: AT 0.9687, MINT 0.9333, MAXT 0.8973,AMINT 0.8800, AMAXT 0.8756) and producedscores on the first principal component. Weused these scores, rather than the original vari-ables, in the multiple regression analyses, to re-duce the number of dependent variables andavoid multicollinearity problems (Tabachnickand Fidell, 1996). For the same reasons, we re-placed the monthly means of male reproduction

variables, STD, GEH, and TV, all highly and sig-nificantly correlated with each other, with thescores on the first principal component (whichexplained 68% of the total variation; eigenvec-tor: STD 0.9774, GEH 0.9571, and TV 0.4030). We regarded these scores as indicativeof the reproductive activity of males. For fe-males, we used the square root of the arcsine ofthe percentage of reproductive females collectedeach month.

We conducted statistical analyses with SYS-TAT version 5.2.1 for the Macintosh (SYSTAT,Inc., Evanston, IL, 1992, unpubl.) and used the

significance level of 5% in all statistical tests.Throughout the text, we report means and stan-dard deviation (SD).

RESULTS

We collected 336 lizards (x 28 lizards/month, range 2233): 194 females and 142

males. We encountered T. torquatus more oftenin disturbed areas, even when adjacent to Cer-rado preserves. Frequently, we observed T. tor-quatus in syntopy with two other lizard species:

Ameiva ameiva and T. itambere.Female Reproductive Cycle.SVL of females

varied from 40 mm to 112 mm (82.4 mm 16.3mm), with the smallest reproductive femalemeasuring 65 mm (Fig. 2). We collected no re-productive females from March to July (Fig. 2).Begining in October, we collected females bear-ing vitellogenic follicles and oviductal eggs orcorpora lutea, indicating the production of mul-tiple clutches during the reproductive season.

Further, we first observed oviductal eggs in Sep-tember and corpora lutea in October. Therefore,apparently less than three months are necessary


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FIG. 2. Reproductive condition of female Tropidu-rus torquatus from October 1997 to September 1998.Top: Grouped by snoutvent length (SVL) in milli-

meters. Bottom: Seasonal changes in ovary develop-ment in adult females (SVL 65 mm). C corporalutea; FEC, vitellogenic follicles and eggs, or vitello-genic follicles and corpora lutea; E, oviductal eggs; F,vitellogenic follicles; NR, nonreproductive. Numbersabove bars indicate sample size.

FIG. 3. Clutch size according to snout-vent lengthin mm, in Tropidurus torquatus from the Cerrado.

for the production of the first clutch of eggs. Be-cause the development of follicles of a secondclutch starts prior to the deposition of eggs ofthe first clutch, it is possible that some femalescan produce three clutches per reproductiveseason.

Recruitment started in March, and we ob-served juveniles ranging from 3140 mm SVLin the mark-recapture study until June. The timenecessary for egg incubation, estimated fromthe first record of corpora lutea to the appear-ance of newborns, was approximately fivemonths.

Stepwise multiple regression indicated thatthe monthly frequency of reproductive females(arcsine transformed) was most strongly corre-lated with precipitation (standardized coeffi-cient 0.31), air humidity (standardized co-efficient 0.38), and day length (standardizedcoefficient 1.33). These three variables ex-

plained 94% of the variation in female repro-ductive activity (F3,8 39.71; P 0.0001).We observed no difference between clutch

size, independent of SVL, as estimated from thenumber of oviductal eggs (5.7 0.3, N 27)and vitellogenic follicles (6.4 0.3, N 29; AN-COVA, F1,53 3.55, P 0.065). Hence, we com-

bined data from both sources to calculate clutchsize, and, when females contained both oviduc-tal eggs and vitellogenic follicles, we used onlythe former, to preserve the independence ofdata. Clutch size varied from 310 (6.1 0.2, N 56) and was positively and significantly cor-related with SVL (r 0.75, N 56, P 0.0001;Fig. 3). Mean egg dry mass was 0.372 0.006g (N 27) and mean egg volume was 892.17 146.45 mm3 (N 25), both estimates calculated

from individual female means, rather than thepooled eggs. The correlations between femaleSVL versus mean egg dry mass (r 0.52, N 27, P 0.0054) and volume (r 0.49, N 25,P 0.014) were significant, indicating that larg-er females produced both larger clutches andeggs. The relative clutch mass (clutch dry mass/female total weight) varied from 0.0560.138(0.089 0.004, N 27) and the mean caloriccontent of the average clutch was 57.72 kJ.

Mean clutch size differed significantly amongmonths, using SVL as a covariate (ANCOVA,F5,49 4.30, P 0.002). Mean clutch size in Sep-

tember (7.50

0.50) was significantly higherthan in December and January (5.44 0.31 and4.50 0.50, respectively). However, we ob-served no differences among months in meanegg volume, dry mass, or wet mass, using SVLas a covariate (ANCOVA, egg volume: F3,20 0.21, P 0.89; egg dry mass: F4,21 0.17, P 0.95; egg wet mass: F4,21 0.35, P 0.84). Theseresults indicate that, as the reproductive seasonprogressed, clutches were smaller, whereas eggsize remained constant.

Male Reproductive Cycle.SVL of males variedfrom 31126 mm, with the smallest reproduc-tive male measuring 70 mm (Fig. 4). We collect-

ed adult males bearing spermatozoa during allmonths, with the exception of March, and alladult males, from August to December, were re-


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FIG. 4. Reproductive condition of male Tropidurustorquatus from October 1997 to September 1998. Top:Grouped by snoutvent length (SVL) in millimeters.Bottom: Seasonal changes in adult males (SVL 70)

according to the most advanced cell type in testes.STZ spermatozoa, STD spermatids, STC sper-matocytes, STG spermatogonia. Numbers above bars indicate sample size.

FIG. 5. Monthly means and standard error of tes-ticular parameters in Tropidurus torquatus from Octo-ber 1997 to September 1998. (A) Germinative epithe-lium height (GEH) in m; (B) adjusted means of sem-iniferous tubule diameter (STD) in m; and (C) adjusted means of the square root of testis volume inmm3 (TV). Numbers above bars indicate sample size.

productively active (Fig. 4). No individual pre-senting spermatocytes or spermatogonia as themost advanced cell type in the testis had sper-matozoa in the epididymides. Moreover, few in-dividuals had spermatozoa in the seminiferoustubules but not in the epididymides. This hap-pened in January (1 individual), April (2), June(1), and August (1), outside the peak of the re-

productive season. These results indicate that, incomparison to females, males produce gametesover a longer period and that, seemingly, stor-age of spermatozoa outside the breeding seasonis not common.

GEH and SVL were not significantly correlat-ed (r 0.16, N 115, P 0.09), whereas cor-relations between STD and SVL (r 0.29, N 115, P 0.002) and between TV and SVL (r 0.41, N 119, P 0.001) were highly signifi-cant. We observed significant differences amongmonths in GEH, STD, and TV (GEH: F11,103 13.92, P 0.001; STD: F11,103 22.95, P 0.001;TV: F11,107 38.71, P 0.001). Mean GEH was

highest in September and lowest in April; meanSTD was highest in September and lowest inMarch; and mean TV was highest in December

and lowest in March (Fig. 5). In general, the pa-

rameters indicating male reproductive activitypresented low values from January to June, withminimum values between March and April,during the end of the rainy season, and maxi-mum values in September, at the end of the dryseason.

The stepwise multiple regression indicatedthat climatic variables most strongly associatedwith male reproductive activity were air humid-ity (standardized coefficient 1.09) and daylength (standardized coefficient 0.72). Thesetwo variables explained 79% of the variation inmale reproductive activity (F2,12 16.47, P 0.001).

Fat Body Cycle.Females had significantlylarger FBM than males (F1,273 29.78, P 0.0001; females: 0.818 0.079 g; males: 0.789


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FIG. 6. Top: Monthly means of the regression re-siduals of fat body mass versus snoutvent length ( ) and of the arcsine of the proportion of repro-ductive females ( ). Bottom: Monthly meansof the regression residuals of fat body mass versussnoutvent length ( ) and mean scores ofthe first principal component of testicular parameters( ).

FIG. 7. Relationship between fat body mass (FBM)in grams and snoutvent length in millimeters in fe-male () and male () juveniles of Tropidurus torqua-tus.

0.083 g). In both sexes FBM was significantlycorrelated with SVL (females: r 0.619, P 0.0001; males: r 0.530, P 0.0001). The re-gression residuals of FBM versus SVL variedsignificantly among months, both for males(F11,115 10.366, P 0.001) and females (F11,160 18.063, P 0.001), and were inversely cor-related with the estimators of reproductive ac-

tivity (males: r

0.777, P

0.003; females: r 0.778, P 0.003). In both sexes, the greatestaccumulation of lipids in fat bodies occurred be-tween February and May, increasing from theend of the reproductive season, whereas mini-mum values coincided with peaks of reproduc-tive activity in males and females (Fig. 6). How-ever, females showed a greater range of FBMvalues, reaching minimum levels in Novembersoon after the appearance of corpora lutea. In

juveniles, accumulation of lipids in fat bodiesincreases with SVL, being noticeable only aftera SVL of 47 mm is reached (Fig. 7).

During the nonreproductive season, females

stored an average of 51.333 kJ in fat bodies,varying from 29.878 kJ in February to 72.688 kJin April. During the reproductive season, the

mean value shifted to 10.272 kJ, varying from2.877 kJ in December to 28.858 kJ in August.

DISCUSSION

Reproduction during a well-delimited portionof the year is characteristic of several tropicallizard species, such as Tropidurus itambere (VanSluys, 1993b), Liolaemus lutzae (Rocha, 1992), and

Mabuya maculilabris (Barbault, 1976). Likewise,reproduction in T. torquatus from Distrito Fed-eral is markedly seasonal, with both sexes con-centrating their reproductive activities in the

wet season. Although spermatozoa are presentin epididymides practically throughout the year,when GEH, STD, and TV are considered, sub-stantial variation is evident, and it peaks duringthe female reproductive season. Further, outsidethe female reproductive season, the frequency ofreproductive males is reduced, suggesting thatdespite being more prolonged male reproduc-tive activity is synchronous with that of females.

In lizards with synchronic reproductive cy-cles, as well as in other vertebrates, male sper-matogenesis and aggressive behaviors are oftenassociated with the production of testosterone

(Marshall and Hook, 1960; Marler and Moore,1987; Moore and Lindzey, 1992). Given that T.torquatus is a highly territorial species (Pinto,1999), the production of sperm in months whenno receptive females are available may resultfrom minimum levels of testosterone necessaryfor the maintenance of territories. Conversely,given that the production of sperm is energeti-cally inexpensive, it may be advantageous formales to be ready to start reproduction at anymoment, as suggested for Agama agama (Mar-shall and Hook, 1960). Nevertheless, outside thefemale breeding season, there is a marked re-duction in testicular parameters (GEH, STD,

and TV) and in the amount of sperm in the tes-tes of T. torquatus. This suggests that even if re-ceptive females were available (and we found


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none), the odds against a successful copulationwould be high. Hence, it is more likely that the

costs of producing testosterone during a periodwhen no receptive females are available are bal-anced by the benefits of territory maintenancerather than by the remote likelihood of a suc-cessful copulation. Alternatively, the presenceof spermatozoa outside the breeding seasonmay be simply a remnant of spermatogenesis,not necessarily bearing an adaptive value. Toevaluate these competing alternatives, it would

be enlightening to know whether males that de-fend territories outside the breeding season dohave high levels of testosterone.

Life-history traits of a population are deter-mined by ancestry, proximal responses to vari-

ations in environmental parameters and ecotyp-ic adaptations (Ballinger, 1983; Stearns, 1992). A

broad diversity of reproductive patterns existsamong species of Tropidurus, from continuousreproduction to breeding in a few months eachyear (Van Sluys, 1993b; Vitt, 1993; Cruz, 1997).Considering that congeneric species share manycharacteristics resulting from common ancestry(Harvey and Pagel, 1991), a significant fractionof the diversity in life-history parametersamong Tropidurus is probably associated withproximal environmental effects and ecotypic ad-aptation.

Climate is perhaps the environmental condi-

tion most often associated with variation in liz-ard reproductive parameters (Dunham et al.,1988). Several studies have investigated the in-fluence of climatic variables by considering onevariable at a time, separately from the others(Colli, 1991; Rocha, 1992; Van Sluys, 1993b;Cruz, 1997; Ramirez-Bautista et al., 1998). Thisunivariate approach cannot detect interactionsamong variables, such as the effects of moistureover a range of temperatures (James and Mc-Culloch, 1990; Tabachnick and Fidell, 1996). Us-ing a multivariate approach, we observed thatin spite of the breeding season being concen-

trated in the wet months, relative air humidityand precipitation (only in females) were inverse-ly correlated with reproductive activity. This re-flects the rise in male and female reproductiveactivity prior to the end of the dry season andits decline even before the end of the wet season.Conversely, day length was positively correlatedwith reproductive activity in both sexes, a pat-tern already documented in other tropical lizardspecies, such as Ameiva plei (Censky, 1995) and

Mabuya frenata (Vrcibradic and Rocha, 1998).Although day length varies little and proba-

bly does not constrain breeding activity in trop-ical regions, it may be an important influence

on reproductive cycles of tropical lizards. Ifbreeding during the wet season is adaptive, de-tection of events associated with its arrival

would be advantageous, given that physiologi-cal responses related to gonadal development

are certainly not immediate (Vrcibradic and Ro-cha, 1998). The Cerrado is an extremely pre-dictable environment (Nimer, 1989), and our re-sults suggest that T. torquatus may use daylength as an environmental cue to regulate itsreproductive cycle. The onset of reproduction insuch predictable environments should vary littlein climatically unusual years, being morestrongly adjusted to the anticipation of long-term climatological conditions.

Seasonal breeding is a strategy usually relat-ed to the existence of periods with superior con-ditions for reproduction (Tinkle, 1969). In manytropical lizards, the breeding season coincides

with periods of high precipitation (Wilhoft andReiter, 1965; Vitt and Lacher, 1981; Rocha, 1992),a pattern repeatedly attributed to associatedchanges in arthropod abundance (Janzen andSchoener, 1968; Van Sluys, 1995). However, thecritical level at which a reduction in arthropodabundance will really affect reproduction hasnever been determined for any lizard species(Colli et al., 1997). Considering that fat bodiesare the main energy storage compartment in liz-ards, being susceptible to variations in foodavailability (Brian et al., 1972; Derickson, 1976),we considered FBM indicative of levels of foodabundance. Tropidurus torquatus has a seasonal

pattern of energy accumulation in fat bodies,with both sexes presenting the highest values ofFBM during the dry season. Basically, four pat-terns of fat storage and accumulation are foundin lizards: (1) acyclic accumulation of fat; (2) cy-clic accumulation of fat and its use in reproduc-tion; (3) cyclic accumulation of fat and its use inmaintenance during hibernation; and (4) cyclicaccumulation of fat and its use in both repro-duction and maintenance during hibernation(Derickson, 1976). In T. torquatus, the variationin FBM resembles pattern (2) above, being neg-atively correlated with reproduction.

The reduction in mean clutch size with theadvancement of the breeding season in T. tor-quatus, coinciding with a reduction in FBM, sug-gests that the amount of stored fat affects repro-ductive potential, reflecting the availability offood in months that precede the breeding sea-son. This correlation between food availabilityand reproductive investment (number and sizeof eggs) has been demonstrated in several spe-cies, such as Cophosaurus texanus (Howland,1992), Sceloporus variabilis (Benabib, 1994), andUrosaurus ornatus (Ballinger, 1977). Although af-fecting clutch size, the energy stored in fat bod-ies is not imperative for female reproduction

(Hahn and Tinkle, 1965). In T. torquatus, femalesbreed in October with low levels of stored fat,indicating that the energy acquired by feeding


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is sufficient for reproduction, being directlychanneled to the production of eggs.

The correlation between food availability andreproductive potential, however, does not implythat the former restricts the breeding period. Itis unlikely that individuals accumulate energyduring periods of food shortage (Derickson,1976), and if the reproductive season in T. tor-quatus was bounded by food availability, onewould not expect the accumulation of energy infat bodies during the dry season. Further, theaverage energy content of fat bodies during thedry season is, in some months, higher that thatnecessary to produce an average clutch, sug-gesting that even with that amount of availableenergy, individuals defray reproduction, prob-

ably because of the influence of other limitingfactors. Thus, the energy accumulated in fat

bodies at the beginning of the reproductive sea-son is seemingly necessary for the productionof a large first clutch and the accumulation offat during the dry season indicates that foodavailability for adults is not the factor respon-sible for the cyclic reproduction in T. torquatus.

However, food availability for juveniles caninfluence the reproductive cycle (Derickson,1976; Rocha, 1992; Vrcibradic and Rocha, 1998):a reduced survivorship of juveniles lowers adultfitness. Juveniles of Tropidurus feed on small ar-thropods (Van Sluys, 1993a; Zerbini, 1998) and

might be favored by the higher arthropod abun-dance during the wet season in the Cerrado(Diniz, 1997). However, in T. torquatus, recruit-ment starts at the end of the rainy season andextends into the first half of the dry season.Also, juveniles begin to accumulate fat at a SVLof 47 mm, indicating that even small individualsobtain enough food for maintenance, growth,and storage during periods of reduced arthro-pod abundance. Hence, food availability fornewborn does not appear to constrain the pe-riod of reproduction in T. torquatus.

Finally, egg survival can be a critical factor

during the early recruitment stages in lizards(Overall, 1994). Low levels of moisture nega-tively affect egg survival and reduce embryossizes, therfore restricting the breeding season(Packard and Packard, 1988). The intensity ofthe dry season in the Cerrado, coupled with apredominance of egg deposition and incubationduring the wet season, suggest that conditionsfor egg development could influence the season-al reproductive pattern observed in T.torquatus.Additional research is necessary to test this hy-pothesis.

Although T. torquatus, a sit-and-wait foragerdisplays seasonal reproduction, A. ameiva, an ac-

tive forager, breeds almost year-round in theCerrado (Colli, 1991). The longer breeding sea-son of active foragers in seasonal environments

might be related to their ability to explore awider range of microhabitats and, even during

the dry season, obtain enough food to permitreproduction (Vitt, 1992). Still, as describedabove, seasonal reproduction in T. torquatus isnot apparently constrained by food shortage.Therefore, differences between the two speciesprobably do not result from a limitation in foodsupply. Because conditions for development ofeggs apparently influence timing of reproduc-tion of T. torquatus in the Cerrado, it is worthinvestigating the hypothesis that active foragerssuch as A. ameiva, being able to explore a widerrange of microhabitats, have access to better ovi-position sites or their eggs are more resistant todesiccation, allowing reproduction during the

dry season. Other factors related to foragingmode, such as relative clutch mass (Vitt andCongdon, 1978), can also affect the timin

reprodução wiederheckeretal2002

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