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Breeding biology of the rapids frog Limnomedusa macroglossa (Anura:Cycloramphidae) in southern BrazilIgor Luis Kaefer a; Camila Both b; Sonia Zanini Cechin c

a Programa de Pós-Graduação em Ecologia, Instituto Nacional de Pesquisas da Amazônia, Manaus, Brazil b

Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazilc Departamento de Biologia, Universidade Federal de Santa Maria, Santa Maria, Brazil

Online Publication Date: 01 May 2009

To cite this Article Kaefer, Igor Luis, Both, Camila and Cechin, Sonia Zanini(2009)'Breeding biology of the rapids frog Limnomedusamacroglossa (Anura: Cycloramphidae) in southern Brazil',Journal of Natural History,43:19,1195 — 1206

To link to this Article: DOI: 10.1080/00222930902767474

URL: http://dx.doi.org/10.1080/00222930902767474

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Breeding biology of the rapids frog Limnomedusa macroglossa (Anura:Cycloramphidae) in southern Brazil

Igor Luis Kaefera,*, Camila Bothb and Sonia Zanini Cechinc

aPrograma de Pos-Graduacao em Ecologia, Instituto Nacional de Pesquisas da Amazonia,Manaus, Brazil; bPrograma de Pos-Graduacao em Ecologia, Universidade Federal do RioGrande do Sul, Porto Alegre, Brazil; cDepartamento de Biologia, Universidade Federal de SantaMaria, Santa Maria, Brazil

(Received 5 September 2008; final version received 15 January 2009)

Limnomedusa is a monotypic genus that occurs in association with rocky outcropsand stream beds. Based on observational and mark–recapture fieldwork from2005 to 2008, we report the breeding biology of Limnomedusa macroglossa insouthern Brazil. The reproductive season lasted from late August to earlyFebruary. Tadpoles were recorded from early September to late February. A clearpattern of emergence/recruitment was observed in juveniles. The occurrence ofreproductive activities was clearly related to the longest photoperiods, when thehighest temperatures occur. Males called from rocky or concrete substrates,mostly under rocks. Amplexus was axillary and the operational sex ratio wasnearly even. Spawn occurred in lentic water bodies but tadpoles also completedtheir development in slow-flowing water. Although using similar habitats forreproduction, L. macroglossa reached lower levels of specialization towardterrestriality than did the cycloramphids Cycloramphus and Thoropa. We classifyL. macroglossa as a breeding habitat specialist that would be threatened by riverdamming.

Keywords: behaviour; Neotropics; photoperiod; reproduction; seasonality

Introduction

Limnomedusa is a monotypic genus of the family Cycloramphidae (Frost et al. 2006).

The sole species of the genus, Limnomedusa macroglossa (Dumeril and Bibron 1841)

is distributed along rocky outcrops and stream beds (Gudynas and Gehrau 1981) in

northern Argentina, Uruguay and southern Brazil (Langone 1994; Manzano et al.

2004; Winck et al. 2006).

Data on the phenology of Limnomedusa macroglossa are included in community-

level studies (e.g. Bernarde and Machado 2001; Both et al. 2008). However, with the

exception of notes by Gudynas and Gehrau (1981) and Langone and Prigioni (1985)

for Uruguayan populations, no study has focused on the reproductive biology of this

species. As a result of the lack of long-term, species-centred studies many aspects of

the life history of this species remain poorly understood, such as: (1) the existence of

parental care (Langone and Prigioni 1985; Langone 1994); (2) adult and larva

habitat specificity (Gudynas and Gehrau 1981; Langone and Prigioni 1985); (3)

seasonal and daily activity patterns (Gudynas and Gehrau 1981; Langone 1994;

Segalla and Langone 2004); and (4) adaptation to anthropogenic environmental

*Corresponding author. Email: igorkaefer@hotmail.com

Journal of Natural History

Vol. 43, Nos. 19–20, May 2009, 1195–1206

ISSN 0022-2933 print/ISSN 1464-5262 online

# 2009 Taylor & Francis

DOI: 10.1080/00222930902767474

http://www.informaworld.com

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disturbance (Segalla and Langone 2004; Both et al. 2008). Additionally, there is no

formal description of the combination of traits that characterize L. macroglossa’s

reproductive mode (Salthe and Duellman 1973; Haddad and Prado 2005). The

accumulation of descriptive information is also important because it may provide

data to understand evolutionary relationships among amphibians (Alcalde and

Blotto 2006; Giaretta and Facure 2008).

In relation to its conservation status, L. macroglossa was considered threatened

in Uruguay (Maneyro and Langone 2001) and in the Brazilian state of Parana

(Segalla and Langone 2004). According to these authors, L. macroglossa populations

from the hydroelectric plants of Salto Caxias and Segredo disappeared after river

damming. Both et al. (2008) also supported the hypothesis that dams are harmful to

this species.

Based on observational and mark–recapture fieldwork from 2005 to 2008, herein

we report the reproductive biology of L. macroglossa in a dam and neighbouring

areas in southern Brazil. Our main objectives were (1) to describe the annual activity

pattern and to evaluate the possible influences of climatic conditions and habitat on

occurrence and reproductive activity; (2) to increase knowledge on morphometry

and sexual dimorphism; and (3) to quantify the sex ratio and describe the courtship

behaviour, reproductive mode and recruitment period.

Material and methods

Study site

This study was conducted in the municipality of Itaara (29u329150 S, 53u479300 W;

approximately 420 m elevation), state of Rio Grande do Sul, southern Brazil. The

climate is classified as subtropical wet (Maluf 2000), with evenly distributed rainfall

throughout the year (1500–1750 mm; Pereira et al. 1989) and seasonality determined

by temperature. Field observations occurred at two closely located sites separated by

the Rodolfo Costa e Silva dam wall:

N S1: Permanent river (Ibicuı-Mirim), adjacent to dam wall. River banks are a

rocky basaltic outcrop, steep and surrounded by trees. The area has

constructed zones of concrete ground. Along the banks there is a set of

temporary ponds periodically connected to each other and with the river

(Figure 1A).

N S2: Lake formed by the dammed river. Banks are stony and flat, with swampy

regions near the backwaters. Bank vegetation is grazed by cattle and soybean

is grown during part of the year. Most of the dam has little aquatic vegetation.

Fieldwork and descriptive variables

Data were taken monthly, concurrently at S1 and S2 between August 2005 and July

2006. Given that we did not detect L. macroglossa individuals in S2 during the first

year, additional observations were restricted to S1 from August 2006 to March 2007

and from September 2007 to February 2008. Field observations were made by two

researchers at each site starting at the beginning of the calling period (dusk) and

continuing until a consistent decrease in L. macroglossa activity. We dedicated a

minimum of 3 h of nocturnal search in each study site even when no individuals or

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signs of reproductive activity were found. Throughout the study, we also made

irregular observations at S1 and S2 during the day. Behaviour was followed focally

(Martin and Bateson 1986), with occasional use of flashlights, from 1–2 m distance.

We measured maximum depth, pH and conductivity of ponds and other

waterbodies of the two sites that contained L. macroglossa egg clutches or tadpoles

using plastic rulers and a digital pH meter, respectively. For each calling male

recorded, we registered the position in relation to water bodies (submerged or

outside) and rocks (under or outside). We sexed mature individuals and measured

their snout–vent length (SVL) with digital callipers to the nearest 0.1 mm and their

mass using dynamometers to the nearest 0.1 g. Mature L. macroglossa were

individually marked by toe clipping (Donnelly et al. 1994) and mark–recapture data

were recorded from September 2006 to February 2008. As juveniles were not toe

clipped, we captured, counted and maintained them in plastic bags during each

survey to avoid overestimation of abundance. Voucher specimens were deposited in

the Herpetological Collection at the Universidade Federal de Santa Maria (ZUFSM

4328, 4329 and 4345). All other individuals were released on the same night at the

position where they were captured.

To determine the structure of the population, individuals were grouped as males,

females and juveniles. Males were considered mature when they were caught during

vocalization or by the presence of nuptial pads on the thumbs (Langone 1994).

Individuals larger than the smallest mature individual captured and that lacked male

characteristics were classified as females.

Figure 1. Partial view of the study site S1 (A); amplexed pair (B) and egg clutch (C) of

Limnomedusa macroglossa in Rio Grande do Sul state, southern Brazil.

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Eggs from clutches deposited by pairs were collected and preserved in 5%

formalin between 24 and 36 h after spawning. The eggs were then counted and

measured to the nearest 0.01 mm under stereomicroscope using a digital calliper.

Data on rainfall, temperature and relative air humidity were obtained from

www.cptec.inpe.br, Centro de Previsoes Climaticas do Tempo e Clima. These data

are recorded at the meteorological station of the municipality Sao Martinho da

Serra, 10 km from the study site. Photoperiod data were obtained from http://

euler.on.br/ephemeris/index.php, Observatorio Nacional Brasileiro. Rainfall data

were based on accumulated rainfall of the observation month. Data on temperature

and relative air humidity are related to sampling nights whereas photoperiod data

were based on the observation day. Climatic data were grouped by month.

Statistical analyses

We evaluated sexual dimorphism in SVL using Mann–Whitney’s U-test (Zar 1999).

The operational sex ratios (OSR) followed Emlen and Oring (1977), where

OSR5(number of adult females at the breeding site) / (total number of adults at

the breeding site).

We determined the abundance of L. macroglossa by a monthly encounter rate

that was considered as the number of individuals (juveniles and adults) recorded by

month divided by monthly sampling effort (hours of fieldwork). This rate was

calculated from April 2006 to March 2007 and from September 2007 to February

2008. We related the encounter rate to climatic descriptors through stepwise multiple

regression (Zar 1999), with backward selection, using STATISTICA 6.0 (Statsoft 2001).

For all analyses, significant results were considered when p,0.05 (Zar 1999).

Results

Reproductive phenology and climatic descriptors

Nocturnal fieldwork totalled 153 h (306 man-hours: 234 man-hours at S1 and 72

man-hours at S2). Individuals and signs of reproductive activity (vocalization, eggs

and tadpoles) of L. macroglossa were found exclusively in S1.

Data on reproductive phenology are presented as a summary of the field

observations made from 2005 to 2008. The reproductive season of L. macroglossa, as

indicated by calling males, lasted from late August to early February. Males started

calling immediately after the end of the coldest months of the winter and stopped

about 1–2 months before the beginning of the next autumn. The calling period

always began after dusk. We did not detect any postmetamorphic individuals during

the day. Amplexes were recorded in October 2005 (n51), September 2006 (n51),

October 2006 (n52) and November 2007 (n51). Tadpoles were recorded from early

September to late February. A clear pattern of emergence/recruitment was observed

in juveniles; they were found exclusively and abundantly from early October to late

February (Figure 2). Most of the L. macroglossa individuals were captured between

September and February. With the exception of one individual captured in

May 2006, there were no active individuals during the coldest months (April to

mid-August).

We marked a total of 45 adults, for 35 of which the sex was determined. From

the total, 15 (33%) were recaptured on subsequent nights. Average time between

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marking and last recapture was 88.1 days (SD5111.4; n515). A female was

recaptured 331 days and a male 325 days after being marked.

Abundance of L. macroglossa, measured through the encounter rate, showed a

linear relationship with photoperiod (R250.86, F1,17531.26, p,0.01) (Figure 3).

Monthly rainfall, air humidity and temperature were removed from the model.

However, temperature and photoperiod were strongly correlated (r50.87, p,0.01).

Figure 2. Bars represent average temperature from 1961 to 1990 in the neighbouring

municipality of Santa Maria, a pattern similar to that of Itaara. Temperature data were

obtained from the website of the Instituto Nacional de Meteorologia, Brazil (www.

inmet.gov.br). Timelines below show the occurrence of vocalization, amplexes/egg deposition,

tadpoles and juveniles of Limnomedusa macroglossa from Rio Grande do Sul state, southern

Brazil.

Figure 3. Relation of encounter rate (number of individuals recorded by month/monthly

sampling effort) of Limnomedusa macroglossa with temperature (A) and photoperiod (B) in

Rio Grande do Sul state, southern Brazil (n518 months).

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Morphometry, sexual dimorphism and sex ratio

Male SVL averaged 46.7 mm (SD54.7; range 37.6–55.0 mm; n525); average mass

was 12.4 g (SD53.4; range 7.3–20.5 g; n525). Female SVL averaged 52.9 mm

(SD57.9; range 39.4–62.6 mm; n512); average mass was 17.8 g (SD57.2; range 6.8–

31.8 g; n512). Therefore, in the studied population, females were significantly larger

(U573.0; p50.012) and heavier (U574.0; p50.013) than males. The five heaviest

females were captured in September and October, early in the breeding season.

Juvenile SVL ranged from 17.2 to 36.0 mm (n543). The operational sex ratio

obtained for nights when females were present averaged 0.409 (SD50.203; range

0.250–1.000; n514 nights).

Calling site, mating behaviour and reproductive mode

Males called from rocky or concrete substrates, with the body partially submerged

(n510) or completely out of the water (n52). They called in open areas (n55), but

mostly under rocks (n57). In September 2006 vocalization occurred during nights as

cold as 13.9uC. We observed an adult L. macroglossa being preyed on by the colubrid

snake Thamnodynastes cf. strigatus under a rock used by males for vocalization.

Below we provide a summary of interactions based on our observations of five

amplectant pairs, from which two mating events resulted in egg spawning. Amplexes

were recorded only at night, with temperatures ranging from 17.5uC to 23uC. In

cases when spawning occurred, amplexes lasted 7.6 and 2.5 h. The amplexes were

axillary (Figure 1B) and the pair moved and jumped many times during the

interaction: two amplexed pairs moved through water bodies and crossed dry and

rocky areas. In both cases the male did not release the female, despite sliding, and

remained amplexed in a semi-inguinal position. When standing on the same place,

the amplexing pair repeatedly changed the body orientation even without the

presence of the observer’s flashlight. Moments before oviposition, the female

performed kick-like movements, mechanically removing algae from the surface of

the water film and forming a clean circular area (Figure 1C). The pair then remained

at the centre of the circle and oviposition occurred over the water film. Female kick-

like movements and oviposition lasted ca. 13 min. After oviposition, the pair

immediately moved away in different directions. In the two events resulting in egg

spawning, oviposition sites had water depths of 10 and 11 mm.

Egg clutches were found exclusively in isolated, but periodically connected

ponds, over rocky or concrete ground. Those ponds were temporary and had shallow

(mean515.5 mm deep; SD56.1; n54), lentic water. Egg clutches were almost

circular, averaging 43 cm (SD524.8; n54) at their largest diameter. Eggs were

rounded; black on the animal pole and beige on the vegetative pole. Jelly capsule

diameter (including yolk) averaged 1.27 mm (SD50.07; n510 eggs; n52 egg

clutches). The mean number of eggs was 396 (SD565.8; n52 egg clutches).

We detected tadpoles in pools with depths ranging from 8 mm (water film) to

464 mm. Water pH ranged from 7.55 to 9.48 and conductivity from 20.75 to 0.48 mS.

We did not find heterospecific tadpoles coexisting with those of L. macroglossa.

Tadpoles moved between ponds and from ponds to the river when those were

connected after rains or dam discharge. Some tadpoles completed their development

in those lentic, periodically connected water bodies, while others reached the river,

where they were found in a contact zone with the rocky riverbanks.

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Discussion

The proximity between sites S1 and S2, as well as the presence of rocky slopes and

the reproduction of other anuran species (see Both et al. 2008) in S2 allow us to infer

that the absence of L. macroglossa from the latter could be a case of local extinction

in response to river damming. Some studies classified L. macroglossa as a specialist

in relation to its habitat requirements (Gudynas and Gehrau 1981; Segalla and

Langone 2004; Both et al. 2008), while others did not (Gudynas and Skuk 1980;

Achaval and Olmos 2003). We support the idea that L. macroglossa is a breeding

habitat specialist and suggest that it is threatened by river damming because the

banks of artificial lakes do not provide conditions for reproductive activity in this

species, and so, for the maintenance of individuals in dammed areas (Segalla and

Langone 2004; this study). However, populations of this species can be maintained in

dammed areas when the spatial structure of marginal ponds is preserved in adjacent

streams. We observed this situation at the large Dona Francisca Hydroelectric dam,

also in southern Brazil (Cechin et al. unpublished data). Moreover, independent of

L. macroglossa habitat specificity, the destruction of marginal ponds and the changes

in physical and chemical features of water that result from river damming (Esteves

1998) can harm the reproduction of many frog species (Brandao and Araujo 2008).

The temporal reproductive strategy of this species, although concentrated in a

season of the year, cannot be considered explosive according to Wells (1977), given

that reproductive events (e.g. vocalization, amplexes) occurred over several weeks.

Therefore, we classify the temporal reproductive strategy of L. macroglossa in Rio

Grande do Sul state as prolonged, although highly seasonal. Reproductive activity

concentrated in the warmest months of the year is broadly documented for anurans

in subtropical domains (e.g. Basso 1990; Kaefer et al. 2007; Both et al. 2008;

Canavero et al. 2008). Scattered data on L. macroglossa reproductive phenology for

Uruguay showed high congruence with our study, given that the records of

reproductive activity are also restricted to the beginning of the warm season, e.g.

oviposition in October (Langone and Prigioni 1985); first tadpoles from late August

to late November (Gudynas and Gehrau 1981). Langone (1994) stated that the L.

macroglossa reproductive period lasts from late September to December in Uruguay.

Alternatively, reports from Parana localities appoint a much larger calling period,

where vocalizing males of L. macroglossa were found throughout the year with the

exception of June and July (Bernarde and Machado 2001). This pattern may be

reflecting the less rigorous winter of Parana lower latitudes as compared with Rio

Grande do Sul state.

As the first juveniles appeared about 1 month after the first spawn, we can infer

that this is the minimum duration of the larval stage for L. macroglossa. We interpret

the clear and pronounced recruitment period observed in this study as an effect of

the high seasonality of this species. Not even visual encounters of active L.

macroglossa individuals were made during the peak of the winter, a pattern similar to

that observed even in abundant frog species such as Leptodactylus ocellatus and

Physalaemus cuvieri (Basso 1990; Both et al. 2008) in subtropical domains.

The occurrence of Limnomedusa macroglossa reproductive activities was clearly

related to the longest photoperiods, when the highest temperatures occur. These

climatic factors play significant roles in the timing of reproductive cycles of

amphibians, mainly among species from temperate zones because of their predictable

seasonal changes (Duellman and Trueb 1994; Pough et al. 2001).This pattern may be

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related to a complex interaction between photoperiod and temperature that controls

anuran biological rhythms by activating hormonal stimuli associated with

reproduction, such as gametogenesis and calling activities (Saidapur and Hoque

1995; Hatano et al. 2002). Correspondingly, as rain and humidity levels are evenly

distributed throughout the year, we believe that it does not characterize a seasonally

variable factor that would explain anuran breeding activity in the study area. We

conclude that these climatic variables were not correlated with anuran activity

because the water from the river and the dam discharge may act as a constant source

of humidity and breeding sites to L. macroglossa.

The toe-clipping technique used in this study (Donnelly et al. 1994) showed

satisfactory results, as indicated by: (1) ease of recognition of specimens (mark was

clear and there was no subsequent growth of the removed phalange); (2) high

number of recaptures, as the time elapsed between recaptures throughout the study

and; (3) immediate recovery of the marked individuals, as suggested by toe-clipped

males that were found vocalizing and in amplexus on the same night of the marking

(Kaefer et al. unpublished data).

Mature females of L. macroglossa attain larger SVL than males (Langone 1994;

this study). The same pattern was recorded by Heyer et al. (1990) for other species of

the Alsodinae subfamily such as Proceratophrys and Thoropa in southeastern Brazil.

Sexual differences in mass were probably influenced by the reproductive season,

given that the heaviest individuals recorded were gravid females found in September

and October, the peak of the ovipositing period.

Male calling sites recorded in this study were similar to those reported for L.

macroglossa in Uruguay (Gudynas and Gehrau 1981; Langone 1994). However,

previous studies indicated that the substrate from which males called when above

rocks was muddy and rarely rocky soil. All calling males we recorded were seen on

rocky substrates, but we recognize that habitat availability may differ among the

studied areas and can influence microhabitat use by anurans (Duellman and Trueb

1994).

The behavioural strategy of male L. macroglossa can be classified as vocalizing

males (sensu Howard 1978), given that it is characterized by the emission of

advertisement calls to attract receptive females. This is the most common strategy

among anurans and is characterized by the absence of an active search for females,

polyandric strategies or even features proposed for prolonged breeders, such as

satellite behaviour and displacing male strategies (Pombal and Haddad 2007). We

did not observe male–male combat or any physical damage to the frogs that would

be indicative of combat. The mentioned alternative male strategies are known to

occur in cases where females occur at low densities at breeding aggregations (Toledo

and Haddad 2005; Pombal and Haddad 2007), which is not the case for this L.

macroglossa population, given that the recorded high operational sex ratio suggests a

nearly equal proportion of males and females at the study site.

The low number of cases of mating behaviour recorded in this study, as well as

the lack of descriptions of L. macroglossa mating behaviour in the literature, limits

the interpretation of our results. Oviposition on the water surface over rocks is

similar in the cycloramphid genera Thoropa (Giaretta and Facure 2004) and

Odontophrynus, such as O. americanus, O. cultripes and O. occidentalis (Cei 1980; see

references in Langone and Prigioni 1985). Data on mean number of eggs per spawn

and egg colouration are very similar to those reported for this species in Uruguay

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(Langone and Prigioni 1985; Langone 1994). The presence of a male L. macroglossa

near an egg clutch reported by Langone and Prigioni (1985) was subsequently cited

in other publications as a probable case of parental care needing further

investigation (e.g. Langone 1994; Winck et al. 2006). In addition, other

cycloramphid genera show parental care (Giaretta and Facure 2003, 2004).

However, we did not find any signs of parental care in L. macroglossa during field

surveys. Following oviposition, both parents were seen moving away from the spawn

and subsequently tadpoles were not attended. As the places where this species breeds

are restricted to rocky, and sometimes patchy, environments, we suggest that the

occurrence of vocalizing males near spawn and tadpoles is fortuitous and not

indicative of parental care.

Information on L. macroglossa reproductive mode was also given by Gudynas

and Gehrau (1981), who stated that L. macroglossa tadpoles are found in

unoccupied, small lentic and stationary environments near stream beds, over rocky

ground and where water flows can link these puddles with others of bigger sizes at

lower zones, transporting L. macroglossa larvae. They also highlighted that during

rains, the previously isolated puddles may form a common flow. Additionally,

Gehrau and de Sa (1980) reinforced the idea that puddle–puddle transport occurs in

this species while Langone and Prigioni (1985) did not dismiss the possibility

(confirmed by this study) that tadpoles could be transported to flowing water during

rains. These descriptions match our observations, showing a clearly lentic but water-

flow-dependent reproductive mode for L. macroglossa. Cei (1980) and Both et al.

(2008) suggested that L. macroglossa could achieve oviposition in lotic systems, but

other observations (Gehrau and de Sa 1980; Gudynas and Gehrau 1981; Langone

and Prigioni 1985; this study) found that oviposition is restricted to lentic or

slow-water systems.

Reproduction that relies on lentic water bodies for spawning or for tadpole

development is one of the most primitive modes usually found in anurans (Duellman

and Trueb 1994). Limnomedusa macroglossa exhibited reproductive mode 1 (sensu

Haddad and Prado 2005), which is characterized by eggs and exotrophic tadpoles in

lentic water. However, some anurans may show both a primary and an alternative

reproductive mode (Haddad and Prado 2005). Limnomedusa macroglossa spawn

occurred in lentic water bodies but tadpoles complete their development both in

lentic and slow-flowing water. This alternative reproductive mode is similar to that

reported for the cycloramphid genera Thoropa and Cycloramphus, which are known

to live on rocky environments and have semiterrestrial tadpoles, which inhabit

shallow and slow-flowing water on surfaces of rocks (Giaretta and Facure 2004;

Haddad and Prado 2005). However, we cannot classify L. macroglossa as having

alternative reproductive mode 19 sensu Haddad and Prado (2005): Limnomedusa

seems to be more aquatic-dependent than Thoropa and Cycloramphus, given that

these latter genera lay eggs directly on the surface of humid rocks and tadpoles have

reduced fins, being classified as semiterrestrial (Giaretta and Facure 2004; Haddad

and Prado 2005). Therefore, these data suggest that, although using similar habitats

for reproduction, the genus Limnomedusa has reached lower levels of specialization

toward terrestriality than have the cycloramphid genera Cycloramphus and Thoropa.

Given that the alternative reproductive mode here described was not listed by

Haddad and Prado (2005), its classification awaits detailed data on the reproductive

biology from other L. macroglossa populations through its geographic range.

Journal of Natural History 1203

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Acknowledgements

We thank Daiani Kochhann, Tiago Dalcin, Gilberto Depra and our colleagues at the

UFSM Herpetology Laboratory for their help in field activities. We also thank Taran

Grant, Mirco Sole and two anonymous reviewers for valuable suggestions on the

manuscript. This study was permitted by RAN/IBAMA (Permit No. 02010.00061/2006-57).

Centro Internacional de Projetos Ambientais (CIPAM) and Petrobras Ambiental provided

logistical support.

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