Anurans of the Serra do Caraça , southeastern Brazil : species composition and phenological patterns of calling activity

Annual patterns of calling and breeding activity of 38 anuran species were studied at Serra do Caraça, an 11,233 ha reserve located in a contact zone between Cerrado and Atlantic forest at the southern Espinhaço range, southeastern Brazil. Five patterns were evident: (1) species that call year-round or nearly year-round with larger aggregations generally observed in the rainy months, (2) species with opportunistic calling activity associated with rainfall during the wettest months of the year, (3) winter species, (4) explosive breeders with intense calling activity triggered by heavy rains during the rainy season or only in the beginning of the rainy season, and (5) summer species with variable breeding seasons. Both the monthly number of species with calling males and the monthly number of species that showed the maximum class of calling males were positively correlated with both mean monthly temperature and monthly precipitation.

This paper describes annual patterns of calling activity of 38 anuran species from Serra do Caraça, southeastern Brazil, by monitoring calling activity of males and evidences of actual reproduction at selected breeding sites.Additionally, we provide for the first time a list of anuran species for this locality.These informations may be used as a point of departure for future evaluations of the conservation status of the populations involved, which is fundamental considering anuran declines and local extinctions suggested in the last two decades for southeastern Brazil (HEYER et al., 1988(HEYER et al., , 1990;;WEYGOLDT, 1989;HADDAD & SAZIMA, 1992;BERTOLUCI & HEYER, 1995;ETEROVICK et al. 2005).

MATERIAL AND METHODS
Field work was carried out at Reserva Particular do Patrimônio Natural Santuário do Caraça, an 11,233 ha reserve of Atlantic rainforest located in the Serra do Caraça, in the Espinhaço range, state of Minas Gerais, southeastern Brazil (20º05'S, 43º28'W).The Serra do Caraça has altitudes between 900 and 2,000 m.The climate is Cwb of Köppen.According to data provided directly by Agência Nacional de Águas, Belo Horizonte, the average annual rainfall from 1984 to 2001 was 2,031.29 ± 480.92 mm.Between October 2001 and September 2002 the annual accumulated rainfall was 2,038.40mm and rainfall was irregularly distributed through the year; the rainy season lasted from October to March (Fig. 1).Mean monthly temperatures for the study period are also shown in Fig. 1.
The vegetation that covers the lower parts of the Serra do Caraça are the Semideciduous Montane Atlantic forest and Cerrado; at higher altitudes montane meadow ("campo rupestre") and misty forest occur.
In order to determine calling and breeding seasons of anuran species, four aquatic habitats with different physiognomies were chosen for year-round monitoring.These habitats, located in open area, forest and forest edge, are as follows: Site R1 is a little stream located in montane meadow (1,600 -1,700 m elevation).It is mainly rocky, with rocky puddles, some containing sand and dead leaves and sticks.The studied portion is 500 m long and, in the rainy season, mean width and mean depth were 4.51 ± 2.29 m (0.40 -8.50 m) and 0.28 ± 0.21 m (0.05 -0.90 m), respectively (n = 26 measurements).Site R2 is a moderately sized stream located in the primary forest (1,250 m elevation).The studied portion is 280 m long and, in the rainy season, mean width and mean depth were 5.78 ± 3.18 m (0.40 -11.50 m) and 0.59 ± 0.44 m (0.20 -1.30 m), respectively (n = 13 measurements).Upstream in the studied portion, there is mainly sandy bottom backwaters and downstream there are rapids and two little waterfalls.Site L1 is a semipermanent lake (1,200 m elevation, 500 m 2 , 1 m deep) located at the edge of a disturbed forest; it was formed by interruption of a small stream.Site L2 is a permanent swamp (1,200 m elevation, 400 m 2 , 0.20 m deep) located in open habitat.
Field work was carried out from October 2001 until September 2002.To determine patterns of calling activity of anurans, the number of calling males for each species was estimated twice a month between 18:00 h and 24:00 h at each selected site.Sites were also visited during the day to verify the occurrence of any diurnal vocalization.The following classes for the number of synchronously calling males per species at each site were established: (1) 1-2, (2) 3-5, (3) 6-10, (4) 11-20, (5) 21-50, (6) more than 50 (AICHINGER, 1987;BERTOLUCI, 1998;BERTOLUCI & RODRIGUES, 2002a).The calling activity of species that do not vocalize in the selected sites or in the selected portions of the sites was determined in a qualitative way.The presence of egg clutches, amplectant pairs, and gravid females were considered evidences of actual reproduction.Correlation between variables were tested using Spearman's Correlations Coefficient (ZAR, 1996).Voucher specimens were deposited in the Herpetological Collection of the Universidade Federal de Minas Gerais, Brazil (UFMG).
The year-round activity of Hypsiboas polytaenius at Serra do Caraça agrees with the continuous pattern described for this species at Boracéia, state of São Paulo, another Atlantic rainforest locality of southeastern Brazil, 600 km southeast of Serra do Caraça, at about 900 m above sea level (BERTOLUCI & RODRIGUES, 2002a).The breeding period of Crossodactylus trachystomus at Serra do Caraça agrees with data found for Crossodactylus sp. from another Atlantic rainforest locality of southeastern Brazil, Botucatu, state of São Paulo (ROSSA-FERES & JIM, 1994).The breeding period of Scinax duartei (B. Lutz, 1951) at Serra do Caraça was much longer than that found at Serra do Cipó, state of Minas Gerais, another montane meadow locality of Espinhaço Range, southeastern Brazil (ETEROVICK & SAZIMA, 2000).This could be explained by the less humid climate of Serra do Cipó (around 1,500 mm; GALVÃO & NIMER, 1965).
About 21% of the species showed opportunistic calling activity (including diurnal) associated with rainfall in the summer.This group includes the endotrophic species, either nidicolous [Leptodactylus bokermanni (Heyer, 1973)] or with direct development (Eleutherodactylus spp.; THIBAUDEAU & ALTIG, 1999).This pattern was also observed for other species of Leptodactylus (L.marmoratus) and Eleutherodactylus (E.guentheri, E. parvus and E. randorum) at Boracéia (BERTOLUCI & RODRIGUES, 2002a), suggesting a dependence of these species on high levels of humidity to spawn.Other species that called exclusively or almost exclusively in the rainy days were Hyalinobatrachium sp.(aff.eurygnatum), H. uranoscopum (Müller, 1924), Odontophrynus cultripes Reinhardt & Lütken, 1862 and Phyllomedusa burmeisteri Boulenger, 1882.The reproductive behaviour of O. cultripes was similar to that observed in O. americanus at Intervales, state of São Paulo, another Atlantic rainforest locality of southeastern Brazil (BERTOLUCI, 1998).At Serra do Caraça O. cultripes did not show the explosive behaviour recorded by O. americanus at Intervales, but its calling activity was closely associated with rain falls.The same behaviour was observed for O. americanus at Serra do Cipó, where this species reproduced immediately after the filling of temporary puddles (ETEROVICK & SAZIMA, 2000).Data obtained for this species in Botucatu disagree to this pattern; there its calling activity was associated to the driest, coldest month of the year (ROSSA-FERES & JIM, 1994).The reproductive period of Phyllomedusa burmeisteri corroborates the pattern found in two other Atlantic forest reserves of southeastern Brazil, the Parque Estadual da Serra do Brigadeiro and the Reserva Particular do Patrimônio Natural Feliciano Miguel Abdala, both also
The breeding activity of anurans at Serra do Caraça was closely related to the rainy season.More than 80% of the species were reproductively active exclusively or located in the state of Minas Gerais (BERTOLUCI et al., 2005).The same pattern was described for P. distincta, a very closely related species, in Intervales (BERTOLUCI, 1998).
The winter activity of species of Scinax of the catharinae group [S. luizotavioi (Caramaschi & Kiteumacher, 1989), S. machadoi (Bokermann & Sazima, 1973), and Scinax sp.2] may represent a strategy that reduces interspecific competition in both adult and larval communities by means of temporal partitioning of the habitat.Together with Hypsiboas polytaenius, the winter activity of these species reveals a high tolerance to low temperatures typical of montane anurans (GUIX, 1996).The calling activity of Scinax machadoi restricted to the dryer months of the year must be interpreted with caution because the advertisement call of this species is very weak, at low volume and irregular, and is easily mismatched with the sounds of the rapids in the rainy season.A longer breeding period for this species is suggested by the presence of gravid females in the breeding site in December, March and August.At Serra do Cipó, S. machadoi reproduce almost year-round (BOKERMANN & SAZIMA, 1973).
The positive correlations between the number of species with calling males and the mean monthly temperature and between the number of species that attained their maximum class of calling males and the mean monthly temperature corroborate the idea that low temperatures inhibit anuran breeding activity (BERTOLUCI, 1998;BERTOLUCI & RODRIGUES, 2002a).The positive correlations of these variables with mean monthly rainfall corroborate the idea that anuran breeding activity at seasonal tropical areas is closely related to the rainy season (TOFT & DUELLMAN, 1979;AICHINGER, 1987;HERO, 1990;GASCON, 1991;DUELLMAN, 1995;BERTOLUCI, 1998;ETEROVICK & SAZIMA, 2000;BERTOLUCI & RODRIGUES, 2002a).

Fig. 1 .
Fig. 1.Mean monthly temperature (line) and monthly rainfall at the study site between October 2001 and September 2002.

Fig. 2 .
Fig.2.Number of species with calling males (black), number of species that attained their maximum class of calling males (white), and number of species that had evidence of breeding (gray) between October 2001 and September 2002 at four aquatic sites of Serra do Caraça, Southeastern Brazil.

Table II .
Calling and breeding patterns of 38 anuran species at Serra do Caraça, southeastern Brazil, from October 2001 to September 2002.Classes of abundance of calling ) more than 50.C indicates not quantified calling activity that occurred outside of the studied sites.Evidence of breeding: a amplectant pair, f gravid female, s spawning.BP, breeding patterns: Y, species that call year-round or nearly year-round with larger aggregations generally observed in the rainy months; O, species with opportunistic calling activity associated with rainfall during the wettest months of the year; W, winter species; E, explosive breeders with intense calling activity triggered by heavy rains during the rainy season or only in the beginning of the rainy season; S, summer species with variable breeding seasons.