Herpetology Notes, volume 13: 245-248 (2020) (published online on 13 March 2020)
It’s raining today! The importance of fine-scale rainfall data to reveal abundance patterns of Brazilian Atlantic Forest frogs
Juliane Pereira-Ribeiro1,*, Átilla Colombo Ferreguetti1, Helena Godoy Bergallo1, and Carlos Frederico Duarte Rocha1
Anurans are particularly susceptible to desiccation, so respond to the rainfall (Boquimpani-Freitas et al., much so that their daily activity and reproduction periods 2007). Therefore, one could expect that measuring often rely on water availability or high relative humidity rainfall during anuran sampling should provide a clearer levels (Duellman and Trueb, 1994).Therefore, most understanding of the relationship between rainfall and anuran activity is somehow affected by environmental anuran activity. factors that can determine desiccation rates, such as In this study, we analysed anuran density in the temperature, rainfall or relative air humidity (Aichinger, community of Vale Natural Reserve, municipality of 1987; Duellman and Trueb, 1994; Bertoluci and Linhares, northern of Espirito Santo State, over the Rodrigues, 2002). For instance, the majority of studies course of a year. We aimed to evaluate how different have found that rainfall affects annual patterns of measures of rainfall collected across different timescales anuran activity, due to a positive relationship between would affect patterns of anuran abundance over time. the cumulative rainfall of a particular month (monthly We hypothesized that the amount of rainfall during accumulated rainfall) and anuran abundance or activity sampling would better explain overall anuran abundance (e.g. Bertoluci and Rodrigues, 2002; Prado et al., variation. 2005). However, less attention has been devoted to the Materials and Methods amount of rain falling just during the sampling period The study was conducted in the Vale Natural Reserve (e.g. Saenz et al., 2006; Steen et al., 2013, Gomez- (VNR) (datum WGS84, 40.0508°W, 19.1125°S, mean Mesa et al., 2017). The overall accumulated monthly elevation = 46 m), located in municipality of Linhares, precipitation does not necessarily reflect the rainfall northern Espírito Santo state, Brazil. The VNR has occurring during the sampling period within each particular month. Although an effort is usually made approximately 23,500 ha and its environmental by researchers to collect environmental data, they are seasonality is determined mostly by rainfall (Garay and sometimes not able to measure relative air humidity or Rizzini, 2004). The climate in the region is tropical hot, rainfall during the exact sampling period. As a result, humid, with annual rainfall of 1,202 mm, and mean o available data from existing stations may be a scale annual temperature of 23.3 C. Vegetation cover of the that does not adequately measure the relative humidity reserve includes the Coastal Plain Forest (“Floresta or rainfall in the exact period or day in which anuran de Tabuleiro”), which can be divided in four distinct sampling was performed. vegetation types: high forest, the sandy soil forest, In relatively drier environments or periods, anuran permanently or seasonally flooded forest and the natural abundance tends to be lower but they can quickly grassland (see Peixoto and Gentry, 1990). Field sampling was carried out from June 2015 to January 2017, encompassing both the dry (Apr to Sep) and rainy (Oct to Mar) seasons. We conducted samplings during the day (11:00 h to 17:30 h) and at night (18:00 h to 23:00 h) in order to increase the probability of 1 Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Rua São Francisco Xavier, 524, Maracanã, 20550- detecting species with different periods of activity. 019, Rio de Janeiro, Rio de Janeiro State, Brazil. We used 21 plots of 250 meters in length distributed * Corresponding author. E-mail: [email protected] proportionally in the vegetation types of coastal plain, 246 Juliane Pereira-Ribeiro et al. sandy soil forests and natural grassland, following the a rainfall event. A study regarding calling activity of RAPELD protocol by Magnusson et al. (2005). frogs and environmental abiotic variables in the USA We sampled anuran activity monthly, with campaigns showed that the short-term rainfall (1-2 days) affected of 10 days per month, by performing transects along the calling activity of some anuran species (Saenz et al., plots, using the active search method, with visual and 2006). Recently, when analysing environmental drivers auditory samplings used to locate the individuals (Crump of anuran calling phenology in southeastern Bolivia, and Scott, 1994) simultaneously by two observers. We Schalk and Saenz (2016) showed that most species carefully inspected each plot during each transect and responded to the amount of rainfall on the night of the recorded and identified all individuals located visually calling event. in an approximate distance of 5 meters on each side from the centreline of the plot. To estimate anuran density in the area (individuals/ha), we calculated the sampling areas of the plots through the R package Devtools (Wickham and Chang 2016) by using the “parcelareadev” function “ which uses the azimuth (compass) and the size of the sample group to process and calculate sampling areas of nonlinear plots. Then, we calculated the total area of search in the plots (considering the sum of the areas of all plots sampled/ month) and divided the number of registered individuals per month by the total area. We obtained the data from monthly accumulated rainfall (sum of the overall precipitation value of the month) and sample-period rainfall (sum of the amount of rain falling only in days of the field sampling period) each month from the Weather Station of Vale Natural Reserve (all in mm), which is located in the western region of the Reserve. The mean distance between plots and the meteorological station was 10.75 km (1.7km – 15.6km). We used multiple regression analysis to explore relationships between sample-period rainfall and monthly accumulated rainfall with the overall density of frogs found active in that particular month. We performed the analysis in the environmental R version 3.2.3 (RStudio Team, 2015).
Results and Discussion We recorded 371 individual frogs belonging to six families and 24 species (Table 1). We found a positive relationship between climatic variables and overall frog 2 densities (Multiple Regression Analysis; F2,14 = 5.673; R = 0.448; p = 0.016). However, only the sample-period rainfall explained an additional part (p = 0.005) of frog abundance after removing the effect of the monthly accumulated rainfall (p = 0.896) (Fig. 1). We found that accumulated rainfall of just the day of sampling period is a better predictor of frog abundance Figure 1. Main results of the Multiple Regression Analysis than monthly accumulated rainfall, which suggests a between (A) anuran density vs. monthly accumulated rainfall clear response of frogs to the amount of rain falling in a and (B) anuran density vs. sample-period rainfall, recorded at short period. It has been demonstrated that the activity Vale Natural Reserve, municipality of Linhares, northern state or abundance of anurans can respond immediately to of Espírito Santo, southeastern Brazil. The importance of fine-scale rainfall data to reveal abundance patterns 247 1
Table 1. Species of anurans recorded in Vale Natural Reserve, municipality of Linhares, northern of Espirito Santo State, Brazil, their respectiveTable abundances, 1. Species period of anurans of the recorded day in whichin Vale the Natural species Reserve, was recorded municipality (D = ofday, Linhares, N = night) northern and recordingof method (V = visual, A = auditory).Espirito Santo State, Brazil, their respective abundances, period of the day in which the species was recorded (D = day, N = night) and recording method (V = visual, A = auditory).
Family / Species Abundance Period Method Bufonidae
Rhinella crucifer (Wied-Neuwied, 1821) 1 N V Craugastoridae Haddadus binotatus (Spix, 1824) 32 D/N V Hylidae
Aparasphenodon brunoi Miranda-Ribeiro, 1920 126 D/N V Boana pombali (Caramaschi, Pimenta & Feio, 2004) 9 N V/A Boana semilineata (Spix, 1824) 2 N V/A Dendropsophus decipiens (Lutz, 1925) 11 D/N V/A Ololygon agilis (Cruz & Peixoto, 1983) 36 D/N V Ololygon argyreornata (Miranda-Ribeiro, 1926) 47 D/N V Phyllodytes luteolus (Wied-Neuwied, 1824) 6 N V/A Scinax alter (Lutz, 1973) 14 N V/A Scinax cuspidatus (Lutz, 1925) 1 N V/A Scinax eurydice (Bokermann, 1968) 5 N V/A Scinax sp1 1 N V Scinax sp2 1 N V Trachycephalus mesophaeus (Hensel, 1867) 26 D/N V/A Leptodactylidae
Leptodactylus fuscus (Schneider, 1799) 9 N V/A Leptodactylus sp. 1 D V Physalaemus aguirrei Bokermann, 1966 3 D/N V/A Physalaemus crombiei Heyer & Wolf, 1989 12 D/N V/A Physalaemus gr. signifer 18 D/N V/A Microhylidae
Chiasmocleis capixaba Cruz, Caramaschi & Izecksohn, 1997 3 N V Chiasmocleis schubarti Bokermann, 1952 3 N V Dasypops schirchi Miranda-Ribeiro, 1924 1 N V Odontophrynidae
Proceratophrys laticeps Izecksohn & Peixoto, 1981 3 N V TOTAL 371
Although the importance of the monthly accumulated pattern of explosive breeding, such as Trachycephalus rainfall on anuran abundance and richness is unequivocal mesophaeus (Wells, 1977; Carvalho-e-Silva and due to its relationship with species’ reproductive activity Garcia, 2004). In any case, we strongly suggest that (e.g. Kopp and Eterovick, 2006; Kopp et al., 2010),we future studies that aim to evaluate the effect of rainfall demonstrated here that considering rain falling in a on frog activity or abundance take into consideration finer scale might better explain anuran activity. We precipitation variables at different scales, whenever this acknowledge that, in our study area, this may have type of data is available. been related to the period of intense atypical drought in the region and the presence of species that show the 248 Juliane Pereira-Ribeiro et al.
Acknowledgements. We thank Vítor C. Rocha for the revision Magnusson, W.E., Lima, A.P., Luizão, R., Luizão, F., Costa, F.R.C., of the manuscript. CNPq provided grants to HGB (process # Castilho, C.V., Kinupp, E.V.F. (2005): RAPELD: A modification 307781/2014-3 and # 457458/2012-7) and CFDR (# 302974/2015- of the Gentry Method for biodiversity surveys in long-term 6 and # 424473/2016-0). FAPERJ provided grants to CFDR ecological research sites. Biota Neotropica 5:1–6. (process E-26/102.765.2012 and E-26/202.920.2015) and to Kopp, K., Eterovick, P. C. (2006): Factors influencing spatial and HGB (process E-26/201.267.2014 and E-26/202.757/2017). This temporal structure of frog assemblages at ponds in southeastern study was financed in part by the CAPES - Finance Code 001. Brazil. Journal of Natural History, 40: 1813–1830. The ICMBio provided the permit for the development of the Kopp, K. A., Signorelli, L., Bastos, R. P. (2010): Distribuição study (license # 46327-4) and the Vale Natural Reserve for the temporal e diversidade de modos reprodutivos de anfíbios Research in the Reserve. anuros no Parque Nacional das Emas e entorno, estado de Goiás, Brasil. Iheringia, 100: 192–200. References Peixoto, A.L., Gentry, A. (1990): Diversidade e composição florística da Mata de Tabuleiro na Reserva Florestal de Linhares Aichinger, M. (1987): Annual activity patterns of anurans in a (Espírito Santo, Brasil). Revista Brasileira de Botânica 13: seasonal neotropical environment. Oecologia 71: 583–592. 19–25. Bertoluci, J., Rodrigues, M. T. (2002): Seasonal patterns of breeding Prado, C.P.A., Uetanabaro, M., Haddad, C.F.B. (2005): Breeding activity of Atlantic Rainforest anurans at Boracéia, Southeastern activity patterns, reproductive modes, and habitat use by anurans Brazil. Amphibia-Reptilia 23:161–167. (Amphibia) in a seasonal environment in the Pantanal, Brazil. Boquimpani-Freitas, L., Marra, R.V., Van Sluys, M., Rocha, Amphibia-Reptilia 26: 211–221. C.F.D. (2007): Temporal niche of acoustic activity in anurans: RStudio Team. (2015): RStudio: Integrated Development for R. interspecific and seasonal variation in a neotropical assemblage RStudio, Inc., Boston, MA. Accessible at: http://www.rstudio. from south-eastern Brazil. Amphibia-Reptilia 28: 269–276 com. Carvalho-e-Silva, S.P., Garcia, P. (2004): Trachycephalus Saenz, D., Fitzgerald, L.A., Baum, K.A., and Conner, R.N. (2006): mesophaeus. 7he IUCN Red List of Threatened Species. Version Abiotic correlates of anuran calling phenology: The importance 2014.3.
Accepted by Renato Nali