Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae)

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(1)See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/265208022. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Article in South American Journal of Herpetology · August 2014 DOI: 10.2994/SAJH-D-13-00036.1. READS. 410. 3 authors, including: Andrés Canavero. Raul Maneyro. University of the Republic, Uruguay. University of the Republic, Uruguay. 20 PUBLICATIONS 213 CITATIONS. 72 PUBLICATIONS 572 CITATIONS. SEE PROFILE. All in-text references underlined in blue are linked to publications on ResearchGate, letting you access and read them immediately.. SEE PROFILE. Available from: Raul Maneyro Retrieved on: 05 August 2016.

(2) Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Author(s): Cecilia Bardier, Andrés Canavero and Raúl Maneyro Source: South American Journal of Herpetology, 9(2):106-113. 2014. Published By: Brazilian Society of Herpetology DOI: http://dx.doi.org/10.2994/SAJH-D-13-00036.1 URL: http://www.bioone.org/doi/full/10.2994/SAJH-D-13-00036.1. BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research..

(3) South American Journal of Herpetology, 9(2), 2014, 106–113 © 2014 Brazilian Society of Herpetology. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier1,*, Andrés Canavero2,3, Raúl Maneyro1 1. Laboratorio de Sistemática e Historia Natural de Vertebrados, Facultad de Ciencias, Universidad de la República, Iguá 4225, CP 11400, Montevideo, Uruguay. Center of Applied Ecology and Sustainability, Departamento de Ecología, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, CP 6513677, Santiago, Chile. 3 Centro Universitario de Rivera, Universidad de la República, Ituzaingó 667, Rivera, Uruguay. * Corresponding author. Email: [email protected] 2. Abstract. Space and time are two of the main dimensions of the ecological niche. Because of their high dependence upon aquatic environments during breeding activity, anuran assemblages are interesting models for studying inter-populational relationships. The overlap in habitat use could be particularly high, especially for seasonal species and among taxa that share a common phylogenetic history. Three species of the Leptodactylus fuscus group occur in a semi-permanent pond at Cerro Verde (Rocha, Uruguay): L. latinasus, L. mystacinus and L. gracilis. The aim of this work was to describe the spatial and temporal calling patterns of the three species and the effects of environmental conditions upon them on a daily scale. Their relative abundance was quantified over four weeks (December 2004–January 2005) during the first half of the night along a transect using acoustic surveys. Nestedness, segregation, Jaccard’s index and association analysis were calculated, revealing a nested pattern with low overlap between species in the occupation of microhabitats. On the temporal axis, the calling behavior of the species seems to be better described by the time of night than by temperature, humidity, or atmospheric pressure. These analyses also showed a non-linear association of activity with time of night, indicating that higher activity occurs at different hours for each species. Keywords. Breeding activity; Microhabitat; Uruguay; Vocalization. Resumen. Tiempo y espacio son dos de las principales dimensiones del nicho ecológico. Debido a su alta dependencia de los ambientes acuáticos durante la actividad reproductiva, los ensambles de anuros son modelos interesantes para el estudio de las relaciones interpoblacionales. La superposición en el uso del hábitat podría ser muy elevada, especialmente para las especies de reproducción estacional y entre los taxones que comparten una historia filogenética en común. Tres especies pertenecientes al grupo de Leptodactylus fuscus fueron registradas en una laguna semi-permanente en Cerro Verde (Rocha, Uruguay): L. latinasus, L. mystacinus y L. gracilis. El objetivo de este trabajo es describir los patrones espaciales y temporales de la actividad de vocalización de las tres especies, y los efectos de las condiciones ambientales sobre tales patrones, a escala diaria. La abundancia relativa fue cuantificada durante cuatro semanas (diciembre/2004 - enero/2005) durante la primera mitad de la noche a lo largo de un transecto, realizando estimaciones acústicas. Se utilizaron índices de anidamiento, segregación, Jaccard y análisis de asociación, los cuales revelaron un patrón anidado con una baja superposición entre las especies en la ocupación de los microhábitats. En el eje temporal, la actividad de vocalización parece ser mejor descrita por la hora de la noche que por la temperatura, humedad o presión atmosférica. Estos análisis también mostraron una asociación no lineal cíclica de la actividad con la hora de la noche, indicando que la mayor actividad se produce a horas diferentes para cada especie.. INTRODUCTION For most of anuran amphibian species, advertisement calls produced by males represent the main behavioral manifestation in their reproductive activity (Wells, 2007). This activity is not usually performed by a single male, or even a single species, at the same time and space, but by males of many species as the local assemblage converges on the same water body to breed (Crump, 1982). Every species forms aggregations that allow individuals to maximize their reproductive chances while minimizing energetic costs and exposure to predators (Ryan et al., 1981; Wong et al., 2004). Many studies have been examined reproductive activity patterns in this synchronopatric species scenario, especially concerning differential resource use by different species (Crump, 1982; Toft, 1985). Main partitioning has been observed regarding the emission of vocalizations Submitted: 21 October 2013 Accepted: 18 July 2014. with different acoustic properties (Hödl, 1977; Martins and Jim, 2003; Amézquita et al., 2011), differential use of calling sites (Crump, 1971; Cardoso et al., 1989; Martins et al., 2006; Santos et al., 2007), and temporal segregation in the use of reproduction sites (Cardoso and Martins, 1987; Cardoso et al., 1989; Gottsberger and Gruber, 2004; Santos et al., 2007). However, breeding patterns are not only the result of interspecific interactions, given that the initiation and maintenance of amphibian reproductive activity are highly dependent on abiotic conditions (Duellman and Trueb, 1994). Air temperature, rainfall, illumination levels, and atmospheric pressure are the most studied factors in relation to vocalization patterns (Wells, 2007). The Neotropical genus Leptodactylus is an interesting model to study patterns of breeding activity and their association with abiotic variables on a daily scale. These species characteristically build foam nests, a feature that. Handling Editor: Cynthia Peralta de Almeida Prado doi: 10.2994/SAJH-D-13-00036.1.

(4) South American Journal of Herpetology, 9(2), 2014, 106–113. allows them to be partially independent from the aquatic environment for reproduction (Heyer, 1969; Duellman and Trueb, 1994). Species of this genus were traditionally distributed in five groups: Leptodatylus ocellatus, L. marmoratus, L. melanonotus, L. pentadactylus, and L. fuscus (Heyer, 1969; Maxson and Heyer, 1988). The species of the L. fuscus group exhibit a high independence in their reproductive function from the aquatic environments because their foam nests are built in subterranean chambers (Heyer, 1969; Philibosian et al., 1974; Martins, 1988; Ponssa, 2008). These chambers are usually associated with temporary and seasonal water bodies, in sites adjacent to the water body, and/or inside the pond basin when it dries (Gallardo, 1964a; Rossa-Feres et al., 1999; Eterovick and Sazima, 2000; Lucas et al., 2008). Males vocalize from or near the subterranean chamber; females are attracted to the chamber and oviposition occurs inside it (Peltzer and Lajmanovich, 2007; Lucas et al., 2008; Oliveira Filho and Giaretta, 2008). This is considered reproductive mode 21 (Duellman and Trueb, 1994; Prado et al., 2005). For this reason, the location of vocalization sites allows the detection of spatial and temporal reproductive activity patterns in these species, which are expected to be similar among species of the L. fuscus group because they are monophyletic (Ponssa, 2008). For many species of the Leptodactylus fuscus group, the reproductive season coincides with the wet and/or warm season (Gallardo, 1964b; Martins, 1988; Gottsberger and Gruber, 2004; Canavero et al., 2008). On a daily scale, the reproductive activity is mostly nocturnal; specifically, it occurs during the first half of the night (Dixon and Heyer, 1968; Martins, 1988; Cardoso and Haddad, 1992). The L. fuscus group is represented by four species in Uruguay: L. furnarius Sazima and Bokermann, 1978, L. gracilis (Duméril and Bibron, 1840), L. latinasus Jiménez de la Espada, 1875 and L. mystacinus (Burmeister, 1861). Leptodactylus furnarius only occurs in Rivera Department (Canavero et al., 2001), and the other three species occur all over the country (Núñez et al., 2004). They share similar habitats and breeding period (September to March: early spring to late summer) (Canavero et al., 2008; Maneyro and Carreira, 2012) and are among the most water-independent anuran species in Uruguay: they are able to vocalize when the water body is dry and no other species is breeding. These facts allow us to study how phylogenetically and ecologically close species share resources during the breeding season, and how the environmental conditions could affect this activity over a short temporal scale. The aim of this study is to describe the spatial and temporal (daily scale) vocalization patterns of three species of the Leptodactylus fuscus group (L. latinasus, L. mystacinus and L. gracilis) and the effects of the environmental conditions over them.. MATERIALS AND METHODS Study area The study area is located at the northern limit of the Protected Area Cerro Verde, Rocha Department, Uruguay (33°54’S, 53°30’W; Fig. 1). This area is characterized by a humid subtropical climate (average temperature 16°C, annual rainfall 950 mm) and an ocean coastline with dunes (20–30 m elevation) and plains (Alonso Paz and Bassagoda, 2003). Samples were taken at a long-term temporary pond (sensu Moreira et al., 2010) of 11,100 m2, which is in the lowest part of a meadow. The pond is surrounded by coastal dunes to the southeast, by grassland to the northeast and by several patches of exotic eucalyptus (Eucalyptus sp.).. Data collection The study area was divided into five different microhabitats according to the main plant and soil composition (Fig. 2): dense rushes (Scirpus sp.; R), mud and scattered rushes (MR), mud (M), mud and aquatic macrophytes (such as Azolla sp.; MA), and grassy meadow (G). Microhabitat M exhibited a disturbed microtopography because. Figure 1. Location of the study area. Empty circle = Cerro Verde, the surrounding area is the Protected Area, star = location of the pond, solid circle = La Coronilla, the nearest populated locality.. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier, Andrés Canavero, Raúl Maneyro. 107.

(5) South American Journal of Herpetology, 9(2), 2014, 106–113. Figure 2. Microhabitats defined in the pond. G = grassy meadow, M = mud, MA = mud and Azolla spp., MR = mud and scattered rushes, R = dense rushes. Numbers indicate the sampling points and the order in which they were surveyed.. of the presence of cattle in the study area. The maximum water level of the pond during the first four nights was 15 cm, with water restricted to the MA habitat. The pond then dried completely and remained that way for the duration of this study. The three species were sampled at the midpoint of their breeding season (December 2004–January 2005), four nights every two weeks, totaling 16 study nights. Calling activity was surveyed every hour from 20:30 h (after sunset, which occurs between 18:40–19:00 h in this period and locality) to 01:30 h and consisted of 15 min at each sampling point at each microhabitat, covering the total surface of the pond. Sampling points were separated 20–30 m from each other, with two sampling points for each microhabitat (some microhabitats shared the same sampling point; Fig. 2). At each of these points, species were identified by their advertisement calls, and these vocalizations were used to indicate breeding activity (Scott and Woodward, 2001). Species of the Leptodactylus fuscus group were recognized based on the vocalizations described in Straneck et al. (1993). Relative quantification of vocalizations was achieved by defining five abundance categories: 0 (no males calling), 1 (one calling male), 2 (two to five calling males), 3 (more than five calling males with calls being distinguishable from each other), and 4 (a chorus, individual calls can not be distinguished; Moulton et al., 1996; Shirose et al., 1997). Air temperature was measured hourly in the field; atmospheric pressure and relative humidity data for each hour of the sampling nights were obtained from the meteorology station of Dirección Nacional de Meteorología placed in Rocha Department (97 km SW from the study area). Rainfall measurements were not included in this study because precipitation was not significant during the study period (below 44.5 mm).. Statistical analyses Spatial patterns A presence (1) and absence (0) matrix was constructed with species as rows (i,j) and microhabitats (k,l). 108. as columns to perform a co-occurrence analysis (only in completely sampled nights) using two metrics: the C-Score (CS) and the Nestedness Based on Overlap and Decreasing Fill (NODF) (Stone and Roberts, 1990; Almeida-Neto et al., 2008). The CS, a measure of segregation of the species in the microhabitats, is calculated as CSij = (Ri - M) (Rj - M), where Ri is the row total for species i, Rj is the row total for species j, and M is the number of microhabitats that contain both species. The CS is calculated for all unique species pairs in the matrix and averaged (Stone and Roberts, 1990). A large CS indicates that more species pairs are segregated in their occurrences. For the index NODF, the DFpaired is the decreasing fill of the species i to j and of microhabitats k to l, and POpaired the paired overlap (percentage of 1’s equally placed) for species i to j and for microhabitats k to l, Npaired = 0 if DFpaired = 0 and Npaired = POpaired if DFpaired = 100, then NODF is calculated as NODF = ∑Npaired / [n(n-1) / 2] + [m(m - 1) / 2], where n (n-1) / 2 is the number of paired columns and m(m-1) / 2 the number of paired rows. Large values of NODF indicate higher patterns of nestedness of the species in the microhabitats. The null model algorithm chosen to contrast observed indices with null expectations and obtain significance levels for co-occurrence and nestedness indices was fixed column–equiprobable row (sequential swap), to allow the row total for species to vary freely but maintaining the column totals for microhabitats (Gotelli, 2000). This model is less restrictive than the fixed column–fixed row model, which is prone to fail because there are too few or even no matrix re-arrangements possible that will simultaneously preserve row and column totals (AlmeidaNeto et al., 2008). The standardized effect size (SES) was also calculated to quantify the direction and degree of deviation from the null model. SES is the Z-transformed score, where Z = (x - ȝ) / ı where x = observed index value, ȝ = arithmetic mean, and ı = SD of the 100 index values from the simulated matrices. SES values below -2.0 or above 2.0 indicate approximate statistical significance at the 5% error level (two-tailed test). Null models, nestedness, and co-occurrence indices were calculated using the software application CoOcurrence (Ulrich, 2006). The differences in the frequency of occurrence of each species at every microhabitat was analyzed using a contingency table for the matrix of species presenceabsence. To determine which microhabitat each species was associated with, Pearson’s chi-squared test was run from the contingency table using Statistica 8.0 (StatSoft, 2007). It was calculated based on the total occupation (at the end of the study) of each microhabitat by the species. To determine the degree of overlap in the use of the microhabitats between species, a cluster analysis was run for the occupation of the microhabitats using Single Linkage grouping method based on Jaccard’s similarity index, considered as highly overlapping when the Cj value was > 0.75, as partly overlapping when 0.50 < Cj < 0.75, and. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier, Andrés Canavero, Raúl Maneyro.

(6) South American Journal of Herpetology, 9(2), 2014, 106–113. as non-overlapping when the Cj was < 0.50. The software used for this analysis was Xlstat 7.5.3 (Addinsoft, 2005). Temporal patterns and environmental variables A correlation table for pairs of abiotic variables was built using the Spearman rank correlation coefficient to obtain intercorrelated variables. The variables included in this analysis were air temperature (°C), atmospheric pressure (hPa), relative humidity (%), and time (hour, numeric model). Spearman rank correlations were also calculated between species relative abundances (summarized as the L. fuscus group, and individually) vs. abiotic variables. A sinusoidal regression was fitted for relative abundances (summarized as the L. fuscus group and individually) to time of night to detect any cyclic, non-linear pattern of activity related to time. The model employed was: Sa = Smean + Samp (sin [2 Pi (M + c) / 24]), where Sa is the abundance of amphibians calling at a given time M of the day, Smean is the mean abundance calling along the time series, Samp is the maximum deviation from Smean (amplitude of the function, daily oscillation of abundance) and c is a correction factor that synchronizes the sinusoidal function with anuran calling data. Model parameters were estimated by an iteration procedure minimizing the sum of squares (Canavero et al., 2008). It is important to note that a significant estimation of the sinusoidal parameter Samp indicates a community with a cyclical calling activity. Temporal analyses were performed using Statistica 8.0 (StatSoft, 2007).. RESULTS The only species found breeding during the study were Leptodactylus gracilis, L. latinasus, and L. mystacinus. Sporadic vocalizations of Scinax squalirostris and S. granulata were heard when the pond was already dry, and, therefore, these species were not breeding.. Spatial patterns The dimensions of the constructed presence-absence matrix were 3 x 50 (3 species x 5 microhabitats surveyed over 10 days), which was filled in 65%. The cooccurrence analysis showed the matrix was significantly nested (NODF = 6.67) and significantly non-segregated (CS = -11.18), with nestedness occurring among the three species in their occupation of the microhabitats of the water body (Table 1). The association of these species with the microhabitats surveyed was significant for the total occupation of the species (Pearson’s ɖ2= 122.88; P < 0.001). Leptodactylus gracilis occurred in every microhabitat, having the highest percentages of occurrence. Figure 3. Percentage occurrence of the species in the microhabitats. G = grassy meadow, M = mud, MA = mud and Azolla spp., MR = mud and rushes, R = rushes, Lgr = Leptodactylus gracilis, Lla = L. latinasus, Lmy = L. mystacinus.. (> 15%) at three of the five sites (MA, MR and R); L. latinasus was also present at every site but occurred most frequently in the MR microhabitat; L. mystacinus occurred at three microhabitats (MR, MA and G) at a low frequency (< 15%) (Fig. 3). The cluster analysis showed a slight partial overlap between L. latinasus and L. gracilis (Cj = 0.52) and no overlap between this group and L. mystacinus (Cj = 0.39) in the use of microhabitats.. Temporal patterns and environmental variables Mean temperature during the sampling period was 19.38 ± 3.24°C, mean pressure: 1012.24 ± 2.90 hPa, and mean relative humidity: 84.34 ± 8.89%. The correlations between abiotic variables indicate that air temperature and atmospheric pressure were negatively correlated, and relative humidity was positively correlated with time (Table 2). Breeding activity of Leptodactylus latinasus and L. gracilis were only correlated to time, neither the activity of L. mystacinus nor the activity of the three species as a group, showed correlation to any abiotic variable (Table 3). All the sinusoidal fits were significant (Samp P-value < 0.001 in all cases), with explanatory power > 30%, except for L. mystacinus (13%), over the breeding activity of the animals (Table 4).. DISCUSSION Spatial patterns Phylogenetically related and ecologically similar species are more prone to exhibit interspecific competition, so their coexistence, in many cases, could be explained by partitioning the resources they share (Begon et al., 2006). Regarding resources used during breeding activity by. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier, Andrés Canavero, Raúl Maneyro. 109.

(7) South American Journal of Herpetology, 9(2), 2014, 106–113. Table 1. Results of the co-occurrence analysis using the segregation C-Score and nestedness NODF metrics. In = obtained value of the index, SimIn: simulated value of the index, StdDevIn: Standard deviation of the SimIn, Z-In = standardized effect size, L95%CIn and U95%CIn = lower and upper 95% confidence interval of each index, respectively. Index C-Score NODF. In 36.00 57.31. SimIn StdDevIn Z-In L95%CIn U95%CIn 83.97 4.29 -11.18 73.67 91.33 53.93 0.51 6.67 52.79 54.83. Table 2. Spearman rank correlation table for pairs of abiotic variables. Bold type indicates significant (P < 0.001) correlations. NM = numeric model of time of night. Time (NM). Atmospheric Tempe- Humipressure rature dity (hPa) (°C) (%). Time of night (NM) Atmospheric pressure (hPa) 0.17 Temperature (°C) -0.13 Humidity (%) 0.58. -0.40 0.10. -0.13. -. Table 3. Spearman rank correlation table for relative abundances of the species (summarized as the Leptodactylus fuscus group and for each species individually) vs. abiotic variables. Bold type indicates significant (P < 0.001) correlations. NM = numeric model of time of night.. 0.21 0.07. 0.04 -0.05. -0.53 -0.18. L. fuscus group -0.06 -0.05. -0.02 0.11. 0.20 0.20. 0.20 -0.17. 0.14 0.07. L. latinasus L. mystacinus L. gracilis Time of night (NM) Atmospheric pressure (hPa) Temperature (°C) Humidity (%). Table 4. Parameters and fit of the sinusoidal model to relative abundances of the species (summarized as the Leptodactylus fuscus group and for each species individually) to time of night. Species L. fuscus group L. gracilis L. latinasus L. mystacinus. R2 0.32 0.32 0.34 0.14. Samp 16.82 3.96 9.30 3.79. SE 2.36 1.06 1.53 1.01. P-value < 0.001 < 0.001 < 0.001 < 0.001. anuran amphibians, main partitioning has been recorded in the emission of advertisement calls with different acoustic properties (Hödl, 1977; Martins and Jim, 2003; Martins et al., 2006). In this sense, the advertisement calls of the species from the Leptodactylus fuscus group in this study have already been described and it has been pointed out that there would not be acoustic interference between them because of the spectral separation of their calls (Barrio, 1965; Straughan and Heyer, 1976). Another resource usually partitioned during the breeding season is the space for calling displays and/ or oviposition sites (Crump, 1971; Hödl, 1977). Spatial segregation in the use of microhabitats for breeding by congeners has been observed in many amphibian species. 110. (Cardoso et al., 1989; Rossa-Feres and Jim 2001; Menin et al., 2005; Martins et al., 2006), even in leptodactylids (Eterovick and Sazima, 2000; Rossa-Feres and Jim, 2001). Instead, similarities in the use of calling sites would be expected in species of the Leptodactylus fuscus group because they constitute a monophyletic group, with a shared reproductive mode: foam nest in burrow, and larvae feeding in ponds after flooding (Ponssa, 2008). The results of this study indicate that L. gracilis, L. latinasus, and L. mystacinus are not segregated in the use of microhabitat, being nested in their spatial occupation of the pond. The nested pattern of species occurrence could be explained by differences in the abundance of each species, with a more abundant species being able to occupy more microhabitats than a less abundant species (Atmar and Patterson, 1993). Leptodactylus mystacinus was the least abundant species and also the least represented in the microhabitats; however, the abundances of L. latinasus and L. gracilis were also low at some hours of the night and the nested scheme of microhabitat occupation was maintained when analyzed using the daily presence-absence data. The permanence of the structure of the assembly indicates absence of density dependence in the use of calling sites by the species, as postulated previously by Crump (1982). On the other hand, the observed nested pattern could also be explained by the nested nature of the microhabitats defined by this study: mud, rushes, and mud and rushes were identified as three different microhabitats, but they share characteristics. This would lead to nested patterns when there is some degree of selectivity for the microhabitats by the species, with some species being more generalist than others and revealing an ordered but not segregated (or partitioned) structure in the use of microhabitats (Ulrich et al., 2009). This is consistent with the observed frequency of microhabitat occupation: Leptodactylus gracilis seems to be the most generalist species and L. mystacinus the most selective. Mud and rushes seems to be the most suitable microhabitat for the three species, whereas rushes are exploited almost exclusively by L. gracilis. Although a nested pattern was observed, there was low overlap among the species. This result suggests the nestedness of the assemblage does not imply interference between species when they share microhabitats for breeding. Spatial avoidance between species from the Leptodactylus fuscus group has been observed (Eterovick and Sazima, 2000), and more studies need to be conducted to determine the strategies of ordination between these leptodactylids at a finer scale (e.g., location of burrows of each species within microhabitats). Also, the observed occupation scheme might change after the pond fills during the breeding season, because of the alteration of the area available for construction of subterranean chambers, thereby increasing the overlap among the vocalization or oviposition sites of these species.. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier, Andrés Canavero, Raúl Maneyro.

(8) South American Journal of Herpetology, 9(2), 2014, 106–113. Because the environment might affect acoustic properties of vocalizations (Bosch and De la Riva, 2004), it would be expected for the species to select microhabitats for their acoustics (Duellman and Trueb, 1994), although some authors argue that there is no evidence that amphibians choose vocalization sites for this reason (Wells and Schwartz, 1982). Other reasons to have different preferences for vocalization sites might be related to the presence of predators in the study area (Wells and Schwartz, 1982). This could influence the tendency of the three species to occupy the mud and rushes microhabitat with vegetation that conceals the organisms from predators, and wet soil to build the chambers. Leptodactylus gracilis also occupied more exposed microhabitats, such as mud alone and mud with Azolla sp., but males were observed calling from within chambers. Interspecific interactions that were not analyzed in this study also might also determine the spatial structure of the assemblage (Crump, 1982; Toft, 1985). Regarding the habitats and microhabitats where each species occurred, the three species are usually associated with semipermanent and long-term temporary ponds like the one we studied (Peltzer and Lajmanovich, 2007). In the present study, Leptodactylus gracilis was generally associated with places having wet soil, as described in Argentina by Gallardo (1964a). Achaval and Olmos (2007) found in association with floodplains during its breeding season in Uruguay. This supports our findings if the whole pond is considered a small, isolated floodplain. Leptodactylus latinasus was associated with similar habitats as those described by Gallardo (1964b) and Basso (1990). The grassland was hardly used by this species; this result differs from what was found by Vaz-Ferreira and Gehrau (1974), who observed that this species’ chambers are often found far from water. Leptodactylus mystacinus was associated with microhabitats similar to those described by Abrunhosa et al. (2001) and Oliveira Filho and Giaretta (2008). Gallardo (1964b) described this species as an inhabitant of grassy places, especially in cleared areas where herbaceous vegetation is present, but with enough environmental plasticity that it is sometimes encountered in dry habitats. In other works, it has been found breeding on dry soil in Eucalyptus sp. plantations and in urban areas (Toledo et al., 2003; Ávila and Ferreira, 2004; Oyamaguchi, 2006). The environmental plasticity attributed with this species was not observed in this study, but the low abundance of the species might be masking its environmental preferences.. Temporal patterns Temperature is considered a main determining factor for breeding activity of amphibians, because they are ectothermic organisms (Feder and Burggren, 1992). In. this study, species activity was not significantly correlated with air temperature, humidity, or atmospheric pressure. In contrast, the activity of Leptodactylus latinasus and L. gracilis was exclusively correlated with the time of night. Indeed, time of night appeared as a determining factor in the activity of Leptodactylus latinasus, L. gracilis, and the L. fuscus group, and in a smaller proportion for L. mystacinus, when analysed as a cyclic function of time. Mainly, the sinusoid model of time explained a large proportion of the activity, indicating a non-linear effect of time on activity. A similar pattern was observed during the first half of the nights (Cardoso and Martins, 1987; Cardoso and Haddad, 1992), although it was not supported for relative abundances of each species. This association of reproductive activity with time of night (and the absence of association to climatic variables) can be explained by the influence of different cyclic factors, such as the association with an unanalyzed daily cyclic environmental (biotic or abiotic) variable, the circadian cycles of these species (which result from the interaction between endogenous cycles and the exogenous variation of the illumination levels) and/or another endogenous cycles of these species (Jørgensen, 1992; Kronfeld-Schor and Dayan, 2003). Regarding illumination levels (photoperiod), they might act as a variable that synthesizes most of the environmental change along the day, allowing the animals to predict the most suitable conditions to breed, rather than responding to a specific weather variable (Bradshaw and Holzapfel, 2007). Cardoso and Haddad (1992) argue that the cycles in the anuran assemblies, on a daily scale, are determined by avoidance of the highest illumination periods of the day (in order to avoid desiccation and/or insolation), as well as the coldest periods of the night. Similar to what was found by Brooke et al. (2000), it was difficult to predict calling intensity on a particular day in our study based on environmental conditions; however, our results indicate that time of night is a better predictor. In addition to possible circadian rhythms, these results might also be related to the reproductive modes of these leptodatylids, which include vocalizations from inside of their chambers, making them quite independent from weather variables (Cardoso and Haddad, 1992). This independence can also be favored by the reproductive activity itself which can modify and maintain stable body temperatures once it begins (Feder and Lynch, 1982). The temporal species activity curves confirm the variation of abundance mentioned for the spatial scale, but also show segregation in the hours of maximum activity of each species, suggesting that species would not overlap in the climax of their activity. This result could be interpreted as indicating the existence of a temporal partition of the acoustic niche, which has been observed previously (Littlejohn and Martin, 1969; Crump, 1982). However, other factors not related to competence could. Temporal and Spatial Activity Patterns of Three Species in the Leptodactylus fuscus Group (Amphibia, Leptodactylidae) Cecilia Bardier, Andrés Canavero, Raúl Maneyro. 111.

(9) South American Journal of Herpetology, 9(2), 2014, 106–113. be guiding the partitioning of the temporal dimension, such as the autecological optimal conditions of each species, predation, or intraspecific competition (Toft 1985). Finally, photoperiod has been identified previously as the main determinant of species breeding activity at a seasonal scale in Neotropical assemblages (Both et al., 2008; Canavero et al., 2008; Canavero and Arim, 2009). These studies also included leptodactylids from the Leptodactylus fuscus group. Focusing on finer scales (e.g., daily scale) could help better understand the relationship between the activity of the species belonging to the Leptodactylus fuscus group and climatic factors and photoperiod.. ACKOWLEDGMENTS We want to acknowledge Alejandro Fallabrino and Andrés Estrades from the NGO KARUMBE and Carlos Romero for the logistic support during the field surveys. 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