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Hydrobiologia

, Volume 827, Issue 1, pp 367–378 | Cite as

Body size and population dynamics of annual fishes from temporary wetlands in Southern Brazil

  • Matheus V. Volcan
  • Ândrio C. Gonçalves
  • Demetrio Luis Guadagnin
Primary Research Paper

Abstract

Annual fishes live exclusively in temporary wetlands where several species coexist. Understanding how annual fishes cohabit in small and isolated pools is still a challenge. In this study, we aimed to examine the prediction that annual fish assemblages in temporary pools in Southern Brazil are structured by temporal differences in body size, specific growth rate and density. Two–three fish species coexisted in each pool. The most abundant and frequent species were Cynopoecilus melanotaenia and Austrolebias nigrofasciatus, while A. wolterstorffi was less abundant and rare. The species differed significantly in body size throughout the flooding phase and showed similar growth patterns, with higher specific growth rates in the first months of flooding and a reduction in growth rate thereafter. The monthly average densities of A. nigrofasciatus and C. melanotaenia did not differ over time, but they were higher than values observed for A. wolterstorffi. Our results provide evidence for hatching synchrony, similar specific growth rates and densities among the most abundant species and differences in body sizes among all species that are more evident after adulthood, suggesting that differences in body size mediate the coexistence of annual fishes in temporary pools.

Keywords

Killifish Austrolebias Cynopoecilus Specific growth rate Density Seasonal pool 

Introduction

The biota in temporary freshwater pools fed by rain differs from permanent pools due to the peculiar spatio-temporal variation of water availability, consisting of a predictable dry phase of 3–5 months (Collinson et al., 1995; Gomes, 1998, Lanés et al., 2016). Annual fish species exclusively inhabit temporary pools (Costa, 2002; Reichard et al., 2009; Volcan et al., 2015). In these environments, seasonality (drought and flood phases of the pools) imposes a synchronized life cycle on cohabiting species (Lanés et al., 2016), as well as unique adaptations for resource sharing (Arim et al., 2009).

Neotropical annual fishes (Cyprinodontiformes; Rivulidae) have evolved adaptations to such temporary habitats, including short life cycles, rapid sexual maturation, continuous spawning, eggs resistant to drought and embryos capable of diapauses (Wourms, 1972; Errea & Danulat, 2001; Volcan et al., 2013; Fonseca et al., 2018). Often, several species of annual fishes cohabit in a single pool, suggesting elaborate ecological relationships among species, possibly derived from adaptive radiation (Costa, 2009). Understanding how annual fish species cohabit is still a fundamental challenge. Some studies suggest that coexistence is enabled by spatial segregation inside pools (Nico & Thomerson, 1989; Costa, 2002). However, many temporary pools are small and lack well-defined microhabitats. In these cases, differences in body size and mouth morphology could influence food selection and resource division within annual fish communities (Arim et al., 2009).

Annual fishes dominate the fish community and are the most abundant and conspicuous predators in small, shallow, isolated temporary pools which rarely exceed 1 hectare in area and 1 m in depth (Costa, 2002; Laufer et al. 2009; Volcan et al. 2010, 2013, 2015; Lanés et al., 2016). Species of Austrolebias and Cynopoecilus often cohabit in these temporary pools in Southern Brazil and Uruguay (Vaz-Ferreira et al. 1966; Costa, 2002; Volcan et al., 2010, 2013; Laufer et al., 2009; Lanés et al., 2014, 2016; Keppeler et al., 2014). In this region, the number of annual fish species found in a single pool ranges from one to four (Laufer et al., 2009; Volcan et al. 2010, 2014; Lanés et al., 2014), while in other locations in South America, the number of species could reach up to seven (Costa, 2002).

In temporary pools inhabited by more than one Rivulidae species, hatching occurs synchronously and differences in size and morphology are generally observed (Laufer et al., 2009; Lanés et al., 2014, 2016; Keppeler et al., 2014). However, no study has analysed how competitive exclusion can be avoided or the factors that favour the coexistence of closely related species. Since the fishes live in small, isolated and highly ephemeral environments, where resource-partitioning opportunities may be limited, it was hypothesized that differences in body size could facilitate their coexistence, by reducing the overlap in resource exploitation and antagonist interactions (Arim et al., 2009; Canavero et al., 2014). If this is true, co-occurring species would minimize size overlap among classes at any time. However, if, how, and when these differences in body size occur remains unknown. Since cohabiting species have hatching synchrony and similar growth patterns (Lanés et al., 2014, 2016), we hypothesized that species hatch synchronically, soon after the flooding of pools, but maintain different body sizes throughout the entire flooding phase.

Some annual fishes, like the Austrolebias elongatus species group, reach large body sizes for Rivulidae species (~ 8–15 cm of standard length), are top predators and tend to be rare in the temporary pools (Costa, 2006, 2009). Others species of annual fishes correspond to small- and medium-sized species that reach ~ 3–7 cm of standard length and are often more abundant in their habitats (e.g. Cynopoecilus spp. and Austrolebias adloffi species group) (Costa, 2009; Volcan et al., 2010; Lanés et al., 2016). The larger species also have larger eggs and embryos (Gonçalves et al., 2011; Volcan et al., 2012; Fonseca et al., 2013). Studies have shown differences in densities among these species/clades within the same pool (e.g. Volcan et al., 2010, 2013, 2014); however, they did not consider either the temporal variation of densities or the life-history traits. Lanés et al. (2014, 2016) observed marked population decline of two cohabiting species of Austrolebias and Cynopoecilus throughout the flooding phase in temporary pools of southern Brazil. This population decline is more related to predation than to density-dependent processes (Reichard et al., 2018).

In this study, we examined the temporal variations in hatching, body size, and density of three coexisting annual fishes from 11 temporary pools in southern Brazil during the entire hydrological cycle. We predicted that annual fish assemblages are formed by a single cohort that hatch synchronously and maintain differences in body size and density between species throughout the flooding phase. We also expected, over time, an increase in mean body size, and, after an initial increase, a steady decrease in density due to the combined effect of mortality and increment in water volume and flooded area.

Materials and methods

Study area

The study area is composed of a set of 11 temporary pools (Fig. 1) located in a floodplain section of about 500 ha on the southern coast of Brazil, between the mouths of two permanent waterbodies—the Pelotas stream and the São Gonçalo channel (31°46′29″S; 52°15′34″W), in the Patos lagoon basin, Pelotas, Rio Grande do Sul. The matrix is a flat sandy grassland used for livestock.
Fig. 1

Map of the study area with the 11 pools sampled in the floodplain of São Gonçalo channel, Rio Grande do Sul, Southern Brazil. White circles represent pools with the three species. Black circles represent pools with A. nigrofasciatus and C. melanotaenia

The climate is humid temperate (CFa) with marine influence (Rosa, 1985). The annual average temperature is 17.8°C, with a mean of 23.2°C in the hottest month (January) and 12.3°C in the coldest month (July). The average annual rainfall is 1,249 mm (monthly average of 67 mm in April to 153 mm in August). The decreasing temperature and increasing rainfall in autumn initiate the flooding phase of the pools, usually between April and November (Volcan et al., 2015).

The study area is composed of a remnant coastal environments, known as Pontal da Barra, which has priority conservation in Brazil due to the occurrence of restricted and endangered annual fish species that are seriously threatened by urban development (MMA, 2007; Volcan et al., 2009). Three species of annual fishes inhabit these pools: Austrolebias nigrofasciatus Costa & Cheffe, 2001, Austrolebias wolterstorffi (Ahl, 1924) and Cynopoecilus melanotaenia (Regan, 1912). Both A. nigrofasciatus and A. wolterstorffi are recognized as endangered (Rosa & Lima, 2008; Volcan et al., 2009) and supported by a national action plan for their conservation (ICMBio, 2013).

In southern Brazil, the pools are fed by the rain during the wet season and remain flooded from early fall (March–April) to mid/end-spring (October–November), with some yearly variation. During the summer (December–March), when rainfall is generally lower and the temperature averages are high, most pools remain totally dry.

The sampled pools are heterogeneous environments with variable depths (generally less than 60 cm) and areas [400–80,000 m2 (Coef. of variation = 186%)], which contain organic matter, high macrophyte diversity and density, and are usually isolated from other pools.

Sampling

We conducted monthly collections that lasted 2 days (intervals of 28–30 days between each collection), in each wetland over the course of a year, between April 2011 and March 2012. The sampling began when the first areas flooded in May 2011 and ended when the last area dried out in December 2011, resulting in a total of 8 months of effective sampling, during the entire hydrological cycle of the studied pools. The first sampling occurred in May, after we checked and found that all pools were desiccated at the beginning of April. Since most of the fishes collected from that campaign were no longer in the larval stage, we estimated that the area flooded about 10–15 days before sampling, which coincided with a high rainfall index in the region. We took the number of months that each wetland remained flooded as measure of the length of the flooding phase.

We collected fishes with a dip net (60 × 40 cm, 2 mm mesh) by sweeping parallel to the pool bottom. We used 25 random sweeps of 1 m, corresponding to approx. 0.6 m2 of area sampled in each wetland smaller than 1/2 ha (total area sampled = 15 m2) and 50 sweeps in pools larger than 1/2 ha (total area sampled = 30 m2). Each sweep was done in a new area during a sampling event. To measure fish abundance in each wetland and month, we calculated the capture per unit area (CPUA) as the number of individuals/m2.

We measured all collected fishes using a calliper (0.1 mm). Body size was considered the average total length (TL) of all individuals from each species in each wetland and sampling occasion. We calculated the mean specific growth rate (SGR) of fishes from each wetland between consecutive months using the equation: SGR = (ln fL − ln iL)/(tf − ti) * 100, where fL is the final length, iL is the initial length and (tf − ti) is the elapsed time in days. We calculated the SGR (% of growth/day) of the populations in each wetland at every sampling occasion. Thus, for each sampling month, we calculated the average SGR of each species.

Fishes that either could not be sexed due to small body size or that lacked dimorphic attributes, such as body pigmentation and typical adult morphology or size of the unpaired fins, were considered juveniles (Costa, 2002, 2006). The collected fishes were measured, counted and returned to the environment. About 40% of the individuals collected were randomly selected to be euthanized for future diet and reproduction analyses. We anaesthetized the fishes in a clove oil bath, fixed them in 10% formalin and preserved them in 70% alcohol. We deposited voucher specimens in the Museu da Universidade Federal do Rio Grande (FURG). Monthly average temperature (°C) and rainfall (mm) were obtained using climatological reports (Embrapa, 2012). Pool depth (cm) was obtained using a ruler in the deepest part of each pool.

Data analysis

We used Generalized Linear Mixed Models, GLMMs (Bolker et al., 2009), to test for differences in body size, SGR and CPUA among species throughout the sampling period. We used random-intercept models with species, months and their interaction as fixed effects and sampling units (pools) as random effects. We ran the analysis using the lmer function in the R package lme4 (Bates et al., 2015). These models provided a fixed-effect estimate for the interaction months*species, which told us whether the rate of change with respect to scores was significantly different among species. To check which species had significant differences in body size, SGR and CPUA in each sampling occasion, we used Tukey’s pairwise post hoc comparisons, calculated in the R package lsmeans (Lenth, 2013). The variance inflation factor (VIF) of all models without interaction terms never exceeded 1.05, which is below the value that causes important collinearity problems (Millar & Anderson, 2004).

We analysed the relationship between the length of the flooding phase and the CPUA of each species through simple linear regression, using Vegan package in the R software (Oksanen et al., 2016). We transformed CPUA and SGR into logarithms. All statistical analyses were performed in R 3.0.1 (R Core Team, 2013). We set the level of significance to P < 0.05.

Results

Of the climatic and hydrological attributes analysed, average air temperature presented the highest amplitude of variation (CV = 17%), with lowest averages associated with the months between July and September and the highest averages in May, November and December (Fig. 2). The accumulated monthly rainfall was homogenous (CV = 11%), with lowest values in November and December and the highest values in September and October (Fig. 2). Pool depth presented the highest average in the coldest months (autumn–winter) and lowest average in December (CV = 34%, Fig. 2), when most areas were dry.
Fig. 2

Monthly accumulated rainfall, air temperature and pool depth data over the eight months of flooding during a hydrological cycle in temporary pools in Southern Brazil

The number of annual fish species ranged from two to three in each pool (Table 1). We recorded Austrolebias nigrofasciatus (An) and Cynopoecilus melanotaenia (Cm) in all pools, while Austrolebias wolterstorffi (Aw) was only found in four pools (Table 1). The extent of the flooding phase in the temporary pools ranged from six to eight months (Coef. of variation = 9%). December was the eighth and final month of flooding, but some areas dried up in early November.
Table 1

Occurrence and population parameters of annual fish species in 11 temporary pools in Southern Brazil during the flooding season of 2011

Species

A. nigrofasciatus

A. wolterstorffi

C. melanotaenia

No. of inhabited pools

11

4

11

Range of occupation

May–November

May–October

May–December

Number of sampled individuals

1366

118

1837

Range of abundance per wetland: Min–Max (CV)

24–267 (64%)

6–66 (94%)

3–533 (90%)

Total Length (mm; mean ± SD)

29.2 ± 10.9

47.0 ± 15.3

25.5 ± 7.0

The number of months that each species occupied the pools varied from four to eight (Fig. 3). Austrolebias wolterstorffi was captured from May to August–October in the four pools, A. nigrofasciatus from May–June to October–November and C. melanotaenia from May–July to September–December, in the end of the flooding phase (Fig. 3).
Fig. 3

Total lengths (mm) and residence times of A. nigrofasciatus, A. wolterstorffi and C. melanotaenia from 11 temporary pools during the flooding season of 2011, Southern Brazil

We captured 164 juveniles of A. nigrofasciatus, which were recorded until the second month of sampling (June), as well as 513 males and 472 females. For A. wolterstorffi, we recorded eight juveniles until the second month of sampling, and 118 adults (43 males and 67 females). We captured 66 juveniles of C. melanotaenia, until the third month of sampling (July), and 895 males and 818 females.

Body size

The body size of A. nigrofasciatus ranged from 4 to 58 mm TL, that of A. wolterstorffi ranged between 17 and 90 mm TL and that of C. melanotaenia ranged between 9 and 46 mm TL (Table 1; Fig. 3, Online Resource 1). The three species differed in body size during months of flooding and between pools (Fig. 3, Online Resource 1). We found a significant effect of month on the average TL of the species and a significant interaction between month*species (Table 2). This result was confirmed by post hoc comparisons of each species pair (lsmeans; An X Aw: t = 23.5, P < 0.0001; An X Cm: t = 7.25, P < 0.0001; Aw X Cm: t = 27.5, P < 0.0001), indicating that the three species differed in body size, but differences depended on months. Visual inspection of Online Resource 1 indicates that such differences between A. nigrofasciatus and C. melanotaenia mainly occurred between July and December, precisely when most individuals were already adults, while A. wolterstorffi had a larger body size since the first month of sampling.
Table 2

Estimates of the fixed effects of month and species identity on the body size, SGR (specific growth rate) and CPUA (capture per unit area) of three Rivulidae annual fish species in a system of temporary pools in Southern Brazil

Fixed factor

Body size

SGR

CPUA

Estimate ± SE

t value

P

Estimate ± SE

t value

P

Estimate ± SE

t value

P

Intercept

13.03 ± 2.43

5.34

< 0.001

0.28 ± 0.06

4.72

< 0.001

1.38 ± 0.27

4.97

< 0.001

Month

4.65 ± 0.40

11.45

< 0.001

− 0.03 ± 0.01

− 2.36

< 0.05

− 0.12 ± 0.05

− 2.22

< 0.05

Aw

3.40 ± 2.72

1.250

 > 0.05

0.17 ± 0.14

1.19

 > 0.05

− 0.65 ± 0.50

− 1.29

 > 0.05

Cm

3.98 ± 1.70

2.33

> 0.05

− 0.19 ± 0.08

− 2.38

< 0.05

0.67 ± 0.32

2.09

 < 0.05

Month*Aw

8.01 ± 0.77

10.38

< 0.001

0.02 ± 0.03

0.65

> 0.05

0.01 ± 0.14

0.05

> 0.05

Month*Cm

− 2.46 ± 0.38

− 6.34

< 0.001

0.03 ± 0.01

1.81

> 0.05

− 0.11 ± 0.07

− 1.59

> 0.05

Aw = A. wolterstorffi; Cm = C. melanotaenia. Austrolebias nigrofasciatus was the reference species

Specific growth rate

The three species showed similar growth patterns, with higher SGR in the first months of flooding and a reduction in SGR thereafter (Fig. 4). The SGRs of the three species were significantly different among the months of flooding; however, the interaction among the months of flooding and the SGR was not significant (Table 2). Comparisons of SGR for each pair of species indicated that A. nigrofasciatus and C. melanotaenia had significantly lower means than A. wolterstorfii, but not between themselves (lsmeans: An X Aw: t = − 4.54, P < 0.0001; An X Cm: t = 1.984, P = 0.12; Aw X Cm: t = 5.43, P < 0.0001).
Fig. 4

Specific growth rates (SGR; mean ± SD) of A. nigrofasciatus, A. wolterstorffi and C. melanotaenia captured in 11 temporary pools during the flooding season of 2011, southern Brazil

Abundance

Cynopoecilus melanotaenia was the most abundant species in six pools, A. nigrofasciatus was the most abundant in five pools, and both species were rare in a single pool. Cynopoecilus melanotaenia showed the highest absolute abundance and A. wolterstorffi the highest variation in abundance among pools, while A. nigrofasciatus showed intermediary abundance and the lowest variation among the pools (Table 1, Fig. 4).

The monthly average CPUA was not significantly different among months of flooding; however, the interaction between month*species was significant, suggesting that CPUA values depended on species and months (Table 2, Online Resource 2). Comparisons of each species pair in each month showed that the monthly averages of CPUA of A. nigrofasciatus and C. melanotaenia did not differ. On the other hand, the CPUAs of both species were significantly higher than that of A. wolterstorffi in every month (lsmeans: An X Aw: t = − 6.41, P < 0.0001; An X Cm: t = − 1.172, P = 0.47; Aw X Cm: t = − 7.58, P < 0.0001).

We found a weak, significant negative relationship between the length of the flooding phase and the CPUAs of C. melanotaenia (r2 = 0.16; P = 0.0011), A. nigrofasciatus (r2 = 0.12, P = 0, 0049) and A. wolterstorffi (r2 = 0.47; P = 0.0049), indicating that the species densities were moderately reduced over flooding time.

Discussion

In this work, we demonstrate that in temporary pools from southern Brazil, despite being small and shallow, several Rivulidae annual fishes can coexist, which is related with synchrony of hatching and the maintenance of differences in body size throughout the flooding phase, favoured by similar specific growth rates among cohabiting species.

Few studies have compared the growth and body size of cohabiting annual fish species (Lanés et al., 2016). Furthermore, most growth studies have been performed with only one fish species (Arenzon et al., 1999; Errea & Danulat, 2001; Volcan et al., 2012; Fonseca et al., 2013). The few studies about cohabiting fish species compared the growth of Cynopoecilus fulgens Costa, 2002 and Austrolebias minuano Costa & Cheffe, 2001 and found a pattern similar to the pattern found in the present study, where A. minuano had a larger body size throughout the flooding phase (Lanés et al., 2014, 2016). Laufer et al. (2009) found significant differences in body size among species of Rivulidae from temporary pools in Uruguay; however, they did not analyse variation throughout the flooding phase. There is evidence that body size influences the trophic level of annual fish communities (Arim et al., 2009; Keppeler et al., 2014). Herein, we provide further evidence, showing species with different body sizes, which may mitigate interspecific competition due to differences in gape limitations and capture of prey.

Some territorial fish species’ populations in permanent environments are also structured by size differences, and individuals in overlapping territories tend to have different sizes (Sakai & Kohda, 1997; Kuwamura, 1984; Kohda & Tanida, 1996; Matsumoto, 2001). However, unlike the fish species in permanent environments, where several generations coexist, generations of annual fishes tend not to overlap, since only one cohort is usually present and all species tend to hatch at the same time in temporary pools (Lanés et al. 2016). Consequently, annual fish populations hatch and age together, and the maintenance of different body sizes for each species over time probably favours coexistence. On the other hand, by having similar size classes over time, intraspecific competition is unavoidable and may be controlled by density and mortality. In variable environments, the coexistence may be favoured if the time scale of resource variation is shorter than the time scale for competitive exclusion (Li & Chesson, 2016), but this holds when different species are favoured at different times. Although we did not address the competitive exclusion directly, we show empirical evidence of a particular situation when potential competing species share the same resources, but not at the same time, due to differences in body size maintained through time despite the synchrony of hatching and similar growth rates.

Growth and survival in the early stages of life strongly influence the success of recruitment and density of adult fish populations (Houde, 1987; Van der Veer et al., 1990). The largest SGR was recorded at the beginning of the flooding phase, which indicates that higher energy conversion in somatic growth occurs early in life and tends to decline towards sexual maturity, at approximately 2–3 months for the studied species (Volcan et al., 2012; Fonseca et al., 2013). The high initial SGR also means that these fishes spend less time in the most vulnerable size ranges, increasing the number of individuals who reach sexual maturity (Van der Veer & Bergman, 1987; Ellis & Gibson, 1995; Sogard, 1997). At this stage, growth rates are reduced as a trade-off of energy used for reproduction (Vazzoler, 1996; Blažek et al., 2013). In this sense, rapid early growth is critical for species inhabiting extreme environments such as temporary pools.

The different densities among the Rivulidae species indicate that abundance may play an important role in the coexistence of species and the structure of the annual fish community. Figure 5 also indicates differences in density among the species in each pool, although there was high variation in densities among pools. According to Córdova-Tapia et al. (2017) environmental filters play a major role in fish community structure in severe environmental conditions. Gonçalves (2013) verified that the landscape structure is the main factor related to the occurrence of A. nigrofasciatus and A. wolterstorffi, while plant cover of the pool is the main factor for the occurrence of C. melanotaenia. These relationships may explain the density differences recorded for the species in the sampled pools. However, A. wolterstorffi presented consistent low density, regardless of habitat and landscape features. This species is considered rare (Lanés et al., 2016), which seems to be the pattern for A. elongatus species group and other large bodied congeners, top predators in temporary pools (Costa, 2009). There is evidence that large-bodied annual fish species occupy high trophic levels (Arim et al., 2009; Keppeler et al., 2014), but they are numerically rare (Cohen et al., 2003).
Fig. 5

CPUA (mean) values of A. nigrofasciatus, A. wolterstorffi and C. melanotaenia captured in 11 temporary pools during the flooding season of 2011, Southern Brazil

Similar to our results, Lanés et al. (2016) verified that the natural lifespan of annual fishes was < 8 months and that these fishes disappeared before habitat desiccation of temporary pools in Southern Brazil. Herein we found that these fishes also have different residence times in the flooding phase of temporary pools. Possible factors explaining this pattern are the progressive reduction of water volume and changes in water chemistry, which affect the availability of resources and exposure to predators (Casciotta et al., 2005; Almirón et al., 2008). Taborsky et al. (2012) argued that size-dependent competition and size-dependent mortality are major life history traits explaining coexistence and adaptation in communities. Experimental data demonstrated that annual fishes show high sex and size specific mortality, long before habitat desiccation, because males and larger individuals are more predated by birds (Reichard et al., 2018), which may also explain the early disappearance of the larger species (A. wolterstorffi).

As seen in other studies with annual fish communities (Lanés et al., 2016), our results suggest that hatching tends to occur soon after flooding, providing longer permanence in the pools and more opportunities to reproduce before desiccation. Moreover, juveniles of both Austrolebias species were present until the second month after flooding and juveniles of C. melanotaenia up to the third month in some pools, providing evidence that hatching may continue after the first flood. We conclude that the delayed and extended hatchings occurred due to the progressive expansion of the pools, where water accumulated from successive rainfalls and flooded shallower areas that were still dry.

Our results provide evidence that annual fish communities from temporary pools in the Neotropical region are structured by body sizes differences among species, which are maintained throughout the flooding phase, mainly after adulthood. The species hatched soon after the pools flooded, but juveniles were found in the first 3 months, indicating that hatching may continue as flooding advances over dry land. These three species showed similar specific growth rates over time, especially between the most abundant species. Density also played an important role in the structure of the annual fish community, as the smaller and more abundant species (C. melanotaenia and A. nigrofasciatus) did not differ in density over time, even though they presented great variation among the pools. On the other hand, they showed a higher density than the larger species (A. wolterstorffi). Further investigation must consider the factors that favour the coexistence of annual fish species in small and isolated pools, such as dietary differences between species over time, predation and intra and interspecific competition, which affect the survival and residence time of species in temporary pools.

Notes

Acknowledgements

The authors thank Alinca P. Fonseca and Luis Esteban K. Lanés for their support in the fish collection. The authors also thank Michel Corrêa for providing the map of the study area, and ICMBio for obtaining the license (28099-1). M.V. Volcan thanks CAPES for the Ph.D. Grant. CNPq provided research fellowship to D. L. Guadagnin (309298/2009-1).

Supplementary material

10750_2018_3789_MOESM1_ESM.pdf (471 kb)
Supplementary material 1 (PDF 471 kb)
10750_2018_3789_MOESM2_ESM.pdf (437 kb)
Supplementary material 2 (PDF 436 kb)

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Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Instituto Pró-Pampa (IPPampa), Laboratório de IctiologiaPelotasBrazil
  2. 2.Programa de Pós Graduação em Biodiversidade Animal, Universidade Federal de Santa Maria (UFSM)Santa MariaBrazil
  3. 3.Universidade Federal do Rio Grande do Sul, Depto. de EcologiaPorto AlegreBrazil

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