Effects of Pasture-burning Management on Anuran Communities in Subtropical Brazilian Grasslands

doi:10.21203/rs.3.rs-5025564/v1

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Effects of Pasture-burning Management on Anuran Communities in Subtropical Brazilian Grasslands

https://doi.org/10.21203/rs.3.rs-5025564/v1

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Anthropogenic fire is a worldwide event that affects many ecosystems and organisms. In Southern Brazil, grassland management with fire has been highly employed since the mid-18th century. Although the practice is regulated by federal law (prescribed fire), there is no detailed information about the impacts of this practice on the small, non-volant fauna. We evaluated the effect of fire management on anuran species richness and community composition in Brazilian grassland areas that have adopted this practice for more than 15 years. Our results show that burning practices lead to a reduction of anuran richness. About 37% of the species occur exclusively in sites free of fire. Sites with fire management have low densities of taller grass and shrubs, which could reduce habitat availability for some anuran species. Nestedness and turnover components of beta diversity did not differ within and between treatments, but there was a tendency for a nestedness organization of the community in burned sites, suggesting that sites with fire management are a subsample of sites where fire is absent. Our results pointed out that prescribed fire practices have potentially negative effects on the anuran diversity. These results suggest that the changes in vegetation, in particular percentages of shrub cover, affect habitat suitability for some species. As a consequence, anuran communities tend to become less diverse and lack arboreal species where fire occurs.

Amphibians

Beta diversity

Brazil

Fire

Grasslands

Pasture

O fogo antropogênico é um evento mundial que afeta muitos ecossistemas e organismos. No Sul do Brasil, o manejo de pastagens com fogo tem sido muito empregado desde meados do século XVIII. Embora a prática seja regulamentada por lei federal (fogo prescrito), não há informações detalhadas sobre os impactos dessa prática sobre a pequena fauna não-voadora. Nós avaliamos o efeito do manejo do fogo na riqueza de espécies de anuros e na composição da comunidade em áreas campestres brasileiras que adotam essa prática há mais de 15 anos. Nossos resultados mostram que as práticas de queimadas levam à redução da riqueza de anuros. Cerca de 37% das espécies ocorrem exclusivamente em locais livres de fogo. Os locais com manejo do fogo apresentam baixas densidades de gramíneas e arbustos mais altos, o que poderia reduzir a disponibilidade de habitat para algumas espécies de anuros. Os componentes de aninhamento e rotatividade da diversidade beta não diferiram entre os tratamentos, mas houve uma tendência para uma organização aninhada da comunidade em locais queimados, sugerindo que locais com manejo de fogo são uma subamostra de locais onde o fogo está ausente. Nossos resultados apontaram que práticas prescritas de fogo têm efeitos potencialmente negativos sobre a diversidade de anuros. Estes resultados sugerem que as alterações na vegetação, em particular as percentagens de cobertura arbustiva, afetam a adequação do habitat para algumas espécies. Como consequência, as comunidades de anuros onde ocorrem incêndios tendem a se tornar menos diversas e a carecer de espécies arbóreas.

Grasslands play an important role in agriculture and animal production and at the same time serve as habitat for several species. For many centuries, grasslands have been managed for animal production and pasture, resulting in a negative impact on several species (Metera et al. 2010). Vegetation burning, for example, is a worldwide management practice that has been applied to facilitate cattle production in grasslands and savanna-like habitats (Ramos-Neto & Pivello 2000, Boldrini 2009, Fidelis & Pivello 2011, Pillar & Lange 2015). Fire has a great power in shaping the ecosystem structure (Bond & Keeley 2005, Bond et al. 2005), and the effects of natural and anthropogenic fires on native fauna have been extensively studied in the last decades (Masterson et al. 2008). Considering this, habitat management practices, which include vegetation burning, are a powerful trigger to ecosystem modification (Hobbs & Huenneke 1992).

Fire can harm animals directly by increasing mortality through heating or toxin absorption, as well as indirectly through changes in vegetation structure, promoting harsher environmental conditions (e.g., dryer microclimate) and loss of microhabitats for shelter and foraging (Pilliod et al. 2003). This negative effect is more dramatic for less mobile organisms, particularly anurans, as many species have permeable skin and high association with moist habitats (Duellman & Trueb 1994). However, some studies indicate that, in some cases, burning processes can increase species richness (Schurbon & Fauth 2003, Mester et al. 2015, Klaus & Noss 2016) and abundance for some species (Kirkland et al. 1996, Brown et al. 2011, Perry et al. 2012, Hossack et al. 2013). The positive effects of fire on anuran fauna are related to changes in the vegetation structure, which leads to the creation of new microhabitats (Bixby et al. 2015). Consequently, we could argue that, although the fires affect the anurans negatively (Pilliod et al. 2003, Cano & Leynaud 2010, Allingham & Harvey 2013), they could favour some species (Schurbon & Fauth 2003, Mester et al. 2015, Klaus & Noss 2016). However, it is important to consider the species’ adaptation to environments that have historically evolved with the periodic action of burn (Brooks et al. 2004).

The native vegetation cover on the highlands of Southern Brazil has been managed with fire for the last 7400 years (Behling et al. 2004), suggesting anthropogenic fires since the arrival of the first humans, but with greater intensity since the mid-18th century (Boldrini 2009, Fidelis et al. 2010). At present days, these grasslands suffer from prescribed burning for pasture management, which is allowed by Brazilian laws (Pillar & Lange 2015). This may indicate that the biodiversity of this region is not adapted to the presence of fire. Although negative effects of fire on anurans were reported in studies from Neotropical habitats (Papp & Papp 2000, Rocha et al. 2008, Cano & Leynaud 2010), research studies disagree on the positive and negative effects of fire on the whole system (Pillar et al. 2009, Pillar & Vélez-Martin 2010, Luza et al. 2014, Carlucci et al. 2016, Overbeck et al. 2016, 2018). However, most studies evaluating the effects of fire on frogs were carried out in temperate and tropical forests, with few evaluating savanna environments and even fewer evaluating grasslands (Dos Anjos et al. 2021).

Results of manipulative grassland-burning experiments showed that fire induces taxonomic and/or functional changes in assemblages of spiders, edaphic detritivorous invertebrates, grasshoppers, and thrips, but also evidenced strong community resilience due to the rapid (ca. 6 to 12 months) return to unburned-like conditions (Podgaiski et al. 2013, 2014, 2018). Natural experiments, comparing managed and unmanaged (not management by fire) grasslands, evidenced similar richness but distinct taxonomic compositions for ground-dwelling ants (Albuquerque et al. 2017), while small non-flying mammals showed simplified species assemblages under livestock and burning management (Pedó et al. 2010, Luza et al. 2016). However, the effects of fire on amphibians in this region are still uncertain.

As presented above, there is some disagreement on the negative effects of fire on Brazilian grasslands. Regarding anurans, habitat loss generated by the expansion of agriculture and animal production areas is considered a main threat to their conservation in Brazil. The southern Brazilian grasslands encompass about 84 amphibian species, of which 14% are endemic (Santos et al. 2014). Beyond the threats imposed by habitat loss and fragmentation (Garcia & Vinciprova 2003), fire could represent a significant and poorly evaluated impact on amphibian communities in this region. In this study, we performed field samplings in grasslands of Southern Brazilian highlands to evaluate the effects of grassland burning management on anurans assemblages. We hypothesize that (1) species richness will be higher where fire management is absent, (2) the abundance of individuals will be higher in sites without fire management, and (3) sites without fire management will present a larger number of exclusive species.

Study site. — Sampling was performed in the highland grasslands of Southern Brazil. The region is locally called “Campos de Cima da Serra”, which is part of the Atlantic Forest domain. The sample units were distributed in the municipalities of Cambará do Sul and São Francisco de Paula (29°10'35.81" S and 50°10'06.93" O). The habitat is formed by a wide area of grasslands interspersed by a mosaic of forest (Araucaria forest) patches (Pillar & Quadros 1997). Following Köppen, the local climate is subtropical with an average air temperature of 18.5°C. The rainfall is well-distributed through the seasons, with an average annual precipitation of 2,252 mm.

Sampling design. —We selected four sampling sites in areas with regular fire management and four in areas without fire management (totalling eight sampling sites with two treatments). We were unable to apply a random distribution of sampling sites due to the low availability of sites without fire practices. Thus, we adopted a preferential sampling design based on a map of fire spots obtained from time-series satellite images from the last 10 years provided by the Brazilian Spatial Agency (Instituto Nacional de Pesquisas Espaciais). Afterwards, eligible sites for each treatment were checked personally to achieve detailed information about the use of fire by landowners (cattle ranchers): frequency of burning and extension and limits of the burning area. Distances between sampling sites were at least 5 km between treatments and at least 2 km within the same treatment. All sampling sites with fire management shared the following characteristics: presence of similar densities of cattle, fire applied seasonally from July to September, annual burning in the last 15 years, and burning practices based on a traditional method for cattle management. The burning area was at least three times larger than the sampling site and encompassed the whole sampling site plus the surrounding area. All sampling sites without fire management were inside an area of 13,141.05 ha excluded from fire. The sampling sites encompass specific areas of Parque Nacional Aparados da Serra, where cattle are present but grasslands were not burned in at least 15 years. We performed a Mantel test to evaluate the spatial independence of the sampling sites, which revealed them to be spatially independent (p > 0.05).

Assessing anuran diversity. —We recorded anuran species in each sampling site through surveys in natural ponds used as breeding sites. Surveys based on breeding sites are a frequent procedure in studies of amphibians and allow a fast and reliable assessment of local diversity (Heyer et al. 1994, Madalozzo et al. 2017). We monitored one pond in each sampling site, which was selected in a preferential manner based on the presence of a large number of species and the criteria of homogeneity of their configuration as follows: all ponds have a circular design, are less than 1 m deep, and have total area varying from 500 m² to 580 m². It is important to highlight that additional ponds per site were monitored during the initial phase of the sampling. However, only those with the previously described characteristics were used as breeding sites by anurans during the sampling period. Selected ponds were monitored monthly from September to October 2016 (three samplings per pond), which corresponds to the peak of the breeding season of anurans in southern Brazil (Both et al. 2008, Santos et al. 2008). We used two methods to detect anuran species: automated recording systems (Bridges & Dorcas 2000, Hutto & Stutzman 2009) and tadpole sampling with a dip net (Heyer 1994, Vasconcelos & Rossa-Feres 2005, Both et al. 2011). The combination of these techniques is considered one of the most effective methods in amphibian inventories (Hsu et al. 2005, Silva 2010, Madalozzo et al. 2017).

Calling surveys (automated recording systems). —From September to October 2016, we performed three calling surveys per pond. All ponds were sampled simultaneously. To perform calling surveys, we installed one digital audio recorder (Sony ICD-PX312/PX312F) at the margin of each pond, placed 1.5 m above the ground (Figueira et al. 2015). Recording periods went from 6 PM to 6 AM (12 hours of full recording), generating a total of 288 recorded hours (3 surveys × 8 ponds × 12 recorded hours per sampling). Each 12-hour audio record (one night) in a sample unit was considered a sample. We inspected the entire recorded file by extracting 5-minute-long subsamples from each recorded hour. Species were identified based on audio reference guides for calling. Estimations of the abundance of calling males were made using abundance classes (adapted from Bertoluci & Rodrigues 2002): a) 1–4 individuals in calling activity; b) 5–9 individuals; c) 10–20 individuals; or d) > 20 individuals. For statistical analysis, we used the highest level recorded during one night of sampling for each sampling site.

Tadpole sampling. —We performed dip net sampling during the daytime to capture tadpoles. The dip net was moved from the border to the centre of the pond to cover the whole area of the pond (Vasconcelos & Rossa-Feres 2005). Captured tadpoles were immediately euthanized using a benzocaine solution and transferred to the laboratory for identification under a stereomicroscope. Identification was done with the aid of identification keys. Animal capture and handling were authorized by the federal regulatory agency and the committee of ethics in animal use and experimentation (permits #55308-1).

Microhabitat evaluation. —We performed microhabitat measurements using four quadrats of 5×5 m in an area surrounding the breeding site (pond). Each quadrat was placed between 30 and 40 m from the margin of the pond in the four cardinal directions. For each quadrat, we performed visual estimations of: (a) % of shrub vegetation: 1 = none; 2 = 1 to 25%; 3 = 26 to 50%; 4 = 51 to 75%; and 5 = 76 to 100%; and (b) average grass cover (Table 1). We also measured the percentage of the pond area occupied by emergent vegetation according to the following classes: 1 = none; 2 = 1 to 25%; 3 = 26 to 50%; 4 = 51 to 75%; and 5 = 76 to 100% (Table 1). We also measured the mean depth (cm) and the following water chemical-physical parameters: pH, dissolved oxygen (mg/ml), and electric conductivity (ms/cm) (Table 1). Measurements were conducted using a multi-parameter water quality meter (HORIBA) and collected on each sampling day.

Table 1

COORDINATES of sampled plots and microhabitat variables surveyed in the eight sampling units in the subtropical fields of southern Brazil, where PF = Plot with fire, PWF = Plot without fire, AD = Average depth, FV = Categories of percentage of floating vegetation, CSV = Categories of percentage of shrub vegetation, AHG = Average height of grasses, CON = Electrical conductivity of water, BOD = Electrical conductivity of water, % = Values in percentage.
Plot	Latitude	Longitude	AD (cm)	FV %	CSV %	AHG (cm)	pH	COM (ms/cm)	BOD (mg/l)
PF 01	-29.299113	-50.470093	19.4	1	1	17.8	7.37	27.5	17.8
PF 02	-29.288531	-50.469056	27.9	1	1	16.0	8.24	22.0	22.1
PF 03	-29.331199	-50.518006	13.8	2	1	24.7	7.80	24.8	19.9
PF 04	-29.171044	-50.164293	31.3	2	1	11.9	7.80	24.8	19.9
PWF 01	-29.177064	-50.133022	36.0	3	3	39.2	7.95	23.9	20.6
PWF 02	-29.181207	-50.123423	35.1	1	2	52.5	7.85	24.5	20.2
PWF 03	-29.170270	-50.100430	23.1	4	3	28.7	7.87	24.4	20.2
PWF 04	-29.164955	-50.080631	24.8	1	2	15.7	7.89	24.2	20.3

Data analysis. —All analyses were performed using R (R Development Core Team 2017). The normal distribution of records and homogeneity of their variances were evaluated using the Shapiro-Wilk test and the Levene test, respectively. We used a Student T-test (Callegari-Jacques 2003) to compare species richness between sample units with and without fire management. We used a non-parametric multidimensional scaling (NMDS) to evaluate the variation of anuran community composition between treatments based on the Jaccard similarity index. This procedure creates a stress value from the original distance matrix and calculated distances. Stress values close to zero represent a better fit between the original and calculated distance matrices. This is a method that produces object ordinations from any distance matrix (Legendre & Legendre 2012). Afterwards, variables obtained from each sample unit were added to the ordination by the envifit function. We used a Similarity Analysis (ANOSIM) (Clarke 1993) estimated from the Jaccard similarity to evaluate differences in species composition between treatments (with and without fire). The analysis was performed using the “vegan package” (Oksanen et al. 2017). We were unable to apply a completely random sampling site distribution due to the limitation on permits to access non-public lands. Additionally, the only available areas free of fire are limited to a single locality.

We conducted a species indicator analysis in areas with and without fire management following Dufrêne & Legendre (1997). The indicative values (IndVal) generated by this analysis are based on species abundance (specificity) and frequency (fidelity). To evaluate the specificity, we used a matrix of species abundance in each sample unit based exclusively on calling records. We adapted this strategy to avoid bias in the sampling effort of species abundance from different field methods (calling estimation x tadpole capturing). We used minimal values of individuals from each abundance category to be more conservative in abundance estimations. This analysis was performed using the Indval function of the labdsv package (Roberts 2016). Beta diversity (βsor) and its portioning between compounds’ turnover (βsim) and nestedness (βnes) were obtained following Baselga (2010). The turnover component explains the changes in community composition by substitution between pairs of species. Nestedness indicates the loss of species between compared pairs (Baselga 2010). This analysis was performed with R software, using the function “beta.pair” from package “betapart” (Baselga 2010). Components values of turnover and nestedness from the eight sampling sites were pulled into three groups: pairs with fire management (N = 6), pairs without fire management (N = 6), and pairs with fire management - without fire management (N = 16). We adopted this comparison to verify which component has a greater influence on beta diversity.

We recorded 16 anuran species belonging to three families: Bufonidae (1 species), Hylidae (9), and Leptodactylidae (6) (Table 2). Species richness was higher in sites without fire management (N = 15) than in those with fire management (N = 10) (t = -3.549, p = 0.001) (Fig. 1). Six species (Boana faber, B. leptolineata, Dendropsophus microps, D. sanborni, Physalaemus nanus, and Rhinella icterica) were recorded exclusively in sites without fire. Only Leptodactylus gracilis was recorded exclusively in sites with fire management. The remaining species (N = 9) were recorded in both treatments.

Table 2

ANURAN species recorded in sites with and without fire management in subtropical grasslands of southern Brazil, where F = with fire management sample unit, W = without fire management sample unit, A = record of adults; T = record of tadpoles.
Family Species	F1	F2	F3	F4	W1	W2	W3	W4
Bufonidae
Rhinella icterica					A			A/T
Hylidae
Dendropsophus microps					A		A
Dendropsophus minutus	T	A/T		A/T	A/T	A/T	A/T	A/T
Dendropsophus sanborni					A	A	A	A
Boana faber					T			T
Boana leptolineata					A/T	A	A/T	A
Boana pulchella	A/T	A/T	A	A/T	A	T	A
Pseudis cardosoi	A/T	A/T	A/T	A/T	A/T	A/T	A/T	A/T
Scinax granulatus		A		A	A	A	A	A/T
Scinax squalirostris	A	A	A	A/T	A	A	A/T
Leptodactylidae
Leptodactylus gracilis			A
Leptodactylus luctator		A	A/T	A	A	A	A/T
Leptodactylus plaumanni	A	A	A	A	A	A	A	A
Physalaemus carrizorum	T		T	A/T	A	A/T	A	A
Physalaemus nanus					A
Physalemus cuvieri				A		A		A
Species richness (sample unit)	5	7	6	9	14	11	11	10
Total number of species	10				15

The NMDS analysis (Fig. 2) showed differences in species composition between sites with and without fire management (stress = 0.02), which was reinforced by the analysis of similarity (ANOSIM; R = 0.59, p = 0.03). The envifit function also showed that the variation in species composition was related to the fire (R² = 0.59, p = 0.026). In addition, ANOSIM showed an influence of shrub vegetation (SV) on the anuran species composition (R² = 0.68, p = 0.038). Sites without fire showed higher percentages of shrub vegetation, and this was associated with the presence of Physalaemus nanus and Dendropsophus microps. This positive relationship between the absence of fire and anurans was greater in sites with higher shrub density (sample units W1 and W3). This result indicates that sites with fire present changes in both the percentage of shrub vegetation (SV) and anuran community composition. The remaining variables of microhabitat did not show significant variation between treatments (average depth: R² = 0.58; p = 0.111; flooding vegetation categories: R² = 0.15, p = 0.67; average grass height: R² = 0.18, p = 0.591; pH: R² = 0.21, p = 0.544; electric conductivity: R² = 0.20, p = 0.553; biological oxygen demand: R² = 0.20, p = 0.547).

Pseudis cardosoi, Scinax squalirostris, Leptodactylus plaumanni, and Dendropsophus minutus reached the highest abundance category (> 20 individuals) in at least one sample unit of each treatment. For these species, fire management does not seem to affect their abundance (Table 3).

Table 3

ABUNDANCE categories of species calling in sample units located in areas with and without fire management in subtropical grasslands in southern Brazil, where F = with fire management sample unit, W = without fire management sample unit. Mean number of individuals calling:
Species	F1	F2	F 3	F4	W1	W2	W3	W4
Dendropsophus microps
Dendropsophus minutus
Dendropsophus sanborni
Boana leptolineata
Boana pulchella
Leptodactylus gracilis
Leptodactylus luctator
Leptodactylus plaumanni
Physalaemus carrizorum
Physalaemus nanus
Physalemus cuvieri
Pseudis cardosoi
Rhinella icterica
Scinax granulatus
Scinax squalirostris
Number of calling species	4	7	5	9	13	10	11	7

1–4	5–9	10–20	> 20
Figures legends

The IndVal analysis indicated Boana leptolineata as an indicator species of sites without fire management (IndVal = 1, p = 0.028). This species was recorded exclusively in sites without burning activities. In addition, B. leptolineata was recorded in all four sample units (high fidelity level), being one of the most abundant species in these sites

Differences in beta diversity (βsor) components, turnover (βsim) and nestedness (βnes), were not statistically significant between sampling sites. There was no difference between the role of nestedness or turnover as drivers to species change either between sites within the same treatment (with fire: t = − 0.4707, p = 0.328; without fire: t = − 0.9354, p = 0.196) or between treatments (with × without fire: w = 97, p = 0.133). However, beta diversity values suggest different patterns in results from comparison within and between treatments. Mean turnover values within treatments were higher (βsim = 0.126–56.92%) than those of nestedness (βnes = 0.103–63.39%) (Fig. 3). On the other hand, nestedness between treatments showed higher mean values (βnes = 0.202–63.09%) than turnover (βsim = 0.118–36.9%), suggesting that anuran communities in sites with fire management are mostly subsets of the communities found in sites without fire.

Our data indicate that fire management favours the reduction of species diversity in grassland habitats of southern Brazil. A similar scenario was also observed in the Argentinean Chaco (Cano & Leynaud 2010). Changes in species composition generated by anthropogenic fire were also recorded in North America (Wilgers & Horne 2006) and South Africa (Masterson et al. 2008). In Brazil, Rocha et al. (2008) observed that frogs from burned sites had fewer prey items per stomach than those from unburned sites, which suggests that fire has negatively affected the species studied. In contrast, De Oliveira Drummond et al. (2018) observed an increase in anuran species richness after a fire event, which demonstrates the need for more studies in this line of research to better understand the effects of fire on Neotropical anurans. However, it is worth highlighting that the study of De Oliveira Drummond et al. (2018) was carried out in a transition zone between the Atlantic Forest and the Cerrado, a region that is affected by natural fires. Therefore, frogs from this region may be more adapted to fire than frogs from southern Brazil.

The negative effects of fire on amphibian diversity have been reported in many ecosystems (Papp & Papp 2000, Rocha et al. 2008, Cano & Leynaud 2010). Such effects include death by overheating and intoxications due to fire-emanating gases (Pilliod et al. 2003, Frizzo et al. 2011, Smith et al. 2012), as well as changes in habitat configuration and a decrease in prey availability (Pilliod et al. 2003, Rocha et al. 2008, Frizzo et al. 2011, Allinghan & Harvey 2013). At the same time, negative impacts vary according to the ecological traits of species, driving differences in their responses to fire (Morais et al. 2011). Some species occurred only in sites without fire, such as Rhinella icterica, Dendropsophus microps, D. sanborni, Boana faber, B. leptolineata, and Physalaemus nanus. Evidence about the ability of fire to change species compositions is shared by other studies (Pilliod et al. 2003, Matthews et al. 2010, Rochester et al. 2010).

At the same time, Pseudis cardosoi, Scinax squalirostris, Leptodactylus plaumanni, and Dendropsophus minutus reached the highest abundance category (4 = > 20 individuals) in at least one sample unit of each treatment. Some studies found that low-intensity fire does not cause a great impact on anuran assemblages (Lemckert et al. 2004, Morais et al. 2011). Some of them argue that some species are even favoured by fire regimes (Kirkland et al. 1996, Schurbon & Fauth 2003, Mester et al. 2015, Klaus & Noss 2016). Many studies highlighted the effects of fire on the vegetation cover (Schurbon & Fauth 2003, Cano & Leynaud 2010, Allinghan & Harvey 2013). Apparently, arboreal anurans are more affected by these modifications in vegetation (Friend 1993, Papp & Papp 2000). Our results reinforce this hypothesis since most arboreal species occurred exclusively in sites without fire (Dendropsophus microps, D. sanborni, Boana faber, B. leptolineata). Although not all species exclusive to these sites were arboreal (e.g., Rhinella icterica), we believe that fire generates a loss of microhabitats, including shelter from predators and extreme climatic conditions. Another non-arboreal species exclusive to non-burned sites is Physalaemus nanus, a terrestrial and forest-associated species (Kwet et al. 2010). We believe that its presence on sites without fire is related to the existence of a denser vegetation cover. The vegetation structure is one of the most representative components of the habitat related to the organization of amphibian communities (Allinghan & Harvey 2013). The presence of Dendropsophus microps, D. sanborni, and Physalaemus nanus, which were positively affected by the availability of shrubs, suggests that fire has an indirect effect on anurans by modifying the vegetation structure. We observed that shrub vegetation and tall grass are present only in sites without fire. Many studies reported a direct relationship between vegetation height and species richness in anuran assemblages (Silva et al. 2012, Allinghan & Harvey 2013). Taller vegetation would offer more opportunities for protection and breeding activities (e.g., calling sites, oviposition sites) (Hazell et al. 2001, Bertoluci & Rodrigues 2002, Conte & Machado 2005). Especially in grassland habitats, vegetation height is a crucial mechanism in determining microclimatic conditions. The reduction of vegetative biomass leads to rapid changes in daytime temperature, humidity, and insolation levels, characterizing a harsh habitat (Pilliod et al. 2003).

At the same time, the small leptodactylid Leptodactylus gracilis was exclusive to sites with fire. This species uses natural burrows or ground depressions for shelter and calling sites (Kwet et al. 2010, Maneyro et al. 2017). This could guarantee a higher probability of escaping from fire (see Raison et al. 1986). The species indicator analysis (IndVal) indicated Boana leptolineata as indicative of sites without fire. This species has affinities with floating vegetation and marginal vegetation of temporary and permanent ponds, which are used as calling sites (Reinke & Deiques 2010, Maneyro et al. 2017). The low availability of this kind of microhabitat could be a limiting factor to the persistence of this species in frequently burned sites.

The beta diversity components revealed no difference between treatments. However, it was possible to observe a trend for a nested organization of the community in burned sites, suggesting that sites with fire are a subsample of sites where fire is absent. In a study carried out in the same region, but in forest fragments within a grassland matrix, a pattern of species turnover (i.e., exchange) was observed (Oliveira 2018). These results may be related to the origin of the studied environment, which is characterized by forest expansion over the grassland matrix (Behling et al. 2004). We must reinforce that the negative effects of fire on anurans could be a complex issue. More than death by burning, fire causes habitat changes that can harm anurans. For example, in the same area as our study, Schuck et al. (2024) observed that fire was associated with changes in the bacteria that inhabit the skin of frogs, in addition to an increase in pathogen loads.

This study sheds some light on the impacts of fires on such sensitive animals. Our results are worrying since the effects of fire on anurans are poorly studied in comparison with other vertebrates (Pastro et al. 2014) and need to be investigated in many more species and habitats. Sites without the presence of fire developed taller vegetation and a higher density of shrubs, which could be viewed as an improvement in habitat complexity. Therefore, we hypothesize that this increase in complexity generates an increase in microhabitat opportunities, favouring a higher species richness in comparison with constantly burned sites. This is the first study evaluating the effects of fire management on anurans in Brazilian subtropical grasslands. Thus, we suggest that fire management should not only consider the impacts on the fauna but also allow the maintenance of tall grass and shrubs around ponds.

Acknowledgements:

We are grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a Master’s scholarship. We also thank Instituto Chico Mendes de Conservação da Biodiversidade for allowing activities with scientific purposes, including in areas of federal conservation units (license no. 55308-1).

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The authors declare no competing interests.

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Effects of Pasture-burning Management on Anuran Communities in Subtropical Brazilian Grasslands

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