Differential responses of anuran assemblages to land use in agroecosystems of central Argentina

Highlights

• We surveyed anurans in 345 agricultural ponds from the Argentinean Pampean Region.

• Ponds conserving aquatic vegetation favored anuran diversity across the entire region.

• Soy crops and cattle raising equally influenced anuran diversity in the Rolling Pampas.

• Burrowing species from the Inland Pampas selected ponds surrounding by soy crops.

• We propose management and conservation actions for achieving agricultural sustainability.

Abstract

Agriculture has been identified as one of the largest contributors to the current global biodiversity crisis. Amphibians are declining worldwide, and the loss of habitat and water contamination related to agricultural land uses have been suggested as the main drivers of this phenomenon. In central Argentina, the Pampean Region combines the highest rates of grassland replacement of South America, the lowest percentage of protected areas of the country, and the lack of studies exploring diversity patterns of native amphibians occurring in agroecosystems. To fill these gaps, we surveyed anuran (frogs and toads) assemblages from 342 breeding ponds located in three ecological units from central Argentina (Rolling, Flooding, and Inland Pampas) during three breeding seasons (2015–2018). We aimed to evaluate the importance of breeding habitat characteristics (ponds) and the surrounding landscape features as drivers of anuran diversity occurring in agricultural landscapes under the primary land uses of the region (cattle grazing and soybean cropping). We tested for the effects of breeding habitat characteristics and landscape features on anuran richness, abundance, and individual species occurrence, using GLMM models and information-theoretic procedures. Results indicated that species richness and total abundances were differently influenced by the habitat and landscape features across the ecological units. Overall, vegetation cover of the ponds and land use were the most important variables influencing richness and anuran abundance. The positive influence of pond vegetation cover on anuran assemblages was registered for all the ecological units, while different patterns emerged when we analyzed the effects of land use surrounding the ponds. Land use expressed as the percentage of soy crop surrounding the ponds negatively affected richness and abundance of anurans of the Flooding Pampas, but the inverse relation was found for assemblages occurring in the Inland Pampas. Moreover, multiple competing models suggested a positive correlation between anuran diversity and land-use heterogeneity, and pond density. The differential responses of anuran assemblages among the ecological units can be related to a combination of several factors encompassing regional soil characteristics (i.e., soil texture), land-use intensity as well as requirements of anuran species. We discussed the particularities of each ecological unit in order to recognize those conservation efforts that will favor anuran diversity in these altered landscapes and further contribute to achieving agricultural sustainability.

Introduction

Occupying 40% of Earth’s land surface, global agriculture feeds over 7 billion people leading to profound global environmental impacts (FAO, 2019). Deforestation, land clearing, habitat fragmentation, and contamination as consequences of agricultural activities are among the major drivers of biodiversity loss (IPBES, 2019). The agricultural expansion and intensification worldwide are expected to undergo further increase, so a more accurate understanding of the effects of land use on biodiversity is, therefore, a critical conservation issue (Newbold et al., 2016).

The Rio de la Plata Grasslands are the main complex of grassland ecosystems in South America and constitute one of the most productive areas in the world (Bilenca and Miñarro, 2004). It includes the Pampas (central Argentina) and the Campos (Uruguay and the southern part of the Rio Grande do Sul State in Brazil) eco-regions. The entire region has been the scene of development, especially during the last century, of a vast livestock industry and a rapid increase in arable agriculture (Soriano, 1991). Notably, the Argentine Pampas has been received the most prominent land-use change related to the conversion of native grassland into agroecosystems, covering about fifty-two million hectares of productive organic soils (Baldi and Paruelo, 2008). This vast flat plain was primarily a livestock-grazing area, but significant land-use changes began between the 1960s and 1970s (Manuel-Navarrete et al., 2009). The most dramatic changes and impacts took place when technological innovation occurred in the 1990s with the introduction of both genetically modified soybeans tolerant to glyphosate in addition to non-tillage systems (Viglizzo et al., 2011).

Amphibians are experiencing population declines in all regions of the world. Nowadays, nearly 41% of amphibian species are threatened with extinction, being the group of vertebrates with more species under threat category in the IUCN Red List (Bishop et al., 2012; IUCN, 2020). The habitat loss associated with agricultural expansion and intensification is likely the single most important human activity affecting amphibian populations (Bishop et al., 2012). On the other hand, many amphibian species have been able to persist in agricultural landscapes around the world (Herzon and Helenius, 2008; Howell et al., 2019; Knutson et al., 2004; Pulsford et al., 2019). Moreover, some species have been found to be positively correlated with high intensity of crop cover and crop diversity (Collins and Fahrig, 2017; Koumaris and Fahrig, 2016), while others have benefited from the new habitats created around agricultural systems, including weirs, irrigation channels and dams (Brand and Snodgrass, 2009). Despite the evidence suggesting that the responses to land-use change could depend on species’ life-history traits, several studies conducted in Europe and the USA identified the vegetation of wetlands and surrounding agricultural land uses as good predictors of anuran diversity (Boissinot et al., 2019; Koumaris and Fahrig, 2016). This growing body of literature also revealed that the amphibian species distribution and abundances might not be accurately predicted using variables describing the quality of a single habitat since amphibians requires a high level of habitat complementation (aquatic and terrestrial habitats) (Boissinot et al., 2019; Hartel et al., 2009). Thus, it is critical to combine multiple spatial scales (from microhabitat to landscapes) and different biological levels (community to species) in order to understand the effects of agricultural disturbance.

In South America, most of the studies that assessed the effects of land use on amphibian assemblages were mainly conducted in Amazonia, Atlantic Forest, and Cerrado Regions (e.g., Ferrante et al., 2017; Ribeiro et al., 2018) while few have explored agricultural impacts in formerly grassland landscapes. Some of them have reported adverse effects of pesticides on tadpoles (Agostini et al., 2020), changes in infection patterns of emerged diseases and abnormalities (Agostini and Burrowes, 2015; Agostini et al., 2013), and high frequency of abnormalities and enzymatic alterations (Brodeur et al., 2011). Other authors have reported detrimental effects at community and population levels in response to crops (Peltzer et al., 2006; Suárez et al., 2016) and differential effects of livestock grazing (Moreira et al., 2015; Verga et al., 2012). Nonetheless, these studies have been conducted at a local level and none of them allow to integrate the results on a more comprehensive scenario to understand how the most important agricultural activities carried out in the South American grasslands are affecting native amphibians.

The anuran diversity of the Pampean Region amounts to 34 species belonging to six families (Frost, 2020). The assemblages are composed of species with varied habitat requirements (terrestrial, burrowing, aquatic, and semi-aquatic habitats and species that climbed as the tree frogs) (Cei, 1980). Although these differences, all species reproduce in temporary and semi-temporary ponds, and their larvae are completely aquatic (Cei, 1980). A few species reproduce during winter, like Boana pulchella and Physalaemus fernandezae (Gallardo, 1974). Nonetheless, all species’ reproductive activity peaks, including those that reproduce in winter, take place in spring and late summer rains (Gallardo, 1974). Especially in sectors with hydric limitations/warm summers and in the absence of hydrographic basins, reproductive choruses become particularly evident after intense rains events (Agostini et al., 2016).

This paper aims to evaluate the importance of breeding habitat characteristics (ponds), and the surrounding landscape features as drivers of anuran diversity occurring in agricultural landscapes under the primary land uses (cattle grazing and soybean cropping) of the Pampean Region. The extension of the Pampean Region is not uniform since differences in historical land-use patterns and the variation of climatic, edaphic, and biogeographic characteristics (Soriano, 1991). Therefore, we first characterized the amphibian assemblages in order to recognize the species composition for three ecological units (Rolling, Flooding, and Inland Pampas). Then, we hypothesize that pond vegetation and land use surrounding the ponds primarily affect anuran species richness and abundance. By contrast, we hypothesize that the contribution of habitat and landscape features to species occurrence varied among taxa. Several authors have reported that the quality of breeding sites is critical for reproduction and larval development (Wells, 2007). The vegetation of the ponds can reflect the quality of water bodies and has been extensively recognized as one of the most critical habitat features supporting amphibian reproduction (e.g., Boissinot et al., 2019; Hartel et al., 2009; Peltzer et al., 2006). Since we conducted the study during the anuran breeding season, we predicted that for all the ecological units, the richness and abundances should be notably favored by the vegetation cover of the ponds. Extensive crops represent the most modified scenario among the productive activities since the original biome is entirely replaced by a monoculture (Viglizzo et al., 2001). Additionally, wetlands occurring adjacent to soy crops are likely to receive high concentrations of pesticides and fertilizers as a result of run-off or spray-drift (Agostini et al., 2020; Carvalho, 2017; Herrera et al., 2013). Therefore, we expect that species richness and total abundance should be negatively related to the percentage of soy crops surrounding the ponds. Simultaneously, human-dominated landscapes with high diversity of patches (crops, pastures, non-grazed grassland, and wetlands) can provide landscape heterogeneity and connectivity (Collins and Fahrig, 2017; Ficetola and De Bernardi, 2004). Then, we predict that land-use heterogeneity and density of ponds should secondarily benefit anuran diversity. Finally, since species conformed anuran assemblages from the Pampean Region differ in life-history traits (Cei, 1980), we expect that habitat and landscape features should differently affect the anuran species. Based on the results obtained, we discuss the conservation outcomes of this work, contributing to agricultural sustainability.