Grassland ecosystems are among the most threatened at global scale due to the great disparity between habitat loss and the low percentage of protected area (Hoekstra et al., 2005). Such ecosystems are submitted to strong anthropic pressure owing mainly to changes in land-use caused by monocultures (Azpiroz et al., 2012; Develey et al., 2008). In Brazil, grasslands of Pampa biome have a high degree of degradation, in the state of Rio Grande do Sul more than 50% of native grasslands has been converted mainly for agriculture and forest plantations (Bencke, 2009; Fontana et al., 2016).

Afforestation and agriculture with nonnative species have expanded over grazed native grasslands in extensive areas of Pampa biome (Azpiroz et al., 2012). The traditional cattle production is a compatible activity with conservation biodiversity if adequately managed (Develey et al., 2008; Isacch and Cardoni, 2011). The moderate grazing does not cause the suppression of native vegetation, maintaining the main characteristics of grassland ecosystems (Overbeck et al., 2007). On the other hand, tree monocultures totally replace the native local vegetation structure, affecting distribution of bird populations by reducing availability of resources that are important for nesting and feeding (Codesido et al., 2008). Tree plantations are known to alter the structure of bird communities in forest ecosystems, benefiting generalist and edge bird species (Jacoboski et al., 2016). However, in grassland landscapes, tree plantations can have more detrimental effects in birds than in forest ecosystems (Filloy et al., 2010).

The legal protection can effectively avoid conversion of native grasslands into other uses, and thus prevent complete loss of grassland biodiversity (Overbeck et al., 2007). Legal protection measures proposed by the Brazilian Forest Code determine the areas that must be preserved and which regions are allowed for cultivation, law n° 12.651/12 (CFB, 2012). Between the vegetation to be protected, is the marginal vegetation surrounding aquatic ecosystems. This vegetation, denominated Permanent Preservation Area (PPA), must be maintained by the delimitation of a buffer zone for both margins, which varies according to the width of a water course. A PPA consists of a protected area, covered or not by native vegetation, with the environmental function of preserving water resources, landscape, geological stability, and biodiversity, as well as of facilitating genetic flow of fauna and flora and protecting the soil. In tree plantations, the regulation of law is performed, however, in cattle ranching farms or soybean, such regulation is often not maintained, and when maintained, the tendency is to consider forest vegetation more than non-forest vegetation, even in grassland biomes (Develey et al., 2008; Overbeck et al., 2015).

Our goal was to investigate whether protected native grasslands (PPAs within Eucalyptus plantation stands) are viable to grassland birds. Furthermore, we aimed to identify whether these species are different from those recorded in non-protected areas (grazed native grasslands). Toward this aim we compared richness, abundance and composition of bird species between PPAs and grazed native grasslands. We hypothesized that (1) PPAs are viable for grassland species use because Eucalyptus stands are located in a matrix of grassland vegetation and possess connections among native grassland areas; (2) species composition should differ between protected and non-protected grasslands areas due to their differences in vegetation structure caused by grazing.

We recorded 36 grassland bird species (Table 1), 24 in the PPAs and 27 in the grazed native grasslands. Most of the recorded species uses both tall and short grasslands. However, only 15 species were shared between areas. The most abundant species were Zonotrichia capensis (n=44) and Ammodramus humeralis (n=49), in the PPAs and in the grazed native grassland, respectively. In relation to sample units, the Mantel test indicated that count points were independent as there was no significant spatial correlation (r=0.02, p=0.15). Both species richness and abundance did not present significant differences between sampled areas (F1,14=1.91, p=0.21 and F1,14=6.61, p=0.07, respectively). On the other hand, species composition differed significantly between areas (F1,14=2.85, p=0.001). A clear segregation of species was observed between PPAs and grazed native grassland in the CCA (Fig. 2).

Fig. 2.

Ordination diagram generated by the Canonical Correspondence Analysis (CCA) of bird species composition in relation to vegetation structure. Dark circles represent areas of grazed native grasslands; empty circles represent Permanent Preservation Areas (PPAs). Arrows represent mean plant height and mean plant density, respectively. Species names acronyms in Table 1.

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The CCA showed an association between birds species composition and vegetation structure. For example, typical tall grass species are associated with PPAs, while grazing selects species are less dependent on tall grasslands.

However, the CCA model was not significant when we tested it with an ANOVA including the two vegetation variables. Both variables were significant when we analyzed them separately: height (F1,14=1.84, p=0.002) and density (F1,14=1.7, p=0.02). Thus, mean plant height explained 12% of the variation in species composition and mean plant density explained 11%. Also, we detected significant differences in plant height and density when we tested PPAs versus grazed native grassland sites with an ANOVA (F1,14=68, p=0.001 and F1,14=40, p=0.001), respectively (Fig. 3).

Fig. 3.

Boxplots of mean plant height (A) and mean plant density in each one of the sampling sites (B), showing differences among sampled sites, with their maximum and minimum values and standard error. Different letters indicate significant differences between treatments.

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Four of the species recorded are threatened in regional or global categories (Sporophila pileata, Sporophila cinnamomea, Culicivora caudacuta, Xanthopsar flavus) and one as regionally near threatened species (Cistothorus platensis). The three first species were exclusively observed in the PPAs, whereas X. flavus was only found in the grazed native grasslands. C. platensis was recorded in both areas.

Our results demonstrate a turnover of species between areas, bird species recorded in the PPAs that depend on tall grass and preserved vegetation (e.g. Sporophila sp.) were replaced by species associated with short grass and (besides) by species that are less dependent on the height of the vegetation in the grazed native grasslands (e.g. Anthus sp.). These results demonstrate that presence of PPAs and grazed native grasslands with moderate levels of grazing are essential for the conservation of grassland birds, because two groups of species are benefited, short and tall grass dependent. Grassland birds differ in their sensitivity to disturbance of grasslands by grazing (Azpiroz et al., 2012). Areas with lower or no grazing are necessary to ensure viable populations of specialized tall grass species (Isacch and Cardoni, 2011). On the other hand, in grazed grasslands, a short grass assemblage of birds is benefited (Azpiroz et al., 2012).

Specific variations in habitat characteristics, such as the difference in recorded plant height and density, demonstrated to determine differences in bird species composition in the study areas. In the studies developed by Fisher and Davis (2010) and Dias et al. (2014), the authors indicated that plant height was the main factor associated with diversity and composition of bird species in grasslands. This difference in vegetation demonstrates the importance of grassland mosaics with plants of different heights for bird diversity. Many grassland birds require a mosaic with different habitat patches to fulfill their reproductive requirements (Dias et al., 2014). Currently, these mosaics are generated by patches with different grazing intensity, thereby contributing to the conservation of a great part of bird diversity (Isacch and Cardoni, 2011). On the other hand, Vickery et al. (1999) recommend that some areas should not be managed, for obtaining the maximum diversity of grassland birds. They also recognize that specific management practices can satisfy the specific requirements of a subset of species, but cannot benefit the others. Thus, this habitat heterogeneity is necessary to ensure species coexistence and maintaining the diversity of grassland bird communities (Codesido et al., 2013; Dias et al., 2014; Hovick et al., 2015).

The register of threatened X. flavus in grazed native grasslands demonstrated the importance of adequate management in private farms for maintain grassland-associated birds (Develey et al., 2008; Fontana et al., 2016). Furthermore, three threatened bird species found in our study were exclusive to the PPAs. These species are typical of tall and well preserved grasslands, in addition to being sensitive to any sort of disturbance (Bencke, 2009). The presence of threatened species in PPAs is satisfactory from the conservation point of view. However, we do not know whether these populations will remain viable in the long run, since indirect effects of afforestation in adjacent areas are still scarcely known. Indirect effects of neighboring tree plantations can affect the physical and biotic characteristics of adjacent areas, such as facilitation of shrub encroachment and increase of nest predation rates (Azpiroz et al., 2012; Reino et al., 2010).

Our results demonstrate the importance of maintaining protected and non-protected grasslands for conservation of grassland bird species. However, it is fundamental to investigate whether populations in the PPAs remain stable or these areas are only a temporary refuge in the face of imminent extinction. Furthermore, the maintenance of grassland PPAs and managed grasslands in a sustainable way might favor a high diversity of bird species in the study region, and help to avoid the processes that lead to extinction of strictly grassland species. Our results also highlighted the necessity of maintaining PPAs, especially in agricultural and grazing areas. Although PPAs in grasslands are protected by law, they are often neglected. For example, in sampled grazed native grasslands, grassy vegetation along the water courses is not protected, and thus cattle have free access to these areas. Therefore, the maintenance of grasslands PPAs by the landowners might be a useful tool to increase protection of the grasslands vegetation in private land, since landowners can act as important agents for the conservation of birds in the grasslands of south Brazil.

This work was supported by CMPC Celulose Riograndense.

The authors declare no conflicts of interest.