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Revista Brasileira de Ornitologia 27(3): 199–206. ARTICLE September 2019 A comparison of bird communities in natural and revegetated grasslands in south Brazil 1,4 2 3 Rafael Gustavo Becker , Gabriela Paise & Marco Aurélio Pizo Programa de Pós-graduação em Diversidade e Manejo da Vida Silvestre, Universidade do Vale do Rio dos Sinos (UNISINOS), São Leopoldo, RS, Brazil. Laboratório de Ecologia de Mamíferos, Departamento de Ciências Biológicas, Universidade Regional do Cariri (URCA), Crato, CE, Brazil. Departamento de Zoologia, Universidade Estadual Paulista (UNESP), Rio Claro, SP, Brazil. Corresponding author: email@example.com Received on 15 October 2018. Accepted on 13 September 2019. ABSTRACT: Natural grasslands are declining due to loss, fragmentation and degradation, resulting in the decline of grassland- associated bird species. The Pampas Biome in south Brazil is not ex ception to this worldwide trend, facing the expansion of croplands and afforestation with exotic tree plantations for cellulose production. To cope with the continuous degradation and loss of grasslands, restoration is an important conservation strategy, but basic information regarding the response of the fauna to restoration practices in southeastern South America grasslands is lacking. Here we compared the structure of bird communities in natural grasslands and revegetated grasslands after mining by planting native and exotic grasses. We sampled birds using 5-min point counts with unlimited radius in three replicates of each habitat (natural and revegetated grasslands; average size 22.2 ± 2.3 ha). We also compared the vegetation density between the two habitat types. The structure of bir d communities at natural and revegetated grasslands differed, with natural grasslands presenting higher species richness (42 vs. 35 species) and abundance (1459 vs. 839 records) than revegetated areas, and also a distinct species composition. Ten of the 11 grassland species that were associated to one of the two habitat types occurred more frequently in natural grasslands, which had higher vegetation density than revegetated areas. Even a decade after the beginning of the restoration process, revegetated areas did not resemble natural grasslands in bird species richness, abundance, and composition. These results differed from another study conducted in the Brazilian Pampas in which native plant species were used to actively restore a grassland. Therefore, until we have additional studies addressing the use of exotic grasses for the recovery of bird communities in South America grasslands, we encourage greater representation of native plant species in restoration projects. KEY-WORDS: exotic grasses, habitat restoration, mining, Pampas Biome. INTRODUCTION issues for proper grassland restoration (e.g., availability of seeds of native grassland species), basic information Recently we saw an upsurge of calls for grassland regarding the response of the fauna to restoration conservation in face of the many threats to grasslands, practices is lacking. Some pending questions about the including afforestation and invasion b y exotic plants (Parr conservation value of restored grasslands are, for example, et al. 2014, Bond 2016). In the Pampas Biome of southern threatened animals. Birds, for instance, can be divided Brazil, for instance, approximately 60% (104,553 km ) of into different categories of dependence on grasslands, former grassland area had been destroyed by 2002, mostly with grassland-restricted species in general among the due to its conversion to arable fields or afforestation most threatened species (Azpiroz & Blake 2009, Azpiroz with exotic trees (Andrade et al. 2015). This makes the et al. 2012): Do such bird species use grasslands restored Pampas the second Brazilian biome regarding the relative by planting mostly exotic grasses? In North America we magnitude of land use changes, getting behind only to know that grasslands planted mostly with non-native the Atlantic Forest (Overbeck et al. 2013). grasses on reclaimed mines supported a community of To confront the continuous degradation and loss bird species typical of natural grasslands (Scott et al. of grasslands, or any other vegetation type, ecological 2002). restoration is an important strategy. However, research Here we compared the structure of bird communities and practice of restoration of tropical grassy biomes has in natural grasslands and grasslands revegetated after traditionally fallen behind other vegetation types, such as mining with the planting of native and exotic species. forests (Overbeck et al. 2013). In addition to technical More specifically, we investigated how the species richness, Bird communities in natural and revegetated grasslands Becker et al. abundance and composition of the bird communities at Fertilizers such as triple superphosphate (NPK) and revegetated areas with such a mixture of native and exotic potassium chloride were added, a mix of mostly exotic (Lolium multiflorum, Urochloa decumbens, Chloris gayana, species (but with a predominance of the latter) compare to natural grasslands. Our ultimate goal is to evaluate the Cynodon dactylon, Trifolium repens) and one native grass efficacy of the restoration procedures currently used by species (Paspalum notatum), were sowed, and again the mining companies from the bird's point of view. Such fertilizer (NPK) and urea were added. Natural grasslands companies follow the Brazilian legislation that permits were not actively managed, but were under fire and ungulate grazing , common and part of the evolutionary the use of exotic plant species in restoration (for more details see Normative Instruction ICMBio 2014). history of natural Pampas grasslands (Pillar & Velez 2010). Areas with revegetated and natural grasslands had similar sizes, ranging from 20 to 25 ha. METHODS Bird and vegetation sampling Study areas We sampled birds from May to December 2006 using This study was carried out in areas of Companhia 5-min unlimited point counts (Bibby et al. 1992) carried Riograndense de Mineração (CRM), at Candiota region in out from early to mid-morning (06:30–10:00 h) and late afternoon (16:00–17:30 h) in three replicates of two the state of Rio Grande do Sul, south Brazil (31 33'S; 53 40'W). This region is largely occupied by open- habitat types (natural and revegetated grasslands). Only pit coal mining areas, revegetated areas, and natural birds seen or heard inside the sampled areas of natural grasslands (Fig. 1). According to the Köppen (1948) and revegetated grasslands were considered. The average classification, the climate in the area is Cfa, with cold distance between sampling areas was c. 1.5 km. In each area we sampled eight points distant 200 m from each winter, hot summer, and rainfall distributed over the year but more pronounced between July and October. The other in each season of the year, totaling 32 points per average relative humidity is 73% in summer and 83% in area and 96 per habitat. The locations of sampling points winter. Average annual rainfall is around 1400 mm. were not fixed but randomized at each season using xy From 9 to 13 years before this study, active coordinates (maintaining, however, the 200 m minimum distance between points). The scientific nomenclature restoration techniques were performed by CRM in which soil from areas that would be mined later was deposited on and taxonomic ordering of birds follow Piacentini et al. mined areas after the reconfiguration of the topography. (2015). Figure 1. Map of the study site showing the location of the natural and revegetated grassland areas in southern Brazil. Revista Brasileira de Ornitologia 27(3): 2019 Bird communities in natural and revegetated grasslands Becker et al. At each sampling area we set two parallel transects randomizations) based on the actual distribution of the of 150 m length each and separated 150 m from each observed data, the species composition is different. The other to assess the vertical structure of the vegetation. At change-corrected within-group agreement (A) provides each 5 m interval we counted the number of times the and effect size of the dissimilarity between groups, vegetation touched a 2-m graded rod (maximum height ranging from < 0 to 1. The smaller is A the greater the of vegetation) in four height classes (0–50, 51–100, 101– heterogeneity between groups, while if A = 1 groups are 150, and 151–200 cm). A quantification of the vertical identical. We tested for correlations in the spatial distance structure was then given by the density of vegetation at (Euclidean distance) and similarity in species composition different height classes. (Bray-Curtis distance) between the studied areas using a Mantel test (Quinn & Keough 2002). We performed all Data analyses these analyses with the “vegan” package in R software (Oksanen et al. 2011, R Core Team 2017). Bird species richness was compared between natural and To test for differences in vegetation density between revegetated grasslands in two ways. Firstly, we did an natural and revegetated grasslands, we used a resampling analysis of rarefaction based on individuals (i.e., number technique performed with the Resampling Stats program of records) implemented with EstimateS version 9.1 (Simon 1997, Blank et al. 2001) in which the mean (Colwell 2013). This is a non-biased way of comparing between-habitat difference for each vegetation height the richness of species between areas, as it is not influenced class was compared with the mean differences obtained by variations in the density of individuals among areas from 10,000 randomizations of the data, accepting as (Colwell & Coddington 1994, Krebs 1999, Gotelli significant observed differences that lied within the 5% & Colwell 2001). In addition, due to possible spatial frequency distribution of the randomized differences. dependence among samples, we compared bird species richness and number of records through a hierarchical RESULTS mixed model test (nested ANOVA) using the function “lme” of the package “nlme” in R software (Oksanen et al. 2011, McDonald 2014). Sampling points were treated We made 2298 records (1459 in natural, and 839 in as random variables within each fixed treatment (Natural revegetated grasslands) of 49 bird species (21 families, vs. Revegetated). 42 species in natural, and 35 in revegetated grasslands; Following Azpiroz et al. (2012), we classified bird Appendix I). The cumulative number of bir d species species according to their association to grasslands in stabilized in both habitats, indicating that we sampled southeastern South America in the following categories: most of the species in the studied areas (Fig. 2). Rarefying (1) grassland-restricted species, i.e., species that do not down the number of records to 800 in both habitats, we use alternative habitats, (2) species that extensively use got 40 species in natural and 35 species in revegetated grassland habitats, but other habitats as well, and (3) grasslands, with non-overlapping confidence intervals species that make extensive use of grassland habitats only indicating different species richness (Fig. 2). in certain subregions of the southeast South American Most species (28 species) were not associated grasslands. with grasslands, while 13 species make extensive use We calculated the species diversity for each habitat of grasslands (category 2 of Azpiroz et al. 2012), and 8 type using the Shannon-Wienner index (log [x]) (Magurran species use grasslands only in certain regions (category 3). 1988). To test if bird species used more frequently any of the two habitats, we performed G tests for the species with 10 or more records. These tests contrasted t he frequencies of records at natural and revegetated grasslands with the expected frequencies based on equal number of records at each habitat. We performed group analysis to test for possible differences in the composition of bird communities between natural and revegetated grasslands using the Multi-Response Permutation Procedures (MRPP) method with Euclidean distances (Zimmerman et al. 1985). This method makes it possible to evaluate the dissimilarity between groups of samples. If the mean Figure 2. Rarefaction curve based on the number of bird records dissimilarities of the species composition observed is less and their respective confidence intervals (95%) in natural and than the dissimilarity between randomized groups (999 revegetated grasslands in southern Brazil. Revista Brasileira de Ornitologia 27(3): 2019 Bird communities in natural and revegetated grasslands Becker et al. No grassland-restricted species (category 1) was recorded general, and grassland-associated species in particular, in (Appendix 1). The representativeness of each category of natural grasslands compared to “improved” grasslands, grassland association did not differ between habitats (G i.e., natural grasslands managed with the addition test: = 1.080, df = 2, P = 0.580). Among the 30 species of fertilizers and exotic species, demonstrating the with 10 or more records, 14 used natural grasslands more importance of natural areas for grassland birds (see also frequently than expected by chance, and only Colaptes Silva et al. 2015). campestris was associated with revegetated grasslands Together with the lower density of vegetation (Appendix I). Considering only grassland-associated birds in revegetated areas, the low number of plant species (categories 2 and 3), 11 out of 14 species were associated sowed, most of them exotics, in the restoration process to a habitat type, once again all but C. campestris used is an additional factor that possibly contributed to the more frequently natural grasslands (Appendix I). lower diversity of birds in revegetated grasslands. In The species with t he highest number of records in comparison, natural grasslands are composed by a much both habitats were Zonotrichia capensis, Sicalis luteola, diverse plant community (Menezes et al. 2018), which Ammodramus humeralis, and Embernagra platensis, naturally promotes spatial heterogeneity. In the sole together accounting for 51% of the total number of comparable study on the recovery of a bird community records (Appendix I). Natural grasslands had greater in actively restored grassland in southeastern South diversity than revegetated areas (H' = 2.986 and 2.625, America, Silva (2019) found different composition, but respectively), a difference mirrored by the species richness similar bird species richness and abundance between (F = 6.240, P < 0.050), and bird abundance (F = 19.508, a 3-yr old grassland restored with native plants and a P < 0.001; Fig. 3). Natural and revegetated grasslands natural grassland area. Limited as the comparison with also differed in species composition (MRPP: observed delta = 10.45, expected delta = 10.54, A = 0.007, P = 0.019). There was no correlation between the distance separating the studied areas and the pairwise dissimilarity in species composition (Mantel r = 0. 198, P = 0.374, 719 permutations), indicating that species composition was not related to spatial relationships among areas. Natural grasslands areas had higher vegetation densities at height classes 0–50 cm (mean difference = 6.28, P = 0.040), 51–100 cm (3.43, P = 0.001), and 101– 150 cm (4.35, P = 0.001), but not at 151–200 cm (1.41, Figure 3. Boxplots showing the median (horizontal line), 25% P = 0.150) in which a few plants were recorded at both – 75% quartiles (box upper and lower limits), and maximum habitats (Fig. 4). and minimum values (indicated by the vertical bars) of the species richness and number of birds recorded at natural and revegetated grasslands in southern Brazil. DISCUSSION The struc ture of bird communities at natural and revegetated grassland areas differed, with natural grasslands presenting higher species richness and abundance than revegetated areas, and also a distinct species composition. In addition, most of the grassland- associated birds occurred more frequently at natural grasslands. Differences in vegetation structure between natural and revegetated grasslands is a factor to explain such differences, since the composition of bird communities in southern Brazilian grasslands (and grasslands in other regions; Hovick et al. 2015) is strongly influenced by the spatial heterogeneity of vegetation, that is, by structural changes in vegetation mostly caused in Figure 4. Vegetation density at different height classes in the region by disturbances like fire and grazing (Ben cke natural and revegetated grasslands as denoted by the number 2009, Dias et al. 2014). The high sensitivity of birds to of touches of the vegetation in a 2 m graded rod. Bars indicate vegetation structure was also observed by Fontana et al. standard errors. Between-habitat differences are indicated by (2016) who found greater species richness of birds in *(P < 0.050) and **(P < 0.010). Revista Brasileira de Ornitologia 27(3): 2019 Bird communities in natural and revegetated grasslands Becker et al. this single study might be, we expected similar results for restoration projects, stimulating policies to overcome the our much older (9–13 years) revegetated areas. That our technical difficulties of making available seeds of native revegetated areas had smaller bird species richness and species for restoration purposes. abundance than natural grassland areas is indicative that the predominance of exotic grasses in the seed mixtures used in the restoration process is inadequate for the ACKNOWLEDGEMENTS recovery of grassland bird communities. Nonetheless, the species richness we recorded in natural grasslands (42 We thank the Brazilian Agricultural Research Corporation species) is within the range found by Silva (2019, 30– (EMBRAPA) for financial and logistic support, Cristiano 46 species), while the richness in our restored sites (35 Alves da Silva for preparing the map of the study area, species) did not greatly differ from her active restoration and two anonymous reviewers whose comments greatly (30 species). improved the paper. 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Use of an Nabinger C., Pilger G.E., Trindade J.P.P., Vélez-Martin E., Walker improved statistical method for group comparisons to study E.A., Zimmermann D.G. & Pillar V.D. 2013. Restoration ecology effects of prairie fire. Eco logy 66: 606–611. in Brazil: time to step out of the forest. Natureza & Conservação 11: 92–95. Associate Editor: Carla S. Fontana. APPENDIX I Bird species recorded in natural grasslands and grasslands revegetated after mining in south Brazil. Number of records Family Grassland P value Species specialization Natural Revegetated Tinamidae Rhynchotus rufescens 269 25 0.009 Nothura maculosa 2 66 31 0.010 Anatidae Amazonetta brasiliensis -0 2 Accipitridae Elanus leucurus 310 Rupornis magnirostris -0 1 Charadriidae Vanellus chilensis 2 2 11 0.055 Columbidae Columbina picui -8 3 Leptotila verreauxi -0 1 Revista Brasileira de Ornitologia 27(3): 2019 Bird communities in natural and revegetated grasslands Becker et al. Number of records Family Grassland P value Species specialization Natural Revegetated Cuculidae Tapera naevia -8 8 Guira guira -8 4 Picidae Colaptes campestris 3 7 40 0.002 Veniliornis spilogaster -1 0 Cariamidae Cariama cristata 206 Thamnophilidae Thamnophilus caerulescens - 60 Thamnophilus ruficapillus - 27 12 0.080 Furnariidae Synallaxis cinerascens - 6 7 0.84 Synallaxis spixi - 13 4 0.08 Furnarius rufus 3 21 6 0.03 Anumbius annumbi 3 19 0 <0.001 Phacellodomus striaticollis 3 72 1 <0.001 Tyrannidae Camptostoma obsoletum -11 11 Serpophaga subcristata - 18 20 0.73 Pitangus sulphuratus - 14 25 0.20 Xolmis cinereus 260 Tyrannus savana 35 2 Vireonidae Cyclarhis gujanensis -3 0 Hirundinidae Pygochelidon cyanoleuca -4 0 Troglodytidae Troglodytes musculus - 13 27 0.11 Turdidae Turdus rufiventris - 8 5 0.55 Turdus amaurochalinus -1 0 Motacillidae Anthus lutescens 20 7 Passerellidae Zonotrichia capensis - 224 164 0.03 Ammodramus humeralis 2 135 122 0.55 Parulidae Geothlypis aequinoctialis -50 16 0.002 Icteridae Chrysomus ruficapillus -5 0 Pseudoleistes virescens 2 19 0 <0.001 Revista Brasileira de Ornitologia 27(3): 2019 Bird communities in natural and revegetated grasslands Becker et al. Number of records Family Grassland P value Species specialization Natural Revegetated Sturnella superciliaris 206 Agelaioides badius - 80 Molothrus bonariensis 3 62 0 <0.001 Thraupidae Microspingus cabanisi -3 0 Poospiza nigrorufa 3 23 2 0.007 Sicalis flaveola - 73 4 <0.001 Sicalis luteola 2 154 179 0.33 Sporophila caerulescens - 2 8 0.15 Volatinia jacarina 207 Donacospiza albifrons 2 87 11 <0.001 Embernagra platensis 2 139 58 <0.001 Paroaria coronata -2 0 Fringillidae Spinus magellanicus - 56 3 <0.001 Association to grasslands in southeastern South America according to Azpiroz et al. (2012): (1) grassland-restricted species, i.e., species that do not use alternative habitats, (2) species that use extensively grassland habitats, but other habitats as well, and (3) species that make extensive use of grassland habitats only in certain subregions of the southeastern South American grasslands. A hyphen denotes species not associated to grasslands. P values for G tests contrasted the frequencies of records at natural and revegetated grasslands with the expected frequencies based on equal number of records at each habitat. Only species with ten or more records were tested. Revista Brasileira de Ornitologia 27(3): 2019
Ornithology Research – Springer Journals
Published: Sep 1, 2019
Keywords: exotic grasses; habitat restoration; mining; Pampas Biome
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