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14 January 2015 Structure of avian assemblages in grasslands associated with cattle ranching and soybean agriculture in the Uruguayan savanna ecoregion of Brazil and Uruguay
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Abstract

Conversion of grasslands into crops is a major factor leading to the decline of grassland birds. Cattle ranching represents another disturbance to natural grasslands, but may be less detrimental to grassland birds. We studied the diversity, density, and composition of bird species in Brazilian and Uruguayan grasslands under two different land use types: cattle ranching on seminatural grasslands, and soybean fields with interspersed patches of grassland. Cattle sites had higher species richness (n = 75 species) than soybean sites (n = 57 species). Most birds showed higher densities in cattle sites, but some common and habitat-generalist species were more abundant in soybean sites. Species composition did not differ significantly with land use. The generalist Eared Dove (Zenaida auriculata), however, was strongly associated with soybean sites. Among species of conservation interest, either regionally or globally, all had higher densities in cattle sites, highlighting the importance of maintaining these ranching areas. The persistence of grassland birds in soybean fields may be related to the presence of seminatural grassland patches within soybean crops.

INTRODUCTION

Agricultural intensification is considered one of the major causes of population declines of grassland birds worldwide (Chamberlain et al. 2000, Askins et al. 2007, Azpiroz et al. 2012b). Agricultural areas support less diverse bird communities than native grasslands, and tend to support generalist species (Herzon and O'Hara 2007, Codesido et al. 2013). Species respond differently to habitat changes, according to characteristics such as life history and plasticity (Filloy and Bellocq 2007, Lemoine et al. 2007, Codesido et al. 2012).

Agriculture brings a number of changes that affect virtually all aspects and processes of ecosystems, reducing the area of original habitats and transforming landscapes, which can result in few isolated fragments of natural habitats (Gilpin et al. 1992, Baldi and Paruelo 2008, Bilenca et al. 2008, 2012, Medan et al. 2011). Conversion of grasslands into crops negatively affects biodiversity, through mechanization and use of herbicides and fertilizers, but livestock production on grasslands also has negative effects (Filloy and Bellocq 2007). However, management practices that increase vegetation heterogeneity in structure or composition tend to be positive for grassland birds (Derner et al. 2009). Similarly, the amount of fallow area on a site and the presence of other seminatural habitats can also be positive for grassland birds.

The significant number of threatened grassland birds (50 species in Brazil and 24 in Uruguay) and the low representation of temperate grasslands in protected areas (2.2% in Brazil and 1.7% in Uruguay) underline the necessity of developing strategies to combine agricultural activities with conservation to maintain the biodiversity of the Uruguayan savanna ecoregion (MMA 2007, Develey et al. 2008). Land use in this ecoregion has been changing, with grasslands replaced by crops, particularly soy (Glycine max) and corn (Zea mays), during the Austral spring and summer, and exotic pastures (oats [Avena sativa] and ryegrass [Lolium multiflorum]) during the Austral fall and winter (Gressler 2008). Planted pastures increased by 32% between 1980 and 1990 in Uruguay (Martino 2004). Moreover, almost 16% of the original vegetation of Rio Grande do Sul State, Brazil, was replaced from 1976 to 2002, mostly through the introduction of exotic species for forage (i.e. ryegrass, lovegrass [Eragrostis plana], and other species), agricultural activity, mainly soybean and rice, and forestry (i.e. Eucalyptus spp. and Pinus spp.; Martino 2004, MMA 2007, Develey et al. 2008, Cordeiro and Hasenack 2009). In addition, areas of seminatural grassland without any sort of production, or that are managed under low densities of livestock, are almost nonexistent in the region. In this ecoregion, grassland patches remaining within soybean fields are typically unsuitable for agriculture because of topography, soil type, or moisture (Isacch et al. 2004). Most soybean fields in the region include patches of seminatural grassland, varying in size, quantity, and shape.

Azpiroz and Blake (2009) considered the value of barley (Hordeum vulgare) and sunflower (Helianthus annuus) fields, pasturelands, and native grasslands for grassland birds. Their results highlighted the importance of natural grasslands for specialist species. Here, we extend their study by including grasslands in Brazil and by including soybean fields containing grassland patches. Soybean agriculture is especially important to consider, as soybeans are currently the main crop causing habitat loss in the temperate grasslands of southern Brazil and Uruguay (Oyhantçabal and Narbondo 2011).

Our goal was to determine differences in bird species richness, density, and community composition in areas under two types of land use: (1) cattle ranching on seminatural grasslands (hereafter referred to as cattle sites), and (2) soybean fields with scattered patches of grassland (soybean sites). We hypothesized that both species richness and species density would be greater in cattle sites. To emphasize birds of conservation concern, we also analyzed the responses of birds classified as near-threatened and threatened, regionally and globally (Azpiroz et al. 2012a, IUCN 2013, DOE 2014).

METHODS

Study Area

We worked in eight 300-ha sites in the Uruguayan savanna ecoregion divided into two land use types, cattle sites (C) and soybean sites (S; Figure 1). Cattle sites (n = 4) were dominated by seminatural grassland (cattle stocking rate ha−1: C1 = 0.96; C2 = 0.57; C3 = 0.89; C4 = 0.75) and were located in Brazil—in Dom Pedrito county (C1: 30°58′58′′S, 54°20′12′′W) in the state of Rio Grande do Sul—and in Uruguay: Rivera (C2: 30°58′19′′S, 55°26′40′′W), Vichadero (C3: 31°40′04′′S, 54°31′30′′W), and Melo (C4: 32°21′03′′S, 53°58′54′′W). Soybean sites (n = 4) had 8–17% coverage of seminatural grasslands, but were dominated by soybean fields during the Austral summer, and either wheat (Triticum vulgare; in Uruguay) or ryegrass (in Brazil) during the Austral winter. The locations of soybean sites and percentage of grassland were as follows: Dom Pedrito county (S1: 31°04′25′′S, 54°20′33′′W; 90% soy and 10% grassland) and Santana do Livramento county (S2: 30°56′39′′S, 55°24′45′′W; 92% soy and 8% grassland), both in the state of Rio Grande do Sul, Brazil; and Vichadero (S3: 31°40′23′′S, 54°33′09′′W; 83% soy and 17% grassland) and Melo (S4: 32°13′29′′S, 54°34′01′′W; 89% soy and 11% grassland) in Uruguay.

FIGURE 1.

Bird species surveys in 2010–2012 in 8 sites in the Uruguayan savanna ecoregion in Brazil and Uruguay: 4 cattle sites (cattle ranching on seminatural grasslands; circles) and 4 soybean sites (soybean fields with scattered patches of grassland; squares).

i0010-5422-117-1-53-f01.tif

We chose our study sites based on similar climatic characteristics, type of soil (deep soils), and topography, which ranged from 100 to 400 m asl with undulating features (called coxilhas) among flat areas, so that any differences in species composition would not be related to differences in these characteristics (Hasenack et al. 2010). We assumed that dominant plant species in grassland patches within soybean fields were the same as those found on cattle sites. Soybean sites had also been used for cattle ranching until the recent introduction of soybeans; the sites we surveyed were in the second and third year of crop plantations (Oyhantçabal and Narbondo 2011). Cattle sites were mainly composed by the following species: Andropogon selloanus, Axonopus affinis, Dichantelium sabulorum, Eragrostis neesii, Mnesithea selloana, Pennisetum clandestinum, Sporobolus indicus, Stipa setigera, Aspilia montevidensis, Chaptalia piloselloides, Chevreulia sarmentosa, Conyza bonariensis, Facelis retusa, Gamochaeta americana, Baccharis spp., Paspalum spp., Piptochaetium spp., Setaria spp., Hypochaeris spp., Lucilia spp., Senecio spp., and Soliva spp. (Dotta 2013, V. Gomes personal communication). All soybean fields had the same type of management, with no-till of genetically modified seeds and use of glyphosate. The sowing period was in October–November, with a few later-maturing varieties being planted in December, and harvesting began in late March to April (T. W. da Silva and G. Dotta personal observation). Our surveys were carried out across all the main growth stages (i.e. recently sown, emergent, in full flower, in full pod, in full seed, and at full maturity; Pedersen et al. 2007).

Bird Sampling

We surveyed each of the 8 sites during the Austral spring–summer, once in 2010–2011 and once in 2011–2012. We distributed 20 points systematically in each site, at least 100 m from the field edge to avoid edge effects (Ricketts et al. 2001); points were circular plots of unlimited radius, separated from each other by 300 m. Birds counted in soybean sites could be either in soybeans per se or in the patches of seminatural grasslands within the soybean fields. All 20 points were sampled in each of the 2 survey periods. We surveyed birds with 5-min point counts, excluding flyovers (Ralph et al. 1995, Bibby et al. 2000, Matsuoka et al. 2014). Surveys started at 06:00 and lasted ∼4 hr. We only carried out surveys on days without wind and/or rain. Distances from the observer to birds were measured with a rangefinder. T. W. da Silva and G. Dotta carried out all surveys. We followed Remsen et al. (2014) for taxonomy.

Statistical Analysis

Species richness

We used ANOVA to test for treatment effects on species richness recorded in all point counts combined in each plot after testing for homoscedasticity with a Levene's test, for all species found and for grassland species only. We estimated species richness for each treatment for all plots combined based on the Chao 1 estimator (Colwell and Coddington 1994), with 100 randomizations, using EstimateS 8.2.0 (Colwell 2009). We also used Chao 1 to estimate numbers of grassland species for each treatment. All statistical analyses were performed using R 2.15.2 (R Development Core Team 2012) package ‘car' (Fox and Weisberg 2011).

Population densities

We estimated the density of individual species in each treatment using the MCDS (Multiple Covariates Distance Sampling) engine in Distance 6.0 (Thomas et al. 2009). Aquatic birds, raptors, and swallows were excluded from the density analyses. Species with >30 observations were analyzed individually (following Fritcher et al. 2004). For these species we poststratified analysis by sample, in order to obtain species density in each site. Other species were assigned into 5 groups using characteristics of habitat and conspicuousness, in order to achieve the minimum number of observations required to produce a reliable detection function with Distance (see Buckland et al. 2001:302, Azpiroz and Blake 2009, Phalan et al. 2011). For species analyzed as a group, we used the group detection probability function and poststratified the model by species to obtain each species' density in each site. We truncated the 10% of the data with the longest distances within each species individually and within each group to avoid double-counting of the same individual, as recommended by Buckland et al. (2001). We compared the following models for each species and group: half-normal and hazard-rate key functions with cosine, simple polynomial, and hermite polynomial series expansion adjustments. We chose the final model based on the Kolmogorov-Smirnov probability test for goodness-of-fit and on Cramér–von Mises uniform and cosine probability tests for plausibility, and then compared model AIC (Akaike's Information Criterion) values to select the model with the lowest value. Density estimates are presented with 95% confidence intervals; species with nonoverlapping intervals are considered to have different densities between land use types.

Community composition

Using Nonmetric Multidimensional Scaling (NMDS) with the Bray-Curtis index, we plotted the 8 sites in a multidimensional space defined by the total number of individuals of each bird species to graphically represent associations among sites. For this analysis we used package ‘vegan' in R 2.15.2 (Oksanen et al. 2012, R Development Core Team 2012). Aquatic birds, raptors, and swallows were again excluded from these analyses.

RESULTS

Species Richness

We recorded 2,998 individuals from 32 families and 87 species (Appendix): 1,453 individuals from 75 species in the seminatural grassland cattle sites, and 1,564 individuals from 57 species in the soybean sites. Among these species, 38 species that were detected in the cattle sites and 30 species detected in the soybean sites are considered representative of southeastern South American grasslands (‘grassland species' hereafter; indicated in the Appendix based on Azpiroz et al. 2012b). Based on raw point count records from each plot, cattle sites had higher species richness than soybean sites for all species (ANOVA, F1,6 = 14.3, P = 0.003) and for just grassland species (ANOVA, F1,6 = 17.9, P = 0.07). Chao 1 curves for all sites combined within each treatment did not reach a plateau for all species or for just grassland species, especially for cattle sites, indicating that more species would be found with more effort (Figure 2). Despite some overlap in 95% CI, the cattle sites showed higher estimated species richness for all species (cattle: Chao 1 estimate = 93 species, 95% CI = 80–140; soybean: Chao 1 estimate = 69 species, 95% CI = 60–105) and for just grassland species (cattle: Chao 1 estimate = 51 species, 95% CI = 40–132; soybean: Chao 1 estimate = 32 species, 95% CI = 30–43).

FIGURE 2.

Sample-based bird species accumulation curves in 8 sites in the Uruguayan savanna ecoregion in Brazil and Uruguay in 2010–2012 from Chao 1 (Colwell and Coddington 1994) estimates (mean ± 95% CI) for each treatment (cattle sites = solid line, soybean sites = dashed line) for all sites combined within each treatment: (A) All species, (B) Grassland species only.

i0010-5422-117-1-53-f02.tif

Population Densities

Among the 56 species for which we analyzed density, most showed higher densities in cattle sites, but only 6 species had nonoverlapping 95% confidence intervals (Table 1): Eared Dove (Zenaida auriculata), Rufous Hornero (Furnarius rufus), Firewood-gatherer (Anumbius annumbi), Great Kiskadee (Pitangus sulphuratus), Grassland Yellow-Finch (Sicalis luteola), and Rufous-collared Sparrow (Zonotrichia capensis). Eared Doves had higher densities in soybean sites, and the other 5 species had higher densities in cattle sites.

TABLE 1.

Density of birds in 2010–2012 in 8 sites in the Uruguayan savanna ecoregion in Brazil and Uruguay based on Distance sampling (individuals ha−1; D), and 95% confidence intervals, at sites with cattle ranching on seminatural grasslands (cattle sites; C) and soybean with grassland patches (soybean sites; S). Nonoverlapping confidence intervals between treatments are in bold.

i0010-5422-117-1-53-t01.eps

Species Composition

The NMDS did not show a clear separation between the two land use types (Figure 3). Although cattle sites were more tightly clustered than soybean sites, two soybean sites fell within that cluster. The Eared Dove was strongly associated with the other two soybean sites, which were highly distinct on NMDS axis 2.

FIGURE 3.

Nonmetric Multidimensional Scaling (NMDS) based on the abundance of bird species of 8 sites in the Uruguayan savanna ecoregion in Brazil and Uruguay in 2010–2012 in the two types of land use: 4 cattle sites (circles, C1–C4) and 4 soybean fields with grassland patches (squares, S1–S4), using the Bray-Curtis similarity index. Species abbreviations are in Table 1.

i0010-5422-117-1-53-f03.tif

Among the species classified in any of the categories of threat or as near-threatened, either regionally or globally, we recorded 5 species (Table 2): Greater Rhea (Rhea americana), Burrowing Owl (Athene cunicularia), Black-and-white Monjita (Xolmis dominicanus), Sedge Wren (Cistothorus platensis; Figure 4), and Saffron-cowled Blackbird (Xanthopsar flavus). The first 3 species were recorded in both soybean and cattle sites. The Sedge Wren and Saffron-cowled Blackbird were recorded only in cattle sites.

TABLE 2.

Number of records and replicates of species of conservation concern in the Uruguayan savanna ecoregion in Brazil and Uruguay in 2010–2012 in cattle sites (C) and soybean sites (S) where threatened species were observed.

i0010-5422-117-1-53-t02.eps

FIGURE 4.

Sedge Wren (Cistothorus platensis). Photo credit: G. Dotta.

i0010-5422-117-1-53-f04.tif

DISCUSSION

Our results showed that the two land use types did not differ in bird species composition or individual species densities for most species. Nevertheless, cattle sites had higher species richness than soybean sites, and also supported more species considered representative of southeastern South American grasslands. Moreover, some threatened species were found only in cattle sites, highlighting the greater value of this land use for bird conservation.

Codesido et al. (2008) found the same pattern for species richness when comparing seminatural grasslands under cattle ranching and crop fields (several crops) in Argentina. The high number of species (57) that we found in soybean fields, including some grassland specialists, is possibly associated with the grassland patches within the soy (Coppedge et al. 2001, Bennett et al. 2006, Cerezo et al. 2011). These patches might increase the heterogeneity of vegetation at the landscape level, supplying areas for foraging that favor the occurrence and abundance of grassland specialists (Herkert 1994, Vickery et al. 1994, Winter and Faaborg 1999, Johnson and Igl 2001, Cerezo et al. 2011). Furthermore, the Black-and-white Monjita and Saffron-cowled Blackbird, which are species of conservation concern, have been reported in crop fields, including soy, albeit not frequently (Azpiroz et al. 2012b, BirdLife International 2014, C. S. Fontana personal observation).

To our knowledge there are no published studies of birds in soybean monoculture in South American grasslands, and it would be useful to examine birds' responses without the presence of interspersed patches of natural habitat. Further, it will be important to understand how grassland patches within row crops change over time in suitability for birds. A relatively high number of bird species can be recorded in crop fields, provided the management processes, from planting to harvest, generate some differences in vegetation structure (Azpiroz and Blake 2009, VanBeek et al. 2014, Weyland et al. 2014). Nevertheless, many bird species are likely to disappear as crops replace natural habitats and as land use switches from a species-rich grassland ecosystem to a simpler system, such as soybean monoculture (Blum et al. 2008).

Agricultural intensification leads to homogeneous landscapes. As such, monocultures affect birds through reducing areas for nesting, food supply, and cover (Filloy and Bellocq 2007, Codesido et al. 2008, Bilenca et al. 2009). Our results on species composition are comparable to those of Filloy and Bellocq (2007) and Codesido et al. (2008), suggesting that replacing seminatural grasslands with crops is more harmful to grassland birds than cattle ranching activities, at least at the vegetation and stocking densities that we sampled. In the grasslands of southern Brazil and Uruguay the matrix is still predominantly composed of seminatural habitat (i.e. grasslands), and although we have not examined the effects of the matrix on bird species composition, the matrix is likely to exert some influence. Moreover, bird communities are likely to be more homogeneous in crop fields than in more complex habitats such as natural grasslands (Hsu et al. 2010).

Among the species of conservation interest, the Greater Rhea was the only one with a larger number of records in soybean fields, highlighting the importance of maintaining other habitats for species of conservation concern. Both Saffron-cowled Blackbird and Black-and-white Monjita populations have been declining, mainly due to natural habitat destruction and alteration of land use (Bencke et al. 2003, Azpiroz et al. 2012a, IUCN 2013). The fact that the Black-and-white Monjita was recorded in soybean fields might represent a legacy effect of the recent conversion of the site, or might reflect actual persistence in soybean fields with interspersed grassland remnants, with these remnants perhaps providing foraging opportunities amongst the soybeans. It is important to note that a pair and a young individual of the species were observed more than once in a seminatural grassland area adjoining a soybean field. On the other hand, Azpiroz and Blake (2009) recorded the Black-and-white Monjita only in crop areas (barley and sunflower fields) in a study carried out in Paysandú and Salto, Uruguay, and Gressler (2008) observed the species adjacent to corn crops. Perhaps additional study will reveal how this species uses mixed agricultural landscapes.

Implications for Conservation

Agricultural production and conservation of biodiversity compete for land in the Uruguayan savanna ecoregion. Conservation practices and agricultural production in this region should be considered together, and discussed among farmers, conservationists, and government agencies. Future studies should focus on monitoring species densities through time and carrying out research on the breeding biology, distribution, and population viability of grassland birds. Our research did not evaluate possible within-season heterogeneity in bird use of soybean fields as the fields developed from sowing through to harvesting, but this could reveal more detailed patterns of bird use, especially whether birds are able to complete breeding cycles. Soybean fields are a recent addition to the region, and remnant patches of seminatural grassland might provide birds with opportunities for feeding and breeding. Our results can be considered a first step in a range of research that is still needed to understand the factors that allow persistence of grassland birds in crops with grassland patches.

ACKNOWLEDGMENTS

We are indebted to the landowners for allowing us to carry out the study on their farms, particularly José Carlos Severo for all the logistical support he provided upon receiving us on his farm. We thank three anonymous reviewers for constructive comments and suggestions on the manuscript.

Funding statement. CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) supplied scholarships to T.W.S. (M.Sc.) and G.D. (Ph.D.). A Rufford Small Grant to G.D. provided financial support for carrying out the fieldwork. No funders had input into the manuscript, nor required manuscript approval prior to submission or publication.

LITERATURE CITED

1.

R. A Askins F Chávez-Ramírez B. C Dale C. A Haas J. R Herkert F. L Knopfand P. D Vickery (2007). Conservation of grassland birds in North America: Understanding ecological processes in different regions. Ornithological Monographs 64:1–46. Google Scholar

2.

A. B Azpirozand J. G Blake (2009). Avian assemblages in altered and natural grasslands in the Northern Campos of Uruguay. The Condor 111:21–35. Google Scholar

3.

A. B Azpiroz M Alfaroand S Jiménez (2012a). Lista Roja de las Aves del Uruguay. Una Evaluación del Estado de Conservación de la Avifauna Nacional con Base en los Criterios de la Unión Internacional para la Conservación de la Naturaleza. Dirección Nacional de Medio Ambiente, Montevideo, Uruguay. Google Scholar

4.

A. B Azpiroz J. P Isacch R. A Dias S. A Di Giacomo C. S Fontanaand C. M Palarea (2012b). Ecology and conservation of grassland birds in southeastern South America: A review. Journal of Field Ornithology 83:217–246. Google Scholar

5.

G Baldiand J. M Paruelo (2008). Land-use and land cover dynamics in South American temperate grasslands. Ecology and Society 13:article 6.  http://www.ecologyandsociety.org/vol13/iss2/art6/ Google Scholar

6.

G. A Bencke C. S Fontana R. A Dias G. N Maurícioand J. K. F Mähler Jr (2003). Capítulo Aves. In Livro Vermelho da Fauna Ameaçada de Extinção no Rio Grande do Sul ( C. S Fontana G. A Benckeand R. E Reis Editors), EDIPUCRS, Porto Alegre, RS, Brazil. Google Scholar

7.

A. F Bennett J. Q Radfordand A Haslem (2006). Properties of land mosaics: Implications for nature conservation in agricultural environments. Biological Conservation 133:250–264. Google Scholar

8.

C. J Bibby N. D Burgess D. A Hilland S. H Mustoe (2000). Bird Census Techniques. Academic Press, London. Google Scholar

9.

D Bilenca M Codesidoand C. G Fischer (2008). Cambios en la fauna pampeana. Ciencia Hoy 18:8–17. Google Scholar

10.

D Bilenca M Codesido C González Fischerand L Pérez Carusi (2009). Impactos de la actividad agropecuaria sobre la biodiversidad en la Ecorregión Pampeana. In Impactos Ambientales en Ecosistemas y Categorización de Tecnologías de Gestión (N. O. Maceira, Editor), Ediciones INTA, Buenos Aires. Google Scholar

11.

D Bilenca M Codesido C González Fischer L Pérez Carusi E Zufiaurreand A Abba (2012). Impactos de la transformación agropecuaria sobre la biodiversidad en la provincia de Buenos Aires. Revista Museo Argentino Ciencias Naturales 14:189–198. Google Scholar

12.

BirdLife International (2014). IUCN Red List for Birds.  http://www.birdlife.org Google Scholar

13.

A Blum I Narbondo G Oyhantcabaland D Sancho (2008). Soja Transgénica y sus Impactos en Uruguay. La Nueva Colonización. Siemenpuu Foundation, Montevideo, Uruguay. Google Scholar

14.

S. T Buckland D. R Anderson K. P Burnham J. L Laake D. L Borchersand L Thomas (2001). Introduction to Distance Sampling: Estimating Abundance of Biological Populations. Oxford University Press, NY, USA. Google Scholar

15.

A Cerezo M. C Condeand S. L Poggio (2011). Pasture area and landscape heterogeneity are key determinants of bird diversity in intensively managed farmland. Biodiversity and Conservation 20:2649–2667. Google Scholar

16.

D. E Chamberlain R. J Fuller R. G. H Bunce J. C Duckworthand M Shrubb (2000). Changes in the abundance of farmland birds in relation to the timing of agricultural intensification in England and Wales. Journal of Applied Ecology 37:771–788. Google Scholar

17.

M Codesido C González-Fischerand D Bilenca (2008). Asociaciones entre diferentes patrones de uso de la tierra y ensambles de aves en agroecosistemas de la región pampeana, Argentina. Ornitologia Neotropical 19:575–585. Google Scholar

18.

M Codesido C González-Fischerand D Bilenca (2012). Agricultural land-use, avian nesting and rarity in the Pampas of central Argentina. Emu 112:46–54. Google Scholar

19.

M Codesido C. M González-Fischerand D. N Bilenca (2013). Landbird assemblages in different agricultural landscapes: A case study in the Pampas of central Argentina. The Condor 115:8–16. Google Scholar

20.

R. K Colwell (2009). EstimateS: Statistical estimation of species richness and shared species from samples, version 8.2.0. University of Connecticut, Storrs, CT, USA.  http://purl.oclc.org/estimates Google Scholar

21.

R. K Colwelland J. A Coddington (1994). Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London, Series B 345:101–118. Google Scholar

22.

B. R Coppedge D. M Engle R. E Mastersand M. S Gregory (2001). Avian response to landscape change in fragmented southern Great Plains grasslands. Ecological Applications 11:47–59. Google Scholar

23.

J. L. P Cordeiroand H Hasenack (2009). Cobertura vegetal atual do Rio Grande do Sul. In Campos Sulinos: Conservação e Uso Sustentável da Biodiversidade ( V. P Pillar S. C Müller Z. S Castilhosand A. A Jacques Editors), Ministério do Meio Ambiente, Brasília, DF, Brazil. Google Scholar

24.

J. D Derner W. K Lauenroth P Stappand D. J Augustine (2009). Livestock as ecosystem engineers for grassland bird habitat in the western great plains of North America. Rangeland Ecology & Management 62:111–118. Google Scholar

25.

P. F Develey R. B Setubal R. A Diasand G. A Bencke (2008). Conservação das aves e da biodiversidade no bioma Pampa aliada a sistemas de produção animal. Revista Brasileira de Ornitologia 16:308–315. Google Scholar

26.

DOE (Diário Oficial do Estado do Rio Grande do Sul) (2014). Espécies da Fauna Silvestre Ameaçadas de Extinção no Estado do Rio Grande do Sul. Decreto n° 51.797, de 08 de Setembro de 2014. Porto Alegre, RS, Brazil. Google Scholar

27.

G Dotta (2013). Agricultural production and biodiversity conservation in the grasslands of Brazil and Uruguay. Ph.D. dissertation, University of Cambridge, Cambridge, UK. Google Scholar

28.

J Filloyand M. I Bellocq (2007). Patterns of bird abundance along the agricultural gradient of the Pampean region. Agriculture, Ecosystems & Environment 120:291–298. Google Scholar

29.

J Foxand S Weisberg (2011). An {R} Companion to Applied Regression, second edition. Sage Publications, Thousand Oaks, CA, USA.  http://socserv.socsci.mcmaster.ca/jfox/Books/Companion Google Scholar

30.

S. C Fritcher M. A Rumbleand L. D Flake (2004). Grassland bird densities in seral stages of mixed-grass prairie. Journal of Range Management 57:351–357. Google Scholar

31.

M Gilpin G. A. E Galland D. S Woodruff (1992). Ecological dynamics and agricultural landscapes. Agriculture, Ecosystems & Environment 42:27–52. Google Scholar

32.

D. T Gressler (2008). Effects of habitat fragmentation on grassland bird communities in a private farmland in Pampa biome. Revista Brasileira de Ornitologia 16:316–322. Google Scholar

33.

H Hasenack E Weber I. I Boldriniand R Trevisan (2010). Mapa de Sistemas Ecológicos da Ecoregião da Savana Uruguaia em Escala 1:500.000 ou Superior e Relatório Técnico Descrevendo Insumos Utilizados e Metodologia de Elaboração do Mapa de Sistemas Ecológicos. Universidade Federal do Rio Grande do Sul, RS, Brazil. Google Scholar

34.

J. R Herkert (1994). The effects of habitat fragmentation on Midwestern grassland bird communities. Ecological Applications 4:461–471. Google Scholar

35.

I Herzonand R. B O'Hara (2007). Effects of landscape complexity on farmland birds in the Baltic States. Agriculture, Ecosystems & Environment 118:297–306. Google Scholar

36.

T Hsu K Frenchand R Major (2010). Avian assemblages in eucalypt forests, plantations and pastures in northern NSW, Australia. Forest Ecology and Management 260:1036–1046. Google Scholar

37.

J. P Isacch S Holz L Ricciand M. M Martínez (2004). Post-fire vegetation change and bird use of a salt marsh in coastal Argentina. Wetlands 24:235–243. Google Scholar

38.

IUCN (2013). IUCN Red List of Threatened Species, version 2013.2.  http://www.iucnredlist.org Google Scholar

39.

D Johnsonand L Igl (2001). Area requirements of grassland birds: A regional perspective. The Auk 18:24–34. Google Scholar

40.

N Lemoine H. C Schaeferand K Böhning-Gaese (2007). Species richness of migratory birds is influenced by global climate change. Global Ecology and Biogeography 16:55–64. Google Scholar

41.

D Martino (2004). Conservación de praderas en el conosur: Valoración de las áreas protegidas existentes. Ecosistemas 13:114–123. Google Scholar

42.

S. M Matsuoka C. L Mahon C. M Handel P Sólymos E. M Bayne P. C Fontaineand C. J Ralph (2014). Reviving common standards in point-count surveys for broad inference across studies. The Condor: Ornithological Applications 116:599–608. Google Scholar

43.

D Medan J. P Torretta K Hodara E. B Fuenteand N. H Montaldo (2011). Effects of agriculture expansion and intensification on the vertebrate and invertebrate diversity in the Pampas of Argentina. Biodiversity and Conservation 20:3077–3100. Google Scholar

44.

MMA (Ministério do Meio Ambiente) (2007). Áreas Prioritárias para Conservação, Uso Sustentável e Repartição de Benefícios da Biodiversidade Brasileira: Atualização Portaria MMA n° 9, 23 de Janeiro de 2007. MMA, Brasília, DF, Brazil. Google Scholar

45.

J Oksanen F. G Blanchet R Kindt P Legendre P. R Minchin R. B O'Hara G. L Simpson P Sólymos M. H. H Stevensand H Wagner (2012). vegan: Community Ecology Package. R package version 2.0–5.  http://cran.r-project.org/web/packages/vegan/index.html Google Scholar

46.

G Oyhantçabaland I Narbondo (2011). Radiografía del Agronegocio Sojero. Redes-AT, Montevideo, Uruguay. Google Scholar

47.

P Pedersen S Kumudini J Boardand S Conley (2007). Soybean growth and development. In Using Foliar Fungicides to Manage Soybean Rust ( A. E Dorrance M. A Draperand D. E Hershman Editors), The Ohio State University, Columbus, OH, USA. Google Scholar

48.

B Phalan M Onial A Balmfordand R. E Green (2011). Reconciling food production and biodiversity conservation: Land sharing and land sparing compared. Science 333:1289–1291. Google Scholar

49.

R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.  http://www.R-project.org Google Scholar

50.

C. J Ralph S Droegeand J. R Sauer (1995). Managing and monitoring birds using point counts: Standards and applications. In Monitoring Bird Populations by Point Counts ( C. J Ralph J. R Sauerand S Droege Editors), USDA Forest Service General Technical Report PSW-GTR-149. Google Scholar

51.

J. V Remsen C. D Cadena A Jaramillo M Nores J. F Pacheco J Pérez-Emán M. B Robbins F. G Stiles D. F Stotzand K. J Zimmer (2014). A classification of the bird species of South America, version 1, October 2014. American Ornithologists' Union.  http://www.museum.lsu.edu/∼Remsen/SACCBaseline.html Google Scholar

52.

T. H Ricketts G. C Daily P. R Ehrlichand J. P Fay (2001). Countryside biogeography of moths in a fragmented landscape: Biodiversity in native and agricultural habitats. Conservation Biology 15:378–388. Google Scholar

53.

L Thomas J. L Laake E Rexstad S Strindberg F. F. C Marques S. T Buckland D. L Borchers D. R Anderson K. P Burnham M. L Burt S. L Hedley et al . (2009). Distance 6.0. Release 2. Research Unit for Wildlife Population Assessment, University of St. Andrews, St. Andrews, Fife, UK.  http://www.ruwpa.st-and.ac.uk/distance Google Scholar

54.

K. R VanBeek J. D Brawnand M. P Ward (2014). Does no-till soybean farming provide any benefits for birds? Agriculture, Ecosystems & Environment 185:59–64. Google Scholar

55.

P. D Vickery M. L Hunter Jrand S. M Melvin (1994). Effects of habitat area on the distribution of grassland birds in Maine. Conservation Biology 8:1087–1097. Google Scholar

56.

F Weyland J Baudryand C. M Ghersa (2014). Rolling Pampas agroecosystem: Which landscape attributes are relevant for determining bird distributions? Revista Chilena de Historia Natural 1:article 1. Google Scholar

57.

M Winterand J Faaborg (1999). Patterns of area sensitivity in grassland-nesting birds. Conservation Biology 13:1424–1436. Google Scholar

APPENDIX

Number of individuals of species sampled in 2010–2012 in the two types of land use of the Uruguayan savanna ecoregion, including aquatic birds, raptors, and swallows. C = cattle sites (cattle ranching on seminatural grasslands) and S = soybean sites (soybean fields with scattered patches of grassland).

i0010-5422-117-1-53-t03.eps
Thaiane Weinert da Silva, Graziela Dotta, and Carla Suertegaray Fontana "Structure of avian assemblages in grasslands associated with cattle ranching and soybean agriculture in the Uruguayan savanna ecoregion of Brazil and Uruguay," The Condor 117(1), 53-63, (14 January 2015). https://doi.org/10.1650/CONDOR-14-85.1
Received: 26 May 2014; Accepted: 1 November 2014; Published: 14 January 2015
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