Birds of a wildlife reserve in the South American Pampa ( Córdoba , Argentina )

In the Pampa ecoregion of South America, the intensification of agriculture has led to the almost total replacement of pristine vegetation by agroecosystems. This has caused a great loss of biodiversity and a decline of bird assemblages. We monitored birds in Dos Hermanas Wildlife Reserve, an integrated ecosystembased management area in preserved natural saline wetland relicts (grasslands and shrublands) with a cultivated sector (sustainable grazing and organic crops). We recorded a total of 170 species, including altitudinal migrants, Nearctic migrants, migrants of the temperate-tropical and cold-temperate systems, and residents. Seven are globally threatened species and three are exotic species. The high diversity of birds recorded at Dos Hermanas Wildlife Reserve highlights the importance of this reserve for the conservation of the regional biota. The application of ecosystem-based management allows the presence of contrasting vegetation structures with positive effects on the diversity of bird assemblages in the Pampa region.


INTRODUCTION
The Río de la Plata grasslands are the largest complex of temperate grasslands ecosystems in South America, covering an area of approximately 750,000 km 2 (Soriano et al. 1991).These grasslands include the Pampa ecoregion of Argentina (540,000 km 2 ) and the Campos ecoregion of Uruguay, northeastern Argentina and southern Brazil (Miñarro and Bilenca 2008).The Pampa ecoregion is dominated by grasslands with few or no trees, together with wetlands and agroecosystems.During the last 40 years, this ecoregion has been facing growing human intervention, marked by a considerable increase in the proportion of cultivated area (45% between 1990 and 2006), mainly for annual crops such as genetically modified soybean (Viglizzo et al. 2006;Gavier-Pizarro et al. 2012).This expansion of intensive agricultural activities replaced extensive livestock grazing -a practice considered less detrimental for the grasslands and therefore for birds (Marino et al. 2013).
On a global scale, several once common grassland bird populations have rapidly declined or undergone reduction in their distribution, with evidence indicating that these declines are associated with intensified agricultural production (Fuller et al. 1995;Shi et al. 1999;Renfrew and Ribic 2001;Vickery et al. 2001).At the same time, in southern South America, the degradation of natural habitats as a consequence of expansion of the agricultural frontier has led to the almost complete disappearance of pristine grasslands and natural wetlands (De la Fuente and Suárez 2008;Brandolin et al. 2013).Relicts of natural vegetation of the Pampa ecoregion remain only in protected areas, on embankments and areas surrounding railroads, or in landscapes not suitable for agriculture (e.g., saline wetlands and flooding areas) (Soriano et al. 1991;Cantero et al. 2013).These relicts provide an opportunity to evaluate the effects of diversity loss due to land use changes (Isacch et al. 2003) and contribute to the conservation of similar habitats that are threatened by similar transformations.

Lists of species
Dos Hermanas Wildlife Reserve (DHWR), at the western border of the Pampa ecoregion, can be used as a model to assess the effectiveness of practices that are compatible with the conservation of birds.This Reserve is a unique example in which ecosystem-based management is practiced (i.e., combined and integrated land use for organic agriculture, ranching and areas of natural habitat under protection) for the purpose of ensuring the physical (biotic and abiotic components) and economic sustainability of the system.This type of management -including crop rotation, controlled grazing, soil and tillage conservation and absence of chemicals like biocides, fertilizers and veterinary products -seems to promote the diversity of birds and benefit conservation in agricultural environments.The variety of activities performed at DHWR allows us to examine the diversity of land uses of the Pampa ecoregion, from natural environments to the current agricultural and livestock production system.Moreover, DHWR offers the ideal conditions to study bird assemblages and the effects of management practices on biodiversity, thereby providing a conceptual basis for the conservation of threatened habitats in the Pampa ecoregion.In this study, we report the results of three years of ornithological monitoring conducted in DHWR.undulating relief are dominated by tall grasslands composed mainly of Nassella spp., Paspalum dilatatum, Bromus catharticus and Jarava ichu, as well as exotic weed species such as Cynodon dactylon, Viola arvensis and Carduus acanthoides.In the depressed areas, which receive surface runoff of low salinity and are temporarily flooded, the representative community is tall grassland of Schoenoplectus californicus.Areas with very saline soils are dominated by a low, deciduous shrubland composed of woody and succulent halophyte species such as Cyclolepis genistoides, Atriplex undulate and Heterostachys ritteriana.In a large area of DHWR, (~56%) the native vegetation has been replaced by organically farmed cereal and legume monocultures, and by perennial pastures.Exotic trees, mainly Eucalyptus (Eucalyptus sp.), Poplars (Populus sp.) and Persian lilac (Melia azedarach) associated with buildings are located in the non-saline highest topographical sectors.

Data collection
We surveyed birds using two complementary approaches: 1) point counts, following Bibby et al. (2000), during which two or three observers recorded all birds heard or seen during five minutes within a defined radius of 100 m.Counts were made during the first four hours after sunrise and we did not carry out point counts under strong wind or rain conditions (Ralph et al. 1995); 2) unsystematic observations carried out in areas different from those covered by point counts, such as forested areas (Eucalyptus sp., Melia sp. and Populus sp.) roadsides and habitation.We walked these areas looking mainly for particularly inconspicuous or silent species.
Ten surveys, of five days each, were carried out in all seasons, from the summer of 2012 to the winter of 2015.Birds were detected and identified using 8 × 40 binoculars and field identification guides (Narosky and Yzurieta 2010;Azpiroz 2012).For secretive species we played bird sound recordings and compared vocalizations with confirmed recordings (Narosky and Yzurieta 2010).Nomenclature follows the South American Classification Committee (Remsen et al. 2016).Records were documented, whenever possible, with photographs or recordings of sounds, deposited at www.ecoregistros .org(Vizentin-Bugoni et al. 2015).Documented records can be accessed online using the voucher numbers listed in Table 1.
Birds were categorized according to their residency in two ways: first we established categories according to our field data as residents, winter or summer visitors and occasional.Second, we used information on the migratory status obtained from the literature on each bird species and the following categories defined by Cueto et al. (2008): (1) "Migrant from the Temperate-Tropical system", species that nest in the study area and move to tropical humid latitudes to spend the austral winter; (2) "Migrants from the Cold-Temperate system", species that nest in cold regions from south and central Argentina and spend the austral winter in the center and north of the country; (3) "Nearctic Migrant", species that nest in the northern hemisphere and migrate to the southern hemisphere in the austral summer; (4) "Altitudinal Migrant", species that nest in the high Andes and move to low regions in the austral winter.We identified the principal habitat used by each species through field observations.The general habitat types were: tall grasslands, short grasslands, native shrublands, low flooded freshwater, shallow lake, crops and exotic tree plantations (Figure 2).For conservation status, we followed López-Lanús et al. (2008) and IUCN (2015b).

RESULTS
We recorded 170 species in 41 families: 114 species were residents, 23 winter visitors, 25 summer visitors and eight were occasional.We provided documentation for 136 species (Table 1).According to their migratory status, 13 species were considered as temperate-tropical, 16 as cold-temperate, 10 species were migratory Nearctic, and only the Andean Flamingo (Phoenicoparrus andinus Philippi, 1854) was an altitudinal migrant.The Cinereous Harrier (Circus cinereus Vieillot, 1816) exhibited seasonal variation but is not considered a migratory species.The Cinnamon Teal (Anas cyanoptera Vieillot, 1816) and the Rosy-billed Pochard (Netta peposaca Vieillot, 1816) are considered species with regular movements between sites, but in DHWR were recorded during the entire study period.The Dark-throated Seedeater (Sporophila ruficollis Cabanis, 1851) is considered a Temperate-tropical migrant, but was only recorded in DHWR during the winter.

Species Accounts
Particularly noteworthy records and the explanations of the diagnostic characters used for the identification of cryptic and rare species are presented below: Rhynchotus rufescens Temminck, 1815: Very elusive and difficult to observe but presents a characteristic song, different from the other Tinamidae species present in the area (Nothura maculosa).
Phoenicoparrus andinus Philippi, 1854: This species has been recorded frequently in DHWR (Brandolin and Avalos 2010).In photographs it is possible to see the characteristic violet tint on the upper breast and the black on the posterior third of the body.
Phimosus infuscatus Lichtenstein, 1823: Although this species can be confused with Plegadis chihi, Phimosus infuscatus looks darker and more opaque with a very characteristic rosy bare face.
Theristicus melanopis Gmelin, 1789: Often considered conspecific with T. caudatus.However, it was considered a separate species by Steinbacher (1979), Fjeldsa and Krabbe (1990), Matheu and del Hoyo (1992) and Ridgely and Greenfield (2001).Morphological differences make it easy to identify it in the field (gray pectoral collar and black only on belly and vent).We use the name proposed in Remsen et al. (2016) until a formal publication clarifies the taxonomy.
Porzana spiloptera Durnford, 1877: synonyms: Laterallus spilopterus.This is a poorly known species.Individuals were identified by the characteristic dotted coverts and confirmed by sound recordings.The brownish streaked back differentiates it from Laterallus jamaicensis apart from having different geographical distribution (Narosky and Yzurieta 2010).
Tringa melanoleuca Gmelin, 1789: Often misidentified with its congener Tringa flavipes, but substantial differences in body size makes them distinguishable when in mixed species groups (which they usually are).In cases where isolated individuals were found, bill proportions and vocalizations were used for identification.
Nycticryphes semicollaris Vieillot, 1816: Very elusive species.It was identified from photographs by the striking design of the dorsal plumage.
Phacellodomus sibilatrix Sclater, 1879: A rare species in the region.We could identify it and confirm its presence in DHWR through recorded vocalizations.
Asthenes hudsoni Sclater, 1874: Elusive and rare species for the region.
Spartonoica maluroides d'Orbigny & Lafresnaye, 1837: Elusive and difficult to observe.We identified its presence by its characteristic song and from photographs.
Synallaxis albescens Temminck, 1823 and Synallaxis frontalis Pelzeln, 1859: The elusive behavior and enclosed habitat of these two species may lead to misidentification.They may be distinguished by their vocalizations.
Serpophaga subcristata Vieillot, 1817 and Serpophaga griseicapilla Straneck, 2007: Morphologically very similar and almost indistinguishable.Straneck (2007) described S. griseicapilla, based on substantial differences in vocalization.Comparisons of songs allowed assignment of individuals to the correct species.
Pseudocolopteryx flaviventris d'Orbigny & Lafresnaye, 1837: Ábalos and Areta (2009) provided evidence that P. flaviventris includes two cryptic species (P.flaviventris and P. citreola) that differ in vocalization and display.With playback experiments we were able to identify which species corresponded to our observations in DHWR.We identified those individuals that responded to the call of the species P. citreola in DHWR, but since the responses were not very loud, these records were not included in this work.
Tachycineta leucorrhoa Vieillot, 1817 and Tachycineta meyeni Meyen, 1834: These two species were identified according to their differences in the color of the underwing coverts (white for T. leucorrhoa and ashygray for T. meyeni).The presence of a white forehead and white half eyebrows facilitated the identification of Tachycineta leucorrhoa.
Sturnus vulgaris Linnaeus, 1758: An exotic species.Identification was made through photographs.
Anthus spp.: Species of this genus are difficult to identify visually because of their similar plumage.Identification of the species in DHWR was made by comparing their songs with the recordings (Narosky and Yzurieta 2010).

DISCUSSION
In this study we generated an exhaustive list of bird species found in different habitats in a highly heterogeneous region of the Pampa of Argentina.The diversity recorded here accounts for about 45% of the total bird species identified by Nores (1996) in the Province of Córdoba, and 61% of the species that Azpiroz (2012) recognized as having probable distribution in the study area.These results indicate that DHWR is a very important site for bird conservation.
DHWR is located in the geographical center of Argentina, and provides a step in the migratory flow of temperate-tropical and cold-temperate systems.Both Patagonian and northern Argentinian species were observed, explaining the high diversity recorded.Also, DHWR offers wintering grounds for one altitudinal migratory species and many Nearctic ones.The Andean Flamingo nests in summer (December to January) in the highlands of northwestern Argentina and moves to lower latitudes within the Andes and to lower altitudes in winter (Brandolin and Avalos 2010;HBW 2015).Generally, there is considerable agreement between residency status observed in DHWR and the migratory status of most species.Species that behave differently than expected in terms of residency are likely to be because of local movements due to various factors such as the availability of food resources and nesting, or because they are species with low population densities and are not easily detected in the field.The Dark-throated Seedeater is rare in winter for this area and probably the records correspond to individuals which did not migrate to the north.For birds in highly modified environments, it is likely that relict of natural grasslands has a quasi-insular behavior within the surrounding agricultural matrix, as birds find this habitat preferable to agricultural environments where they do not find a suitable habitat (Carrascal and Tellería 1988).
The European Starling is a species with major invasive potential and it is expanding its population in central Argentina.It competes with native bird species and in large numbers it can become a significant pest for agricultural production (Klavins and Álvarez 2012).So far, this introduced species had been reported only in urban areas in the Pampa ecoregion, but our records confirm its presence in agroecosystems, highlighting a concern about the expansion of the species.
Given the fragmentation of natural ecosystems of the Pampa in recent decades, the high diversity of birds at DHWR, including nine species threatened at national and international level shows that this reserve represents an important place for the conservation of the regional biota.The species recorded in DHWR showed a high specificity in the use of habitat which is consistent with a close relationship between bird species and structural and floristic characteristics of the vegetation (Graham and Blake 2001;Naugle et al. 2001;Skowno and Bond 2003;Wakeley et al. 2007;Di Giacomo and Lopez De Casenave 2010).This suggests that increasing complexity in habitat structure (horizontal, vertical and qualitative variation of elements present) generates greater resources for birds, allowing the persistence of a greater number of species and guilds than in less complex habitats (MacArthur and MacArthur 1961;Tews et al. 2004;Codesido et al. 2013).
In general, natural and less-modified habitats in the Pampa are more frequently used by birds than highly modified habitats (Filloy et al. 2010).On the other hand, any disturbances in the landscape that increase structural complexity and plant diversity (e.g.selective grazing) promote greater bird species richness (Isacch et al. 2003).In terms of planning and management, the spatial coexistence of contrasting vegetation structures (e.g., grassland-shrubland-crops), generates high landscape diversity values and has a positive effect on the diversity of bird assemblages in the Pampa ecoregion (Brandolin et al. in press).Our results are supporting the hypothesis that land management with mixed farming (agriculture and livestock) using certified organic methods, long cycles of crop and pasture rotation, restrictions on the use of chemical fertilizers and fumigants and the sparingly grazed lakeside (considered to be one of the last relicts of the original Pampa environments) can generate a highly desirable patchy habitat structure and thus support a wide variety of birds.
The advance of the agricultural frontier is a common threat to all temperate grasslands in South America, including the southeast of Cordoba province.Due to this growing trend of agricultural expansion on natural environments in Argentina and worldwide, there is a clear need for a change in conservation strategies.Organic land management, as at DHWR, or other systems that ensure environmental sustainability (e.g., multifunctional landscapes) would offer promising alternative scenarios for long-term stability between human activity and bird populations (Petit et al. 1995).The generation of knowledge about the functioning of environments in relict sites and in agroecosystems, especially in threatened environments such as the grasslands and wetlands of the Pampa ecoregion, is essential for establishing a point of comparison and baseline for future research and evaluation of management practices.

Figure 1 .
Figure 1.Location of the Dos Hermanas Wildlife Reserve in central Argentina (A) and southeastern Cordoba province (B).The different types of habitats present within DHWR are indicated (C).
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Brandolin et al. | Birds of a wildlife reserve in the Pampa, Argentina