This study shows the magnitude of the avifauna occurring in the Brazilian Chaco biome, located in the central region of South America. The Chaco formation is present in Brazil, Paraguay, Bolivia and Argentina, comprising a large phyto physiognomy of nearly 800,000km², of which 9,000km² is located in Brazil, near the town of Porto Murtinho, a transition zone of the Pantanal wetland. It is formed by spiny trees which lose their small leaves during the dry season. During our field work we registered 326 species of wild birds, and, when added to other published surveys, this number totalizes 355 species living within the Brazilian Chaco. The most common species were Tyrannidae (13.2%), followed by Thraupidae (9.2%) and Icteridae (4.9%). Fourteen officially listed threatened bird species were detected during our field work. Our results contribute to the knowledge on bird diversity living in the Brazilian Chaco, and to the potential attraction for sustainable tourism, as an incentive to protect the avifauna and their habitats, achieving conservation for the biodiversity of the region.

Keywords: avifauna, birdwatching, chaco, conservation, threatened bird species

The Chaco is one of the largest biomes in South America, rich in biodiversity, but facing increasing environmental disruptions due to demographic expansion and unsustainable use of natural resources. Wild species of birds can attract tourism as one element to conserve nature, providing economic incentives since biodiversity can represent important socioeconomic and environmental activities.^1,2 The Chaco is an arid subtropical biome in the center of South America, dominated by savanna vegetation and rare low forest. It is the second largest biome in South America.³ This steppe Savanna vegetation formation, as it is known, comprises 520,000km² (46%) in Argentina, 230,000km² (32%) in Paraguay, 90,000km² (15%) in Bolivia and 9,000km² (7%) in Brazil. There is a predominance of xenomorphic vegetation, with deciduous trees, cacti and bromeliads.^3–6 The vast Quaternary plain between the Paraguay Parana rivers and the foothills of the western ranges, known as the 'Gran Chaco', is a natural region, 700km wide in the east west direction and roughly 1,500km from north to south, comprising an area estimated to range from 800,000 to 1,000,000km².^3,4,7

In its extreme eastern portion is the Paraguay River in Brazilian territory,³ south of the Pantanal wetland, in the sub regions Porto Murtinho and Nabileque, and this comprises the wet Chaco.^5,8 It is a transition area among the surrounding biomes of the Pantanal wetland, namely the Cerrado (savanna), and the Dry Forests there is an interception among the vegetation formations, forming ecotones that cannot easily be identified by sight. There is high density of the palm tree "caranda" (Copernicia alba Morong), and other trees such as "paratudo" (Handroanthus aureus Mattos) and "piuva" (H. heptaphylla (Vell.) Mattos).^3,6 The Chaco forest in north eastern Argentina and Paraguay, entering Brazilian territory, near the city of Porto Murtinho, is dominated by a hardwood tree red quebracho (Schinopsis balansae Engl) which is typical of this region.^3,8 The Brazilian Chaco has lately received increasing research attention, especially in plant sciences, but there have been few studies on wild birds. Some studies have even stressed the lack of avian surveys for that region.^9,10 The last survey carried out in the Brazilian Chaco region reached 282 bird species.¹¹ This list of species includes previously collected secondary data.^9,12 The aim of the present study is to contribute to the knowledge of the rich and diverse avifauna of the Brazilian Chaco region, to pursue conservation and to attract tourists to the region, and thus to implement sustainable use through tourism and birdwatching activities.

Study area

This study was conducted throughout the Chaco region of Porto Murtinho, in the southwestern part of the state of Mato Grosso do Sul, in Brazil.³ The regional climate is hot and dry, with annual average rainfall of 970.3 mm and temperature of 25 °C, with a rainy season from November to February.¹³ The environmental seasonality within this region is more marked by rainfall than by change in temperature. Different kinds of habitats were surveyed, including riparian forest, open dry and flooded fields, savanna (Cerrado) and steppe savanna (Chaco), forest and areas under human use, such as pastures (Figure 1).

Figure 1 The Chaco in South America comprising the countries of Argentina, Bolivia, Paraguay and Brazil.

Field surveys

Short term and intensive bird surveys were carried out in the field from 2002 to 2015. Six expeditions were conducted with variable length of duration, covering terrestrial and fluvial routes, starting at 06h00 and going until 11h00, and then from 14h00 until 17h30. The search for nocturnal species ran from 19h00 until 22h00. Occasional and opportunistic bird registers were also recorded during our journeys, including directed visual observation and bird vocalization signals. The detected species were photographed whenever possible, to serve as evidence of occurrence. The surveyed areas are shown in Table 1.

Characteristics of the surveyed sites

Cachoeirado apa municipal park: This Park is located at the margins of the Perdido and Apa rivers, on the border between Brazil and Paraguay. The habitats include gallery forest, seasonal forest and savanna formations (Cerrado) with influence of Chaco environment. The Park is included in the rural area, lying 85 km from the urban zone of Porto Murtinho.

Urban area of porto murtinho and paraguay river banks: The urban zone of the town of Porto Murtinho is located on the left bank of the Paraguay River, and despite the presence of 15,000 inhabitants, there are still some remnants of natural vegetation. Some key-trees are present: species of Prosopis, Zizyphus, Schinopsis, Aspidosperma and others.

Barranco branco station: This site is characterized by typical Chaco vegetation, including the predominance of the caranda palm Copernicia alba (common in steppe park savanna) on the left bank of the Paraguay River. Flooded fields are present along with the typical phyto physiognomies of Chaco: woody-grassy savanna, steppe scrub savanna and forested steppe savanna.

Ingazeira station: This area also presents typical Chaco vegetation such as riparian forest, deciduous forest, savanna forest; swamp sand flooded open fields with significant presence of woody-grassy savanna, steppe scrub savanna, steppe park savanna and forested steppe savanna.

Dam to control flooding and rural area: The vegetation cover of this study site is mainly formed by steppe woody-grassy savanna, steppe park savanna, forest steppe savanna and steppe scrub savanna. Besides the presence of the palm caranda Copernicia alba, other trees were noted such as Proposis spp. and Zizyphus oblongifolius.

Road BR-267/MS: Along this road and its surroundings there is vegetation cover like savanna (Cerrado), remnants of seasonal deciduous forest, and transitions to the Pantanal wetland.

Cerro pora cattle ranch: This region shows a predominance of savanna (Cerrado), seasonal deciduous forest and gallery forest. The Chaco vegetation is restricted to some transition to Cerrado. Open fields are present. The area is used for cattle ranching.

Cangalha cattle ranch: This area is also used for cattle ranching, with some vegetation cover still present, including Cerrado and flooded fields. The species names and taxonomic arrangements adopted here follow.¹⁴

Chaco or “chaku”, in the Quechua language, means hunting territory, with high bird richness. The Brazilian part of the Chaco harbors different habitats for bird species, with influence of the savanna floral province (Cerrado) and the Pantanal wetland. However, the dry vegetation formation of the Chaco has its own characteristics: it is an environment that is more xeric than hydric, with some plant species like S. balansae, Aspidosperma quebracho-blanco, Caesalpinia paraguariensis, Acacia spp., Prosopis spp. and others. We registered 326 bird species during our survey. The most representative bird families were Tyrannidae (13.2%), Thraupidae (9.2%) and Icteridae (4.9%). Among the non Passeriformes the families with most representatives were Accipitridae (8.3%), Picidae (7.7%) and Psittacidae (7.7%). The Tyrannidae is the largest bird taxonomic family of the Neotropics, representing about 18% of the passeri forms of South America.¹⁵ This family includes frugivore and phytovore species.¹⁴ Among the Icteridae are the blackbirds, much sought after by birdwatchers. The list of the bird species encountered during our survey is summarized in Table 2. The number of bird species (326), registered in our present field survey, contributes to the ornithological knowledge of the region. Our results show that 253 species had already been registered in a previous survey.¹¹ Comparing our study to another survey carried out in the Argentine Chaco,¹⁶ which accounted for the occurrence of 96 species living in the understory of the forest, 69 species were coincident with our present study. Comparing our results to Bolivia, 80 species out of a total of 110 species found in a Bolivian Chaco survey¹⁷ were also recorded in our present study. In connection with the Paraguay part of the Chaco, 233 bird species were registered there,¹⁸ and 194 species of those were also registered in this present study. Therefore, our survey shows the occurrence of 73 bird species which represent a new register for the Brazilian Chaco. Thus, the present survey plus the previous one for the Brazilian Chaco¹¹ totalize 355 bird species for the region. The species Saltator multicolor deserves special reference, as it was recently found in the region, and its photographic register is documented in Wiki Aves.¹⁹ This is an endemic species living in xeric forest of the Chaco.^7,20,21 Our present study also registered the occurrence of representative or endemic species of the Chaco, previously registered by other researchers,^7,20,22,23 such as Rhea americana (cf. R. americana araneipes), Nothura boraquira, Ortalis canicollis, Phaethornis subochraceus, Nystalus striatipectus, Melanerpes cactorum, Celeus lugubris, Campephilus leucopogon, Cariama cristata, Thectocercus acuticaudatus, Aratinga nenday, Pyrrhura devillei, Myiopsitta monachus, Amazona aestiva(cf. Amazona aestiva xanthopteryx), Thamnophilus doliatus, Thamnophilus caerulescens (cf. T. caerulescens paraguayensis), Campylorhamphus trochilirostris(cf. C. trochilirostris lafresnayanus), Xiphocolaptes major, Pseudoseisura unirufa, Xenopsaris a. albinucha, Suiriri suiriri, Xolmis irupero, Paroaria capitata, Saltatricula multicolor and Microspingus melanoleucus.

The birds of the Chaco exhibit very low avian endemism ⁷ and they present very close affinities with the surrounding avifauna.^10,24-27 However, the region of Porto Murtinho presents species of birds which are particular to the Chaco,²³ with a close bio geographical connection with the nearby Cerrado and the Pantanal biomes. Considering the location of the Chaco and its limits to the west with the Andes, the Amazon in the north, and the Pampas and Patagonia in the south, there has been a high bio geographical interest in the region.^20,23,28-30 Open habitats favor insectivore species, and the Tyrannidae are more abundant. We found 35.6% of insectivore species in our survey. They rely mostly on arthropod prey, complementing their diet with other items.¹⁵ Besides, many Tyrannidae species are austral migrants. Among the omnivores, the combination of terrestrial and hydric habitats favor the offer of invertebrate preys, amphibians and fish, depending on the annual seasonality.³¹ We found 32.6% of omnivore species. Our results show that the majority of the species occurrence was found in open areas (n= 130; 39.9%), and the other portion occurs in generalist habitats: forest, open areas and modified habitats (n= 87; 26.7%), only in forest (n= 44; 13.5%), and in aquatic areas (n= 65; 19.9%). Some birds depend upon the presence of well preserved open habitats, including species of Furnariidae, Tyrannidae, Thraupidae, and Cardinalidae. Therefore, deforestation and conversion of natural vegetation, particularly open natural areas, is one of the major threats to be considered in conservation measures.^3,4,8,28-30

Some of our recorded species were only recently recorded for the Pantanal wetland, including: Nothura boraquira, Aramides ypecaha, Pardirallus maculatus, Calidris himantopus, Dendrocolaptes platyrostris, Elaenia chilensis, E. parvirostris, Platyrinchus mystaceus, Hymenops perspicillatus, Pachyramphus validus, Xenopsaris albinucha, Pseudoleites guirahuro, Sporophila ruficollis, S. palustris .¹⁰ A considerable number of species migrate to the Pantanal wetland,³² and others are present in the Pantanal in Cerrado vegetation.²⁶ Species such as Cyanocorax cristatellus and Saltatricula atricollis, common in open areas associated with Cerrado vegetation, were found in this study in similar habitats, showing the transitional feature of the Porto Murtinho region. There are migrant species that occur in the region. The Tyrannidae Austral migrants, for example, arrive in general by the end of the dry season, fixing home ranges in the region throughout the wet season, coinciding with greater abundance of food.^33,34 Some of the species registered deserve special attention since they are officially listed as threatened under national and international guidelines,^35,36 considering the alteration and loss of their natural habitats. When dealing with threatened species, the value of rarity is one trophy for the birders, which requires a fair conservation strategy in order to balance protection and visiting strategies.³⁷ On the other hand, the number of threatened species found in this study reinforces the need for a reliable conservation strategy. Natural habitats have been modified and the increasing deforestation has reached the study area.⁵ There are no protected areas designated for the Porto Murtinho region to preserve the native Chaco natural habitats and their associated biodiversity. All activities in the region related to the exploitation of biodiversity resources have been unsustainable in recent years, for example the use of the red quebracho (S. balansae)to extract tannin, the leaves of erva mate (Ilex paraguariensis)for tea, as well as predatory fisheries. In addition to the intrinsic value of biodiversity, its conservation needs to consider a combination of multiple strategies. For example, biodiversity plays an important role to human well-being and health, providing basic products and ecosystem services. Thus, conservation is also related to the social and economic dimensions of development. But although this relationship, human land occupation has become the dominant force that negatively impacts the biological system. The avifauna of the Chaco expresses the fascination of the local people, who have generated stories and folklore associated with mystic birds, aggregating cultural heritage. The knowledge on birds can improve not only scientific support but ways to develop sustainable tourism in the region. The benefits of nature-based tourism to biodiversity conservation are often rarely to profitability of local environmentally-based rational use to achieve sustainability. The protection of biodiversity is essential in the fight to reduce local human poverty and to achieve sustainable development. The challenge is to pursue responsible travel to relatively undisturbed natural area, such as the Brazilian portion of Chaco, with the specific objective of studying, admiring, and enjoying the scenery and its wildlife, as well as any existing cultural manifestations found in the region. However, in its broadest sense, nature-based tourism has to be sustainable in terms of its potential negative effects on the environment, for its successful conduct.

The present results contribute to knowledge of the great diversity of bird species in the region, which may be an attraction for sustainable tourism through birdwatching activities. This should be an incentive to protect the avifauna and their habitats, achieving conservation for the biodiversity of the region.

We are thankful to the Prefeitura Municipal de Porto Murtinho, to the Brazilian Army-2ª Cia Fronteira, and to Fabio Santos for all the support received during the field work, especially during the activities 2008-2015. Flavia Batista helped to elaborate the map.

No conflict of interest was detected during the work carried out in the field or for its publication.

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