Birds of the Pantanal floodplains, Brazil: historical data, diversity, and conservation

The Pantanal floodplains of Brazil are a region of rich biodiversity. To date, the true richness of the Pantanal avifauna has not been explored satisfactorily caused by a lack of studies in the region and, especially, by the divergence of opinion among the works published by various authors on the many species found in the region. This is due to the lack of criteria in examining records, both with regard to the reliability of the identifications and in the precise geographical allocation. Therefore, in the study, we collage findings from various studies and records created by us in the last few decades from 199 distinct locations to produce a list of birds in the Pantanal floodplains. We grouped the results into three lists: primary, secondary, and tertiary. We found that the avifauna of the Pantanal floodplain is composed of a total of 617 species, of which 571 (92%) have supporting records of occurrence (primary list) and 46 still lack documentation (secondary list). The number of species listed here for the Pantanal floodplain represents 32% of all avifauna known to the Brazilian territory. This reflects the importance of the biome, as part of the national territory, for the maintenance of a meaningful avifaunistic richness. Migratory birds (n = 183), notably northern ones (n = 43), are among the main players involved in ecological processes of nutrient cycling and dispersion of ISSN On-Line: 1807-0205 ISSN Printed: 0031-1049 ISNI: 0000-0004-0384-1825 Pap. Avulsos Zool., 2021; v.61: e20216182 http://doi.org/10.11606/1807-0205/2021.61.82 http://www.revistas.usp.br/paz http://www.scielo.br/paz Edited by: Luís Fábio Silveira Received: 12/04/2021 Accepted: 12/07/2021 Published: 27/09/2021 ARTICLE

Although the contribution of ornithological information about this vast perimeter is considered reasonable than 800 species of birds in the Upper Paraguay Basin (Brazil, Bolivia, and Paraguay) of which, at least, 567 had already been recorded in the Brazilian Pantanal region. Petermann (2010) points out between 469 and 522 species for the Pantanal region, whereas Nunes (2011a) related the occurrence of 582 species for the lowland.
Field guides, such as that by Gwynne et al. (2010), indicate a richness of 740 species of birds in central Brazil and, among these, 496 were credited by these authors to the Pantanal region. Pivatto & Bernardon (2012) and Cintra (2014) published guides for the identification of Pantanal avifauna and listed 455 and 523 species for the region, respectively.
Despite being relevant contributions, most of the publications cited here have questionable records and, in some cases, are based on vague geographical limits, thereby making it difficult the understanding of birds occurring in the Pantanal. Thus, in this study, we aim to present a consolidated list of birds for the lowland of the Brazilian Pantanal, obtained through data collection in the field as well as through the compilation and review of a wide range of reliable historical and contemporary records to provide a safer reference list.

The Pantanal floodplains: location, landscape, and environment
The Pantanal is one of the largest continuous wetlands on the planet. It is located in the center of South America and is cover over more than 140,000 km² across the Upper Paraguay River Basin and its tributaries that drain the Cerrado region of Central Brazil, and areas of Bolivia's Chaco region and Paraguay (Harris et al., 2005). In Brazil, the Pantanal extends for approximately 250 km in an east-west direction and 450 km in a north-south direction and, despite several elevations that exist inside, many of them isolated, the altitude varies only from 60 to 150 m (Hamilton et al., 1996).
The landscape in the floodplain of the Brazilian Pantanal is complex, diversified, and occurs in mosaics with diverse phytophysiognomies and ecological situations that are ordered by topographic gradients and flood pulses (Junk et al., 2014). Natural vegetation of the region is influenced by the adjacent phytogeographic provinces such as Cerrado (Brazilian savanna), Chaco (dry woodland or dry forest), Amazon and Atlantic Forest (Nunes & Tomas, 2004a;Silva & Santos, 2005).
The coverage and land use of the Pantanal region is currently made up of natural non-forest formations (grasslands and marshes of perennial or seasonal vegetation) and forest (savanna and seasonal forest) to spaces used by agriculture (pastures and monocultures), in addition to various bodies of water of different natures (Miranda et al., 2017;Souza-Jr. et al., 2020). All these landscape units are regulated by annual and multi-annual rain cycles that intersect with rainy and dry periods and promote extreme events of floods and droughts, the latter often being combined with large fires (Nunes Da Cunha & Junk, 2004). In general, the Pantanal climate is predominantly hot and humid, with an average annual rainfall of 1,500 mm and a maximum average temperature of 32℃ and a minimum of 20℃ (Alvares et al., 2014).
In this study, we considered the area recognized as the floodplain of the Brazilian Pantanal region (Fig. 1) within whose limits the respective records of the occurrence of the various bird species were plotted. It encompasses a perimeter of 150,000 km² exclusively in the Brazilian territory, 4.6% of which is represented by protected areas including 18 private reserves, 1 national park, 3 state parks, 1 municipal park, 1 environmental protection area, and 1 ecological station (Brazil, 2020). For the elaboration of our database, 199 locations in the states of Mato Grosso and Mato Grosso do Sul that presented one or more records of avifauna were evaluated.

Data collection
For the elaboration of the consolidated list of birds of the Pantanal floodplain, we considered the records created by us in the last decades, whether from systematic samplings or not: Allen (1891, 1892, 1893); Naumburg et al. (1930); Naumburg (1935) Benites & Mamede (in press). In all, 199 locations were visited, 29 of which could not be georeferenced. The information on these locations, period of observations, and authors of the records can be accessed in Table S1. Also, the occurrences are mentioned in the literature (Rv/sP), in the authors' field works (Rv/sNP), and in the form of specimens deposited in museums and institutional ornithological collections in Brazil and abroad (ExM). In addition, data in the form of photographic records deposited in institutional museums (FoM), cited in scientific journals (FoP) or private collection (FoAP), photographic records (FoI) and sound (ASI) records available on internet data platforms, audiovisual (ViM) and sound records (ASM) deposited in institutional museums, and sound records (ASI) deposited in data platforms are available for online consultation (Carlos et al., 2010).

Figure 1.
Localities with ornithological inventories in Pantanal wetland. The circles correspond to different sample sites, whose geographic coordinates can be found in Table S1. The dark gray spots correspond to burned areas in 2020 fire gray spots correspond to burned areas in 2020 fire according to ALARMES-HISTÓRICO (LASA/ UFRJ, 2021; Pinto et al., 2020).
Data on specimens deposited in institutional museums in Brazil and abroad were obtained by consulting Tubelis & Tomas (2003a) and the website (Vertnet, 2021). Sound archives deposited in institutional museums obtained from the Arquivo Sonoro Prof. Elias Coelho (ASEC), from the Federal University of Rio de Janeiro and at the Neotropical Fonoteca Jacques Vielliard (FNJV) of the Zoology Museum of the State University of Campinas. Regarding the photographic and sound records available on digital media, we evaluated those hosted until Mach 2021 in the WikiAves (WikiAves, 2021 -http://www.wikiaves.com), Xeno-canto (Xeno-Canto, 2021 -https://www.xeno-canto/databases. org), and Visual Resources of Ornithology/VIREO (VIREO, 2021 -http://vireo.ansp.org) databases. Records in municipalities that include stretches of plateau (e.g., Corumbá, Miranda, Aquidauana, Coxim, Rio Verde de Mato Grosso, Cáceres, and Santo Antônio do Leverger) were carefully investigated by confirming their locations with the authors to ensure that only records collected from the floodplain were included in the study. When such records were cited in publications without specific details on location, the species were not included in the main list.

Data requirements for inclusion into inventory lists
We adopted the taxonomic classification proposed by the Brazilian Ornithological Records Committee (Pacheco et al. 2021). The primary list, which was composed of species with at least one occurrence record in the Pantanal floodplain provided with documentary evidence, i.e., item/(s) available for independent consultation as a full or partial specimen, photograph, and audio/ video recording, which allow the safe and indisputable determination of the taxon. The secondary list includes species with one or more visual and/or sound records in the Pantanal floodplain, but whose documentary evidence is unknown or unavailable. In this context, the filtering protocol is the detailing of the information allusive to the record, necessarily associated with consistency of the distribution and dispersion patterns of the species based on documentary evidence. The primary and secondary lists constitute the main list.
In addition to extinct taxa of nature or those not validated as full species, some species that, although mentioned in some of the consulted sources, presented questionable records with incompatible distribution and/or occurrence only marginal to the Pantanal floodplain were excluded and are present in the tertiary list. In brief, the main list includes only the species that have been proven to occur within the defined geographical limits, based on the following superior evidence, in hierarchical order: ExM, FoM, FoP, FoI, ViM, ASM, and ASI (for details, see Carlos et al., 2010).

Species categorization
The species were categorized according to their conservation status based on the global redlist (Handbook of the Birds of the World & BirdLife International, 2020): Deficient Data (DD), Near Threatened (NT), vulnerable (VU), Endangered (EN), and Critically endangered (CR). Also, we considering the National lists of threatened species (ICMBio, 2014). In addition, we highlight species that show a global population decline (Handbook of the Birds of the World & BirdLife International, 2020). Based on the lists of migratory birds proposed by  and Somenzari et al. (2018), the species were initially distinguished as intercontinental (INTER) or intracontinental (INTRA) migrants. The former includes species that make large displacements from the northern hemisphere (Canada and northern USA) towards southern South America (Patagonia). The latter category includes species that move from the southernmost portions of South America towards its northernmost regions (mainly Amazonia) and vice versa.

RESULTS AND DISCUSSION
According to our study, the avifauna of the Pantanal floodplain is composed of a total of 617 species, of which 571 (92%) have supporting records of occurrence (primary list) and 46 still lack documentation (secondary list) (Tables 1 and S1). In the tertiary list, we include 63 species whose records were based questionable information or incompatible with the floodplain region (Table 2). Of the migratory species occurring in Brazil, 183 species use the Pantanal floodplain during migratory movements. Most are composed of southern migrants (140 species), especially those moving from the southern portions of South America towards Central Brazil and the Amazon. In this group, the most important species belong to the family Tyrannidae (37 species), genus Sporophila (15 species), and family Hirundinidae (7 species). The northern migrants add up to 43 species, almost half (45%) the number being formed by members of family Scolopacidae. Species linked to aquatic environments account for 38% of the migrant species and those dependent on native grasslands in good condition account for 12% (21 species).
With regard to conservation, 25 species are included in some category of threat in the lists of threatened species with global extinction (Handbook of the Birds of the World & BirdLife International, 2020); of these, four are classified as "Endangered" and "Critically Endangered". In the National territory (ICMBio, 2014), three and two species were classified as "Endangered" and "Critically Endangered", respectively. In the global and national lists, 22 and 13 species are considered "Near Threatment", respectively. In addition, 13 species are inserted in the category "Data Deficient", which reinforces the unknown situation of their populations that are possibly subject to numerous types of threats.
The number of species listed here for the Pantanal wetland represents 32% of all avifauna known to the Brazilian territory (Pacheco et al., 2021). In the present study, 153 species were addrd to the previous list proposed by Tubelis & Tomas (2003a). This reflects the importance of the biome, as part of the national terri- Table 1. Main list of bird species occurring in the Pantanal, Brazil. Taxa highlighted in square brackets are on the secondary list and lack adequate supporting documentation. Conservation status: * (globally declining population), NT (Near Threatened with extinction), VU (Vulnerable), EN (Endangered), CR (Critically Endangered), PE (Probably extinct), DD (Data Deficient), GL (Global List/Handbook of the Birds of the World & BirdLife International, 2020), BL (Brazilian List/ICMBio, 2014). Status of migration: INTRA (intracontinental migrant), INTER (intercontinental migrant). Evidence: ExM (specimen deposited in a national institutional museum and/or abroad), Rv/sP (visual and/or sound records quoted in a scientific journal), Rv/sNP (visual and/or sound records obtained by the authors and not published), FoI (photo published on the internet), FoAP (photo in particular collection); ASI (sound file available on the internet). tory, for the maintenance of a meaningful avifaunistic richness. The avifauna of this region can be considered quite rich compared to that found in other wetlands of the world, such as the Okavango Delta in Botswana with more than 450 species (Hancock et al., 2007) and the "Esteros del Iberá" in Argentina with 344 species (Giraudo et al., 2003). In Brazil, 373 species are listed in the Upper Paraná River floodplain (Paraná and Mato Grosso do Sul) alone (Gimenes et al., 2007), with an additional, 230 species (Pereira & Poerschke, 2010) listed in Lagoa do Peixe (Rio Grande do Sul).
The increasing advent of "Citizen Science" practices have made it possible to make an expressive contribution to everything that was previously known about the Pantanal avifauna, especially with the advent of digital platforms such as WikiAves and Xeno-Canto that have been fundamental in expanding knowledge and supporting documentation. However, it is emphasized that there are some limitations to the inadvertent use of this data, such as reliability in identification and inaccuracy of location, which need to be checked directly with the authors of the records. Despite notable advances in the knowledge of the composition of the Pantanal avifauna, there are great geographical gaps, notably in the regions of Cáceres, Paiaguás, and Chaco (Fig. 1), as evidenced in the studies by Frota et al. (2020b) and Fernandez-Arellano et al. (2021), who identified a series of locations with poorly sampling effort for the bird inventory.

Biogeographic affinities
The avifauna occurring in the Pantanal floodplain is composed mostly of species that are widely distributed in other South American phytogeographic provinces as well, such as the Cerrado and Chaco regions and, to a lesser extent, in the Amazon, Bosques Secos Chiquitanos, and Atlantic forests (Nunes & Tomas, 2004a). The similarities between the bird communities of the Pantanal region and the Cerrado region are to be expected as onethird of the Pantanal region is covered by the savanna phytophysiognomies (Ratter et al., 2003). Species with a wide distribution in the Cerrado region (Silva, 1995;Silva & Bates, 2002) such as Penelope ochrogaster, Uropelia campestris, Alipiopsitta xanthops, Saltatricula atricollis, and Basileuterus culicivorus are also widespread in the floodplain. The Chaco province enters a few kilometers in to Brazil, notably around the municipality of Porto Murtinho, in the southern part of the Pantanal region (Prado 1993a, b;Prado & Gibbs, 1993;Straube et al., 2006a), and the only species that can be considered endemic to this region is Saltatricula multicolor. However, there are some taxa, whose distribution is largely centered in the Upper Paraguay River Basin, notably in the lowland and western edge of the Pantanal, and which, in a way, can be considered typical of the Chaco region: Ortalis canicollis, Aratinga nenday, Nystalus striatipectus, Melanerpes cactorum, Celeus lugubris, Xiphocolaptes major, Paroaria coronata, and Microspingus melanoleucus.

Migration movement
Of the migratory species occurring in Brazil (Somenzari et al., 2018), at least a third use the Pantanal floodplain as a stopover or wintering site during migratory movements across the American continent to a greater or lesser extent. Waterfowl migratory displacements represent a significant portion of inter-and intracontinental migrants, which is expected for seasonally flooded environments (Oliveira, 2006;Donatelli et al., 2017). In this context, some anatids (Coscoroba coscoroba, Callonetta leucophrys, Anas bahamensis, Spatula platalea, Netta peposaca, and Oxyura vittata) stand out, which reproduce mainly in Rio Grande do Sul, southern Bolivia, and northwestern Argentina regions, then move to the floodplain of the Pantanal during the winter and spend the dry periods in southern South America . With regard to migrants dependent on aquatic habitats, sandpipers (genera Tringa and Calidris) stand out for their long-distance displacement from breeding areas in the tundra to wintering sites in Patagonia , therefore being the Pantanal mudflats habitats a very important stopover for Scolopacidae family (Serrano, 2010;Frota et al., 2020c). The occurrence of Nearctic migratory species, such as Numenius hudsonicus, Arenaria interpres, Calidris alba, C. pusilla, C. minutilla, C. bairdii, Xema sabini, Leucophaeus pipixcan, and Chlidonias niger, can be considered accidental since the Pantanal floodplain not usual route for these species (Serrano, 2010;Kantek & Onuma, 2013;Frota et al., 2020a). Antas et al. (2016) reported that young Rynchops niger birds banded in the SESC Pantanal in Barão de Melgaço (MT) were recaptured in the Mar Chiquita lagoon near Mar del Plata in Argentina, and in Lagoa do Peixe (Rio Grande do Sul). After the reproductive period, which coincides with the end of the rainy season, the population of Pheucticus aureoventris disperses from the Andes pre-mountain range to the Pantanal floodplain and surrounding plateaus from May to August (Nunes, 2008).
There is a great flow of migratory birds coming from the southernmost regions of South America, notably the seedeaters (Sporophila), to central and northern Brazil. Some species (S. hypoxantha, S. caerulescens, S. iberaensis, S. palustris, and S. ruficollis) reproduce in the hydromorphic fields in the southern regions of South America and appear in large numbers in the native fields of the Pantanal during the winter .
Migratory birds, notably northern ones, are among the main players involved in ecological processes of nutrient cycling and dispersion of important pathogens between the two continents (Kawamoto et al., 2005;Araújo et al., 2014).

Endangered species
According to the Handbook of the Birds of the World & BirdLife International (2020), 231 species occurring in the Pantanal region are experiencing population declines. However, most of them comprise common species with viable and vigorous populations in the floodplains, a fact that highlights the Pantanal region as an important biological refuge for birds in South America (Nunes, 2009). Of these, Rhea americana and Crax fasciolata are considered "Near Threatened" and "Vulnerable", respectively, at a global scale. Hasenclever et al. (2004) estimated 6,500 R. americana individuals across the Pantanal floodplain, whereas the estimated population ranged from 1 to 2 individuals per km² in western Nhecolândia (Gräbin et al., 2012). In turn, the density estimates of C. fasciolata in western Nhecolândia varied according to habitat, between 3 and 5 individuals per hectare in open and forested areas, respectively (Nunes, 2015).
In addition to deforestation and replacement of natural landscapes by cultivated pastures , extreme drought and fires (Marengo et al., 2021;Pivello et al., 2021) that have occurred in recent years have seriously threatened regional richness and diversity (Berlinck et al., 2021). The fires that occurred in the Pantanal region in 2020 destroyed 29% of the native vegetation; more than 4% of the burned area corresponded to conservation sites . Four million hectares of forest, cerrado, and savanna were burned, with the northern portion of the floodplain being the most affected by the fires . It is noteworthy that the region affected by the fires coincides with the refuges of large populations of two of the most threatened species occurring in the Pantanal floodplain: the Chestnut-bellied Guan (Penelope ochrogaster) and the Hyacinth Macaw (Anodorhynchus hyacinthinus). In addition, many migratory species, notably those dependent on native grasslands habitats such as most seedeaters , were also affected by the loss of feeding sites due to these fires. Based on the type of habitat they explore and nesting sites, it is speculated that more than half of the bird species that occur in the Pantanal may have had their populations affected to a higher or lower extent by the fires. However, the effects of these events on populations of endangered, migrant, and even common species in the Pantanal are still unknown. Considering the future scenario of climate change, the traditional and sustainable management of the Pantanal, sustainable fire management, and maintenance of the mosaic and spatial arrangement of the landscape units intact and continuous is essential to maintain the diversity in this unique and fragile ecosystem.