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Bird checklist and contributions to conservation of the Atlantic forest-cerrado ecotone in Três Lagoas municipality, Brazil

Abstract

Although Três Lagoas municipality is located in a rare and highly fragmented Atlantic Forest-Cerrado ecotone, there is scarcity of biodiversity data to guide conservation decisions. Therefore, this study aimed to compile the first bird checklist in 31 localities in this municipality to propose conservation strategies based on avian richness, conservation and migratory status. A total of 419 bird species were recorded, of which 412 were exclusive to the Atlantic Forest-Cerrado ecotone and seven to the Cerrado domain (C. minor, L. xenopterus, P. unicinctus, T. curucui, S. pileata, S. melanopis and S. luteola). According to the results, 12 species are included in the Near Threatened category, four are vulnerable (C. fasciolata, L. xenopterus, A. tricolor and S. hypoxantha) and one is endangered (U. coronata). Regarding migratory birds, 112 were recorded (95 intracontinental, 17 intercontinental). Since the majority of these species are recorded in grasslands, aquatic habitats and Seasonal Deciduous Alluvial Forest, they necessarily have highest priority for conservation and restoration. Thus, we recommend that: (1) areas 2, 11 and 24 be considered as both Important Bird Area and “Area de Proteção Ambiental”; (2) riparian forest restoration along the Paraná river act as a local ecological corridor among these areas, allowing the recolonization, genetic exchange and restoration of locally reduced populations of migratory and near/threatened bird species.

Keywords
Avifauna; Conservation policies; Neotropical environments; Restoration

INTRODUCTION

Três Lagoas municipality (TLM) stands out for its extensive economic growth in recent years (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
), mainly due to the increased number of industries locally installed (Tisott et al., 2017Tisott, S.T.; Schmidt, V. & Waquil, P.D. 2017. Atividade florestal e o desenvolvimento socioeconômico em Três Lagoas e região: uma análise baseada na abordagem de cluster. Desenvolvimento em Questão, 15(38): 228-260. https://doi.org/10.21527/2237-6453.2017.38.228-260.
https://doi.org/10.21527/2237-6453.2017....
). This high number of industries made TLM one of the world’s largest centers of pulp for paper production (Mendonça et al., 2020Mendonça, M.R.; Teixeira, J.C; Freitas Mariano, A.J. & Medeiros, G.N. 2020. O município de Três Lagoas/MS como maior produtor/exportador de celulose do mundo: a ideologia do progresso e suas contradições. Caderno Prudentino de Geografia, 3(42): 50-76.). The region is attractive because it is located at the junction of some of the main roads, rivers and rail networks in Brazil (SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
). Therefore, it is believed that this municipality will continue to grow exponentially, both economically and demographically (IBGE, 2022Instituto Brasileiro de Geografia e Estatística (IBGE). 2022. Instituto Brasileiro de Geografia e Estatística. Available: Available: https://www.ibge.gov.br . Access: 21/06/2022.
https://www.ibge.gov.br...
), which in turn will impact the local landscape.

TLM is inserted in a region of ecological tension between the Atlantic Forest and the Cerrado domain. Thus, its growth must consider environmental policies aimed at conserving the local biota, since the Atlantic Forest and the Cerrado are two of the five hotspots and most threatened biomes on the planet, with a high number of endemic plant and vertebrate species (Myers et al., 2000Myers, N.; Mittermeier, R.A.; Mittermeier, C.G.; Fonseca, G.A. & Kent, J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403(6772): 853-858. https://doi.org/10.1038/35002501.
https://doi.org/10.1038/35002501...
). However, these biomes are extremely fragmented by pastures and monocultures in the northwest portion of the Atlantic Forest in the Alto Paraná ecoregion (Rodrigues & Bononi, 2008Rodrigues, J.H. & Bononi, V.L.R. 2008. Diretrizes para conservação e restauração da biodiversidade no Estado de São Paulo. 2. ed. São Paulo, Secretaria do Meio Ambiente. 248p.; Uezu & Metzger, 2016Uezu, A. & Metzger, J.P. 2016. Time-Lag in Responses of Birds to Atlantic Forest Fragmentation: Restoration Opportunity and Urgency. PLoS One, 11(1): e0147909. https://doi.org/10.1371/journal.pone.0147909.
https://doi.org/10.1371/journal.pone.014...
), especially the Seasonal Deciduous Alluvial Forest along the Paraná River, which has the most threatened Atlantic Forest phytophysiognomy, with only 1% of the remaining forest (Fundação Ipardes, 1992Fundação Ipardes. 1992. Diagnóstico para a implantação de políticas para o setor florestal no Paraná. Curitiba, Fundação Ipardes. 48p.).

The studies of avifauna in the Mato Grosso do Sul state (MGS) have always focused on the western region, that is, the Pantanal domain due to its tourist structure and peculiar biome (Nunes et al., 2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
). This justifies why historically there were rare significant bird expeditions to TLM. Cypsnagra hirundinacea was the first bird collected in TLM by J. Steinbach (Museum of Comparative Biology, Harward University) in 1918. There were two main expeditions to collect birds in TLM: a) in 1931 by the Museum of Comparative Biology and; b) in 1936 by the Field Museum of Natural History (https://vertnet.org). The closest historical expedition to TLM was carried out at “Fazenda Capão Bonito” (Sidrolândia municipality) in 1937 by Emmet Blake, who collected several bird specimens now deposited at the Field Museum of Natural History in Chicago/USA (Straube, 2011Straube, F.C. 2011. A viagem de Emmet Blake ao Brasil (1937). Atualidades Ornitológicas , 164: 37-50.). The first scientific papers focused on birds in TLM were performed by Augusto João Piratelli (Piratelli et al., 2001Piratelli, A.J.; Melo, F.P.D. & Caliri, R.F. 2001. Dados morfométricos de aves de sub-bosque da região leste de Mato Grosso do Sul. Revista Brasileira de Zoologia, 18(2): 305-317. https://doi.org/10.1590/S0101-81752001000200001.
https://doi.org/10.1590/S0101-8175200100...
; Piratelli & Pereira, 2002Piratelli, A. & Pereira, M.R. 2002. Dieta de aves na região leste de Mato Grosso do Sul, Brasil. Ararajuba, 10(2): 131-139.; Piratelli, 2003Piratelli, A. 2003. Mesh size and bird capture rates in Mato Grosso do Sul State, Brazil. Brazilian Journal of Biology , 63(1): 105-111. https://doi.org/10.1590/S1519-69842003000100014.
https://doi.org/10.1590/S1519-6984200300...
; Piratelli & Blake, 2006Piratelli, A. & Blake, J.G. 2006. Bird communities of the southeastern Cerrado region, Brazil. Ornitología Neotropical, 17: 213-225.) and José Ragusa-Netto (Ragusa-Netto, 2002Ragusa-Netto, J. 2002. Fruiting phenology and consumption by birds in Ficus calyptroceras (Miq.) Miq. (Moraceae). Brazilian Journal of Biology , 62(2): 339-346. https://doi.org/10.1590/S1519-69842002000200018.
https://doi.org/10.1590/S1519-6984200200...
). In the last two decades, many excursions and studies have been performed by us in several environments in TLM. However, there is no bird checklist compilation regarding the species found in this municipality up to now.

The strategy of providing a list of species is the first step toward conservation efforts, being highly recommended by the Chico Mendes Institute for Biodiversity Conservation (ICMBio, 2013Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2013. Aplicação de citérios e categorias da UICN na Avaliação da Fauna Brasileira. Brasília, MMA. 45p.). In addition, the avifauna can be used as a bioindicator of environmental changes, since it can be found at different trophic levels, constitutes one of the most studied groups of vertebrates and is extremely sensitive to environmental disturbances (Bierregaard et al., 1992Bierregaard, J.R.; Lovejoy, T.E.; Kapos, V.; Dos Santos, A.A. & Hutchings, R.W. 1992. The biological dynamics of tropical rainforest fragments. Biological Science, 412(11): 859-866. https://doi.org/10.2307/1312085.
https://doi.org/10.2307/1312085...
; Stotz et al., 1996Stotz, D.F.; Fitzpatrick, J.W.; Parker III, T.A. & Moskovits, D.K. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. 478p.). Thus, it is important to observe some patterns in bird communities in order to predict the impact that past improper land use had on natural environments and make efforts towards their restoration and conservation (Sodhi et al., 2011Sodhi, N.S.; Sekercioglu, C.H.; Barlow, J. & Robinson, S.K. 2011. Conservation of tropical birds. Nova Jersey, John Wiley & Sons. 312p.). Although Nunes et al. (2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) highlight the main historical excursions of ornithologists and collectors to the state of MGS, none is focused on the territory of the municipalities. In fact, Brazilian bird checklists usually do not cover all the municipality area, but particular areas or environments, as is the case of the studies conducted by Pivatto et al. (2006Pivatto, M.A.; Manco, D.D.; Straube, F.C.; Urben-Filho, A. & Milano, M. 2006. Aves do Planalto da Bodoquena, Estado do Mato Grosso do Sul (Brasil). Atualidades Ornitológicas , 129: 1-26.), Simpson et al. (2012Simpson, R.; Cavarzere, V. & Simpson, E. 2012. List of documented bird species from the municipality of Ubatuba, state of São Paulo, Brazil. Papéis Avulsos de Zoologia , 52(21): 233-254. https://doi.org/10.1590/S0031-10492012002100001.
https://doi.org/10.1590/S0031-1049201200...
), Lees et al. (2013Lees, D.; Sherman, C.D.; Maguire, G.S.; Dann, P.; Cardilini, A. & Weston, M.A. 2013. Swooping in the suburbs; parental defense of an abundant aggressive urban bird against humans. Animals, Basel, 3(3): 754-766. https://doi.org/10.3390/ani3030754.
https://doi.org/10.3390/ani3030754...
), Corrêa & De Mello (2013Corrêa, L.L.C. & De Mello, L.M. 2013. Update the diversity of birdlife in the municipality of Bagé, region campaign, Rio Grande do Sul, Brazil. Revista Eletrônica de Gestão em Educação e Tecnologia, 17: 3215-3229. https://doi.org/10.5902/223611709303.
https://doi.org/10.5902/223611709303...
) and Schunck et al. (2019Schunck, F.; Silveira, L.F. & Nascimento, V.S. 2019. 118 years of ornithological knowledge of a forgotten region of the Atlantic Forest near the largest city in South America. Wilson Journal of Ornithology, 131(4): 758-773. https://doi.org/10.1676/1559-4491-131.4.758.
https://doi.org/10.1676/1559-4491-131.4....
), making it difficult to outline conservation strategies through municipal policies.

Therefore, in the present study we provide the first bird checklist for Três Lagoas municipality, including all of its environments, in addition to discussing conservation strategies for this region based on bird richness and status of conservation and migration.

MATERIAL AND METHODS

Area of study

TLM is located in the sedimentary plateau of the Paraná River Basin with predominantly sandy soils. Its area comprises 10.206,949 km² (20°45′04″S and 51°40′42″W) (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
; SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
) and it is under the influence of a tropical savanna climate (Aw), according to the Köppen-Geiger classification (Peel et al., 2007Peel, M.C.; Finlayson, B.L. & McMahon, T.A. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth System Science, 11(5): 1633-1644. https://doi.org/10.5194/hess-11-1633-2007.
https://doi.org/10.5194/hess-11-1633-200...
), with an annual mean temperature of 26℃. The total annual rainfall is between 900 mm and 1.400 mm/year, with a rainy season during the summer and a dry season during the winter (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
). Although located mainly in the Cerrado domain, TLM contains a Cerrado-Atlantic Forest ecotone area. In fact, the municipality of TLM is characterized by the presence of Atlantic Forest strips arranged perpendicularly in relation to the banks of the Paraná River (Fig. 1). These strips alternate with the Cerrado vegetation until they narrow and disappear as they move away from the river towards the northwest portion of TLM, which is exclusively covered by the Cerrado vegetation (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
). As a result, these aspects create high biodiversity in this region. However, its environments have been largely modified, initially due to beef cattle production, and from the year 2000 onwards, due to extensive eucalyptus plantations (SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
). In particular, the areas of the Semideciduous Atlantic Forests and Cerrado Forests (Cerradão) have been suppressed, resulting in few isolated and small remnants (SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
).

Figure 1
Três Lagoas Municipality map, Atlantic forest-cerrado ecotone and survey and localities (1-31).

According to Fig. 1, the descriptions of all 31 studied areas are: 1=Lakes, Semideciduous Atlantic Forest and Cerradão Forest of Três Lagoas municipality (urban environment) - 20°47′03.08″S, 51°42′42.76″W; 2=Semideciduous Atlantic Forest, including the Seasonal Deciduos Alluvial Atlantic Forest of the Parque Natural Municipal das Capivaras - 20°44′48.15″S, 51°39′25.76″W; 3=Semideciduous Atlantic Forest, including the Seasonal Deciduous Alluvial Atlantic Forest: 20°37′42.08″S, 51°37′39.81″O; 4=Cerradão Forest in the interchange with Inocência municipality - 20°38′59.65″S, 51°45′05.24″W; 5=Cerradão Forest, riparian forest and grassland - 20°47′08.30″S, 51°47′23.92″W; 6=Semideciduous Atlantic Forests, Cerradão, riparian forest, wet grassland and Vereda of Suzano Papel e Celulose - 20°59′17.22″S, 51°46′55.66″W; 7=Riparian forest and grassland of the Água Tirada stream - 20°31′22.13″S, 51°58′23.91″W; 8=Riparian forest and grassland of the Pinto stream - 20°43′21.82″S, 51°46′42.76″W; 9=Semideciduous Atlantic Forest, including the Seasonal Deciduos Alluvial Atlantic Forest of the Paraná River - 21°05′04.02″S, 51°54′00.75″W; 10=Cerradão Forest, Brazilian savanna and riparian forest of the Parque Natural Municipal do Pombo - 20°21′23.16″S, 52°37′53.20″W; 11=Semideciduous Atlantic Forest, including the Seasonal Deciduos Alluvial Atlantic Forest of Cargill - 20°50′29.45″S, 51°42′22.16″W; 12=Open grassland of Petrobras UFN3 - 20°59′31.23″S, 51°53′22.60″W; 13=Semideciduous Atlantic and riparian forests of Eldorado Brasil Celulose - 20°35′56.77″S, 51°37′31.01″W; 14=Brazilian savanna and riparian forest of the Crioulinho Arapuá stream - 20°42′11.83″S, 52°06′54.97″W; 15=Cerradão forest at the SP 158 Sucuriú road - 20°41′01.40″S, 51°46′30.71″W; 16=Brazilian savanna and riparian forest of the Bebedouro stream - 20°27′42.43″S, 51°50′25.43″W; 17=Brazilian savanna of the SITREL - 20°47′12.81″S, 51°51′29.33″W; 18=Brazilian savana and riparian forest of the CTR Buriti - 20°35′39.84″S, 52°25′43.21″W; 19=Riparian forest of the Curtume of Três Lagoas municipality - 20°51′34.09″S, 51°45′05.08″W; 20=Cerradão and riparian forests of Fazenda Rio Verde - 20°54′44.9″S, 52°11′58.5″W; 21=Brazilian savanna and riparian forest of the Palmito stream - 20°54′17.5″S, 51°45′40.9″W; 22=Cerradão Forest and Brazilian savanna of Fazenda Primavera - 20°36′16.7″S, 51°48′23.8″W; 23=Cerradão Forest and Brazilian savanna of Fazenda Paranoá - 20°38′18.9″S, 51°41′18.4″W; 24=Semideciduous Atlantic Forest of APA Jupiá - 20°47′18.4″S, 51°39′21.7″W; 25=Brazilian savanna and open grassland close to MS road - 20°43′14″S, 51°44′55″W; 26=Brazilian savanna, open grassland and small patches of the riparian forest of the Verde River - 20°55′38″S, 52°19′57″W; 27=Cerradão Forest of Fazenda Vista Alegre - 20°27′02″S, 52°14′11″W; 28=Cerradão Forest and wet grassland of Fazenda Mata Verde - 19°38′04.47″S, 52°25′19.36″W; 29=Cerradão Forest of Fazenda Santa Izabel - 19°36′45.37″S, 52°28′47.76″W; 30=Cerradão Forest, Brazilian savanna, riparian forest of the Ribeirão Imbaúva stream and wet grassland of Fazenda Santa Vitória, Embay and Timbaí and 31=Brazilian savanna and Cerradão Forest of Fazenda Serrinha - 20°37′16.42″S, 52°15′23.27″W.

Bird survey

A total of 31 areas (see above), including all the environments found in TLM, were surveyed, namely, urban environments, open and/or wet grasslands, Brazilian savanna (Cerrado sensu stricto), and Cerradão, riparian and semideciduous Atlantic forests.

For the elaboration of the consolidated list of birds found in TLM (Table 1), we adopted the method described by Nunes et al. (2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) with some modifications. We considered the records made by the authors’ fieldwork from 2007 to 2022 (Rv/sNP followed by the authors’ initials) derived from transections surveys. We also collected records available in the literature (Rv/sP), such as the studies conducted by: Piratelli et al. (2001Piratelli, A.J.; Melo, F.P.D. & Caliri, R.F. 2001. Dados morfométricos de aves de sub-bosque da região leste de Mato Grosso do Sul. Revista Brasileira de Zoologia, 18(2): 305-317. https://doi.org/10.1590/S0101-81752001000200001.
https://doi.org/10.1590/S0101-8175200100...
); Ragusa-Netto (2002Ragusa-Netto, J. 2002. Fruiting phenology and consumption by birds in Ficus calyptroceras (Miq.) Miq. (Moraceae). Brazilian Journal of Biology , 62(2): 339-346. https://doi.org/10.1590/S1519-69842002000200018.
https://doi.org/10.1590/S1519-6984200200...
); Piratelli & Pereira (2002Piratelli, A. & Pereira, M.R. 2002. Dieta de aves na região leste de Mato Grosso do Sul, Brasil. Ararajuba, 10(2): 131-139.); Piratelli (2003Piratelli, A. 2003. Mesh size and bird capture rates in Mato Grosso do Sul State, Brazil. Brazilian Journal of Biology , 63(1): 105-111. https://doi.org/10.1590/S1519-69842003000100014.
https://doi.org/10.1590/S1519-6984200300...
) and Piratelli & Blake (2006Piratelli, A. & Blake, J.G. 2006. Bird communities of the southeastern Cerrado region, Brazil. Ornitología Neotropical, 17: 213-225.); Godoi et al. (2011Godoi, M.N.; Capek, M.; Pivatto, M.A.C.; Literak, I. & Kokes, J. 2011. Masked Tityra in Mato Grosso do Sul. Revista Brasileira de Ornitologia , 19(3): 428-433., 2012aGodoi, M.N.; Costacurta, M.D.B.; Nunes, A.P.; Patrial, E.W. & Morante-Filho, J.C. 2012a. Primeiros registros da maria-preta-de-penacho (Knipolegus lophotes, Tyrannidae) no estado de Mato Grosso do Sul, Brasil. Biota Neotropica, 12(3): 311-314. https://doi.org/10.1590/S1676-06032012000300030.
https://doi.org/10.1590/S1676-0603201200...
, bGodoi, M.N.; Morante-Filho, J.C.; Faxina, C.; Modena, E.S.; Pivatto, M.A.C.; Manço, D.D.G. & Stavis, V.K. 2012b. Aves de rapina raras no estado de Mato Grosso do Sul. Atualidades Ornitológicas, 170: 41-47., 2013Godoi, M.N.; Morante-Filho, J.C.; Módena, E.S.; Faxina, C.; Tizianel, F.A.T.; Bocchese, R.; Pivatto, M.A.C.; Nunes, A.P. & Posso, S.R. 2013. Birds of Upper Paraná River Basin in the State of Mato Grosso do Sul, Brazil. Revista Brasileira de Ornitologia , 21(3): 176-204.), Previatto et al. (2013Previatto, D.M.; Mizobe, R.S. & Posso, S.R. 2013. Birds as potential pollinators of the Spathodea nilotica (Bignoniaceae) in the urban environment. Brazilian Journal of Biology , 73(4): 737-741. https://doi.org/10.1590/S1519-69842013000400008.
https://doi.org/10.1590/S1519-6984201300...
) and Gabriel & Godoy (2019Gabriel, V.A. & Godoy, F.I. 2019. Comunidade de aves em um mosaico de Eucalyptus e vegetação nativa em Três Lagoas, MS, Brasil. Oecologia Australis, 23(3): 403-431. https://doi.org/10.4257/oeco.2019.2303.02.
https://doi.org/10.4257/oeco.2019.2303.0...
). However, we did not consider Campylopterus largipennis recorded by Previatto et al. (2013Previatto, D.M.; Mizobe, R.S. & Posso, S.R. 2013. Birds as potential pollinators of the Spathodea nilotica (Bignoniaceae) in the urban environment. Brazilian Journal of Biology , 73(4): 737-741. https://doi.org/10.1590/S1519-69842013000400008.
https://doi.org/10.1590/S1519-6984201300...
) due to its restricted distribution in the northern region of the Amazon Forest. In addition, we also took into account the photographic and sound information (FSI) available until August 2022 on WikiAves (https://www.wikiaves.com), Xeno-canto (https://www.xeno-canto.org), eBird (https://ebird.org), iNaturalist (https://www.inaturalist.org), Macaulay library (https://www.macaulaylibrary.org) and GBIF (https://www.gbif.org). We also consulted the Vertnet library (https://vertnet.org) to include species collected in TLM by museums. Thus, we included each species in a list composed of species with at least one occurrence in TLM, along with documentary evidence, that is, published papers and item(s) available for independent consultation in the form of a complete or partial specimen, photograph, audio or video recording, which allowed us to safely and indisputably determine the species. In this context, the filtering protocol is the detailing of information referring to the record, coherently associated with the species distributional and dispersion patterns established based on documentary evidence.

Table 1
List of bird species in Três Lagoas municipality/MS. Captions: a=Intracontinental migrant; aa=Intracontinental waterfowl migrant; b=Intercontinental migrant; bb=Intercontinental waterfowl migrant; 1=Globally Near Threatened; 2=Data Deficient in Brazil and Globally Near Threatened; 3=Globally Vulnerable; 4=Data Deficient in Brazil and Globally Vulnerable; 5=Data Deficient in Brazil; 6=Near Threatened in Brazil; 7=Near Threatened in Brazil and globally; 8=Endangered in Brazil and globally; 9=Vulnerable in Brazil; FSI=photo and/or song published on the internet; Rv/sP=visual and/or sound records quoted in a publication; Rv/sNP=visual and/or sound records obtained by the authors: SRP=Sérgio R. Posso; MNG=Maurício N. Godoi; VAG=Vagner de A. Gabriel; FIG=Fernando Igor de Godoy; LPS=Lys P. de Souza); CF=Claudenice Faxina; MAVV=Marcelo Alejandro Villegas Vallejos and LAC=Luiz Arthur C. Cintra.

We adopted the taxonomic classification and bird vernacular names proposed by the Brazilian Ornithological Records Committee (CBRO) (Pacheco et al., 2021Pacheco, J.F.; Silveira, L.F.; Aleixo, A.; Agne, C.E.; Bencke, G.A.; Bravo, G.A.; Brito, G.R.R.; Cohn-Haft, M.; Maurício, G.N.; Naka, L.N.; Olmos, F.; Posso, S.R.; Lees, A.C.; Figueiredo, L.F.A; Carrano, E.; Guedes, R.C.; Cesari, E.; Franz, I.; Schunck, F. & de Piacentini, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. 2.ed. Ornithogical Research, 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x.
https://doi.org/10.1007/s43388-021-00058...
).

The species were divided into four categories according to their conservation status based on the global (IUCN, 2022International Union for Conservation of Nature and Natural Resources (IUCN). 2022. The IUCN Red List of threatened species, version 2022. Available: Available: https://www.iucnredlist.org . Access: 24/05/2022.
https://www.iucnredlist.org...
) and national (ICMBio, 2022Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2022. Livro Vermelho da Fauna Ameaçada de Extinção. Aves. Brasília, ICMBio/MM. v. 2, 709p.) lists of threatened species, namely, Near Threatened, Vulnerable, Endangered and Critically Endangered.

We considered the migratory status following the migratory bird lists for the state of MGS (Nunes et al., 2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) and the Brazilian territory (Somenzari et al., 2018Somenzari, M.; Amaral, P.P.D.; Cueto, V.R.; Guaraldo, A.D.C.; Jahn, A.E.; Lima, D.M.; Lima, P.C.; Lugarini, C.; Machado, C.G.; Martinez, J.; Nascimento, J.L.X; Pacheco, J.F; Paludo, D.; Prestes, N.P; Serafini, P.P.; Silveira, L.F; Sousa, A.E.B.A; Sousa, N.A.; Souza, M.A; Telino-Júnior, W.R & Whitney, B.M. 2018. An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia , 58(3): 1-66. https://doi.org/10.11606/1807-0205/2018.58.03.
https://doi.org/10.11606/1807-0205/2018....
). In addition, the species were distinguished between intercontinental and intracontinental migrants. In the intercontinental category, we included species that perform large displacements from the Northern Hemisphere (Canada and northern United States) to southern South America (until Patagonia), while in the intracontinental category we considered species that move from the southernmost portions of South America to the northernmost regions (mainly the Amazon basin) and vice-versa.

RESULTS

According to our list compilation, the avifauna of TLM is composed of 419 species. We recorded an overall number of 412 species in the Atlantic Forest-Cerrado ecotone (all areas except 7, 10, 14, 16, 18, 20, 26-31; Fig. 1 and Table 1) and seven only in the Cerrado domain (P. unicinctus and T. curucui in area 10; S. pileata, S. melanopis and S. luteola in area 18 and C. minor and L. xenopterus in area 30 (Table 1)). The bird richness in the areas varies from 50 to 250 species recorded. The exceptions are areas 2 and 6, where we recorded more than 300 species (Table 1).

Seventeen species are included in some categories of conservation status in global and/or national lists of endangered species. The majority, in contrast, is included in the Near Threatened category (R. americana, P. superciliaris, S. papa, S. ornatus, A. xanthops, A. aestiva, A. auricapillus, P. maracana, P. pectoralis, C. eucosma and N. fasciata), while four are in the Vulnerable category (C. fasciolata, L. xenopterus, A. tricolor and S. hypoxantha) and only one is in the Endangered category (U. coronata). We gathered evidence of 11 species categorized at some level of threat in areas 2, 6, 8, 10 and 12, particularly 2 and 10, with eight and ten species, respectively (Table 1). We also recorded 10 near threatened or threatened species in grassland regions (areas 7, 8, 10 and 12): R. americana, S. papa, A. xanthops, N. fasciata, P. pectoralis, S. pileata, C. eucosma, L. xenopterus, A. tricolor and S. hypoxantha.

Our list comprises 112 migratory birds recorded mainly in areas 2, 3, 11, 13 and 19 (87, 63, 46, 42 and 39 species, respectively) (Table 1). Most species (96) are intracontinental migrants, whereas 15 are intercontinental migrants (C. americanus, C. minor, P. dominica, B. longicauda, T. flavipes, T. solitaria, C. fuscicollis, A. macularius, P. haliaetus, E. forficatus, P. subis, R. riparia, H. rustica, P. pyrrhonota and C. fuscescens). A total of 29 species are aquatic migratory birds, of which most (23) are intracontinental migrants, whereas six are intercontinental migrants (P. dominica, B. longicauda, T. flavipes, T. solitaria, C. fuscicollis and A. macularius). The non-aquatic migratory species belong mainly to the Tyrannidae family (23 species) and to the Sporophila genus (S. lineola, S. plumbea, S. caerulescens, S. leucoptera, S. pileata, S. hypoxantha and S. bouvreuil).

DISCUSSION

The number of bird species recorded in TLM represents 61% of all known avifauna of MGS (n=679) (Nunes et al., 2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) and 21% (n=1971) of the Brazilian territory (Pacheco et al., 2021Pacheco, J.F.; Silveira, L.F.; Aleixo, A.; Agne, C.E.; Bencke, G.A.; Bravo, G.A.; Brito, G.R.R.; Cohn-Haft, M.; Maurício, G.N.; Naka, L.N.; Olmos, F.; Posso, S.R.; Lees, A.C.; Figueiredo, L.F.A; Carrano, E.; Guedes, R.C.; Cesari, E.; Franz, I.; Schunck, F. & de Piacentini, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. 2.ed. Ornithogical Research, 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x.
https://doi.org/10.1007/s43388-021-00058...
). This high bird richness in the TLM territory can be attributed to: (1) the Atlantic Forest-Cerrado ecotone, which has a high number of small patches with different vegetation and environments (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
); (2) the high heterogeneity of aquatic environments in the upper Paraná River floodplain and the TLM territory (SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
); and (3) the two South American migratory routes in the TLM territory (Stotz et al., 1996Stotz, D.F.; Fitzpatrick, J.W.; Parker III, T.A. & Moskovits, D.K. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. 478p.).

According to Bierregaard et al. (1992Bierregaard, J.R.; Lovejoy, T.E.; Kapos, V.; Dos Santos, A.A. & Hutchings, R.W. 1992. The biological dynamics of tropical rainforest fragments. Biological Science, 412(11): 859-866. https://doi.org/10.2307/1312085.
https://doi.org/10.2307/1312085...
), birds are sensitive to environmental disturbances and can be found at different trophic levels. Thus, as the patterns observed in bird communities can predict the impact that past improper land use had on natural environments, they can be used as bioindicators of these environmental changes (Sodhi et al., 2011Sodhi, N.S.; Sekercioglu, C.H.; Barlow, J. & Robinson, S.K. 2011. Conservation of tropical birds. Nova Jersey, John Wiley & Sons. 312p.). In this context, we found 10 near threatened or threatened species in grassland. All of them are considered rare in the Atlantic Forest-Cerrado ecotone of MGS (Godoi et al., 2013Godoi, M.N.; Morante-Filho, J.C.; Módena, E.S.; Faxina, C.; Tizianel, F.A.T.; Bocchese, R.; Pivatto, M.A.C.; Nunes, A.P. & Posso, S.R. 2013. Birds of Upper Paraná River Basin in the State of Mato Grosso do Sul, Brazil. Revista Brasileira de Ornitologia , 21(3): 176-204.), except for R. americana and A. xanthops. The importance of this ecotone was highlighted for some threatened and migratory species (mentioned bellow), however, two near threatened birds were also recorded in this environment, i.e., P. pectoralis and N. fasciata. The latter is endemic to the Cerrado and needs grasslands with sparse trees (Brazilian savanna or Cerrado sensu stricto) (Sick, 2001Sick, H. 2001. Ornitologia brasileira. Rio de Janeiro, Editora Nova Fronteira. 862p.). Unfortunately, savannas and grasslands are two of the most impacted environments by agriculture in Brazil (Foley et al., 2005Foley, J.A.; Asner, R.D.G.; Barford, C.; Bonan, G.; Carpenter, S.R.; Chapin, F.S.; Coe, M.T.; Daily, G.C.; Gibbs, H.K.; Helkowski, J.H.; Holloway, T.; Howard, E.A.; Kucharik, C.J.; Monfreda, C.; Patz, J.A.; Prentice, I.C.; Ramankutty, N. & Snyder, P.K. 2005. Global consequences of land use. Science, 309(5734): 570-574. https://doi.org/10.1126/science.1111772.
https://doi.org/10.1126/science.1111772...
). Nunes et al. (2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) also included many other threatened grassland bird species found in MGS, but some might have gone locally extinct in TLM, such as T. nanus, N. minor, G. poeciloptera, C. melanotis, S. nigrorufa and S. cinnamomea. Given the high number of grassland migrants, near threatened or threatened grassland species and local extinctions, it becomes clear that the grasslands of TL M(7, 8, 10 and 12 areas, Fig. 1) deserve more attention in terms of conservation policies developed by local (SEMEA - Secretariat of Environment and Agribusiness of Três Lagoas) and federal agencies (IBAMA - Brazilian Institute of Environment and Renewable Natural Resources). Area 10, for example, is now protected by SEMEA, which created the “Parque Natural Municipal do Pombo” in 2019 (SEMEA, 2019Secretaria Municipal de Meio Ambiente e Agronegócio (SEMEA). 2019. Plano de Manejo. Parque Natural Municipal do Pombo. Organização de Flávio Henrique Fardin. Três Lagoas-MS, 109p. https://www.treslagoas.ms.gov.br/plano-de-manejo-e-executado-no-parque-do-pombo.
https://www.treslagoas.ms.gov.br/plano-d...
). However, we still recommend protective and restoration measures for the other aforementioned grass land areas.

According to Stotz et al. (1996Stotz, D.F.; Fitzpatrick, J.W.; Parker III, T.A. & Moskovits, D.K. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. 478p.), 230 species of birds migrate in South America, most of them from southern portions of South America to Central Brazil and the Amazon basin. Somenzari et al. (2018Somenzari, M.; Amaral, P.P.D.; Cueto, V.R.; Guaraldo, A.D.C.; Jahn, A.E.; Lima, D.M.; Lima, P.C.; Lugarini, C.; Machado, C.G.; Martinez, J.; Nascimento, J.L.X; Pacheco, J.F; Paludo, D.; Prestes, N.P; Serafini, P.P.; Silveira, L.F; Sousa, A.E.B.A; Sousa, N.A.; Souza, M.A; Telino-Júnior, W.R & Whitney, B.M. 2018. An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia , 58(3): 1-66. https://doi.org/10.11606/1807-0205/2018.58.03.
https://doi.org/10.11606/1807-0205/2018....
) listed 198 migratory species in the Brazilian territory, which corresponds to 10% of all species in the country (Pacheco et al., 2021Pacheco, J.F.; Silveira, L.F.; Aleixo, A.; Agne, C.E.; Bencke, G.A.; Bravo, G.A.; Brito, G.R.R.; Cohn-Haft, M.; Maurício, G.N.; Naka, L.N.; Olmos, F.; Posso, S.R.; Lees, A.C.; Figueiredo, L.F.A; Carrano, E.; Guedes, R.C.; Cesari, E.; Franz, I.; Schunck, F. & de Piacentini, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. 2.ed. Ornithogical Research, 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x.
https://doi.org/10.1007/s43388-021-00058...
). Nevertheless, we found a high percentage of migrants in TLM (26%). Moreover, the 111 migratory birds recorded herein correspond to 56% of all Brazilian migratory species - a very high percentage considering the small territory of TLM (10.206 km²) in comparison with that of Brazil (8.547.403 km²) (IBGE, 2022Instituto Brasileiro de Geografia e Estatística (IBGE). 2022. Instituto Brasileiro de Geografia e Estatística. Available: Available: https://www.ibge.gov.br . Access: 21/06/2022.
https://www.ibge.gov.br...
). Most of these migrants are species that perform intracontinental displacements, using the region as a point of departure during their migrations across the South American continent (Anjos & Gimenes, 2005Anjos, L.E. & Gimenes, M.R. 2005. Avifauna. In: Vazzoler, A.E.; Agostinho A.A. & Hahn, N.S. A planície de inundação do alto rio Paraná: aspectos físicos, biológicos e socioeconômicos. Maringá, EDUEM/NUPELIA. p. 206-212.; Gimenes & Anjos, 2007Gimenes, M.R. & Anjos, L. 2007. Variação sazonal na sociabilidade de forrageamento das garças Ardea alba (Linnaeus, 1758) e Egretta thula (Molina, 1782) (Aves: Ciconiiformes) na planície alagável do alto rio Paraná, Brasil. Revista Brasileira de Ornitologia , 15(3): 409-416.). In fact, some species disperse from the Pre-Andes Mountains to the Pantanal and surrounding plateaus just after the reproductive period, which coincides with the end of the rainy season (Nunes et al., 2008Nunes, A.P.; da Silva P.A. & Tomas, W.M. 2008. New records to the checklist of birds from Pantanal, Brazil. Revista Brasileira de Ornitologia , 16(2): 160-164.), while others extend their migratory routes to the Paraná River basin (Faxina et al., 2010Faxina, C.; Fischer, E. & Benites, M. 2010. O rei-do-bosque vai além do Pantanal: registros de Pheucticus aureoventris (Cardinalidae) na bacia do Paraná. Revista Brasileira de Ornitologia, 18(4): 349-351.) where TLM is located. The species found in the southern areas of South America are mainly tyrannids and seedeaters (Sporophila) (Nunes et al., 2008Nunes, A.P.; da Silva P.A. & Tomas, W.M. 2008. New records to the checklist of birds from Pantanal, Brazil. Revista Brasileira de Ornitologia , 16(2): 160-164.), which corroborates the records in TLM. Some seedeaters appear in large numbers to breed in the hydromorphic grassland areas during the winter (Nunes et al., 2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
), except for S. lineola, which appears in Central Brazil in September and, after the reproductive period in January, leaves together with the juveniles, returning to the Amazon basin and the northern portion of South America (Nunes et al., 2008Nunes, A.P.; da Silva P.A. & Tomas, W.M. 2008. New records to the checklist of birds from Pantanal, Brazil. Revista Brasileira de Ornitologia , 16(2): 160-164.; Jaramilo & Kirwan, 2020Jaramilo, A. & Kirwan, G.M. 2020. Lined Seedeater (Sporophila lineola), version 1.0. In: Hoyo Del J et al. (Eds.). Birds of the World. Ithaca, Cornell Lab of Ornithology. Available: Available: https://doi.org/10.2173/bow.linsee1.01 . Access: 01/06/2022.
https://doi.org/10.2173/bow.linsee1.01...
).

In TLM there is also a high flow of migratory species dependent on aquatic environments, mainly from the Pantanal to the upper Paraná River floodplain (e.g., P. ajaja and R. niger), during the dry season (Nunes et al., 2008Nunes, A.P.; da Silva P.A. & Tomas, W.M. 2008. New records to the checklist of birds from Pantanal, Brazil. Revista Brasileira de Ornitologia , 16(2): 160-164.; Lima et al., 2022Lima, B.M.; Ragusa-Neto, J.; Donatelli, R.J. & Posso, S.R. 2022. Composition and spatio-temporal dynamics of aquatic bird community in humid areas of Alto Parana Atlantic Forest. Brazilian Journal of Biology, 84: e251438-10. https://doi.org/10.1590/1519-6984.251438.
https://doi.org/10.1590/1519-6984.251438...
). It is noteworthy that out of the 15 Northern Hemisphere migratory species recorded, six are waterfowls represented by species of the Order Charadriiformes (Pacheco et al., 2021Pacheco, J.F.; Silveira, L.F.; Aleixo, A.; Agne, C.E.; Bencke, G.A.; Bravo, G.A.; Brito, G.R.R.; Cohn-Haft, M.; Maurício, G.N.; Naka, L.N.; Olmos, F.; Posso, S.R.; Lees, A.C.; Figueiredo, L.F.A; Carrano, E.; Guedes, R.C.; Cesari, E.; Franz, I.; Schunck, F. & de Piacentini, V.Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee. 2.ed. Ornithogical Research, 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x.
https://doi.org/10.1007/s43388-021-00058...
). Lima et al. (2022Lima, B.M.; Ragusa-Neto, J.; Donatelli, R.J. & Posso, S.R. 2022. Composition and spatio-temporal dynamics of aquatic bird community in humid areas of Alto Parana Atlantic Forest. Brazilian Journal of Biology, 84: e251438-10. https://doi.org/10.1590/1519-6984.251438.
https://doi.org/10.1590/1519-6984.251438...
) studied aquatic birds in a small area very close to TLM (Castilho municipality and surroundings) and found a high richness of waterfowls (52 species). The authors attributed this richness to the high heterogeneity of local aquatic environments in the upper Paraná River floodplain, the habitat selection combined with seasonality, and the absence of other humid locations in the surroundings. Indeed, the upper Paraná River floodplain where TLM is located has three large rivers (Paraná, Sucuriú and Tietê), as well as several small aquatic environments, such as streams, lakes and ponds (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
; SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
), which partially explains the high richness of aquatic migratory birds recorded in our study. This great variety of aquatic habitats can also hold a high diversity of intracontinental and intercontinental aquatic migratory birds in TLM, which take two main migratory South American routes in the territory: Central Brazil and Central Amazon/Pantanal routes (Stotz et al., 1996Stotz, D.F.; Fitzpatrick, J.W.; Parker III, T.A. & Moskovits, D.K. 1996. Neotropical birds: ecology and conservation. University of Chicago Press. 478p.). All of these data highlight the importance of the TLM territory as an area that harbors these birds during their migratory movements in South America, making even more evident the necessity to develop conservation strategies for the aquatic environments of this municipality, especially area 2, which has the highest richness of migratory waterfowls.

The forests in TLM have been impacted by beef cattle production, irregular land occupation, dam construction, and unsustainable use of the native forest, which in turn has led to illegal hunting (SEMAC, 2011Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul (SEMAC). 2011. Secretaria de Estado de Meio Ambiente, do Planejamento, da Ciência e Tecnologia do Mato Grosso do Sul. Caderno SEMAC, 402p. https://www.imasul.ms.gov.br.
https://www.imasul.ms.gov.br...
; SEMADE, 2015Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico (SEMADE). 2015. Secretaria de Estado de Meio Ambiente e Desenvolvimento Econômico. Diagnóstico Socioeconômico de Mato Grosso do Sul. SEMADESC. https://www.semadesc.ms.gov.br/diagnostico-socioeconomico-de-ms-2015.
https://www.semadesc.ms.gov.br/diagnosti...
; Lima et al., 2022Lima, B.M.; Ragusa-Neto, J.; Donatelli, R.J. & Posso, S.R. 2022. Composition and spatio-temporal dynamics of aquatic bird community in humid areas of Alto Parana Atlantic Forest. Brazilian Journal of Biology, 84: e251438-10. https://doi.org/10.1590/1519-6984.251438.
https://doi.org/10.1590/1519-6984.251438...
). As a result, the forest formations (Atlantic Forest and Cerradão) are the most impacted habitats in TLM, which became isolated small patches. These large alterations in land cover reduces the number of forest habitats and change their configuration, affecting biodiversity, and consequently leading to species extinction (Hill & Curran, 2003Hill, J.L. & Curran, P.J. 2003. Area, shape and isolation of tropical forest fragments: effects on tree species diversity and implications for conservation. Journal of Biogeography, 30(9): 1391-1403. https://doi.org/10.1046/j.1365-2699.2003.00930.x.
https://doi.org/10.1046/j.1365-2699.2003...
). The isolation affects negatively the species persistence and decrease individual movements among habitat patches (Fahrig, 2003Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution and Systematics, 34: 487-515. https://doi.org/10.1146/annurev.ecolsys.34.011802.132419.
https://doi.org/10.1146/annurev.ecolsys....
; Fischer & Lindenmayer, 2007Fischer, J. & Lindenmayer, D.B. 2007. Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography, 16(3): 265-280. https://doi.org/10.1111/j.1466-8238.2007.00287.x.
https://doi.org/10.1111/j.1466-8238.2007...
). In fact, the small and isolated forest patches are strongly related to a decrease in animal population size, an interruption of gene flow and the probability of local extinctions (Temple & Cary, 1988Temple, S.A. & Cary, J.R. 1988. Modeling dynamics of habitat‐interior bird populations in fragmented landscapes. Biological Conservation, 2(4): 340-347. https://doi.org/10.1111/j.1523-1739.1988.tb00198.x.
https://doi.org/10.1111/j.1523-1739.1988...
), especially sensitive bird species (Martensen et al., 2012Martensen, A.C.; Ribeiro, M.C; Banks-Leite, C.; Prado, P.I. & Metzger, J.P. 2012. Associations of forest cover, fragment area and connectivity with Neotropical understory bird species richness and abundance. Conservation Biology, 26(6): 1100-1111. https://doi.org/10.1111/j.1523-1739.2012.01940.x.
https://doi.org/10.1111/j.1523-1739.2012...
). The bird checklist proposed by Nunes et al. (2022Nunes, A.P.; Straube, F.C.; Posso, S.R.; Laps, R.R.; Vasconcelos, M.F. de, Hoffmann, D.; Morante-Filho, J.C.; Donatelli, R.J.; Ragusa-Netto, J.; Faxina, C.; Godoi, M.N.; Urben-Filho, A.; Castro, S.L.R. de, Lopes, E.V.; Anjos, L. dos, Tomas, W.M.; Mendonça, L.B.; Silva, P.A.; Pivatto, M.A. de C.; Costacurta, M. de B.; Melo, A.V. de, Hass, A.; Braz, V. da S.; Módena, É. de S.; Freitas, G.O. de, Souza, R.A.D. de, Benites, M.; Mamede, S. & Menq, W. 2022. Checklist of the birds of Mato Grosso do Sul state, Brazil: diversity and conservation. Papéis Avulsos de Zoologia, 62(29): 3-34. https://doi.org/10.11606/1807-0205/2022.62.029.
https://doi.org/10.11606/1807-0205/2022....
) and the results of Emmet Blake’s visit in 1937 (Straube, 2011Straube, F.C. 2011. A viagem de Emmet Blake ao Brasil (1937). Atualidades Ornitológicas , 164: 37-50.) - the closest historical expedition to TLM (Fazenda Capão Bonito, Sidrolândia municipality) - lead us to suppose that many local extinctions of forest-dependent key species (e.g., T. solitarius, O. capueira, T. chrysochloros, N. swainsoni, R. vitellinus, C. lineata, C. campanisona, P. nudicollis, C. caudata, P. leucoptera and S. fuliginous) took place in TLM. As these species have large forest area needs (Sick, 2001Sick, H. 2001. Ornitologia brasileira. Rio de Janeiro, Editora Nova Fronteira. 862p.), the local extinctions probably occurred because of the disappearance of largest Atlantic Forest patches in the slopes and sides of the Paraná River due to flooding, leading to the construction of a dam for hydroelectric energy production (Jupiá Dam) in the ‘60s (Vianna, 2015Vianna, M.P. 2015. From Industrial Heritage to a Regional Development Core in the 20th Century: The Case of Ilha Solteira. Journal of Civil Engineering and Architecture, 9: 583-590. https://doi.org/10.17265/1934-7359/2015.05.010.
https://doi.org/10.17265/1934-7359/2015....
), together with irregular land occupation and illegal hunting in the region (Lima et al., 2022Lima, B.M.; Ragusa-Neto, J.; Donatelli, R.J. & Posso, S.R. 2022. Composition and spatio-temporal dynamics of aquatic bird community in humid areas of Alto Parana Atlantic Forest. Brazilian Journal of Biology, 84: e251438-10. https://doi.org/10.1590/1519-6984.251438.
https://doi.org/10.1590/1519-6984.251438...
). We still recorded four near threatened or threatened bird species in the Atlantic Forest-Cerrado ecotone (i.e., P. superciliaris, C. fasciolata, S. ornatus and P. maracana) that can be extinct in a few decades for the previously mentioned reasons - although the first two are common in the Atlantic Forest-Cerrado ecotone in MGS state (Godoi et al., 2013Godoi, M.N.; Morante-Filho, J.C.; Módena, E.S.; Faxina, C.; Tizianel, F.A.T.; Bocchese, R.; Pivatto, M.A.C.; Nunes, A.P. & Posso, S.R. 2013. Birds of Upper Paraná River Basin in the State of Mato Grosso do Sul, Brazil. Revista Brasileira de Ornitologia , 21(3): 176-204.).

These results lead to the conclusion that grasslands, aquatic habitats and the Semideciduous Atlantic Forest in TLM should be preserved and strong efforts should be addressed to restore those with some level of disturbance. Therefore, we believe that this list, which included endangered and migratory species, will be an important tool to guide public policies and conservation/restoration strategies in TLM.

The criteria for Important Bird Areas (IBAs) proposed by Bird Life International establish some bird conservation efforts (Develey, 2021Develey, P.F. 2021. Bird conservation in Brazil: challenges and practical solutions for a key megadiverse country. Perspectives in Ecology and Conservation, 19(2): 171-178. https://doi.org/10.1016/j.pecon.2021.02.005.
https://doi.org/10.1016/j.pecon.2021.02....
). According to this author, there are 237 IBAs in the Brazilian territory based on the following criteria: threatened species, endemism and congregatory species. We observed an overall number of 412 species in the Atlantic Forest-Cerrado ecotone, of which 16 are globally and/or nationally near threatened or threatened, four are vulnerable and one is endangered. Moreover, we recorded many endemic species in the Cerrado and the Atlantic Forest, in addition to a high richness of both migratory and congregatory species (dry and wet seasons). Thus, according to the criteria for IBAs and our results, we recommend the inclusion of a large Atlantic Forest-Cerrado ecotone area in TLM (areas 2, 11 and 24; Fig. 1) as an Important Bird Area (IBA). This recommendation can help TLM establish strategies and raise funds for the conservation of its birds and habitats. Additionally, most part of this ecotone is not under protection, except for the “Parque Natural Recantos das Capivaras” and Jupiá Park (areas 2 and 24, respectively), which are partially protected (up to 70 ha) by guidelines created by SEMEA. We also recommend political and scientific procedures in order to recognize this Atlantic Forest-Cerrado ecotone area as an Environmental Protection Area (APA=“Área de Proteção Ambiental”), according to the ICMBIO (2013Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2013. Aplicação de citérios e categorias da UICN na Avaliação da Fauna Brasileira. Brasília, MMA. 45p.) criteria. This ecotone is a large area with urban environments, including industries and fisherman villages, and the APA units exist to reconcile human occupation and sustainable use of natural resources (ICMBIO, 2013Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2013. Aplicação de citérios e categorias da UICN na Avaliação da Fauna Brasileira. Brasília, MMA. 45p.). The idea is the conservation of natural processes and biodiversity through guidance, development and adaptation of various human activities to the environmental characteristics of the area aiming at a sustainable development. The further positive benefit is that APAs can be implemented in areas of private and/or public domain by the Union, states or municipalities, without the need to expropriate private lands (ICMBIO, 2013Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). 2013. Aplicação de citérios e categorias da UICN na Avaliação da Fauna Brasileira. Brasília, MMA. 45p.). Furthermore, we also recorded three near threatened species in these areas, namely, A. auricapillus, A. xanthops and A. aestiva. They live in heterogeneous landscapes such as semi-open areas, but feed and rest in forest habitats (Collar et al., 1997Collar, N.J. 1997. Family Psittacidae (Parrots). In: Del Hoyo, J.; Elliot, A.E. & Sargatal, J. Handbook of the Birds of the World - Sandgrouse to cuckoos. Barcelona, Linx Edition. p. 280-477.). Therefore, the maintenance of forests also becomes essential for bird conservation since they provide them with resources, such as seeds and nesting cavities.

Additionally, we recommend the restoration of the riparian vegetation along the Paraná River that connects areas 2, 11 and 24 (Fig. 1). During the bird surveys, SRP observed that the riparian vegetation of the Paraná River between areas 2, 11 and 24 is partially fragmented with severe modifications caused by irregular and illegal human land occupation, mainly in the most threatened Atlantic Forest formation, the Seasonal Deciduous Alluvial Forest, with only 1% of the remaining (Fundação Ipardes, 1992Fundação Ipardes. 1992. Diagnóstico para a implantação de políticas para o setor florestal no Paraná. Curitiba, Fundação Ipardes. 48p.). This connectivity of riparian vegetation restoration among the forests patches will allow species movements (Fischer & Lindenmayer, 2007Fischer, J. & Lindenmayer, D.B. 2007. Landscape modification and habitat fragmentation: a synthesis. Global Ecology and Biogeography, 16(3): 265-280. https://doi.org/10.1111/j.1466-8238.2007.00287.x.
https://doi.org/10.1111/j.1466-8238.2007...
) and the improvement of colonization dynamics (Brown & Kodric-Brown, 1977Brown, J.H. & Kodric-Brown, A. 1977. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology, 58(2): 445-449. https://doi.org/10.2307/1935620.
https://doi.org/10.2307/1935620...
). According to Corenblit et al. (2007Corenblit, D.; Tabacchi, E.; Steiger, J.; & Gurnell, A. 2007. Reciprocal interactions and adjustments between fluvial landforms and vegetation dynamics in river corridors: A review of complementary approaches. Earth Science Review, 84(1-2): 56-86. https://doi.org/10.1016/j.earscirev.2007.05.004.
https://doi.org/10.1016/j.earscirev.2007...
), as these riparian forests act as corridors, connecting isolated fragments, these measures can increase the size and survival chances of forest-dependent bird species populations, such as the near-threatened P. superciliaris, S. ornatus, A. xanthops, A. aestiva, A. auricapillus, P. maracana, and N. fasciata found in or close to these areas. Moreover, they allow recolonization with populations of locally reduced and endemic species of the Atlantic Forest, e.g., B. ruficapillus and P. frontalis, which are found only in very small and isolated Atlantic Forest patches (areas 2 and 11), in addition to a reduction of pressure in the surroundings of protected areas (Mech & Hallett, 2001Mech, S.G. & Hallett, J.G. 2001. Evaluating the effectiveness of corridors: a genetic approach. Conservation Biology , 15(2): 467-474. https://doi.org/10.1046/j.1523-1739.2001.015002467.x.
https://doi.org/10.1046/j.1523-1739.2001...
). Another strong reason to recommend riparian corridors is that it is one of the easiest, cheapest and most effective methods for creating connectivity measures (Corenblit et al., 2007Corenblit, D.; Tabacchi, E.; Steiger, J.; & Gurnell, A. 2007. Reciprocal interactions and adjustments between fluvial landforms and vegetation dynamics in river corridors: A review of complementary approaches. Earth Science Review, 84(1-2): 56-86. https://doi.org/10.1016/j.earscirev.2007.05.004.
https://doi.org/10.1016/j.earscirev.2007...
). Moreover, birds are preferentially used by researchers seeking to assess the effectiveness of restored areas due to their mobility, the speed at which they colonize new environments, their ability to connect habitats through seed dispersal, and their maintenance of gene flow between plant populations (Lindig-Cisneros et al., 2012Lindig-Cisneros, R.; Fors, I.M.; Ortega-Alvarez, R. & Blanco-García, A. 2012. Restoration and the sustainable use of complex landscapes: An integrative conceptual model. In: Suthar, S. Land management. Nova Science Publishers. p. 113-124.). The avifauna essential role in pollination and seed dispersal has a great effect on the maintenance of forest succession and the restructuration of ecosystems (Sekercioglu, 2006Sekercioglu, C.H. 2006. Increasing awareness of avian ecological function. Trends in Ecology and Evolution, 21(8): 464-471. https://doi.org/10.1016/j.tree.2006.05.007.
https://doi.org/10.1016/j.tree.2006.05.0...
; Pizo & Galetti, 2010Pizo, M.A. & Galetti, M. 2010. Métodos e perspectivas da frugivoria e dispersão de sementes por aves. In: Von Matter, S.; Straube, F.C.; Piacentini, V.; Cândido, J.F. Ornitologia e conservação: ciência aplicada, técnicas de pesquisa e levantamento. Rio de Janeiro, Technical Books Editora. p. 493-506.).

Finally, the high richness, the 112 migratory birds and the 12 near-threatened and five threatened bird species found in TLM can also enhance birdwatching activities and offer other forms of ecotourism. This is the main reason why we adopted both bird vernacular and English names in our list compilation. In recent years, the birdwatching activity has grown considerably in Brazil, and birdwatchers have expressed their interest and involvement in conservation efforts (Develey, 2021Develey, P.F. 2021. Bird conservation in Brazil: challenges and practical solutions for a key megadiverse country. Perspectives in Ecology and Conservation, 19(2): 171-178. https://doi.org/10.1016/j.pecon.2021.02.005.
https://doi.org/10.1016/j.pecon.2021.02....
). Undoubtedly, bird-based tourism in the Neotropical region brings significant economic benefits (Maldonado et al., 2018Maldonado, J.H.; Moreno-Sánchez, R.D.P.; Espinoza, S.; Bruner, A.; Garzón, N. & Myers, J. 2018. Peace is much more than doves: The economic benefits of bird-based tourism as a result of the peace treaty in Colombia. World Development, 106: 78-86. https://doi.org/10.1016/j.worlddev.2018.01.015.
https://doi.org/10.1016/j.worlddev.2018....
), which strongly justify the need for preserving the habitats and birds in TLM.

ACKNOWLEDGMENTS:

We are grateful to Renato Cipriano Rocha, Nayara Rodrigues de Souza, Clara Luz Braga Sant’Anna (Suzano Papel e Celulose) and Elson Fernandes de Lima. We also thank Daniel Henrique Homem and Thainá Cassola Carreiro for the images obtained by trap-camera during mammal monitoring. We also thank Mariana Devito for the English version of this article. Part of this work was supported by Universidade Federal do Mato Grosso do Sul (SRP) and by Suzano Papel e Celulose as part of the terrestrial fauna monitoring and diagnostics conducted by Casa da Floresta Ambiental Ltda. Guilherme Serpa and Silvio Juraski kindly provided records of the l calities of C. minor and B. longicauda, respectively, in WikiAves.

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  • FUNDING INFORMATION:

    This project did not use any external financial support.
  • Published with the financial support of the “Programa de Apoio às Publicações Cientícas da Universidade de São Paulo”
Edited by: Luís Fábio Silveira

Publication Dates

  • Publication in this collection
    23 Oct 2023
  • Date of issue
    2023

History

  • Received
    25 Aug 2022
  • Accepted
    22 Aug 2023
  • Published
    02 Oct 2023
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