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Are recaptures of banded birds efficient at detecting altitudinal migrations in the Atlantic Forest?

ABSTRACT

Altitudinal migration in birds comprises seasonal movements between breeding and non-breeding areas in mountainous regions, attributed to biotic and abiotic factors. Different authors have suggested the existence of altitudinal migration between high and low areas of the mountains of the Atlantic Forest, with movement from high to low during the winter when birds would be fleeing the cold and in search of food, but there is no documented evidence. Through recaptures of understory birds, we investigated possible altitudinal migration in a region of the Atlantic Forest in Southeast Brazil. Twenty mist-nets were set at four locations between 15 and 729 m a.s.l. during 143 days of field work, distributed over 54 months and covering all seasons of the year. A total of 1946 birds (98 species) were captured/banded with 558 being recaptured (28.6%; 45 species). However, only 42 of the recaptures were at a different elevation. Most of the movements were of short distances and performed only once by birds, showing no seasonal pattern. These movements may be better interpreted as daily movements undertaken by birds of mixed-species flocks looking for food or moving around their respective home-ranges. Our results show that mist-nets may not be an effective tool in detecting altitudinal movements of birds and that other methods should be evaluated for this purpose.

KEY WORDS:
Bird banding; banded bird recovery; Serra do Mar; Southeast Brazil

INTRODUCTION

The altitudinal migration of birds - the regular, seasonal movements of birds up and down mountain slopes - is a widely known phenomenon, although it is poorly understood. Such movements have been commonly attributed to seasonal variation in environmental factors, such as temperature, precipitation, availability of resources, and predation risk (Hsiung et al. 2018). In contrast to traditional migrations (i.e., latitudinal and/or longitudinal migrations), altitudinal migrations cover shorter distances, with a significant occurrence of partial seasonal altitudinal movements; that is, migrations carried out only by individuals of a population of a given species (Johnson and Maclean 1994Johnson DN, Maclean GL (1994) Altitudinal migration in Natal. Ostrich 65: 86-94. https://doi.org/10.1080/00306525.1994.9639670
https://doi.org/10.1080/00306525.1994.96...
, Boyle 2011Boyle WA (2011) Short-distance partial migration of Neotropical birds: a community-level test of the foraging limitation hypothesis. Oikos 120: 1803-1816. https://doi.org/10.1111/j.1600-0706.2011.19432.x
https://doi.org/10.1111/j.1600-0706.2011...
, Hsiung et al. 2018Hsiung AC, Boyle WA, Cooper RJ, Chandler RB (2018) Altitudinal migration: ecological drivers, knowledge gaps, and conservation implications. Biological Reviews 93: 2049-2070. https://doi.org/10.1111/brv.12435
https://doi.org/10.1111/brv.12435...
).

Birds stand out as the most studied vertebrate group with regards to altitudinal migration. Global knowledge of altitudinal migrations of birds have been obtained via five main methodi cal approaches: 1) presence/absence sampling (observations) at different altitudes (e.g., Dixon and Gilbert 1964Dixon KL, Gilbert JD (1964) Altitudinal migration in the mountain chickadee. The Condor 66: 61-64. https://doi.org/10.2307/1365238
https://doi.org/10.2307/1365238...
, Dixit et al. 2016Dixit S, Joshi V, Barve S (2016) Bird diversity of the Amrutganga Valley, Kedarnath, Uttarakhand, India with an emphasis on the elevational distribution of species. Checklist 12: 1-11. https://doi.org/10.15560/12.2.1874
https://doi.org/10.15560/12.2.1874...
); 2) sampling with mist-nests (e.g., Loiselle and Blake 1991Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72: 180-193. https://doi.org/10.2307/1938913
https://doi.org/10.2307/1938913...
) or by point-counts (e.g., Betts et al. 2005Betts MG, Simon NPP, Nocera JJ (2005) Point count summary statistics differentially predict reproductive activity in bird-habitat relationship studies. Journal of Ornithology 146: 151-159. https://doi.org/10.1007/s10336-005-0074-9
https://doi.org/10.1007/s10336-005-0074-...
) to determine seasonal fluctuations in abundance; 3) altitudinal recapture of banded birds (e.g., Rabenold and Rabenold 1985Rabenold KN, Rabenold PP (1985) Variation in altitudinal migration, winter segregation, and site tenacity in two subspecies of Dark-eyed Juncos in the southern Appalachians. The Auk 102: 805-819. https://doi.org/10.1093/auk/102.4.805
https://doi.org/10.1093/auk/102.4.805...
); 4) radiotelemetry and GPS (e.g., Laymon 1989Laymon S (1989) Altitudinal migration movements of Spotted Owls in the Sierra-Nevada, California. The Condor 91: 837-841. https://doi.org/10.2307/1368067
https://doi.org/10.2307/1368067...
, Norbu et al. 2013Norbu N, Wikelski MC, Wilcove DS, Partecke J, Tenzin U, Tempa T (2013) Partial Altitudinal Migration of a Himalayan Forest Pheasant. Plos One 8: e60979. https://doi.org/10.1371/journal.pone.0060979
https://doi.org/10.1371/journal.pone.006...
); and 5) analysis of stable hydrogen isotopes using biological samples from birds (e.g., Hardesty and Fraser 2010Hardesty JL, Fraser KC (2010) Using deuterium to examine altitudinal migration by Andean birds. Journal of Field Ornithology 81: 83-91. https://doi.org/10.1111/j.1557-9263.2009.00264.x
https://doi.org/10.1111/j.1557-9263.2009...
). The use of mist-nets to recapture marked individuals has generated some data, but with extremely low recapture rates among different altitudes (Rabenold and Rabenold 1985Rabenold KN, Rabenold PP (1985) Variation in altitudinal migration, winter segregation, and site tenacity in two subspecies of Dark-eyed Juncos in the southern Appalachians. The Auk 102: 805-819. https://doi.org/10.1093/auk/102.4.805
https://doi.org/10.1093/auk/102.4.805...
in the United States; Loiselle and Blake 1991Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72: 180-193. https://doi.org/10.2307/1938913
https://doi.org/10.2307/1938913...
in Costa Rica; Burgess and Mlingwa 2000Burgess ND, Mlingwa COF (2000) Evidence for altitudinal migration of Forest birds between montane Eastern Arc and lowland forests in East Africa. Ostrich 71: 184-190. https://doi.org/10.1080/00306525.2000.9639908
https://doi.org/10.1080/00306525.2000.96...
and Fraser et al. 2008Fraser KC, Kyser TK, Ratcliffe LM (2008) Detecting altitudinal migration events in Neotropical birds using stable isotopes. Biotropica 40: 269-272. https://doi.org/10.1111/j.1744-7429.2008.00408.x
https://doi.org/10.1111/j.1744-7429.2008...
in Africa; and Merkord 2010Merkord CL (2010) Seasonality and elevational migration in an Andean community. Ph.D. Thesis, University of Missouri, Columbia, 154 pp. https://doi.org/10.32469/10355/8289
https://doi.org/10.32469/10355/8289...
in Peru).

Altitudinal movements of birds have been anecdotally mentioned since the beginning of the 19th Century for a mountainous region of the Atlantic Forest called the Serra do Mar, located in the Southeast and South regions of Brazil (Descourtilz 1983Descourtilz JT (1983) História natural das aves do Brasil. Ornitologia brasileira . Itatiaia, Belo Horizonte, 224 pp., Goeldi 1894Goeldi EA (1894) As aves do Brasil. I Parte (Monographias brasileiras II). Livraria Clássica de Alves & Cia, Rio de Janeiro, 311 pp.). The Serra do Mar is a geological formation that extends latitudinally for about 1000 km between the states of Rio de Janeiro (RJ) and Santa Catarina (SC), in Southeast and South regions, respectively; and is recognized as a steep plateau edge facing the Atlantic Ocean with an average of 800 m a.s.l. difference in level with a maximum peak of 2,275 m a.s.l. in the Serra dos Órgãos, RJ (Almeida and Carneiro 1998Almeida FFM, Carneiro CDR (1998) Origem e Evolução da Serra do Mar. Revista. Brasileira de Geociências 28: 135-150.). This geologi cal formation presents different environmental characteristics along its altitudinal range involving temperature (a decrease of 0.6 °C for every 100 m of elevation), humidity (higher at higher altitudes), soil (poorer nutrients at the highest altitudes), fauna and flora (with partially distinct altitudinal compositions), and many plants (e.g., Juçara palm) with seasonal fruit ripening throughout the year in relation to altitude (Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp., Galetti et al. 1999Galetti M, Zipparro V, Morellato PC (1999) Fruit phenology and frugivory on the palm Euterpe edulis in a lowland Atlantic forest of Brazil. Ecotropica 5: 115-122., Nettesheim et al. 2010Nettesheim FC, Menezes LFT, Carvalho DC, Conde MMS, Araújo DSD (2010) Influence of environmental variation on Atlantic Forest tree-shrub-layer phytogeography in southeast Brazil. Acta Botanica Brasilica 24: 369-377. https://doi.org/10.1590/S0102-33062010000200007
https://doi.org/10.1590/S0102-3306201000...
, Joly et al. 2012Joly CA, Assis MA, Bernacci LC, Tamashiro JY, Campos MCR, Gomes JAMA, Lacerda MS, Santos FAM, Pedroni F, Pereira LS, Padgurschi MCG, Prata BEM, Ramos E, Torres RB, Rochelle A, Martins FR, Alves LF, Vieira AS, Martinelli LA, Camargo PB, Aidar MPM, Eisenlohr PV, Simões E, Villani JP (2012) Florística e fitossociologia em parcelas permanentes da Mata Atlântica do sudeste do Brasil ao longo de um gradiente altitudinal. Biota Neotropica 12: bn01812012012. https://doi.org/10.1590/S1676-06032012000100012
https://doi.org/10.1590/S1676-0603201200...
, Caglioni et al. 2018Caglioni E, Uhlmann A, Curcio GR, Ramos MR, Bonnet A, Junckes AR (2018) Altitude e solos determinam variações abruptas da vegetação em gradiente altitudinal de Mata Atlântica. Rodriguesia 69: 2055-2068. https://doi.org/10.1590/2175-7860201869436
https://doi.org/10.1590/2175-78602018694...
). Based on this environmental and climatic variation, along with variation in bird behavior, some authors (e.g., Santos 1940Santos E (1940). Pássaros do Brasil: Vida e costumes. F. Briguiet & Cia, Rio de Janeiro, 281 pp., Berla 1944Berla HF (1944) Lista das aves colecionadas em Pedra Branca, município de Parati, Estado do Rio de Janeiro, com algumas notas sobre sua biologia. Boletim do Museu Nacional 18: 1-21., Davis 1945Davis DE (1945) The annual cycle of plants, mosquito, birds and mammals in two brazilian forest. Ecological Monographs 15: 243-295. https://doi.org/10.2307/1943247
https://doi.org/10.2307/1943247...
, Mitchell 1957Mitchell MH (1957) Observations on birds of southeastern Brazil. University of Toronto, Toronto, 258 pp., Sick 1968Sick H (1968) Vogelwanderungen im kontinentalen Südamerika. Die Vogelwarte 24: 217-242., 1979Sick H (1979) Migrações de aves no Brasil. Brasil Florestal 9: 7-10., 1983Sick H (1983) Migração de aves na América do Sul Continental. Centro de Estudos de Migrações de Aves, IBDF, Publicação Técnica n° 2, 86 pp., Sick and Pabst 1968Sick H, Pabst LF (1968) As aves do Rio de Janeiro (Guanabara), lista sistemática e anotada. Arquivos do Museu Nacional 53: 99-160., Snow 1973Snow D (1973) The classification of the Cotingidae (Aves). Breviora 409: 1-27., 1982Snow D (1982) The cotingas. Oxford University Press, Oxford, 203 pp., Willis 1979Willis EO (1979) The composition of avian communities in remanescent woodlots in southern Brazil. Papéis Avulsos Zoologia 33: 1-25., Gonzaga 1983Gonzaga LP (1983) Notas sobre Dacnis nigripes Pelzeln, 1856 (Aves, Coerebidae). Iheringia, Série Zoologia 63: 45-58.), have independently described a possible pattern of altitudinal migration of birds. Accordingly, birds, mainly frugivores, which occupy the canopy and forest understory (e.g., Bare-throated Bellbird Procnias nudicollis (Vieillot, 1817) and White-necked Thrush Turdus albicollis (Vieillot, 1818), move from the high part to the low part of the Serra do Mar during the coldest period of the year (May-August), presumably to escape the more intense low temperatures of the high part during the winter and to seek food in the coastal plains, following the fruiting of some plant species. Turdus albicollis is the only bird species from the Atlantic Forest/Serra do Mar that has had an altitudinal movement of 800 m detected by individual marking. One individual was banded in May 2006 at 800 m a.s.l and recaptured in August of the same year at sea level (Schunck et al. 2022Schunck F, Candia-Gallardo C, Benedicto GA, Yabe RS, Antas PTZ (2022) A importância das áreas particulares na conservação da avifauna do estado de São Paulo, sudeste do Brasil. Biodiversidade 21: 19-57.). This proposed altitudinal migration continued to be widely mentioned by different authors (e.g., Barçante et al. 2017Barçante LB, Vale MM, Alves MAS (2017) Altitudinal migration by birds: a review of the literature and a comprehensive list of species. Journal of Field Ornithology 88: 321-335. https://doi.org/10.1111/jofo.12234
https://doi.org/10.1111/jofo.12234...
, Somenzari et al. 2018Somenzari M, Amaral PP, Cueto VR, Guaraldo AC, Jahn AE, Lima DM, Lima PC, Lugarini C, Machado CG, Martinez J, Nascimento JLX, Pacheco JF, Paludo D, Prestes NP, Serafini PP, Silveira LF, Sousa AEBA, Sousa NA, Souza MA, Telino-Júnior WR, Whitney MM (2018) An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia 58: 1-66. https://doi.org/10.11606/1807-0205/2018.58.03
https://doi.org/10.11606/1807-0205/2018....
- that cite 16 species), including the review by Schunck (2019Schunck F (2019) Birds of the mountains of Brazil: general history and altitudinal patterns of richness, composition and seasonal movements in a region of Serra do Mar. PhD Thesis, Universidade de São Paulo, São Paulo, 360 pp. https://www.teses.usp.br/teses/disponiveis/41/41133/tde-02082019-123904/pt-br.php
https://www.teses.usp.br/teses/disponive...
) that mentions 80 species, but the few studies that have focused on this subject (e.g., Galetti et al. 1997Galetti M, Martuscelli P, Olmos F, Aleixo A (1997) Ecology and Conservation of the Jacutinga Pipile Jacutinga. Biological Conservation 82: 31-39. https://doi.org/10.1016/S0006-3207(97)00004-9
https://doi.org/10.1016/S0006-3207(97)00...
, Galetti 2001Galetti M (2001) Seasonal movements and diet of the Plumbeous pigeon (Columba plumbea) in a Brazilian Atlantic forest. Melopsittacus 4: 39-43., Castro et al. 2012Castro ER, Côrtes MC, Navarro L, Galetti M, Morellato LPC (2012) Temporal variation in the abundance of two species of thrushes in relation to fruiting phenology in the Atlantic rainforest. Emu 112: 137-148. https://doi.org/10.1071/MU11023
https://doi.org/10.1071/MU11023...
) failed to detect such migrations and so there remains a significant knowledge gap about the movements and ecology of Atlantic Forest birds.

The use of mist-nets to investigate possible altitudinal movements of birds in Brazil has long been recommended (e.g., Gonzaga 1983Gonzaga LP (1983) Notas sobre Dacnis nigripes Pelzeln, 1856 (Aves, Coerebidae). Iheringia, Série Zoologia 63: 45-58., Alves 2007Alves MAS (2007) Sistemas de migrações de aves em ambientes terrestres no Brasil: exemplos, lacunas e propostas para o avanço do conhecimento. Revista. Brasileira de Ornitologia 15: 231-238.) but still little applied in the field, raising doubts about its effectiveness. Among the studies that have used mist-nets, only three, which remain unpublished abstracts from ornithological meetings or theses, mention the recapture of individually marked birds at different altitudes (Gouvêa et al. 1996Gouvêa E, Alves ERMG, Carvalho MS, Silva MC (1996) 10 anos de anilhamento de aves no Parque Nacional do Itatiaia, RJ - 1984/1994. V Congresso Brasileiro de Ornitologia, Sociedade Brasileira de Ornitologia, Campinas, 41., Gouvêa 2006Gouvêa ERM (2006) Variação altitudinal em comunidade de aves na região do Parque Nacional do Itatiaia, RJ. Boletim do Parque Nacional do Itatiaia 12: 22-22., Barçante 2013Barçante LB (2013) Distribuição e deslocamento altitudinais de aves na Mata Atlântica, ênfase em beija-flores. Ph.D. Thesis, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, 194 pp. https://bdtd.ibict.br/vufind/Record/UERJ_932671852571578a892ad1fd2dc85ded
https://bdtd.ibict.br/vufind/Record/UERJ...
). Based on this scenario, and to determine whether mist-nets are effective for studies on altitudinal migration, we present the results of a long-term investigation based on the extensive capture/recapture of understory birds in a region of the Serra do Mar in Southeast Brazil.

MATERIAL AND METHODS

Study area

Núcleo Curucutu (23°56’S; 46°39’W) is one of ten administrative centres of the Parque Estadual da Serra do Mar, the largest conservation unit in the state of São Paulo and one of the largest in the Atlantic Forest of Southeast Brazil, with around 332,000 ha (Fig. 1). Núcleo Curucutu encompasses 36,134 ha with an altitudinal gradient ranging from 5 m to 1,050 m above sea level, with different vegetation typologies (Garcia and Pirani 2003Garcia RJF, Pirani JR (2003) Revisão sobre o diagnóstico e caracterização da vegetação campestre junto à crista de serras, no Parque Estadual da Serra do Mar, SP, Brasil. Hoehnea 30: 217- 241., Pessenda et al. 2009Pessenda LCR, De Oliveira PE, Mofatto M, Medeiros VB, Garcia RJF, Aravena R, Bendassoli JA, Leite AZ, Saad AR, Etchebehere ML (2009) The evolution of a tropical rainforest/grassland mosaic in southeastern Brazil since 28,000 14C yr BP based on carbon isotopes and pollen records. Quaternary Research 71: 437-452. https://doi.org/10.1016/j.yqres.2009.01.008
https://doi.org/10.1016/j.yqres.2009.01....
). According to Tarifa and Armani (2000Tarifa JR, Armani G (2000) Unidades climáticas urbanas da cidade de São Paulo. In: Atlas Ambiental do Município de São Paulo. Prefeitura Municipal de São Paulo, São Paulo.), the climate of the region is Tropical Super Humid through the interior of the Atlantic Plateau, and Tropical Oceanic Super Humid on the seaward face. Temperature varies between 0 °C (winter) and 34 °C (summer), with annual rainfall ranging from 3,497 to 4,435 mm between 2008 and 2011 (data from the local meteorological station; Malagoli 2013Malagoli LR (2013) Diversidade e distribuição dos anfíbios anuros do Núcleo Curucutu do Parque Estadual da Serra do Mar, SP. Ph.D. Thesis, Universidade Estadual Paulista Júlio de Mesquita Neto, Rio Claro, 211 pp. https://repositorio.unesp.br/handle/11449/99581
https://repositorio.unesp.br/handle/1144...
).

Figure 1
Geographic location of the Curucutu region. Altitudinal schematic of Núcleo Curucutu, showing the study locations A. Cota 30; B. Cota 200; C. Cota 400 and D. Cota 700, highlighted by the white rectangle. Model adapted from Malagoli (2013Malagoli LR (2013) Diversidade e distribuição dos anfíbios anuros do Núcleo Curucutu do Parque Estadual da Serra do Mar, SP. Ph.D. Thesis, Universidade Estadual Paulista Júlio de Mesquita Neto, Rio Claro, 211 pp. https://repositorio.unesp.br/handle/11449/99581
https://repositorio.unesp.br/handle/1144...
).

Data collection

The following four locations were sampled, with average altitude following the name: Location A - Cota 30 (31 a.s.l.); Location B - Cota 200 (247 a.s.l.); Location C - Cota 400 (533 a.s.l.); and Location D - Cota 700 (717 a.s.l.). The locations are situated along a slope facing the Atlantic Ocean with continuous forest cover. The vegetation at locations A, B and C is predomi nantly Dense Ombrophilous Forest while that at locality D is Dense High Montane Ombrophilous Forest (Fig. 1; Supplementary Material - Table S1 Supplementary Material 1 Table S1. Description of the study locations on the slope of the Núcleo Cuructu. Author: Fabio Schunck Data type: Table with descriptive text. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ). Data were collected during 18 field campaigns between May 2007 and June 2011. Each campaign spent three days at each location such that data were collected at all locations four times/year (one location at a time), for a total of 143 days of fieldwork (Supplementary Material - Table S2 Supplementary Material 2 Table S2. Field effort for the four study locations (A, B, C and D) on the slope of the Núcleo Curucutu. Author: Fabio Schunck Data type: Table with field information. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Twenty mist-nets (30 mm, 12 x 2 m, four bags) were used per location with two lines of 10 nets each with at least 100 m distance between net lines and the bird banding base. The nets were opened at dawn and closed at dusk for the first two days and closed at 12:00 pm on the third day. The straight-line distance and altitudinal difference between net lines of adjacent locations, in sequence from low to high altitude, are as follows: A to B = 900 m distance and 130 m altitudinal difference; B to C = 770 m distance and 285 m altitudinal difference; and C to D = 1,700 m distance and 255 m altitudinal difference (Figs 1, 2). This method produced a total sampling effort of 21,237.8 net-hr, allocated among locations as follows: A = 18 campaigns, 51 days, 8,058.2 net-hr; B = 14 campaigns, 39 days, 5,288.1 net-hr; C = 14 campaigns, 41 days and 6,086.5 net-hr; and D = 04 campaigns, 12 days, 1,805 net-hr. Due to unfavourable weather events and logistical problems (common occurrences for studies carried out in mountains, according to Blake and Loiselle 2000Blake JG, Loiselle BA (2000) Diversity of birds along an elevational gradient in the Cordillera Central, Costa Rica. The Auk 117: 663-686. https://doi.org/10.1093/auk/117.3.663
https://doi.org/10.1093/auk/117.3.663...
), we had less sampling effort at location D, which made it impossible to fully standardize field effort (Supplementary Material - Table S2 Supplementary Material 2 Table S2. Field effort for the four study locations (A, B, C and D) on the slope of the Núcleo Curucutu. Author: Fabio Schunck Data type: Table with field information. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ). Captured birds were photographed and marked with a metal band from Centro Nacional de Pesquisa e Conservação de Aves Silvestres (CEMAVE/ICMBio), and basic biometric and biological data were taken.

Biological and climatic data were not collected from the study locations because the main objective of the study was to detect whether there is seasonal altitudinal migration in the Serra do Mar, and then investigate possible causes.

Characteristics of the movements

Recaptures at different altitudes were classified according to their: (i) direction of travel (higher to lower elevation, lower to higher elevation); (ii) seasonality (dry season = autumn and winter; rainy season = spring and summer); (iii) number of recaptures of each individual at a given altitude (how many times the same individual was recaptured at a different location (altitude) from where it was marked or last captured); (iv) altitudinal range of movements based on the distance between locations (short distance = adjacent locations; medium distance = non-adjacent locations; long distance = between the extremes of the altitudinal gradient); and (v) age and sex of birds, when possible.

Analyses

Given that count data are usually not normally distributed (Bolker 2008Bolker BM (2008) Ecological Models and Data in R. Princeton University Press, Oxford, 408 pp. https://doi.org/10.1515/9781400840908
https://doi.org/10.1515/9781400840908...
), we assessed the occurrence of seasonal altitudinal movements using General Linear Models with Poisson-type distribution of errors. We grouped all species for this analysis because the main hypothesis deals with the altitudinal migration of “birds” from Serra do Mar, and consequently the low number of observations prevented analysing species separately (see Introduction). Despite this grouping and the lower sampling effort in one location (D), we believe that this analysis can detect seasonal altitudinal movements if they are held by the most abundant captured species. Therefore, this analysis is based on the detection of seasonal altitudinal movements by the most abundant species, since detection of movements is a much more informative result than lack of detection.

We built three candidate models (scenarios) in which the number of altitudinal movements varied depending on different variables or combinations of variables: (1) ‘Season Model’, in which the number of movements varied only according to season (dry/rainy), a scenario that represents an increase in movements according to season, regardless of direction; (2) ‘Season x Displacement Direction Model’, in which the number of movements varied according to an interaction between season and direction of displacement, a scenario that represents seasonal altitudinal movements (i.e., the direction of movements would change depending on the season) and (3) ‘Null Model’, in which movements would vary at random, a scenario that represents an absence of a pattern for the movements with regard to season or direction. Candidate models were selected using the Akaike information criterion (AIC) and related metrics (Burnham and Anderson 2002Burnham KP, Anderson DR (2002) Model Selection and Multimodel Inference. Springer, New York, 2nd ed., 488 pp.). The analyses were performed using R software (R Core Team 2020R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org [Accessed: 12/11/2020]
https://www.R-project.org...
).

Maps were prepared using QGis 2.14 software. The layout of the latitudinal profile of the slope of Núcleo Curucutu (including vegetation) from Malagoli (2013Malagoli LR (2013) Diversidade e distribuição dos anfíbios anuros do Núcleo Curucutu do Parque Estadual da Serra do Mar, SP. Ph.D. Thesis, Universidade Estadual Paulista Júlio de Mesquita Neto, Rio Claro, 211 pp. https://repositorio.unesp.br/handle/11449/99581
https://repositorio.unesp.br/handle/1144...
) was adapted. Satellite imagery of the locations of net lines and the movements of marked birds was obtained from Google Earth Pro version 7.3.1. The species list used adopted the taxonomy and nomenclature of the Brazilian Committee for Ornithological Records (Pacheco et al. 2021Pacheco JF, Silveira LF, Aleixo A, Agne CE, Bencke GA, Bravo G, Brito GRR, Cohn-Haft M, Maurício G, Naka LN, Olmos F, Posso S, Lees AC, Figueiredo LF, Carrano E, Guedes RC, Cesari E, Franz I, Schunck F, Piacentini VQ (2021) Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee - second edition. Ornithology Research 29: 94-105. https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
). Endemic species of the Atlantic Forest follows Vale et al. (2018Vale MM, Tourinho L, Lorini ML, Rajão H, Figueiredo MSL (2018) Endemic birds of the Atlantic Forest: traits, conservation status, and patterns of biodiversity. Journal Field Ornithology 89: 193-206. https://doi.org/10.1111/jofo.12256
https://doi.org/10.1111/jofo.12256...
). Threatened species follows IUCN (2022IUCN (2022) The IUCN Red List of Threatened Species. International Union for Conservation of Nature, v. 2021-3. http://www.iucnredlist.org [Accessed: 15/04/2022]
http://www.iucnredlist.org...
), MMA (2022MMA (2022) Altera os Anexos da Portaria nº 443, de 17 de dezembro de 2014, da Portaria nº 444, de 17 de dezembro de 2014, e da Portaria nº 445, de 17 de dezembro de 2014, referen tes à atualização da Lista Nacional de Espécies Ameaçadas de Extinção. Diário Oficial da União. 108. Seção 1. Publicado em 07/06/2022. Ministério do Meio Ambiente, Brasília. https://www.in.gov.br/en/web/dou/-/portaria-mma-n-148-de-7-de-junho-de-2022-406272733 [Accessed: 10/06/2022]
https://www.in.gov.br/en/web/dou/-/porta...
), and São Paulo (2018São Paulo (2018) Decreto Estadual N° 63.853 de 27 de novembro de 2018. Declara as espécies da fauna silvestre do Estado de São Paulo regionalmente extintas, as ameaçadas de extinção, as quase ameaçadas e as com dados insuficientes para avaliação de seu grau de conservação, bem como as diretrizes a que estão sujeitas. Diário Oficial do Estado de São Paulo, seção 1, vol. 128, #221. Governo do Estado de São Paulo, São Paulo.), brought together in a single category when coincident. All birds were captured and banded under appropriate permits for Brazil and authorization by the respective ethics committees.

RESULTS

A total of 1946 individuals of 98 species were captured and marked with metal bands, of which 558 were recaptured (28.6%, 45 species). The captures included no threatened species but seven Atlantic Forest endemic species. However, only 42 individuals of 14 species were recaptured at different altitudes (locations) from where they had been originally banded. Of the total of 98 species captured, 21 are considered altitudinal migrants in the Brazilian literature (Schunck 2019Schunck F, Silveira LF, Nascimento VS (2019) 118 years of ornithological knowledge of a forgotten region of the Atlantic Forest near the largest city in South America. The Wilson Journal of Ornithology 131: 758-773. https://doi.org/10.1676/1559-4491-131.4.758
https://doi.org/10.1676/1559-4491-131.4....
), but only four were recaptured at different altitudes. The species of birds recaptured at different altitudes represent three orders and ten families and are mostly understory birds that are usually detected with mist-nets (Table 1; Supplementary Material - Tables S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 , S4 Supplementary Material 4 Table S4. General list of species recorded at the four study locations. End. Endemic species of the Atlantic Forest (Vale et al. 2018); Thr. Threatened species (São Paulo 2018, IUCN 2022, MMA 2022). Author: Fabio Schunck Data type: Species table. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Table 1
Species recaptured at different altitudes.

There were 28 higher to lower altitudinal movements (done by 14 species) and 17 lower to higher (done by seven species). There were 28 movements during the dry season, with 15 in winter and 13 in autumn, and 17 during the rainy season, with 10 in spring and seven in summer. Of the 28 movements made from higher to lower elevations, 17 were during the dry season (nine in winter and eight in autumn) and 11 in rainy season (eight in spring and three in summer). For the 17 movements from lower to higher elevations, 11 were during the dry season (six in winter and five in fall) and six were during rainy season (four in summer and two in spring) (Fig. 2; Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Figure 2
Frequency of altitudinal movements by season (Rainy and Dry) and displacement direction (lower and higher).

Among the three GLM models evaluated, only two were considered plausible (i.e., with AIC > 3, Table 2). The model that best fit the data was the ‘Null Model’ (ΔAIC = 0, wAIC = 0.7) followed by the ‘Season Model’ (ΔAIC = 2.19, wAIC = 0.2), suggesting that altitudinal movements varied by chance, with a tendency that their frequency (regardless of direction) differed between seasons (more movements in the dry season). Nevertheless, the effect of season in the latter model did not differ significantly from zero (Table 3), suggesting that the hypothesis of random altitudinal movements is the most plausible according to the data.

Table 2
AIC values and related metrics for the three models built to explain the number of altitudinal movements. Modnames: Model name; K: Number of parameters of each model; AICc: Akaike Information Criterion (corrected for small sample sizes) of each model; Delta_AICc: Difference between AICc of each model and model with lowest AICc value; ModelLik: Likelihood of each model; AICcWt: Akaike Information Criterion weight for each model; Cum.Wt: Cumulative Akaike Information Criterion weight.

Table 3
Values of parameters estimated by the ‘Season’ model. Parameter: model parameter; Estimate: parameter value estimated according to data; std.error: standard error of each parameter estimate; statistic: value of t statistic for each parameter estimation; p.value: p- value for each parameter estimation.

As for the number of recaptures at different altitudes, 39 individuals had only one recapture and three had two. The altitudinal range of movements included 38 short-distance movements, that is between adjacent altitudinal levels, and seven medium-distance movements, between non-adjacent altitudinal levels. There were no long-distance movements, that is, movements between locations A and D at opposite extremes of the altitudinal gradient (Fig. 3; Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ). Nine of the short-distance movements were from location A to location B, and 14 in the opposite direction, about 900 m straight-line distance and an altitudinal difference of 130 m. Four short-distance movements were from B to C, and 11 in the opposite direction, about 770 m straight-line distance and an altitudinal difference of 285 m. Two medium-distance movements were from A to C, and three in the opposite direction, about 1,650 m straight-line distance and an altitudinal difference of 415 m. Two other individuals were included in this category but performed movements over a higher altitudinal range than the others as they moved from the slope (locations B and C) to the plateau (location D), passing precisely through the region of location C where mist-nets could not be employed due to the steep slope and irregularities of the terrain (Figs 1, 2). The first individual was Black-goggled Tanager Trichothraupis melanops (Vieillot, 1818), which moved from locality C to locality D, a straight-line distance of about 1,700 m and an altitudinal difference of 255 m. The second was White-shouldered Fire-eye Pyriglena leucoptera (Vieillot, 1818), which moved from B to D, a straight-line distance of about 2,450 m and an altitudinal difference of 540 m, the greatest distance and greatest altitudinal range obtained by a recapture on the Curucutu slope (Fig 3; Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Figure 3
Schematic illustration of the altitudinal movements recorded on the slope of Núcleo Curucutu by the recapture of individually marked birds. White lines indicate the two lines of mist-nets at each locality. Source: Google Earth Pro (Image Landsat/Copernicus 2015).

There was a prevalence of adult individuals among the birds that showed altitudinal movements, with only three T. melanops being captured and recaptured as younglings, while the rest of the younglings were recaptured as adults, even over short time intervals, in which case they were probably subadult individuals when recaptured. A low number of individuals had their sex determined, with 10 males and eight females (Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

DISCUSSION

This study contributes to filling a knowledge gap in Brazilian ornithology, and thus addresses the recommendations made by different researchers (e.g., Gonzaga 1983Gonzaga LP (1983) Notas sobre Dacnis nigripes Pelzeln, 1856 (Aves, Coerebidae). Iheringia, Série Zoologia 63: 45-58., Alves 2007Alves MAS (2007) Sistemas de migrações de aves em ambientes terrestres no Brasil: exemplos, lacunas e propostas para o avanço do conhecimento. Revista. Brasileira de Ornitologia 15: 231-238.) regarding the need to use mist nets to obtain data on altitudinal recaptures of individually banded birds in mountainous regions of Brazil.

Our data of altitudinal recaptures suggest an absence of seasonal patterns of altitudinal movements for the understory birds sampled in the region of Núcleo Curucutu, contrary to descriptions of annual migrations for Atlantic Forest birds by several authors (e.g., Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp., Somenzari et al. 2018Somenzari M, Amaral PP, Cueto VR, Guaraldo AC, Jahn AE, Lima DM, Lima PC, Lugarini C, Machado CG, Martinez J, Nascimento JLX, Pacheco JF, Paludo D, Prestes NP, Serafini PP, Silveira LF, Sousa AEBA, Sousa NA, Souza MA, Telino-Júnior WR, Whitney MM (2018) An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia 58: 1-66. https://doi.org/10.11606/1807-0205/2018.58.03
https://doi.org/10.11606/1807-0205/2018....
). Nonetheless, our data did show the presence of altitudinal movement by understory birds along the slope of Curucutu, allowing some inferences to be made.

Núcleo Curucutu stands out as one of the best-known regions, with regard to bird biology and distribution, along the entire Atlantic Forest domain, with a confirmed total of 382 bird species (Schunck et al. 2019Schunck F, Silveira LF, Nascimento VS (2019) 118 years of ornithological knowledge of a forgotten region of the Atlantic Forest near the largest city in South America. The Wilson Journal of Ornithology 131: 758-773. https://doi.org/10.1676/1559-4491-131.4.758
https://doi.org/10.1676/1559-4491-131.4....
). The high diversity of bird species, coupled with our significant field effort, are the main factors responsible for the 1,946 banded individuals of 98 species, with a total of 558 recaptures (28.6%, 45 species). A sampling effort of more than four continuous years is uncommon in standardized ornithological studies carried out in the Atlantic Forest. Studies in this domain are usually done over shorter periods of time (one year or less), with most having up to three years of field sampling (e.g., Develey 2004Develey PF (2004) As aves da Estação Ecológica Juréia-Itatins. In: Marques OAV, Duleba W (Eds) A Estação Ecológica Juréia-Itatins: ambiente físico, flora e fauna. Holos, Ribeirão Preto, 278-295., Castro et al. 2012Castro ER, Côrtes MC, Navarro L, Galetti M, Morellato LPC (2012) Temporal variation in the abundance of two species of thrushes in relation to fruiting phenology in the Atlantic rainforest. Emu 112: 137-148. https://doi.org/10.1071/MU11023
https://doi.org/10.1071/MU11023...
, Hasui et al. 2012Hasui E, Ramos FN, Tamashiro JY, Silva WR (2012) Non-sequential fruit tracking by birds along an altitudinal gradient. Acta Oecologica 45: 66-78. https://doi.org/10.1016/j.actao.2012.10.001
https://doi.org/10.1016/j.actao.2012.10....
). Gouvêa et al. (1996Gouvêa E, Alves ERMG, Carvalho MS, Silva MC (1996) 10 anos de anilhamento de aves no Parque Nacional do Itatiaia, RJ - 1984/1994. V Congresso Brasileiro de Ornitologia, Sociedade Brasileira de Ornitologia, Campinas, 41.) stands out as the only partially published study (conference abstract) that included data about altitudinal movements. During the 10 years of sampling in Itatiaia, RJ, Gouveia et al. (1996Gouvêa E, Alves ERMG, Carvalho MS, Silva MC (1996) 10 anos de anilhamento de aves no Parque Nacional do Itatiaia, RJ - 1984/1994. V Congresso Brasileiro de Ornitologia, Sociedade Brasileira de Ornitologia, Campinas, 41.) recaptured 10% of their 3,090 banded birds, with only three altitudinal recaptures: Gray-hooded Flycatcher Mionectes rufiventris Cabanis, 1846, Ruby-crowned Tanager Tachyphonus coronatus (Vieillot, 1822), and Swallow-tailed Manakin Chiroxiphia caudata (Shaw & Nodder, 1793). Movements of all three of these species were short-range, between 400 and 500 m in altitude, in a region with altitudinal variation (in relation to sea level) between 400 and 1,200 m a.s.l., but the straight-line distances between locations were not provided by the authors.

The low number of altitudinal recaptures in Itatiaia was probably due to the long distances between sampling localities. Low numbers of altitudinal recaptures and difficulty in obtaining this type of information with use of mist-nets have been mentioned by studies involving greater altitudinal gradients in other regions of the world (e.g., Rabenold and Rabenold 1985Rabenold KN, Rabenold PP (1985) Variation in altitudinal migration, winter segregation, and site tenacity in two subspecies of Dark-eyed Juncos in the southern Appalachians. The Auk 102: 805-819. https://doi.org/10.1093/auk/102.4.805
https://doi.org/10.1093/auk/102.4.805...
, Loiselle and Blake 1991Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72: 180-193. https://doi.org/10.2307/1938913
https://doi.org/10.2307/1938913...
Burgess and Mlingwa 2000Burgess ND, Mlingwa COF (2000) Evidence for altitudinal migration of Forest birds between montane Eastern Arc and lowland forests in East Africa. Ostrich 71: 184-190. https://doi.org/10.1080/00306525.2000.9639908
https://doi.org/10.1080/00306525.2000.96...
, Merkord 2010Merkord CL (2010) Seasonality and elevational migration in an Andean community. Ph.D. Thesis, University of Missouri, Columbia, 154 pp. https://doi.org/10.32469/10355/8289
https://doi.org/10.32469/10355/8289...
). The low recapture rates of these studies may be mediated, in part, by the use of coloured bands (e.g., Rabenold and Rabenold 1985Rabenold KN, Rabenold PP (1985) Variation in altitudinal migration, winter segregation, and site tenacity in two subspecies of Dark-eyed Juncos in the southern Appalachians. The Auk 102: 805-819. https://doi.org/10.1093/auk/102.4.805
https://doi.org/10.1093/auk/102.4.805...
, Morrissey 2004Morrissey CA (2004) Effect of altitudinal migration within a watershed on the reproductive success of American dippers. Canadian Journal of Zoology 82: 800-807. https://doi.org/10.1139/z04-042
https://doi.org/10.1139/z04-042...
, Merkord 2010Merkord CL (2010) Seasonality and elevational migration in an Andean community. Ph.D. Thesis, University of Missouri, Columbia, 154 pp. https://doi.org/10.32469/10355/8289
https://doi.org/10.32469/10355/8289...
), so that re-sightings of marked birds can augment mist-net recapture data. Coloured bands have yet to be used to investigate possible seasonal altitudinal movements of birds in mountainous regions of Brazil, but they hold promise since documentation by re-sighting can be carried out by researchers, birdwatchers, and photographers, thus advancing research through complementary citizen science (Dickinson et al. 2010Dickinson JL, Zuckerberg B, Bonter DN (2010) Citizen science as an ecological research tool: challenges and benefits. Annual Review of Ecology, Evolution and Systematics 41: 149-172. https://doi.org/10.1146/annurev-ecolsys-102209-144636
https://doi.org/10.1146/annurev-ecolsys-...
).

Among the species of altitudinal recaptures in Núcleo Curucutu, we highlight three families (Thamnophilidae, Platyrinchidae and Cardinalidae) and 11 species - Saw-billed Hermit Ramphodon naevius (Dumont, 1818), Blond-crested Woodpecker Celeus flavescens (Gmelin, 1788), Star-throated Antwren Rhopias gularis (Spix, 1825), Pyriglena leucoptera, Plain-winged Woodcreeper Dendrocincla turdina (Lichtenstein, 1820), Olivaceous Woodcreeper Sittasomus griseicapillus (Vieillot, 1818), Lesser Woodcreeper Xiphorhynchus fuscus (Vieillot, 1818), Planalto Woodcreeper Dendrocolaptes platyrostris Spix, 1825, Greenish Schiffornis Schiffornis virescens (Lafresnaye, 1838), White-throated Spadebill Platyrinchus mystaceus Vieillot, 1818, and Red-crowned Ant-Tanager Habia rubica (Vieillot, 1817) - as never having been reported exhibiting any kind of altitudinal movement (e.g., Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp., Schunck 2019Schunck F, Silveira LF, Nascimento VS (2019) 118 years of ornithological knowledge of a forgotten region of the Atlantic Forest near the largest city in South America. The Wilson Journal of Ornithology 131: 758-773. https://doi.org/10.1676/1559-4491-131.4.758
https://doi.org/10.1676/1559-4491-131.4....
).

Although there is just one record of a woodcreeper (Dendrocolaptidae) performing altitudinal movement - White-throated Woodcreeper Xiphocolaptes albicollis (Vieillot, 1818); Mallet-Rodrigues and Noronha (2003Mallet-Rodrigues F, Noronha MLM (2003) The avifauna of low elevations in the Serra dos Órgãos. Cotinga 20: 51-56.) -, this family represented the greatest number of movements in our study, involving four species (D. turdina, S. griseicapillus, X. fuscus and D. platyrostris), with D. turdina accounting for 16% of all altitudinal recaptures. The other two most frequently recorded species in our study (R. naevius and T. melanops) belong to families that are widely known for having species that perform altitudinal migrations in different regions of the Neotropics (Trochilidae and Thraupidae; Barçante et al. 2017Barçante LB, Vale MM, Alves MAS (2017) Altitudinal migration by birds: a review of the literature and a comprehensive list of species. Journal of Field Ornithology 88: 321-335. https://doi.org/10.1111/jofo.12234
https://doi.org/10.1111/jofo.12234...
). With the exception of R. naevius, all the understory species recorded by altitudinal recaptures in our study participate in some way in mixed-species flocks (Develey and Peres 2000Develey PF, Peres CA (2000) Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic Forest of southeastern Brazil. Journal of Tropical Ecology 16: 33-53. https://doi.org/10.1017/S0266467400001255
https://doi.org/10.1017/S026646740000125...
).

The confirmation of seasonal altitudinal movements of birds through altitudinal recaptures or documented re-sighting of marked individuals is possible only if a certain pattern exists. In the case of the Serra do Mar, this general pattern would be the altitudinal movement of birds from the high plateau to low plain during the dry season (autumn-winter), possibly due to low temperatures and supposedly low food availability (several authors - see introduction). However, our data for direction of movement and season revealed no predominant pattern for the Curucutu slope. The number of recaptures of birds that moved from the higher to lower elevations in the dry season (autumn-winter; 17) was close to the number that did the reverse during the rainy season (spring-summer; 11), suggesting a balance between the two seasons, both at community and species levels. These data support the hypothesis that birds on the Curucutu slope make altitudinal movements at random, without a clear association between season and direction (Fig. 2; Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Birds that were recaptured at different altitudes only once represented 86% of all altitudinal recaptures. This high percentage of one-time recaptures was unexpected, considering the sampling effort, temporal-seasonal coverage and, mainly, the relative proximity and linearity among our sampling locations, which would be expected to provide a greater number of altitudinal recaptures if there was a pervasive seasonal altitudinal movement of birds. Additionally, 84% of the altitudinal recaptures were for short altitudinal distances and ranges, suggesting limited movements, with little environmental and climatic variation. The only two movements that reached greater distances were performed by a P. leucoptera and a T. melanops between localities B-D and C-D, respectively. These took place between autumn and winter (both in the dry season) of the same year, which is contrary to what was expected for the Serra do Mar according to the hypothesis defended by different authors.

The mark-and-recapture method allowed us to confirm short movements for some species, such as an individual of X. fuscus, which moved up and down the slope between 30 and 200 m a.s.l. in four different years. Finally, 95% of the recaptured birds were adult individuals, suggesting that they had already defined their home ranges and territories, in contrast to young birds who tend to disperse in search of new areas to settle. Some of these adult individuals were recaptured several times at the same location, showing fidelity to their respective home ranges. It was not possible to relate movements to the sex of birds since most individuals could not be sexed do the lack of sexual dimorphism for most species (Supplementary Material - Table S3 Supplementary Material 3 Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined. Author: Fabio Schunck Data type: Table with information on recaptured birds. Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited. Link: https://doi.org/10.1590/S1984-4689.v39.e22025 ).

Our data indicate that the absence of seasonal altitudinal movements for some species may be attributed to the daily movements of birds of mixed understory flocks and movements of birds within their respective home ranges. All species recorded in the field attended mixed species flocks, five of which (H.rubica, X. fuscus, D. turdina, S. griseicapillus and M. rufiventris), are among the most common species in these flocks (Develey and Peres 2000Develey PF, Peres CA (2000) Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic Forest of southeastern Brazil. Journal of Tropical Ecology 16: 33-53. https://doi.org/10.1017/S0266467400001255
https://doi.org/10.1017/S026646740000125...
). Previous studies involving mixed species flocks in the Serra do Mar did not consider altitudinal gradients with complete amplitudes (e.g., Stotz 1993Stotz DF (1993) Geographic variation in species composition of mixed species flocks in lowland humid forests in Brazil. Papéis Avulsos de Zoologia 38: 61-75., Develey and Peres 2000Develey PF, Peres CA (2000) Resource seasonality and the structure of mixed species bird flocks in a coastal Atlantic Forest of southeastern Brazil. Journal of Tropical Ecology 16: 33-53. https://doi.org/10.1017/S0266467400001255
https://doi.org/10.1017/S026646740000125...
), which prevents a better understanding of potential seasonal altitudinal movements and behaviors of birds in mountainous regions. Such an approach with mixed flocks in mountainous areas has been carried out in other regions of the world (e.g., Merkord 2010Merkord CL (2010) Seasonality and elevational migration in an Andean community. Ph.D. Thesis, University of Missouri, Columbia, 154 pp. https://doi.org/10.32469/10355/8289
https://doi.org/10.32469/10355/8289...
), with interesting results for this natural system of grouping birds that move together in search of food. In Brazil, possible seasonal altitudinal movements by birds have been justified by climatic variation and the search for resources, with an emphasis on frugivorous and some insectivorous species (e.g., Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp.), but there is no mention of seasonal altitudinal movements by species known to participate in mixed flocks.

The home range size of understory passerine bird species vary, ranging from a few to many hectares (Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp., Ribon and Marini 2016Ribon R, Marini MA (2016) Small territory sizes and high densities of insectivorous birds in an Atlantic Forest secondary fragment, Brazil. Revista Brasileira de Ornitologia 24: 303-313.). Some species, such as P. leucoptera, can have home ranges of 0.3 to 2.5 ha, and even reaching up to 23.9 ha probably during the search for food when moving after army ants (Sick 1997Sick H (1997) Ornitologia Brasileira. Nova Fronteira, Rio de Janeiro, 862 pp., Hansbauer et al. 2008Hansbauer MM, Storch I, Leu S, Nieto-Holguin J, Pimentel RG, Knauer F, Metzger JPW (2008) Movements of neotropical understory passerines affected by anthropogenic forest edges in the Brazilian Atlantic rainforest. Biological Conservation 141: 782-791. https://doi.org/10.1016/j.biocon.2008.01.002
https://doi.org/10.1016/j.biocon.2008.01...
). This behavior of seeking food in more distant areas may explain the more significant displacement of this species on the Curucutu slope, where an individual of P. leucoptera moved 2,450 m straight line distance and 540 m altitudinally from location B to D. Our data indicate that, for the studied birds, daily activities within home ranges explain the movements recorded by the altitudinal recaptures on the Curucutu slope. The fact that the study area was an Atlantic slope, a geographically steep region, means that any direction of displacement carried out by birds between two different points is necessarily an altitudinal displacement, whether seasonal or not.

Based on our study, and on the results of Gouvêa et al. (1996Gouvêa E, Alves ERMG, Carvalho MS, Silva MC (1996) 10 anos de anilhamento de aves no Parque Nacional do Itatiaia, RJ - 1984/1994. V Congresso Brasileiro de Ornitologia, Sociedade Brasileira de Ornitologia, Campinas, 41.), mist-netting may not be the ideal approach for documenting altitudinal movements. Marking birds with coloured rings and tracking individuals through radio telemetry and/or GPS to obtain data with greater precision are certainly better, easier and, possibly, overall, less expensive than the continuous use of mist-nets to detect altitudinal movements, if any do exist.

It is necessary to invest in individual tracking technologies through telemetry or GPS to obtain more accurate data on possible seasonal altitudinal movements by birds in the mountains of Brazil and especially the Serra do Mar.

ACKNOWLEDGMENTS

We are thankful to the following institutions and people: Fundação Florestal de São Paulo-COTEC and CEMAVE/ICMBio; Fundação Grupo Boticário for financial support between 2007 and 2009; Núcleo Curucutu team; researchers and park guards for field assistance; Antonio, Alcir, Zé Pretinho, Carlos Ferreira (Kaká), and Jose Machado (Zé) for support at Itanhaem; Leo R. Malagoli for friendship and help throughout the study; Dione Seripierri and the MZUSP library staff; Bret Whitney for prior manuscript review; Betty Petersen (American Birding Association; in memoriam) and the Birder’s Exchange Program for the donation of equipment; and Conselho Nacional de Desenvolvimento Científico e Tecnológico for the grants to the authors FS (42076/2014-7) and LFS (302291/2015-6 and 308337/2019-0). This work was supported by grants from Fundação Grupo Boticário (grant #0732-20062) and Conselho Nacional de Desenvolvimento Científico e Tecnologico (grant #42076/2014-7 and #2017/23548-2) to the authors FS and LFS. Erik Wild performed the English edition and final revision.

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Supplementary Material 1

Table S1. Description of the study locations on the slope of the Núcleo Cuructu.

Author: Fabio Schunck

Data type: Table with descriptive text.

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: https://doi.org/10.1590/S1984-4689.v39.e22025

Supplementary Material 2

Table S2. Field effort for the four study locations (A, B, C and D) on the slope of the Núcleo Curucutu.

Author: Fabio Schunck

Data type: Table with field information.

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: https://doi.org/10.1590/S1984-4689.v39.e22025

Supplementary Material 3

Table S3. List of individuals recaptured at different altitudes. Sequence according to the largest number of individuals caught per species. Campaign: number refers to one of the 18 field expeditions carried out between 2007 and 2011. Status: ‘captured’ is when a bird was banded; ‘recapture’ is when a bird was recaptured. Age: A. Adult; Y. Youngling. Sex: M. Male; F. Female; U. Undetermined.

Author: Fabio Schunck

Data type: Table with information on recaptured birds.

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: https://doi.org/10.1590/S1984-4689.v39.e22025

Supplementary Material 4

Table S4. General list of species recorded at the four study locations. End. Endemic species of the Atlantic Forest (Vale et al. 2018); Thr. Threatened species (São Paulo 2018, IUCN 2022, MMA 2022).

Author: Fabio Schunck

Data type: Species table.

Copyright notice: This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.

Link: https://doi.org/10.1590/S1984-4689.v39.e22025

Edited by

Editorial responsibility

Claudia Hermes

Publication Dates

  • Publication in this collection
    25 Nov 2022
  • Date of issue
    2022

History

  • Received
    10 May 2022
  • Accepted
    18 July 2022
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