Latitudinal Variation in Species Composition of Passerine Birds in the Brazilian Atlantic Forest Using Citizen Science

Favretto, M. A. 2020. Latitudinal variation in species composition of Passerine birds in the Brazilian Atlantic Forest using citizen science

Boletim do Centro Português de Geo-História e Pré-História 2 (1) 2020 : 49-53 https://www.cpgp.pt/boletim.php ISSN (print): 2184-4518. ISSN (online): 1645-9806. ISSN (CD-ROM): 2184-4194.

Latitudinal variation in species composition of Passerine birds in the Brazilian Atlantic Forest using citizen science

Mario Arthur Favretto1

1Universidade Federal de Santa Catarina, Centro Universitário, Bairro Trindade, Florianópolis, estado de Santa Catarina, Brasil.

Recebido: 30 julho 2020 / Aceite: 15 novembro 2020 / Disponível online: 1 março 2021

Resumo A Mata Atlântica foi um dos primeiros biomas do Brasil a ser explorado no início de sua colonização portuguesa, restando 8% de sua área original. Esse bioma se estende do nordeste ao sul do Brasil, abrangendo quase toda a sua costa. O presente trabalho procurou analisar como ocorre a variação latitudinal de aves da ordem Passeriformes neste bioma, verificando se há variação e quais padrões de distribuição ocorrem, usando um banco de dados de ciência cidadã. Com esses dados verificamos que o aumento da riqueza de espécies teve relação positiva com o aumento da latitude, diferente de outros estudos que demonstram uma relação inversa destas variáveis em grupos animais. Também registramos um gradiente de variação das aves do norte ao sul neste bioma. A composição de espécies formou grupos de similaridade de espécies que refletem os centros de endemismo e especiação do bioma, resultado da história geológica da Mata Atlântica que é fortemente influenciada pelos períodos de glaciação, tendo ocorrido períodos de expansões e de retrações das fitofisionomias florestais que a formam. Palavras-chave: aves; endemismo; especiação; refúgios florestais.

Abstract The Atlantic Forest was one of the first biomes in Brazil to be exploited during the Portuguese colonization; which culminated in, today, it holding 8% of its original area. This biome extends from the northeast to the south of Brazil, covering almost the entire coast of the country. The present work attempts to unveil the latitudinal variation of Passerine birds (Passeriformes) in this biome, checking if there is variation and which distribution patterns occur; all using a database made with citizen science data. With these data we found that the increase in species richness has a positive correlation with the increase in latitude, different from other studies that show an inverse relationship of these variables in animal groups. We also recorded a gradient in variation of birds from north to south in this biome. The species composition formed groups of similarity of species that reflect the centers of endemism and speciation of the biome, a result of the geological history of the Atlantic Forest which is strongly influenced by the periods of glaciation, with periods of expansion and retractions of the forest types that form it. Keywords: birds; forest refuges; endemism; speciation.

1. INTRODUCTION large gradient of latitudinal variation, being distributed over different climatic conditions. Related to these variations there are also changes in the species composition that occur along The Brazilian Atlantic Forest is a biome that has been their geographical distribution. Latitudinal variations generate exploited since the very beginning of the Portuguese gradients of different habitat conditions that influence the colonization in Brazil; this biome spreads throughout geographic distribution of species of different taxonomic almost the entire coastal area of that country, which extends groups, creating specific regional ecological conditions(Prata latitudinally. Its original area was approximately 1,360,000 et al., 2018; Kinlock et al., 2018; Piovesan et al., 2018). km2, an area that is currently reduced to 8% of it (MMA, 2002). To add to this the fact, it is notable that 70% of the The variation of species along latitudinal gradients is a Brazilian population resides within the area of this biome, pattern that is repeated in all parts of the globe, with species which includes the largest cities in Brazil (MMA, 2002). richness increasing closer to the equatorial regions (lower Despite the constant anthropic impacts that this biome suffers, latitude) and decreasing closer to the polar regions (higher its rate of deforestation has been reduced in the last decades latitude), both in the northern and southern hemispheres (SOS Mata Atlântica / INPE, 2018). (Hildebrand, 2004; Mittelbach et al., 2007). Due to its long extension, the Atlantic Forest forms a Following this pattern, the composition of birds also Favretto, M. A.  Boletim do Centro Português de Geo-História e Pré-História 2 (1) 2020  49-53 varies in a latitudinal way, in some situations with expressive Brazilian changes, influencing even the amount of eggs laid by the birds Municipality/State Coordinate geopolitical and the survival of their offspring (Morrison et al., 2010; region Stegen et al., 2013; Muñoz et al., 2018). However, specific Torres (RS) 29° 20' 06" S, 49° 43' 37" W South regional conditions may result in an absence of this variation, making the avifauna more homogeneous, eventually being a Florianópolis (SC) 27° 35' 49" S, 48° 32' 56" W South reflection of the homogenization of the habitats themselves Paranaguá (PR) 25° 31' 12" S, 48° 30' 32" W South (Filloy et al., 2015). São Vicente (SP) 23° 57' 46" S, 46° 23' 31" O Southeast

For the Atlantic Forest, there are some recognized centers Campos de Goytacazes (RJ) 21° 45' 14" S, 41° 19' 26" W Southeast of endemism of species that occur along its latitudinal lines. These areas reflect the history of forest retractions and São Mateus (ES) 18° 43' 00" S, 39° 51' 31" W Southeast expansions during glaciations of the Pleistocene period and Canavieiras (BA) 15° 40' 30" S, 38° 56' 49" W Northeast contact or isolation with other South American forest biomes Aracaju (SE) 10° 54' 36" S, 37° 04' 12" W Northeast (Ribeiro et al., 2009; Silva et al., 2012). Maceió (AL) 09° 39' 57" S, 35° 44' 06" W Northeast Based on these considerations, the present work performs Recife (PE) 08° 03' 14" S, 34° 52' 51" W Northeast an analysis of the latitudinal variation of Passerine birds (order Passeriformes) in the Brazilian Atlantic Forest, between the João Pessoa (PB) 07° 05' 00" S, 34° 50' 00" W Northeast latitudes 7°S and 29°S, in order to verify if the use of citizen Table 1 Geographic coordinates of the municipalities used in the evaluation of the science data reflects known biogeographical patterns for the latitudinal variation of Passerine birds of the Brazilian Atlantic Forest. distribution of birds of this biome.

composition of Passerine bird species, the following statistical 2. MATERIALS AND METHODS methods were performed: linear regression analysis between species richness and degrees of latitude; cluster analysis using UPGMA algorithm and Jaccard distance; NMDS analysis This study was conducted with the objective of analyzing and ANOSIM, to check the similarities and differences in how the latitudinal variation of Passerine birds occurs along the composition of bird species between the different areas; the Atlantic Forest on the coast of Brazil by using citizen and Detrended Correspondence Analysis (DCA). All of these science data. For our analysis we utilized the data available on analyses were generated through the software Past, version the website Wikiaves (2019); this website is a citizen science 2.16 (Hammer et al., 2001). initiative, which currently hosts a database with a huge amount of Brazilian bird occurrence records, to be precise, a total of 3,270,834 bird records from 35,431 users. We’ve retrieved the 3. RESULTS lists of species available on this website that occurred within a 50 km radius from 11 municipalities distributed from the In this study, information from 430 Passerine bird species, northeast to the south of the Brazilian coast (tab. 1, fig. 1). with records of distribution between latitudes 7°S and 29°S, To determine if and which variations occurred in the was used. The regression analysis showed that there was a

Fig. 1. Location of the sampling municipalities and the Atlantic Forest biome in Brazil. A - location of Brazil in South America (in black); B - original distribution of the Atlantic Forest biome in Brazil before the beginning of the European occupation (in green); C - current distribution of the Atlantic Forest biome in Brazil (in green) and deforested areas (in light yellow), and location of the municipalities used in this study (black circles). Adapted from: SOS Mata Atlântica / INPE (2018).

50 Favretto, M. A.  Boletim do Centro Português de Geo-História e Pré-História 2 (1) 2020  49-53 positive and significant relationship between the increase in latitude and the increase in Passerine species richness (R2 = 0.52; p = 0.01; fig. 2).

Fig. 2. Regression analysis of the relationship between latitude and species richness of Passerine birds in the Brazilian Atlantic Forest (R2 = 0.52; p = 0.01).

The cluster analysis demonstrated the formation of three distinct groups of species composition (fig. 3 and fig. 4). These Fig. 4. Location of the latitudinal species composition groups found in groups followed a latitudinal pattern, one group encompassing cluster analysis in the Brazilian Atlantic Forest. Adapted from: SOS Mata areas of the southeast and south regions of Brazil (southeast- Atlântica/INPE (2018). south group), another group area of the southeast and northeast regions, encompassing the central region of the Brazilian coast (southeast-northeast group) and another yet the northeast region (northeast group) (coph. corr. = 0.93).

Fig. 5. NMDS analysis of the species composition of Passerine birds along different latitudes in the Brazilian Atlantic Forest.

Fig. 3. Cluster analysis of the species composition of Passerine birds along different latitudes in the Brazilian Atlantic Forest, using UPGMA algorithm and Jaccard distance (ccc = 0.93). Dotted lines indicate the groups formed.

When the NMDS analysis was performed, utilizing the cluster analysis groups, we verified the occurrence of the same pattern of segregation by regions and latitudinal variation (fig. 5). Indicating a larger similarity between the southeast- northeast and northeast areas, in accordance with the results of the cluster analysis. In fact, when these regional groupings are considered, there was a significant difference in the composition of species between them (ANOSIM: R = 0.97, p Fig. 6 - Detrended Correspondence Analysis (DCA) of the species = 0.0002). composition of Passerine birds along different latitudes in the Brazilian Atlantic Forest. The Detrended Correspondence Analysis showed that the ordering of bird species is distributed along the sample areas forming a gradient (fig. 6). Indicating that the composition of species varies gradually along the Atlantic Forest.

51 Favretto, M. A.  Boletim do Centro Português de Geo-História e Pré-História 2 (1) 2020  49-53 4. DISCUSSION The data on the distribution of birds also corroborates the hypothesis of the existence of an ecological gradient, since the Results obtained in Argentina found a reduction in species species vary gradually along its extension. This hypothesis richness associated with increased latitude (see: Filloy et al., states that as the Atlantic Forest is isolated and surrounded by 2015). However, in our study in the Brazilian Atlantic Forest, biomes of open areas, such as Caatinga, Cerrado and Pampas, the opposite occurs, with the higher latitudes having greater it develops different characteristics along its area (Dantas et richness of Passerine birds; furthermore, the composition of al., 2011). It is also known that the flora of the Atlantic Forest species here varies and changes along the latitudinal gradient. undergoes changes in its composition along the latitudinal gradient, influenced mainly by changes in temperature and These results seem to contradict the latitudinal gradient rainfall. It is possible that this floristic composition also hypothesis, which posits that there should be greater species influences the composition of birds or reflects a similar pattern richness at lower latitudes, i.e., closer to tropical areas (Prata et al., 2018). (Hildebrand, 2004; Mittelbach et al., 2007). The bird fauna The understanding of the factors that influence the in the Atlantic Forest seems to contradict said hypothesis in latitudinal distribution of animals is still limited, considering other fronts as well, such as in the genetic variations of its that many of these may not be sufficient to explain the current bird residents, with some species having less genetic stability distribution of birds, such as ecological characteristics, body in regions of lower latitude, whereas larger stability should be size, life strategies and climate change, since the last maximum expected closer to tropical regions (D’Horta et al., 2011). of glaciation (Weir & Schluter, 2007; Smith et al., 2017). In Possibly the lower richness in low latitudes of the Atlantic this context, latitudinal differences could only be the result Forest occurs due to the diminished extension of this biome of higher extinction rates or differences in time for speciation towards those latitudes, a reflection of the fact that those areas between different latitudes (Weir & Schluter, 2007; Smith et were the first to be colonized in Brazil, and have suffered major al., 2017). environmental degradation (Mittermeier et al., 2005; Silva et These data show that, at least in the coastal region of the al., 2018). In addition, the lower latitude regions occur close Atlantic Forest, the general notion that there should be a to another biome, with a semi-arid climate, called Caatinga decrease in species richness with the increase of latitude is (Fritzsons et al., 2017; Silva et al., 2018). not applicable, the opposite in fact occurring for this biome. The Brazilian Atlantic Forest has a dynamic history To understand this, it is necessary to consider the historical from the last millions of years, having suffered expansions aspects that occurred over geological time in these areas. The and retractions of its forest areas, as well as oscillations of processes of isolation of Passerine bird populations in forest glaciation periods, sometimes more intense and sometimes refuges during the Pleistocene certainly contributed to their reduced. These changes in forest areas were also reflected speciation and even after the expansion of forest areas the species composition maintained its regional characteristics; in the fauna, with population expansions and retractions, in with different Passerine bird species replacing each other addition to population isolations in forest fragments or specific throughout the biome and only part of them occurring within habitats that resulted in processes of speciation or intra-species all its extension. Finally, the data used here, originated from genetic variations (Sobral-Souza et al., 2015; Françoso et al. citizen science, proved to be robust to explore biogeographical 2016; Batalha-Filho & Miyaki, 2016). patterns of bird species, corroborating previously recognized In fact, the groupings formed in our analysis coincide with patterns of distribution of birds in the Brazilian Atlantic Forest. the philogeographic discontinuities of the Atlantic Forest, reflecting areas of forest refuge that were formed during the Pleistocene period, when, in times of glaciations, forest 5. REFERENCES retractions occurred (Carnaval & Moritz, 2008; Batalha-Filho & Miyaki, 2011). These philogeographic events are currently Batalha-Filho, H. & Miyaki, C. Y. (2011). Filogeografia da Mata reflected even in the genetic information of some species of Atlântica. Revista da Biologia, Vol. Esp. 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