Ornithology Research (2025) 33:19

https://doi.org/10.1007/s43388-025-00224-5

RESEARCH

“Together is better”: the contribution of academy, citizen science

and gray literature for the knowledge of the urban avifauna of a
megadiverse easternmost Amazonian ecotonal border
Sara Miranda Almeida1 · Gustavo Gonsioroski2 · Nubia Carla Santos Marques1 · Fernanda Guimarães Fava1 ·
João Marcelo da Silva Abreu1 · Letícia Gomes da Silva1 · Rafaela Velloso Missagia1 ·
Vanessa Guimarães Lopes1 · Verônica Maria de Oliveira1 · Erick Cristofore Guimarães1 ·
Pedro Walfir M. Souza-Filho1 · Valéria da Cunha Tavares1,3,4

Received: 8 January 2024 / Revised: 27 December 2024 / Accepted: 6 January 2025

© The Author(s), under exclusive licence to Sociedade Brasileira de Ornitologia 2025

Abstract
The Metropolitan Region of Greater São Luís (MRGSL) is located in northern Brazil, along the Amazon Coast, in
the central part of the shore of Maranhão State. This region lacks a comprehensive checklist of bird species, which is
essential to support conservation efforts. To present a list of birds for the MRGSL, we gathered records from published
literature, environmental assessment reports, data repositories (GBIF, VertNet), and online citizen science (CS) platforms
(WikiAves, iNaturalist, and eBird). Each record was subjected to several filters before being included in our compilation.
We compiled 9,824 records for 399 bird species. Most species (78.44%) had documented records, of which 96.80% were
photos or audio recordings taken by CS amateurs and deposited on WikiAves. Seven species are threatened with extinc-
tion according to the IUCN Red List and 12 species are considered under threat in Brazil. Of the total species, 37 are
migratory birds, and five are mangrove-exclusive birds. As our results show, CS has contributed disproportionately to the
knowledge of species occurrence in the region. This study adds to the knowledge of the region’s avifauna and provides
insight into the structure of bird communities. However, there is a lack of systematic studies on key biological aspects of
birds, including population dynamics, community structure, and the environmental factors that regulate them. In addition,
studying the synergistic influences of impacts on these populations and communities is critical for effective conservation.

Keywords Birds · Checklist · Habitat associations · Mangrove · Nearctic migrants · Urban areas

Introduction

The Brazilian state of Maranhão encompasses the ecotonal

area between the eastern Amazon and the northern Cer-
rado, bordered to the north by the Atlantic Ocean. It has a
very diverse avifauna, which currently lists 735 species of
Sara Miranda Almeida birds (Oren 1991; Carvalho et al. 2020; IMESC 2023). This
[email protected]
avian diversity is a result of the high environmental hetero-
1
Vale Institute of Technology, Sustainable Development, Rua geneity of the mosaic of landscapes present in the region,
Boaventura da Silva, 955 – Nazaré, Belém, PA including ecosystems of the Cerrado, Amazon, and Caat-
66055-090, Brazil inga biomes, as well as land-sea ecosystems, such as salt
2
Fauna-MA Pesquisa e Consultoria, São Luís, MA, Brazil marshes and mangroves (Teixeira and Souza-Filho 2009;
3
Departamento de Sistemática e Ecologia, Programa de Pós- Carvalho et al. 2020). Bordered by the states of Pará (PA) to
Graduação em Ciências Biológicas, Universidade Federal da the west, Piaui (PI) to the east, and Tocantins to the south,
Paraíba (UFPB), João Pessoa, Brazil Maranhão has approximately 640 km of coastline extending
4
Programa de Pós-Graduação em Biodiversidade e Evolução, from the mouth of the Gurupi River (PA) to the delta of the
Museu Paraense Emílio Goeldi, Belém, Brazil

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Parnaíba River (PI) (El-Robrini et al. 2006). In the central Biodiversity Information Facility (GBIF; www.gbif.org), a
coastal portion of the state is the Gulf of Maranhão, where platform that gathers species occurrence across the globe,
is located the capital of Maranhão, São Luís, and the Met- come from eBird. WikiAves (WA; www.wikiaves.com.br),
ropolitan Region of Greater São Luís (MRGSL), which is launched in 2008, is the most popular photo-based online
composed of 13 municipalities inserted in the Amazon and CS platform in Brazil, hosting more than four million pho-
Coastal biomes (IBGE 2023). tographic records of Brazilian birds (Tubelis 2023). Scien-
The Gulf of Maranhão has been recognized as a key area tists are increasingly using this platform for studies on bird
for migratory shorebirds that depend on wetlands for resting migration patterns (Schubert et al. 2019), species conser-
and feeding (Silva and Rodrigues 2015; CEMAVE/ICMBio vation (Carvalho et al. 2017), and species distribution and
2020). This region is part of one of the largest concentra- occurrence (Vitorino et al. 2018). In this way, WA is rapidly
tions of mangroves in the world, encompassing the coasts of becoming very important for the elaboration of annotated
Maranhão, Pará and Amapá, which together form the Ama- species lists at local and/or regional scales (Vitorino et al.
zon Coast (Souza-Filho 2005; Rebelo-Mochel and Ponzoni 2018; Tubelis 2023). Therefore, it is crucial to evaluate and
2007; Teixeira and Souza-Filho 2009). take into account the records from digital platforms when
To date, ornithological studies in the MRGSL have compiling bird species lists for a region.
mainly focused on the abundance and seasonal distribu- In this study, we compiled and systematized data on the
tion of coastal birds, as the region annually receives large avifauna of the Metropolitan Region of Greater São Luís,
concentrations of migratory shorebirds (Rodrigues 2000; incorporating all available records from peer-reviewed stud-
Carvalho and Rodrigues 2011; Souza and Rodrigues 2015). ies, gray literature, and CS platforms. We characterized the
On the other hand, knowledge of the avifauna in the dif- avifauna of the region according to trophic guilds, identified
ferent habitats of the MRGSL is still lacking, as is a com- the main databases containing these records, and examined
prehensive understanding of the overall avian diversity of how this knowledge about the avifauna is distributed across
the region. Surprisingly, there are a handful of data sources the municipalities of the MRGSL. Finally, we present a
on birds in the region, including information produced comprehensive list of bird species of the region.
and available outside of peer-reviewed published articles
(known as “gray literature”), such as technical reports, the-
ses and dissertations, and many datasets available on open Methods
digital platforms. For instance, there is a large amount of
data generated from licensing and environmental monitor- Study area
ing projects that can enhance the knowledge of the local
avifauna, given those studies follow strict state and federal The Metropolitan Region of Greater São Luís (MRGSL, or
laws and should be properly validated and curated, such as Greater São Luís) is located in the extreme north of Mara-
vouchered material deposited in scientific collections (Car- nhão, Northeast of Brazil, in the central part of the state’s
valho et al. 2020). coast. The region is situated in the Gulf of Maranhão,
Digital platforms have also significantly enhanced our formed by the bays of São Marcos and São José, which are
knowledge of avifauna, particularly through contribu- separated by the island of São Luís (or officially, Upaon-açu
tions from citizen science (CS). Citizen science initiatives Island) (Fig. 1).
(e.g., eBird, iNaturalist, WikiAves) are very popular among According to the Brazilian Institute of Geography and
birdwatchers, hobbyists, and professional ornithologists Statistics (IBGE 2023), the Greater São Luís has more than
(Chandler et al. 2017; Tubelis 2023). These platforms allow 1,000 km² and a population of 1,621,102 inhabitants dis-
volunteers with little or no experience to make observations tributed in 13 municipalities: Alcântara, Axixá, Bacabeira,
of a variety of species and include data validation by experts Cachoeira Grande, Icatu, Morros, Paço do Lumiar, Presi-
(Chandler et al. 2017). These initiatives are accelerating the dente Juscelino, Raposa, Rosário, Santa Rita, São José de
accumulation of bird records worldwide, helping to fill bio- Ribamar, and São Luís (the capital of the State of Maranhão).
diversity data gaps, and supporting a growing range of basic Four of these municipalities—Paço do Lumiar, Raposa, São
and applied research (Amano et al. 2016; Chandler et al. José de Ribamar and São Luís— form the island of São Luís
2017; Aristeidou et al. 2021). and concentrate more than one million people. The climate
Developed by the Cornell Lab of Ornithology and Audu- of the region is humid tropical with two well-defined sea-
bon and launched in 2002, eBird (ebird.org) is the world’s sons: a rainy season from January to June and a dry season
largest biodiversity-related citizen science initiative, collect- from July to December (Pinheiro et al. 2020).
ing records of bird observations worldwide (Sullivan et al. The MRGSL has part of its territory within eight pro-
2014). For example, over one billion records on the Global tected areas: five areas of environmental protection with

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Ornithology Research (2025) 33:19 Page 3 of 12 19

Fig. 1 Map of the Metropolitan

Region of Greater São Luís, Mara-
nhão, Brazil, showing occurrence
records of bird species (red filled
circles) compiled from various
data sources

sustainable use of natural resources (APA) and three State The region is located in a transition zone between the Ama-
Parks. São Luís, the state capital, includes areas within the zon and Northeastern vegetation of Eastern South America
APA do Itapiracó, APA do Maracanã and APA Upaon-Açu/ (Freire and Monteiro 1993) and includes diverse vegetation
Miritiba/Alto Preguiças (ISA 2023). Due to its importance types such as ombrophylous forest, babassu groves, pioneer
for bird conservation, part of this region is also designated formations, floodplains, cerrado, transitional areas between
as an Important Bird Area (IBA), known as Baixada Maran- deciduous forest/cerrado/caatinga, and coastal and estuarine
hense (BirdLife International 2023). habitats like mangroves, mudflats, restinga forests, dunes
and beaches (ISA 2023). This mosaic of habitats provides

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a refuge for wildlife (Yang et al. 2020), especially given the (3) Environmental impact assessment and monitoring
high degree of urbanization in the region, a role reinforced (technical reports). We searched for bird records in 18 envi-
by the network of protected areas, including the APAs and ronmental reports made available by the company Vale S.A.,
State Parks, that aim to conserve its biodiversity. containing avifauna sampling carried out between 2006 and
2016 in the area of influence of the Ponta da Madeira Port
Compilation, curation of species occurrence records, Terminal, on the island of São Luís. These reports relate to
and maps fauna rescue in areas of vegetation suppression and environ-
mental monitoring required as part of the licensing process.
We applied the pipeline proposed by Marques et al. (2024) A variety of sampling methods were used to survey birds,
to retrieve and standardize secondary biodiversity data from including transects, point counts, 10-species lists, and cap-
multiple sources. Records of bird species were obtained tures. Additional details on sampling methods, data sources,
from three data sources: and locations are available in this dataset on OSF.io (​ ​​​h​t​t​p​s​:​
(1) Scientific papers and specialized literature. Our lit- /​/​o​s​f​.​i​o​/​g​h​9​y​m​/​​​​)​ ​.​​
erature search was performed in September 2021 in the Web Each record was subjected to several filters before being
of Science, Scopus and Google Scholar using the following included in our compilation. We examined all occurrences
keywords: (bird* OR aves) AND (maranhão OR “amazon and excluded 27 species for which documented evidence is
coast” OR “litoral amazônico” OR “golfão maranhense” unknown, questionable for the region, or due to misidenti-
OR “Gulf of Maranhão” OR “Baía de São Marcos” OR fication in museum collections. These species were consid-
“São Marcos Bay” OR “Baía de São José” OR “São José ered “unlikely to occur” in the Greater São Luís based on
Bay” OR “Amazônia oriental” OR “eastern Amazon”). their known distribution according to the Handbook of the
We found 345 scientific papers in these databases, 234 in Birds of the World Alive (HBW, https://www.hbw.com/),
Web of Science, 87 in Scopus and 24 in Google Scholar. specialized literature, and expert knowledge (Gustavo Gon-
We did not find any unpublished theses or dissertations in sioroski pers. obs.). They were removed from the consoli-
our search. After excluding duplicates, 135 articles were dated list for the MRGSL and presented separately in an
selected, of which 28 were retained based on title and annotated list of dubious records (Supplementary Material
abstract using Sysrev (https://sysrev.com/). After reading Table S4).
the articles, 14 were excluded because they were outside We checked taxonomy and species nomenclature
the study area. Thus, 14 articles were compiled, which were based on the Brazilian Ornithological Records Committee
carried out in five municipalities of the Greater São Luís. (Pacheco et al. 2021), which we also followed regarding
We also compiled records for the municipality of Bacabeira species migratory status. Information on species occurrence
from an e-book chapter (Gonsioroski et al. 2020). was organized into spreadsheets using DarwinCore stan-
(2) Interactive content from websites. Our search included dards (the same required by GBIF), widely used to compile
the Global Biodiversity Information Facility (GBIF, ​h​t​t​p​:​/​/​ and organize biodiversity data for easy sharing (Wieczorek
w​w​w​.​g​b​i​f​.​o​r​g​​​​)​ ​, VertNet (http://vertnet.org), and Species et al. 2012).
Link (http://splink.cria.org.br), as well as the online citizen Each bird species recorded was assigned to a trophic
science platforms WikiAves ​(​h​​ ​t​t​p​:​/​/​w​w​w​.​w​i​k​i​a​v​e​s​.​c​o​m​.​b​ guild based on its main food resources (shown in paren-
r​​​​​)​, iNaturalist (https://www.inaturalist.org), eBird ​(​​​h​t​t​p​s​:​/​ theses), following Tobias et al. (2022): frugivores (fruits),
/​e​b​i​r​d​.​o​r​g​​​​​)​, and Xeno-canto (http://www.xeno-canto.org). granivores (seeds or nuts), nectarivores (nectar), herbi-
The datasets available through GBIF included bird records vores (other plant material in non-aquatic systems, includ-
from the following institutions and databases: iNaturalist, ing leaves, buds, and flowers), aquatic herbivores (plant
eBird, Los Angeles County Museum (LACM), Museum of material in aquatic systems, including algae and aquatic
Comparative Zoology (MCZ), Museu Nacional do Rio de plant leaves), invertivores (terrestrial invertebrates, such as
Janeiro (MNRJ), and Royal Ontario Museum (ROM). Data insects, worms, and arachnids), vertivores (terrestrial ver-
were downloaded from GBIF on April 29, 2022, and from tebrates, including mammals, birds, and reptiles), aquatic
WikiAves in August 2022. WikiAves had 5,781 bird pho- predators (aquatic vertebrates and invertebrates, including
tos and audio recordings for the municipalities in this study. fish, crustaceans, and mollusks), scavengers (carrion, offal
However, since individual records could not be extracted or refuse), and omnivores (species that use multiple niches,
from this platform, we used the species list for each munici- within or across trophic levels, in relatively equal propor-
pality, counting each listed species as a single record from tions). In the same way as Mancini et al. (2018), we grouped
WikiAves. No records were found on Xeno-canto for this the species into waterbirds and terrestrial birds, where water-
region. birds are those species that live on or near water, including
marine and coastal species, shorebirds and wetland birds.

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Ornithology Research (2025) 33:19 Page 5 of 12 19

We also checked for the occurrence of exclusive mangrove Based on these records, we present a list of 399 bird spe-
species following the classification of Mancini et al. (2023). cies for the Greater São Luís (see Supplementary Material
Geographic coordinates of bird records were converted Table S1). Most species (313; 78.44%) have documented
to the shapefile format, with place names and correspond- records through photographs, audio recordings, or museum
ing codes in the attribute table. Additional data on boundar- specimens, while 86 species lack documentation but are
ies from the political division of the territory were obtained expected to occur in the MRGSL as suggested by the HBW,
from the official data service IBGE (Brazilian Institute specialized literature, and expert knowledge. Considering
for Geography and Statistics). The map was created using this list of valid species (documented and expected), eBird
QGIS 3.28.6 (QGIS Development Team 2022). Due to the covered the largest number of species (313; 78.44%), fol-
scale, each point on the map may correspond to one or more lowed by WikiAves (303, 75.93%) and technical reports
collection sites, depending on their geographical proximity (230; 57.64%) (Fig. 2b). These data sources also recorded a
(Fig. 1). higher number of unique species, i.e. species not reported in
the other sources (Fig. 2c). Furthermore, of the 313 species
with documented records for the MRGSL, 96.80% were
Results documented in WikiAves.
Among the municipalities, the highest richness (327 spe-
Overview and data sources cies) and 53.73% of the records were obtained for São Luís.
The other municipalities with high species richness were
We compiled 9,824 records, of which 7,507 (76.41%) were Bacabeira (238), São José de Ribamar (180), Raposa (157)
from GBIF, 1,069 (10.88%) from unpublished technical and Alcântara (154) (Fig. 3). Furthermore, the number of
reports, 847 (8.62%) from WikiAves, 192 (1.95%) from an species recorded in the municipalities was strongly related
e-book, 148 (1.50%) from scientific articles, and 60 from to the number of records (r = 0.81; p = 0.0008; Supplemen-
vertNet (0.61%). Of the records found on GBIF, the major- tary Material Fig. S1).
ity were from eBird (7,303; 97.28%), 146 from iNaturalist
(1.94%), and 58 (0.77%) from museums: RMNH (2), MNRJ Bird assemblage structure and trophic guilds
(51), ROM (3), MCZ (1), and LACM (1). We presented the
data obtained from GBIF in two ways: including only the Passerine birds (order Passeriformes) comprised 167 spe-
eBird records and excluding them (hereinafter referred to cies (41.85%), while Charadriiformes accounted for 12.03%
as “GBIF”). Thus, the highest number of bird records for (48 spp.), and 184 species (46.11%) were from other orders.
MRGSL came from eBird (74.33%) (Fig. 2a). The families with more species were Tyrannidae (41

Fig. 2 Number of bird records

(a), species richness (b), and
number of exclusive species
recorded by each data source
(c) in the Metropolitan Region
of Greater São Luís, Maranhão,
Brazil

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Fig. 3 Number of bird species recorded in 13 municipalities (shaded darker greens indicating areas of higher species richness and lighter
in green) of the Metropolitan Region of Greater São Luís, Maranhão, greens indicating areas of lower richness
Brazil. The green gradient represents species richness classes, with

spp.; 10.27%), Thraupidae (30 spp.; 7.51%), Accipitridae

(5.01%), Laridae (4.76%), and Scolopacidae (4.26%).
The trophic structure of the bird assemblage in the
MRGSL was predominantly composed of invertivores (168
species; 42.10% of the total), followed by aquatic preda-
tors (78 spp.; 19.55%), omnivores (53 spp.; 13.28%), fru-
givores (30 spp.; 7.51%), vertivores (23 spp.; 5.76%),
granivores (22 spp.; 5.51%), nectarivores (16 spp.; 4.01%),
aquatic herbivores (5 spp.; 1.25%), and scavengers (4 spp.;
1%). Three-quarters of the recorded species were terres-
trial birds (299 species; 74.94%) and covered the different
guilds (except aquatic predators and aquatic herbivores),
with a predominance of invertivores (158 species; 52.8%
of the terrestrial species; Fig. 4). The remaining 100 species
(25.06%) were classified as waterbirds, represented mainly
by aquatic predators (78% of the aquatic species; Fig. 4), 10
invertivores (10%), seven omnivores (7%) and five aquatic
herbivores (5%).
Among the recorded species, five are considered man-
Fig. 4 Trophic structure and main habitats of the bird assemblage in grove-exclusive birds: the mangrove cuckoo (Coccyzus
the Metropolitan Region of Greater São Luís, Maranhão, Brazil minor), tricolored heron (Egretta tricolor), mangrove rail

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(Rallus longirostris), scarlet ibis (Eudocimus ruber), and the metropolitan region of Belém in the eastern Amazon,
rufous crab hawk (Buteogallus aequinoctialis). Novaes and Lima (1998) compiled a list of 482 bird spe-
cies. In the Amazonian coast of Pará State, Lees et al. (2014)
Conservation status reported the occurrence of 323 bird species in different
habitat types (e.g., estuary, beach, mangrove and secondary
Among the recorded species, seven are listed as threatened forest), but the biodiversity of this region remains threat-
with extinction (Vulnerable-VU or Endangered-EN) accord- ened by habitat loss, hunting, and large-scale infrastructure
ing to the IUCN Red List (IUCN 2024): Pluvialis squa- development (Lees et al. 2014).
tarola (VU), Herpsilochmus pectoralis (VU), Hydrobates Passerine birds from the families Tyrannidae (tyrant fly-
leucorhous (VU), Calidris fuscicollis (VU), Limnodromus catchers) and Thraupidae (tanagers and their allies) were the
griseus (VU), Tringa flavipes (VU), and Malacoptila minor most representative in number of species. This is expected,
(EN). Nine other species are recognized by the IUCN as as these families are the most species-rich in the Neotropics
Near Threatened (NT): Arenaria interpres, Calidris canu- and occupy a wide range of habitats, including open grass-
tus, Calidris minutilla, Calidris pusilla, Tringa melano- lands, savannas, coastal environments, scrub and forests
leuca, Primolius maracana, Conirostrum bicolor, Penelope (Kennedy et al. 2014; Winkler et al. 2020). This pattern is
superciliaris, and Buteogallus aequinoctialis. Twelve spe- similar to that observed in other urban avifauna in Brazil,
cies are listed in the Brazilian Red List of Threatened Spe- where many species from these families are commonly
cies (MMA 2022), of which three species are endemic to found in gardens, plantations, and other modified habitats
Brazil and in the category ‘VU’ (Malacoptila minor, Pyr- because they are well adapted to anthropogenic environ-
rhura coerulescens, and Dendrocolaptes medius), and eight ments and exploit a variety of resources (Lees and Moura
species are shorebirds: Numenius hudsonicus (VU), Calid- 2017; Enedino et al. 2018; Barros et al. 2021). On the other
ris canutus (VU), Sterna dougallii (VU), Charadrius wil- hand, the Thamnophilidae and Dendrocolaptidae families,
sonia (VU), Calidris pusilla (EN), Limnodromus griseus which are typically species-rich passerine families in the
(EN), Thalasseus acuflavidus (VU), and Thalasseus maxi- Brazilian Amazon (Pacheco et al. 2021; Barros et al. 2022),
mus (EN). The national list also includes the seabird Sula were underrepresented in MRGSL, with only 11 and four
sula (EN). species, respectively. Although these families are dominant
in Neotropical forests (Lees and Moura 2017; Almeida et
Introduced species and migratory status al. 2018; Barros et al. 2022), they tend to be more sensi-
tive to environmental changes and often inhabit undisturbed
Three species recorded in the MRGSL are non-native birds forests (Barlow et al. 2007; Stratford and Stouffer 2013).
that were introduced to Brazil (the rock pigeon Columba Thus, a low representation of forest birds is expected, given
livia domestica, the common waxbill Estrilda astrild, and that the region has experienced decades of deforestation
the house sparrow Passer domesticus), while 17 are endemic driven by urban expansion and industrial projects, unlike
to the country (e.g., Ortalis superciliaris, Phaethornis other parts of the Brazilian Amazon, where deforestation is
maranhaoensis and Conopophaga roberti) (Supplementary primarily driven by agribusiness (Rêgo et al. 2018).
Material Table S1). Thirty-seven species are considered Forested areas in the region are particularly affected, as
migratory, of which 27 are Charadriiformes of the families seen in the municipalities of Bacabeira and Rosário, where
Scolopacidae (14 species), Charadriidae (03 species), Lari- the petrochemical industry is driving land use changes,
dae (09 species), and Stercorariidae (02 species) (Supple- and contributing to the increase in population density in
mentary Material Table S1). Five species recorded in the the MRGSL (Ribeiro and Castro 2016; Soares et al. 2017).
MRGSL are considered vagrants in Brazil: Calidris mauri, Today, herbaceous plants dominate habitats that were once
Tringa inornata, Xema sabini, Leucophaeus pipixcan, and occupied by shrubs and trees (Rêgo et al. 2018). Thus,
Larus fuscus. species of conservation concern that are typical of for-
est areas (H. pectoralis, M. minor, P. coerulescens, and D.
medius), as well as other forest-dependent birds (Procnias
Discussion averano, Dendrocincla fuliginosa, Formicarius analis, and
Conopophaga roberti), appear to be suffering from the his-
The number of bird species listed here for the Greater torical and ongoing deforestation in the region, with long-
São Luís (399 species) represents 54.28% of the currently term consequences (Soares et al. 2017; MMA 2022; IUCN
known avifauna for the state of Maranhão (Oren 1991; Car- 2024). On the other hand, Picumnus pygmaeus, Icterus
valho et al. 2020; IMESC 2023) and 20.29% of the bird spe- jamacaii and Paroaria dominicana, species characteristic of
cies occurring in Brazil (Pacheco et al. 2021). Similarly, in the Caatinga recorded in the MRGSL, are benefiting from

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deforestation, and expanding their distribution to other Bra- data, but this is a relatively small number compared to the
zilian biomes (Jaramillo 2020). total number of records compiled from this source. We also
emphasize that most of the reports (at least 75%) consid-
Databases, the importance of citizen science and ered in the present study have a high technical quality in the
the technical quality of environmental impact identification of species, since they were prepared by expert
studies researchers-ornithologists, especially when dealing with
coastal birds. Thus, data from environmental impact assess-
The highest number of species was recorded through the ment and monitoring studies can be an important source of
citizen science platforms eBird and WikiAves, while the information on the occurrence of bird species. However,
lowest species richness was recorded in published articles these data, along with other non-peer-reviewed records,
and on the vertNet data portal. WikiAves and eBird were should be critically analyzed and used with caution.
the main sources for obtaining documented records through The species richness compiled from published articles
photographs and sound recordings that allow verification was relatively low compared to the other data sources men-
by specialized observers/ornithologists, reducing misiden- tioned above. This is because scientific studies in the region
tifications and dubious records. Following the global and have focused on specific groups, mainly migratory shore-
national trends, these platforms are very popular among birds, as the Gulf of Maranhão is recognized nationally and
birdwatchers in the state, as evidenced by the number of internationally as one of the most important wintering areas
records and species observed. To date, Maranhão has records for these birds, which rest and feed in the region before
of 703 bird species on WikiAves, with 409 observers, while returning to the northern hemisphere (Silva and Rodrigues
eBird has documented 678 bird species and 172 observers 2015; CEMAVE/ICMBio 2020). Another source of bias is
from the state. Furthermore, CS approaches can optimize the evident disparity in the number of researchers, students,
and complement efforts in fieldwork and museum data col- and institutions across different regions of Brazil (Alves et
lection, while also maximizing limited financial resources al. 2008). For example, ornithological research is concen-
(Schubert et al. 2019). trated in central-southern Brazil (Alves et al. 2008), which
It is worth noting that the benefits of CS through bird- may result in greater support for research from scientific
watching go beyond scientific results, as they include social funding agencies in this region, while leading to less invest-
impacts such as raising awareness of wildlife conservation, ment in the northern and northeastern regions.
facilitating democratic participation in local issues and
building social capital, among others (Farias et al. 2022; Structure of the bird assemblage in Greater São Luís
Bowler et al. 2022). In the United States, for example, bird-
watching is one of the most popular outdoor activities, with The avifauna of Greater São Luís is composed of terrestrial
a total economic impact of approximately $85 billion annu- and water birds that exploit the resources in different ways.
ally (Whelan et al. 2008). The most representative guild of terrestrial birds were the
Environmental impact assessment and monitoring stud- invertivores, followed by omnivores, frugivores and grani-
ies have been fundamental in increasing knowledge of spe- vores. Since these birds usually feed on insects, fruits and
cies occurrence in the region, as evidenced by the significant seeds, they play an important role in the dispersal and pro-
number of species documented in the reports and eBook. In liferation of plant species in urban areas, and in the control
Brazil, most environmental impact assessments and moni- of insect populations (Luck et al. 2013; Enedino et al. 2018).
toring studies lack hypothesis testing and robust experimen- Previous studies in urban and other anthropized areas in the
tal designs (e.g. comparisons between control and impacted Neotropics have also reported a proportionally higher rich-
areas), which limits their effectiveness in detecting impacts ness of invertivores and omnivores (Lees and Moura 2017;
and reduces their value to decision makers and stakeholders Bhakti et al. 2020; Barros et al. 2021). Omnivores are well
(Silveira et al. 2010; Dias et al. 2019, 2022). Data from these adapted to human-modified habitats due to their ability to
assessments have been valuable in improving knowledge of exploit a variety of resources (Fagan 1997), while arthro-
species occurrence in the MRGSL. However, the lack of a pods, as one of the main components of the global biomass
detailed sampling design and geographic coordinates lim- (Bar-On et al. 2018), are also not a limiting resource for
ited our analyses to the municipal level. We recommend invertivores (Nyffeler et al. 2018).
that environmental impact assessments and monitoring pro- Vertivores included owls (Strigidae), hawks, eagles and
grams adhere to minimum standards for data and metadata kites (Accipitridae), and caracaras (Falconidae), all consid-
to improve documentation quality and usability. ered terrestrial birds. It is worth noting that estuarine habi-
Of the 27 species classified in the tertiary list (i.e., dubi- tats are also important for terrestrial species, as they support
ous records), 19 (70.37%) came from environmental report terrestrial invertebrates that serve as prey for passerines

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Ornithology Research (2025) 33:19 Page 9 of 12 19

(Mancini et al. 2023). Falcons and hawks hunt passerines species are restricted to mangroves throughout most of their
and other small animals in the marshes, while scavengers range but occur in other habitat types: the bicolored conebill
such as vultures patrol the vegetation and water edges in (Conirostrum bicolor), which also inhabits the varzea flood-
search of dead fish, crabs, and shellfish (Mancini et al. plain forests of the Amazon basin, and the little wood-rail
2023). (Aramides mangle), which has a population in a salt marsh
Aquatic predators were the second most representative area in southern Brazil (Mancini et al. 2023).
guild in the MRGSL and the most important guild among
waterbirds. This guild consisted of coastal, wetland, and Introduced non-native species
marine species and was represented mainly by Charadri-
iformes (gulls, terns, plovers and sandpipers) and Pele- We recorded three introduced species in the MRGSL,
caniformes (herons and egrets). These birds prey on fish Columba livia, Estrilda astrild, and Passer domesticus.
and benthic invertebrates such as crustaceans (e.g., crabs, Introduced to Brazil in the 16th century, C. livia is a com-
shrimp), mollusks and insects, and play an important role in mon species in large urban centers where it can cause prob-
the cross-transfer processes of energy and nutrients between lems by damaging monuments with its corrosive feces and
aquatic and terrestrial systems (Green and Elmberg 2013; transmitting disease to humans (Sick 1997; Fontoura et al.
Frota et al. 2022). 2013). The common waxbill (E. astrild), in turn, is native
We found that 52.17% of the 92 species of Charadri- to Africa and is believed to have been brought to Brazil on
iformes recorded for Brazil occur in the MRGSL, including slave ships during the reign of Dom Pedro I (Fontoura et
sandpipers and willets (Scolopacidae), and plovers (Char- al. 2013). This species forages for seeds in grasslands but
adriidae). Eight of the 12 species recorded in Greater São does not appear to conflict with native birds (e.g. seedeaters,
Luís that appear on the Brazilian Red List of Threatened Sporophila spp.) (Sick 1997). Finally, the house sparrow (P.
Species are shorebirds, seven are migratory species (or par- domesticus), native to Eurasia and Africa, has been intro-
tially migratory), and one is resident (Charadrius wilsonia). duced to other parts of the world, including South America
Shorebirds are the most diverse group of Charadriiformes (Lowther and Cink 2020). Passer domesticus was intro-
and are experiencing population declines worldwide, pri- duced from Portugal to Rio de Janeiro in 1905 and arrived
marily due to water pollution from industrial effluents, in northern Brazil in the state of Pará in the 1970s (Silva
urban expansion, and coastal habitat degradation (Baker et and Oren 1990; Sick 1997). Although Sick (1997) suggests
al. 2020; Hicklin and Gratto-Trevor 2020). that this species may compete with native Brazilian birds for
The island of São Luís has had port activity since 1970, food and nesting sites, studies on the extent of this impact
and currently, the region has one of the largest port com- are lacking.
plexes in the country, along with urban growth, predatory It is also important to mention that records of Anodo-
tourism, and land use changes, has caused environmental rhynchus hyacinthinus and Icterus cayanensis were found
pollution and disturbance to migratory and coastal species for the Greater São Luís (see the tertiary list in Supplemen-
(Ribeiro and Castro 2016; IMESC 2023). We found that the tary Material Table S4). Although these species occur natu-
region still supports an important and diverse community of rally in Brazil, the individuals observed in the MRGSL were
coastal birds, including migratory shorebirds. However, it probably captive birds and the records in the region are due
is necessary to monitor the population dynamics of species, to escape or release from captivity, as confirmed by expe-
especially those at risk of extinction. For example, Calidris rienced ornithologists (Gustavo Gonsioroski and André De
canutus, suffered a decline of about 80% in the municipality Luca, pers. comm.).
of São José de Ribamar between 1997 and 2012 (Souza and
Rodrigues 2015). Final considerations
In Brazil, mangroves are valuable coastal ecosystems
that provide important habitats for resident and migra- The metropolitan region of Greater São Luís has a very
tory birds to rest, roost and nest, as well as food resources diverse avifauna, representing more than 50% of the bird
(shrimp, crabs and fish) (Mancini et al. 2023). In Greater species documented in the state of Maranhão. This diver-
São Luís we recorded five mangrove-exclusive birds, Coc- sity reflects the variety of habitats in the region, supporting
cyzus minor, Egretta tricolor, Rallus longirostris, Eudo- species from several ecological groups. Our compilation
cimus ruber, and Buteogallus aequinoctialis. The latter reveals a high proportion of bird species well adapted to
species is listed as Near Threatened by the IUCN and has a anthropogenic environments, common in urban areas of
specialized diet (crabs only); it is found in most coastal hab- the Amazon. However, it also includes many forest-depen-
itats in eastern South America, where it is the most common dent birds, mangrove-exclusive species, and shorebirds.
raptor in mangroves (Bierregaard et al. 2020). Two other This study increases knowledge of the region’s avifauna,

13
 19 Page 10 of 12 Ornithology Research (2025) 33:19

composition. Stud Neotropical Fauna Environ 58:104–115. ​h​t​t​​p​s​:​

including endangered and conservation priority species, and /​​/​d​o​​i​.​o​​r​g​/​1​0​.​1​0​8​0​/​0​1​6​5​0​5​2​1​.​2​0​2​1​.​1​9​1​4​2​9​5​​​​​​​
provides insight into the structure of bird communities. We Barros FC, Almeida SM, Godoy BS, Silva RR, Silva LC, Moraes KF,
also highlight the need for further research to fill knowledge Santos MPD (2022) Taxonomic and functional diversity of bird
gaps and improve understanding of the region’s avifauna. communities in mining areas undergoing passive and active res-
toration in eastern Amazon. Ecol Eng 182:106721. ​h​t​t​​p​s​:​/​​/​d​o​​i​.​o​​r​g​
/​1​0​.​1​0​1​6​/​j​.​e​c​o​l​e​n​g​.​2​0​2​2​.​1​0​6​7​2​1​​​​​​​
Supplementary Information The online version contains Bhakti T, Pena JC, Rodrigues M (2020) Unplanned urban growth and
supplementary material available at ​h​t​t​​p​s​:​/​​/​d​o​​i​.​o​​r​g​/​1​0​.​1​0​0​7​/​s​4​3​3​8​8​-​0​ its potential impacts on bird species in a South American City.
2​5​-​0​0​2​2​4​-​5​​​​​.​​ Floresta E Ambiente 27:e20190111. ​h​t​t​​p​s​:​/​​/​d​o​​i​.​o​​r​g​/​1​0​.​1​5​9​0​/​2​1​7​
9​-​8​0​8​7​.​0​1​1​1​1​9​​​​​​​
Acknowledgements We thank Vale S.A., which through the Instituto Bierregaard RO, Kirwan GM, Boesman PFD, Sharpe CJ (2020)
Tecnológico Vale financed the project “Biodiversity of São Marcos Rufous Crab Hawk (Buteogallus aequinoctialis). In: del Hoyo J,
and São José Bays, Maranhão, Brazil”. Elliott A, Sargatal J, Christie DA, de Juana E (eds) Birds of the
World. Cornell Lab of Ornithology, Ithaca, NY, USA. ​h​t​t​​p​s​:​/​​/​d​o​​i​.​
Author contributions Conceptualization: [SMA, GG]; literature o​​r​g​/​1​0​.​2​1​7​3​/​b​o​w​.​r​u​c​h​a​w​1​.​0​1​​​​.​ Accessed 23 February 2023
search: [SMA]; data curation: [SMA, GG]; data analysis: [SMA]; writ- BirdLife I (2023) Important Bird Areas factsheet: Baixada Maran-
ing - original draft preparation: [SMA]; funding acquisition: [PWS-F]; hense. http://​datazon​e.birdl​ife.o​rg/site/factsheet/22224. Accessed
supervision: [VT]. ECG prepared the maps, and all authors critically 23 February 2023
reviewed the work. Bowler DE, Bhandari N, Repke L et al (2022) Decision making of
citizen scientists when recording species observations. Sci Rep
Funding This work was funded by Vale S.A., project “Biodiversity of 12:11069. https:/​/doi.or​g/10.10​38/s4​1598-022-15218-2
São Marcos and São José Bays, Maranhão, Brazil”. Carvalho DL, Rodrigues AAF (2011) Spatial and temporal distribution
of migrant shorebirds (Charadriiformes) on Caranguejos Island in
Data availability Dataset is available on OSF.io ​(​h​​ ​t​t​p​s​:​/​/​o​s​f​.​i​o​/​g​h​9​y​m​ the Gulf of Maranhão, Brazil. Rev Bras Ornitol 19:486–492
/​​​​​)​.​​ Carvalho DL, Sousa-Neves T, Cerqueira PV, Gonsioroski G, Silva SM,
Silva DP, Santos MPD (2017) Delimiting priority areas for the
conservation of endemic and threatened neotropical birds using a
Declarations nichebased gap analysis. PLoS ONE 12:e0171838. ​h​t​t​​p​s​:​/​​/​d​o​​i​.​o​​r​g​
/​1​0​.​1​3​7​1​/​j​o​u​r​n​a​l​.​p​o​n​e​.​0​1​7​1​8​3​8​​​​​​​
Competing interests The authors declare no competing interests. Carvalho DL, Silva SM, Souza-Neves T, Silva DP, Santos MPD (2020)
An updated documented inventory and new records of bird spe-
cies for the Brazilian state of Maranhão. Ornithol Res 28:77–85.
https:/​/doi.or​g/10.10​07/s4​3388-020-00013-2
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