Open-access The high biodiversity of the Serra de Baturité Environmental Protection Area, Ceará, Brazil

A alta biodiversidade da Área de Proteção Ambiental Serra de Baturité, Ceará, Brasil

Abstract

The present work carried out an inventory of species in the Environmental Protection Area (EPA) of Serra de Baturité. Five kingdoms of living beings were recorded, analyzing 135 publications and using Jardim’s virtual herbarium online platform Botanist of Rio de Janeiro. Data includes occurrence, conservation status, endemism and exotic and migratory species. In total, 1,338 taxa distributed in nine phyla, 20 classes, 92 orders and 261 families. Of these, 672 species belong to the Kingdom Animalia, 654 to Kingdom Plantae, 10 to Kingdom Fungi, one to Kingdom Monera and one to the Protista Kingdom. Were identified 206 species endemic to Brazilian territory and 110 species threatened at national and international level. Additionally, 39 species of exotic animals and plants and 33 migratory birds were recorded. These numbers highlight the Serra de Baturité EPA as a priority area for preservation, of extreme biological importance. The region has great biodiversity and a rich distribution of taxa, facilitating scientific dissemination and research, in addition to contributing to the conservation and preservation of biodiversity in the face of overexploitation of natural resources.

Keywords Baturité Massif; Preservation; Endemic; Endangered; Migratory; Exotic

Resumo

O presente trabalho realizou um inventário de espécies na Área de Proteção Ambiental (APA) da Serra de Baturité. Foram registrados cinco reinos de seres vivos, analisando 135 publicações e utilizando a plataforma online do herbário virtual do Jardim Botânico do Rio de Janeiro. Os dados incluem ocorrência, status de conservação, endemismo e espécies exóticas e migratórias. No total, foram compilados 1.338 táxons distribuídos em nove filos, 20 classes, 92 ordens e 261 famílias. Destes, 672 espécies pertencem ao Reino Animalia, 654 ao Reino Plantae, 10 ao Reino Fungi, uma ao Reino Monera e uma ao Reino Protista. Foram identificadas 206 espécies endêmicas do território brasileiro e 110 espécies ameaçadas em nível nacional e internacional. Além disso, 39 espécies de animais e plantas exóticas e 33 aves migratórias foram registradas. Esses números destacam a APA da Serra de Baturité como uma área prioritária para preservação, de extrema importância biológica. A região apresenta grande biodiversidade e uma rica distribuição de táxons, facilitando a divulgação e pesquisa científica, além de contribuir para a conservação e preservação da biodiversidade em face da superexploração dos recursos naturais.

Palavras-chave Maciço de Baturité; Preservação; Endêmico; Em Perigo; Migratório; Exótico

Introduction

The Baturité Massif macroregion, located approximately 60 km from Fortaleza in the northeast of the State of Ceará, Brazil, spans an area of about 377,138 hectares. This region comprises 13 municipalities: Acarape, Aracoiaba, Aratuba, Barreira, Baturité, Capistrano, Guaramiranga, Itapiúna, Mulungu, Ocara, Pacoti, Palmácia, and Redenção (SETUR, 2014; Ribeiro et al., 2022) (Figure 1a, b, c). The Serra de Baturité, positioned to the northwest of this macroregion, features variable elevations reaching up to 1,114 meters at its highest peak. It covers approximately 38,220 hectares (Cavalcante, 2005; Moro et al., 2015). This mountainous area captures humidity and precipitation from Atlantic air masses, resulting in annual average temperatures of 20.5 °C and high rainfall rates (1023–1866 mm/year) in the highest altitude municipalities (SEINFRA, 2002). In contrast, the surrounding landscape is characterized by higher temperatures and lower, more irregular precipitation (Moro et al., 2015).

Figure 1
Serra de Baturité Enviromental Protection Area. (a) Location of the State of Ceará in Brazil. (b) Location of the Baturité Massif in the State of Ceará. (c) Municipalities and delimitations of the Baturité Massif, highlighting the Serra de Baturité EPA. (d) Municipality and delimitations of the Serra de Baturité EPA. (e) Specimen registration locations in the Serra de Baturité EPA. (f) Escarpment of the Serra de Baturité. (g) View of the interior of the forest in the Serra de Baturité EPA, registered in the municipality of Pacoti. (Photos: J.C. Pires).

Settlement in the Serra de Baturité began in the 17th century with the Portuguese colonization, displacing indigenous groups like the Tarairiús (Girão, 1984; Freire & Souza, 2006). The 19th century saw increased migration due to severe droughts, leading to deforestation for agriculture and urban expansion, significantly impacting the original ecosystems (Moro et al., 2015; Silva, 2015). Currently, the main threats include deforestation, agricultural burning, urbanization, predatory hunting, and the introduction of exotic species (Moro et al., 2015; Silva, 2015; Diogo, 2017; Borges-Nojosa & Cascon, 2018).

In response to these threats, the Serra de Baturité Environmental Protection Area (EPA) was established in the early 1990s under State Decree No. 20.956. This EPA, the largest protected area created by the state, covers 32,690 hectares, about 10% of the total Baturité Massif area (SETUR, 2014; Ribeiro et al., 2022) (Figure 1d). It is classified as a Sustainable Use Protected Area (PASU) by Federal Law No. 9.985/2000 (Brasil, 2000) and includes nine municipalities to varying extents (Ribeiro et al., 2022). The EPA is noted for its unique high-altitude mesoclimate, thick soils, and humid forest vegetation, contrasting sharply with the surrounding semiarid hinterlands (Freire & Lima, 2014; Moro et al., 2015) (Figure 1f, g).

The EPA’s vegetation is a humid forest, part of the Evergreen Rainforest-Nebular Tropical Forest and the Subevergreen Rainforest-Nebular Tropical Forest, making it one of the last remnants of the Atlantic Forest in Ceará (Borges-Nojosa & Cascon, 2018; Silva et al., 2016b). This region also holds remnants of the Atlantic Forest and Amazon Forest domains, which were connected in the Pliocene and Pleistocene epochs (Batalha-Filho et al., 2013; Cohen et al., 2022). These forests retreated during the terminal Pleistocene, creating forest refuge areas that now house relic and endemic species isolated by the surrounding Caatinga (Ab’Saber, 2003).

Despite its protected status, the EPA struggles to conserve local biodiversity effectively. Endemic and endangered species are still at risk due to persistent threats such as hunting, deforestation, fires, and urbanization, exacerbated by insufficient enforcement (Silva, 2015). The absence of comprehensive data on species diversity, threats, and endemism hinders conservation efforts and policy implementation (Arruda & Fedel, 2020).

Scientific interest in the Baturité Massif’s biodiversity dates back to the late 18th century, starting with expeditions by naturalists like João da Silva Feijó and followed by others including Huber, Ducke, and Loetzelburg, who documented the region’s flora and fauna (Paiva, 2002). Subsequent studies have expanded this knowledge base, particularly in botany, entomology, ornithology, and herpetology (Rodrigues et al., 2004; Hites et al., 2005; Araújo et al., 2007; Westerkamp et al., 2007; Albano & Girão, 2008; Lima & Mansano, 2011; Lima-Verde et al., 2014; Roberto & Loebmann, 2016; Silvera et al., 2020). However, a comprehensive compilation of this information is necessary to support educational projects and policy development.

To address this gap, we have compiled a biodiversity checklist of the Serra de Baturité EPA, including species from the five kingdoms of living organisms. This compilation highlights endemic, exotic, endangered, and migratory species, providing crucial data for scientific research, conservation efforts, and public dissemination.

Material and Methods

We examined species occurrences within the Serra de Baturité EPA, which is located between 4°08′ and 4°27′ South latitude and 38°50′ and 39°05′ West longitude, covering an area of 32,690 hectares (SEMA, 1992; Ribeiro et al., 2022). Our analysis included 135 publications and data from the online virtual herbarium of the Rio de Janeiro Botanical Garden (https://floradobrasil.jbrj.gov.br/reflora/herbarioVirtual) (Chart 1). This review identified specimens from 76 distinct locations within the Serra de Baturité EPA (Figure 1e; Chart 2).

Chart 1
Kingdom, phylum, and class of organisms registered in the Serra de Baturité EPA and their respective references (The numbers in brackets were used in charts 3 to 7 to cite the references that were used to record the occurrence).
Chart 2
List of recording locations of the five kingdoms of living beings, indicating the municipalities (in bold) and places of occurrence in the Serra de Baturité EPA (The numbers in curly braces were used in figures 1e, 2, 4, 5 and 7 to indicate registration locations for each taxa in the Serra de Baturité EPA. The coordinates in parentheses indicate properties that did not have their coordinates indicated in published works, these were obtained using the Google Earth Pro software and the Mapcarta online platform).

The searches for occurrence records began in July 2020 and ended in August 2023, also carried out on three online search platforms: Google Scholar, JSTORr, and Web of Science. We carried out searches using keywords in Portuguese and English related to locations in the region, as well as different taxa, always followed by the locality “Baturité”, aiming to include both studies carried out in the Baturité Massif and only in the Serra de Baturité. We chose the search taxa based on the results found for the localities, searching for large taxa that were not listed (or listed in small quantities) in previous search results. That way, in addition to the following keywords, the word ‘Baturité’ has been added: Places: “EPA”; “Atlantic Forest”; “Forest Mountains” and “Ceará”; “Humid Forest” and “Ceará”; “Humid Forest”; “Massif”; “Mountain Forest”; “Northeast”; “Rainforest”; “Ridge”; “Semi-Arid Region of Brazil”. Taxa: “Acari”; “Agaricales”; “Amphibia”; “Amylocorticiales”; “Anura”; Arachnida”; “Araneae”; “Archaeosporales”; “Arthoniomycetes”; “Atheliales”; “Auriculariales”; “Aves”; “Bacteria”; “Basidiomycota”; “Blastocladiales”; “Blattodea”; “Boletales”; “Cantharellales”; “Caudata”; “Ciliophora”; “Chilopoda”; “Chytridiales”; “Coleoptera”; “Collembola”; “Condrictes”; “Corticiales”; “Crustacea”; “Cyanophyta”; “Dermaptera”; “Diplopoda”; “Diptera”; “Diversisporales”; “Dothideomycetes”; “Embioptera”; “Ephemeroptera”; “Eurotiomycetes”; “Fishs”; “Flagellata”; “Flora”; “Funga”; “Geastrales”; “Gigasporales”; “Gloeophyllales”; “Glomerales”; “Gomphales”; “Gastropoda” “Gymnophiona”; “Harpochytridiales”; “Hemiptera”; “Hymenochaetales”; “Hymenoptera”; “Hysterangiales”; “Insecta”; “Isoptera”; “Jaapiales”; “Laboulbeniomycetes”; “Lecanoromycetes”; “Lepidoptera”; “Lepidostromatales”; “Leotiomycetes”; “Mammalia”; “Mantodea”; “Mecoptera”; “Megaloptera”; “Merostomata”; “Microcoryphia”; “Monoblepharidales”; “Mollusca”; “Monera”; “Neolectomycetes”; “Neuroptera”; “Odonata”; “Orbiliomycetes”; “Orthoptera”; “Osteíctes”; “Ostracodermos”; “Paraglomerales”; “Pezizomycetes”; “Phallales”; “Phasmatodea”; “Phthiraptera”; “Pisces”; “Placodermes”; “Plecoptera”; “Pneumocystidomycetes”; “Polyporales”; “Protist”; “Psocoptera”; “Raphidioptera”; “Reptilia”; “Russulales”; “Saccharomycetes”; “Sarcodina”; “Schizophyta”; “Schizosaccharomycetes”; “Scorpionida”; “Sebacinales”; “Siphonaptera”; “Sporozoa”; “Strepsiptera”; “Sordariomycetes”; “Symphyla”; “Taphrinomycetes”; “Thelephorales”; “Trechisporale”; “Trichoptera”; “Thysanoptera”; “Thysanura”; “Zoraptera”; “Zygomycetes”.

When accessing the publications from the search results, we searched for the following keywords in all studies found in the results: “Aratuba”; “Baturité”; “Capistrano”; “Caridade”; “Guaramiranga”; “Mulungu”; “Pacoti” and “Redenção”. When finding the word(s), the existence of a more precise location of the occurrence record was checked, such as coordinates, altitude elevations, indicative maps or property names. Such properties had their coordinates checked using the Google Earth Pro software and the Mapcarta online platform (https://mapcarta.com/) to verify whether the occurrence is located within the Serra de Baturité EPA. When such information was non-existent, the occurrence was discarded, except of those that had an explicit indication that the species was registered in “Serra de Baturité EPA”, “Ombrophylous Forest” or “Rainforest” in one of the municipalities used as a keyword, as well as records that reported only “Guaramiranga” as the place of occurrence was considered, taking into account that 93.43% of the territory of the municipality of Guaramiranga belongs to the EPA (Ribeiro et al. 2022). We checked in parallel geospatial data from Serra de Baturité EPA to analyze whether the coordinates obtained are included in the EPA, a map of the region was drawn up based on geospatial data with municipal delimitations and EPA delimitations obtained from the Environmental Spatial Data Platform of the State of Ceará (PEDEA-CE, from the acronym in Portuguese) (https://pedea.sema.ce.gov.br/portal/), and on the official data platform of the National System of Protected Areas, by the Ministry of the Environment (https://cnuc.mma.gov.br/), respectively, being plotted in the Google Earth Pro software (Figure 1c, d).

Thereafter, we analyzed the CiteScore (https://www.scopus.com/sources) of the journal in which the record was published and analyzed, which would have to be greater than or equal to 0.9. When the CiteScore was not included for the journal, we considered Qualis Periodicals classification, by the Federal agency CAPES that coordinates graduate courses in the country (Qualification of periodicals for the four year 2017–2020) (https://sucupira.capes.gov.br/sucupira/public/consultas/coleta/veiculoPublicacaoQualis/listaConsultaGeralPeriodicos.xhtml), with restrictions on periodicals belonging to strata A1 to B3. Therefore, undergraduate monographies and dissertations were not considered in this study, since they are unpublished works and therefore not valid. We verified that compared to other journal impact metrics, the CiteScore database covered a greater number of journals used in this study, which is why its metrics were chosen.

A search was also made for management plans for Protected Area defined as Private Natural Heritage Reserves (RPPN, from the acronym in Portuguese) that are limited to the Serra de Baturité EPA, with the search being carried out for such units on the RPPN Computerized Monitoring System platform - SIMRPPN (https://sistemas.icmbio.gov.br/simrppn/publico/rppn/CE/), followed by the search for individual management plans using the online platform of the Chico Mendes Institute for Biodiversity Conservation (https://www.gov.br/icmbio/pt-br/assuntos/biodiversidade/unidade-de-conservacao/unidades-de-biomas/mata-atlantica/lista-de-ucs/). Six RPPNs included in the Serra de Baturité EPA were identified: RPPN Sítio Palmeira Natural Reserve; RPPN Natural Serra da Pacavira (Sítio Horizonte Belo); RPPN Sítio Lagoa; RPPN Belo Monte; RPPN Gália; and RPPN Passaredo, however, only the first three have a sustainability management plan, which had their species occurrence records considered in this work, being cited as: Asa-Branca, 2011 a, b; and Portela et al. 2022, respectively. Aiming to verify all types of protected areas in the region, we also analyzed the management plan for the “Periquito Cara-Suja” Wildlife Refuge, however, the only species mentioned in it is Pyrrhura griseipectus Salvadori, 1900 (Periquito-Cara-suja).

After compiling the data, the scientific nomenclature of the taxa was reviewed, using the online platforms: Catalog of Life (https://www.catalogueoflife.org/data/search); Flora and Funga of Brazil - Rio de Janeiro Botanical Garden (http://floradobrasil.jbrj.gov.br/); and the Taxonomic Catalog of Brazilian Fauna (TCBF) (http://fauna.jbrj.gov.br/). The vernacular (common) names of each taxon were also indicated when available in publications or on the online platforms of the Agrolink (https://www.agrolink.com.br/); American Museum Of Natural History (https://amphibiansoftheworld.amnh.org/); Arboretum Program for Conservation and Restoration of Forest Diversity (https://www.programaarboretum.eco.br/); Biodiversity4all (https://www.biodiversity4all.org/); Biofaces (https://www.biofaces.com); Brazilian Biodiversity Information System (https://ala-bie.sibbr.gov.br/ala-bie/); Cerrado Museum (https://museucerrado.com.br/); Digital Flora Project (https://floradigital.ufsc.br/); Embrapa (https://www.embrapa.br/busca-de-publicacoes/); Fruit Collecting Project (https://www.colecionandofrutas.com.br/); Leguminosae in Brazil (https://rubens-plantasdobrasil.blogspot.com); National Flora Conservation Center (http://cncflora.jbrj.gov.br); Online Dendrological Identification System (http://florestaombrofilamista.com.br/); Pl@ntNet (https://identify.plantnet.org/); Royal Botanic Gardens, Kew (https://powo.science.kew.org/); Trees of the Cerrado Biome (https://www.arvoresdobiomacerrado.com.br/); USP Botany Garden Project - Ribeirão Preto (https://sites.usp.br/jardimdabotanicausprp/) and WikiAves (https://www.wikiaves.com.br/). We chose to share the common name in Portuguese as it can be useful for communicating locally. We consider Whittaker’s (1959) classification, contemplating the division of living beings into five kingdoms: Monera, Protist, Fungi, Plantae, and Animalia. We chose this classification due to its synoptic characteristic and easy relationship with ecological principles, making it still the most used in modern discussion of textbooks (Hagen, 2012).

We investigated the registered species of the Serra de Baturité EPA to account for endemic and exotic cases to the Brazilian territory, migratory taxa and endangered. We carried out searches on the online platforms Flora and Funga of Brazil - Rio de Janeiro Botanical Garden (http://floradobrasil.jbrj.gov.br/), on the Taxonomic Catalog of the Brazilian Fauna (TCBF) (http://fauna.jbrj.gov.br/), and in the American Museum of Natural History (https://amphibiansoftheworld.amnh.org/), as well as in the occurrence record publications for some species: Rodrigues et al. 2004, 2014; Guedes et al. 2014; Roberto & Loebmann, 2016; Vale et al. 2018; Nogueira et al. 2019; Pacheco et al. 2021; Uchôa et al. 2022) to collect data on the species. To verify the species threatened with extinction, the official list of fauna and flora species threatened with extinction was analyzed - Decree MMA No. 148, of June 7, 2022 (MMA, 2022), which results from the assessment of the risk of extinction of species carried out by ICMBio between 2015 and 2021, as well as Appendices I, II, and III of the Convention on International Trade in Endangered Species of Wild Fauna and Flora - CITES (CITES, 2023). The CITES defines and classifies more than 35,000 species to be protected according to the degree of threat, with three different levels listed (Appendices I, II, and III) protection against overexploitation (MRE, 2014; CITES, 2023). Appendix I contains threatened species whose international trade is prohibited; Appendix II contains species where the level of threat is of little concern; however, international trade must be strictly controlled to avoid an increase in the level of threat. Appendix III includes species protected in certain countries, which request assistance from other countries to prevent exploitation and control trade of these species (CITES, 2023).

We used the online platforms of Flora and Funga of Brazil - Rio de Janeiro Botanical Garden (http://floradobrasil.jbrj.gov.br/); the Taxonomic Catalog of the Brazilian Fauna (TCBF) (http://fauna.jbrj.gov.br/); and the Brazilian Biodiversity Information System - SiBBr (https://specieslist.sibbr.gov.br/speciesListItem/list/drt1629923907803) to research the exotic species present in the EPA of Serra de Baturité. We obtained data on migratory species through the work of Somenzari et al. 2018 and CEMAVE, 2023, who carried out panoramic studies on migratory birds in Brazil.

Finally, in order to compare diversity based on biotic change, we analyzed Beta diversity (β) to measure how much diversity between spatial units differs from each other, using Sorensen’s dissimilarity index (1948), “seen as one of the most effective presence/absence similarity measures” (Magurran, 2013), with formula DS = 2a / (2a + b + c) (Provete et al. 2011; Magurran, 2013). Where “a” is the number of species shared by both sampling units; “b” is number of species present in sample one but not in sample two, and “c” represents the number of species present in sample two that are not present in sample one (Provete et al. 2011; Magurran, 2013). According to the formula, if the sampling units do not have any shared species, the similarity value (CS) will be equal to zero, and when they share all species, the value will be equal to one (Provete et al. 2011). We used data on presence/absence of floristic diversity in the Serra de Baturité EPA compared to three National Parks located in different Brazilian biogeographic regions; the Itatiaia National Park, belonging to the Atlantic Forest, the Pico da Neblina National Park, belonging to the Amazon Forest and the Sempre-Vivas National Park, in the Cerrado. These Protected Areas are those with the most species records for each respective biome on the online platform of the Plant Catalog of Conservation Units in Brazil - Rio de Janeiro Botanical Garden (https://catalogo-ucs-brasil.jbrj.gov.br), platform where we obtained species occurrence data, being compiled and analyzed from August 2023 to November 2023.

Results

A total of 1,338 taxa have been recorded for the Serra de Baturité EPA, distributed across 261 families, 92 orders, 20 classes, and nine phyla, representing the five kingdoms of life. This includes one species of Monera, one species of Protist, nine species of Fungi, 654 species of Plantae, and 672 species of Animalia. Of these taxa, 165 (12%) were identified only at the genus level.

1.

Kingdoms

1.1.
Monera

A single record of the Monera kingdom was found in the municipality of Guaramiranga, belonging to the Serra de Baturité EPA, where the undetermined bacteria Rickettsia sp. was recorded by Moerbeck et al. (2018) (Chart 3) (Figure 2a).

Chart 3
Record list of the Monera kingdom, reference, and occurrence in the Serra de Baturité EPA (with municipality: locality).
Figure 2
Map of taxon registration sites in the Serra de Baturité EPA. (a) Class Alphaproteobacteria. (b) Class Kinetoplastea. (c) Class Sordariomycetes. (d) Class Agaricomycetes. (e) Class Pucciniomycetes. (f) Class Glomeromycetes. (The location corresponding to the numbers are indicated in Chart 2).
1.2.
Protist

A single record was also made for the kingdom Protist, where Trypanosoma cruzi Chagas (Kinetoplastea, Euglenozoa) was recorded in the municipality of Guaramiranga by Cavalcante et al. (2020) (Chart 4) (Figure 2b).

Chart 4
Record list of the Protist kingdom, reference, and occurrence in the Serra de Baturité EPA (with municipality: locality).
1.3.
Fungi

For the kingdom Fungi, 10 species of fungi were listed, distributed across three phyla (Ascomycota, Basidiomycota, and Glomeromycota) (Chart 5).

Chart 5
Record list of the Fungi kingdom, reference, and occurrence in the Serra de Baturité EPA (with municipality: locality).

In the phylum Ascomycota, three species were recorded in the Serra de Baturité EPA, distributed across the families Cordycipitaceae and Ophiocordycipitaceae (Hypocreales, Sordariomycetes). These species are arthropod-parasitic fungi, with Gibellula aurea (Mendes-Pereira et al. 2022) associated with spiders of the species Macrophyes pacoti (Brescovit et al. 2019) (Aranha), Ophiocordyceps camponoti-atricipis J.P.M. (Araújo et al. 2015) found on ants of the species Camponotus atriceps Smith, 1858 (Formiga), and Ophiocordyceps humbertii (C.P. Robin) Petch, 2007 associated with wasps of the species Agelaia pallipes (Olivier, 1792) (Vespa-social) and Apoica (Apoica) flavissima Vecht, 1972 (Marimbondo-chapéu). These fungi were recorded through three studies (Sobczak et al., 2017b; Sobczak et al., 2020a; Mendes-Pereira et al., 2022), conducted at two locations within the Serra de Baturité EPA (Figure 2c; Figure 3a).

Figure 3
Taxons registered in the Serra de Baturité EPA. (a) Fungi Ophiocordyceps humbertii (C.P. Robin) Petch, 2007 (Ophiocordycipitaceae, Hypocreales) parasitizing wasp Apoica (Apoica) flavissima (Vespidae, Hymenoptera) (Marimbondo-chapéu). (b) Cyathus sp. (Nidulariaceae, Agaricales) (Ninho-de-passarinho). (c) Bryophyte Hyophila cf. involuta (Pottiaceae, Pottiales). (d) Lycopodiopsida Selaginella sulcata (Desv. ex Poir.) Spring. (Selaginellaceae, Selaginellales). (e) Commelina benghalensis L. (Commelinaceae, Commelinales) (Trapoeraba). (f) Lantana camara L. (Verbenaceae, Lamiales) (Camará-chumbinho) (Photos: J.C. Pires). Scale bars: 1 cm.

As for the phylum Basidiomycota, four species distributed in three families were recorded in the Serra de Baturité EPA: Cyathus hortensis R. Cruz & Baseia (Nidulariaceae, Agaricales) (Ninho-de-pássaro) (Figure 3b), Blumenavia angolensis (Welw. & Curr.) Dring, and Blumenavia baturitensis Melanda, M.P. Martín & Baseia (Phallaceae, Phallales) and Dasyspora frutescentis Beenken (Uropyxidaceae, Pucciniales). Being recorded through five studies (Beenken et al. 2012; Rodrigues & Baseia, 2013; Cruz & Baseia, 2014; Melanda et al. 2020; Lima et al. 2021) that took place mainly in the municipality of Guaramiranga (Figure 2d, e).

For phylum Glomeromycota, Błaszkowski et al. (2021) recorded two species (Dominikia glomerocarpica Jobim, Błaszk., Niezgoda, Magurno & B.T. Goto and Epigeocarpum crypticum Błaszk., Niezgoda, Magurno & B.T. Goto) belonging to the Glomeraceae family (Glomerales, Glomeromycetes) in the municipality of Guaramiranga (Figure 2f).

1.4.
Plantae

The Kingdom Plantae was the second richest in this work, with 654 species recorded, distributed in seven classes: Bryopsida, Pteridopsida, Polypodiopsida, Lycopodiopsida, Pinopsida, Liliopsida, Magnoliopsida, 44 orders and 125 families (Chart 6).

Chart 6
List highlighting the record of species from the kingdom Plantae, indicating their vernacular names (common), vulnerability status, CITES Appendix number, exotic status, records locations in the Serra de Baturité EPA and references; also being indicated: (Ѫ) species threatened with extinction at the national level; (Ѧ) internationally threatened species; (Ψ) species endemic to Brazilian territory; (ɸ) exotic species.

Three species were listed for the Bryopsida class, Squamidium leucotrichum (Taylor) Broth. (Brachytheciaceae, Hypnales); Meteorium deppei (Müll. Hal.) Mitt (Meteoriaceae, Hypnales); and Hyophila involuta (Hook.) A.Jaeger (Pottiaceae, Pottiales) (Figure 3c), was recorded through three studies (Yano & Peralta, 2009; Costa, 2014; Costa, 2015) in the municipality of Guaramiranga (Figure 4a).

Figure 4
Map of taxon registration sites in the Serra de Baturité EPA. (a) Class Bryopsida. (b) Class Pteridopsida. (c) Class Polypodiopsida. (d) Class Lycopodipsida. (e) Class Pinopsida. (f) Class Liliopsida. (The location corresponding to the numbers are indicated in Chart 2).

For the Pteridopsida class, six species were verified for the Serra de Baturité EPA, recording six sampling sites belonging to the municipalities of Guaramiranga, Pacoti, and Baturité (Figure 4b). Three species belonging to the Anemiaceae family, order Schizaeales: Anemia hirta (L.) Sw. (Espiga-de-ferrugem); A. nervosa Pohl; A. phyllitidis (L.) Sw. (Pluma-de-cacho); and the others: Lygodium venustum Sw. (Samambaia); Dicksonia sellowiana Hook (Xaxim); and Cyathea microdonta (Desv.) Domin (Palma-boba), belonging to the families Lygodiaceae (Schizaeales), Dicksoniaceae (Cyatheales), and Cyatheaceae (Cyatheales), respectively. Among these, Anemia nervosa Pohl (Anemiaceae, Schizaeales) is classified as an endemic species in Brazilian territory.

For the Polypodiopsida class, 25 species were inventoried, distributed in 11 families and one order (Polypodiales) (verified by Asa-Branca, 2011a; Schwartsburd, 2014; Lima & Salino, 2018; Pinheiro et al. 2022; and the online platform https://floradobrasil.jbrj.gov.br/reflora/herbarioVirtual). The families with the highest number of species were Aspleniaceae, with six species of the genus Asplenium recorded in the municipalities of Guaramiranga (in the locality of Pico Alto, Sítio Mucunã), Mulungu (Sítio Santa Clara) and Pacoti (Sítio Munguba). Polypodiaceae with five species: Microgramma vacciniifolia (Langsd. & Fisch.) (Erva-da-mamãe-oxum); Pecluma robust (Fée) M.Kessler & A.R.Sm. (Samambaia); Pleopeltis gyroflexa (Christ) Schwartsb. (Samambaia); Pleopeltis astrolepis (Liebm.) E.Fourn (Samambaia); and Serpocaulon triseriale (Sw.) A.R.Sm. (Samambaia), the first three being recorded in the municipality of Guaramiranga (Pico Alto, Sítio Brejo) and the others in Pacoti (at the Experimental Campus of Environmental Education and Ecology of UECE) and Pteridaceae four species: Adiantum deflectens Mart. (Avenca-chorona); Adiantum petiolatum Dev. (Samambaia); Pteris denticulata Sw. (Samambaia); and Pityrogramma calomelanos (L.) Link (Samambaia), recorded in the Serra de Baturité EPA mainly in the municipality of Pacoti (Figure 4c).

In the Lycopodiopsida class, four species were recorded in the Serra de Baturité EPA, Selaginella muscosa Spring; Selaginella sulcata (Desv. ex Poir.) Spring (Figure 3d), (Selaginellaceae-Selaginellales); Palhinhaea cernua (L.) Franco & Vasc. (Lycopodiaceae-Lycopodiales) (Musgo-de-veado); and Phlegmariurus taxifolius (Sw.) Á. Löve & D. Löve (Lycopodiaceae-Lycopodiales), the latter being classified as threatened with extinction according to the official list of species of fauna and flora threatened with extinction - MMA Decree No. 148, 2022. Such species were recorded in the municipalities of Mulungu (Sítio Santa Clara) and Guaramiranga (Sítio Venezuela, Hotel Remanso de Serra, and Pico Alto) (Figure 4d) (Engler & Krause, 1914; Matias & Sousa, 2011; Andrade et al. 2013; Silvera et al. 2020; and on the online platform https://floradobrasil.jbrj.gov.br/reflora/herbarioVirtual).

Still in the Plantae kingdom, one species was listed for the Pinopsida class, Podocarpus sellowii Klotzsch ex. Endl. (Pinheiro-bravo), belonging to the Podocarpaceae family, order Pinales. The species was recorded in the EPA by Silveira et al. (2020) in the municipality of Pacoti (Sítio Arvoredo) (Figure 4e).

Followed by the Liliopsida class, with 87 species listed in six orders in the Serra de Baturité EPA (Alismatales, Arecales, Asparagales, Commelinales, Liliales, and Poales) and 14 families. The most diverse family was Orchidaceae (Asparagales) with 27 species listed for the Serra de Baturité EPA, followed by Bromeliaceae (Poales) with 23 species and by the Araceae family (Alismatales) with 10 species. Having wide distribution in the Serra de Baturité EPA (Figure 4f). 19 endemic species of Liliopsida were listed in the Serra de Baturité EPA, such as Attalea speciosa Mart. ex Spreng (Arecaceae, Arecales) (Babaçu); Hippeastrum stylosum Herb. (Amaryllidaceae, Asparagales) (Açucena); different species of Bromeliaceae, Poales: Vriesea rodigasiana E.Morren (Croatá); Guzmania monostachia (L.) Rusby ex Mez (Croatá); Aechmea aquilega (Salisb.) Griseb. (Croatá); and others. In addition to 27 threatened species listed in appendix II of CITES, (2023) including six species of the genus Epidendrum L. (Orchidaceae). As well as three exotic species to the Brazilian territory: Commelina benghalensis L. (Commelinaceae, Commelinales) (Trapoeraba) (Figure 3e); Tradescantia zebrina Heynh. ex Bosse (Commelinaceae, Commelinales) (Zebrinha); and the Dendrocalamus giganteus Wall. ex Munro (Poaceae-Poales) (Bambu-Gigante).

Magnoliopsida (Plantae) was the most diverse class in this study, with 528 recorded species distributed across 90 families and 32 orders. The five families with the greatest diversity were Fabaceae (Fabales), Myrtaceae (Myrtales), Euphorbiaceae (Malpighiales), Rubiaceae (Gentianales), and Piperaceae (Piperales), with 106, 44, 24, 22, 22 species recorded respectively. Magnoliopsida is the class with the most research carried out (46 of the 135 studies), having several sampling points throughout the Serra de Baturité EPA (Figure 5a). 133 species endemic to Brazilian territory belonging to the Magnoliopsida class were recorded, such as Begonia reniformis Dryand. (Begoniaceae, Cucurbitales) (Begonia); Begonia convolvulacea (Klotzsch) A.DC. (Begoniaceae, Cucurbitales) (Begonia); Manilkara rufula (Miq.) H.J.Lam (Sapotaceae, Ericales) (Maçaranduba); the Cereus jamacaru DC. subsp. jamacaru (Cactaceae, Caryophyllales) (Mandacarú); among others. As well as 20 species indicated as exotic, such as the Amaranthus cruentus L. (Amaranthaceae, Caryophyllales) (Crista-de-galo); Pachira aquatica Aubl. (Malvaceae, Malvales) (Munguba); (Syzygium cumini (L.) Skeels (Myrtaceae, Myrtales) (Jambolão); the Azadirachta indica A.Juss. (Meliaceae, Sapindales) (Neem-Indiano); the Lantana camara L. (Verbenaceae, Gentianales) (Camará-chumbinho) (Figure 3f); and others, in addition to 11 species being threatened with extinction, such as the Cedrela odorata L. (Meliaceae, Sapindales) (Cedro) and the Cereus jamacaru DC. subsp. jamacaru (Cactaceae, Caryophyllales) (Mandacarú), all present in the Serra de Baturité EPA.

Figure 5
Map of taxon registration sites in the Serra de Baturité EPA. (a) Class Magnoliopsida. (b) Class Secernentea. (c) Class Gastropoda. (d) Class Insecta. (e) Class Arachnida. (f) Class Amphibia. (The location corresponding to the numbers are indicated in Chart 2).
1.5.
Animalia

In the Serra de Baturité EPA, 672 species belonging to the Animalia kingdom were listed, distributed in 127 families, 41 orders, eight classes, and four phyla (Nematoda, Mollusca, Arthropoda, and Chordata) (Chart 7).

Chart 7
List highlighting the record of species from the kingdom Animalia, indicating their vernacular names (common), vulnerability status, CITES Appendix number, exotic status, records locations in the Serra de Baturité EPA and references; also being indicated: (Ѫ) species threatened with extinction at the national level; (Ѧ) internationally threatened species; (Ψ) species endemic to Brazilian territory; (Ҩ) migratory species; (ɸ) exotic species.

For the phylum Nematoda, one species was recorded, Meloidogyne javanica (Treub) Chitwood (Nematóide-das-galhas), belonging to the family Heteroderidae (Tylenchida, Secernentea), recorded by Assunção & Souza-Junior, (2022) in the municipality of Guaramiranga (Figure 5b).

For the phylum Mollusca Betanho et al. (2016), recorded 13 taxa distributed in the Serra de Baturité EPA in five locations, in the municipalities of Guaramiranga, Mulungu and Pacoti (Figure 5c). These species are subdivided into nine families belonging to the order Stylommatophora and class Gastropoda. The occurrence of a species endemic to Brazilian territory Tomigerus rochai Ihering, 1905 (Odontostomidae) (Caracol) and an exotic species Achatina (Lissachatina) fulica (Bowdich, 1822) (Achatinidae) (Caramujo-gigante-africano) was verified.

For the phylum Arthropoda were hired in this work 234 species of arthropods were listed for the Serra de Baturité EPA, subdivided in two classes, Arachnida (with 16 species listed) and Insecta (with 234 species), subdivided into five orders: Diptera, Hemiptera, Hymenoptera, Lepidoptera. The five families with the highest number of species were Apidae (Hymenoptera) (Figure 6a) with 82 species listed, followed by Formicidae (Hymenoptera) with 71 spp., Psychodidae (Diptera) with 18 spp. and Megachilidae (Hymenoptera) with 10 spp. A total of 23 studies were carried out that analyzed 14 sampling sites located in the municipalities of Guaramiranga, Mulungu, and Pacoti (Figure 5d). Seven species of endemic insects belonging to the orders Diptera (Deanemyia samueli (Deane, 1955) (Mosquito-palha); Micropygomyia (Sauromyia) villelai (Mangabeira, 1942) (Mosquito-palha)); and Hymenoptera (Melitoma ipomoearum Ducke, 1912 (Abelha); Melitomella cf. murihirta (Abelha); Mesonychium asteria (Smith, 1854) (Abelha)); as well as two endangered species, the and bees: Melipona (Michmelia) rufiventris Lepeletier, 1836 (Abelha); and Melipona (Michmelia) scutellaris Latreille, 1811 (Abelha). Four species of introduced exotic Diptera were also recorded: Evandromyia (Aldamyia) sericea (Floch & Abonnenc, 1944) (Mosquito-palha); Micropygomyia (Sauromyia) quinquefer (Dyar, 1929) (Mosquito-palha); Micropygomyia (Sauromyia) trinidadensis (Newstead, 1922) (Mosquito-palha); and Sciopemyia sordellii (Shannon & Del Ponte, 1927) (Mosquito-palha).

Figure 6
Taxons registered in the Serra de Baturité EPA. (a) Centris tarsata Smith, 1874. (Apidae, Hymenoptera) (Abelha-de-óleo). (b) Macrophyes pacoti Brescovit et al. (2019) (Aranha) (Anyphaenidae, Araneae). (c) Rhinella dapsilis (Myers & Carvalho, 1945) (Bufonidae, Anura) (Sapo-folha). (d) Boa constrictor constrictor Linnaeus, 1758 (Boidae, Squamata) (Jibóia). (e) Columbina talpacoti (Temminck, 1811) (Columbidae, Columbiformes) (Rolinha-caldo-de-feijão). (f) Glossophaga soricina (Pallas, 1766) (Phyllostomidae, Chiroptera) (Morcego-beija-flor) feding on banana flower nectar Musa sp. (Musaceae, Zingiberales) (Bananeira) (Photos: J.C. Pires). Scale bars: 1 cm.

For the class Arachnida (Arthropoda), 16 species were listed, distributed across four orders (Araneae, Ixodida, Opiliones and Scorpiones) and nine families, with Linyphiidae (Araneae) and Theridiidae (Araneae) being the most diverse, with three species listed for each family, followed by Araneidae (Araneae), Ixodidae (Ixodida) and Stygnidae (Opiliones) with two species each; and by the Buthidae family (Scorpiones) with one species (Tityus maranhensis Lourenço, Jesus Junior & Limeira-de-Oliveira, 2006 (Escorpião-amarelo)). 13 studies carried out records in seven sampling sites belonging to the Serra de Baturité EPA, distributed in the municipalities of Guaramiranga, Mulungu and Pacoti (Figure 5e), among them the study by Brescovit et al. (2019), which recorded the spider Macrophyes pacotiBrescovit et al. 2019 (Aranha) as a new species (Figure 6b).

Studies aimed at recording the occurrence from classe Amphibia in the Serra de Baturité EPA are concentrated in the municipality of Guaramiranga, Baturité and Pacoti (Figure 5f), being registered 49 species in the Serra de Baturité EPA, distributed in two orders (Anura and Gymnophiona) and nine families, with Hylidae (Anura) being the most diverse family with 15 described species, followed by the family Leptodactylidae (Anura) with 13 species. Such as the Rhinella dapsilis (Myers & Carvalho, 1945) (Sapo-folha) (Figure 6c); the Proceratophrys cristiceps (Müller, 1884) (Sapo-boi); the Caecilia tentaculata Linnaeus, 1758 (Cobra-cega); among other species. 20 endemic Anura species were listed, including some species from the genera Rhinella Fitzinger, 1826 (Bufonidae); Dendropsophus Fitzinger, 1843 (Bufonidae); Leptodactylus Fitzinger, 1826 (Leptodactylidae); Scinax Wagler, 1830 (Hylidae), Proceratophrys Miranda-Ribeiro, 1920 (Odontophrynidae), among others. In addition to three invasive alien species: Rhinella jimi (Stevaux, 2002) (Bufonidae) (Sapo-boi); Scinax x-signatus (Spix, 1824) (Hylidae) (Perereca); and Leptodactylus labyrinthicus (Spix, 1824) (Leptodactylidae) (Rã-pimenta).

In the Serra de Baturité EPA, the Reptilia class was the second most diverse between Chordata, with 84 species distributed in 18 families and one order (Squamata), inventoried through 19 studies that took place in 23 sampling sites, having a wide distribution throughout of the Serra de Baturité EPA (Figure 7a). With 41 species, the Colubridae family was the most diverse, followed by Gymnophthalmidae with seven spp.. They are generally habitat specialists, often not surviving in distinct or anthropically altered environments (MMA, 2008b), which encourages the preservation of this EPA. 13 endemic Squamata species are indicated, among them the Leposoma baturitensisRodrigues & Borges, 1997 (Gymnophthalmidae) (Calango), the Epicrates assisi Machado, 1945 (Boidae) (Jibóia-arco-íris); the Dipsas albifrons (Sauvage, 1884) (Colubridae) (Dormideira), the Micrurus ibiboboca (Merrem, 1820) (Elapidae) (Cobra-coral), the Bothrops erythromelas Amaral, 1923 (Viperidae) (Jararaca-da-seca), the Tropidurus semitaeniatus (Spix, 1825) (Tropiduridae) (Calango-de-lajeiro), among other endemic species, in addition to seven threatened species, among them the Boa constrictor constrictor Linnaeus, 1758 (Boidae) (Jibóia) (Figure 6d).

Figure 7
Map of taxon registration sites in the Serra de Baturité EPA. (a) Class Reptilia. (b) Class Aves. (c) Class Mammalia. (The location corresponding to the numbers are indicated in Chart 2).

The Aves class (Chordata) had the largest number of cataloged animal species for the Serra de Baturité EPA, with 259 species distributed in 20 orders and 51 families recorded through six studies (Rodrigues et al. 2004; Albano & Girão, 2008; Capllonch & Soria, 2009; Asa-Branca, 2011a, b; Portela et al. 2022). Tyrannidae (Passeriformes) was the family with greater richness, consisting of 45 species, followed by Thraupidae (Passeriformes) with 28 spp., Furnariidae (Passeriformes) with 19 spp., Trochilidae (Apodiformes) with 17 spp. and Accipitridae (Accipitriformes) with 15 recorded species. Due to great public sympathy, such species can be used as “flag species”. They can also promote the protection of habitats, in which species have fidelity to use, being good indicators of environmental conservation (MMA, 2008b). Some species, such as the Columbina talpacoti (Temminck, 1811) (Rolinha-caldo-de-feijão) (Figure 6e), have adapted to urban environments for a long time, having larger populations in anthropogenically altered locations than in their original habitats. (WikiAves, 2023). The occurrence sites are concentrated in the municipality of Guaramiranga, with records also being made in Baturité and Pacoti (Figure 7b). Among Aves, 26 endemic species, 38 endangered species, and 33 migratory species were recorded. The Pyrrhura griseipectus Salvadori, 1900 (Psittacidae, Psittaciformes) (Periquito-Cara-suja); the Anopetia gounlei (Boucard, 1891) (Trochilidae, Apodiformes) (Marronzinho) and the Heliomaster squamosus (Temminck, 1823) (Trochilidae, Apodiformes) (Beija-flor-bico-reto-de-banda-branca), deserve attention sice they are endemic and threatened species.

For the Mammalia class in the Serra de Baturité EPA, 33 species were listed, distributed in eight orders (Artiodactyla, Carnivora, Chiroptera, Cingulata, Didelphimorphia, Pilosa, Primates, Rodentia) and 16 families, obtained through six studies (Tribe, 2005; Percequillo et al. 2008; Asa-Branca, 2011a; Fernandes-Ferreira et al. 2015; Leal et al. 2017; Portela et al. 2022) that occurred in seven sampling locations in the municipalities of Baturité, Guaramiranga, Mulungu and Pacoti (Figure 7c). Phyllostomidae (Chiroptera) was the most diverse family with nine species recorded, followed by Felidae (Carnivora) and Didelphidae (Didelphimorphia) with three spp. registered to the EPA. Seven species were listed as endemic, the primate Callithrix jacchus (Linnaeus, 1758) (Callitrichidae) (Sagui) and the rodents: Galea spixii (Wagler, 1831) (Caviidae) (Preá); the Kerodon rupestris (Wied-Neuwied, 1820) (Caviidae) (Mocó); the Cerradomys langguthiPercequillo, Hingst-Zaher & Bonvicino, 2008 (Rato-do-chão), and the Rhipidomys cariri baturitensisTribe, 2005 (Rato-da-árvore) belonging to the Cricetidae family; the Thrichomys apereoides (Lund, 1839) (Echimyidae) (Punaré) and the Coendou baturitensis Feijó & Langguth, 2013 (Erethizontidae) (Coandú), in addition to nine endangered species.

2.

Endemic species

In this study, there were 206 endemic species in the Brazilian territory, they were listed in the Serra de Baturité EPA, representing 15% of the total species listed. Among the 153 endemic plant species (Chart S1), the Magnoliopsida class had 133 endemic species, followed by the Lilipsida and Pteridopsida classes with respectively 19 and one endemic species. In addition, 73 endemic species: 26 aves, 20 amphibians, 13 reptiles, seven mammals), seven insects (Arthropoda) and a single gastropod (Mollusca) (Chart S2).

3.

Endangered species

Habitat fragmentation, the introduction of invasive species (with 36 exotic species already listed), hunting, and animal trafficking, among other factors observed within the Protected Area, cause various damages to biodiversity, and threaten populations most affected when in smaller numbers (Fernandes-Ferreira et al. 2015). In particular, hunting has put at the risk of extinction six species that are prey to carnivores or carnivores themselves (invluding top predators): Penelope jacucaca (Jacu-verdadeiro); Odontophorus capueira Spix, 1825 (Uru); Leopardus pardalis Linnaeus, 1758 (Jaguatirica); Leopardus tigrinus Schreber, 1775 (Gato-do-mato-pequeno); Leopardus wiedii Schinz, 1821 (Gato-maracajá); Puma concolor Linnaeus, 1771 (Onça-parda) and Puma yagouaroundi (Gato-mourisco). Animal trafficking, in turn, has mainly put pressure on three species of birds: Pyrrhura griseipectus Salvadori, 1900 (Periquito-Cara-suja); Procnias averano Hermann, 1783 (Ferreiro); Tangara cyanocephala cearensis Cory, 1916 (Pintor-da-serra-de-Baturité), and Spinus yarrellii Audubon, 1839 (Pintassilgo-do-nordeste). Furthermore, according to Fernandes-Ferreira et al. (2015), in the Baturité Massif: “Some species are also kept by residents as pets, such as Callithrix jacchus Linnaeus, 1758 (Sagui); Procyon cancrivorus Cuvier, 1798 (Guaxinim); Mazama gouazoubira Fischer, 1814 (Veado-catingueiro); Puma yagouaroundi (Gato-mourisco) and Tamandua tetradactyla Linnaeus, 1758 (Tamanduá-mirim), or even for medicinal practices”.

3.1.
Threatened species according to MMA decree No. 148, 2022

In this study we indicate 16 species as Vulnerable, as well 16 Endangered (EN), and 2 Critically Endangered species, totaling 34 species threatened with extinction in Serra de Baturité EPA (MMA, 2022). Of these, 13 species are endemic to Brazilian territory, all Vulnerable to extinction, namely Xiphocolaptes falcirostris Spix, 1824 (Arapaçu-do-nordeste); Xiphorhynchus atlanticus (Cory, 1916) (Arapaçu-rajado); Tangara cyanocephala cearensis Cory, 1916 (Pintor-da-serra-de-Baturité); Hemitriccus mirandae Snethlage, 1925 (Maria-do-nordeste) and Penelope jacucaca Spix, 1825 (Jacupemba); in addition to the birds Conopophaga cearae Cory, 1916 (Chupa-dente); Sclerurus cearensis Snethlage, 1924 (Vira-folhas); Pyrrhura griseipectus Salvadori, 1900 (Periquito-Cara-suja); the reptiles Atractus ronniePassos, Fernandes & Borges-Nojosa, 2007 (Cobra-da-terra) and Leposoma baturitensisRodrigues & Borges, 1997; the endemic plant Callianthe bezerrae (Monteiro) Donnel classified as In Danger of extinction; and the amphibian Rhinella casconiRoberto, Brito & Thomé, 2014 and the bird Odontophorus capueira (Spix, 1825) (Uru-do-Noreste) was considered Critically Endangered (Chart S3, S4).

3.2.
Threatened species according to appendices I, II and III of CITES (2023)

We listed 76 threatened species for Serra de Baturité EPA. In Chart S5, two threatened species present in the Serra de Baturité EPA whose international trade is prohibited were listed: Falco peregrinus Tunstall, 1771 (Falcão-peregrino) and Leopardus tigrinus (Schreber, 1775) (Gato-do-mato-pequeno); as well as 72 species distributed in the kingdoms Plantae and Animalia, 34 species of animals and 38 species of plants, whose level of threat is of little concern, however, international trade must be strictly controlled to avoid an increase in the level of threat, among which mainly several species of orchids (Orchidaceae) and hummingbirds (Trochilidae) are listed; in addition to two species protected in certain countries: Platyrrhinus lineatus (E. Geoffroy, 1810) (Morcego-de-linha-branca) and Crotalus durissus Linnaeus, 1758 (Cascavel).

4.

Exotic species

In Serra de Baturité EPA, 36 species exotic to Brazilian territory were listed, 23 being plants and 13 animals, among them the plants: Coffea arabica Linn. (Rubiaceae, Fabales) (Café), the Dendrocalamus giganteus Wall. ex Munro (Poaceae, Poales) (Bambu-gigante), the Mangifera indica L. (Anacardiaceae, Sapindales) (Mangueira), among others; as well as birds: Estrilda astrild Linnaeus, 1758 (Bico-de-lacre), Passer domesticus Linnaeus, 1758 (Pardal); the amphibian Rhinella jimi (Stevaux, 2002) (Sapo-cururu); the mollusc Achatina (Lissachatina) fulica (Bowdich, 1822) (Caramujo-gigante-africano), among other species (Chart S6, S7).

5.

Migratory species

Only birds were recorded as migratory, and 33 species were found, such as the species Sublegatus modestus (Wied-Neuwied, 1831) (Sertanejo), the Lathrotriccus euleri (Cabanis, 1868) (Enferrujado), the Machetornis rixosa (Vieillot, 1819) (Bem-ti-vi-do-gado), the Pitangus sulphuratus (Linnaeus, 1766) (Bem-ti-vi), the Falco peregrinus Tunstall, 1771 (Falcão-peregrino), the Anthracothorax nigricollis (Vieillot, 1817) (Beija-flor-de-vesta-preta), and others (Somenzari et al. 2018) (Chart S8).

6.

Beta diversity analysis - sorensen similarity index

We list 2,652 plant species in the Itatiaia National Park, 1,029 in the Pico da Neblina National Park, 770 species in the Sempre-Vivas National Park, compared to the 654 plant species present in the Serra de Baturité EPA. Of which, the Serra de Baturité EPA shares 128, 31, and 30 species, with the national parks of Itatiaia, Pico da Neblina, and Sempre-Vivas, respectively (Figure 8).

Figure 8
Venn diagram with four sets indicating species sharing of flora species between the Protected Areas.

Low similarity values were obtained in all spatial units, with the Itatiaia National Park unit showing greater similarity compared to the Sempre-Vivas National Park and the Serra de Baturité EPA (CS = 0.08 and CS = 0.07). In the comparison between the Serra de Baturité EPA and the Pico da Neblina National Park, the values of CS = 0.03 were obtained, followed by the analysis between the Serra de Baturité EPA and the Sempre-Vivas National Park, with the values of 0.04 similarity. The lowest similarity values were found comparing the flora of the Pico da Neblina National Park, with the Itatiaia and Sempre-Vivas National Parks, with similarity values of 0.02 (Table 1).

Table 1
Number of plant species present and shared by each spatial unit analyzed to obtain the Sorensen Similarity Index.

Discussion

The present research represents the first effort to realize the biodiversity compilation of the five kingdoms in the Serra de Baturité EPA. An inventory of Flora and Fauna in the State of Ceará was recently carried out, documenting 6,333 species (SEMA, 2021a, b, c). The Flora list is made up of 2,465 species, belonging to 153 families. For Fauna, 3,868 species of animals were listed, of which 1,275 are vertebrates and 2,593 invertebrates distributed in 19 different groups (SEMA, 2021a, b, c). Our results point out to the fact that the biodiversity at the Serra de Baturité EPA is relatively high, representing 21% of total species registered to Ceará state, in addition to differing from those found in studies carried out in other protection units that posses great diversity (Table 2). Despite that, we notice that some groups did not have an adequate inventory to verify the region’s real biodiversity, a sampling bias was observed focusing records from the kingdoms Plantae and Animalia. This can be observed mainly in relation to the Monera, Protista and Fungi kingdoms.

Table 2
Comparison of kingdom diversity at different geographic scales.

For the Monera kingdom only one specimen was recorded incidentally, belonging to the genus Rickettsia. The Monera kingdom is made up of unicellular microorganisms with great ecosystem importance, being essential in the nitrogen, sulfur, carbon, and oxygen cycles (Moreira, 2015). Around 10,00 species from this kingdom are cataloged (Brusca et al. 2018). Currently, they are widely used in the food and pharmaceutical industries, whether in the production of antibiotics or in the manufacture of yogurt, wine, cheese, and other foods, in addition to having great medical importance due to some species being pathogenic to humans (Moreira, 2015). The Rickettsia genus has around 30 species described worldwide, some species such as R. prowazekii da Rocha-Lima, 1916, R. typhi (Wolbach & Todd, 1920) Philip, 1943, and R. rickettsii (Wolbach, 1919) Brumpt, 1922, which infect animals and later, humans, causing Typhus disease (transmitted by lice, fleas) and Maculosa fever (usually transmitted by hard ticks) (Ismael, 2022). Therefore, more studies on the Rickettsia species present in the Serra de Baturité EPA are extremely important to prevent and control cases in the region, as well as more studies aimed at new records of other groups from the Monera kingdom.

As in the Protista kingdom, which currently has around 200,000 described species (Brusca et al. 2018), with only one species incidentally recorded (Trypanosoma cruzi) at the Serra de Baturité EPA. This species has medical importance because it transmits Chagas disease (Dias, 2006), with a great genetic diversity, Chagas disease is caused by the parasite T. cruzi, which is transmitted to animals and people by insect vectors (Hemíptera, Reduviidae, Triatominae) (Dias, 2006). Protists play multiple roles in the biosphere, having a fundamental role in carbon and nutrient cycling in aquatic and terrestrial ecosystems (Singer et al. 2021). Despite this importance, the richness of protists is not truly described (Singer et al. 2021).

It was registered from the Serra de Baturité EPA, to the Fungi kingdom, 10 species subdivided in three Phyla (Ascomycota, Basidiomycota e Glomeromycota), however this number is underrated, once that the Fungi kingdom represents the second largest group of eukaryotes, only behind insects (Heads et al. 2017). Approximately 99,000 species of fungi are cataloged (Kirk et al. 2008), representing only 6.6% of the estimated 1.5 million species worldwide (Hawksworth, 2001). For the phylum Ascomycota, around 3,710 species are known in Brazil (Lewinsohn & Prado, 2005), present in different places, such as in soil, air, water, manure, plants (wood, leaves, fruits, etc.), animals (including humans), and other substrates (Lacaz et al. 1970). As for the phylum Basidiomycota, around 9,000 species are recorded at the Brazilian territory (Lewinsohn & Prado, 2005). Such fungi use varied substrates, acting as saprophytes or parasites in the soil, wood, and living plants or decomposing organic matter (Lacaz et al. 1970). The phylum Glomeromycota is the result of a process of co-evolution of symbiotic associations between the roots of higher plants, and is currently well documented in most plants, being called mycorrhiza (Siqueira & Franco, 1988). Around 75% of known vascular plants carry out such an association, where the plant benefits from the increased capacity to capture water and nutrients from the soil, and in exchange the fungus receives carbohydrates and vitamins essential for its development (Sotão et al. 2004). Such interaction has great commercial utility, aiming to increase agricultural production, reduce costs and environmental data arising from the use of fertilizers in modern systems (Souza et al. 2006).

In the floristic survey, 654 species were found that belong to the Plantae kingdom. This number highlights that more studies are still needed to inventory the true biodiversity of the Serra de Baturité EPA, once that there are known between 263,800 and 279,400 plant species that are currently recognized worldwide (Lewinsohn & Prado, 2005), of which 46,447 are in Brazil (ICMBio, 2018a), where around 40,000 species belong to the Magnoliopsida class (Lewinsohn & Prado, 2005), being the most diverse class of the group. About the families registered by the survey, Magnoliopsida, Liliopsida, stood out for the greater species richness, Magnoliopsida and Liliopsida, representing 94% (615 species) from the studies species. However, yet there are groups that haven’t been studied enough, such as the Bryopsida class, where only three species were found, therefore this number is underrated, once it appears in great diversity and abundance in areas with high humidity, managing to establish itself in places unsuitable for other plants since they are present even on granite cliffs (Raven et al. 1992). Where around 3,100 species of this class are known for the Brazilian territory (Lewinsohn & Prado, 2005). They can be used as environmental indicators due to their sensitivity to atmospheric pollution, therefore, the absence of certain species indicates low environmental quality, mainly related to high levels of carbon dioxide (Raven et al. 1992).

As for the animal kingdom, we found that the Serra de Baturité EPA has important zoological representation, where the phylum Chordata is the richest among animals, with 426 spp. distributed into four classes (Amphibia, Reptilia, Aves, Mammalia). However, this is a consequence of a scientific bias mainly related to extensive surveys recording Aves species present in the Serra de Baturité EPA, responsible for 60% of Chordata records. Therefore, although Arthropoda has more research in the EPA than Chordata (35 and 30 publications, respectively), publications on Chordata aim to study a larger number of taxa. The Animalia kingdom comprises more than one million species known worldwide of vertebrates and invertebrates (Felix et al. 2010), in Brazilian territory currently 117,096 species are recognized, where around 94,000 species are arthropods and 9,000 vertebrates (ICMBio, 2018a, c). Among vertebrates, we can mention the class Reptilia (Chordata) has 8,000 species registered worldwide, of which 732 species are found in Brazil (Brasil, 2008b; ICMBio 2018d). Just like amphibians, there are 6,100 known species in the Amphibia (Chordata) class in the world, of which 1,080 species are located in Brazil, the country with the greatest amphibian richness in the world (MMA, 2008b; ICMBio, 2018e). Species in this class have great ecological importance since they are excellent predators, capturing mainly invertebrates in aquatic and terrestrial environments, as well as being algae eaters, carnivores, detritivores, filter feeders, detritivores or omnivores in their larval phase, since numerous species have a two-phase life cycle (Brasil, 2008b). They serve as food for various animals, such as reptiles, birds, mammals, fish, and even other amphibians and invertebrates. Furthermore, they are indicators of environmental quality due to their permeable and exposed skin, and they also secretly activate biological substances used in pharmacological research (Brasil, 2008b).

Still in the phylum Chordata, a total of 732 species of mammals are recognized at the Brazilian territory, distributed in 12 orders, covering continental (681 spp.) and aquatic mammals (51 spp.), making Brazil the second country with the greatest richness of mammals in the world. world (ICMBio, 2018a, b, f). Due to their beauty, diversity, and usefulness, Homo sapien’s interest in other mammals is long-standing, starting from the coexistence with the Neotropical megafauna existing in South America (Reis et al. 2006). Currently, people’s interest in mammals is still great, which is also evidenced by the problems they can cause (Reis et al. 2006), for example, rodents that can be considered urban pests but can also be used as guinea pigs in experiments in biological sciences and medical (Reis et al. 2006). Other species are hunted for food, such as primates and wild pigs (Reis et al. 2006; Brasil, 2008b), as well as being hunted because they are carnivores, to the detriment of livestock farmers and domestic animal breeders (Brasil, 2008b). Furthermore, this class of living beings has great ecological importance, such as individuals of the order Chiroptera, which regulate insect populations, disperse plant seeds and pollen, in addition to providing nutrients through fertilizer (guano) (Reis et al. 2006), such as the Glossophaga soricina (Pallas, 1766) (Morcego-beija-flor) (Figure 6f).

Thus, 33 species of mammals, 84 species of reptiles and 49 amphibians and 248 invertebrates were listed. Therefore, we also observed a sampling bias for Chordata, once that the five most diverse classes are insects with 83,000 species, arachnids with 6,200 spp., fish with 4,545 spp., molluscs with 3,100 spp., and birds with 1,979 species registered in Brasil (ICMBio, 2018a, c) with 67 specimens, focused on a vertebrates bias. An example of this is the class Nematoda, where only one specie were found.

Another underrated class are the Molluscs, being found 13 species and it has great ecological and economic importance, playing important roles in the different trophic levels of ecosystems, but can also be considered agricultural pests or used as a food resource (MMA, 2008 a). A total of 3,000 species are known in the Brazilian territory (Lewinsohn & Prado, 2005). It is estimated that there are 50,000 to 200,000 species in the world (Brasil, 2008b), being considered the second most diverse group in the kingdom Animalia (MMA, 2008a).

Just like arthropods, which in the phylum Arthropoda, where only 234 species were recorded, however there are more than one million species are known worldwide, of which around 118,290 are in Brazil (Lewinsohn & Prado, 2005), however, it is assumed that there is a seven times greater quantity that has not yet been discovered (Lewinsohn & Prado, 2005).

As well as understanding migration patterns of such species and their population dynamics at different times of the year is of great importance for planning broad and long-term conservation actions, as well as understanding the causes and ecological and evolutionary mechanisms that drive such migrations. (Somenzari et al. 2018). Such as understanding that threatened species are those that are at risk of extinction because their populations are in sharp decline, as are their habitats (MMA, 2014). Therefore, it is essential to study and map such species to avoid their extinction. Since in this study 33 migratory species, 110 endangered species and 206 endemic species of Brazilian territory were cataloged, highlighting the importance of the Serra de Baturité EPA, as a shelter and restoration environment for organisms that perform important ecological functions, The preservation of this relictual area is of utmost importance in a State (Ceará) that has around 80% of its territory altered by human actions (MMA, 2006).

In addition, raising awareness about the introduction of exotic species, since 36 exotic species have been listed. The introduction of species threatens the permanence of native species, since introduced species generally do not encounter predators or competitors and thus multiply, occupying large areas more easily, being considered the second main cause of biodiversity loss in the world, originating accidentally or intentionally (SMA, 2010). Although the removal of these non-indigenous species is possible, the process will cause unpredictable negative impacts on non-target species, requiring planning that identifies the behaviors and population dynamics of these exotic species, as well as promoting the cooperation of the remaining communities (Myers et al. 2000).

The implementation of the Serra de Baturité EPA has contributed to the protection and recovery of a considerable part of the biological diversity (Silva, 2015; Ribeiro et al. 2022), however in terms of management, there is still no consolidated program for the conservation of flora and fauna, as well as more specific policies for the conservation of threatened or endemic species present in the region (Silva, 2015). Given this, as the Serra de Baturité EPA is a Sustainable-use Protected Area, it is essential that the management council also rethink some paradigms related to land use and occupation in the region, which must be based on the concept of sustainable cities. In order to reach the sustainability of natural resources, preservation of biodiversity and human development, it is necessary to provide socio-economic environmental education actions to residents, aiming to inform and raise awareness of what is at stake, knowing the context of the Protected Area and its biodiversity. This can subsidize conservation planning and actions, such as water reuse projects, afforestation with native plants, and avoiding the occupation of slopes.

Some solutions can be implemented to make the region more sustainable, in addition to monitoring and offering technical training courses and development of ecotourism (ONU, 2015; Silva et al. 2016b; Zanini & Rocha, 2020), especially in areas with greater tourist demand, such as Baturité, Guaramiranga, Mulungu and Pacoti (Arruda & Fedel, 2020, Ribeiro et al. 2022), as well as in areas that are yet to be explored, as is the case of the municipality of Aratuba, which has 56.70% of its territory in the Serra de Baturité EPA, but only two studies were found (Lima & Mansano, 2011; Franco et al. 2017). It would also be important to involve the population, ensuring participatory management in the protection of the perimeter covered by the Protected Area, and surroundings, also helping in reporting indiscriminate actions of degradation and, thus, discouraging the suppression of biodiversity caused by habitat loss, agriculture, real estate speculation, wild animal trafficking, and hunting (Albano & Girão, 2008).

The current overexploitation of natural resources puts biodiversity and the maintenance of ecological processes provided by it at risk. Therefore, the decrease in biodiversity must be treated as a high environmental priority, just like climate change, also requiring public investment to carry out field collections and the implementation of local museum collections, which allow to carry out conservation and ecological awareness actions with residents and tourists (Alho, 2008; MMA, 2008a). For example, the Pyrrhura griseipectus Salvadori, 1900) (Periquito-Cara-suja), classified as endanger of extinction, has been studied (distribution, biology and identification) since 2007 by the NGO AQUASIS combined with educational actions with residents to preserve the species and implement nest boxes aimed at reproductive management of the Black-faced parakeet population, contributing to reproductive success and population increase (Nunes, 2017).

Thus, despite the great dissimilarity between the communities the spatial units analyzed, it is suggestive that the biodiversity of the Serra de Baturité EPA was influenced by the biodiversity of the Amazon Forest (Pico da Neblina National Park, as well as the Atlantic Forest (Itatiaia National Park), having greater similarity with the latter; being influenced by the union of these biomes in the Pliocene and Pleistocene, where isolation in the terminal Pleistocene provided the diversification of endemic biodiversity evidenced in this work (Mendonça, 2001; Batalha-Filho et al. 2013; Abreu & Barbosa, 2016). Therefore, it is essential to preserve the entire structure of these communities, especially the Serra de Baturité EPA, since this “altitude marsh” has a much smaller geographic size when compared to the Pico da Neblina and Sempre-Vivas National Parks, in addition to being isolated from other forest fragments, and above all because it is a Sustainable Use Protected Area, further enabling a decrease in the number of species and an increase in extinction rates, thus, it is urgent to reduce the negative pressures that negatively affect the probability of survival of species present in the Serra de Baturité EPA (Peroni & Hernández, 2011).

Conclusion

The total number of species listed in this work (1,338) in the Serra de Baturité EPA represents 21% of the total species (6,333) in the State of Ceará, highlighting the importance of preserving this relictual area that houses species from the five kingdoms of living beings; among them a species of Monera, a species of Protista, nine species of Fungi, 654 species of Plantae, and 672 species of Animalia. Of which 15% (206) are species endemic to Brazilian territory. In addition to being a refuge for 110 threatened species and 33 species of migratory birds. Therefore, the Serra de Baturité EPA constitutes an area of extreme biological importance, being a priority area for the conservation of flora and fauna (MMA, 2000; Bencke et al. 2006).

We hope that this article can serve as another argument for society to guarantee the continuity of biodiversity in the Serra de Baturité EPA, as it highlights the large number of species and their distribution in the region’s native forestand, in this way, also preserving the remaining Atlantic Forest in the Northeast, since today this biome occupies less than 10% of its original territory (Campanili & Prochnow, 2006), being considered the second most endangered biome in the world and also being among the top five on the lists of global hotspots (Campanili & Prochnow, 2006), since it reports on the various endemic species, threatened with extinction, as well as migratory and exotic species, promoting knowledge of the biota of this relictual area, facilitating dissemination and consequently promoting the need to preserve the biota of the Baturité Massif in its entirety. We also hope to have encouraged new studies on biodiversity, as the biodiversity listed represents only a small portion of the real biodiversity, and the kingdoms Monera, Protist and Fungi (Figure 9a) can be mentioned, as well as the classes Briopsida (Plantae) and Pteridopsida (Plantae), Arachnida (Animalia), Gastropoda (Animalia) and orders such as Diptera (Animalia) and Hemiptera (Animalia) which have great biodiversity in Brazil, however, few species were recorded for the Serra de Baturité EPA.

Figure 9
Taxons not yet recorded in the Serra de Baturité EPA. (a) Mushroom Coprinus comatus (Müller, 1780) (Agaricaceae, Agaricales). (b) Platyphora sp. (Chrysomelidae, Coleoptero) (c) Eryphanis automedon (Cramer, 1775) (Nymphalidae, Lepidoptera). (d) Insects of the order Orthoptera. (e) Insect Phrictus diadema (Fulgoridae, Hemiptera) (Jequitiranabóia-cabeça-de-verruga). (f) Insect of the order Phasmatodea (Bicho-pau) (Photos: J.C. Pires). Scale bars: 1 cm.

More drastically, there is no record of several broad taxa, for example, fish and algae, as well as large orders of arthropods, such as Acari, Blattodea, Coleoptera (Figure 9b), Isoptera, Lepidoptera (Figure 9c), Mantodea, Orthoptera (Figure 9d), among others (Figure 9e, f). Therefore, it is clear that new studies are needed to understand the true diversity of the region, avoiding gaps between knowledge of biodiversity (Hortal et al. 2015) and potential future scientific values.

Supplementary Material

The following online material is available for this article:

Chart S1 - List of plant species endemic to Brazilian territory. Species that are threatened with extinction nationally are also indicated, according to MMA ordinance n° 148, 2022 (symbol Ѫ); internationally threatened species, according to CITES Appendices I, II, III (symbol Ѧ).

Chart S2 - List of animal species endemic to Brazilian territory, their vernacular names (common) and citation references for endemics. Nationally endangered species are indicated, according to MMA Ordinance No. 148, 2022 (Ѫ); internationally threatened species, according to CITES Appendices I, II, III (Ѧ); and migratory (Ҩ).

Chart S3 - List of threatened animal species according to MMA Ordinance No. 148, 2022, with their vernacular names and vulnerability status indicated, and species endemic to Brazilian territory (Ψ) and threatened with extinction internationally, according to CITES Appendices I, II, III (Ѧ).

Chart S4 - List of threatened plant species according to MMA Ordinance No. 148, 2022, with their vernacular names and vulnerability status indicated. They are also indicated as species endemic to Brazilian territory (Ψ); and internationally threatened species, according to CITES Appendices I, II, III (Ѧ).

Chart S5 - List of threatened species (animals and plants) according to the Appendices CITES (Convention on International Trade in Endangered Species of Wild Flora and Fauna), with their vernacular names and vulnerability status indicated, as well as endemic species (Ψ); threatened with extinction nationally, according to MMA ordinance n° 148, 2022 (Ѫ); exotic (ɸ) and migratory (Ҩ) species.

Chart S6 - List of plant species exotic to Brazilian territory, indicating their vernacular names (common), exotic status and their status and citation reference for exotic species.

Chart S7 - List of species of animals exotic to Brazilian territory, indicating their vernacular names (common), exotic status and citation reference of exotic species, also identifying species threatened with extinction internationally, according to CITES Appendices I, II, III (Ѧ).

Chart S8 - List of migratory bird species, indicating their vernacular names (common) and reference citing migration, as well as endemic (Ψ) and internationally threatened species, according to CITES Appendices I, II, III (Ѧ).

Acknowledgments

This study was financed in part by the Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (FUNCAP) – Process Numbers UNI-0210-0485.01.00/23 Jober Fernando Sobczak; PS1-0186004110100/21 Jober Fernando Sobczak; 150272/2023-5 (Pós-Doutorado Júnior - (PDJ)) German Antonio Villanueva Bonilla; and by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001 Joedson Castro Pires.

Data Availability

Supporting data are available at <https://doi.org/10.48331/scielodata.5ZLMNF>.

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Edited by

  • Associate Editor
    Carlos Joly

Publication Dates

  • Publication in this collection
    10 Jan 2025
  • Date of issue
    2024

History

  • Received
    12 Apr 2024
  • Accepted
    16 Nov 2024