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Checklist of Odonata species from Serra of Itabaiana National Park, and an update and new records for the state of Sergipe, Brazil

Checklist das espécies de Odonata do Parque Nacional da Serra de Itabaiana, e uma atualização e novos registros para o estado de Sergipe, Brasil

Abstract

Understanding species diversity and distribution cannot be overstated in the development of effective management and biological conservation strategies. Our goal was to address the knowledge gap regarding dragonfly diversity in the northeastern Atlantic Forest, specifically in the Serra of Itabaiana National Park in the state of Sergipe, Brazil. During our study, we recorded 40 species and 969 Odonata individuals across six families and 25 genera. This study contributes 27 new occurrence records of Odonata species in Sergipe, Brazil, highlighting the significance of preserving and protecting the habitats of this region. Our findings provide valuable information on the distribution of dragonfly species in the state of Sergipe and the Northeast region.

Keywords
Atlantic Forest; Conservation; Dragonfly; Damselflies; Inventory

Resumo

A compreensão da diversidade e distribuição das espécies é fundamental para o desenvolvimento de estratégias efetivas de manejo e conservação biológica. Nosso objetivo foi abordar a lacuna de conhecimento sobre a diversidade de libélulas na Mata Atlântica nordestina, especificamente na Serra do Parque Nacional de Itabaiana, no estado de Sergipe, Brasil. Durante nosso estudo, registramos 40 espécies e 969 indivíduos de Odonata em seis famílias e 25 gêneros. Este estudo contribui com 27 novos registros de ocorrência de espécies de Odonata em Sergipe, Brasil, destacando a importância de preservar e proteger os habitats desta região. Nossos resultados fornecem informações valiosas sobre a distribuição das espécies de libélulas no estado de Sergipe e na região Nordeste.

Palavras-chave
Mata Atlântica; Conservação; Libélulas; Donzelinhas; Inventário

Introduction

Odonates are widely distributed worldwide, with Antarctica as an exception (Von Ellenrieder 2009VON ELLENRIEDER, N. 2009. Databasing dragonflies: State of knowledge in the Neotropical region. Agrion. 13(2):58–72., Rodrigues & Roque 2017RODRIGUES, M.E. & ROQUE, F.O. 2017. Checklist de odonata do estado de Mato Grosso do Sul, Brasil. Iheringia – Ser. Zool. 107:1–4.). They comprise 6,405 species (Paulson & Schorr 2024PAULSON, D., SCHORR, M., ABBOTT, J., BOTA-SIERRA, C., DELIRY, C., DIJKSTRA, K.-D. & LOZANO, F. 2024. World Odonata List. Odonata Central, University of Alabama, Tuscaloosa, Alabama. Available from: https://www.odonatacentral.org/app/#/wol/ (last access in 14/02/2024).
https://www.odonatacentral.org/app/#/wol...
), which are mainly associated with freshwater ecosystems (Kalkman et al. 2008KALKMAN, V.J., CLAUSNITZER, V., DIJKSTRA, K.D.B., ORR, A.G., PAULSON, D.R. & VAN TOL, J. 2008. Global diversity of dragonflies (Odonata) in freshwater. Hydrobiologia. 595(1):351–363.). Approximately 1,800 species are found in the Neotropical region (Von Ellenrieder 2009VON ELLENRIEDER, N. 2009. Databasing dragonflies: State of knowledge in the Neotropical region. Agrion. 13(2):58–72.), and it is estimated that over 870 Odonata species and 152 genera of dragonflies are recorded in Brazil (IUCN 2024INTERNATIONAL UNION FOR CONSERVATION OF NATURE – IUCN. 2024. The IUCN Red List of Threatened Species. Version 2024-1. https://www.iucnredlist.org. (last access in 15/02/2024).
https://www.iucnredlist.org...
), with four families of Anisoptera and 11 families of Zygoptera (Hamada et al. 2014HAMADA, N., NESSIMIAN, J.L. & QUERINO, R.B. 2014. Insetos Aquáticos na Amazônia brasileira: Taxonomia, Biologia e Ecologia. Editora INPA. 724p.). Recent years have witnessed a significant upsurge in ecological studies centered on Odonata diversity in Brazil (Miguel et al. 2017MIGUEL, T.B., CALVÃO, L.B., VITAL, M.V.C. & JUEN, L. 2017. A scientometric study of the order Odonata with special attention to Brazil. Int. J. Odonatol. 20(1):27–42., Koroiva et al. 2022KOROIVA, R., GOMES, V.G.N. & VILELA, D.S. 2022. DNA Barcoding and new records of odonates (Insecta: Odonata) from Paraíba State, Brazil. Diversity. 14(3):203.). As a result, Brazil has emerged as one of the top contributors to the global corpus of Odonata-focused publications (Oliveira-Junior et al. 2022OLIVEIRA-JUNIOR, J.M.B., ROCHA, T.S., VINAGRE, S.F., MIRANDA-FILHO, J.C., MENDOZA-PENAGOS, C.C., DIAS-SILVA, K., JUEN, L. & CALVÃO, L.B. 2022. A bibliometric analysis of the global research in odonata: trends and gaps. Diversity. 14:1074.). However, this knowledge is distributed asymmetrically among Brazilian geographic regions, with the highest concentration of studies located mainly in the Southeast, North, and Midwest regions (Miguel et al. 2017MIGUEL, T.B., CALVÃO, L.B., VITAL, M.V.C. & JUEN, L. 2017. A scientometric study of the order Odonata with special attention to Brazil. Int. J. Odonatol. 20(1):27–42., Koroiva et al. 2021KOROIVA, R., PEREIRA-COLAVITE, A., RABELO, F. & VILELA, D.S. 2021. Checklist and contribution to the knowledge of the odonatofauna of Paraíba state, Brazil. Biota Neotrop. 21(3):1–10. https://doi.org/10.1590/1676-0611-BN-2021-1196 (last access in 15/02/2024).
https://doi.org/10.1590/1676-0611-BN-202...
). Knowledge in the Northeast region presented sporadic collections (De Marco-Júnior & Vianna 2005DE MARCO-JÚNIOR, P. & VIANNA, D.M. 2005. Distribuição do esforço de coleta de Odonata no Brasil–subsídios para escolha de áreas prioritárias para levantamentos faunísticos. Lundiana: International Journal of Biodiversity. 6(sup.):13–26., Vianna & De Marco-Júnior 2012VIANNA, D.M. & DE MARCO-JÚNIOR, P. 2012. Higher-taxon and cross-taxon surrogates for odonate biodiversity in Brazil. Nat. Conservação. 10(1):34–39., Miguel et al. 2017MIGUEL, T.B., CALVÃO, L.B., VITAL, M.V.C. & JUEN, L. 2017. A scientometric study of the order Odonata with special attention to Brazil. Int. J. Odonatol. 20(1):27–42.). However, in the last decade, emerging research groups have been consolidating and improving regional knowledge (Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.). A brief literature review revealed that Odonata inventory studies have been published in the following states: Ceará (Takiya et al. 2016TAKIYA, D.M., SANTOS, A.P.M., PINTO, A.P., HENRIQUES-OLIVEIRA, A.L., CARVALHO, A.L., SAMPAIO, B.H.L., CLARKSON, B., MOREIRA, F.F.F., AVELINO-CAPISTRANO, F., GONÇALVES, I.C., CORDEIRO, I.R.S., CÂMARA, J.T., BARBOSA, J.F., DE SOUZA, W.R.M. & RAFAEL, J.A. 2016. Aquatic insects from the Caatinga: Checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil. Biodivers. Data J. (4):e8354.), Sergipe (Santos et al. 2020SANTOS, J.C., VILELA, D.S., ALMEIDA, W.R., SANTOS, B., SANTOS, A.E., BEZERRA, L.M.M., SANTOS, L., NETO, A.M.S., VENÂNCIO, H. & CARNEIRO, M.A.A. 2020. A rapid survey of dragonflies and damselflies (Insecta: Odonata) reveals 29 new records to Sergipe State, Brazil. Hetaerina. 2(2):29–34.), Bahia (Ribeiro et al. 2021aRIBEIRO, C., FIRME, B., ARAUJO, S.A., SÁ, A., ZANDER, F., TEIXEIRA, K., SANTOS, L.R. & RODRIGUES, M.E. 2021a. Check-list of Odonata from the state of Bahia, Brazil: Ecological information, distribution, and new state records. Odonatologica. 50(3–4):161–186.), Paraíba (Koroiva et al. 2021KOROIVA, R., PEREIRA-COLAVITE, A., RABELO, F. & VILELA, D.S. 2021. Checklist and contribution to the knowledge of the odonatofauna of Paraíba state, Brazil. Biota Neotrop. 21(3):1–10. https://doi.org/10.1590/1676-0611-BN-2021-1196 (last access in 15/02/2024).
https://doi.org/10.1590/1676-0611-BN-202...
), and Alagoas (Godé & Ferreira-Peruquetti 2015GODÉ, L. & FERREIRA-PERUQUETTI, P.S. 2015. Libélulas (ODONATA) da Reserva Biológica de Pedra Talhada. In Biodiversidade da Reserva Biológica de Pedra Talhada (Alagoas, Pernambuco – Brasil) (STUDER, A., L. NUSBAUMER & R. SPICHIGER, eds) Boissiera. (68):199–203., Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.). In addition, there are studies on occurrence records of species in other northeastern states (Mesquita & Matteo 1991MESQUITA, H.G. & MATTEO, B.C. 1991. Contribuição ao Conhecimento dos Odonata da Ilha de Fernando de Noronha, Pernambuco, Brasil. Iheringia – Ser. Zool. 71:157–160., De Marco-Júnior 2008DE MARCO-JÚNIOR, P. 2008. Libellulidae (Insecta: Odonata) from Itapiracó Reserve, Maranhão, Brazil: new records and species distribution information. Acta Amaz. 38(4):819–822., Carvalho & Bravo 2014, Irusta & Lencioni 2015IRUSTA, J.B. & LENCIONI, F.A.A. 2015. First record of Pseudostigmatidae (Insecta: Odonata) in the northeast region of Brazil. Check List. 11(2):10–12., Nobre 2016NOBRE, C.E.B. 2016. Erythrodiplax leticia: Description of the female and updated geographic distribution (Odonata: Libellulidae). Zootaxa. 4067(4):469–472., Bastos et al. 2019BASTOS, R.C., BRASIL, L.S., CARVALHO, F.G., CALVÃO, L.B., SILVA, J.O.A. & JUEN, L. 2019. Odonata of the state of Maranhão, Brazil: Wallacean shortfall and priority areas for faunistic inventories. Biota Neotrop. 19(4):e20190734. https://doi.org/10.1590/1676-0611-BN-2019-0734 (last access in 15/02/2024).
https://doi.org/10.1590/1676-0611-BN-201...
, Lacerda & Machado 2019LACERDA, D.S.S. & MACHADO, A.B.M. 2019. The damselfly genus Mecistogaster (Odonata: Pseudostigmatidae) from the Brazilian Atlantic Forest with a description of three new species and a neotype designation for M. amalia (Burmeister, 1839). Zootaxa. 4668(2):207–228., Ribeiro et al. 2021bRIBEIRO, C., JUEN, L. & RODRIGUES, M.E. 2021b. The Zygoptera/Anisoptera ratio as a tool to assess anthropogenic changes in Atlantic Forest streams. Biodivers. Conserv. 30(5):1315–1329., Garcia-Junior et al. 2022GARCIA-JUNIOR, M.D.N., DAMASCENO, M.T.S., VILELA, D.S. & SOUTO, R.N.P. 2022. The Brazilian Legal amazon odonatofauna: A perspective of diversity and knowledge gaps. EntomoBrasilis 15(e977):1–18., Koroiva et al. 2022KOROIVA, R., GOMES, V.G.N. & VILELA, D.S. 2022. DNA Barcoding and new records of odonates (Insecta: Odonata) from Paraíba State, Brazil. Diversity. 14(3):203.).

Until a few years ago, Sergipe was a state that was largely unknown regarding its odonate fauna. Currently, Sergipe has 37 known dragonfly species, which is the result of rapid inventory and recent collection efforts (Machado 2015MACHADO, A.B.M. 2015. Perilestes eustaquioi sp. nov. and new distributional records of Perilestidae (Odonata) in Brazil. Zoologia. 32(5):428–430., Santos et al. 2020SANTOS, J.C., VILELA, D.S., ALMEIDA, W.R., SANTOS, B., SANTOS, A.E., BEZERRA, L.M.M., SANTOS, L., NETO, A.M.S., VENÂNCIO, H. & CARNEIRO, M.A.A. 2020. A rapid survey of dragonflies and damselflies (Insecta: Odonata) reveals 29 new records to Sergipe State, Brazil. Hetaerina. 2(2):29–34., Vilela et al. 2021aVICENTE, A., RIBEIRO, A.S., SANTOS, E.A. & FRANCO, C.R.P. 2005. Levantamento Botânico. In Parque Nacional Serra de Itabaiana – Levantamento da Biota (C.M. CARVALHO & J.C. VILAR, eds) Universidade Federal de Sergipe, São Cristóvão, p.131., bVILELA, D.S., LENCIONI, F.A.A. & SANTOS, J.C. 2021b. Leptagrion itabaiana sp. nov. (Odonata: Coenagrionidae) from Serra de Itabaiana National Park, Sergipe state, Northeastern Brazil. Zootaxa. 4980(3):558–564., 2022VILELA, D.S., LENCIONI, F.A.A., FURIERI, K.S. & SANTOS, J.C. 2022. The rediscovery of Machadagrion garbei (Santos, 1961) (Odonata: Coenagrionidae) with notes on the hitherto unknown female. Zootaxa. 5124(3):391–396.). Given this context, to minimize the asymmetry of knowledge regarding Odonata in Brazil and the Atlantic Forest, the objective of this study was to inventory dragonfly species in the Serra of Itabaiana National Park, addressing richness, abundance, diversity, and new records for the state of Sergipe. To our knowledge, there are few Odonata species inventory studies for federal conservation units in Brazil, such as the Biological Reserve of Pedra Talhada (Godé & Ferreira-Peruquetti 2015GODÉ, L. & FERREIRA-PERUQUETTI, P.S. 2015. Libélulas (ODONATA) da Reserva Biológica de Pedra Talhada. In Biodiversidade da Reserva Biológica de Pedra Talhada (Alagoas, Pernambuco – Brasil) (STUDER, A., L. NUSBAUMER & R. SPICHIGER, eds) Boissiera. (68):199–203.), Ubajara National Park, and Sete Cidades National Park (Takiya et al. 2016TAKIYA, D.M., SANTOS, A.P.M., PINTO, A.P., HENRIQUES-OLIVEIRA, A.L., CARVALHO, A.L., SAMPAIO, B.H.L., CLARKSON, B., MOREIRA, F.F.F., AVELINO-CAPISTRANO, F., GONÇALVES, I.C., CORDEIRO, I.R.S., CÂMARA, J.T., BARBOSA, J.F., DE SOUZA, W.R.M. & RAFAEL, J.A. 2016. Aquatic insects from the Caatinga: Checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil. Biodivers. Data J. (4):e8354.), Chico Mendes Extractive Reserve, and Cazumbá–Iracema Extractive Reserve (Filho et al. 2022FILHO, J.C.M., PENAGOS, C.C.M., CALVÃO, L.B., MIGUEL, T.B., BASTOS, R.C., FERREIRA, V.R.S., LIMA, D.V.M., VIEIRA, L.J.S., BRASIL, L.S. & JUEN, L. 2022. Checklist of Damselflies and Dragonflies (Odonata) from Acre state, and the first record of Drepanoneura loutoni von Ellenrieder & Garrison, 2008 for Brazil. Biota Neotrop. 22:e20211320. https://doi.org/10.1590/1676-0611-BN-2021-1320 (last access in 15/02/2024).
https://doi.org/10.1590/1676-0611-BN-202...
). The Red List of Threatened Species in Brazil, which is maintained by Instituto Chico Mendes de Biodiversidade – ICMBio, was utilized to designate the conservation status of the species. Thus, our study is significant because it can contribute to the evaluation of the conservation status and distribution of Brazilian odonates.

Material and Methods

1. Study area

The Serra of Itabaiana National Park (SINP) is composed of three mountain ranges (Serra of Itabaiana, Serra Comprida, and Serra of Cajueiro), covering an area of approximately 7,966 ha, distributed among the municipalities of Areia Branca, Itabaiana, Laranjeiras, Itaporanga D’ ajuda, and Campo do Brito in the state of Sergipe, Brazil (Vicente et al. 2005VICENTE, A., RIBEIRO, A.S., SANTOS, E.A. & FRANCO, C.R.P. 2005. Levantamento Botânico. In Parque Nacional Serra de Itabaiana – Levantamento da Biota (C.M. CARVALHO & J.C. VILAR, eds) Universidade Federal de Sergipe, São Cristóvão, p.131., Silva et al. 2019SILVA, A.C.C., OLIVEIRA, E.V.S., ALVES, M., FARIAS, M.C.V., MOTA, A.C., SOUZA, C.A.S. & PRATA, A.P.D.N. 2019. Lista atualizada da flora vascular do Parque Nacional (PARNA) Serra de Itabaiana, Sergipe, Brasil. Pesqui. Ensino Ciênc. Exatas Nat. 3(1):40.) (Figure 1). SINP is a conservation unit with the characteristic biomes of the Atlantic Forest and Caatinga (Vicente et al. 2005VICENTE, A., RIBEIRO, A.S., SANTOS, E.A. & FRANCO, C.R.P. 2005. Levantamento Botânico. In Parque Nacional Serra de Itabaiana – Levantamento da Biota (C.M. CARVALHO & J.C. VILAR, eds) Universidade Federal de Sergipe, São Cristóvão, p.131., Silva et al. 2019SILVA, A.C.C., OLIVEIRA, E.V.S., ALVES, M., FARIAS, M.C.V., MOTA, A.C., SOUZA, C.A.S. & PRATA, A.P.D.N. 2019. Lista atualizada da flora vascular do Parque Nacional (PARNA) Serra de Itabaiana, Sergipe, Brasil. Pesqui. Ensino Ciênc. Exatas Nat. 3(1):40.). Additionally, the SINP is an important component of the hydrographic basin of the state of Sergipe (ICMBio 2016INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE – ICMBIO. 2016. Plano de Manejo Parque Nacional Serra de Itabaiana. p.1–178.), represented by water bodies such as the Coqueiro, dos Negros, and Água Fria streams, all of which are associated with the remaining Atlantic Forest.

Figure 1
Sampling points for Odonata species in Serra of Itabaiana National Park, Sergipe, Brazil.

2. Sampling

Odonates were sampled between December 2020 and February 2021 on sunny days between 7:00 am and 4:00 pm. Only adult individuals were sampled using entomological nets by two collectors for 1 h at each sampling point along a 100 m transect. The sampling points were distributed in streams, waterfalls, pools, bromeliads phytotelmata, and around the ICMBio headquarters (Figure 2, Table 1). A total of 24 locations were systematically sampled, totaling a sampling effort of 48 h. Specimens collected during 14 sporadic events were also considered, as they added new records to the SINP. In these events, individuals were captured using an entomological net by only one collector for approximately 1 h, without walking a predetermined distance. Of the 14 sporadic events, only two occurred recently (September 23 and 25, 2022), while all others were from the same period as the standardized collections. The specimens were prepared in P.A. acetone, based on the methodology proposed by Lencioni (2005LENCIONI, F.A.A. 2005. Damselflies of Brazil, an illustrated identification guide: I—the non-Coenagrionidae families. All Print Editora, São Paulo., 2017LENCIONI, F.A.A. 2017. Damselflies of Brazil: an illustrated identification guide Southeast Region. 1 ed. Jacareí, São Paulo.), placed in silk envelopes, and subsequently identified at the species level by Dr. Diogo Silva Vilela. All specimens were deposited in the Odonate Collection of the Ecology and Biodiversity Laboratory (LEBIO) of the Ecology Department at the Federal University of Sergipe (UFS), in São Cristóvão, Sergipe. Two specimens each of Heteragrion lencionii Vilela, Farias & Santos, 2021 and Leptagrion itabaiana Vilela, Lencioni & Santos, 2021 were deposited in the Frederico A. A. Lencioni Collection, Jacareí, São Paulo, Brazil (FAAL). The specimens were collected with the approval of Instituto Chico Mendes de Conservação da Biodiversidade – ICMBio (SISBIO #83369/1).

Figure 2
Sampling points for Odonata in Serra of Itabaiana National Park, Sergipe, Brazil: (A–D) streams in forests; (E-F) streams in open areas with small waterfalls; and (G-H) streams and pools in open areas. Photos: (A–H) J.C.S 2021.
Table 1
Sampling points and their respective environmental information, dates, and geographic coordinates in the Serra of Itabaiana National Park, Sergipe, Brazil. Legend: A – Open area; B – Closed area with canopy; C – Waterfall; D – Stream; E – Pool; F – Lentic; G – Lotic; H – Semilotic; I – Shaded environment; J – Environment with high solar incidence; K – Small open areas with low solar incidence; L – Mixed environment with partially shaded open and closed areas; M – Anthropized environment; N – Artesian well; O – Bromeliaceae phytotelmata. Between P1 and P24, collections were standardized, and between P25 and P38, collections were sporadic. See Figure 1 for a clearer visual representation of the spatial arrangement of the sampling points.

3. Species distribution, conservation status and data analysis

To gather information on the distribution of Odonata species in the state of Sergipe, we conducted a comprehensive search of online academic databases, including the ISI Web of Knowledge, Google Scholar, Scielo, Scopus, and JStor. To optimize our search results, we employed a variety of keywords, such as “dragonflies”, “odonates”, “odonata”, and “Sergipe”, which were combined in various ways. As we were unable to identify any relevant publications in languages other than English and Portuguese, we conducted searches in both languages. We then selected all available publications, excluding unpublished studies, such as theses and dissertations. Thus, we compiled species distributions from the following literature: Calvert (1909)CALVERT, P.P. 1909. Contributions to a knowledge of the Odonata of the Neotropical region, exclusive of Mexico and Central America. Ann. Carnegie Mus. 6(1):73–280., Belle (1988BELLE, J. 1988. A synopsis of the species of Phyllocycla Calvert, with descriptions of four new taxa and a key to the genera of Neotropical Gomphidae (Odonata, Gomphidae). Tijdschr. Entomol. (131):73–102., 1992BELLE, J. 1992. A revision of the South American species of Aphylla Selys, 1854 (Odonata: Gomphidae). Zool. Meded. 66(12):239–264.), Machado (2015)MACHADO, A.B.M. 2015. Perilestes eustaquioi sp. nov. and new distributional records of Perilestidae (Odonata) in Brazil. Zoologia. 32(5):428–430., Santos et al. (2020)SANTOS, J.C., VILELA, D.S., ALMEIDA, W.R., SANTOS, B., SANTOS, A.E., BEZERRA, L.M.M., SANTOS, L., NETO, A.M.S., VENÂNCIO, H. & CARNEIRO, M.A.A. 2020. A rapid survey of dragonflies and damselflies (Insecta: Odonata) reveals 29 new records to Sergipe State, Brazil. Hetaerina. 2(2):29–34.; Vilela et al. (2021aVICENTE, A., RIBEIRO, A.S., SANTOS, E.A. & FRANCO, C.R.P. 2005. Levantamento Botânico. In Parque Nacional Serra de Itabaiana – Levantamento da Biota (C.M. CARVALHO & J.C. VILAR, eds) Universidade Federal de Sergipe, São Cristóvão, p.131., bVILELA, D.S., LENCIONI, F.A.A. & SANTOS, J.C. 2021b. Leptagrion itabaiana sp. nov. (Odonata: Coenagrionidae) from Serra de Itabaiana National Park, Sergipe state, Northeastern Brazil. Zootaxa. 4980(3):558–564.), Vilela et al. (2022)VILELA, D.S., LENCIONI, F.A.A., FURIERI, K.S. & SANTOS, J.C. 2022. The rediscovery of Machadagrion garbei (Santos, 1961) (Odonata: Coenagrionidae) with notes on the hitherto unknown female. Zootaxa. 5124(3):391–396.. A comprehensive list of all Odonata species occurring in Sergipe is presented in the results. Finally, to assess the conservation status of each species, we consulted the Red List of Threatened Species databases of ICMBio (ICMBio 2024INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE – ICMBio. 2024. Sistema de Avaliação do Risco de Extinção da Biodiversidade – SALVE. https://salve.icmbio.gov.br/. (last access in 15/02/2024).
https://salve.icmbio.gov.br/...
) and the International Union for Conservation of Nature (IUCN 2024INTERNATIONAL UNION FOR CONSERVATION OF NATURE – IUCN. 2024. The IUCN Red List of Threatened Species. Version 2024-1. https://www.iucnredlist.org. (last access in 15/02/2024).
https://www.iucnredlist.org...
).

For this study, each sampling point was considered a sampling unit. To estimate species richness and measure the efficiency of the sampling effort, interpolation and extrapolation curves were constructed for the total number of sampled points and suborders (Anisoptera and Zygoptera). The curves (Hill number q – 0) were based on specimen abundance and confidence intervals (95%) were determined from 1,000 bootstraps (Chao et al. 2014CHAO, A., GOTELLI, N.J., HSIEH, T.C., SANDER, E.L., MA, K.H., COLWELL, R.K. & ELLISON, A.M. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84(1):45–67., Hsieh et al. 2016HSIEH, T.C., MA, K. & CHAO, A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7(12):1451–1456.), with extrapolation estimated to be three times the number of specimens sampled (Chao et al. 2014CHAO, A., GOTELLI, N.J., HSIEH, T.C., SANDER, E.L., MA, K.H., COLWELL, R.K. & ELLISON, A.M. 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84(1):45–67.). In addition, the distribution of species abundance was plotted to visually compare the total species dominance patterns. Interpolation and extrapolation curves were generated using the “iNEXT” package (Hsieh et al. 2020HSIEH, T.C., MA, K. & CHAO, A. 2020. iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.20. http://chao.stat.nthu.edu.tw/wordpress/software-download/.
http://chao.stat.nthu.edu.tw/wordpress/s...
) and all analyses were performed using the “R” software version 4.2.2 (R Core Team 2022R CORE TEAM. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
https://www.R-project.org/...
).

Results

This study recorded a total of 40 species and 969 individuals of Odonata in the SINP, distributed among the suborders Anisoptera and Zygoptera, six families, and 25 genera. Of these, 109 were from Anisoptera, and 860 were from Zygoptera. Libellulidae was the most diverse family, with 19 species, followed by Coenagrionidae with 12 species. The suborder Zygoptera had the highest abundance, with 89% of the collected individuals, with Coenagrionidae as the most representative family. The most abundant species were Heteragrion aurantiacum Selys, 1862, Argia reclusa Selys, 1865, and A. smithianaCalvert, 1909CALVERT, P.P. 1909. Contributions to a knowledge of the Odonata of the Neotropical region, exclusive of Mexico and Central America. Ann. Carnegie Mus. 6(1):73–280. (Figures 3 and 4). The suborder Anisoptera comprised 11% of the collected individuals, with Libellulidae being the most abundant family.

Figure 3
Distribution of the abundance of Odonata species in the Serra of Itabaiana National Park, Sergipe, Brazil.
Figure 4
Odonates from Serra of Itabaiana National Park: A) Hetaerina longipes Hagen, 1853; B) Heteragrion aurantiacum Selys, 1862 (male); C) Heteragrion aurantiacum Selys, 1862 (female); D) Perilestes fragilis (Hagen, 1862); E) Argia reclusa Selys, 1865 (male); F) Argia reclusa Selys, 1865 (female); G) Erythrodiplax fusca (Rambur, 1842); H) Castoraeschna cf. longfieldae (Kimmins, 1929); I) Perithemis lais (Perty, 1834); and J) Dythemis nigra (Martin, 1897). Photos (B; D; E) A.B.S.F. 2021, (A; C; F-J) J.C.S. 2021.

Our study revealed 27 recent sightings of the Odonata species in the state of Sergipe (Table 2). Consequently, Sergipe has documented 64 species, 35 genera, and nine families (Table 3). Most of the species collected in this study were classified by the Chico Mendes Institute for Biodiversity Conservation (ICMBio, 2024INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE – ICMBio. 2024. Sistema de Avaliação do Risco de Extinção da Biodiversidade – SALVE. https://salve.icmbio.gov.br/. (last access in 15/02/2024).
https://salve.icmbio.gov.br/...
) as least concern (LC). The exceptions are Leptagrion itabaiana and Heteragrion lencionii, which still do not have information about their respective conservation statuses, and Leptagrion garbei Santos, 1961, which is classified as having insufficient data (Table 3).

Table 2
List of species, abundance (number of individuals), and new records (*) of dragonflies and damselflies (Insecta: Odonata) in the state of Sergipe. Between P1 and P24, collections were standardized, and between P25 and P38, collections were sporadic. (See Table 1). See Figure 1 for a clearer visual representation of the spatial arrangement of the sampling points.
Table 3
List of Odonata species recorded in the state of Sergipe, Brazil. Legends: Least Concern (LC); Data Deficient (DD); Not evaluated (N/A) (IUCN 2024INTERNATIONAL UNION FOR CONSERVATION OF NATURE – IUCN. 2024. The IUCN Red List of Threatened Species. Version 2024-1. https://www.iucnredlist.org. (last access in 15/02/2024).
https://www.iucnredlist.org...
. ICMBio 2024INSTITUTO CHICO MENDES DE CONSERVAÇÃO DA BIODIVERSIDADE – ICMBio. 2024. Sistema de Avaliação do Risco de Extinção da Biodiversidade – SALVE. https://salve.icmbio.gov.br/. (last access in 15/02/2024).
https://salve.icmbio.gov.br/...
).

The extrapolation curve for the total number of Odonata collected in the SINP did not show a stabilizing trend, indicating that additional sampling efforts may have resulted in the discovery of more species (Figure 5). When analyzed independently, the curve for Anisoptera did not approach stabilization, indicating that more sampling effort is needed to record a higher number of species (Figure 5). However, the curve for Zygoptera was close to the asymptote for the 18 sampled species and was extrapolated for 20 species (Figure 5).

Figure 5
Rarefaction curve with 95% confidence interval for the Odonata species sampled in Serra of Itabaiana National Park, Sergipe, Brazil. The solid line represents the interpolation of the observed number of species, and the dashed line shows the extrapolation of what is expected with a greater sampling effort.

Among the most frequent species, Argia reclusa, Heteragrion aurantiacum, and Hetaerina longipes Hagen in Selys, 1853 were found at 65%, 64%, and 55% of the sampling points, respectively (Table 2; Figure 3). Several species, including Acanthagrion longispinosum Leonard, 1977, Castoraeschna colorata (Martin, 1908), Elasmothemis cannacrioides (Calvert, 1906), Erythrodiplax castanea (Burmeister, 1839), Erythrodiplax latimaculata Ris, 1911, Macrothemis rupicola Rácenis, 1957, Micrathyria ocellata Martin, 1897, Orthemis discolor (Burmeister, 1839), O. flavopicta Kirby, 1889, Oxyagrion impunctatumCalvert, 1909CALVERT, P.P. 1909. Contributions to a knowledge of the Odonata of the Neotropical region, exclusive of Mexico and Central America. Ann. Carnegie Mus. 6(1):73–280., and Tauriphila australis (Hagen, 1867), were considered singletons; and Brachymesia herbida (Gundlach, 1889), Erythemis mithroides (Brauer, 1900), Heteragrion lencionii, and Miathyria marcella (Selys in Sagra, 1857) were considered doubletons (Figure 3).

Discussion

This is the first inventory study of Odonata species in a conservation unit in the state of Sergipe. A total of 40 Odonata species were sampled, with particular emphasis on Heteragrion lencionii and Leptagrion itabaiana, which were recently described (Vilela et al. 2021aVILELA, D.S., FARIAS, A.B.S. & SANTOS, J.C. 2021a. Heteragrion lencionii (Odonata: Heteragrionidae) sp. nov. from Serra de Itabaiana National Park, Northeastern Brazil. Zootaxa. 4966(4):476–482., bVILELA, D.S., LENCIONI, F.A.A. & SANTOS, J.C. 2021b. Leptagrion itabaiana sp. nov. (Odonata: Coenagrionidae) from Serra de Itabaiana National Park, Sergipe state, Northeastern Brazil. Zootaxa. 4980(3):558–564.), and Leptagrion garbei, a recently rediscovered species (Vilela et al. 2022VILELA, D.S., LENCIONI, F.A.A., FURIERI, K.S. & SANTOS, J.C. 2022. The rediscovery of Machadagrion garbei (Santos, 1961) (Odonata: Coenagrionidae) with notes on the hitherto unknown female. Zootaxa. 5124(3):391–396.) from data obtained in this study. Additionally, 27 new records of Odonata species have been added for the state of Sergipe. This brings the total number of registered Odonata species for Sergipe to 37 for 64 species (Santos et al. 2020SANTOS, J.C., VILELA, D.S., ALMEIDA, W.R., SANTOS, B., SANTOS, A.E., BEZERRA, L.M.M., SANTOS, L., NETO, A.M.S., VENÂNCIO, H. & CARNEIRO, M.A.A. 2020. A rapid survey of dragonflies and damselflies (Insecta: Odonata) reveals 29 new records to Sergipe State, Brazil. Hetaerina. 2(2):29–34., Vilela et al. 2021aVILELA, D.S., FARIAS, A.B.S. & SANTOS, J.C. 2021a. Heteragrion lencionii (Odonata: Heteragrionidae) sp. nov. from Serra de Itabaiana National Park, Northeastern Brazil. Zootaxa. 4966(4):476–482., bVILELA, D.S., LENCIONI, F.A.A. & SANTOS, J.C. 2021b. Leptagrion itabaiana sp. nov. (Odonata: Coenagrionidae) from Serra de Itabaiana National Park, Sergipe state, Northeastern Brazil. Zootaxa. 4980(3):558–564., Vilela et al. 2022VILELA, D.S., LENCIONI, F.A.A., FURIERI, K.S. & SANTOS, J.C. 2022. The rediscovery of Machadagrion garbei (Santos, 1961) (Odonata: Coenagrionidae) with notes on the hitherto unknown female. Zootaxa. 5124(3):391–396.), an increase of 73% in the knowledge of Odonata in the state. Currently, the richness of Odonata in Sergipe represents approximately 7.5% of the 870 species known to occur in Brazil (IUCN 2024).

The Odonatofauna of Sergipe is comparable to the lists of known Odonata species in other states in the northeast region (sensu based on the literature consulted and considering only species with a specific epithet). Bahia had the highest number of occurrence records, with 178 species (Lacerda & Machado 2019LACERDA, D.S.S. & MACHADO, A.B.M. 2019. The damselfly genus Mecistogaster (Odonata: Pseudostigmatidae) from the Brazilian Atlantic Forest with a description of three new species and a neotype designation for M. amalia (Burmeister, 1839). Zootaxa. 4668(2):207–228., Ribeiro et al. 2021aRIBEIRO, C., FIRME, B., ARAUJO, S.A., SÁ, A., ZANDER, F., TEIXEIRA, K., SANTOS, L.R. & RODRIGUES, M.E. 2021a. Check-list of Odonata from the state of Bahia, Brazil: Ecological information, distribution, and new state records. Odonatologica. 50(3–4):161–186., bRIBEIRO, C., FIRME, B., ARAUJO, S.A., SÁ, A., ZANDER, F., TEIXEIRA, K., SANTOS, L.R. & RODRIGUES, M.E. 2021a. Check-list of Odonata from the state of Bahia, Brazil: Ecological information, distribution, and new state records. Odonatologica. 50(3–4):161–186., Vilela et al. 2022VILELA, D.S., LENCIONI, F.A.A., FURIERI, K.S. & SANTOS, J.C. 2022. The rediscovery of Machadagrion garbei (Santos, 1961) (Odonata: Coenagrionidae) with notes on the hitherto unknown female. Zootaxa. 5124(3):391–396.), followed by Maranhão (90 spp.; De Marco-Júnior 2008DE MARCO-JÚNIOR, P. 2008. Libellulidae (Insecta: Odonata) from Itapiracó Reserve, Maranhão, Brazil: new records and species distribution information. Acta Amaz. 38(4):819–822., Bastos et al. 2019BASTOS, R.C., BRASIL, L.S., CARVALHO, F.G., CALVÃO, L.B., SILVA, J.O.A. & JUEN, L. 2019. Odonata of the state of Maranhão, Brazil: Wallacean shortfall and priority areas for faunistic inventories. Biota Neotrop. 19(4):e20190734. https://doi.org/10.1590/1676-0611-BN-2019-0734 (last access in 15/02/2024).
https://doi.org/10.1590/1676-0611-BN-201...
, Garcia-Junior et al. 2022GARCIA-JUNIOR, M.D.N., DAMASCENO, M.T.S., VILELA, D.S. & SOUTO, R.N.P. 2022. The Brazilian Legal amazon odonatofauna: A perspective of diversity and knowledge gaps. EntomoBrasilis 15(e977):1–18., Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.), Ceará (74 spp.; Carvalho & Bravo 2014CARVALHO, J. & BRAVO, F. 2014. Odonata do semiárido. In Artrópode do Semiárido: Biodiversidade e Conservação (F. Bravo & A. Calor, eds) Printmídia, Feira de Santana, p.298., Takiya et al. 2016TAKIYA, D.M., SANTOS, A.P.M., PINTO, A.P., HENRIQUES-OLIVEIRA, A.L., CARVALHO, A.L., SAMPAIO, B.H.L., CLARKSON, B., MOREIRA, F.F.F., AVELINO-CAPISTRANO, F., GONÇALVES, I.C., CORDEIRO, I.R.S., CÂMARA, J.T., BARBOSA, J.F., DE SOUZA, W.R.M. & RAFAEL, J.A. 2016. Aquatic insects from the Caatinga: Checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil. Biodivers. Data J. (4):e8354.), Paraíba (63 spp.; Koroiva et al. 2021KOROIVA, R., PEREIRA-COLAVITE, A., RABELO, F. & VILELA, D.S. 2021. Checklist and contribution to the knowledge of the odonatofauna of Paraíba state, Brazil. Biota Neotrop. 21(3):1–10. https://doi.org/10.1590/1676-0611-BN-2021-1196 (last access in 15/02/2024).
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, 2022KOROIVA, R., GOMES, V.G.N. & VILELA, D.S. 2022. DNA Barcoding and new records of odonates (Insecta: Odonata) from Paraíba State, Brazil. Diversity. 14(3):203.), Sergipe (62 spp.; this study), Alagoas (46 spp.; Godé & Ferreira-Peruquetti 2015GODÉ, L. & FERREIRA-PERUQUETTI, P.S. 2015. Libélulas (ODONATA) da Reserva Biológica de Pedra Talhada. In Biodiversidade da Reserva Biológica de Pedra Talhada (Alagoas, Pernambuco – Brasil) (STUDER, A., L. NUSBAUMER & R. SPICHIGER, eds) Boissiera. (68):199–203., Lacerda & Machado 2019LACERDA, D.S.S. & MACHADO, A.B.M. 2019. The damselfly genus Mecistogaster (Odonata: Pseudostigmatidae) from the Brazilian Atlantic Forest with a description of three new species and a neotype designation for M. amalia (Burmeister, 1839). Zootaxa. 4668(2):207–228., Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.), Pernambuco (23 spp.; Mesquita & Matteo 1991MESQUITA, H.G. & MATTEO, B.C. 1991. Contribuição ao Conhecimento dos Odonata da Ilha de Fernando de Noronha, Pernambuco, Brasil. Iheringia – Ser. Zool. 71:157–160., Carvalho & Bravo 2014CARVALHO, J. & BRAVO, F. 2014. Odonata do semiárido. In Artrópode do Semiárido: Biodiversidade e Conservação (F. Bravo & A. Calor, eds) Printmídia, Feira de Santana, p.298., Nobre 2016NOBRE, C.E.B. 2016. Erythrodiplax leticia: Description of the female and updated geographic distribution (Odonata: Libellulidae). Zootaxa. 4067(4):469–472., Takiya et al. 2016TAKIYA, D.M., SANTOS, A.P.M., PINTO, A.P., HENRIQUES-OLIVEIRA, A.L., CARVALHO, A.L., SAMPAIO, B.H.L., CLARKSON, B., MOREIRA, F.F.F., AVELINO-CAPISTRANO, F., GONÇALVES, I.C., CORDEIRO, I.R.S., CÂMARA, J.T., BARBOSA, J.F., DE SOUZA, W.R.M. & RAFAEL, J.A. 2016. Aquatic insects from the Caatinga: Checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil. Biodivers. Data J. (4):e8354., Bastos et al. 2019BASTOS, R.C., BRASIL, L.S., CARVALHO, F.G., CALVÃO, L.B., SILVA, J.O.A. & JUEN, L. 2019. Odonata of the state of Maranhão, Brazil: Wallacean shortfall and priority areas for faunistic inventories. Biota Neotrop. 19(4):e20190734. https://doi.org/10.1590/1676-0611-BN-2019-0734 (last access in 15/02/2024).
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, Lacerda & Machado 2019LACERDA, D.S.S. & MACHADO, A.B.M. 2019. The damselfly genus Mecistogaster (Odonata: Pseudostigmatidae) from the Brazilian Atlantic Forest with a description of three new species and a neotype designation for M. amalia (Burmeister, 1839). Zootaxa. 4668(2):207–228., Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.), Piauí (6 spp.; Takiya et al. 2016TAKIYA, D.M., SANTOS, A.P.M., PINTO, A.P., HENRIQUES-OLIVEIRA, A.L., CARVALHO, A.L., SAMPAIO, B.H.L., CLARKSON, B., MOREIRA, F.F.F., AVELINO-CAPISTRANO, F., GONÇALVES, I.C., CORDEIRO, I.R.S., CÂMARA, J.T., BARBOSA, J.F., DE SOUZA, W.R.M. & RAFAEL, J.A. 2016. Aquatic insects from the Caatinga: Checklists and diversity assessments of Ubajara (Ceará State) and Sete Cidades (Piauí State) National Parks, Northeastern Brazil. Biodivers. Data J. (4):e8354.), and Rio Grande do Norte (4 spp.; Carvalho & Bravo 2014CARVALHO, J. & BRAVO, F. 2014. Odonata do semiárido. In Artrópode do Semiárido: Biodiversidade e Conservação (F. Bravo & A. Calor, eds) Printmídia, Feira de Santana, p.298., Irusta & Lencioni 2015IRUSTA, J.B. & LENCIONI, F.A.A. 2015. First record of Pseudostigmatidae (Insecta: Odonata) in the northeast region of Brazil. Check List. 11(2):10–12., Nobre 2016NOBRE, C.E.B. 2016. Erythrodiplax leticia: Description of the female and updated geographic distribution (Odonata: Libellulidae). Zootaxa. 4067(4):469–472., Farias et al. 2023FARIAS, A.B.S., VENTURA, I.M.C., BARÃO, K.R., VILELA, D.S. & SANTOS, J.C. 2023. Lista preliminar e novos registros de libélulas e donzelinhas (Insecta: Odonata) para o Sul do estado de Alagoas, Brasil. Hetaerina. 5(1):17–28.).

The Odonata sampling method applied in this study is the most effective compared to other methods (Cezário et al. 2021CEZÁRIO, R.R., PENA FIRME, P., PESTANA, G.C., VILELA, D.S., JUEN, L., CORDERO-RIVERA, A. & GUILLERMO, R. 2021. Sampling methods for dragonflies and damselflies. In Measuring arthropod biodiversity: A handbook of sampling methods (J.C. SANTOS & G.W. FERNANDES, eds), Springer, Cham, p.223–240.). However, the use of other sampling methodologies such as malaise and light traps can increase the sample size and enable the capture of other species, including families that were not represented in this study, rare species (Almeida et al. 2013ALMEIDA, M.V.O., PINTO, Â.P., CARVALHO, A.L. & TAKIYA, D.M. 2013. When rare is just a matter of sampling: Unexpected dominance of clubtail dragonflies (Odonata, Gomphidae) through different collecting methods at Parque Nacional da Serra do Cipó, Minas Gerais State, Brazil. Rev. Bras. Entomol. 57(4):417–423.), species that reach great heights, and species with crepuscular habits (Bedê et al. 2000BEDÊ, L.C., PIPER, W., PETTERS, G. & MACHADO, A.B.M. 2000. Phenology and oviposition behaviour of Gynacantha bifida Rambur in Brazil (Anisoptera: Aeshnidae). Odonatologica 29(4):317–324.). Therefore, the use of these methodologies could complement species sampling, especially Anisoptera, since the extrapolation for this suborder is far from reaching an asymptote. However, sporadic collections have made it possible to collect several species that are usually not sampled using the standardized method. For example, individuals collected at sporadic collection points (P26, P27, P28, P29, P37, and P38) showed curious aggregation behavior, where numerous dragonfly individuals grouped and flew regularly in the same spot. At most collection points, individuals of the species Miathyria simplex (Rambur, 1842) were collected. In some collection events, 11 individuals (two males and one female, P38; five males and three females, P37) of the species Gynacantha bifida Rambur 1842 were also captured, which showed the same aggregation behavior. This species has crepuscular habits, and the individuals were captured between 5:00 pm and 5:45 pm in an open area close to vegetation cover, flying at high speed and at a considerably high altitude (between 2 and 4 m), as described in the literature (Bedê et al. 2000BEDÊ, L.C., PIPER, W., PETTERS, G. & MACHADO, A.B.M. 2000. Phenology and oviposition behaviour of Gynacantha bifida Rambur in Brazil (Anisoptera: Aeshnidae). Odonatologica 29(4):317–324.).

Conclusion

This study on the odonatofauna of SINP significantly contributes to the knowledge of the distribution of Odonata species in the state of Sergipe and the Northeast region. Additionally, new records of Odonata species have been added to the Northeastern Atlantic Forest, highlighting the importance of maintaining and conserving the habitats of this region. In general, more species inventory studies are needed for Odonata in the state of Sergipe, especially when considering the heterogeneity of ecosystems found in the state, such as the Atlantic Forest, Restinga, and Caatinga. Finally, this study can assist SINP managers in decision-making regarding the conservation of dragonfly species and park habitats.

Acknowledgments

Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) [Bolsas CNPq 316489/2021-2 para J.C.S] and Programa de Pós-Graduação em Ecologia e Conservação (PPEC/UFS). Coordination for the Improvement of Higher Education Personnel – Brazil (CAPES) [PDPG/CAPES Bolsa de Código Financeiro 001 para A.B.S.F]. We would like to thank Anderson Eduardo Santos, Bruna dos Santos, Marina Verissimo and Matheus Dantas for their support in field collections. We would also like to thank the anonymous reviewers for their revisions that contributed to the manuscript.

Data Availability

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

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Edited by

Associate Editor
José Mermudes

Publication Dates

  • Publication in this collection
    13 May 2024
  • Date of issue
    2024

History

  • Received
    21 Dec 2023
  • Accepted
    05 Apr 2024
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