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The high biodiversity of benthic organisms in a coastal ecosystem revealed by an integrative approach

A alta biodiversidade de organismos bentônicos em um ecossistema costeiro revelada por uma abordagem integrativa

Abstract

Increasing habitat modification and species loss demand consistent efforts to describe and understand biodiversity patterns. The BIOTA/FAPESP Program was created in this context and it has been a successful initiative to promote studies on biodiversity and conservation in Brazil. The BIOTA/Araçá is an interdisciplinary project that provided a detailed evaluation of the biodiversity of Araçá Bay, a coastal seascape located on the North coast of the state of São Paulo, Southeast Brazil. The bay encompasses multiple habitats, such as beaches, mangroves, rocky shores, and a tidal flat, and provides important ecosystem services. Unfortunately, the bay is the subject of complex social-environmental conflicts that oppose economic, social, and environmental demands (i.e., the expansion of neighboring harbor activities vs. small-scale artisanal fisheries and protection of biodiversity). The present study presents a survey of the benthic species occurring in the different habitats of Araçá Bay, including data obtained during the BIOTA/Araçá project and previous assessments of the area. The benthic species play an important role in marine environments and studying the diversity of these organisms that live associated with the bottom is indispensable for comprehending the environment’s functioning. The macrofauna, meiofauna, and microorganisms associated with soft and hard bottom were listed, and additional information, such as the habitat and geographical distribution, were provided for each species. The checklist includes 826 species, almost 70% recorded during the BIOTA/Araçá project. The most speciose taxa were the annelids (225 spp.), mollusks (194 spp.), and crustaceans (177 spp.). Seven benthic species are endemic to Araçá Bay, 14 are considered threatened, and seven are economically exploited. Furthermore, the bay is the type locality of many taxa, and 11 new benthic species were described based on specimens sampled during the project. This project shows the importance of Araçá Bay as a unique biologically rich environment and highlights the need for conservation efforts in light of the current threats.

Keywords
Araçá Bay; checklist; macrofauna; meiofauna; microorganism; conservation

Resumo

O aumento da modificação dos habitats e da perda de espécies demanda esforços consistentes para descrever e compreender os padrões de biodiversidade. O programa BIOTA/FAPESP foi criado nesse contexto e é uma iniciativa de sucesso para promover estudos em biodiversidade e conservação no Brasil. O BIOTA/Araçá é um projeto interdisciplinar que promoveu uma avaliação detalhada da biodiversidade da Baía do Araçá, um ecossistema costeiro localizado ao Norte do estado de São Paulo, Sudeste do Brasil. A baía engloba múltiplos habitats, tais como praias, manguezais, costões rochosos, e uma planície de maré, e também fornece importantes serviços ecossistêmicos. Infelizmente, a baía está sujeita à conflitos sócio-ambientais complexos que contrastam demandas econômicas, sociais e ambientais (i.e. a expansão das atividades do porto vizinho vs. a pesca artesanal de pequena escala e a proteção da biodiversidade). O presente estudo apresenta um levantamento das espécies bentônicas que ocorrem nos diferentes habitats da Baía do Araçá, incluindo dados obtidos durante o projeto BIOTA/Araçá e de investigações realizadas anteriormente na área. As espécies bentônicas desempenham um papel importante no ambiente marinho, e estudar a diversidade desses organismos que vivem associados ao fundo é indispensável para compreender o funcionamento do meio ambiente. A macrofauna, meiofauna, e microorganismos associados aos fundos consolidado e inconsolidado foram listados, e informações adicionais foram fornecidas para cada espécie, tais como a distribuição geográfica e nos habitats. O checklist inclui 826 espécies, quase 70% registradas durante o projeto BIOTA/Araçá. Os taxa mais especiosos foram os anelídeos (225 spp.), moluscos (194 spp.), e crustáceos (177 spp.). Entre as espécies bentônicas listadas, sete são endêmicas da Baía do Araçá, 14 são consideradas ameaçadas de extinção, e sete são exploradas economicamente. A baía é a localidade tipo de vários taxa, e 11 novas espécies bentônicas foram descritas com base em espécimes amostrados durante o projeto. Este projeto mostra a importância da Baía do Araçá como um ambiente de riqueza biológica única e demonstra a necessidade de esforços para a sua conservação considerando as atuais ameaças.

Palavras-chave
Baía do Araçá; checklist; macrofauna; meiofauna; microorganismos; conservação

Introduction

Over the past decades, the growing human population and the effects of climate change have accelerated extinction rates and significantly changed the structure and functioning of ecosystems (IPCC 2022IPCC (2022). Climate Change 2022: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [H.-O. Pörtner, D.C. Roberts, M. Tignor, E.S. Poloczanska, K. Mintenbeck, A. Alegría, M. Craig, S. Langsdorf, S. Löschke, V. Möller, A. Okem, B. Rama (Eds.)]. Cambridge, UK and New York, NY: Cambridge University Press. https://doi.org/10.1017/9781009325844.
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). Estimates suggest that thousands of species disappear each year, many of them unknown to science (Pimm & Raven 2019PIMM, S. L. & RAVEN, P. H. (2019). The state of the World’s biodiversity. In: Dasgupta, P., Raven, P.H. & Mcivor, A.L. (Eds.), Biological Extinction: New Perspectives (pp. 80–112). Cambridge: Cambridge University Press., Cowie et al. 2022COWIE, R.H., BOUCHET, P. & FONTAINE B. (2022). The Sixth Mass Extinction: fact, fiction or speculation? Biological Reviews 97:640–663. doi: 10.1111/brv.12816.
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). To successfully protect our ecosystems in the long term, it is necessary to increase efforts in assessing biodiversity so that the available information is sufficient to identify key areas for conservation and improve management strategies (Amaral & Jablonski 2005AMARAL, A.C.Z. & JABLONSKY, S. (2005). Conservation of Marine and Coastal Biodiversity in Brazil. Conservation Biology (Online), 19, 3, p. 625–631. https://doi.org/10.1111/j.1523-1739.2005.00692.x.
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). Unfortunately, a complete biodiversity assessment is usually precluded by the reduced number of taxonomic specialists and the time-consuming work to sample and identify organisms (Myers et al. 2000MYERS, N., MITTERMEIER, R.A., MITTERMEIER, C.G., DA FONSECA, G.A.B., KENT, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403:853–858., Heino 2010HEINO, J. (2010). Are indicator groups and cross-taxon congruence useful for predicting biodiversity in aquatic ecosystems? Ecological Indicator 10:112–117., Corte et al. 2017CORTE, G.N., CHECON, H.H., FONSECA, G., VIEIRA, D.C., GALLUCCI, F., DOMENICO, M.D. & AMARAL, A.C.Z. (2017). Cross-taxon congruence in benthic communities: Searching for surrogates in marine sediments. Ecological Indicators 78:173–182. https://doi.org/10.1016/j.ecolind.2017.03.031.
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). This situation is even more critical in developing countries like Brazil (Amaral et al. 2016aAMARAL, A.C.Z., CORTE, G.N., ROSA FILHO, J.S., DENADAI, M.R., COLLING, L.A., BORZONE, C.A., VELOSO, V., OMENA, E.P., ZALMON, I., ROCHA-BARREIRA, C.A., SOUZA, J.R.B., ROSA, L.C., ALMEIDA, T.C.M. (2016a). Brazilian sandy beaches: characteristics, ecosystem services, impacts, knowledge and priorities. Brazilian Journal of Oceanography (Online) 64:5–16. https://doi.org/10.1590/S1679-875920160933064sp2.
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, Fernandes et al. 2017FERNANDES, G.W., VALE, M.M. OVERBECK, G.E., BUSTAMANTE, M.M.C., GRELLE, C.E.V., BERGALLO, H.G., MAGNUSSON, W.E., AKAMA, A., ALVES, S.S., AMORIM, A., ... PILLAR, V.D. (2017). Dismantling Brazil’s science threatens global biodiversity heritage. Perspectives in Ecology and Conservation 15(3):239–243. https://doi.org/10.1016/j.pecon.2017.07.004.
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).

Brazil is considered one of the most biologically diverse countries in the world, presenting between 15 and 20% of the total number of known species (Joly & Bicudo 1999JOLY, C.A. & BICUDO, C.E.M. (org.). (1999). Biodiversidade do Estado de São Paulo, Brasil: Síntese do conhecimento ao final do século XX. São Paulo: FAPESP, 176p. , Lewinsohn & Prado 2005LEWINSOHN, T.M. & PRADO, P.I. (2005). How many species are there in Brazil? Conservation Biology 19:619–624. https://doi.org/10.1111/j.1523-1739.2005.00680.x.
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). Nonetheless, due to anthropic environmental impacts, many species are lost day after day before being recognized (Miola et al. 2019MIOLA, D.T.B., MARINHO, A.P., DAYRELL, R.L.C. & SILVEIRA, F.A.O. (2019). Silent loss: Misapplication of an environmental law compromises conservation in a Brazilian biodiversity hotspot. Perspectives in Ecology and Conservation 17(2):84–89. https://doi.org/10.1016/j.pecon.2019.04.001
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). Considering this scenario, in 1999, the Program for the Characterization, Restoration and Sustainable Use of the Biodiversity (BIOTA/FAPESP Program – www.biota.org.br), was created with the support of the São Paulo Research Foundation (FAPESP). The main goal of the program is to support studies targeting the diagnose of the biological diversity from the state of São Paulo. The biological knowledge at the time was published in a series of seven books, named “Biodiversidade do Estado de São Paulo, Brasil: síntese do conhecimento ao final do século XX” (orgs., Joly & Bicudo, 1999JOLY, C.A. & BICUDO, C.E.M. (org.). (1999). Biodiversidade do Estado de São Paulo, Brasil: Síntese do conhecimento ao final do século XX. São Paulo: FAPESP, 176p. ), containing diagnoses, taxonomic, and distribution data of the biota from São Paulo. One of the volumes focused on marine invertebrates, and gathered a considerable knowledge of more than thirty known phyla from the state of São Paulo, highlighting that most of these taxa presented outdated data or had no active specialists (Migotto & Tiago 1999HADEL, V.F., MONTEIRO, A.M.G., DITADI, A.S.F., TIAGO, C.G. & TOMMASI, L.R. (1999). Echinodermata. In: Migotto, Á.E. & Tiago, C.G. (Eds) Biodiversidade do Estado de São Paulo, Brasil: síntese do conhecimento ao final do século XX (pp. 260–271). São Paulo: FAPESP.). Aside from the characterization of biodiversity, the BIOTA/FAPESP Program was designed to ensure the means for the theoretical and practical training of a significant number of young researchers and substantially improved the production of knowledge and scientific competence in studies on conservation and marine management in the state of São Paulo.

One of the initiatives supported by the program, the BIOTA/Araçá project, carried out from 2012 to 2017, was designed to assess and characterize the biodiversity of Araçá Bay, a seascape located on the northern coast of the state of São Paulo. This project brought together about 170 researchers from different scientific areas and institutions, allowing the integration of multiple dimensions, from ecological, social, economic, and political points of view (Amaral et al. 2016bAMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume.). The interdisciplinarity and high number of specialists in the project opened a realistic dialogue between scientists and decision-makers and allowed for a holistic assessment of the benthic biodiversity (Amaral et al. 2016bAMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume., Turra et al. 2016AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume.). The biodiversity data obtained was partially included in identification guides, such as the “Manual de Identificação dos Invertebrados Marinhos da região sudeste-sul do Brasil - Volume 2” (Steiner et al. 2021STEINER, T.M., AMARAL, A.C.Z. & BORGES, M. (2021). Manual de Identificação dos Invertebrados Marinhos da Região Sudeste-Sul do Brasil, Volume 2. São Paulo: Editora da USP. 340p.).

The Araçá Bay, located in the São Sebastião Channel, is part of the Marine Environmental Protection Area of the North Coast of the State of São Paulo and the Municipal Environmental Protection Area of Alcatrazes. The remarkable heterogeneity of this small bay, associated with its accessibility, allowed detailed documentation of its high biodiversity (Amaral et al. 2016bAMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume.). The bay is locally and regionally important, providing important ecosystem services to society. In addition to harboring a high biological diversity, the bay is a stronghold of artisanal fishermen, provides shelter for vessels and access to the sea, hosts scientific and educational activities, and plays a relevant role in effluent depuration and carbon stocking (Amaral et al. 2016bAMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume., Carrilho & Sinisgalli 2018CARRILHO, C.D. & SINISGALLI, P.A. DE A. (2018). Contribution to Araçá Bay management: The identification and valuation of ecosystem services. Ocean & Coastal Management 164:128–135. https://doi.org/10.1016/j.ocecoaman.2018.03.023.
https://doi.org/10.1016/j.ocecoaman.2018...
). However, due to its proximity to the urban area, it has been historically exposed to various anthropogenic disturbances, such as irregular occupations, sewage disposal, and harbor activities (Port of São Sebastião), including one of the most important oil terminals in Brazil (Terminal Aquaviário de São Sebastião). The bay has also been threatened with occupation by the expansion of the nearby port, which would likely severely compromise the ecosystem functioning and its biodiversity (Turra et al. 2017AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C.L.D.B.R. & SCHAEFFER-NOVELLI, Y. (Eds.). (2017). Métodos de estudo em ecossistemas costeiros: biodiversidade e funcionamento. São Paulo: ComArte Júnior.). These conflicts between environment and economic development mirror issues of complex resolutions typical of coastal regions worldwide (Gari et al. 2015GARI, S., NEWTON, A. & ICELY, J. (2015). A review of the application and evolution of the DPSIR framework with an emphasis on coastal social-ecological systems. Ocean and Coastal Management 103:63–77. https://doi.org/10.1016/j.ocecoaman.2014.11.013.
https://doi.org/10.1016/j.ocecoaman.2014...
).

In this context, this study presents a checklist of benthic species found in Araçá Bay, combining data obtained within the BIOTA/Araçá project with past data from previous assessments of the area. Also, the geographical and habitat distribution data were provided for each species, as well as information about material deposited in museum collections, the availability of molecular data, and the status according to the threatened species list. This work is a main outcome of the BIOTA/Araçá project and provides essential information to ensure the long-term sustainability of the bay.

Material and Methods

1. Study area

The Araçá Bay is located on the continental side of the São Sebastião Channel, a 25 km strait on the northern coast of the state of São Paulo, southeastern Brazil (Figure 1). The bay shelters beaches, mangrove stands, rocky shores, and a tidal flat that can exceed 300 m in length. The bay also encompasses a subtidal zone that reaches a maximum depth of 30 m in the São Sebastião Channel. Besides the anthropic impact, the interaction between physical, biological, and geological features makes the bay an area of special interest for different studies (Amaral et al. 2016bAMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume.).

Figure 1
Map of the Araçá Bay, São Paulo state, Brazil. The blue dashed line represents the offshore sewage outfall. Adapted from Amaral et al. (2016b)AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., ROSSI-WONGTSCHOWSKI, C.L.D.B. & SCHAEFFER-NOVELLI, Y. (Eds.). (2016b). Life in Araçá Bay: diversity and importance. 3. ed. São Paulo: Lume..

An exhaustive sampling effort was performed to assess the biodiversity and functioning of the bay. All the different habitats from Araçá Bay were identified and mapped according to the substrate type and their communities’ composition. The sampling to investigate the benthic organisms from the soft and hard bottom was conducted as described in Amaral et al. (2017)AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C.L.D.B.R. & SCHAEFFER-NOVELLI, Y. (Eds.). (2017). Métodos de estudo em ecossistemas costeiros: biodiversidade e funcionamento. São Paulo: ComArte Júnior.. The collaboration of taxonomists during samplings was mandatory for a more comprehensive description of the biodiversity, mainly because of specific sampling procedures that allowed adequate preservation of specimens and for the assessment of microhabitats that eventually would go unnoticed by non-specialist researchers.

2. Soft bottom

2.1. Sampling design

The soft bottom of the bay was sampled to assess the macrobenthic, meiobenthic, bacterial, and fungal biodiversity. Sampling was performed at four campaigns (October 2012, February, June, and September 2013). Thirty-seven sampling stations were established from the intertidal and sublittoral area at the bay (up to a depth of 25 m). Sampling stations were positioned to encompass habitat heterogeneity (i.e., different sediment types and depths), and achieve a reasonable dispersion and spatial coverage. The same locations (±1 m) were sampled during each campaign using a GPS. In the intertidal and shallow sublittoral (< 3 m deep), four samples were taken using a corer of 10 cm diameter and 20 cm depth for the evaluation of macrofauna, and one sample of 2.5 cm in diameter and 5 cm depth for meiofauna at each station. The sampling was performed using the multi-corer (macro and meiofauna), van Veen (macrofauna), and rectangular Dredge (macrofauna) methods in depths ranging from 3 to 25 m. Sediment samples for microorganism analyses were collected in the 37 sampling stations at the bay, according to Zampieri et al. (2016)ZAMPIERI, B.D.B., PINTO, A.B., SCHULTZ, L., DE OLIVEIRA, M.A. & DE OLIVEIRA, A.J.F.C. (2016). Diversity and distribution of heavy metal-resistant bacteria in polluted sediments of the Araçá Bay, São Sebastião (SP), and the relationship between heavy metals and organic matter concentrations. Microbial Ecology 72:582–594. https://doi.org/10.1007/s00248-016-0821-x.
https://doi.org/10.1007/s00248-016-0821-...
and Doi et al. (2018)DOI, S.A., PINTO, A.B., CANALI, M.C.D., POLEZEL, R., CHINELLATO, R.A.M. & DE OLIVEIRA, A.J.F.C. (2018). Density and diversity of filamentous fungi in the water and sediment of Araçá bay in São Sebastião, São Paulo, Brazil. Biota Neotropica 18(1):e20170416. http://dx.doi.org/10.1590/1676-0611-BN-2017-0416.
https://doi.org/10.1590/1676-0611-BN-201...
. Additional samples were taken at each station to evaluate environmental parameters.

2.2. Samples processing

Macrofauna samples were stored in plastic bags and posteriorly sieved with a 0.3 mm mesh. The fauna retained was sorted into taxonomic groups and fixed in 70% or absolute ethanol. The specimens were identified at the lowest level possible by the specialists of each group.

Meiofauna samples were immediately fixed in 4% formaldehyde, posteriorly washed through a 45 µm mesh sieve, then extracted by flotation with Ludox TM 50 (specific density 1.18) (Heip et al. 1985HEIP, C., VINCX, M. & VRANKEN, G. (1985). The ecology of marine nematodes. Oceanography and Marine Biology 23:399–489.). The retained material was stored in formaldehyde 4% and stained with Rose Bengal. The morphological identification of these tiny animals is time-consuming and demands high-quality microscopy and specialized knowledge (Giere 2009GIERE, O. (2009). Meiobenthology - The Microscopic Motile Fauna of Aquatic Sediments. 2nd edition. Berlin: Springer Verlag.). Thus, the morphological identification of many taxa in the present study remained at higher taxonomical levels. Since there is no regional identification key for the meiofauna species, identification down to the species level was done based on the original descriptions.

Bacteria were isolated using the Pour Plate Method in Marine Agar 2216 (MA, Difco) and identified using 16S rRNA gene sequencing (∼1360 nucleotides). The Fungi were isolated using the Spread Plate Method in Potato Dextrose Agar (PDA) and identified using yeast NL1 and NL4 (Pagnocca et al. 2008PAGNOCCA, F.C., RODRIGUES, A., NAGAMOTO, N.S., BACCI, M. JR. (2008). Yeasts and filamentous fungi carried by the gynes of leaf-cutting ants. Antonie Van Leeuwenhoek 94:517–526. http://doi:10.1007/s10482-008-9268-5.
https://doi.org/10.1007/s10482-008-9268-...
). For filamentous fungi, two different nuclear DNA markers were amplified for phylogenetic analysis (LSU and ITS) (Möller et al. 1992). The Technique of Membrane Filtration was used to check the presence of the contaminant microorganism (Candida sp., Escherichia coli, and Enterococcus sp.).

3. Rocky Shore

3.1. Sampling design

The samplings on the rocky shores were carried out from the entrance to the bottom of the bay, near the mouth of the Mãe Isabel River, including those of Pernambuco Island, and the artificial substrate formed by boulders near the port (Figure 1).

The occurrence of common species in the hard bottom was registered and the macrofauna was sampled for later identification (Amaral et al. 2017AMARAL, A.C.Z., TURRA, A., CIOTTI, A.M., WONGTSCHOWSKI, C.L.D.B.R. & SCHAEFFER-NOVELLI, Y. (Eds.). (2017). Métodos de estudo em ecossistemas costeiros: biodiversidade e funcionamento. São Paulo: ComArte Júnior.). The qualitative (active search) and quantitative (20 parcels of 10 × 10 cm, DiasDIAS, G.M., CHRISTOFOLETTI, R.A., KITAZAWA, K. & JENKINS, S.R. (2018). Environmental heterogeneity at small spatial scales affects population and community dynamics on intertidal rocky shores of a threatened bay system. Ocean & Coastal Management 164:52–59. https://doi.org/10.1016/j.ocecoaman.2017.12.001.
https://doi.org/10.1016/j.ocecoaman.2017...
et al. 2018) sampling was carried out at different times, for almost two years (October 2012, February, July, November 2013, March, and June 2014), allowing ephemeral species with a short life cycle to be sampled. Additionally, the pebbles found at the interface with the hard substrate were visually inspected and the sessile and mobile organisms that occupied these microhabitats were collected.

3.2. Samples processing

Macrofauna specimens were anesthetized (MgCl2 or menthol) and preserved in 70% ethanol, while macroalgal samples were fixed in 10% formalin with seawater. The sediment associated with the organisms sampled, mainly macroalgae, sponges, and arborescent bryozoans, was also examined under a stereomicroscope to obtain meiofaunal organisms while they were still alive. Afterward, the samples were divided into taxonomic groups and, when possible, in morpho-species for posterior identification.

To visualize the eyes of the macrofaunal Platyhelminthes, they were dehydrated in an ascending series of ethanol before clearing in clove oil. For observing the anatomical details, other samples were embedded in paraffin, sectioned at 7 µm, and transferred to glass slides coated with albumen-glycerine. Tissues were stained with the Mallory method modified by Canson (1950)CANSON, J.E. (1950). A rapid one-step Mallory Heidenhain stain for connective tissue. Stain Technology 25:225–226. https://doi.org/10.3109/10520295009110996.
https://doi.org/10.3109/1052029500911099...
.

4. Collections

Most of the specimens collected in the different environments were deposited in the Museu de Diversidade Biológica, Instituto de Biologia, Universidade Estadual de Campinas (MDBio/IB-UNICAMP) and in the Museu de Zoologia, Universidade de São Paulo (MZUSP/USP). Material was also deposited in other collections in national and international museums. Much of the deposited material is cataloged and available at https://specieslink.net/ and https://sibbr.gov.br. A list with acronyms and full names of the museums is shown in Table 1.

Table 1
Acronyms, full names and locations of the museums where specimens from Araçá Bay are deposited.

5. Procedures for preparing the Araçá Bay checklist

The current survey of the species from Araçá Bay includes records from the previous assessments and new records consisting of unpublished data obtained during the BIOTA/Araçá project. The checklist by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
provided the starting point. The present review also includes species from scientific collections, previously sampled in the bay, and recently identified by the specialists. The validity of each taxa name was confirmed in specific databases, such as WoRMS (http://www.marinespecies.org/aphia.php?p=search) and TCBF - Taxonomic Catalog of the Brazilian Fauna (http://fauna.jbrj.gov.br). The checklist was divided into three sections (Macrofauna, Meiofauna, and Microorganism), and the phyla were listed in alphabetical order within each section.

When appropriate, the following symbols were used ahead of species names:

β – species sampled during the BIOTA/Araçá project;

® – species recorded in the Araçá Bay for the first time in the current checklist.

We provided relevant data about each species, such as the geographical and habitat distribution. The information was presented in the following sections:

Original name – when needed, the name originally given to the species was presented.

Record in Araçá Bay – for those species previously recorded in the bay, the publication reporting the species in the area was included (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
or a study published thereafter). When the species had been reported with another name, it was indicated between parentheses.

Main taxonomic references – main references related to the taxonomy, phylogeny and/or functional anatomy of the species.

Habitat – information on the environments of occurrence of the species, not restricted to Araçá Bay (such as bathymetry, the type of substrate, and association with different species, among other pertinent information).

Geographical range – localities where the species is recorded, corresponding countries and information such as oceans and/or seas.

Deposited material – information on specimens from Araçá Bay deposited in the museum’s collections. The museum acronym(s) were presented accompanied by a maximum of five lots or the interval between them (e.g., ZUEC BIV 5119 – 5141). When over five registration numbers were available, only the acronym of the museum (s) was informed. Species with no deposit register were reported as NR (no record).

Molecular data – the information about the availability of nucleotide sequences deposited in GenBank was given as AV (available) when there was deposited material; or NR (no record) for species with no deposit register.

Conservation status – status of the species according to the “Red List (ICMBIO)” (https://www.gov.br/icmbio/pt-br/centrais-de-conteudo/publicacoes/publicacoes-diversas/livro-vermelho/livro-vermelho-da-fauna-brasileira-ameacada-de-extincao-2018) or “IUCN – The IUCN Red List of Threatened species” (http://www.iucnredlist.org). The species listed here were classified according to their risk status: Least concern (LR), Vulnerable (VU), Endangered (EN), Critically Endangered (CR), or NR (no record) for unregistered species.

Results and Discussion

During the five years of development of the BIOTA/Araçá project, unprecedented and invaluable results about the biodiversity of Araçá Bay were produced, surpassing studies carried out there between 1950 and 2010 (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
). These results revealed that the bay and the adjacent region (area of the São Sebastião Channel closer to the bay) sustain high biodiversity, with a total of 1177 benthic taxa identified (including identifications at the level of species, genera, or morphotypes). Among those, 276 were recorded for the first time at the Araçá Bay (®), and 11 new species were described (Table 2). Parallel to these results, several papers have been published exploring ecological, social, and economic aspects, which together are generating subsidies for debates about the management and conservation of the bay (e.g., Angelini et al. 2018ANGELINI, R., CONTENTE, R.F., ROSSI-WONGTSCHOWSKI, C.L.D.B., SOARES, L.S.H., SCHAEFFER-NOVELLI, Y., LOPES, R.M., MANCINI, P.L., COLL, M., AMARAL, A.C.Z. (2018). Ecosystem modeling as a framework to convert a multi-disciplinary research approach into a useful model for the Araçá Bay (Brazil). Ocean & Coastal Management 159:1–23. https://doi.org/10.1016/j.ocecoaman.2018.02.007.
https://doi.org/10.1016/j.ocecoaman.2018...
, Checon et al. 2018CHECON, H.H., VIEIRA, D.C., CORTE, G.N., SOUSA, E.C.P.M., FONSECA, G., AMARAL, A.C.Z. (2018). Defining soft bottom habitats and potential indicator species as tools for monitoring coastal systems: a case study in a subtropical bay. Ocean & Coastal Management 164:68–78. https://doi.org/10.1016/j.ocecoaman.2018.03.035.
https://doi.org/10.1016/j.ocecoaman.2018...
, Dias et al. 2018DIAS, G.M., CHRISTOFOLETTI, R.A., KITAZAWA, K. & JENKINS, S.R. (2018). Environmental heterogeneity at small spatial scales affects population and community dynamics on intertidal rocky shores of a threatened bay system. Ocean & Coastal Management 164:52–59. https://doi.org/10.1016/j.ocecoaman.2017.12.001.
https://doi.org/10.1016/j.ocecoaman.2017...
, Stori et al. 2019STORI, F.T., PERES, C.M., TURRA, A., PRESSEY, R.L. (2019). Traditional ecological knowledge supports ecosystem-based management in disturbed coastal marine social-ecological systems. Frontiers in Marine Science 6:571. https://doi.org/10.3389/fmars.2019.00571.
https://doi.org/10.3389/fmars.2019.00571...
, Gallucci et al. 2020GALLUCCI, F., CHRISTOFOLETTI, R.A., FONSECA, G. & DIAS, G.M. (2020). The effects of habitat heterogeneity at distinct spatial scales on hard-bottom-associated communities. Diversity 12(1):39. https://doi.org/10.3390/d12010039.
https://doi.org/10.3390/d12010039....
, Kitazawa et al. 2021KITAZAWA, K., DEBASTIANI, B.R., LÓPEZ, M.S., DUARTE, R.C. & DIAS, G.M. (2021) Can the variation of physical and biological parameters explain the distinct sessile communities from cryptic habitats across a coastal bay? Estuarine, Coastal and Shelf Science 257:107–395. https://doi.org/10.1016/j.ecss.2021.107395.
https://doi.org/10.1016/j.ecss.2021.1073...
).

Table 2
Number of taxa of the groups listed within this checklist. BIOTA: species sampled during the BIOTA/Araçá project; N. id.: taxa not identified at the species level; Reg.: new records; Depos.: species with material from Araçá Bay deposited in museum collections; Mol.: species with molecular data available; Threat.: threatened species; New sp.: species described based on individuals sampled during the BIOTA/Araçá project; Endm.: species endemic to Araçá Bay; Exot.: exotic species, nonnative or introduced to the bay; Econ.: economically exploited.

The current checklist includes 826 species, almost 70% (553 spp.) recorded during the BIOTA/Araçá project (Annex; Supplementary Material). Annelids (225 spp., including macro- and meiofaunal species), mollusks (194 spp.), and crustaceans (177 spp.) were the most speciose taxa. Among the meiofaunal organisms, the nematodes were the most abundant and diversified, however, they were identified only at the morphospecies level (195 morphospecies). The survey presented here reveals seven benthic species endemic to Araçá Bay, 14 threatened species, and seven economically exploited species (see Table 2). Therefore, Araçá Bay shelters not only a diverse fauna but also presents endemism and houses threatened species, justifying the need for the protection of this environment.

More than half of the species listed here have molecular data available (60%) and /or material deposited in the museum’s collections (67%). Those are valuable data sources for future studies in the fields of taxonomy, phylogeny, biogeography, and conservation biology. The results and discussions by groups of organisms sampled by the BIOTA/Araçá project, as well as from records in available literature (mainly Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
) and from museum collections are presented below. The phyla with less than five species recorded (Entoprocta, Phoronida, Hemichordata, and Nemertea) were treated together in the section “Other groups” (1.18).

1. Macrofauna

1.1. Annelida – “Polychaeta”

Polychaetes are among the most diversified benthic organisms and were the most speciose taxa in Araçá Bay. A total of 211 macrofaunal species belonging to 37 families were included in the present checklist (Table 2). As a comparison, the previous survey of the species in the area listed 158 polychaetes identified at the species level (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
). There are about 1350 species reported in Brazil, more than 400 of which are found in the state of São Paulo (Amaral et al. 2023AMARAL, A.C.Z., NALLIN, S.A.H., STEINER, T.M., FORRONI, T.O., GOMES-FILHO, D., ARAÚJO, G.R., FREITAS, R., COSTA, C.A.O., RUTA, C., GOMES, K.R.E. & BONALDO, R.O. (2023). Catálogo das espécies de Annelida “Polychaeta” do Brasil. http://www.ib.unicamp.br/museu_zoologia/files/lab_museu_zoologia/Catalogo_Polychaeta_Amaral_et_al_2022.pdf. Retrieved September 22, 2023.
http://www.ib.unicamp.br/museu_zoologia/...
). Therefore, the number of species recorded in the bay represents more than half of the total polychaete diversity known to the state.

The family Syllidae presented the highest number of species (30), followed by Spionidae (21), Nereididae (14), and Eunicidae (12). In descending order, the most abundant species found during the project were: Capitella nonatoi, Laeonereis acuta, Scoloplos (Leodamas) sp. A, Armandia hossfeldi, Isolda pulchella and Haploscoloplos sp. A. Eight new species for science were described based on specimens sampled during the BIOTA/Araçá project (Fukuda & Nogueira 2014FUKUDA, M.V. & NOGUEIRA, J.M.M. (2014). A new species of Exogone (Syllidae: Exogoninae) from off the State of São Paulo (south-east Brazil). Memoirs of Museum Victoria 71:79–84. http://doi.org/10.24199/j.mmv.2014.71.08.
https://doi.org/10.24199/j.mmv.2014.71.0...
, Silva et al. 2017SILVA, C.F., Seixas, V.C., Barroso, R., Di Domenico, M., Amaral, A.C.Z. & Paiva, P.C. (2017). Demystifying the Capitella capitata complex (Annelida, Capitellidae) diversity by morphological and molecular data along the Brazilian coast. PLoS One 12:e0177760. https://doi.org/10.1371/journal.pone.0177760.
https://doi.org/10.1371/journal.pone.017...
, Silva & Amaral 2019SILVA, C.F. & Amaral, A.C.Z. (2019). Scyphoproctus Gravier, 1904 (Annelida, Capitellidae): description of three new species and relocation of Heteromastides Augener, 1914 in Scyphoproctus. Zootaxa (Online) 4560:95–120. https://doi.org/10.11646/ZOOTAXA.4560.1.5.
https://doi.org/10.11646/ZOOTAXA.4560.1....
), seven classified in Capitellidae family (Capitella aracaensis, C. biota, C. neoaciculata, C. nonatoi, Scyphoproctus paivai, S. profundus, and S. robustus) and one Syllidae (Exogone cebimar).

Besides the eight new species to science, 28 were new records for Araçá Bay and 58 taxa were identified only at the genus level, which may indicate possible new records or new species for science. Additionally, the bay is the type locality of about 20 species of the group, which highlights the importance of the area. The species Eunice sebastiani and those of the Diopatra cuprea complex, found in the area, are classified as threatened, which is aggravated by the fact that they are collected and marketed as bait for recreational fishing.

1.2. Annelida – Echiura

Three echiuran species were registered for Araçá Bay. Two of them, Arhynchite paulensis and Lissomyema exilii, were first described based on material from the Brazilian coast.

1.3. Annelida – Sipuncula

The current list of Sipuncula from Araçá Bay includes eight species, representatives of three families: Sipunculidae, comprising large worms, with trunk up to 35 cm in length; Golfingiidae, with a high degree of morphological diversity; Aspidosiphonidae with hardened structures called shields close to the anus (anal shield) and at the posterior end (caudal shield). The most abundant species collected during the BIOTA/Araçá project is Thysanocardia catharinae. A few specimens sampled during the project were only identified at the genus level, and according to their external anatomy, they were identified as Nephasoma sp. and Phascolion sp., the latter representing the first record of the genus for the São Sebastião Channel.

Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
registered ten species for the Araçá Bay, but Sipunculus multisulcatus should be excluded from this list because it is a junior synonym of S. phalloides, a species already listed for the bay. We could not find the specimens of Sipunculus sp. recorded by Jorge et al. (1969)JORGE, F.B.DE, PETERSEN, J.A. & DITADI, A.S.F. (1969). Iodine accumulation by de nephridia of Sipunculus (Sipuncula). Experientia Basel 25:1147–1148., but according to Ditadi (1982a)DITADI, A.S.F. (1982a). Intertidal Sipunculans (Sipunculus) from Southern Brazil. Revista Brasileira de Biologia 42:785–800. there are three species of Sipunculus in the area (S. nudus, S. phalloides, S. polymyotus). Considering that S. phalloides and S. polymyotus are already on the list of Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
, Jorge et al.´s species can be one of the two previous ones. Sipunculus sp. in Kawauchi (2005)KAWAUCHI, G.Y. (2005) Sipuncula do litoral Sul e Sudeste do Brasil. [Doctoral thesis, Universidade de São Paulo]. http://dx.doi.org/10.5962/bhl.title.109986.
https://doi.org/10.5962/bhl.title.109986...
are confirmed as S. nudus. Thirty-nine species are reported from Brazil (Kawauchi 2005KAWAUCHI, G.Y. (2005) Sipuncula do litoral Sul e Sudeste do Brasil. [Doctoral thesis, Universidade de São Paulo]. http://dx.doi.org/10.5962/bhl.title.109986.
https://doi.org/10.5962/bhl.title.109986...
), and five have the type localities in the country. It is important to note, however, that the diversity of Sipuncula along the Brazilian coast is still poorly known (Schulze & Kawauchi 2021SCHULZE, A. & KAWAUCHI, G.Y. (2021). How Many Sipunculan Species Are Hiding in Our Oceans? Diversity 13:43. https://doi.org/10.3390/d13020043.
https://doi.org/10.3390/d13020043....
).

1.4. Arthropoda – Crustacea, Decapoda

The decapod crustaceans of Araçá Bay were represented by 124 species and 33 families. The composition was dominated by western Atlantic species typical from estuaries and mangroves. Most species are free-living, whereas others are obligate burrow-dwellers or live associated with other invertebrates including bryozoans, echinoderms, polychaetes, and sponges. The white shrimp Litopenaeus schmitti and the swimming crabs of the genus Callinectes are taxa of commercial importance registered in the area. One invasive taxon, Charybdis (Charybdis) hellerii, a nonindigenous portunid from the Indo-West Pacific, widespread in the western Atlantic Ocean (Tavares & Mendonça 1996TAVARES, M. & Mendonça Jr, J.B. (1996). Charybdis hellerii (A. Milne Edwards, 1867) (Brachyura, Portunidae), eighth nonindigenus marine decapod record from Brazil. Crustacean Research 25,151–157. https://doi.org/10.18353/crustacea.25.0_151.
https://doi.org/10.18353/crustacea.25.0_...
, Tavares 2011TAVARES, M. (2011). Alien Decapod Crustaceans in the Southwestern Atlantic Ocean. In: B.S. Galil et al. (Eds.), In the Wrong Place – Alien Marine Crustaceans: Distribution, Biology and Impacts, Invading Nature (pp. 251–268). Springer Series in Invasion Ecology 6.), was also registered. There are no endangered species of decapods living in the bay currently.

Twelve species of hermit crabs were registered in Araçá Bay. Diogenidae is represented by nine species, while Paguridae by three species. All sampled species are restricted to the Western Atlantic (Melo 1996MELO, G.A.S. (1996). Manual de identificação dos Brachyura (caranguejos e siris) do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Plêiade Fapesp, São Paulo., 1999MELO, G.A.S. (1999). Manual de identificação dos Crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea, Astacidea. Plêiade Fapesp, São Paulo.), however with wide latitudinal distribution from the southeastern US coast until southern Brazil or South America. The hermit crab species occur in the intertidal zone or shallow water up to 50 m deep, although Petrochirus diogenes can reach 130 m in depth. Gastropod shells are an important and limiting resource for hermit crabs, which they need to substitute as they grow (Turra et al. 2005DENADAI, M.R., AMARAL, A.C.Z. & TURRA, A. (2005). Structure of molluscan assemblages in sheltered intertidal unconsolidated environments. Brazilian Archives of Biology and Technology 48:825–839. https://doi.org/10.1590/S1516-89132005000600019.
https://doi.org/10.1590/S1516-8913200500...
, Turra & Denadai 2004TURRA, A. (2004). Intersexuality in hermit crabs: reproductive role and fate of gonopores in intersex individuals. Journal of the Marine Biological Association of the United Kingdom 84:757–759. https://doi.org/10.1017/S0025315404009877h.
https://doi.org/10.1017/S002531540400987...
). In this way, the high diversity and abundance of gastropod species in Araçá Bay, due to its high environmental heterogeneity (Denadai et al. 2005TURRA, A., DENADAI, M.R. & LEITE, F.P.P. (2005). Predation on gastropods by shell-breaking crabs: effects on shell availability to hermit crabs. Marine Ecology Progress Series 286:279–291. https://doi.org/10.3354/meps286279.
https://doi.org/10.3354/meps286279...
), make possible the co-occurrence of several hermit crab species in this area. Six new records were presented here (Paguristes puncticeps, Paguristes tortugae, Pseudopaguristes calliopsis, Petrochirus diogenes, Pagurus brevidactylus, and Pagurus leptonyx). However, three of them (Paguristes tortugae, Petrochirus diogenes, and Pagurus brevidactylus) were only visually recorded. Studies on hermit crabs in Araçá Bay are numerous due to the group’s high diversity and abundance in this region. The species registered by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
are the most commonly found in the region and for which there are some studies on biology and ecology (Leite et al. 1998LEITE, F.P.P., TURRA, A. & GANDOLFI, S.M. (1998). Hermit crabs (Crustacea: Decapoda: Anomura), gastropod shells and environmental structure: their relationship in southeastern Brazil. Journal of Natural History 32:1599–1608. https://doi.org/10.1080/00222939800771131.
https://doi.org/10.1080/0022293980077113...
, Turra & Leite 2000TURRA, A. & LEITE, F.P.P. (2000). Population biology and growth of three sympatric species of intertidal hermit crabs in south-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 80(6):1061–1069. https://doi.org/10.1017/S002531540000312X.
https://doi.org/10.1017/S002531540000312...
, 2001TURRA, A. & LEITE, F.P.P. (2001). Fecundity of three sympatric populations of hermit crabs (Decapoda, Anomura, Diogenidae). Crustaceana 74(10):1019–1027., 2002TURRA, A. & LEITE, F.P.P. (2002). Shell utilization patterns of a tropical intertidal hermit crab assemblage. Journal of the Marine Biological Association of the United Kingdom 82(1):97–107. https://doi.org/10.1017/S0025315402005210.
https://doi.org/10.1017/S002531540200521...
, 2003TURRA, A. & LEITE, F.P.P. (2003). The molding hypothesis: linking shell use with hermit crab growth, morphology, and shell-species selection. Marine Ecology. Progress Series 265:155–163., 2004TURRA, A. & LEITE, F.P.P. (2004). Shell-size selection by intertidal sympatric hermit crabs. Marine Biology 145:251–257. https://doi.org/10.1007/s00227-004-1323-9.
https://doi.org/10.1007/s00227-004-1323-...
, 2007TURRA, A. & LEITE, F.P.P. (2007). Embryonic development and duration of incubation period of tropical intertidal hermit crabs (Decapoda, Anomura). Revista Brasileira de Zoologia 24:677–686. https://doi.org/10.1590/S0101-81752007000300020.
https://doi.org/10.1590/S0101-8175200700...
, Turra & Denadai 2001TURRA, A. & LEITE, F.P.P. (2001). Fecundity of three sympatric populations of hermit crabs (Decapoda, Anomura, Diogenidae). Crustaceana 74(10):1019–1027., 2002TURRA, A. & LEITE, F.P.P. (2002). Shell utilization patterns of a tropical intertidal hermit crab assemblage. Journal of the Marine Biological Association of the United Kingdom 82(1):97–107. https://doi.org/10.1017/S0025315402005210.
https://doi.org/10.1017/S002531540200521...
, 2003TURRA, A. & LEITE, F.P.P. (2003). The molding hypothesis: linking shell use with hermit crab growth, morphology, and shell-species selection. Marine Ecology. Progress Series 265:155–163., Nucci et al 2001NUCCI, P.R. & MELO, G.A.M. (2001). First record of Upogebia inomissa Williams, 1993 (Decapoda, Thalassinidea, Upogebiidae) in Brazil. Nauplius 9(1):71–71., Turra 2003TURRA, A. & LEITE, F.P.P. (2003). The molding hypothesis: linking shell use with hermit crab growth, morphology, and shell-species selection. Marine Ecology. Progress Series 265:155–163., 2004TURRA, A. & LEITE, F.P.P. (2004). Shell-size selection by intertidal sympatric hermit crabs. Marine Biology 145:251–257. https://doi.org/10.1007/s00227-004-1323-9.
https://doi.org/10.1007/s00227-004-1323-...
, 2007TURRA, A. & LEITE, F.P.P. (2007). Embryonic development and duration of incubation period of tropical intertidal hermit crabs (Decapoda, Anomura). Revista Brasileira de Zoologia 24:677–686. https://doi.org/10.1590/S0101-81752007000300020.
https://doi.org/10.1590/S0101-8175200700...
, Dominciano et al. 2009DOMINCIANO, L.C.C., SANT’ANNA, B.S. & TURRA, A. (2009). Are the preference and selection patterns of hermit crabs for gastropod shells species- or site-specific? Journal of Experimental Marine Biology and Ecology 378:15–21. https://doi.org/10.1016/j.jembe.2009.07.002.
https://doi.org/10.1016/j.jembe.2009.07....
, Sant’Anna et al. 2010SANT’ANNA, B.S., TURRA, A. & ZARA, F.J. (2010). Simultaneous activity of male and female gonads in intersex hermit crabs. Aquatic Biology 10:201–209. https://doi.org/10.3354/ab00283.
https://doi.org/10.3354/ab00283...
, 2012aSANT’ANNA, B.S., SANTOS, D.M. DOS, DE MARCHI, M.R.R., ZARA, F.J. & TURRA, A. (2012a). Effects of tributyltin exposure in hermit crabs: Clibanarius vittatus as a model. Environmental Toxicology and Chemistry, 31:632–638. https://doi.org/10.1002/etc.1724.
https://doi.org/10.1002/etc.1724...
, 2012bSANT’ANNA, B.S., SANTOS, D.M.DOS, SANDRON, D.C., SOUZA, S.C.DE, DE MARCHI, M.R.R., ZARA, F.J. & TURRA, A. (2012b). Hermit crabs as bioindicators of recent tributyltin (TBT) contamination. Ecological Indicators 14:184–188. https://doi.org/10.1016/j.ecolind.2011.08.010.
https://doi.org/10.1016/j.ecolind.2011.0...
, 2014SANT’ANNA, B.S., SANTOS, D.M., MARCHI, M.R.R., ZARA, F.J. & TURRA, A. (2014). Surface-sediment and hermit-crab contamination by butyltins in southeastern Atlantic estuaries after ban of TBT-based antifouling paints. Environmental Science and Pollution Research 21:6516–6524. https://doi.org/10.1007/s11356-014-2521-8.
https://doi.org/10.1007/s11356-014-2521-...
, Turra & Gorman 2014GORMAN, D., BARROS, F.M.O. & TURRA, A. (2014). What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants, and previous experience. Hydrobiologia 743:285–297., Gorman et al. 2014GORMAN, D., BARROS, F.M.O. & TURRA, A. (2014). What motivates hermit crabs to abandon trapped shells? Assessing the influence of shell value, olfactory attractants, and previous experience. Hydrobiologia 743:285–297., 2015GORMAN, D., SIKINGER, C.E. & TURRA, A. (2015). Spatial and temporal variation in the predation risk for hermit crabs in a subtropical bay. Journal of Experimental Marine Biology and Ecology 462:98–104., 2016GORMAN, D., SOUZA, E.C.F., LEITE, F.P.P. & TURRA, A. (2016). Olfactory selectivity in intertidal hermit crabs: aggregation behavior by Pagurus criniticornis (Decapoda, Anomura) in response to simulated predation on the gastropod Cerithium atratum. Hydrobiologia 772:31–43. http://dx.doi.org/10.1007/s10750-015-2621-6.
https://doi.org/10.1007/s10750-015-2621-...
, Ribeiro et al. 2015RIBEIRO, F.B., MATTHEWS-CASCON, H., MANTELATTO, F.L.M. & BEZERRA, L.E.A. (2015). Shell occupation and ectosymbionts of two hermit crab species in the South Atlantic: a comparative analysis. Journal of the Marine Biological Association of the UK 96(7):1535–1545. https://doi.org/10.1017/S0025315415001836.
https://doi.org/10.1017/S002531541500183...
, Souza et al. 2015SOUZA, E.C.F., TURRA, A., LEITE, F.P.P. & Gorman, D. (2015). Intra-specific competition drives variation in the fundamental and realized niches of the hermit crab, Pagurus criniticornis. Bulletin of Marine Science 91:343–361. https://doi.org/10.5343/bms.2015.1005.
https://doi.org/10.5343/bms.2015.1005...
, Ragagnin et al. 2016RAGAGNIN, M.N., SANT’ANNA, B.S., GORMAN, D., CASTRO, C., TSCHIPTSCHIN, A. & TURRA, A. (2016). What makes a good home for hermits? Assessing gastropod shell density and relative strength. Marine Biology Research 12:379–388. https://doi.org/10.1080/17451000.2016.1148818.
https://doi.org/10.1080/17451000.2016.11...
, 2018RAGAGNIN, M.N., MCCARTHY, I.D., FERNANDEZ, W.S., TSCHIPTSCHIN, A. & TURRA, A. (2018). Vulnerability of juvenile hermit crabs to reduced seawater pH and shading. Marine Environmental Research 142:130–140. https://doi.org/10.1016/j.marenvres.2018.10.001.
https://doi.org/10.1016/j.marenvres.2018...
, Dahlet et al. 2019DAHLET, L.I., CHECON, H.H., YOKOYAMA, L.Q. & TURRA, A. (2019). Patterns of shell utilization by hermit crabs as a proxy of gastropod population dynamics. Marine Biology Research 15:424–433. https://doi.org/10.1080/17451000.2019.1662446.
https://doi.org/10.1080/17451000.2019.16...
).

1.5. Arthropoda – Crustacea, Peracarida

The list of Peracarida species from Araçá Bay comprises 44 valid species distributed in three orders: Amphipoda, Isopoda, and Tanaidacea. The Amphipoda was the most diverse with 29 species, whereas Isopoda and Tanaidacea were represented by nine and six species, respectively. The knowledge about the composition of peracarid species in the bay increased with the register of new occurrences, such as the amphipods Eudevenopus capuciatus and Ampelisca soleata, registered for the first time for the state of São Paulo. In addition, five probable new species were recognized, two of the order Amphipoda (Ampelisca sp. and Monocorophium sp.) and three of Isopoda (Natatolana sp, Discerciles sp., and Uromunna sp.), which can further increase the known diversity of the group for the Brazilian coast. The species of amphipods Elasmopus rapax, Leucothoe alada and L. spinicarpa, and the isopod Cirolana parva previously recorded for Araçá Bay (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
) were not included in the present checklist, since recent taxonomic reviews (Senna & Souza-Filho 2011SENNA, A.R. & SOUZA-FILHO, J.F. (2011). A new species of the Elasmopus rapax complex (Crustacea: Amphipoda: Maeridae) from Brazilian waters. Cahier Biologie Marine 52:57–70. https://doi.org/10.1590/S0001-37652011005000027.
https://doi.org/10.1590/S0001-3765201100...
, White 2011WHITE, K.N. (2011). A taxonomic review of the Leucothoidae (Crustacea: Amphipoda). Zootaxa 3078:1–113. https://doi.org/10.11646/zootaxa.3078.1.1.
https://doi.org/10.11646/zootaxa.3078.1....
, Paiva & Souza-Filho 2014PAIVA, R.J. & SOUZA-FILHO, J.F. (2014). A new species of Cirolana (Leach, 1818) (Isopoda, Cymothoidea, Cirolanidae) from Brazilian coast. Nauplius 22(2):91-102. https://doi.org/10.1590/S0104-64972014000200003.
https://doi.org/10.1590/S0104-6497201400...
) do not indicate the occurrence of these species in Brazil.

1.6. Arthropoda – Crustacea, Stomatopoda

Five species of Stomatopoda in three families were recorded in the Araçá Bay (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
). All species are broadly distributed in the Western Atlantic Ocean.

1.7. Arthropoda – Crustacea, Cirripedia

All four cirripeds species listed here were previously reported by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
. The barnacle Chthamalus bisinuatus dominated the supra-littoral stratum of the Araçá Bay rock shores, and the mid-littoral stratum is characterized by the presence of Tetraclita stalactifera (Dias et al. 2018DIAS, G.M., CHRISTOFOLETTI, R.A., KITAZAWA, K. & JENKINS, S.R. (2018). Environmental heterogeneity at small spatial scales affects population and community dynamics on intertidal rocky shores of a threatened bay system. Ocean & Coastal Management 164:52–59. https://doi.org/10.1016/j.ocecoaman.2017.12.001.
https://doi.org/10.1016/j.ocecoaman.2017...
).

1.8. Bryozoa

After the review of all specimens in different collections, as well as those reported by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
, 40 species of bryozoans are known from Araçá Bay, 15 of which classified in Ctenostomata, 24 in Cheilostomata, and one in Cyclostomata. Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
listed 40 bryozoan species from the area, but there are some misidentifications in that list (e.g., Scrupocellaria bertholletii is now recognized as Cradoscrupocellaria atlantica, see Vieira et al. 2013aVIEIRA, L.M., SPENCER JONES, M. & WINSTON, J.E. (2013a). Cradoscrupocellaria, a new bryozoan genus for Scrupocellaria bertholletii (Audouin) and related species (Cheilostomata, Candidae): taxonomy, biodiversity and distribution. Zootaxa 3707(1):1–63. http://dx.doi.org/10.11646/zootaxa.3707.1.1.
https://doi.org/10.11646/zootaxa.3707.1....
), some duplicate entries (e.g., Scrupocellaria regularis and Scrupocellaria sp. refer to the same species: Aspiscellaria piscaderaensis), and also unnamed taxa (e.g., Bugula sp.). We have recognized five taxa that still require review (Celleporaria sp., Microporella sp.1, Microporella sp.2, Parasmittina sp. and Schizoporella sp.), which may refer to undescribed species. Particularly, ctenostomatous species are abundant and the most common bryozoans in shallow waters, with dominant species belonging to the genus Amathia.

1.9. Chordata – Ascidiacea

The list of ascidians found in Araçá Bay includes 29 species, 17 of which had been previously listed by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
. This number represents almost half of the total diversity known for the state of São Paulo (Rocha et al. 2011ROCHA, R.M., DIAS, G.M. & LOTUFO, T.M.C. (2011). Checklist of ascidians (Tunicata, Ascidiacea) from São Paulo State, Brazil. Biota Neotropica 11(1):749–759. https://doi.org/10.1590/S1676-06032011000500036.
https://doi.org/10.1590/S1676-0603201100...
). The high diversity is surprising given the scarceness of hard substrates in the bay. The bay is the type locality of only one species, Botryllus tabori. The high number of introduced (10) and cryptogenic species of wide geographical distribution (13) found may be explained by the proximity to the São Sebastião port, which may be a source of larvae from nonindigenous species. None of those species is abundant inside the bay, but a few are quite common in the region of the São Sebastião Channel (e.g., Clavelina oblonga, Didemnum psammatodes, Polyclinum constellatum). Ciona robusta, Ecteinascidia styeloides, and Molgula occidentalis were new records in the area, probably very recently introduced in the bay. Ciona robusta is a harmful species for bivalve cultivation (Wilson et al. 2022WILSON, E.R., MURPHY, K.J. & WYETH, R.C. (2022). Ecological Review of the Ciona Species Complex. The Biological Bulletin 242:153–171. https://doi.org/10.1086/719476.
https://doi.org/10.1086/719476...
) and its presence in the region is a threat to this economic activity. The other species are of tropical origin and their presence in the area highlights the dangers of seawater temperature elevation.

1.10. Cnidaria

Cnidarians are represented in the Araçá Bay by the polyp stages of species belonging to the classes Hydrozoa (34 spp.) and Anthozoa (17 spp., including sea anemones), totaling 51 species. Despite some large, noticeable hydroid colonies and polyps of a few sea anemones, most hydroids and anthozoans present in the bay are inconspicuous by their small size and habits, living in crevices or as epibionts of colonial invertebrates or macroalgae. Most cnidarians from the bay are associated with hard substrates. The ones collected by dredging, such as Halecium spp. and Lytocarpia tridentata, for instance, were attached to pebbles, vacant mollusk shells, and corals scattered on the surface of the soft sediment. Dynamena crisioides is one of the few hydroids that colonizes the intertidal zone; in Araçá Bay it is found on vertical rocky walls in the mid-littoral zone, covering large areas of the rock in the form of sparse, yellow colonies. Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
list 27 species of cnidarians, almost half of the species here reported, showing a considerable increase in the recognition of the diversity of Cnidaria in the area.

The present study has increased to eleven the number of species of sea anemones in Araçá Bay (Milanelli 2003MILANELLI, J.C.C. (2003). Biomonitoramento de costões rochosos: Instrumento para avaliação de impactos gerados por vazamentos de óleo na região do Canal de São Sebastião - São Paulo. [Doctoral thesis, Universidade de São Paulo]. https://doi.org/10.11606/T.21.2003.tde-03042007-215200
https://doi.org/10.11606/T.21.2003.tde-0...
, Amaral et al. 2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
. The eleven species belong to ten genera and six families and include seven species recorded from other localities in the state of São Paulo (Silveira & Morandini 2011SILVEIRA, F.L. & MORANDINI, A.C. (2011). Checklist dos Cnidaria do Estado de São Paulo, Brasil. Biota Neotropica 11(1):445–454. https://doi.org/10.1590/S1676-06032011000500016.
https://doi.org/10.1590/S1676-0603201100...
). Most species recorded here belong to the family Actiniidae (Milanelli 2003MILANELLI, J.C.C. (2003). Biomonitoramento de costões rochosos: Instrumento para avaliação de impactos gerados por vazamentos de óleo na região do Canal de São Sebastião - São Paulo. [Doctoral thesis, Universidade de São Paulo]. https://doi.org/10.11606/T.21.2003.tde-03042007-215200
https://doi.org/10.11606/T.21.2003.tde-0...
, Amaral et al. 2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
, being predominantly large and conspicuous polyps that are often abundant in shallow water habitats. The bay is the type locality of two species of burrowing sea anemones: Metapeachia schlenzae and Edwardsia migottoi (Gusmão 2016GUSMÃO, L.C. (2016). Metapeachia schlenzae sp. nov. (Cnidaria: Actiniaria: Haloclavidae) a new burrowing sea anemone from Brazil, with a discussion of the genus Metapeachia. Zootaxa 4072:373–383. http://dx.doi.org/10.11646/zootaxa.4072.3.6.
https://doi.org/10.11646/zootaxa.4072.3....
, Gusmão et al. 2016GUSMÃO, L.C., BRANDÃO, R.A. & DALY, M. (2016). Edwardsia migottoi sp. nov., the first sea anemone species of Edwardsia de Quatrefages 1842 (Anthozoa: Actiniaria: Edwardsiidae) from the Southwestern Atlantic. Marine Biodiversity 48:1313–1323. https://doi.org/10.1007/s12526-016-0585-z.
https://doi.org/10.1007/s12526-016-0585-...
). Metapeachia schlenzae is a burrowing haloclavid species described from specimens collected in the Araçá Bay and Barequeçaba beach in São Sebastião as well as Monte Alto in Rio de Janeiro. Edwardsia migottoi was described using material collected by the BIOTA/Araçá project (Gusmão et al. 2016GUSMÃO, L.C., BRANDÃO, R.A. & DALY, M. (2016). Edwardsia migottoi sp. nov., the first sea anemone species of Edwardsia de Quatrefages 1842 (Anthozoa: Actiniaria: Edwardsiidae) from the Southwestern Atlantic. Marine Biodiversity 48:1313–1323. https://doi.org/10.1007/s12526-016-0585-z.
https://doi.org/10.1007/s12526-016-0585-...
). This was the first record of the genus Edwardsia for the Southwestern Atlantic, highlighting the advantages of a long-term study to uncover the diversity of anemones with cryptic habits and small sizes.

The Taxonomic Catalog of the Brazilian Fauna records 684 species of cnidarians in Brazil (Oliveira 2017OLIVEIRA, O.M.P. (2017). Cnidaria in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br/fauna/faunadobrasil/22. Retrieved February 20, 2017.
http://fauna.jbrj.gov.br/fauna/faunadobr...
), 565 of which marine. Despite its extensive coastline, only 63 species of sea anemones have been recorded from Brazil (Gusmão & Rodríguez 2021GUSMÃO, L.C. & RODRÍGUEZ, E. (2021). Deep-Sea Anemones (Cnidaria: Anthozoa: Actiniaria) from the South Atlantic. Bulletin of the American Museum of Natural History 444(1):1–69. https://doi.org/10.1206/0003-0090.444.1.1.
https://doi.org/10.1206/0003-0090.444.1....
), most of which exhibit large polyps and are abundant in rocky shores and shallow waters (Belém & Preslercravo 1973BELÉM, M.J.C. & PRESLERCRAVO, J.C. (1973). Contribuições ao conhecimento da fauna de Cnidários do Espírito Santo, Brasil. 1. Considerações sobre Actiniaria do Município de Aracruz, ES. Boletim do Museu de Biologia Prof. Mello Leitão (Zoologia) 80:1–14.). Sea anemones are conspicuous members of benthic habitats on the Southeastern coast of Brazil with 22 species recorded for the state of São Paulo (Zamponi et al. 1998ZAMPONI, M.O., BELÉM, M.J.C., SCHLENZ, E. & ACUÑA, F.H. (1998). Distribution and some ecological aspects of Corallimorpharia and Actiniaria from shallow waters of the South American Atlantic coasts. Physis 55:31–45., Silveira & Morandini 2011SILVEIRA, F.L. & MORANDINI, A.C. (2011). Checklist dos Cnidaria do Estado de São Paulo, Brasil. Biota Neotropica 11(1):445–454. https://doi.org/10.1590/S1676-06032011000500016.
https://doi.org/10.1590/S1676-0603201100...
, Fautin 2013FAUTIN, D.G. (2013). Hexacorallians of the World. http://geoportal.kgs.ku.edu/hexacoral/anemone2/index.cfm. Retrieved February 25, 2016.
http://geoportal.kgs.ku.edu/hexacoral/an...
, Gusmão & Rodríguez 2021GUSMÃO, L.C. & RODRÍGUEZ, E. (2021). Deep-Sea Anemones (Cnidaria: Anthozoa: Actiniaria) from the South Atlantic. Bulletin of the American Museum of Natural History 444(1):1–69. https://doi.org/10.1206/0003-0090.444.1.1.
https://doi.org/10.1206/0003-0090.444.1....
).

1.11. Echinodermata

A total of 32 species, belonging to 24 genera, 17 families, and five classes of Echinodermata were recorded in the soft and hard bottom of Araçá Bay. Ophiuroidea was the most representative taxon with 16 species, followed by Asteroidea (7 spp), Holothuroidea (5 spp), Echinoidea (4 spp), and Crinoidea (1 spp). Ophiuroidea was sampled mainly in the intertidal zone up to 20 m deep and the most frequent species were Ophiactis lymani, Microphiopholis subtilis, Ophioderma januarii, Microphiopholis atra and Hemipholis cordifera. Luidia senegalensis was the most abundant Asteroidea collected in the intertidal and subtidal zone. Among Echinoidea, the black sea urchin Arbacia lixula was the most abundant in the study area and Protankyra benedeni was the most frequent Holothuroidea collected in the intertidal and subtidal zone.

In Brazil, there are about 340 registered species of Echinodermata (Ventura et al. 2013VENTURA, C.R.R., BORGES, M., CAMPOS, L.S., COSTA-LOTUFO, L.V., FREIRE, C.A., HADEL, V.F., MANSO, C.L.C., SILVA, J.R.M.C., TAVARES, Y. & TIAGO, C.G. (2013). Echinoderm from Brazil: Historical research and the current state of biodiversity knowledge. In: Alvarado, J.J. & Solís-Marín, F.A. (Eds.), Echinoderm research and diversity in Latin America (pp. 301–344). Berlin/Heidelberg: Springer.), and in the state of São Paulo, nearly 120 species (Hadel et al. 1999HADEL, V.F., MONTEIRO, A.M.G., DITADI, A.S.F., TIAGO, C.G. & TOMMASI, L.R. (1999). Echinodermata. In: Migotto, Á.E. & Tiago, C.G. (Eds) Biodiversidade do Estado de São Paulo, Brasil: síntese do conhecimento ao final do século XX (pp. 260–271). São Paulo: FAPESP., Borges et al. 2006BORGES, M., MONTEIRO, A.M.G. & AMARAL, A.C.Z. (2006). A new species of Ophiomisidium (Echinodermata: Ophiuroidea) from the continental shelf and slope off southern Brazil. Journal of the Marine Biological Association of the United Kingdom 86:1449–1454. https://doi.org/10.1017/S0025315406014500.
https://doi.org/10.1017/S002531540601450...
, Borges & Amaral 2007BORGES, M. & AMARAL, A.C.Z. (2007). Ophiuroidea (Echinodermata): quatro novas ocorrências para o Brasil. Revista Brasileira de Zoologia 24:855–864.). Despite the perimeter of the bay (3 km) amounting to only 0.03% of the length of the Brazilian coastline (8,500 km), the diversity of Echinoderms registered in Araçá Bay represented 8.3% of the species known in Brazil and 26% in the state of São Paulo (Alitto et al. 2016ALITTO, R.A.S., BUENO, M.L., DI DOMENICO, M. & BORGES, M. (2016). Annotated checklist of Echinoderms from Araçá Bay, Southeastern Brazil. Check List 12:1–15. http://dx.doi.org/10.15560/12.1.1836.
https://doi.org/10.15560/12.1.1836...
).

The present study includes 14 new records to the area (such as Amphiura kinbergi, Amphiura princeps, Luidia alternata alternata, Ophioplocus januarii, Ophiothela mirabilis, and Protankyra benedeni), and five species in the Red List (ICMBIO), Astropecten brasiliensis, Astropecten marginatus, Luidia clathrata, Luidia senegalensis, Lytechinus variegatus. Therefore, the conservation of the bay is crucial to support the regional diversity of Echinodermata.

1.12. Mollusca – Bivalvia

Throughout the BIOTA/Araçá project, more than 1800 individuals of bivalves were sampled in hard (rocky shores, associated with rocks, shells, chunks of wood, mangrove roots) and soft bottom (mud, sand). They were identified into 77 species, and three taxa at higher levels. The list of bivalves also includes nine species previously sampled in the bay, totaling 86 species. Tellinidae (14 spp) and Veneridae (13 spp) were the most representative families, followed by Mytilidae (8 spp). This work provided 28 new records for the region, including some rare species such as the carnivorous bivalve Cardiomya cleryana, the endolithic bivalve Lamychaena hians, and also bivalves of the family Corbulidae, such as Caryocorbula chittyana and Caryocorbula marmorata.

For the Brazilian coast, there are about 510 valid species of bivalves recorded (Machado et al. 2023MACHADO, F.M., MIRANDA, M.S., SALVADOR, R.B., PIMENTA, A.D., CÔRTES, M.O., MIYAHIRA, I.C., AGUDO-PADRÓN, I., OLIVEIRA, C.D.C., CAETANO, C.H.S., COELHO, P.R.S., … SIMONE L.R.L. (2023). How many species of Mollusca are there in Brazil? A collective taxonomic effort to reveal this still unknown diversity. Zoologia (Curitiba) (accepted for publication).) of which about 190 have already been registered for the state of São Paulo (Ihering 1897aIHERING, H. (1897a). Os moluscos marinhos do Brasil. Revista do Museu Paulista 2:73–112., bIHERING, H. (1897b). A ilha de São Sebastião. Revista do Museu Paulista 2:129–171., Morretes 1949CORRÊA, D.D. (1949). Sobre o gênero Zygantroplana. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 99:173–218., Haas 1953HAAS, F. (1953). Mollusks from Ilha Grande, Rio de Janeiro, Brazil. Fieldiana (Zoology) 34:203–209., Klappenbach 1965KLAPPENBACH, M. (1965). Lista preliminar de los Mytilidae brasileños. Anais da Acadêmia Brasileira de Ciências 37:327–352., Narchi 1974NARCHI, W. (1974). Aspectos ecológicos e adaptativos de alguns bivalves do litroral paulista. Papéis Avulsos de Zoologia 27:235–262., Lopes & Narchi 1993LOPES, S.G.B.C. & NARCHI, W. (1993). Levantamento e distribuição das espécies de Teredinidae (Mollusca: Bivalvia) no manguezal de Praia Dura, Ubatuba, São Paulo, Brasil. Boletim do Instituto Oceanográfico 41:29–38. https://doi.org/10.1590/S0373-55241993000100003.
https://doi.org/10.1590/S0373-5524199300...
, Migotto et al. 1993MIGOTTO, A.E, TIAGO, C.G. & MAGALHÃES, A.R.M. (1993). Malacofauna marinha da região costeira do Canal de São Sebastião, SP, Brasil: Gastropoda, Bivalvia, Polyplacophora e Scaphopoda. Boletim do Instituto Oceanográfico 41:13–27. https://doi.org/10.1590/S0373-55241993000100002.
https://doi.org/10.1590/S0373-5524199300...
, Simone 1997SIMONE, R. (1997). Mollusca. In: Migotto, A.E. & Thiago, C.G. (Eds.) Biodiversidade do Estado de São Paulo, síntese do conhecimento ao final do século XX, 3: Invertebrados marinhos (pp. 33–46). São Paulo: FAPESP., Salvador et al. 1998SALVADOR, L.B., DOMANESCHI, O., AMARAL, A.C.Z., MORGADO, E.H. & HENRIQUES, S.A. (1998). Malacofauna da região entremarés de praias da Ilha de São Sebastião (São Paulo, Brasil). Revista Brasileira de Zoolologia 15:1013–1035., Machado et al. 2017MACHADO, F., MORTON, B. & PASSOS, F. (2017). Functional morphology of Cardiomya cleryana (d’Orbigny, 1842) (Bivalvia: Anomalodesmata: Cuspidariidae) from Brazilian waters: New insights into the lifestyle of carnivorous bivalves. Journal of the Marine Biological Association of the United Kingdom 97(2):447–462. doi:10.1017/S0025315416000564.
https://doi.org/10.1017/S002531541600056...
). Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
and Tallarico et al. (2014)TALLARICO, L.F., PASSOS F.D., MACHADO, F.M., CAMPOS, A., RECCO-PIMENTEL, S.M. & INTROÍNI, G.O. (2014). Bivalves of the São Sebastião Channel, north coast of the São Paulo State, Brazil. Check List 10:97–105. https://doi.org/10.15560/10.1.97.
https://doi.org/10.15560/10.1.97...
have further expanded the number of species known to the state of São Paulo, mainly for the São Sebastião Channel. Although the total area of Araçá Bay is relatively small when compared to other nearby areas, the incredible biodiversity and the presence of rare bivalve species show its importance as a reservoir for Brazilian malacological knowledge.

1.13. Mollusca – Gastropoda

The gastropod fauna from Araçá Bay was very speciose (101 species), spanning species from all main groups and habits: herbivores (e.g., Diodora cayenensis and Strombus pugilis), detritivores, predators (e.g., Siratus senegalensis), ectoparasites (e.g., Eulima mulata) and even filter-feeders (e.g., Crepidula protea). There is a balance in species from hard and soft bottom habitats, and even a relatively good abundance of shell-lacking species (e.g., Doris januarii). Despite the Araçá Bay being relatively well documented previously, the present survey resulted in 42 new reports for the area. On the other hand, Cerithiopsis emersoni and Mangelia quadrilineata, recorded by Amaral et al. (2010)AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
, were not sampled during the study. As these taxa are easily misidentified, and the previous samples could not be checked, their occurrence in the region remains doubtful.

1.14. Mollusca – Polyplacophora

The current overview showed two families, four genera, and five species of polyplacophores. One species, Ischnoplax pectinata, was recorded for the first time in the bay.

1.15. Mollusca – Scaphopoda

The register of the two first scaphopods species for Araçá Bay, Paradentalium disparile and Pertusiconcha callithrix, was made during the BIOTA/Araçá project. The low number of species and records of scaphopods in the area may be due to the type of soft bottom found in the bay, predominantly muddy sand, which restricts the occurrence of this group.

1.16. Platyhelminthes

A total of seven species of macrofaunal platyhelminths were identified, and another 18 taxa were identified at the genus level. A few species are potentially new to science. It is interesting to note that the Araçá Bay is included in or close to many type localities of the described Brazilian species, namely Ubatuba, São Sebastião, Ilhabela, Santos, and Guarujá (Marcus 1947MARCUS, E. (1947). Turbelários marinhos do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 12:99–206., 1948MARCUS, E. (1948). Turbellaria do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 13:111–243., 1949MARCUS, E. (1949). Turbellaria brasileiros (7). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 14:7–155., 1950MARCUS, E. (1950). Turbellaria brasileiros (8). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 15:69–190., 1952MARCUS, E. (1952). Turbellaria brasileiros (10). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 17:5–186.), but it also houses taxa not previously recorded there. Among these taxa, one is a new record for Brazil (Notoplana queruca) and two others are most likely new species. This evidence leads to the presumption that this environment is characterized by a relatively rich diversity for the group.

Most of the existing data on Platyhelminthes diversity in Brazil results from collections from the coast of the state of São Paulo, very near the Araçá Bay (Marcus 1947MARCUS, E. (1947). Turbelários marinhos do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 12:99–206., 1948MARCUS, E. (1948). Turbellaria do Brasil. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 13:111–243., 1949MARCUS, E. (1949). Turbellaria brasileiros (7). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 14:7–155., 1950MARCUS, E. (1950). Turbellaria brasileiros (8). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 15:69–190., 1952MARCUS, E. (1952). Turbellaria brasileiros (10). Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 17:5–186., 1954MARCUS, E. (1954). Turbellaria brasileiros (11). Papeis Avulsos do Departamento de Zoologia Secretaria de Agricultura–São Paulo 11:419–489., Corrêa 1949CORRÊA, D.D. (1949). Sobre o gênero Zygantroplana. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 99:173–218., du Bois-Reymond Marcus 1955DU BOIS-REYMOND MARCUS, E. (1955). On Turbellaria and Polygordius from the Brazilian coast. Boletim da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, Zoologia 20:19–53. http://dx.doi.org/10.11606/issn.2526-3382.bffclzoologia.1955.120211.
https://doi.org/10.11606/issn.2526-3382....
, 1957DU BOIS-REYMOND MARCUS, E. (1957). On Turbellaria. Academia Brasileira de Ciências 29(1):153–191., 1958DU BOIS-REYMOND MARCUS, E. (1958). On South American Turbellaria. Academia Brasileira de Ciências 30(3):391–417., 1965DU BOIS-REYMOND MARCUS, E. (1965). Drei neotropische Turbellarien. Sitzungen de Gesellschaft naturforschender Freunde zu Berlin 5:129–135., Smith 1960SMITH, E.H. (1960). On a new Polyclad commensal of Prosobranchs. Anais da Academia Brasileira de Ciências 32(3-4):1–4.), and a few records from other regions (Corrêa 1958CORRÊA, D.D. (1958). A new polyclad from Brazil. Boletim do Instituto Oceanográfico 7:81–86., du Bois-Reymond Marcus & Marcus 1968DU BOIS-REYMOND MARCUS, E. & MARCUS, E. (1968). Polycladida from Curaçao and faunistically related regions. Studies on the Fauna of Curaçao and other Caribbean Islands 101:1–133.), totaling 66 species (Carbayo & Froehlich 2008CARBAYO, F. & FROEHLICH, E.M. (2008). Estado do conhecimento dos macroturbelários (Platyhelminthes) do Brasil. Biota Neotropica 10:1131–1134. https://doi.org/10.1590/S1676-06032008000400018.
https://doi.org/10.1590/S1676-0603200800...
). Recently, new studies on the fauna from the Northeastern coast of Brazil and Rio de Janeiro state augmented the number of reported species to 72 (Bulnes & Torres 2014BULNES, V.N. & TORRES, Y. (2014). Pseudoceros astrorum, a new species of Polycladida (Cotylea, Pseudocerotidae) from Northeastern Brazil. Zootaxa 3881(1):94–100. http://dx.doi.org/10.11646/zootaxa.3881.1.7.
https://doi.org/10.11646/zootaxa.3881.1....
, Bahia et al. 2012BAHIA, J., PADULA, V. & DELGADO, M. (2012). Five new records and morphological data of polyclad species (Platyhelminthes: Turbellaria) from Rio Grande do Norte, Northeastern Brazil. Zootaxa 3170:31–44. https://doi.org/10.11646/zootaxa.3170.1.3.
https://doi.org/10.11646/zootaxa.3170.1....
, 2014BAHIA, J., PADULA, V., PASERI LAVRADO, H. & QUIROGA, S. (2014). Taxonomy of Cotylea (Platyhelminthes: Polycladida) from Cabo Frio, southeastern Brazil, with the description of a new species. Zootaxa 3873(5):495–525. https://doi.org/10.11646/zootaxa.3873.5.3.
https://doi.org/10.11646/zootaxa.3873.5....
, 2015BAHIA, J., PADULA, V., DORIGO CORREIA, M. & SOVIERZOSKI, H. (2015). First records of the order Polycladida (Platyhelminthes, Rhabdithophora) from reef ecosystems of Alagoas State, north-eastern Brazil, with the description of Thysanozoon alagoensis sp. nov. Journal of the Marine Biological Association of the United Kingdom 95(8):1653–1666. http://dx.doi.org/10.1017/S0025315415000922.
https://doi.org/10.1017/S002531541500092...
, Bahia & Schrödl 2018BAHIA, J. & SCHRÖDL, M. (2018). Brazilian Polycladida (Rhabditophora: Platyhelminthes): Rediscovery of Marcus’ type material and general revision. Zootaxa 4490:1–121. https://doi.org/10.11646/ZOOTAXA.4490.1.1.
https://doi.org/10.11646/ZOOTAXA.4490.1....
) and pointed to an underestimation of the polyclad fauna of the country.

1.17. Porifera

The present study listed 15 species, 12 genera, and 11 families of sponges (Porifera) found in the Araçá Bay. One species, Haliclona (Soestella) cf. caerulea, was registered for the first time on the southeastern coast of Brazil. Six species were registered for the first time in the area: Callyspongia (C.) pallida, Chondrosia aff. reniformis, Lissodendoryx (L.) isodictyalis, Mycale (Carmia) microsigmatosa, Pachychalina alcaloidifera, and Suberites aurantiacus. Most species registered were broadly distributed in the Western Tropical Atlantic (11 spp.). Three species are found only in Brazil: Chondrosia aff. reniformis (Saint Peter and Saint Paul Rocks, Rocas Atoll, from Pernambuco to São Paulo); Halichondria (H.) sulfurea (endemic to the state of São Paulo); and Pachychalina alcaloidifera (endemic to southeastern Brazil).

Large efforts are still needed to describe the diversity of marine sponges in Brazil, with only 563 species recorded to date (Muricy 2023MURICY, G. (2023). Porifera in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br/fauna/faunadobrasil/6 Retrieved September 22, 2023.
http://fauna.jbrj.gov.br/fauna/faunadobr...
). For the state of São Paulo, 146 marine species were listed (Custódio & Hajdu 2011CUSTÓDIO, M.R. & HAJDU, E. (2011). Checklist de Porifera do Estado de São Paulo, Brasil. Biota Neotropica 11, 427–444. https://doi.org/10.1590/S1676-06032011000500015.
https://doi.org/10.1590/S1676-0603201100...
– including records from the gray literature). Sponges inhabiting the northern coast of the state of São Paulo, especially those from the rocky shores of the municipalities of Ilhabela and São Sebastião, proved to be unexpectedly rich (Hajdu et al. 1999HAJDU, E., BERLINCK, R.G.S. & FREITAS, J.C. (1999). Porifera. In: Migotto, A.E. & Tiago, C.G. (Eds.). Biodiversidade do Estado de São Paulo. Síntese do Conhecimento ao Final do Século XX. 3: invertebrados marinhos. São Paulo: FAPESP., Custódio & Hajdu 2011CUSTÓDIO, M.R. & HAJDU, E. (2011). Checklist de Porifera do Estado de São Paulo, Brasil. Biota Neotropica 11, 427–444. https://doi.org/10.1590/S1676-06032011000500015.
https://doi.org/10.1590/S1676-0603201100...
).

1.18. Other groups

Four Entoprocta species were recorded in Araçá Bay, one sampled during the BIOTA/Araçá project (Barentsia discreta). The synopsis of the Entoprocta from Brazil, including species from Araçá Bay, was published by Vieira and Migotto (2011)VIEIRA, L.M. & MIGOTTO, A.E. (2011). Checklist dos Entoprocta do Estado de São Paulo, Brasil. Biota Neotropica 11(1):497–501. https://doi.org/10.1590/S1676-06032011000500018.
https://doi.org/10.1590/S1676-0603201100...
. Also, four species of hemichordates were registered, one originally described based on specimens from Araçá Bay, Willeyia loya. This species is endemic to the bay and is considered threatened.

One broadly distributed species of Nemertea was registered in the area, Baseodiscus delineatus, previously reported as Baseodiscus curtus (Amaral et al. 2010AMARAL, A.C.Z., MIGOTTO, A.E., TURRA, A. & SCHAEFFER-NOVELLI, Y. (2010). Araçá: biodiversidade, impactos e ameaças. Biota Neotropica 10(1):219–264. http://dx.doi.org/10.1590/s1676-06032010000100022.
https://doi.org/10.1590/s1676-0603201000...
). Finally, a single species of phoronid, Phoronis hippocrepia, is here first reported for Araçá Bay.

2. Meiofauna

There were eight meiofaunal phyla recorded at the Araçá Bay: Annelida, Arthropoda, Gastrotricha, Gnathostomulida, Kinorhyncha, Nematoda, Platyhelminthes, and Tardigrada. Nematodes comprised the most abundant and diverse phylum, with 195 morphospecies. However, organisms that could not be identified at the species level were not included in this report. Here were included a total of 19 meiofaunal species: nine platyhelminths, four kinorhynchs, two gastrotrichs, three polychaetes, and one tardigrade. Three kinorhynch species were first described based on specimens sampled in the Araçá Bay, Echinoderes ajax, E. astridae, and E. marthae (Sørensen 2014SØRENSEN, M.V. (2014). First account of echinoderid kinorhynchs from Brazil, with the description of three new species. Marine Biodiversity 44:251–274. https://doi.org/10.1007/s12526-013-0181-4.
https://doi.org/10.1007/s12526-013-0181-...
).

The marine meiofauna is an abundant and diverse group of animals, comprehending 24 of the 35 metazoan phyla, that can be found mainly inhabiting soft bottoms (Giere 2009GIERE, O. (2009). Meiobenthology - The Microscopic Motile Fauna of Aquatic Sediments. 2nd edition. Berlin: Springer Verlag.). Although some species are cosmopolitan, local communities may contain hundreds of unknown species, allowing only a rough estimate of the total number of existing species (Robertson et al. 2000ROBERTSON, A.L., RUNDLE, S.D. & SCHMID-ARAYA, J.M. (2000). Putting the meio- into stream ecology: current findings and future directions for lotic meiofaunal research. Freshwater Biology 44:177–183. https://doi.org/10.1046/j.1365-2427.2000.00592.x.
https://doi.org/10.1046/j.1365-2427.2000...
, Lambshead & Boucher 2003LAMBSHEAD, P.J.D. & BOUCHER, G. (2003). Marine nematode deep-sea biodiversity - hyperdiverse or hype? Journal of Biogeography 30:475–485. https://doi.org/10.1046/j.1365-2699.2003.00843.x.
https://doi.org/10.1046/j.1365-2699.2003...
). The number of taxonomical studies along the Brazilian coast has expanded in the last decades. Nevertheless, these studies are still localized and there is a vast potential for revealing new species (Fonseca et al. 2014FONSECA, G., NORENBURG, J. & DI DOMENICO, M. (2014). Editorial: diversity of marine meiofauna on the coast of Brazil. Marine Biodiversity 44:459–462. http://dx.doi.org/10.1007/s12526-014-0261-0.
https://doi.org/10.1007/s12526-014-0261-...
).

3. Microorganism

A total of 14 bacteria species were recorded herein for Araçá Bay. The genetic molecular analysis from the gene of the 16S rRNA subunit revealed the prevalence of Bacillus sp. out of the 50 strains isolated in this study. Quantitatively, only four species account for 75% of the bacteria identified for the Araçá Bay. Bacillus pumilus occurred most frequently in the samples (38%), followed by Bacillus cereus (18%), Vibrio alginolyticus (10%) and Planococcus maritimus (8%). The abundance of other bacteria varied from 2% (Bacillus thuringiensis, Bacillus safensis and Bacillus boroniphilus) to 3% (Bacillus aerophilus, Enterobacter asburiae, Exiquobacterium sp., Micrococcus luteus, Staphylococcus aureus, Staphylococcus sp., 2 Staphylococcus epidermidis, Staphylococcus warneri). Another important result is the elevated prevalence of Enterococcus sp. and Escherichia coli, which are used as an indicator of the water quality, showing that the bay has a high fecal contamination. Bacteria may be one of the most abundant and species-rich groups of organisms, and they mediate many critical ecosystem processes (Horner-Devine et al. 2004HORNER-DEVINE, M., LAGE, M., HUGHES, J. & BOHANNAN, B.J.M. (2004). A taxa–area relationship for bacteria. Nature 432:750–753. https://doi.org/10.1038/nature03073.
https://doi.org/10.1038/nature03073...
). However, the diversity of these microorganisms is little explored, especially in Brazil (Cury et al. 2011CURY, J.C., ARAUJO, F.V., COELHO-SOUZA, S.A., PEIXOTO, R.S., OLIVEIRA, J.A.L., SANTOS, H.F., DÁVILA, A.M.R. & ROSADO, A.S. (2011) Microbial diversity of a brazilian coastal region influenced by an upwelling system and anthropogenic activity. PLoS ONE 6(1):e16553. https://doi.org/10.1371/journal.pone.0016553
https://doi.org/10.1371/journal.pone.001...
).

Sixteen fungi species were registered for Araçá Bay. The most frequent genera were Candida, Aspergillus, and Penicillium. Marine yeasts are generally associated with nutrient concentration, pollution, plankton blooms, and macroalgae, suggesting that fungi are also important saprotrophs in marine environments (Kohlmeyer & Kohlmeyer 1979KOHLMEYER, J. & KOHLMEYER, E. (1979). Marine Mycology. The Higher Fungi. New York: Academic Press.). Phylogenetic analysis of environmental marine fungal sequences shows several sequences branching closely to known saprotrophic fungi, including Aspergillus (Richards et al. 2012RICHARDS, T.A., JONES, M.D.M., LEONARD, G. & BASS, D. (2012). Marine Fungi: their ecology and molecular diversity. Annual Review of Marine Science 4:495–522. https://doi.org/10.1146/annurev-marine-120710-100802.
https://doi.org/10.1146/annurev-marine-1...
).

Anthropogenic impacts on the marine environment have threatened microorganisms, altering their abundance and diversity. The study of marine microbial biodiversity is of vital importance to the understanding of the different processes of the ocean, which may present novel microorganisms for screening of bioactive compounds (Das et al. 2006DAS, S., LYLA, P.S. & KHAN, A. (2006). Marine microbial diversity and ecology: importance and future perspectives. Current Science 90:1325–1335.).

Supplementary Material

The following online material is available for this article:

Supplementary - Checklist of benthic species from Araçá Bay.

Table S1 – List of the species recorded in the Araçá Bay and included in the present checklist. The table indicates the species sampled during the BIOTA/Araçá project (β) and those registered for the first time at the Araçá Bay in the present work (x).

Acknowledgments

We are grateful to the institutions, researchers, and students, whose support, knowledge, work, and dedication made the Biota/FAPESP-Araçá project possible. This work was supported by the São Paulo Research Foundation - FAPESP (Proc. 2011/50317-5; 2018/10313-0). ACZA is supported by CNPq (301551/2019-7).

Data Availability

Supporting data are available in <https://doi.org/10.5281/zenodo.10909959>.

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Edited by

Associate Editor
Tito Lotufo

Publication Dates

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

History

  • Received
    26 Oct 2023
  • Accepted
    26 Mar 2024
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