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Shrimps of genus Lysmata Risso, 1816 (Caridea: Lysmatidae) from Queimada Grande Island region, southeastern Brazil

Abstract

The objective of this study is to report the first occurrences of three species from the genus Lysmata Risso, 1816 in an area of the Queimada Grande Island (QGI), a conservation unit on the southern coast of São Paulo, southeastern Brazil. The specimens were sampled manually in August 2018 from a small rocky formation from the QGI region. The species Lysmata bahia Rhyne and Lin, 2006, Lysmata uncicornis Holthuis and Maruin, 1952, and Lysmata vittata (Stimpson, 1860) are reported, of which the last two are not native to the Western Atlantic waters. The present study reports L. uncicornis for the first time on the coast of São Paulo State. The records informed herein not only provide more information about biodiversity, but can also help in the development of management plans and conservation.

Keywords
Aquarium trade; Decapoda; Geographical distribution; Peppermint shrimp; Western Atlantic

INTRODUCTION

The genus LysmataRisso, 1816Risso, A. 1816. Histoire Naturelle des Crustacés des Environs de Nice. Librairie Grecque­-Latine-Allemande, Paris, 175p., which belongs to the family Lysmatidae Dana, 1852Dana, J.D. 1852b. Conspectus Crustaceorum & Conspectus of the Crustacea of the Exploring Expedition under Capt. C. Wilkes, U.S.N. Macroura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1852, 10-29.b, is composed of widely distributed species with distinct behavior (social and sexual) and life habits in different marine environments (Bauer, 2000Bauer, R.T. 2000. Simultaneous hermaphroditism in caridean shrimps: A unique and puzzling sexual system in the Decapoda. Journal of Crustacean Biology, 20: 116-128.; Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Baeza, 2009Baeza, A. 2009. Protrandic simultaneous hermaphroditism is a conserved trait in Lysmata (Caridea: Hippolytidae): implications for the evolution of hermaphroditism in the genus. Smithsonian Contributions to Marine Science, 38: 95-110.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.). Currently, the genus includes 47 species distributed worldwide (Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.), with 18 reported in the Atlantic (Chace, 1972Chace, F. 1972. The Shrimps of the Smithsonian-Bredin Caribbean Expeditions with a Summary of the West Indian Shallow-water Species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 98: 1-179.; Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Baeza and Anker, 2008Baeza, A. and Anker, A. 2008. Lysmata hochi n. sp., a new hermaphroditic shrimp from the Southwestern Caribbean Sea (Caridea: Hippolytidae). Journal of Crustacean Biology, 28: 148-145. ; Anker and Cox, 2011Anker, A. and Cox, D. 2011. A new species of the shrimp genus Lysmata Risso, 1816 (Crustacea, Decapoda) from Guam. Micronesica, 41: 197-214; De Grave and Fransen, 2011De Grave, S. and Fransen, C.H.J.M. 2011. Carideorum Catalogus: The recent species of the Dendrobranchiate, Stenopodidean, Procarididean and Caridean shrimps (Crustacea: Decapoda). Zoologische Mededeligen, 89: 195-589.; Rhyne et al., 2012Rhyne, A.L.; Calado, R. and Santos, A.D. 2012. Lysmata jundalini, a new peppermint shrimp (Decapoda, Caridea, Hippolytidae) from the Western Atlantic. Zootaxa, 3579: 71-79.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Gan and Li, 2016Gan, Z. and Li, X. 2016. Lysmata leptodactylus, a new species of lysmatid shrimp (Crustacea: Decapoda: Caridea) from China. Zootaxa, 4138: 181-188.; Pachelle et al., 2016Pachelle, P.P.G.; Anker, A.; Mendes, C.B. and Bezerra, L.E.A. 2016. Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131: 1-63.; Prakash and Baeza, 2017Prakash, S. and Baeza, J.A. 2017. A new species of Lysmata Risso, 1816 (Crustacea, Decapoda, Lysmatidae) from the Gulf of Mexico. Zootaxa, 4363: 576-582.; Wang and Sha, 2018Wang, Y.-R. and Sha, Z.-L. 2018. Description of two new species of Lysmata Risso, 1816 (Decapoda, Lysmatidae) from the China seas, with remarks on Lysmata vittata (Stimpson 1860). Zootaxa, 4392: 28-40.; De Grave and Anker, 2018De Grave, S. and Anker, A. 2018. A new, distinctly coloured species of Lysmata Risso, 1816 (Malacostraca: Decapoda: Lysmatidae) from the south-central Atlantic. Zootaxa, 4429: 390-400.; González-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.) and 11 of these on the Brazilian coast in which three of them, Lysmata lipkeiOkuno and Fiedler, 2010Okuno, J. and Fiedler, G.C. 2010. Lysmata lipkei, a new species of peppermint shrimp (Decapoda, Hippolytidae) from warm temperature and subtropical waters of Japan. p. 597-610. In: C.H.J.M. Fransen; S. De Grave and P.K.L. Ng (eds), Studies on Malacostraca: Lipkei Bijdeley Holthuis Memorial Volume Crustaceana Monographs, vol. 14. Leiden, Brill., Lysmata uncicornisHolthuis and Maruin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202., and Lysmata vittata (Stimpson, 1860Stimpson, W. 1860. Prodomus descriptionis animallium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republic Federata missa, Cadwaladore Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VIII, Crustacea, Macrura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1860: 22-47.), are exotic (Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

The genus Lysmata has species that are highly valuable in the ornamental aquarium industry (Calado et al., 2003Calado, R.; Narciso, L.; Morais, S.; Rhyne, A.L. and Lin, J. 2003. A rearing system for the culture of ornamental decapod crustacean larvae. Aquaculture, 218: 329-339.; Baeza and Behringer, 2017Baeza, J.A. and Behringer, D.C. 2017. Integrative taxonomy of the ornamental ‘peppermint’ shrimp public market and population genetics of Lysmata boggessi, the most heavily traded species worldwide. PeerJ, 5: e3786.; Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.; González-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.) because they help control pests (anemones of the genus AiptasiaGosse, 1858Gosse, P.H. 1858. Synopsis of the families, genera, and species of the British Actiniae. Annals and Magazine of Natural History, 1: 414-419.) in aquariums, and are visually appealing due to their vivid color patterns (Karplus, 2014Karplus, I. 2014. Symbiosis in Fishes: The Biology of Interspecific Partnerships. Chichester, John Wiley & Sons Press, 460p.; Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.). Due to the popularity of Lysmata in the aquarium trade, the demand for them has grown among marketed marine invertebrates (Wabnitz et al., 2003Wabnitz, C.; Taylor, M.; Green, E. and Razak, T. 2003. From Ocean to Aquarium: The Global Trade in Marine Ornamental Species. Cambridge, UK, UNEP, 65p.; Calado et al., 2007Calado, R.; Vitorino, A.; Dionísio, G. and Dinis, M.T. 2007. A recirculated maturation system for marine ornamental decapods. Aquaculture, 263: 68-74.; Rhyne et al., 2017Rhyne, A.L.; Tlusty, M.F.; Szczebak, J.T. and Holmberg, R.J. 2017. Expanding our understanding of the trade in marine aquarium animals. PeerJ, 5: e2949.). Therefore, areas where Lysmata species occur are targeted for the commercialization of these organisms, including the southeastern coast of Brazil.

Queimada Grande Island (QGI) is part of an Area of Relevant Ecological Interest (AREI) encompassing Queimada Grande and Queimada Pequena Islands; a “sustainable use” marine protected area on the southern coast of São Paulo State, Brazil (Pivetta et al., 2012Pivetta, A.P.D.; de Morais, M.M. and Joelico, E. 2012. Caracterização preliminar quantitativa da estrutura de assembléias de peixes recifais da Ilha da Queimada Grande-SP. Revista Ceciliana, 4: 7-83.). Additionally, QGI is part of the Marine Environmental Protected Area “Litoral Centro”, and this area has different types of zones, according to the zoning protocol - version 18/12/2018 - measuring the level of permission for human activity (APAMLC, 2018APAMLC. FF. 2018. Área de Proteção Ambiental Marinha do Litoral Centro de São Paulo. Fundação Florestal. Minuta de zoneamento da APA Marinha do Litoral Centro. Available at Available at https://www.sigam.ambiente.sp.gov.br/sigam3/Repositorio/511/Documentos/APAM_LC/Minuta_Zoneamento_APAMLC_Comite%20final_limpo_v1.pdf . Accessed on 28 February 2021.
https://www.sigam.ambiente.sp.gov.br/sig...
). Queimada Pequena Island is inside a Zone of Special Protection (ZSP), forbidding any human activity in a radius of 1 km from the island coast. QGI is inside a Zone for Low-Scale Uses (ZLSU) within a radius of 3 km from the island coast and a Zone of Intensive Use (ZUI) beyond this 3 km, allowing some fisheries activities. Studies on the fauna of the subtidal region in QGI have already been reported, including on reef fish (Pivetta et al., 2012Pivetta, A.P.D.; de Morais, M.M. and Joelico, E. 2012. Caracterização preliminar quantitativa da estrutura de assembléias de peixes recifais da Ilha da Queimada Grande-SP. Revista Ceciliana, 4: 7-83.) and coral reefs (Pereira-Filho et al., 2019Pereira-Filho, G.H.; Shintate, G.S.; Kitahara, M.V.; Moura, R.L.; Amado-Filho, G.M.; Bahia, R.G.; Moraes, F.C.; Neves, L.M.; Francini, C.L.B.; Gibran, F.Z. and Motta, F.S. 2019. The southernmost Atlantic coral reef is off the subtropical island of Queimada Grande (24° S), Brazil. Bulletin of Marine Science, 95: 277-287.). Despite this, the biodiversity of crustaceans has not yet been studied in this area. Thus, the aim of the present study is to register the occurrence of Lysmata bahiaRhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204., L. uncicornis, and L. vittata at Queimada Grande Island, using an integrative approach (morphological and molecular analysis). In addition, we expanded the knowledge about the distribution of two invasive species in the Western Atlantic, with a relevant record of these species in a conservation unit area.

MATERIAL AND METHODS

Sampling of Lysmata shrimps

Sampling was accomplished by artisanal collectors who catch ornamental marine organisms. The shrimps were removed from areas near the Queimadas Area of Relevant Ecological Interest (AREI) (Fig. 1) by free divers who collected the shrimps using a hand net from a small rocky formation with biogenic substrate at 6 to 12 m deep (C.H.A. Marques, artisanal fisherman, personal communication). The collection information and the shrimps were voluntarily transferred to one of us (AC-B) to be used in the present study. The sampled specimens were individually stored in plastic bags, kept in insulated boxes with ice and transported to the laboratory. Individuals were identified according to an identification key (Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.) and deposited in the carcinological collection of the Museum of Zoology at the University of São Paulo (MZUSP).

Figure 1.
Sampling region in the Area of Relevant Ecological Interest (AREI) Queimada Grande and Queimada Pequena Islands and the Marine Environmental Protected Area “Litoral Centro” in the Zone of Special Protection (Queimada Pequena Island) and Zone for Low-Scale Use (Queimada Grande Island), southeastern Brazil.

Morphology analysis

Each shrimp was measured and sexed. The carapace length (CL, the distance from the posterior orbital margin to the posterior margin of the carapace) was measured with a Vernier caliper (accuracy 0.01 mm). Due to protandric hermaphroditism reported in many species of the genus Lysmata (see Bauer, 2006Bauer, R.T. 2006. Same sexual system but variable sociobiology: evolution of protandric simultaneous hermaphroditism in Lysmata shrimps. Integrative and Comparative Biology, 46: 430-438.; Alves et al., 2019Alves, D.F.R.; López Greco, L.S.; Barros-Alves, S. de P. and Hirose, G.L. 2019. Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean. PLOS ONE, 14: e0210723.), individuals were simply divided into ovigerous (ov.) and non-ovigerous (non-ov.) specimens. For identification shrimps were examined using a Leica MZ12S stereomicroscope equipped with a camera lucida. The following morphological characters were analyzed: [1] armature of the rostrum, [2] presence or absence of sharp tooth on pterygostomial margin, [3] number of free articles on accessory ramus of lateral antennular flagellum, [4] reach of rostrum in relation to distal margin of third article of antennular peduncle, [5] reach of stylocerite in relation to row of spiniform setae on dorsal surface of first article of antennular peduncule, [6] length of carpus of first pereopod in relation to height in lateral view, [7] number of subdivisions on carpus of second pereopod, [8] length of merus of second pereopod in relation to ischium length, [9] number of fused articles on lateral antennular flagellum before bifurcation with accessory ramus, [10] number of subdivisions on merus of second pereopod, and [11] intraorbital process form. These characters were used because of their importance in the previous identification of Lysmata species (Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

Molecular analysis of Lysmata shrimps

Molecular analysis was based on the 16S rRNA mitochondrial DNA segment following the protocols provided by Schubart et al. (2000Schubart, C.D.; Niegel, J. and Felder, D.L. 2000. Use of mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. p. 817-830. In: C.J.C. Von Vaupel Klein and F.R. Schram (eds.), The Biodiversity Crisis and Crustacea. Crustacean Issues, Vol. 12. Rotterdam, Routledge and CRC Press.). The analysis was carried out to genetically compare the specimens received, with 27 species of Lysmata and ExhippolysmataStebbing, 1915Stebbing, T.R.R. 1915. South African Crustacea. Part VIII of S.A. Crustacea, for the Marine Investigations in South Africa. Annals of the South African Museum, 15: 57-103. (Tab. 1).

Table 1.
Details of specimens and sequences used in the phylogenetic analyses in this study. The new sequences obtained in this study are highlighted. CCDB = Crustacean Collection of Biology Department of FFCLRP, University of São Paulo; IEO-CDCAD = Decapoda and Stomatopoda Crustacean Collection of Spanish Institute of Oceanography in Cadiz; CNCR = National Crustacean Collection of the Universidad Nacional Autónoma de México; LCP/UFSC = Laboratory of Crustaceans and Plankton Collection of Santa Catarina Federal University; MNRJ = Crustacean Collection of National Museum of Rio de Janeiro; MZUSP = Zoological Collection of Museum of Zoology of the University of São Paulo; RMNH = Naturalis Biodiversity Center (formerly Rijksmuseum van Natuurlijke Historie); SMF = Collection of the Senckenberg Natural History Museum; UMML = Collection of The Marine Laboratory, University of Miami.

Total genomic DNA was extracted from abdominal muscle tissue using the Wizard® Genomic DNA Purification Kit (Promega, Madison, WI, USA) following the manufacturer’s protocol. For amplification of the 16S gene segment, we used primers 16 L2 (5′-TGCCTGTTTATCAAAAACAT-3′) and 1472 (5′-AGATAGAAACCAACCTGG-3′) (Schubart et al., 2000Schubart, C.D.; Niegel, J. and Felder, D.L. 2000. Use of mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. p. 817-830. In: C.J.C. Von Vaupel Klein and F.R. Schram (eds.), The Biodiversity Crisis and Crustacea. Crustacean Issues, Vol. 12. Rotterdam, Routledge and CRC Press.; 2002Schubart, C.D.; Cuesta, J.A. and Felder, D.L. 2002. Glycoptograsidae, a new brachyuran family from Central America: larval and adult morphology, and molecular phylogeny of the Grapsoidea. Journal of Crustacean Biology, 22: 28-44. ). PCR reactions were performed in a Veriti® Thermal Cycler (Applied Biosystems, Foster City, CA, USA) and included 12.5 mL of PCR Buffer Go Taq Green (Promega, Madison, WI, USA), 1.0 mL of each primer, 8.5 mL of Milli-Q water (Milipore, Billerica, MA, USA) and 2 mL of each sample at a final volume of 25 mL. PCR cycles proceeded as follows: initial denaturation at 95 °C for 5 min; 40 cycles of 95 °C for 45 sec, 52 °C for 45 sec, and 72 °C for 1 min; and final extension at 72 °C for 5 min. Negative controls (sterile water) were used in all reactions. The results were checked on a 1.5 % agarose gel stained with GelRed. The PCR products were purified using the Wizard® SV Gel and PCR Clean-Up System (Promega) and sequenced on an ABI 3500 Genetic Analyzer (Applied Biosystems) in the Bioinformatics and Evolutionary Biology Laboratory in the Genetics Department at the Federal University of Pernambuco, Brazil.

Forward and reverse sequences were aligned to obtain the consensus sequence in BioEdit v.7.0.5 (Hall, 1999Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleir Acids Symposium Series, 41: 95-98.). Consensus sequences alignment was performed using ClustalW (Thompson et al., 1994Thompson, J.D.; Higgins, D.G. and Gibson, T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. NucleicAcids Research, 22: 4673-4680.) enforcement in BioEdit v.7.0.5 (Hall, 1999Hall, T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleir Acids Symposium Series, 41: 95-98.). The selection of an optimal model of base substitution, based on AICc and conducted in MEGA 7 (see Kumar et al., 2016Kumar, S.; Stecher, G. and Tamura, K. 2016. Mega7: Molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33: 1870-1874.), identified an HKY + G + I evolutionary model (-lnL = -3914.411). Phylogenetic analysis was estimated via the Maximum Likelihood (ML) method in MEGA 7. The robustness of the ML tree topologies was assessed by bootstrap resampling of the observed data 1000 times. To verify intra- and interspecific genetic divergence among the studied sequences, a matrix of genetic divergence was calculated in MEGA 7 based on the p distance (Kumar et al., 2016Kumar, S.; Stecher, G. and Tamura, K. 2016. Mega7: Molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33: 1870-1874.).

RESULTS

In the present study, five individuals of Lysmata were collected from areas around Queimada Grande Island, with two L. bahia, two L. uncicornis, and one L. vittata.

Systematics

Order Decapoda Latreille, 1802Latreille, P.A. 1802. Histoire naturelle, générale et particulière des Crustacés et des Insectes. Paris. 476p.

Infraorder Caridea Dana, 1852aDana, J.D. 1852a. Conspectus of the Crustacea of the Exploring Expedition under Capt. C. Wilkes, U.S.N. Paguridea, continued, Megalopidea and Macroura. The American Journal of Science and Arts, 14: 116-125.

Family Lysmatidae Dana, 1852bDana, J.D. 1852b. Conspectus Crustaceorum & Conspectus of the Crustacea of the Exploring Expedition under Capt. C. Wilkes, U.S.N. Macroura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1852, 10-29.

Lysmata Risso, 1816Risso, A. 1816. Histoire Naturelle des Crustacés des Environs de Nice. Librairie Grecque­-Latine-Allemande, Paris, 175p.

Lysmata bahia Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.

Lysmata bahiaRhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.: 191, figs. 16-18, pls. 1F, 2; Barros-Alves et al., 2015Barros-Alves, S.D.P.; Alves, D.F.R.; Silva, S.L.R.; Guimarães, C.R.P. and Hirose, G.L. 2015. New records of decapod crustaceans from the coast of Sergipe state, Brazil. Check List, 11: 1-7. : 3, figs. 1C, 3; Pachelle et al., 2016Pachelle, P.P.G.; Anker, A.; Mendes, C.B. and Bezerra, L.E.A. 2016. Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131: 1-63.: 16, tab. 1; Pachelle et al., 2020: 60, figs. 3-4.

Hyppolysmata (Hippolysmata) wurdemanni: Fausto Filho, 1970Fausto Filho, J. 1970. Quarta contribuição ao inventário dos crustáceos decápodos marinhos do nordeste brasileiro. Arquivos de Ciência do Mar, 10: 55-60.: 56; Coelho and Ramos, 1972Coelho, P.A. and Ramos, M.A. 1972. A constituição e a distribuição da fauna de decápodos do litoral leste da América do Sul entre as latitudes de 5ºN e 39ºS. Trabalhos do Instituto Oceanográfico da Universidade Federal de Pernambuco, 13: 133-236.: 153 (partim?) [not L. wurdemanni (Gibbes, 1850Gibbes, L.R. 1850. On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science, 3: 165-201.), see Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.]

Lysmata wurdemanni: Chace, 1972Chace, F. 1972. The Shrimps of the Smithsonian-Bredin Caribbean Expeditions with a Summary of the West Indian Shallow-water Species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 98: 1-179.: 129 (remarks on São Paulo material); Coelho et al., 2006Coelho, P.A.; Almeida, A.O.; Souza-Filho, J.F.; Bezerra, L.E.A. and Giraldes, B.W. 2006. Diversity and distribution of the marine and estuarine shrimps (Dendrobrachiata, Stenopodidea and Caridea) from North and Northeast Brazil. Zootaxa, 1221: 41-62.: 121, tab. 3 (partim?) [not L. wurdemanni (Gibbes, 1850Gibbes, L.R. 1850. On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science, 3: 165-201.)]

Material examined. 1 ov. specimen (10.86 mm CL), 1 non-ov. specimen (10.26 mm CL), MZUSP 41122, Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. Santos harbor (Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.).

Distribution. Western Atlantic: Panama and Brazil (Ceará, Sergipe, Bahia, Rio de Janeiro, São Paulo) (Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Barros-Alves et al., 2015Barros-Alves, S.D.P.; Alves, D.F.R.; Silva, S.L.R.; Guimarães, C.R.P. and Hirose, G.L. 2015. New records of decapod crustaceans from the coast of Sergipe state, Brazil. Check List, 11: 1-7. ; Pachelle et al., 2016Pachelle, P.P.G.; Anker, A.; Mendes, C.B. and Bezerra, L.E.A. 2016. Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131: 1-63.; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.; present study).

Remarks. Lysmata bahia was first reported from Brazil by Fausto Filho (1970Fausto Filho, J. 1970. Quarta contribuição ao inventário dos crustáceos decápodos marinhos do nordeste brasileiro. Arquivos de Ciência do Mar, 10: 55-60.) as Hippolysmata wurdemanniGibbes, 1850Gibbes, L.R. 1850. On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science, 3: 165-201., followed by the first occurrence in São Paulo as Lysmata wurdemanni (Gibbes, 1850Gibbes, L.R. 1850. On the carcinological collections of the United States, and an enumeration of species contained in them, with notes on the most remarkable, and descriptions of new species. Proceedings of the American Association for the Advancement of Science, 3: 165-201.) by Chace (1972Chace, F. 1972. The Shrimps of the Smithsonian-Bredin Caribbean Expeditions with a Summary of the West Indian Shallow-water Species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 98: 1-179.), which were later considered paratypes of L. bahia by Rhyne and Lin (2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.). It is also one of the three species that belongs to the L. wurdermanni complex in Brazil, along with Lysmata ankeriRhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204. and L. wurdermanni (see Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). The analyzed specimens presented all the diagnostic characteristics of L. bahia, according to Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). The two specimens presented long stylocerites, almost reaching the distal margin of the first article of the antennular peduncle, which is a characteristic that differentiates L. bahia from L. ankeri and L. wurdemanni (which have a comparatively shorter stylocerite) (Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). However, the two specimens presented the carpus of the first pereiopod about 4 times longer than tall, instead of 4.5 times, as indicated by Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

Lysmata uncicornis Holthuis and Maurin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202.

Lysmata uncicornisHolthuis and Maurin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202.: 198, figs. 1-2; Lagardère, 1971Lagardère, J.P. 1971. Les crevettes des côtes du Maroc. Travaux de l’Institut Scientifique Cherifen, Série Zoologie, 36: 1-140.: 99, figs. 232-235; González-Ortégon et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.: 26, figs. 1-4.

Lysmata arvoredensisGiraldes, Macedo, Brandão, Baeza and Freire, 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.: 5, figs 1-4F.

Material examined. 2 ov. specimens (10.09, 10.12 mm CL), MZUSP 41123 (Fig. 1), Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. Present study.

Distribution. Eastern Atlantic: from Morocco to Congo; Gulf of Cadiz (between Spain and Portugal). Western Atlantic: Brazil (Santa Catarina [as L. arvoredensis] and São Paulo) (Holthuis and Maurin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202.; Lagardère, 1971Lagardère, J.P. 1971. Les crevettes des côtes du Maroc. Travaux de l’Institut Scientifique Cherifen, Série Zoologie, 36: 1-140.; Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.; González-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.; present study).

Remarks. Lysmata uncicornis was recently classified as a senior synonym of L. arvoredensis (see González-Ortégon et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.). The record of L. uncicornis in São Paulo mentioned by Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.) was made via photographic register from a mussel farm in 2012, but was not tracked and remained an uncertain record. Therefore, the present study offers the first documented record of the occurrence of this species on the coast of São Paulo State, based on morphological and molecular analysis, and is the northern limit for the species in Western Atlantic waters. The occurrence of L. uncicornis in Brazilian waters may be associated with the introduction of non-native species by anthropogenic influence related to the marine aquarium trade (González-Ortégon et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.). Both specimens presented all diagnostic characteristics and expected morphological variation for L. uncicornis, according to Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.) (Fig. 2). The species differs from L. bahia by the proportion of the length and height of the carpus of the first pereiopod (longer in L. bahia); by the number of subdivisions in the carpus of the second pereiopod (22-24 versus 29-32 in L. bahia); and the length of the free portion of the accessory ramus of the antennular flagellum (shorter in L. uncicornis).

Figure 2.
Lysmata uncicornisHolthuis and Maurin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202.. A, Specimen collected in the area near to the border of the protected area of Queimada Grande Island, lateral view; B, lateral view, rostrum details and absence of pterogostomial spine; C, dorsal view, reach of rostrum in relation to distal margin of third article of antennular peduncle; D, dorsal antennular flagellum with trace of accessory branch; E, dactyl of pereopod 3, lateral view; F, second pereopod, lateral view, number of subdivisions on carpus; G, first pereopod, lateral view, length of carpus in relation to height. Scale bars, A = 1cm; B-F = 1mm. Photographs by R. C. Santos.

Lysmata vittata ( Stimpson, 1860Stimpson, W. 1860. Prodomus descriptionis animallium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republic Federata missa, Cadwaladore Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VIII, Crustacea, Macrura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1860: 22-47. )

Hippolysmata vittataStimpson, 1860Stimpson, W. 1860. Prodomus descriptionis animallium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republic Federata missa, Cadwaladore Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VIII, Crustacea, Macrura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1860: 22-47.: 26.

Nauticaris unirecedensSpence Bate, 1888Spence Bate, C. 1888. Report on the Crustacea Macrura collected by H.M.S. Challenger during the Years 1873-76. In: J. Murray (ed.), Zoology. Report on the Scientific Results of the Voyage of H.M.S. Challenger During the Years 1873-76 Under the Command of Captain George S. Nares, R.N., F.R.S. and the Late Captain Frank Tourle Thomson, R.N. C. Wyville Thomson and J. Murray (series eds), vol. 24. Edinburgh, Neill and Company. i-xc, 942p., pls. 1-157.: 608, pl. 110, fig. 1

Hippolysmata vittata var. subtilisThallwitz, 1891Thallwitz, J. 1891. Decapoden-Studien, insobesondere basirt auf A.B. Meyer’s Sammlungen im Ostindischen Archipel, nebst einer Aufzählung der Decapoden und Stomatopoden des Dresdener Museums. Abhandlungen und Berichte des Königlichen Zoologischen und Anthropologisch-Etnographischen Museum zu Dresden, 3: 1-56.: 22.

Lysmata vittata: Bruce, 1990Bruce, A.J. 1990. Redescriptions of five Hong Kong carideans first described by William Stimpson, 1860. p. 569-610. In: B. Morton (ed), The Marine Flora and Fauna of Hong Kong and Southern China. Proceedings of the Second International Marine Biological Workshop, Hong Kong, 1986. Hong Kong, Hong Kong University Press.: 601, figs. 23-28; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.: 67; Alves et al., 2018Alves, D.F.R.; Lima, D.J.M.; Hirose, G.L.; Martinez, P.A.; Dolabella, S.S. and De Paiva Barros-Alves, S. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526: 41-55.: figs. 1B, 3; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.: 83.

Hippolysmata durbanensisStebbing, 1921Stebbing, T.R.R. 1921. Some Crustacea from Natal. Annals of the Durban Museum, 3:12-26.: 20, pl. 5.

Lysmata rauliLaubenheimer and Rhyne, 2010Laubenheimer, H. and Rhyne, A.L. 2010. Lysmata rauli, a new species of peppermint shrimp, (Decapoda: Hippolytidae) from the southwestern Atlantic. Zootaxa, 2372: 298-304.: 299, figs. 1-3; Soledade et al. 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.: 67, fig. 2C.

Material examined. 1 non-ov. specimen (7.02 mm CL), MZUSP 41124, Queimada Grande Island, Peruíbe, São Paulo State, Brazil, collector Marques, C.H.A. (artisanal fisherman), 01.viii.2018.

First record for São Paulo. São Vicent Estuary (Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.).

Distribution. Indo-West Pacific: from Mozambique to Hong Kong; Philippines, Japan, Russia, Australia, and New Zealand. Mediterraean Sea. Western Atlantic: Brazil (Sergipe, Bahia, Rio de Janeiro, São Paulo) (Barnard, 1955Barnard, K.H. 1955. Additions to the fauna-list of South Africa Crustacea and Pycnogonida. Annals of the South African Museun, 43: 1-107.; Chace, 1997Chace, F. 1997. The caridean shrimps (Crustacea: Decapoda) of the Albatros Philippine expedition, 1907-1910, part 7: families Atyidae, Eugonatonodidae, Rhynchocinetidae, Bathypalaemonellidae, Processidae, and Hippolitydae. Smithsonian Contributions to Zoology, 587: 1-106.; Ahyong, 2010Ahyong, S.T. 2010. New species and new records of Caridea (Hippolytidae: Pasiphaeidae) from New Zealand. Zootaxa, 2372: 341-357.; Laubenheimer and Rhyne, 2010Laubenheimer, H. and Rhyne, A.L. 2010. Lysmata rauli, a new species of peppermint shrimp, (Decapoda: Hippolytidae) from the southwestern Atlantic. Zootaxa, 2372: 298-304.; Marin et al., 2012Marin, I.N.; Korn, O.M. and Kornienko, E.S. 2012. The caridean shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Hippolytidae): A new species for the fauna of Russia. Russian Journal of Marine Biology, 38: 359-363.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Abdelsalam, 2018Abdelsalam, K.M. 2018. First record of exotic Lysmatid shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Caridea: Lysmatidae) from the Egyptian Mediterranean coast. Mediterranean Marine Science, 19: 124-131.; Alves et al., 2018Alves, D.F.R.; Lima, D.J.M.; Hirose, G.L.; Martinez, P.A.; Dolabella, S.S. and De Paiva Barros-Alves, S. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526: 41-55.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa, 4438: 128-136.; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.; Present study).

Remarks. It is the first non-native species of Lysmata reported on the Brazilian coast (Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.), followed by L. lipkei (see Pachelle et al., 2016Pachelle, P.P.G.; Anker, A.; Mendes, C.B. and Bezerra, L.E.A. 2016. Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131: 1-63.). Recently recognized as a senior synonym of L. rauli (see Laubenheimer and Rhyne, 2010Laubenheimer, H. and Rhyne, A.L. 2010. Lysmata rauli, a new species of peppermint shrimp, (Decapoda: Hippolytidae) from the southwestern Atlantic. Zootaxa, 2372: 298-304.) and due to its wide distribution and diverse color patterns may be considered a species complex (Marin et al. 2012Marin, I.N.; Korn, O.M. and Kornienko, E.S. 2012. The caridean shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Hippolytidae): A new species for the fauna of Russia. Russian Journal of Marine Biology, 38: 359-363.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Anker and De Grave 2016Anker, A. and De Grave, S. 2016. An updated and annotated cheklist of marine and brackish caridean shrimps of Singapore (Crustacea, Decapoda). Raffles Bulletin of Zoology, 34: 343-454.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa, 4438: 128-136.; 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). The analyzed specimen was very damaged, with several broken appendages. However, despite the damage the identification by morphological characteristics was possible, since the rostrum and some appendages were still intact. Thus, it was possible to verify: [1] the presence of a sharp tooth on the pterygostomial margin; [2] seven dorsal and three ventral teeth on the rostrum; [3] a single short free article in the accessory ramus of the antennular flagellum; [4] stylocerite longer, overreaching distal margin of cornea; [5] intraorbital process of carapace longer than wide in lateral view; and [6] first pereopod carpus short, about three times as long as wide in lateral view. These characteristics can be used as morphological evidence, allowing the analyzed specimen to be identified according to the key proposed by Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). The proposition of L. vittata as a senior synonym of L. rauli may be carefully checked using more extensive material and through morphological and molecular analysis because of the possibility of L. vittata being a species complex (Marin et al., 2012Marin, I.N.; Korn, O.M. and Kornienko, E.S. 2012. The caridean shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Hippolytidae): A new species for the fauna of Russia. Russian Journal of Marine Biology, 38: 359-363.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.; Pachelle et al., 2018Pachelle, P.P.G.; Leray, M.; Anker, A. and Lasley, R. 2018. Five new records of marine shrimps (Decapoda: Caridea, Stenopodidea) from the Caribbean coast of Panama. Zootaxa, 4438: 128-136.; 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

Molecular analysis

The two sequences obtained for L. bahia from QGI (Brazil) matched with the sequence from a L. bahia specimen from Sergipe State (Brazil) and Panama (Fig. 3). The genetic divergence among these three L. bahia specimens varied from 0 to 0.004 (p distance). The two sequences obtained for L. uncicornis specimens from QGI (Brazil) matched with the sequences of L. uncicornis from Florianópolis, Santa Catarina State, Brazil (Fig. 3). There were no differences among the four sequences of this species (p distance = 0). The sequence of L. vittata from Ilha da Queimada Grande matched with the sequences of L. vittata from Thailand and Sergipe and Bahia States (Brazil) (Fig. 3). The genetic divergence among the five L. vittata specimens varied from 0 to 0.007 (p distance).

Figure 3.
Phylogenetic tree of genus Lysmata (Risso, 1816Risso, A. 1816. Histoire Naturelle des Crustacés des Environs de Nice. Librairie Grecque­-Latine-Allemande, Paris, 175p.), including Lysmata bahiaRhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204., Lysmata uncicornisHolthuis and Maurin, 1952Holthuis, L.B. and Maruin, C. 1952. Note sur Lysmata uncicornis nov. spec. et sur deux autres espèces intéressantes de crustacés décapodes macroures de la côte Atlantique du Maroc. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, 55: 197-202., and Lysmata vittata (Stimpson, 1860Stimpson, W. 1860. Prodomus descriptionis animallium evertebratorum, quae in Expeditione ad Oceanum Pacificum Septentrionalem, a Republic Federata missa, Cadwaladore Ringgold et Johanne Rodgers Ducibus, observavit et descripsit. Pars VIII, Crustacea, Macrura. Proceedings of the Academy of Natural Sciences of Philadelphia, 1860: 22-47.) from Queimada Grande Island, Brazil (indicated in red), constructed via Maximum Likelihood analysis of the 16S DNA gene. Numbers are support values for 1000 bootstraps; values < 50 % were not included.

DISCUSSION

Through morphological and molecular analyses, the present study confirms the first record of three species from the genus Lysmata in areas surrounding the Queimada Grande Island, southern coast of São Paulo State, of which two species are non-native to the Western Atlantic. Integrative techniques, such as DNA (16S) and morphological characters, contributed and complemented the identification process of Lysmata, which had already proven to be arduous due to ambiguous morphological characteristics, and consequently, by the presence of species complexes (Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Baeza, 2010Baeza, J.A. 2010. Molecular systematics of peppermint and cleaner shrimps: phylogeny and taxonomy of the genera Lysmata and Exhippolysmata (Crustacea: Caridea: Hippolytidae). Zoological Journal of the Linnean Society, 160: 254-265.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Baeza and Behringer, 2017Baeza, J.A. and Behringer, D.C. 2017. Integrative taxonomy of the ornamental ‘peppermint’ shrimp public market and population genetics of Lysmata boggessi, the most heavily traded species worldwide. PeerJ, 5: e3786.; Wang and Sha, 2018Wang, Y.-R. and Sha, Z.-L. 2018. Description of two new species of Lysmata Risso, 1816 (Decapoda, Lysmatidae) from the China seas, with remarks on Lysmata vittata (Stimpson 1860). Zootaxa, 4392: 28-40.; González-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

Lysmata bahia is widely distributed on the Brazilian coast since its description by Rhyne and Lin (2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.). The present record is the southern-most limit of this species occurrence in the Western Atlantic, after the occurrence record in Santos Bay, São Paulo State (Rhyne and Lin, 2006Rhyne, A.L. and Lin, J. 2006. A western Atlantic peppermint shrimp complex: redescription of Lysmata wurdemanni, description of four new species, and remarks on Lysmata rathbunae (Crustacea: Decapoda: Hippolytidae). Bulletin of Marine Science, 79: 165-204.; Alves et al., 2018Alves, D.F.R.; Lima, D.J.M.; Hirose, G.L.; Martinez, P.A.; Dolabella, S.S. and De Paiva Barros-Alves, S. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526: 41-55.; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.). Regarding the non-native species found in the QGI area, L. vittata has already been well established in Brazilian waters (Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Alves et al., 2018Alves, D.F.R.; Lima, D.J.M.; Hirose, G.L.; Martinez, P.A.; Dolabella, S.S. and De Paiva Barros-Alves, S. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526: 41-55.; 2019Alves, D.F.R.; López Greco, L.S.; Barros-Alves, S. de P. and Hirose, G.L. 2019. Sexual system, reproductive cycle and embryonic development of the red-striped shrimp Lysmata vittata, an invader in the western Atlantic Ocean. PLOS ONE, 14: e0210723.), while there have been few occurrence records for L. uncicornis on the coast of Brazil (Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561.; Gonzáles-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

Our results confirm the presence of L. uncicornis on the coast of São Paulo State. This species was previously recorded in São Paulo by Pachelle et al. (2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.), however, this record could not be confirmed because the specimen was lost. Thus, the present study extends the range of L. uncicornis in the Western Atlantic (from 27°25’ S to 24°29’ S of latitude) (Giraldes et al., 2018Giraldes, B.W.; Macedo, T.P.; Brandão, M.C.; Baeza, J.A. and Freire, A.S. 2018. Lysmata arvoredensis nov. sp. a new species of shrimp from the south coast of Brazil with a key to species of Lysmata (Caridea: Lysmatidae) recorded in the southwestern Atlantic. PeerJ, 6: e5561., González-Ortégon et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.). Lysmata uncicornis is the sixth species of Lysmata to be confirmed on the São Paulo State coast, along with L. ankeri, L. bahia, Lysmata intermedia (Kingsley, 1878Kingsley, J.S. 1878. Notes on the North American Caridea in the Museum of the Peabody Academy of Science at Salem, Mass. Proceedings of the Academy of Natural Sciences of Philadelphia, 1878: 89-98.), L. vittata, and L. wurdemanni, and is the second non-native species to be recorded there (Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Pachelle et al., 2016Pachelle, P.P.G.; Anker, A.; Mendes, C.B. and Bezerra, L.E.A. 2016. Decapod crustaceans from the state of Ceará, northeastern Brazil: an updated checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131: 1-63.; Barros-Alves et al., 2016Barros-Alves, S.D.P.; Alves, D.F.R.; Hirose, G.L. and Cobo, V.J. 2016. New records of caridean shrimps, Lysmata ankeri and L. cf. intermedia, from southeast coast of Brazil. Marine Biodiversity Records, 9: 34: 1-9.; Terossi et al., 2018Terossi, M.; Almeida, A.O.; Buranelli, R.C.; Castilho, A.L.; Costa, R.C.; Zara, F.J. and Mantelatto, F.L. 2018. Checklist of decapods (Crustacea) from the coast of the São Paulo state (Brazil) supported by integrative molecular and morphological data: I. Infraorder Caridea: families Hippolytidae, Lysmatidae, Ogyrididae, Processidae and Thoridae. Zootaxa, 4370: 76-94.; Pachelle et al., 2020Pachelle, P.P.G.; Carvalho, L.; Alves, D.F.R. and Anker, A. 2020. A revision of the Brazilian species of Lysmata Risso, 1816 (Decapoda: Caridea: Lysmatidae), with discussion of the morphological characters used in their identification. Zootaxa, 4789: 55-90.).

The dispersal vector responsible for the presence of exotic Lysmata species on the São Paulo coast is still uncertain, nevertheless, ballast water transportation, as previously registered for other Decapoda crustaceans, as well as the high demand of Lysmata specimens for the marine aquarium trade are the most likely causes (Mantelatto and Dias, 1999Mantelatto, F.L.M. and Dias, L.L. 1999. Extension of the known distribution of Charybdis hellerii (A. Milne-Edwards, 1867) (Decapoda, Portunidae) along the Western Tropical South Atlantic. Crustaceana, 72: 617-620.; Calado, 2009Calado, R. 2009. Marine Ornamental Shrimp: Biology, Aquaculture and Conservation. Chichester, John Wiley & Sons Press, 280p.; Pachelle et al., 2011Pachelle, P.P.G.; Mendes, C.B. and Anker, A. 2011. The Indo-West Pacific alpheid shrimp Athanas dimorphus Ortmann, 1894: first record for Brazil and the western Atlantic. Nauplius, 19: 87-96.; Tavares, 2011Tavares, M. 2011. Alien Decapod Crustaceans in the Southwestern Atlantic Ocean. p. 251-268. In: B.S. Galil; P.F. Clark and J.T. Carlton (eds), In the Wrong Place - Alien Marine Crustaceans: Distribution, Biology and Impacts, Invading Nature - Springer Series in Invasion Ecology. Dordrecht, Springer Netherlands.; Soledade et al., 2013Soledade, G.O.; Baeza, J.A.; Boehs, G.; Simões, S.M.; Souza Santos, P.; Costa, R.C. and Almeida, A.O. 2013. A precautionary tale when describing species in a world of invaders: morphology, coloration and genetics demonstrate that Lysmata rauli is not a new species endemic to Brazil but a junior synonym of the Indo-Pacific L. vittata. Journal of Crustacean Biology, 33: 66-77.; Barros-Alves et al., 2016Barros-Alves, S.D.P.; Alves, D.F.R.; Hirose, G.L. and Cobo, V.J. 2016. New records of caridean shrimps, Lysmata ankeri and L. cf. intermedia, from southeast coast of Brazil. Marine Biodiversity Records, 9: 34: 1-9.). The increased demand for these shrimps may result in deregulated exploitation, as well as inappropriate trade, which can lead to the introduction of exotic species, as is the case for L. lipkei, L. uncicornis, and L. vittata on the Brazilian coast, which are originally from Indo-West Pacific (Alves et al., 2018Alves, D.F.R.; Lima, D.J.M.; Hirose, G.L.; Martinez, P.A.; Dolabella, S.S. and De Paiva Barros-Alves, S. 2018. Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526: 41-55.).

The introduction of non-native species by the ornamental aquarium trade needs to be explored (González-Ortegón et al., 2020González-Ortegón, E.; García-Raso, J.E.; Calado, R.; de la Rosa, I.L.; Guerrero, M. and Cuesta, J.A. 2020. Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis and Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50: 26, 1-9.; Alves et al., 2021Alves, D.R.R.; Barros-Alves, S.P.; Dolabella, S.S.; Almeida, A.C. and Martinez, P.A. 2021. Invasive shrimp Cinetorhynchus erythrostictus (Decapoda: Caridea) misidentified in the marine aquarium trade: Niche overlap with a native congeneric species. Estuarine, Coastal and Shelf Science, 258: 107411.). According to Mainka and Howard (2010Mainka, A.A. and Howard, W. 2010. Climate change and invasive species: double jeopardy. Integrative Zoology, 5: 102-111. ), the occurrence of invasive species is currently one of the largest causes of biodiversity loss on the planet along with climate change. The ecological consequences of this introduction can be direct, with the loss of native species, or indirect, through the transmission of pathogens (Rodríguez and Suárez, 2001Rodríguez, G. and Suárez, H. 2001. Anthropogenic dispersal of Decapod crustaceans in aquatic environments. Interciencia, 26: 282-288.; Tavares, 2003Tavares, M. 2003. Espécies exóticas aquáticas e saúde ambiental. Mundo Saúde (Impresso), 27: 530-537.; Almeida et al., 2012Almeida, A.O.; Simões, S.M.; Costa, R.C. and Mantelatto, F.L. 2012. Alien shrimps in evidence: new records of the genus Athanas Leach, 1814 on the coast of São Paulo, southern Brazil (Caridea: Alpheidae). Helgoland Marine Research, 66: 557-565.).

The present study is the first to report crustacean species in areas near to Queimada Grande Island AREI, but is limited to the genus Lysmata. We highlight the importance of carrying out new studies that use new sampling techniques in this area in order to more effectively determine the local diversity in different substrates, as well as mechanisms that may evaluate the process of non-native species introduction and how it occurs; such as molecular analysis. This information could facilitate management and conservation measures that decrease the possible impacts that invasive species have on native species in this conservation unit.

ACKNOWLEDGEMENTS

The authors thank MSc. Isabela R.R. Moraes and Dra. Jessica Colavite for help with the figure 2 construction. The authors thank the anonymous reviewers that improved the quality of the manuscript and the free divers who collected and donated the specimens used in the study. This research was financed by “Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP/SP” (scholarship Nº 2018/00739-0, granted to RCS).

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Publication Dates

  • Publication in this collection
    21 July 2021
  • Date of issue
    2021

History

  • Received
    25 Nov 2020
  • Accepted
    31 Mar 2021
Sociedade Brasileira de Carcinologia Instituto de Biociências, UNESP, Campus Botucatu, Rua Professor Doutor Antônio Celso Wagner Zanin, 250 , Botucatu, SP, 18618-689 - Botucatu - SP - Brazil
E-mail: editor.nauplius@gmail.com