Abstract
The genus Rimapenaeus Pérez Farfante & Kensley, 1997 occurs in shallow waters and includes six species, being four restricted to Pacific Ocean and two restricted to Atlantic Ocean. Along the Brazilian coast, Rimapenaeus constrictus (Stimpson, 1874) (called camarão ferrinho in Brazil) is one of the species most often accidentally caught during fishery activities, but due to its small size and abundance, it is not commercially exploited. Considering its wide distribution in the western Atlantic the purpose of this study was to examine from a molecular and morphological perspective specimens identified as R. constrictus sampled at the two extremes of its distribution (USA and southeastern Brazil). The phylogenetic trees (16S mtDNA and Cytochrome oxidase subunit I genes) showed a split of these specimens in two well-supported lineages: lineage A from USA (Maryland, Virginia, Florida and Gulf of Mexico) and lineage B from southeastern Brazil (Rio de Janeiro and São Paulo). The genetic distance observed between them (16S: 3.2%; COI: 9.4%) is high to be intraspecific, mainly when compared with other Dendrobranchiata studied. Instead of it none clear pattern that allows the morphological separation of these lineages was observed. We conclude that the shrimps usually called of Rimapenaeus constrictus, widely distributed in the Atlantic, actually represents two species and the Brazilian lineage probably is a new species, not described yet.
References
Almeida, A.O., Terossi, M. & Mantelatto, F.L. (2014) Morphology and DNA analyses reveal a new cryptic snapping shrimp of the Alpheus heterochaelis Say, 1818 (Decapoda: Alpheidae) species complex from the western Atlantic. Zoosystema, 36, 53–71. https://doi.org/10.5252/z2014n1a4
Anker, A. (2012) Revision of the western Atlantic members of the Alpheus armillatus H. Milne Edwards, 1837 species complex (Decapoda, Alpheidae), with description of seven new species. Zootaxa, 3386 (1), 1–109. https://doi.org/10.11646/zootaxa.3386.1.1
Anker, A. & Baeza, J.A. (2021) Thor dicaprio sp. nov., a new, conspicuously coloured shrimp from the tropical western Atlantic, with taxonomic remarks on the T. amboinensis (De Man, 1888) complex (Decapoda: Caridea: Thoridae). Zootaxa, 5039, 495–517. https://doi.org/10.11646/zootaxa.5039.4.3
Anker, A., Hultgren, K.M. & De Grave, S. (2017) Synalpheus pinkfloydi sp. nov., a new pistol shrimp from the tropical eastern Pacific (Decapoda: Alpheidae). Zootaxa, 4254, 111–119. https://doi.org/10.11646/zootaxa.4254.1.7
Anker, A., Hurt, C., Jara, J.A. & Knowlton, N. (2008) Revision of the Alpheus cylindricus Kingsley, 1878 species complex (Crustacea: Decapoda: Alpheidae), with revalidation of A. vanderbilti Boone, 1930. Zootaxa, 1943 (1), 53–68. https://doi.org/10.11646/zootaxa.1943.1.4
Burkenroad, M.D. (1934) Littoral Penaeidea chiefly from the Bingham Oceanographic Collection, with a revision of Penaeopsis and descriptions of two new genera and eleven new American species. Bulletin of the Bingham Oceanographic Collection, 4, 1–109.
Burkenroad, M.D. (1938) The Templeton Crocker Expedition. XIII. Penaeidae from the region of Lower California and Clarion Island, with descriptions of four new species. Zoologica, 23, 55–91. https://doi.org/10.5962/p.184696
Carvalho-Batista, A., Negri., M., Pileggi, L.G., Castilho, A.L., Costa, R.C. & Mantelatto, F.L. (2014) Inferring population connectivity across the range of distribution of the stiletto shrimp Artemesia longinaris Spence Bate, 1888 (Decapoda, Penaeidae) from DNA barcoding: implications for fishery management. ZooKeys, 457, 271–288. https://doi.org/10.3897/zookeys.457.6569
Carvalho-Batista, A., Negri, M., Tamburus, A.F., Costa, R.C., Castilho, A.L., Zara, F.J. & Mantelatto, F.L. (2018) Genetic comparison of the red shrimp Pleoticus muelleri (Decapoda: Solenoceridae) using the barcode gene reveals the absence of cryptic speciation along its distribution. Regional Studies in Marine Science, 24, 392–399. https://doi.org/10.1016/j.rsma.2018.10.003
Carvalho-Batista, A., Terossi, M., Zara, F.J., Mantelatto, F.L. & Costa, R.C. (2019) A multigene and morphological analysis expands the diversity of the seabod shrimp Xiphopenaeus Smith, 1869 (Decapoda: Penaeidae), with descriptions of two new species. Scientific Reports, 9, 15281. https://doi.org/10.1038/s41598-019-51484-3
Carvalho-Batista, A., Terossi, M., Zara, F.J., Mantelatto, F.L. & Costa, R.C. (2020) Validation of Xiphopenaeus dincao Carvalho-Batista, Terossi, Zara, Mantelatto & Costa and Xiphopenaeus baueri Carvalho-Batista, Terossi, Zara, Mantelatto & Costa (Decapoda: Penaeidae) from western Atlantic. Zootaxa, 4772 (3), 597–599. https://doi.org/10.11646/zootaxa.4772.3.10
Chace, F.A. (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. https://doi.org/10.5479/si.00810282.98
Chan, T.-Y., Cleva, R. & Chu, K.H. (2016) On the genus Trachysalambria Burkenroad, 1934 (Crustacea, Decapoda, Penaeidae), with descriptions of three new species. Zootaxa, 4150 (3), 201–254. https://doi.org/10.11646/zootaxa.4150.3.1
Chan, T-Y., Tong, J., Tam, Y.K. & Chu, K.H. (2008) Phylogenetic relationships among the genera of the Penaeidae (Crustacea: Decapoda) revealed by mitochondrial 16S rRNA gene sequences. Zootaxa, 1694 (1), 38–50. https://doi.org/10.11646/zootaxa.1694.1.2
Chowdhury, L.M., Kathirvelpandian, A., Divya, P.R., Basheer, V.S., Shanis, R., Chelath, M., Pavan-Kumar, A. & Krishna, G. (2019) Molecular identification and phylogenetic assessment of species under genus Parapenaeopsis Alcock, 1901, from Indian waters, Mitochondrial DNA, Part A, 30, 191–200. https://doi.org/10.1080/24701394.2018.1472249.
Coelho, P.A. & Ramos-Porto, M. (1980) Crustáceos decápodos da costa do Maranhão, Brasil. Boletim do Instituto Oceanográfico, 29 (2), 135–138. https://doi.org/10.1590/S0373-55241980000200028
Costa, R.C. & Fransozo, A. (2004) Reproductive biology of the shrimp Rimapenaeus constrictus (Decapoda, Penaeidae) in the Ubatuba region of Brazil. Journal of Crustacean Biology, 24, 274–281. https://doi.org/10.1651/C-2437
Costa, R.C., Fransozo, A., Mantelatto, F.L. & Castro, R.H. (2000) Occurrence of shrimp species (Crustacea: Decapoda: Natantia: Penaeidea and Caridea) in Ubatuba Bay, Ubatuba, SP, Brazil. Proceedings of Biological Society of Washington, 113, 776–781.
Cunha, A.M., Terossi, M., Mantelatto, F.L. & Almeida, A.O. (2021) Genetic variation and cryptic diversity of the Alpheus lobidens complex (Decapoda: Alpheidae) associated with marine ecoregions. Marine and Freshwater Research, 73, 319–327. https://doi.org/10.1071/MF21043
De Grave, S. & Fransen, C.H.J.M. (2011) Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen, 85, 195–589.
D’Incao, F. (1998) Malacostraca. Eucarida. Dendrobranchiata. In: Young, P.S. (Ed.), Catalogue of Crustacea of Brazil. Museu Nacional, Rio de Janeiro, pp. 311–321.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. https://doi.org/10.1093/nar/gkh340
Evans, A. (1967) Syntypes of Decapoda described by William Stimpson and James Dana in the collections of the British Museum (Natural History). Journal of Natural History, 1, 399–411. https://doi.org/10.1080/00222936700770391
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.
Garcia, J.R., Wolf, M.R., Costa, R.C. & Castilho, A.L. (2016) Growth and reproduction of the shrimp Rimapenaeus constrictus (Decapoda: Penaeidae) from the southeastern coast of Brazil. Regional Studies in Marine Science, 6, 1–9. https://doi.org/10.1016/j.rsma.2016.02.006
Gusmão, J., Lazoski, C., Monteiro, F.A. & Solé-Cava, A.M. (2006) Cryptic species and population structuring of the Atlantic and Pacific seabob shrimp species, Xiphopenaeus kroyeri and Xiphopenaeus rivetii. Marine Biology, 149, 491–502. https://doi.org/10.1007/s00227-005-0232-x
Hall T. (2005) BioEdit 7.0.5. North Carolina State University, Department of Microbiology. Available from: http://www.mbio.ncsu.edu/BioEdit/bioedit.html (accessed 17 May 2022)
Han, Z., Zhu, W., Zheng, W., Li, P. & Shui, B. (2015) Significant genetic differentiation between the Yellow Sea and East China Sea populations of cocktail shrimp Trachypenaeus curvirostris revealed by the mitochondrial DNA COI gene. Biochemical Systematics and Ecology, 59, 78–84. https://doi.org/10.1016/j.bse.2014.12.028
Hay, W.P. & Shore, C.A. (1918) The Decapod crustaceans from Beaufort, N.C., and the surrounding region. Bulletin of the United States Bureau of Fisheries, 55, 369–475.
Heller, C. (1862) Neue Crustaceen, gesammelt während der Weltumseglung der k.k. Fregatte Novara. Zweiter vorläufiger Bericht. Verhandlungen der kaiserlich-königlichen zoologisch-botanischen Gesellschaft in Wien, 12, 519–528.
Hiroki, K.A.N., Fransozo, A., Costa, R.C., Castilho, A.L., Shimizu, R.M. & Furlan, M. (2011) Bathymetric distribution of the shrimp Rimapenaeus constrictus (Stimpson, 1874) (Decapoda: Penaeidae) in two locations off the southeastern Brazilian coast. Marine Biology Research, 7, 176–185. https://doi.org/10.1080/17451000.2010.489614
Huff, J.A. & Cobb, S.P. (1979) Penaeoid and sergestoid shrimps (Crustacea: Decapoda). Memoirs of the Hourglass Cruises, 5 (4), 1–102.
Kumar, K., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi.org/10.1093/molbev/msy096
Latreille, P.A. (1817) Pénée. Penaeus. Nouveau Dictionnaire d’Histoire Naturelle, 25, 152–156.
Lopes, A., Grabowski, R.C., Garcia, J.R., Fransozo, A., Costa, R.C., Hiroki, K.A. & Castilho, A.L. (2017) Population dynamics of Rimapenaeus constrictus (Stimpson, 1874) (Penaeoidea) on the southeastern Brazilian coast: implications for shrimp fishing management from a 5-year study on a bycatch species. Anais da Academia Brasileira de Ciências, 89, 1013–1025. https://doi.org/10.1590/0001-3765201720160567
Mantelatto, F.L., Tamburus, A.F., Carvalho-Batista, A., Rossi, N., Buranelli, R.C., Pantaleo, J., Teles, J.N., Zara, F.J., Carvalho, F.L., Bochini, G.L., Terossi, M., Robles, R., Castilho, A.L. & Costa, R.C. (2022) Checklist of decapod crustaceans from the coast of the So Paulo state (Brazil) supported by integrative molecular and morphological data: V. Dendrobranchiata and Pleocyemata [Achelata, Astacidea, Axiidea, Caridea (Alpheoidea and Processoidea excluded), Gebiidea, Stenopodidea]. Zootaxa, 5121 (1), 1–74. https://doi.org/10.11646/zootaxa.5121.1.1
Mathews, L.M. & Anker A. (2009) Molecular phylogeny reveals extensive ancient and ongoing radiations in a snapping shrimp species complex (Crustacea, Alpheidae, Alpheus armillatus). Molecular Phylogenetics and Evolution, 50, 268–281. https://doi.org/10.1016/j.ympev.2008.10.026
Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 gateway computing environments workshop (GCE), Ieee, November, 2010, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129.
Milne Edwards, A. & Bouvier, E.L. (1909) Reports on the results of dredging under the supervision of Alexander Agassiz, in the Gulf of Mexico (1877–78) in the Caribbean Sea (1878–79), and Along the Atlantic coast of the United States (1880), by the U.S. Coast Survey Stamer “Blake”. XLIV Les Pénéides et Sténopides. Memoirs of the Museum of Comparative Zoology of Harvard College, 27 (3), 179–274.
Obarrio, J.L. (1954) Investigación del Camarón en Panamá. Segundo Centro Latinoamericano de Capacitación Pesquera. Trabajos presentados al final del curso por los señores becados, 41, 1–6.
Oliveira, C.M.C.A., Mantelatto, F.L. & Terossi, M. (2021) Systematics of the shrimp genus Atya (Decapoda, Atyidae) in the light of multigene-based phylogenetic and species delimitation inference. Zoologica Scripta, 50, 780–794. https://doi.org/10.1111/zsc.12503
Oliveira-Souza, W. & Lavrado, H.P. (2017) Population structure and temporal variation of the roughneck shrimp Rimapenaeus constrictus (Decapoda: Penaeoidea) in a coastal bay of the southwestern Atlantic. Marine Biology Research, 13, 1073–1083. https://doi.org/10.1080/17451000.2017.1342846
Palumbi, S.R. & Benzie, J. (1991) Large mitochondrial DNA differences between morphologically similar Penaeid shrimp. Molecular Marine Biology and Biotechnology, 1, 27–34.
Pérez Farfante, I. (1967) A new species and two new subspecies of shrimp of the genus Penaeus from the Western Atlantic. Proceedings of the Biological Society of Washington, 80, 83–100.
Pérez Farfante, I. (1971) A key to the American Pacific shrimps of the genus Trachypenaeus (Decapoda, Penaeidae), with the description of a new species. Fishery Bulletin, 69, 635–646.
Pérez Farfante, I. (1988) Illustrated Key to Penaeoid Shrimps of Commerce in the Americas. NOAA Technical Report, NMFS, 64, 1–32.
Pérez Farfante, I. & Kensley, B. (1997) Penaeoid and sergestoid shrimps and prawns of the world. Keys and diagnoses for the families and genera. Mémoires du Muséum national d’histoire naturelle. Tome 175. Editions du Museum national d’Histoire naturelle, Paris, 233 pp.
Pierjorge, R.M., Pontes, M.N., Duarte, A.V.B. & Gusmão, J. (2014) Haplotype-specific singlelocus multiplex PCR assay for molecular identification of sea-bob shrimp, Xiphopenaeus kroyeri (Heller, 1862), cryptic species from the Southwest Atlantic using a DNA pooling strategy for simultaneous identification of multiple samples. Biochemical Systematics and Ecology, 54, 348–353. https://doi.org/10.1016/j.bse.2014.03.023
Purushothaman, P., Chakraborty, R.D., Kuberan, G. & Maheswarudu, G. (2019) Integrative taxonomy of commercially important deep water penaeoid shrimps from India. Journal of Genetics, 98, 12. https://doi.org/10.1007/s12041-018-1052-3
Schmitt, W.L. (1935) Crustacea, Macrura and Anomura of Porto Rico and the Virgin Islands. Scientific Survey of Porto Rico and the Virgin Islands, New York Academy of Sciences, 15 (2), 12–227. https://doi.org/10.5962/bhl.title.10217
Smith, S.I. (1885) On some genera and species of Penaeidae, mostly from dredgings off the east coast of the United States Fish Commission. Proceedings of the United States National Museum, 8, 170–190. https://doi.org/10.5479/si.00963801.507.170
Soledade, G.O., Terossi, M., Scioli, J.A., Mantelatto, F.L. & Almeida, A.O. (2019) A new western Atlantic snapping shrimp of the Alpheus macrocheles group (Caridea, Alpheidae) revealed by morphological, molecular and color data. European Journal of Taxonomy, 581, 1–21. https://doi.org/10.5852/ejt.2019.581
Stimpson, W. (1874) Notes on North American Crustacea, in the museum of the Smithsonian Institution. No. III. Annals of the Lyceum of Natural History of New York, 10 (6), 119–163.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Williams, A.B. (1965) Marine decapod crustaceans of the Carolinas. Fishery Bulletin, 65 (10), 1–298.
Williams, A.B. (1984) Shrimps, lobsters, and crabs of the Atlantic Coast of the Eastern United States, Maine to Florida. Smithsonian Institution Press, Washington, D.C., 545 pp.