Abstract
An integrative approach was used, combining morphological and molecular analyses, to provide the first report of Lysmata lipkei and L. vittata in Sergipe State, Brazil, and confirm that both species are invasive of the Atlantic Ocean. Lysmata shrimps were sampled in the estuary region of the Vaza-Barris river, Sergipe State, northeastern Brazil, and identified as L. lipkei (n = 8) and L. vittata (n = 20). To molecular phylogenetic analysis was used 16S DNA fragments, comparing 26 species of the Lysmata-Exhippolysmata clade and two species of the genus Merguia (outgroup). Phylogenetic analysis indicated the absence of consistent genetic divergence (p distance < 0.018) between specimens from Atlantic and Indo-Pacific oceans. We conclude that L. lipkei and L. vittata have successfully invaded the western Atlantic and are also present in Sergipe State, northeastern Brazil.
References
Abdelsalam, K.M. (2018) First record of the exotic lysmatid shrimp Lysmata vittata (Stimpson, 1860) (Decapoda: Caridea: Lysmatidae) from the Egyptian Mediterranean coast. Mediterranean Marine Science, 19 (1), 124–131.
https://doi.org/10.12681/mms.15591Ahyong, S.T. (2010) New species and new records of Caridea (Hippolytidae: Pasiphaeidae) from New Zealand. Zootaxa, 357, 341–357.
Amat, F., Hontoria, F., Ruiz, O., Green, A.J., Sánchez, M.I., Figuerola, J. & Hortas, F. (2005) The American brine shrimp as an exotic invasive species in the western Mediterranean. Biological Invasions, 7, 37–47.
https://doi.org/10.1007/s10530-004-9634-9Anker, A. & De Grave, S. (2016) An updated and annotated checklist of marine and brackish caridean shrimps of Singapore (Crustacea, Decapoda). Raffles Bulletin of Zoology, 2016, 343–454.
Anker, A., Baeza, J.A. & De Grave, S. (2009) A new species of Lysmata (Crustacea, Decapoda, Hippolytidae) from the Pacific Coast of Panama, with observations of its reproductive biology. Zoological Studies, 48, 682–692.
Baeza, 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.
https://doi.org/10.1111/j.1096-3642.2009.00605.xBaeza, J.A. & Anker, A. (2008) Lysmata hochi n. sp., a new hermaphroditic shrimp from the southwestern caribbean sea (Caridea: Hippolytidae). Journal of Crustacean Biology, 28, 148–155.
https://doi.org/10.1651/07-2839R.1Baeza, J.A. & Fuentes, M.S. (2013) Exploring phylogenetic informativeness and nuclear copies of mitochondrial DNA (Numts) in three commonly used mitochondrial genes: Mitochondrial phylogeny of peppermint, cleaner, and semi-terrestrial shrimps (Caridea: Lysmata, Exhippolysmata, and Merguia). Zoological Journal of the Linnean Society, 168, 699–722.
https://doi.org/10.1111/zoj.12044Baeza, J.A., Schubart, C.D., Zillner, P., Fuentes, S. & Bauer, R.T. (2009) Molecular phylogeny of shrimps from the genus Lysmata (Caridea: Hippolytidae): the evolutionary origins of protandric simultaneous hermaphroditism and social monogamy. Biological Journal of the Linnean Society, 96, 415–424.
https://doi.org/10.1111/j.1095-8312.2008.01133.xBarros-Alves, S.P., Alves, D.F.R., Hirose, G.L. & Cobo, V.J. (2016) New records of caridean shrimps, Lysmata ankeri and L. cf. intermedia, from southeast coast of Brazil. Marine Biodiversity Records, 9, 2–5.
https://doi.org/10.1186/s41200-016-0037-2Bruce, A.J. (1983) Lysmata debelius new species, a new hippolytid shrimp from the Philippines. Revue française d’Aquariologie, 9, 115–120. [for 1982]
Bruce, A.J. (1986) Redescriptions of five Hong Kong carideans first described by William Stimpson, 1860. In: Morton, B. (Ed.), Proceedings of the Second International Marine Biological Workshop: the Marine Flora and Fauna of Hong Kong and Southern China. Hong Kong University Press, Hong Kong, pp. 569–610.
Candolin, U., Bertell, E. & Kallio, J. (2018) Environmental disturbance alters the ecological impact of an invading shrimp. Functional Ecology, 32 (5), 1370–1378.
https://doi.org/10.1111/1365-2435.13078Chace, 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.00810282.98Chace, F.A. (1997) The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine Expedition, 1907-1910, Part 7: Families Atyidae, Eugonatonotidae, Rhynchocinetidae, Bathypalaemonellidae, Processidae, and Hippolytidae. Smithsonian Contributions to Zoology, 587, 1–106.
Cohen, A.N. & Carlton, J.T. (1998) Accelerating invasion rate in a highly invaded estuary. Science, 279, 555–558.
https://doi.org/10.1126/science.279.5350.555Crafton, R.E. (2014) Modeling invasion risk for coastal marine species utilizing environmental and transport vector data. Hydrobiologia, 746, 349–362.
https://doi.org/10.1007/s10750-014-2027-xCunha, A.M., Terossi, M., Mantelatto, F.L. & Almeida, A.O. (2017) Morphological and molecular analyses support the amphi-Atlantic distribution and taxonomic status of the snapping shrimp Alpheus intrinsecus Spence Bate, 1888 (Crustacea: Decapoda: Alpheidae). Zootaxa, 4303 (4), 573–589.
https://doi.org/10.11646/zootaxa.4303.4.8De 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, 195–304.
De Grave, S. & Anker, A. (2018) A new, distinctly coloured species of Lysmata Risso, 1816 (Malacostraca: Decapoda: Lysmatidae) from the south-central Atlantic. Zootaxa, 4429 (2), 390–400.
https://doi.org/10.11646/zootaxa.4429.2.13De Grave, S., Chan, T.Y., Fujita, Y. & Okuno, J. (2012) Hippolytidae and Barbouriidae (Decapoda: Caridea) collected during the Ryukyu “KUMEJIMA 2009” Expedition. Zootaxa, 3367, 95–102.
Dohrn, P.F.R. & Holthuis, L.B. (1950) Lysmata nilita, a new species of prawn (Crustacea Decapoda) from the Western Mediterranean. Pubblicazioni della Stazione Zoologica di Napoli, 22, 339–347.
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29 (8), 1697–1973.
https://doi.org/10.1093/molbev/mss075Fiedler, G.C., Rhyne, A.L., Segawa, R., Aotsuka, T. & Schizas, N.V. (2010) The evolution of euhermaphroditism in caridean shrimps: a molecular perspective of sexual systems and systematics. BMC evolutionary biology, 10, 297.
https://doi.org/10.1186/1471-2148-10-297Fransen, C.H.J.M. (1991) Lysmata olavoi, a new shrimp of the family Hippolytidae (Decapoda, Caridea) from the Eastern Atlantic Ocean. Life and Earth Sciences, 9, 63–73.
Geller, J.B. (1999) Decline of a native mussel masked by sibling species invasion. Conservation Biology, 13, 661–664.
https://doi.org/10.1046/j.1523-1739.1999.97470.xGeller, J.B., Walton, E.D., Grosholz, E.D. & Ruiz, G.M. (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Molecular Ecology, 6, 901–906.
https://doi.org/10.1046/j.1365-294X.1997.00256.xGibbes, 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.
Giraldes, B.W., Macedo, T.P., Brandão, M.C., Baeza, J.A. & 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.
https://doi.org/10.7717/peerj.5561Gordon, I. (1935) On new and imperfectly known species of Crustacea Macrura. The Journal of the Linnean Society, 39, 307–351.
https://doi.org/10.1111/j.1096-3642.1935.tb00075.xGrosholz, E. (2002) Ecological and evolutionary consequences of coastal invasions. Trends in Ecology & Evolution, 17, 22–27.
https://doi.org/10.1016/S0169-5347(01)02358-8Gust, N. & Inglis, G.J. (2006) Adaptive multi-scale sampling to determine an invasive crab’s habitat usage and range in New Zealand. Biological Invasions, 8, 339–353.
https://doi.org/10.1007/s10530-004-8243-yHale, H.M. (1929) The Crustaceans of South Australia. Part 2. Handbooks of the Flora and Fauna of South Australia, issued by the British Science Guild (South Australia Branch). Government Printer, Adelaide, 179 pp. [pp. 201–380]
Hayashi, K. (2007) Lysmata dispar sp. nov., a new shrimp from the Dampier Archipelago, Western Australia, with notes on other species of the family Hippolytidae (Crustacea: Decapoda: Caridea). Records of the Western Australian Museum, 73, 85–95.
https://doi.org/10.18195/issn.0313-122x.73.2007.085-095Hiller, A. & Lessios, H.A. (2017) Phylogeography of Petrolisthes armatus, an invasive species with low dispersal ability. Scientific Reports, 7, 3359.
https://doi.org/10.1038/s41598-017-03410-8Holland, B.S. (2000) Genetics of marine bioinvasions. Hydrobiologia, 420, 63–71.
https://doi.org/10.1023/A:1003929519809Holland, B.S., Dawson, M.N., Crow, G.L. & Hofmann, D.K. (2004) Global phylogeography of Cassiopea (Scyphozoa: Rhizostomeae): Molecular evidence for cryptic species and multiple invasions of the Hawaiian Islands. Marine Biology, 145, 1119–1128.
https://doi.org/10.1007/s00227-004-1409-4Holthuis, L.B. (1947) The Hippolytidae and Rhynchocinetidae collected by the Siboga and Snellius expeditions, with remarks on other species. The Decapoda of the Siboga-Expedition. Part IX. Siboga-Expedition, Monograph, 39a8, 1–100.
Holthuis, L.B. (1948) Note on some Crustacea Decapod Natantia from Surinam. Proceedings van de Koninklijke Nederlandsche Akademie van Wetenschappen, 51, 1104–1113.
Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755.
https://doi.org/10.1093/bioinformatics/17.8.754Kemp, S. (1914) Notes on Crustacea Decapoda in the Indian Museum. V. Hippolytidae. Records of the Indian Museum, 10, 81–129.
https://doi.org/10.5962/bhl.part.5624Kingsley, J.S. (1879) List of the North American Crustacea belonging to the suborder Caridea. Bulletin of the Essex Institute, 10, 53–71. [for 1878]
Knowlton, N. (1993) Sibling Species in the Sea. Annual Review of Ecology and Systematics, 24, 189–216.
https://doi.org/10.1146/annurev.es.24.110193.001201Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for Bigger Datasets. Molecular biology and evolution, 33, 1870–1874.
https://doi.org/10.1093/molbev/msw054Levitt, Y., De Grave, S. & Shenkar, N. (2014) First record of an invasive shrimp from the family Processidae (Crustacea, Decapoda) in the Mediterranean Sea. Mediterranean Marine Science, 15, 650–653.
https://doi.org/10.12681/mms.956Lohan, K.M.P., Hill-Spanik, K.M., Torchin, M.E., Strong, E.E., Fleischer, R.C. & Ruiz, G.M. (2015) Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean. Marine Biology, 162, 957–968.
https://doi.org/10.1007/s00227-015-2637-5Lohrer, A.M. & Whitlatch, R.B. (2002) Relative impacts of two exotic brachyuran species on blue mussel populations in Long Island Sound. Marine Ecology Progress Series, 227, 135–144.
https://doi.org/10.3354/meps227135Lopes, E.M., Ferreira, C.E.L. & Ventura, C.R.R. (2017) Occurrence of the genus Pseudoboletia (Echinoidea: Toxopneustidae) in the South-Western Atlantic: morphological and molecular approaches. Revista de Biología Tropical, 65, 299–308.
https://doi.org/10.15517/rbt.v65i1-1.31698Man, J.G. de (1888) Report on the podophthalmous Crustacea of the Mergui Archipelago, collected for the Trustees of the Indian Museum, Calcutta, by Dr. John Anderson F.R.S., Superintendent of the Museum. The Journal of the Linnean Society, 22, 1–305.
Marin, I.N., Korn, O.M. & Kornienko, E.S. (2012a) On the presence of the caridean shrimp Lysmata vittata (Decapoda, Hippolytidae) in the Russian waters of the Sea of Japan. Crustaceana, 85, 123–124.
https://doi.org/10.1163/156854012X623548Marin, I.N., Korn, O.M. & Kornienko, E.S. (2012b) 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.
https://doi.org/10.1134/S1063074012040062Negri, M., Schubart, C.D. & Mantelatto, F.L. (2018) Tracing the introduction history of the invasive swimming crab Charybdis hellerii (A. Milne-Edwards, 1867) in the Western Atlantic: evidences of high genetic diversity and multiple introductions. Biological Invasions, 1–28. [published online]
https://doi.org/10.1007/s10530-018-1660-0Okuno, J. & Fiedler, C. (2010) Lysmata lipkei, a new species of peppermint shrimp (Decapoda, Hippolytidae) from warm temperate and subtropical waters of Japan. In: Fransen, C. de Grave, S. & Ng, P. (Eds.), Crustaceana Monographs: Studies on Malacostraca: Lipke Bijdeley Holthuis Memorial Volume. Brill, Leiden, pp. 597–610.
Pachelle, P.P.G., Anker, A., Mendes, C.B. & 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), 1–63.
https://doi.org/10.11646/zootaxa.4131.1.1Prakash, S. & Baeza, J.A. (2017) A new species of Lysmata Risso, 1816 (Crustacea, Decapoda, Lysmatidae) from the Gulf of Mexico. Zootaxa, 4363, 576–582.
https://doi.org/10.11646/zootaxa.4363.4.10Rathbun, M.J. (1900) Results of the Branner-Agassiz Expedition to Brazil. I. The decapod and stomatopod Crustacea. Proceedings of the Washington Academy of Sciences, 2, 133–156.
Rathbun, M.J. (1901) Investigations of the Aquatic Resources and Fisheries of Porto Rico by the United States Fish Commission Steamer Fish Hawk in 1899. The Brachyura and Macrura of Porto Rico. Bulletin of the United States Fish Commission, 20, 1–127.
Reiss, H., Birchenough, S., Borja, A., Buhl-Mortensen, L., Craeymeersch, J., Dannheim, J., Darr, A., Galparsoro, I., Gogina, M., Neumann, H., Populus, J., Rengstorf, A.M., Valle, M., van Hoey, G., Zettler, M.L. & Degraer, S. (2014) Benthos distribution modelling and its relevance for marine ecosystem management. ICES Journal of Marine Science, 72 (2), 297–315.
https://doi.org/10.1093/icesjms/fsu107Rhyne, A.L. & 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.
Rhyne, A.L. & Anker, A. (2007) Lysmata rafa, a new species of peppermint shrimp (Crustacea, Caridea, Hippolytidae) from the subtropical western Atlantic. Helgoland Marine Research, 61, 291–296.
https://doi.org/10.1007/s10152-007-0077-4Risso, A. (1816) Histoire naturelle des crustacés des environs de Nice. Librairie Grecque-Latine-Allemande, Paris, 175 pp., 3 pls.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.
https://doi.org/10.1093/sysbio/sys029Schmitt, W.L. (1924) The Macrura and Anomura collected by the Williams Galapagos Expedition, 1923. Zoologica, 4, 161–171.
Schubart, C., Neigel, J. & Felder, D. (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. In: Von Vaupel Klein, J.C. & Schram, F.R. (Eds.), The Biodiversity Crisis and Crustacea. Crustacean Issues. Vol. 12. A.A. Balkema, Rotterdam, pp. 817–830.
Schwindt, E., López Gappa, J., Raffo, M.P., Tatián, M., Bortolus, A., Orensanz, J.M., Alonso, G., Diez, M.E., Doti, B., Genzano, G., Lagger, C., Lovrich, G., Piriz, M.L., Mendez, M.M., Savoya, V. & Sueiro, M.C. (2014) Marine fouling invasions in ports of Patagonia (Argentina) with implications for legislation and monitoring programs. Marine Environmental Research, 99, 60–68.
https://doi.org/10.1016/j.marenvres.2014.06.006Soledade, G.O., Baeza, J.A., Boehs, G., Simões, S.M., Santos, P.S., Da Costa, R.C. & 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.
https://doi.org/10.1163/1937240X-00002122Spence Bate, C. (1888) Report on the Crustacea Macrura collected by the Challenger during the years 1873-76. Report on the Scientific Results of the Voyage of H.M.S. “ “Challenger” during the years 1873–76, 24, i–xc + 1–942.
Stebbing, 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.
Stebbing, T.R.R. (1921) Some Crustacea from Natal. Annals of the Durban Museum, 3, 12–26.
Stimpson, W. (1860) Prodromus descriptionis animalium 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.
Stimpson, W. (1866) Descriptions of new genera and species of Macrurous Crustacea from the Coasts of North America. Proceedings of the Chicago Academy of Sciences, 1, 46–48.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.
https://doi.org/10.1093/molbev/msr121Tavares, M. (2011) Alien Decapod Crustaceans in the Southwestern Atlantic Ocean. In: Galil, B.S. (Ed), In the Wrong Place—Alien Marine Crustaceans: Distribution, Biology and Impacts. Invading Nature, Springer Series in Invasion Ecology, 6, pp. 251–268.
https://doi.org/10.1007/978-94-007-0591-3_7Terossi, M., Almeida, A.O., Buranelli, R.C., Castilho, A.L., Costa, R.C., Zara, F.J. & 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 (1), 76–94.
https://doi.org/10.11646/zootaxa.4370.1.6Thallwitz, J. (1892) Decapoden-Studien, insbesondere 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 Museums zu Dresden, 3, 1–56. [for 1890/91]
Wicksten, M.K. (2000a) The species of Lysmata (Caridea: Hippolytidae) from the Eastern Pacific Ocean. Amphipacifica, 2, 3–22.
Wicksten, M.K. (2000b) A new species of Lysmata (Caridea, Hippolytidae) from the Eastern Pacific. Crustaceana, 73, 207–213.
https://doi.org/10.1163/156854000504273