Abstract
Considering the importance of establishing different approaches to the early detection of invasive species, the present study aimed to describe and illustrate the morphology of the early larval stages of the shrimp Lysmata lipkei, an invasive species in the Western Atlantic. Additionally, we did a morphological comparison and a review of the other Lysmata species from the Western Atlantic Ocean with a known larvae description. The larvae used in this study were obtained by the maintenance, under laboratory conditions, of ovigerous hermaphrodites of L. lipkei, collected in the wild. Then, larvae were dissected under a stereo microscope and illustrated using a microscope equipped with a camera lucida. The first three larval stages (zoeae) of L. lipkei were illustrated, described, and compared to other species of Lysmata previously described of the Western Atlantic. Some features of the larval morphology of L. lipkei are very similar when compared to other Lysmata species with previous larval descriptions, such as a rostrum long and simple, the eyes stalked with a long peduncle from the second zoeae, one pterygostomian spine and several denticles along the anterior ventral margin of the carapace, similarities in the segmentation of the maxillipeds, and the presence of dorsolateral spines on the posterior margin of the 5th pleomere, among other features. Also, unique features were observed for L. lipkei, such as differences in the setation of some structures, including the antennule, antenna, maxillule, and maxillipeds. Using the morphological descriptions, we expect to identify species from the plankton, especially invaders, that might be present in the Western Atlantic, as well as assist in several areas in which the larval morphology is relevant.
References
Ahyong, S.T. (2010) New species and new records of Caridea (Hippolytidae: Pasiphaeidae) from New Zealand. Zootaxa, 2372 (1), 341–357.
https://doi.org/10.11646/zootaxa.2372.1.26
Almeida, A.O., Simões, S.M., Costa, R.C. & 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.
https://doi.org/10.1007/s10152-012-0291-6
Alves, D.F.R., Lima, D.J.M., Hirose, G.L., Martines, P.A., Dolabella, S.S. & Barros-Alves, S.P. (2018) Morphological and molecular analyses confirm the occurrence of two sympatric Lysmata shrimp (Crustacea, Decapoda) in the southwestern Atlantic. Zootaxa, 4526 (1), 41–55.
https://doi.org/10.11646/zootaxa.4526.1.3
Alves, D.F.R., López-Greco, L.S., Barros-Alves, S.P. & Hirose, G.L. (2019) Sexual system, reproductive cycle and embryonic development of the red-stripped shrimp Lysmata vittata, an invader in the western Atlantic Ocean. PLoS ONE, 14, e0210723.
https://doi.org/10.1371/journal.pone.0210723
Anger, K. (2006) Contributions of larval biology to crustacean research: a review. Invertebrate Reproduction and Development, 49 (3), 175–205.
https://doi.org/10.1080/07924259.2006.9652207
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 (5), 682–692.
Baeza, J.A., Bolaños, J.A., Hernandez, J.E. & López, R. (2009) A new species of Lysmata (Crustacea, Decapoda, Hippolytidae) from Venezuela, southeastern Caribbean Sea. Zootaxa, 2240 (1), 60–68.
https://doi.org/10.11646/zootaxa.2240.1.4
Baeza, J.A., Guéron, R., Simpson, L. & Ambrosio, L.J. (2016) Population distribution, host-switching and chemical sensing in the symbiotic shrimp Lysmata pederseni: implications for its mating system in a changing reef seascape. Coral reefs, 35, 1213–1224.
https://doi.org/10.1007/s00338-016-1467-3
Barros-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, 34.
https://doi.org/10.1186/s41200-016-0037-2
Barros-Alves, S.P., Alves, D.F.R., Antunes, M., López-Greco, L.S. & Negreiros-Fransozo, M.L. (2018) Nutritional vulnerability in zoeal stages of the yellowline arrow crab Stenorhynchus seticornis (Brachyura: Majoidea). Marine and Freshwater Research, 69 (6), 962–970.
https://doi.org/10.1071/MF17145
Bartilotti, C., Calado, R., Rhyne, A. & dos Santos, A. (2012) Shedding light on the larval genus Eretmocaris: morphological larval features of two closely related trans-isthmian Lysmata species (Decapoda: Crustacea: Hippolytidae) described on the basis of laboratory cultured material. Helgoland Marine Research, 66, 97–115.
https://doi.org/10.1007/s10152-011-0251-6
Bauer, R.T. & Newman, W.A. (2004) Protandric simultaneous hermaphroditism in the marine shrimp Lysmata californica (Caridea: Hippolytidae). Journal of Crustacean Biology, 24, 131–139.
https://doi.org/10.1651/C-2426
Bohn, T., Amundsen, P. & Sparrow, A. (2008) Competitive exclusion after invasion? Biological Invasions, 10, 359–368.
https://doi.org/10.1007/s10530-007-9135-8
Calado, R. (2008) Marine ornamental shrimp: Biology, aquaculture and conservation. Blackwell Publishing, Oxford, 280 pp.
Calado, R., Bartilotti, C., Narciso, L. & dos Santos, A. (2004) Redescription of the larval stages of Lysmata seticaudata (Risso, 1816) (Crustacea, Decapoda, Hippolytidae) reared under laboratory conditions. Journal of Plankton Research, 26 (7), 737–752.
https://doi.org/10.1093/plankt/fbh072
Calado, R., Figueiredo, J., Rosa, R., Nunes, M.L. & Narciso, L. (2005) Effects of temperature, density, and diet on development, survival, settlement synchronism, and fatty acid profile of the ornamental shrimp Lysmata seticaudata. Aquaculture, 245, 221–237.
doi:10.1016/J.AQUA CULTURE.2004.11.034
Candolin, U., Bertell, E. & Kallio, J. (2018) Environmental disturbances alters the ecological impact of an invading shrimp. Functional Ecology, 32 (5), 1370–1378.
https://doi.org/10.1016/j.aquaculture.2004.11.034
Chace, F.A. Jr. (1972) The Shrimps of the Smithsonian—Bredin Caribbean Expeditions with a Summary of the West Indian Shallow-Water Species. Smithsonian Contributions to Zoology 98. Smithsonian Institution Press, Washington, D.C., x + 179 pp.
https://doi.org/10.1111/1365-2435.13078
Clark, P.F., Calazans, D.K. & Pohle, G.W. (1998) Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction and Development, 33 (2–3), 127–144.
https://doi.org/10.1080/07924259.1998.9652627
Darling, J.A. & Blum, M.J. (2007) DNA-based methods for monitoring invasive species: a review and prospectus. Biological Invasions, 9, 751–765.
https://doi.org/10.1007/s10530-006-9079-4
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.4429.2.13
De Grave, S. & Fransen, C.H.J.M. (2011) Carideorum Catalogus: The recent species of the Dendrocranchiate, Stenopodidean, Procarididean and Caridean shrimps (Crustacea: Decapoda). Zoologische Mededelingen, 85, 195–589.
Dittel, A.I., Hines, A.H., Ruiz, G.M. & Ruffin, K.K.E. (1995) Effects of shallow water refuge on behavior and density-dependent mortality of juvenile blue crabs in Chesapeake Bay. Bulletin of Marine Science, 57, 902–916.
Fiedler, 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 system and systematics. BMC Evolutionary Biology, 10, e297.
https://doi.org/10.1186/1471-2148-10-297
Garm, A. (2004) Mechanical functions of setae from the mouth apparatus of seven species of decapod crustaceans. Journal of Morphology, 260, 85–100.
https://doi.org/10.1002/jmor.10213
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.5561
González-Ortegón, E., García-Raso, J.E., Calado, R., Lópes de la Rosa, I., Guerrero, M. & Cuesta, J.A. (2020) Atlantic expansion of the African caridean shrimp Lysmata uncicornis Holthuis & Maurin, 1952 (Caridea: Lysmatidae). Marine Biodiversity, 50, 26.
https://doi.org/10.1007/s12526-020-01056-w
Gregati, R.A., Fransozo, V., López-Greco, L.S. & Negreiros-Fransozo, M.L. (2010) Reproductive cycle and ovarian development of the marine ornamental shrimp Stenopus hispidus in captivity. Aquaculture, 306, 185–190.
https://doi.org/10.1016/j.aquaculture.2010.05.009
Guerao, G. & Cuesta, J.A. (2014) Caridea. In: Martin, J.W., Olesen, J. & Hoeg, J.T. Atlas of crustacean larvae. Johns Hopkins University press, Baltimore, Maryland, pp. 250–255.
Gurjão, L.M. & Lotufo, T.M. (2018) Native species exploited by marine aquarium trade in Brazil. Biota Neotropica, 18 (3), e20170387.
https://doi.org/10.1590/1676-0611-bn-2017-0387
Knowlton, R.E. & Alavi, M.R. (1995) The larval morphology of Lysmata anchisteus Chace (Crustacea: Decapoda) compared with other Lysmata spp. Caribbean Journal of Science, 31, 289–310.
Kurata, H. (1970) Studies on the life histories of decapod Crustacea of Georgia. The University of Georgia, Marine Institute, Athens, Georgia, 192 pp. [unpublished report]
Landeira, J.M., Lozano-Soldevilla, F. & González-Gordillo, J.I. (2009) Morphology of first seven larval stages of the striped soldier shrimp, Plesionika edwardsii (Brandt, 1851) (Crustacea: Decapoda: Pandalidae) from laboratory reared material. Zootaxa, 1986 (1), 51–66.
https://doi.org/10.11646/zootaxa.1986.1.2
Marin, I.N., Korn, O.M. & 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 (4), 359–363.
https://doi.org/10.1134/S1063074012040062
Marques, F.P.L., Pohle, G.W. & Vrbova, L. (2003) On the larval stages of Macrocoeloma diplacanthum (Decapoda: Brachyura: Majidae), and a review of mithracine phylogenetic aspects. Journal of Crustacean Biology, 23, 187–200.
https://doi.org/10.1163/20021975-99990326
Okuno, J. & Fiedler, G.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.
https://doi.org/10.1163/9789047427759_042
Pachelle, P.P.G., Anker, A., Mendes, C.B. & Bezerra, L.E.A. (2016) Decapod crustaceans from the state of Ceará, northeastern Brazil: an update checklist of marine and estuarine species, with 23 new records. Zootaxa, 4131 (1), 1–63.
https://doi.org/10.11646/zootaxa.4131.1.1
Pachelle, P.P.G, Carvalho, L., Alves, D.F.R. & 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 (1), 55–90.
https://doi.org/10.11646/zootaxa.4789.1.2
Pantaleão, J.A.F., Gregati, R.A., Costa, R.C., Lópes-Greco, L. & Negreiros-Fransozo, M.L. (2017) Post-hatching development of the ornamental “Red Cherry Shrimp” Neocaridina davidi (Bouvier, 1904) (Crustacea, Caridea, Atyidae) under laboratory conditions. Aquaculture Research, 48, 553–569.
https://doi.org/10.1111/are.12903
Pohle, G., Mantelatto, F.L.M., Negreiros-Fransozo, M.L. & Fransozo, A. (1999) Larval Decapoda (Brachyura). In: Boltovskoy, D. (Ed.), South Atlantic Zooplankton. Backhuys Publisher, Leiden, pp. 869–1706.
Prakash, S. & Baeza, J.A. (2017) A new species of Lysmata Risso, 1816 (Crustacea, Decapoda, Lysmatidae) from the Gulf of Mexico. Zootaxa, 4363 (4), 576–582.
https://doi.org/10.11646/zootaxa.4363.4.10
Rhyne, 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 Sciences, 79, 165–204.
Rhyne, A.L., Tlusty, M.F., Szczebak, J.T. & Holmberg, R.J. (2017) Expanding our understanding of the trade in marine aquarium animals. PeerJ, 5, e2949.
https://doi.org/10.7717/peerj.2949
Soledade, G., Baeza, J.A., Boehs, G., Simões, S.M., Santos, P.S., Costa, R.C. & Almeida, A.O. (2013) 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-00002122
Tavares, 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. Springer Series in Invasion Ecology, 6, pp. 251–268.
https://doi.org/10.1007/978-94-007-0591-3_7
Vaughan, D.B., Grutter, A.S., Ferguson, H.W., Jones, R. & Hutson, K.S. (2018a) Cleaner shrimp are true cleaners of injured fish. Marine Biology, 165, 118.
https://doi.org/10.1007/s00227-018-3379-y
Vaughan, D.B., Grutter, A.S. & Hutson, K.S. (2018b) Cleaner shrimp remove parasite eggs on fish cages. Aquaculture Environment Interactions, 10, 429–436.
https://doi.org/10.3354/aei00280
Wang, Y. & Sha, Z. (2018) Descriptions of two new species of Lysmata Risso, 1816 (Decapoda, Lysmatidae) from the China seas, with remarks on Lysmata vittata (Stimpson, 1860). Zootaxa, 4392 (1), 28–40.
https://doi.org/10.11646/zootaxa.4392.1.2
Wehrtmann, I.S. (1990) Distribution and reproduction of Ambidexter panamense and Palaemonetes schimitti in Pacific Costa Rica (Crustacea, Decapoda). Revista de Biologia Tropical, 38 (2A), 327–329.
Wirtz, P. (1997) Crustacean symbionts of the sea anemone Telmatactis cricoides at Madeira and the Canary Islands. The Zoological Society of London, 242, 799–811.
https://doi.org/10.1111/j.1469-7998.1997.tb05827.x
Wunsch, M. (1996) Larval development of Lysmata amboinensis (De Man, 1888) (Decapoda: Hippolytidae) reared in laboratory with a note on L. debelius (Bruce, 1983). Master’s dissertation, University of Wales, Cardiff, Wales, 10 pp.
Yang, H.J. & Kim, C.H. (2010) Zoeal stages of Lysmata vittata (Decapoda: Caridea: Hippolytidae) reared in the laboratory. Korean Journal of Systematic Zoology, 26 (3), 261–278.
https://doi.org/10.5635/KJSZ.2010.26.3.261