Abstract
Of the 12 species of Thor described until present date, only three (25%) have their complete larval development known. Present work describes the complete larval development of Thor amboinensis, based on laboratory-reared material. The spent females were identified through the analysis of the partial sequences of the mitochondrial DNA barcode, also used for the reconstruction of the phylogenetic relationships within the recently resurrected and recognized family Thoridae Kingsley, 1879. Eight zoeal stages and one decapodid complete this species larval development. In the genus Thor, the number of zoeal stages varies greatly from two (T. dobkini) to eight (T. amboinensis and T. floridanus). The larvae of T. ambionensis and T. floridanus are readily distinguished from each other by the ornamentation of the ventral margin of the carapace and the pereiopods development. The first zoeal stage of T. amboinensis described by Yang & Okuno (2004) and the one described in present study are very similar. A brief discussion on the morphological characters and on the number of zoeal stages of the genus, as well as of the previous larval descriptions is made. The phylogenetic analysis suggest cryptic speciation for geographical separated populations of T. amboinensis, paraphyly of the genus Eualus, and the reassignment of E. cranchii to a different genus.
References
Anger, K. (2001) The biology of decapod crustacean larvae. Crustacean Issues, Volume 14, A.A. Balkema Publishers, Rotterdam, 420 pp.
Araújo, R. & Calado, R. (2003) Crustáceos decápodes do arquipélago da Madeira. Direcção Regional do Ambiente: Grafimadeira, S.A., Madeira, 236 pp.
Aznar-Cormano, L., Brisset, J., Chan, T.-Y., Corbari, L., Puillandre, N., Utge, J., Zbinden, M., Zuccon, D. & Samadi, S. (2015) An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods. Genetica, 143, 195–205.
http://dx.doi.org/10.1007/s10709-014-9807-0Baeza, J.A. & Piantoni, C. (2010) Sexual system, sex ratio, and group living in the shrimp Thor amboinensis (De Man): relevance to resource-monopolization and sex-allocation theories. The Biological Bulletin, 219, 151–165.
Bracken, H., De Grave, S., Felder, D. (2009) Phylogeny of the Infraorder Caridea based on mitochondrial and Nuclear Genes (Crustacea: Decapoda). In: Martin, J.W., Crandall, K.A. & Felder, D.L. (Eds.), Decapod Crustacean Phylogenetics. Crustacean Issues, 18, pp. 281–305.
http://dx.doi.org/10.1201/9781420092592-c14Broad, A.C. (1957) Larval development of the crustacean Thor floridanus Kingsley. Journal of the Mitchell Society, 73, 317–328.
Calado, R., Vitorino, A., Dionisio, G. & Dinis, M.T. (2006) A recirculation maturation system for marine ornamental decapods. Aquaculture, 263, 68–74.
http://dx.doi.org/10.1016/j.aquaculture.2006.10.013Calado, R., Lin, J., Rhyne, A.L., Araújo, R. & Narciso, L. (2003a) Marine ornamental decapods- popular, pricey, and poorly studied. Journal of Crustacean Biology, 23, 963–973.
http://dx.doi.org/10.1651/C-2409Calado, R., Narciso, L., Morais, S., Rhyne, A.L. & Lin, J. (2003b) A rearing system for the culture of ornamental decapod crustacean larvae. Aquaculture, 218, 329–339.
http://dx.doi.org/10.1016/S0044-8486(02)00583-5Chace, F.A. Jr. (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.
http://dx.doi.org/10.5479/si.00810282.98Clark, P.F., Calazans, D.K. & Pohle, G.W. (1998) Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction and Development, 33, 127–144.
http://dx.doi.org/10.1080/07924259.1998.9652627Costa, F.O., deWaard, J.R., Boutillier, J., Ratnasingham, S., Dooh, R., Hajibabaei, M. & Hebert, P.D.N. (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Science, 64, 272–295.
http://dx.doi.org/10.1139/f07-008De 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, 195–588.
De Grave, S., Li, C.P., Tsang, L.M., Chu, K.H. & Chan, T.-Y. (2014) Unweaving hippolytoid systematics (Crustacea, Decapoda, Hippolytidae): resurrection of several families. Zoologica Scripta, 43, 496–507.
http://dx.doi.org/10.1111/zsc.12067Debelius, H. (2001) Crustacea guide of the world. IKAN—Unterwasserarchive, Frankfurt, 318 pp.
Dobkin, S. (1968) The larval development of a species of Thor (Caridea, Hippolytidae) from South Florida, USA. Crustaceana, 2 (Supplement), 1–18.
Edgar, R.C. (2004a) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.
http://dx.doi.org/10.1093/nar/gkh340Edgar, R.C. (2004b) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics, 5, 113.
http://dx.doi.org/10.1186/1471-2105-5-113Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791.
http://dx.doi.org/10.2307/2408678Garm, A. (2004) Revising the definition of the crustacean seta and setal classification systems based on examinations of the mouthpart setae of seven species of decapods. Zoological Journal of the Linnean Society, 142, 233–252.
http://dx.doi.org/10.1111/j.1096-3642.2004.00132.xGiménez, L. (2006) Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans. Integrative and Comparative Biology, 46, 615–622.
http://dx.doi.org/10.1093/icb/icl010Gore, R.H. (1985) Molting and growth in decapod larvae. In: Wenner, A.M. (Ed.), Crustacean Issues, 2, pp. 1–65.
Guo, C.C., Hwang, J.S. & Fautin, D.G. (1996) Host selection by shrimps with sea anemones: A field survey and experimental laboratory analysis. Journal of Experimental Marine Biology and Ecology, 202, 165–176.
http://dx.doi.org/10.1016/0022-0981(96)00020-2Gurney, R. (1937) Larvae of decapod crustacea. Part IV. Hippolytidae. Discovery Reports, 14, 351–404.
Hall G.H. (2013) Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution, 30, 1229–1235.
http://dx.doi.org/10.1093/molbev/mst012Haynes, E.B. (1985) Morphological development, identification, and biology of larvae of Pandalidae, Hippolytidae, and Crangonidae (Crustacea, Decapoda) of the northern North Pacific Ocean. Fishery Bulletin, 83, 253–288.
Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B-Biological Sciences, 270, 313–321.
http://dx.doi.org/10.1098/rspb.2002.2218Lebour, M.V. (1940) The larvae of the British species of Spirontocaris and their relation to Thor (Crustacea, Decapoda). Journal of the Marine Biological Association of the United Kingdom, 24, 505–514.
http://dx.doi.org/10.1017/S0025315400045410Lefébure, T., Douady, C.J., Gouy, M. & Gibert, J. (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: Proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution, 40, 435–447.
http://dx.doi.org/10.1016/j.ympev.2006.03.014Lobo, J., Costa, P.M., Teixeira, M.A.L., Ferreira, M.S.G., Costa, M.H. & Costa, F.O. (2013) Enhanced primers for amplification of DNA barcodes from a broad range of marine metazoans. BMC Ecology, 13, 34.
http://dx.doi.org/10.1186/1472-6785-13-34Marco-Herrero, E., González-Gordillo, J.I. & Cuesta, J.A. (2015) Larval morphology of the family Parthenopidae, with the description of the megalopa stage of Derilambrus angulifrons (Latreille, 1825) (Decapoda: Brachyura), identified by DNA barcode. Journal of the Marine Biological Association of the United Kingdom, 95, 513–521.
http://dx.doi.org/10.1017/S0025315414001908Meyer, R., Weis, A. & Melzer, R.R. (2013) Decapoda of southern Chile: DNA barcoding and integrative taxonomy with focus on the genera Acanthocyclus and Eurypodius. Systematics and Biodiversity, 11, 389–404.
http://dx.doi.org/10.1080/14772000.2013.833143Nye, V., Copley, J.T. & Linse, K. (2013) A new species of Eualus Thallwitz, 1892 and new record of Lebbeus antarcticus (Hale, 1941) (Crustacea: Decapoda: Caridea: Hippolytidae) from the Scotia Sea. Deep-Sea Research II, 92, 145–156.
http://dx.doi.org/10.1016/j.dsr2.2013.01.022Pike, R.B. & Williamson, D.I. (1961) The larvae of Spirontocaris and related genera (Decapoda, Hippolytidae). Crustaceana, 2, 187–208.
http://dx.doi.org/10.1163/156854061X00167Plaisance, L., Knowlton, N., Paulay, G. & Meyer, C. (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs, 28, 977–986.
http://dx.doi.org/10.1007/s00338-009-0543-3Plouviez, S., Jacobson, A., Wu, M. & Van Dover, C.L. (2015) Characterization of vent fauna at the Mid-Cayman Spreading Center. Deep-Sea Research I, 97, 124–133.
http://dx.doi.org/10.1016/j.dsr.2014.11.011Puillandre, N., Macpherson, E., Lambourdière, J., Cruaud, C., Boisselier-Dubayle, M.-C. & Samadi, S. (2011) Barcoding type specimens helps to identify synonyms and an unnamed new species in Eumunida Smith, 1883 (Decapoda : Eumunididae). Invertebrate Systematics, 25, 322–333.
http://dx.doi.org/10.1071/IS11022Radulovici, A.E., Sainte-Marie, B. & Dufresne, F. (2009) DNA barcoding of marine crustaceans from the Estuary and Gulf of St Lawrence: a regional-scale approach. Molecular Ecology Resources, 9 (Supplement), 181–187.
http://dx.doi.org/10.1111/j.1755-0998.2009.02643.xRhyne, A.L. & Lin, J. (2004) Effects of different diets on larval development in a peppermint shrimp (Lysmata sp. (Risso)). Aquaculture Research, 35, 1179–1185.
http://dx.doi.org/10.1111/j.1365-2109.2004.01143.xSarver, D. (1979) Larval culture of the shrimp Thor amboinensis (De Man, 1888) with reference to its symbiosis with the anemone Antheopsis papillosa (Kwietniwski, 1898). Crustaceana, 5 (Supplement), 176–178.
Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences, 105, 13486–13491.
http://dx.doi.org/10.1073/pnas.0803076105Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.
http://dx.doi.org/10.1093/molbev/mst197Terossi, M., Cuesta, J.A., Wehrtmann, I.S. & Mantelatto, F. (2010) Revision of the larval morphology (Zoea I) of the family Hippolytidae (Decapoda, Caridea), with a description of the first stage of the shrimp Hippolyte obliquimanus Dana, 1852. Zootaxa, 2624, 49–66.
Thatje, S., Schnack-Schiel, S. & Arntz, W.E. (2003) Developmental trade-offs in Subantarctic
meroplankton communities and the enigma of low decapod diversity in high southern latitudes. Marine Ecology Progress Series, 260, 195–207.
http://dx.doi.org/10.3354/meps260195Verrill, A.E. (1922) Decapod Crustacea of Bermuda. Part II, Macrura. Transactions of the Connecticut Academy of Arts and Sciences, 26, 1–179.
Wehrtmann, I.S. & Albornoz, L. (2003) Larvae of Nauticaris magellanica (Decapoda: Caridea: Hippolytidae) reared in the laboratory differ morphologically from those in nature. Journal of the Marine Biological Association of the United Kingdom, 83, 949–957.
http://dx.doi.org/10.1017/S0025315403008130hWirtz, P. (1997) Crustacean symbionts of the sea anemone Telmatactis cricoids at Madeira and the Canary Islands. Journal of Zoology, 242, 799–811.
http://dx.doi.org/10.1111/j.1469-7998.1997.tb05827.xYang, H.J. & Okuno, J. (2004) First larvae of Lebbeus comanthi and Thor amboinensis (Decapoda: Hippolytidae) in the laboratory. Korean Journal of Biological Sciences, 8, 19–25.
http://dx.doi.org/10.1080/12265071.2004.9647729