Hostname: page-component-84b7d79bbc-lrf7s Total loading time: 0 Render date: 2024-07-28T05:33:07.443Z Has data issue: false hasContentIssue false

The complete description of larval stages of the lobster shrimp Leonardsaxius amurensis (Kobjakova, 1937) (Decapoda: Axiidea: Axiidae) identified by DNA barcoding

Published online by Cambridge University Press:  02 May 2017

Elena S. Kornienko*
Affiliation:
A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia
Darya D. Golubinskaya
Affiliation:
A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia
Olga M. Korn
Affiliation:
A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia
Svetlana N. Sharina
Affiliation:
A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia Far Eastern Federal University, Vladivostok 690091, Russia
*
Correspondence should be addressed to: E.S. Kornienko, A.V. Zhirmunsky Institute of Marine Biology, National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok 690041, Russia email: kornielena@mail.ru

Abstract

The complete larval development of the lobster shrimp Leonardsaxius amurensis (Kobjakova, 1937) (Decapoda: Axiidea: Axiidae) is described and illustrated for the first time. The first zoeae of this species were collected from the plankton samples and reared in the laboratory before moulting to the megalopa. A molecular genetic analysis based on comparison of partial mitochondrial COI, 12S rDNA and 16S rDNA sequence data confirmed the identity of axiid larvae found in the plankton and L. amurensis adults collected in the same area. The larval development of L. amurensis includes five zoeal stages and a single megalopa. Zoeae I of L. amurensis are characterized by the presence of one short posterodorsal spine on the fifth pleonite in contrast to the larvae of related sympatric species Boasaxius princeps having four posterodorsal spines on the pleonites 2–5. Leonardsaxius amurensis occupies an intermediate position between lobster shrimps with abbreviated pelagic development (2–3 zoeal stages) and species with long development (up to eight zoeal stages). Thus, the number of zoeal stages in the family Axiidae varies widely, similarly to that in the families Callianassidae and Upogebiidae.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ahyong, S.T., Lai, J.C.Y., Sharkey, D., Colgan, D.J. and Ng, P.K.L. (2007) Phylogenetics of the brachyuran crabs (Crustacea: Decapoda): the status of Podotremata based on small subunit nuclear ribosomal RNA. Molecular Phylogenetics and Evolution 45, 576586. http://dx.doi.org/10.1016/j.ympev.2007.03.022.Google Scholar
Ahyong, S.T., Lowry, J.K., Alonso, M., Bamber, R.N., Boxshall, G.A., Castro, P., Gerken, S., Karaman, G.S., Goy, J.W., Jones, D.S., Meland, K., Rogers, D.C. and Svavarsson, J. (2011) Subphylum Crustacea Brünnich, 1772. In Zhang, Z.-Q. (ed.) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness. Auckland: Magnolia Press, pp. 165191.Google Scholar
Alasaad, S., Rossi, L., Maione, S., Sartore, S., Soriguer, R.C., Pèrez, J.M., Rasero, R., Zhu, X.Q. and Soglia, D. (2008) HotSHOT Plus ThermalSHOCK, a new and efficient technique for preparation of PCR-quality mite genomic DNA. Parasitology Research 103, 14551457. http://dx.doi.org/10.1007/s00436-008-1127-9.Google Scholar
Ampuero, D., Palma, A.T., Veliz, D. and Pardo, L.M. (2010) Description, seasonal morphological variation, and molecular identification of Paraxanthus barbiger megalopae obtained from the natural environment. Helgoland Marine Research 64, 117123. http://dx.doi.org/10.1007/s10152-009-0172-9.Google Scholar
Barber, P. and Boyce, S.L. (2006) Estimating diversity of Indo-Pacific coral reef stomatopods through DNA barcoding of stomatopod larvae. Proceedings of the Royal Society of London B: Biological Sciences 273, 20532061. http://dx.doi.org/10.1098/rspb.2006.3540.Google Scholar
Barnich, R. (1996) The larvae of the Crustacea Decapoda (excl. Brachyura) in the plankton of the French Mediterranean coast (Identification keys and systematic review). Göttingen: Cuvillier.Google Scholar
Bracken, H.D., De Grave, S., Toon, A., Felder, D.L. and Crandall, K.A. (2010) Phylogenetic position, systematic status, and divergence time of the Procarididea (Crustacea: Decapoda). Zoologica Scripta 39, 198212. http://dx.doi.org/10.1111/j.1463-6409.2009.00410.x.Google Scholar
Bracken-Grissom, H.D., Felder, D.L., Vollmer, N.L., Martin, J.W. and Crandall, K.A. (2012) Phylogenetics links monster larva to deep-sea shrimp. Ecology and Evolution 2, 23672373. http://doi.org/10.1002/ece3.347.Google Scholar
Brandão, M.C., Freire, A.S. and Burton, R.S. (2016) Estimating diversity of crabs (Decapoda: Brachyura) in a no-take marine protected area of the SW Atlantic coast through DNA barcoding of larvae. Systematics and Biodiversity 14, 288302. http://dx.doi.org/10.1080/14772000.2016.1140245.Google Scholar
Chen, H.-N., Tsang, L.M., Chong, V.C. and Chan, B.K.K. (2014) Worldwide genetic differentiation in the common fouling barnacle, Amphibalanus amphitrite. Biofouling 30, 10671078. http://dx.doi.org/10.1080/08927014.2014.967232.Google Scholar
Chen, J., Li, Q., Kong, L. and Yu, H. (2011) How DNA barcodes complement taxonomy and explore species diversity: the case study of a poorly understood marine fauna. PLoS ONE 6, e21326. http://doi.org/10.1371/journal.pone.0021326.Google Scholar
Clark, P.F., Calazans, D.K. and Pohle, G.W. (1998) Accuracy and standardization of brachyuran larval descriptions. Invertebrate Reproduction and Development 33, 127144.Google Scholar
Cook, C.E., Austin, J.J. and Disney, R.H.L. (2004) A mitochondrial 12S and 16S rRNA phylogeny of critical genera of Phoridae (Diptera) and related families of Aschiza. Zootaxa 593, 111.Google Scholar
Costa, F.O., deWaard, J.R., Boutillier, J., Ratnasingham, S., Dooh, R.T., Hajibabaei, M. and Hebert, P.D.N. (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272295. http://dx.doi.org/10.1139/F07-008.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772. http://dx.doi.org/10.1038/nmeth.2109.Google Scholar
De Grave, S., Chan, T.-Y., Chu, K.H., Yang, C.-H. and Landeira, J.M. (2015) Phylogenetics reveals the crustacean order Amphionidacea to be larval shrimps (Decapoda: Caridea). Scientific Reports 5, 17464. http://dx.doi.org/10.1038/srep17464.Google Scholar
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797. http://dx.doi.org/10.1093/nar/gkh340.Google Scholar
Elofsson, R. (1959) A new decapod larva referred to Calocarides coronatus (Trybom). Publications from the Biological Station, Espegrend 7, 110.Google Scholar
Felder, D.L. and Robles, R. (2009) Molecular phylogeny of the family Callianassidae based on preliminary analyses of two mitochondrial genes. In Martin, J.W., Crandall, K.A. and Felder, D.L. (eds) Decapod crustacean phylogenetics. Boca Raton, FL: CRC Press, pp. 327342.Google Scholar
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Guerao, G., Hernández, E. and Urzúa, Á. (2011) Early zoeal development of the shrimp Hippolyte leptocerus (Decapoda, Caridea, Hippolytidae). Zootaxa 2988, 5365.Google Scholar
Gurney, R. (1942) Larvae of decapod Crustacea. London: Ray Society.Google Scholar
Haynes, 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, 253288.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. and deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270, 313321. http://dx.doi.org/10.1098/rspb.2002.2218.Google Scholar
Huelsenbeck, J.P. and Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.Google Scholar
Kappner, I. and Bieler, R. (2006) Phylogeny of venus clams (Bivalvia: Venerinae) as inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 40, 317331. http://dx.doi.org/10.1016/j.ympev.2006.02.006.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120. http://dx.doi.org/10.1007/BF01731581.Google Scholar
Knight, M. and Omori, M. (1982) The larval development of Sergestes similis Hansen (Crustacea, Decapoda, Sergestidae) reared in the laboratory. Fishery Bulletin 80, 217243.Google Scholar
Knowlton, N. and Weigt, L.A. (1998) New dates and new rates for divergence across the Isthmus of Panama. Proceedings of the Royal Society of London B: Biological Sciences 265, 22572263.Google Scholar
Konishi, K., Quintana, R.R. and Fukuda, Y. (1990) A complete description of larval stages of the ghost shrimp Callianassa petalura Stimpson (Crustacea: Thalassinidea: Callianassidae) under laboratory conditions. Bulletin of the National Research Institute of Aquaculture, Nansei, Japan 17, 2749.Google Scholar
Kornienko, E.S. and Korn, O.M. (2010) Illustrated key for the identification of brachyuran larvae in the northwestern Sea of Japan. Vladivostok: Dalnauka.Google Scholar
Kornienko, E.S. and Korn, O.M. (2012) First stage larva of the lobster shrimp Allaxius princeps (Boas, 1880) (Decapoda: Axiidea: Axiidae) obtained in the laboratory. Zootaxa 3527, 8387.Google Scholar
Kornienko, E.S., Korn, O.M. and Golubinskaya, D.D. (2014) The complete larval development of the lobster shrimp Boasaxius princeps Boas, 1880 (Decapoda: Axiidea: Axiidae) obtained in the laboratory. Journal of Natural History 48, 17371769. http://dx.doi.org/10.1080/00222933.2014.897765.Google Scholar
Kornienko, E.S., Korn, O.M. and Golubinskaya, D.D. (2015) The number of zoeal stages in larval development of Nihonotrypaea petalura (Stimpson, 1860) (Decapoda: Axiidea: Callianassidae) from Russian waters of the Sea of Japan. Zootaxa 3919, 343361. http://dx.doi.org/10.11646/zootaxa.3919.2.7.Google Scholar
Koufopanou, V., Reid, D.G., Ridgway, S.A. and Thomas, R.H. (1999) A molecular phylogeny of the patellid limpets (Gastropoda: Patellidae) and its implications for the origins of their antitropical distribution. Molecular Phylogenetics and Evolution 11, 138156. http://dx.doi.org/10.1006/mpev.1998.0557.Google Scholar
Kurata, H. (1965) Larvae of decapod Crustacea of Hokkaido. 9. Axiidae, Callianassidae and Upogebiidae (Anomura). Bulletin of Hokkaido Regional Fisheries Research Laboratory 30, 110.Google Scholar
Marco-Herrero, E., Gonzáles-Gordillo, J.I. and Cuesta, J.A. (2014) Morphology of the megalopa of the mud crab, Phithropanopeus harrisii (Gould, 1841) (Decapoda, Brachyura, Panopeidae), identified by DNA barcode. Helgoland Marine Research 68, 201208. http://dx.doi.org/10.1007/s10152-014-0381-8.Google Scholar
Marco-Herrero, E., Gonzáles-Gordillo, J.I. and 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, 513521. http://dx.doi.org/10.1017/S0025315414001908.Google Scholar
Marco-Herrero, E., Torres, A.P., Cuesta, J.A., Guerao, G., Palero, F. and Abelló, P. (2013) The systematic position of Ergasticus (Decapoda, Brachyura) and allied genera, a molecular and morphological approach. Zoologica Scripta 42, 427439. http://dx.doi.org/10.1111/zsc.12012.Google Scholar
Marin, I. (2015) Complete morphological re-description of mud-dwelling axiid Leonardsaxius amurensis (Kobjakova, 1937) with remarks on Axiidae (Crustacea: Decapoda: Axiidea) from the Russian coast of the Sea of Japan. Zootaxa 3937, 549563. http://dx.doi.org/10.11646/zootaxa.3937.3.7.Google Scholar
Meyer, C.P. and Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, e422. http://dx.doi.org/10.1371/journal.pbio.0030422.Google Scholar
Meyer, R., Weis, A. and 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, 389404. http://dx.doi.org/10.1080/14772000.2013.833143.Google Scholar
Miller, M.A., Pfeiffer, W. and Schwartz, T. (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, pp. 18.Google Scholar
Miyabe, S., Konishi, K., Fukuda, Y. and Tamaki, A. (1998) The complete larval development of the ghost shrimp, Callianassa japonica Ortmann, 1891 (Decapoda: Thalassinidea: Callianassidae), reared in the laboratory. Crustacean Research 27, 101121.Google Scholar
Nakano, T. and Ozawa, T. (2004) Phylogeny and historical biogeography of limpets of the order Patellogastropoda based on mitochondrial DNA sequences. Journal of Molluscan Studies 70, 3141.Google Scholar
Pan, M., McBeath, A.J.A., Hay, S.J., Pierce, G.J. and Cunningham, C.O. (2008) Real-time PCR assay for detection and relative quantification of Liocarcinus depurator larvae from plankton samples. Marine Biology 153, 859870. http://dx.doi.org/10.1007/s00227-007-0858-y.Google Scholar
Pardo, L.M., Ampuero, D. and Véliz, D. (2009) Using morphological and molecular tools to identify megalopae larvae collected in the field: the case of sympatric Cancer crabs. Journal of the Marine Biological Association of the United Kingdom 89, 481490. http://dx.doi.org/10.1017/S0025315409003233.Google Scholar
Pohle, G. and Santana, W. (2014) Gebiidea and Axiidea (= Thalassinidea). In Martin, J.W., Olesen, J. and Høeg, J.T. (eds) Atlas of crustacean larvae. Baltimore, MD: Johns Hopkins University Press, pp. 263271.Google Scholar
Pohle, G., Santana, W., Jansen, G. and Greenlaw, M. (2011) Plankton-caught zoeal stages and megalopa of the lobster shrimp Axius serratus (Decapoda: Axiidae) from the Bay of Fundy, Canada, with a summary of axiidean and gebiidean literature on larval descriptions. Journal of Crustacean Biology 31, 8299. http://dx.doi.org/10.1651/10-3321.1.Google Scholar
Porter, M.L., Pérez-Losada, M. and Crandall, K.A. (2005) Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution 37, 355369. http://dx.doi.org/10.1016/j.ympev.2005.06.021.Google Scholar
Rao, S., Liston, A., Crampton, L. and Takeyasu, J. (2006) Identification of larvae of exotic Tipula paludosa (Diptera: Tipulidae) and T. oleracea in North America using mitochondrial cytB sequences. Annals of the Entomological Society of America 99, 3340. http://dx.doi.org/10.1603/0013-8746(2006)099[0033:IOLOET]2.0.CO;2.Google Scholar
Ratnasingham, S. and Hebert, P.D.N. (2013) A DNA-based registry for all animal species: the Barcode Index Number (BIN) system. PLoS ONE 8, e66213. http://dx.doi.org/10.1371/journal.pone.0066213.Google Scholar
Raupach, M.J., Barco, A., Steinke, D., Beermann, J., Laakmann, S., Mohrbeck, I., Neumann, H., Kihara, T.C., Pointner, K., Radulovici, A., Segelken-Voigt, A., Wesse, C. and Knebelsberger, T. (2015) The application of DNA barcodes for the identification of marine crustaceans from the North sea and adjacent regions. PLoS ONE 10, 123. http://dx.doi.org/10.1371/journal.pone.0139421.Google Scholar
Raupach, M.J. and Radulovici, A.E. (2015) Looking back on a decade of barcoding crustaceans. ZooKeys 539, 5381. http://dx.doi.org/10.3897/zookeys.539.6530.Google Scholar
Rodrigues, S. de A. (1994) First stage larva of Axiopsis serratifrons (A. Milne Edwards, 1873) reared in the laboratory (Decapoda: Thalassinidea: Axiidae). Journal of Crustacean Biology 14, 314318.Google Scholar
Ronquillo, J.D., Saisho, T. and McKinley, R.S. (2006) Early developmental stages of the green tiger prawn, Penaeus semisulcatus de Haan (Crustacea, Decapoda, Penaeidae). Hydrobiologia 560, 175196. http://dx.doi.org/10.1007/s10750-005-1448-y.Google Scholar
Sakai, K. (2011) Axioidea of the world and a reconsideration of the Callianassoidea (Decapoda, Thalanassidea, Callianassida). Crustaceana Monographs 13. Leiden: Brill.Google Scholar
Sakai, K. and de Saint Laurent, M. (1989) A check list of Axiidae (Decapoda, Crustacea, Thalassinidea, Anomura), with remarks and in addition descriptions of one new subfamily, eleven new genera and two new species. Naturalists 3, 1104.Google Scholar
Schindel, D.E. and Miller, S.E. (2005) DNA barcoding a useful tool for taxonomists. Nature 435, 17.Google Scholar
Schubart, C.D., Cuesta, J.A., Diesel, R. and Felder, D.L. (2000) Molecular phylogeny, taxonomy, and evolution of nonmarine lineages within the American grapsoid crabs (Crustacea: Brachyura). Molecular Phylogenetics and Evolution 15, 179190. http://dx.doi.org/10.1006/mpev.1999.0754.Google Scholar
Schubart, C.D., Diesel, R. and Hedges, S.B. (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393, 363365.Google Scholar
Spivak, E.D. and Schubart, C.D. (2003) Species status in question: a morphometric and molecular comparison of Cyrtograpsus affinis and C. altimanus (Decapoda, Brachyura, Varunidae). Journal of Crustacean Biology 23, 212222.Google Scholar
Stamatakis, A. (2014) RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 13121313. http://dx.doi.org/10.1093/bioinformatics/btu033.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739. http://dx.doi.org/10.1093/molbev/msr121.Google Scholar
Tang, R.W.K., Yau, C. and Ng, W.-C. (2010) Identification of stomatopod larvae (Crustacea: Stomatopoda) from Hong Kong waters using DNA barcodes. Molecular Ecology Resources 10, 439448. http://dx.doi.org/10.1111/j.1755-0998.2009.02794.x.Google Scholar
Terossi, M., Cuesta, J.A., Wehrtmann, I.S. and Mantelatto, F.L. (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, 4966.Google Scholar
Trivedi, S., Aloufi, A.A., Ansari, A.A. and Ghosh, S.K. (2016) Role of DNA barcoding in marine biodiversity assessment and conservation: an update. Saudi Journal of Biological Sciences 23, 161171. http://dx.doi.org/10.1016/j.sjbs.2015.01.001.Google Scholar
Vaidya, G., Lohman, D.J. and Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27, 171180. http://dx.doi.org/10.1111/j.1096-0031.2010.00329.x.Google Scholar
Vences, M., Thomas, M., Bonett, R.M. and Vieites, D.R. (2005) Deciphering amphibian diversity through DNA barcoding: chances and challenges. Philosophical Transactions of the Royal Society B: Biological Sciences 360, 18591868. http://dx.doi.org/10.1098/rstb.2005.1717.Google Scholar
Vinogradov, L.G. (1950) Classification of shrimps, prawns and crabs from the Far East. Izvestiya TINRO 33, 179358.Google Scholar
Wong, J., Pérez-Moreno, J.L., Chan, T.Y., Frank, T.M. and Bracken-Grissom, H.D. (2015) Phylogenetic and transcriptomic analyses reveal the evolution of bioluminescence and light detection in marine deep-sea shrimps of the family Oplophoridae (Crustacea: Decapoda). Molecular Phylogenetics and Evolution 83, 278292. http://dx.doi.org/10.1016/j.ympev.2014.11.013.Google Scholar