Abstract
The pelagic marine copepod family Oncaeidae is highly diversified (over 100 species worldwide) and includes a great number of sibling species, which are difficult to identify morphologically, because of their very small size (0.18–1.2 mm total length as adults). Global investigations of oncaeid biodiversity are severely hampered by insufficient taxonomic knowledge, in particular for species which have first been described from the European Mediterranean Sea (type locality). Many of these species have been reported as key taxa of small-sized copepod communities in very distant oceanic regions. However, due to the taxonomic uncertainties it cannot be excluded that at least some of these allegedly cosmopolitan species in reality represent a complex of distinct, yet closely related, species. To improve the basis for the identification of Oncaeidae of Mediterranean origin, new diagnostic characters in combination with traditional methods were applied in the present study. Copepods were sampled with fine nets of 0.1 mm mesh size down to a maximum depth of 1,000 m on a west-east-transect in the Mediterranean Sea. Oncaeid species and form variants were predefined morphologically and the genetic identity of the morphospecies was analysed by about 650 and 500 bp region of the mitochondrial COI and 12S srRNA gene sequence, respectively (barcoding). A total of 67 individuals from 24 oncaeid species and forms were successfully analysed, including 12 species and one form of Mediterranean origin. For Oncaeidae, the 12S amplification turned out to be more successful (23 species) than the COI amplification (13 species and 1 form). Together, the morphological and molecular results are discussed with respect to three topics: (1) confirmation of a genetic distinction of three Triconia species, which have been interpreted as sibling species by morphological characters, (2) genetic distance of species within the ovalis-complex of oncaeids and (3) the taxonomic status of two form variants of Oncaea mediterranea (Claus).
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References
Akaike, H., 1974. New look at statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.
Bensasson, D., D.-X. Zhang, D. L. Hartl & G. M. Hewitt, 2001. Mitochondrial pseudogenes: evolution′s misplaced witnesses. TRENDS in Ecology & Evolution 16: 314–321.
Birky, C. W. Jr., 2007. Workshop on barcoded DNA: application to rotifer phylogeny, evolution, and systematics. Hydrobiologia 593: 175–183.
Böttger-Schnack, R., 1997. Vertical structure of small metazoan plankton, especially non-calanoid copepods.II. Deep Eastern Mediterranean (Levantine Sea). Oceanologica Acta 20: 399–419.
Böttger-Schnack, R., 1999. Taxonomy of Oncaeidae (Copepoda: Poecilostomatoida) from the Red Sea. I. 11 species of Triconia gen. nov., and a redescription of T. similis (Sars) from Norwegian waters. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 96: 39–128.
Böttger-Schnack, R., 2001. Taxonomy of Oncaeidae (Copepoda: Poecilostomatoida) from the Red Sea. II. Seven species of Oncaea s. str. Bulletin of the Natural History Museum London (Zoology) 67: 25–84.
Böttger-Schnack, R., 2002. Taxonomy of Oncaeidae (Copepoda, Poecilostomatoida) from the Red Sea. VI. Morphology and zoogeography of Oncaea bispinosa sp. nov., a sistertaxon of O. zernovi Shmeleva. Journal of Plankton Research 24: 1107–1129.
Böttger-Schnack, R., 2003. Taxonomy of Oncaeidae (Copepoda, Poecilostomatoida) from the Red Sea. V. Three species of Spinoncaea gen. nov. (ivlevi-group), with notes on zoogeographical distribution. Zoological Journal of the Linnean Society 137: 187–226.
Böttger-Schnack, R., 2005. Taxonomy of Oncaeidae (Copepoda, Cyclopoida s.l.) from the Red Sea. VII. Oncaea cristata, a new species related to the ovalis-complex, and a revision of O. ovalis Shmeleva and O. bathyalis Shmeleva from the Mediterranean. Cahiers de Biologie Marine 46: 161–209.
Böttger-Schnack, R., 2009. Taxonomy of Oncaeidae (Copepoda, Cyclopoida s.l.) from the Red Sea. IX. Epicalymma bulbosa sp. nov., first record of the genus in the Red Sea. Journal of Plankton Research 31: 1027–1043.
Böttger-Schnack, R. & G. A. Boxshall, 1990. Two new Oncaea species (Copepoda: Poecilostomatoida) from the Red Sea. Journal of Plankton Research 12: 861–871.
Böttger-Schnack, R. & R. Huys, 1997. Morphological observations on Oncaea mediterranea (Claus, 1863) (Copepoda: Poecilostomatoida) with a comparison of Red Sea and eastern Mediterranean populations. Bulletin of the Natural History Museum London (Zoology) 63: 137–147.
Böttger-Schnack, R. & R. Huys, 1998. Species groups within the genus Oncaea (Copepoda, Poecilostomatoida). Journal of marine Systems 15: 369–371.
Böttger-Schnack, R. & R. Huys, 2001. Taxonomy of Oncaeidae (Copepoda, Poecilostomatoida) from the Red Sea. III. Morphology and phylogenetic position of Oncaea subtilis Giesbrecht, 1892. Hydrobiologia 453(454): 467–481.
Böttger-Schnack, R. & R. Huys, 2004. Size polymorphism in Oncaea venusta Philippi, 1843 and the validity of O. frosti Heron, 2002: a commentary. Hydrobiologia 513: 1–5.
Böttger-Schnack, R. & D. Schnack, 2009. Taxonomic diversity and identification problems of oncaeid microcopepods in the Mediterranean Sea. Marine Biodiversity 39: 131–145.
Böttger-Schnack, R., J. Lenz & H. Weikert, 2004. Are taxonomic details of relevance to ecologists? An example from oncaeid microcopepods of the Red Sea. Marine Biology 144: 1127–1140.
Boxshall, G. A. & R. Böttger, 1987. Two new species of Oncaea (Copepoda: Poecilostomatoida) from the Red Sea and a redescription of O. atlantica Shmeleva. Journal of Plankton Research 9: 553–564.
Bucklin, A., 2000. Methods for population genetic analysis of zooplankton. In Harris, R., H.-R. Skjoldal, J. Lenz, P. Wiebe & M. Huntley (eds), ICES Zooplankton Methodology Manual. Academic Press, Paris: 533–570.
Buhay, J. E., 2009. “COI” sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29: 96–110.
Claus, C. 1863. Die freilebenden Copepoden mit besonderer Berücksichtigung der Fauna Deutschlands, der Nordsee und des Mittelmeeres. Wilhelm Engelmann, Leipzig I-X: 230, 37 plates.
Di Capua, I. & G. A. Boxshall, 2008. Records of Oncaeidae (Copepoda) from the Gulf of Naples, with new records of three species of Triconia. Journal of the Marine Biological Association of the United Kingdom 88: 1407–1415.
Elvers, D., 2003. Plankton sampling for molecular population genetic studies. In Hemleben, C., K. Hoernle, B. B. Jorgensen, W. Roether (eds), 2001, Ostatlantik – Mittelmeer – Schwarzes Meer – Cruise No. 51, 12 September-28 December 2001. METEOR-Berichte, Universität Hamburg 03-1: 2/41-2/42.
Elvers, D., R. Böttger-Schnack, D. Blohm & W. Hagen, 2006. Sympatric size variants of the microcopepod Oncaea venusta exhibit distinct lineages in DNA sequences. Marine Biology 149: 503–513.
Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Goetze, E., 2003. Cryptic speciation on the high seas; global phylogenetics of the copepod family Eucalanidae. Proceedings of the Royal Society of London, series B, 270: 2321–2331.
Gordeyeva, K. T., 1972. New species of the genus Oncaea (Copepoda, Cyclopoida) from the tropical zone of the Atlantic Ocean. Zoologicheskii Zhurnal 51: 963–968. (in Russian, English summary).
Gordeyeva, K. T., 1975. Pelagic Cyclopoida (Copepoda) from the tropical Atlantic and South Seas. Zoologicheskii Zhurnal 54: 776–779. (in Russian, English summary).
Hasegawa, M., H. Kishino & T. Yano, 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.
Hebert, P. D. N., A. Cywinska, S. L. Ball & J. R. deWaard, 2003a. Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270: 313–321.
Hebert, P. D. N., S. Ratnasingham & J. R. de Waard, 2003b. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B (Supplement) 270: S96–S99.
Hemleben, C., K. Hoernle, B. B. Jørgensen, & W. Roether (eds) 2003. Ostatlantik-Mittelmeer-Schwarzes Meer, Cruise no. 51, 12 September-28 December 2001. Meteor-Berichte, Universität Hamburg, 03-1: 225.
Heron, G. A., 1977. Twenty-six species of Oncaeidae (Copepoda : Cyclopoida) from the Southwest Pacific Antarctic area. In L. Pawson (ed.), Biology of the Antarctic Seas, VI. Antarctic Research Series, Washington 26: 37–96.
Heron, G. A. & J. M. Bradford-Grieve, 1995. The marine fauna of New Zealand: Pelagic Copepoda: Poecilostomatoida: Oncaeidae. New Zealand Oceanographic Institut Memoir 104: 1–57.
Heron, G. A. & B. W. Frost, 2000. Copepods of the family Oncaeidae (Crustacea: Poecilostomatoida) in the northeast Pacific Ocean and inland coastal waters of Washington State. Proceedings of the Biological Society of Washington 113: 1015–1063.
Heron, G. A., T. S. English & D. M. Damkaer, 1984. Arctic Ocean Copepoda of the genera Lubbockia, Oncaea and Epicalymma (Poecilostomatoida: Oncaeidae), with remarks on distributions. Journal of Crustacean Biology 4: 448–490.
Hopcroft, R. R., J. C. Roff & F. P. Chavez, 2001. Size paradigms in copepod communities: a re-examination. Hydrobiologia 453: 133–141.
Huelsenbeck, J. P. & F. Ronquist, 2001. MrMAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.
Huys, R. & R. Böttger-Schnack, 2008 [“2007”]. Taxonomy of Oncaeidae (Copepoda, Poecilostomatoida) from the Red Sea. – VIII. Morphology and phylogenetic position of Oncaea tregoubovi Shmeleva, 1968 and the closely related O. prendeli Shmeleva, 1966 from the Mediterranean Sea. Mitteilungen aus dem Hamburgischen Zoologischen Museum und Institut 104: 89–127. (dated 2007).
Katoh, K. & H. Toh, 2008. Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286–298.
Kovalev, A. V. & A. A. Shmeleva, 1982. Fauna of Copepoda in the Mediterranean. Ekologija Morja 8: 82–87. (in Russian).
Kršinic, F., 1998. Vertical distribution of protozoan and microcopepod communities in the South Adriatic Pit. Journal of Plankton Research 20: 1033–1060.
Kršinic, F. & B. Grbec, 2002. Some distributional characteristics of small zooplankton at two stations in the Otranto Strait (Eastern Mediterranean). Hydrobiologia 482: 119–136.
Lee, C. E., 2000. Global phylogeographic of a cryptic copepod species complex and reproductive isolation between genetically proximate “populations”. Evolution 54: 2014–2027.
Machida, R. J., M. U. Miya, M. Nishida & S. Nishida, 2002. Complete mitochondrial DNA sequence of Tigriopus japonicus (Crustacea: Copepoda). Marine Biotechnology 4: 406–417.
Machida, R. J., M. U. Miya, M. Nishida & S. Nishida, 2004. Large-scale gene rearrangements in the mitochondrial genomes of two calanoid copepods Eucalanus bungii and Neocalanus cristatus (Crustacea), with notes on new versatile primers for the srRNA and COI genes. Gene 332: 71–78.
Maddison, D. R. & W. P. Maddison, 2003. MacClade 4: Analysis of Phylogeny and Character Evolution. Sinauer Associates, Sunderland, MA.
Malt, S. J., 1983. Studies on the taxonomy and ecology of the marine copepod genus Oncaea Philippi. PhD dissertation, University of London: 500.
Malt, S. J., S. Lakkis & R. Ziedane, 1989. The copepod genus Oncaea (Poecilostomatoida) from the Lebanon: taxonomic and ecological observations. Journal of Plankton Research 11: 949–969.
Nishibe, Y. & T. Ikeda, 2004. Vertical distribution, abundance and community structure of oncaeid copepods in the Oyashio region, western subarctic Pacific. Marine Biology 145: 931–941.
Nylander, J. A. A., 2004. MrModeltest 2.0. Program Distributed by the Author. Evolutionary Biology Centre, Uppsala University, Uppsala.
Rezai, H., F. M. Yusoff, A. Arshad, A. Kawamura, S. Nishida & O. B. H. Ross, 2004. Spatial and temporal distribution of copepods in the Straits of Malacca. Zoological Studies 43: 486–497.
Schander, C. & E. Willassen, 2005. What can biological barcoding do for marine biology? Marine Biology Research 1: 79–83.
Schizas, N. V., G. T. Street, B. C. Coull, G. T. Chandler & J. M. Quattro, 1997. An efficient DNA extraction method for small metazoans. Molecular Marine Biology and Biotechnology 6: 381–383.
Shmeleva, A. A., 1969. Espèces nouvelles du genre Oncaea (Copepoda, Cyclopoida) de la mer Adriatique. Bulletin de l′Institut Océanographique, Monaco 68: 1–28.
Shmeleva, A. A., 1979. New species and some previously unknown males of the genus Oncaea (Copepoda, Cyclopoida) from the Mediterranean. Zoologicheskii Zhurnal 58: 491–498. (in Russian, English summary).
Swofford, D. L., 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Massachusetts.
Webber, M. K. & J. C. Roff, 1995. Annual structure of the copepod community and its associated pelagic environment off Discovery Bay, Jamaica. Marine Biology 123: 467–479.
Weikert, H. & H.-C. John, 1981. Experiences with a modified Bé multiple opening-closing plankton net. Journal of Plankton Research 3: 167–176.
Yang, Z., 1994. Maximum likelihood phylogenetic estimation from DNA sequences with variable rates over sites: approximate methods. Journal of Molecular Evolution 39: 306–314.
Zervoudaki, S., E. D. Christou, T. G. Nielsen, et al., 2007. The importance of small-sized copepods in a frontal area of the Aegean Sea. Journal of Plankton Research 29: 317–338. 8 co-authors.
Zwickl, D. J., 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin.
Acknowledgments
We wish to thank D. Elvers (University of Bremen) for collecting the fine mesh net plankton samples during RV ′Meteor` cruise 51/2. Thanks are due to Prof. K. Lochte (formerly IFM-GEOMAR, now AWI, Bremerhaven) and Prof. U. Riebesell (IFM-GEOMAR) for providing excellent working conditions to R.B.S. Special thanks are given to Prof. D. Schnack for commenting on the manuscript and to Elisabeth Samusch for personal support to R.B.S. This study was supported by a research grant from the German Science Foundation to R.B.S (Schn 455/4-1). The funding of travel expenses to the 10th ICOC in Thailand by the German Science Foundation (Schn 455/5-1) is gratefully acknowledged. We gratefully acknowledge the support of the Alfred P. Sloan Foundation. Additional support for this project was provided to R. J. M. by a Grant-in-Aid for Scientific Research No. 20241003 from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Data Integration & Analysis System from the Ministry of Education, Culture, Sports, Science and Technology of Japan provided funding to R. J. M. This study is a contribution from the Census of Marine Zooplankton (CMarZ), an ocean realm field project of the Census of Marine Life.
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Guest editors: L. Sanoamuang & J. S. Hwang / Copepoda: Biology and Ecology
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Böttger-Schnack, R., Machida, R.J. Comparison of morphological and molecular traits for species identification and taxonomic grouping of oncaeid copepods. Hydrobiologia 666, 111–125 (2011). https://doi.org/10.1007/s10750-010-0094-1
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DOI: https://doi.org/10.1007/s10750-010-0094-1