Diversity and life-cycle analysis of Pacific Ocean zooplankton by videomicroscopy and DNA barcoding: Hydrozoa

Autoři: Peter J. Bryant aff001;  Timothy E. Arehart aff002
Působiště autorů: Department of Developmental and Cell Biology, University of California, Irvine, Irvine, CA, United States of America aff001;  Crystal Cove Conservancy, Newport Coast, CA, United States of America aff002
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0218848


Most, but not all cnidarian species in the class Hydrozoa have a life cycle in which a colonial, asexually reproducing hydroid phase alternates with a free-swimming, sexually reproducing medusa phase. They are not well known, in part because many of them are microscopic, at least in the medusa phase. Matching the two phases has previously required rearing of the organism from one phase to another, which has not often been possible. Here we show that DNA barcoding makes it possible to easily link life-cycle phases without the need for laboratory rearing. Hydrozoan medusae were collected by zooplankton tows in Newport Bay and the Pacific Ocean near Newport Beach, California, and hydroid colonies were collected from solid substrates in the same areas. Specimens were documented by videomicroscopy, preserved in ethanol, and sent to the Canadian Centre for DNA Barcoding at the University of Guelph, Ontario, Canada for sequencing of the COI DNA barcode. In the order Anthoathecata (athecate hydroids), DNA barcoding allowed for the discrimination between the medusae of eight putative species of Bougainvillia, and the hydroid stages were documented for two of these. The medusae of three putative species of Amphinema were identified, and the hydroid stages were identified for two of them. DNA barcodes were obtained from medusae of one species of Cladonema, one adult of the by-the wind Sailor, Velella velella, five putative species of Corymorpha with the matching hydroid phase for one; and Coryne eximia, Turritopsis dohrnii and Turritopsis nutricula with the corresponding hydroid phases. The actinula larvae and hydroid for the pink-hearted hydroid Ectopleura crocea were identified and linked by DNA barcoding. In the order Leptothecata (thecate hydroids) medusae were identified for Clytia elsaeoswaldae, Clytia gracilis and Clytia sp. 701 AC and matched with the hydroid phases for the latter two species. Medusae were matched with the hydroid phases for two species of Obelia (including O. dichotoma) and Eucheilota bakeri. Obelia geniculata was collected as a single hydroid. DNA barcodes were obtained for hydroids of Orthopyxis everta and three other species of Orthopyxis. One member of the family Solmarisidae, representing the order Narcomedusae, and one member (Liriope tetraphylla) of the order Trachymedusae were recognized as medusae. The results show the utility of DNA barcoding for matching life-cycle stages as well as for documenting the diversity of this class of organisms.

Klíčová slova:

Coral reefs – Corals – Crystals – DNA barcoding – Islands – Larvae – Life cycles – Oceans


1. Daly M., Brugler M.R., Cartwright P., Collins A.G., Dawson M.N., Fautin D.G., France S.C., Mcfadden C.S., Opresko D.M., Rodriguez E., Romano S.L. and Stake J.L. (2007). The phylum Cnidaria: A review of phylogenetic patterns and diversity 300 years after Linnaeus. Zootaxa 1668:127–182.

2. Marques A.C., and Collins A.G. (2004). Cladistic analysis of medusozoa and cnidarian evolution. Inv. Biol. 123 1: 23–42

3. Werner B., Cutress C. E. & Studebaker J. P. 1971. Life cycle of Tripedalia cystophora Conant (Cubomedusae). Nature 232: 582–583. doi: 10.1038/232582a0 16063105

4. Straehler-Pohl I., Matsumoto G.I., and Acevedo M.J. (2017) Recognition of the Californian cubozoan population as a new species Carybdea confusa n. sp. (Cnidaria, Cubozoa, Carybdeida). Plankton Benthos Res 12: 129–138.

5. Evans N. M.; Lindner A.; Raikova E. V.; Collins A. G.; Cartwright P. (2008). Phylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the Phylum Cnidaria. BMC Evolutionary Biology. 8: 139. doi: 10.1186/1471-2148-8-139 18471296

6. Zrzavý J. & Hypša V. (2003). Myxozoa, Polypodium, and the origin of the Bilateria: The phylogenetic position of "Endocnidozoa" in light of the rediscovery of Buddenbrockia. Cladistics 19(2): 164–169.

7. Hubert N. and Hanner R. (2015). DNA Barcoding, species delineation and taxonomy: a historical perspective. DNA Barcodes 3: 44–58.

8. Vannucci M. and Rees W. L., W. L. (1961). A revision of the genus Bougainvillia (Anthomedusae). Bol. Inst. Ocean, 11: 57–100.

9. Schuchert P. (2007). The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Filifera Part 2.Revue Suisse de Zoologie, 114, 195–396.

10. Hyman L. H. (1947). Two new hydromedusae from the California Coast. Trans. Am. Microsc. Soc. 66: 262–268.

11. Schuchert P. (2006). The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Capitata Part 1. Revue Suisse de Zoologie 113: 325–410.

12. Schuchert P. (2010). The European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Capitata Part 2. Revue Suisse de Zoologie, 117, 337–555.

13. Sassaman C. and Rees J.T. (1978). The life cycle of Corymorpha (= Euphysora) bigelowi (Maas, 1905) and its significance in the systematics of corymorphid hydromedusae. Bio. Bull. 154: 485–496.

14. Schuchert P. (2001). Survey of the family Corynidae (Cnidaria, Hydrozoa). Revue Suisse de Zoologie 108: 739–878.

15. Bouillon J., Medel M.D., Pagès F., Gili J.-M., Boero F., and Gravili C. (2004). Fauna of the Mediterranean Hydrozoa. Sci. Mar. 68 Suppl. 2: 1–449.

16. Miglietta M.P., Maggioni D., and Matsumoto Y. (2019). Phylogenetics and species delimitation of two hydrozoa (phylum Cnidaria): Turritopsis (McCrady, 1857) and Pennaria (Goldfuss, 1820). Marine Biodiversity 49, 1085–1100.

17. Schuchert P. (2004). Revision of the European athecate hydroids and their medusae (Hydrozoa, Cnidaria): Families Oceanidae and Pachycordylidae. Revue Suisse de Zoologie 111: 315–369.

18. Brinckmann-Voss (1970). Anthoathecata/Athecatae (Hydrozoa, Cnidaria) of the Mediterranean. Part I. Capitata. Fauna e Flora del Golfo di Napoli. 39. Stazione Zoologica. pp. 1–96.

19. Fofonoff, P.W., Ruiz, G.M., Steves, B., Simkanin, C., and Carlton, J.T. (2019). National Exotic Marine and Estuarine Species Information System. http://invasions.si.edu/nemesis/. Access Date: 14-Aug-2019

20. Cornelius P.F.S. (1982). Hydroids and medusae of the family Companulariidae recorded from the eastern north Atlantic, with a world synopsis of genera. Bull. Brit. Mus. (Nat. Hist.) 42, 37–148.

21. Lindner A., Govindarajan A.F., and Migotto A.E. (2011). Cryptic species, life cycles, and the phylogeny of Clytia (Cnidaria: Hydrozoa: Campanulariidae) Zootaxa 2980: 23–36.

22. He J., Zheng L., Zhang W., Lin Y., & Cao W. (2015). Morphology and molecular analyses of a new Clytia species (Cnidaria: Hydrozoa: Campanulariidae) from the East China Sea. J. Marine Biol. Assoc. U.K., 95(2), 289–300.

23. Cornelius P.F.S. (1975). The hydroid species of Obelia (Coelenterata, Hydrozoa: Campanulariidae), with notes on the medusa stage. Bull. Brit. Mus. (Nat. Hist.) Zoology 28: 251–293.

24. Cunha A.F., Genzano G.N., and Marques A.C. (2015). Reassessment of morphological diagnostic characters and species boundaries requires taxonomical changes for the genus Orthopyxis L. Agassiz, 1862 (Campanulariidae, Hydrozoa) and some related campanulariids. PLoS One;10:e0117553. doi: 10.1371/journal.pone.0117553 25723572

25. Torrey H.B. (1909). The Leptomedusae of the San Diego Region. University of California Publications in Zoology 6: 11–31.

26. Schuchert, P. (2019a). World Hydrozoa Database. Solmarisidae Haeckel, 1879. Accessed through: World Register of Marine Species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=16848 on 2019-05-27

27. Schuchert, P. (2019b). World Hydrozoa Database. Liriope tetraphylla (Chamisso & Eysenhardt, 1821). Accessed through: World Register of Marine Species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=117568 on 2019-05-28

28. McFadden C. S., Haverkort-Yeh R., Reynolds A. M., Halàsz A., Quattrini A. M., Forsman Z. H., Benayahu Y., and Toonen R. J. (2017). Species boundaries in the absence of morphological, ecological or geographical differentiation in the Red Sea octocoral genus Ovabunda (Alcyonacea: Xeniidae). Mol. Phylogenet. Evol. 112:174–184. doi: 10.1016/j.ympev.2017.04.025 28467886

29. van Beneden P. J. (1843). Mémoire sur les campanulaires de la côte d'Ostende considérés sous le rapport physiologique, embryogénique et zoologique. Ann. Sci. Nat. (Zool.) (2)20: 350–369.

30. Russell F. S. (1954). The Medusae of the British Isles. v. 1. Anthoathecata, Leptoathecata, Limnomedusae, Trachymedusae and Narcomedusae. Cambridge University Press, New York

31. Russell F. S. (1970). Medusae of the British Isles. v. 2. Pelagic Scyphozoa with a supplement to the first volume on Hydromedusae. Cambridge University Press, New York.

32. Waugh J. (2007). DNA barcoding in animal species: progress, potential and pitfalls. BioEssays 29: 188–197. doi: 10.1002/bies.20529 17226815

33. Hebert P.D.N., Ratnasingham S. and deWaard J.R. (2003). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proc. Bio. Sci. 270 (Suppl. 1), S96–S99.

34. Prasanna Kumar, C. and Qinqhua, Z. (2018) Validating DNA barcodes for Anthozoans: What we know after scanning 126 mitochondrial whole genome? STAPCOR 2018: International Conference on Status and Protection of Coral Reefs held at Bangaram Island, Lakshadweep, India.

Článek vyšel v časopise


2019 Číslo 10