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Systematics of Hypnea (Cystocloniaceae, Rhodophyta) from coastal North Carolina, with a first report of Calliblepharis saidana from the United States Atlantic Coast

  • Jason T. Campbell

    Jason T. Campbell completed his Master of Science degree at the University of North Carolina at Wilmington in May 2021. His research focused on the phylogenetics of Hypnea species throughout the Western. He is currently working as a Fisheries Observer in the Gulf of Mexico Shrimp and Reef fish fishery out of Bayou la Batre, AL.

    , D. Wilson Freshwater

    D. Wilson Freshwater is researcher at the Center for Marine Science, University of North Carolina Wilmington. His current research interests include molecular phylogeny and taxonomy of marine algae, marine floristics, Pomatomus saltatrix aggressive behavior, and ecology of marine hard bottom communities.

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    and J. Craig Bailey

    J. Craig Bailey is researcher at the Center for Marine Science, University of North Carolina Wilmington. His current research interests include the evolution stramenopiles and red algae. He is a failed humorist.

From the journal Botanica Marina

Abstract

Complete and/or partial DNA sequences for the plastid-encoded rbcL gene and the 5′ end of the mitochondrial cytochrome oxidase I (COI-5P) gene were used to re-examine the systematics of Hypnea species (Cystocloniaceae, Rhodophyta) from North Carolina, USA. These data, combined with light microscopic observations, indicate that two species (Hypnea cryptica and H. musciformis sensu stricto) are present in nearshore waters of coastal North Carolina. Molecular and morphological analyses with topotype material of Hypnea volubilis from North Carolina offshore waters revealed that it and Calliblepharis saidana are conspecific. Hypnea volubilis is proposed as a heterotypic synonym of C. saidana. This is the first report of Calliblepharis from the United States Atlantic coast and only the second report from the western hemisphere.


Corresponding author: D. Wilson Freshwater, Center for Marine Science, University of North Carolina at Wilmington, 5600 Marvin K. Moss Lane, Wilmington, NC 28409, USA, E-mail:

Award Identifier / Grant number: DEB-0742437

Award Identifier / Grant number: DEB-0743334

Funding source: CMS DNA-Algal Trust

About the authors

Jason T. Campbell

Jason T. Campbell completed his Master of Science degree at the University of North Carolina at Wilmington in May 2021. His research focused on the phylogenetics of Hypnea species throughout the Western. He is currently working as a Fisheries Observer in the Gulf of Mexico Shrimp and Reef fish fishery out of Bayou la Batre, AL.

D. Wilson Freshwater

D. Wilson Freshwater is researcher at the Center for Marine Science, University of North Carolina Wilmington. His current research interests include molecular phylogeny and taxonomy of marine algae, marine floristics, Pomatomus saltatrix aggressive behavior, and ecology of marine hard bottom communities.

J. Craig Bailey

J. Craig Bailey is researcher at the Center for Marine Science, University of North Carolina Wilmington. His current research interests include the evolution stramenopiles and red algae. He is a failed humorist.

Acknowledgements

The authors wish to thank the Center for Marine Science’s Marine Operations division, the Coastal Oceans Research and Monitoring Program (CORMP) and late NOAA-NURC program for assistance with the collection of offshore specimens. We are especially indebted to captains and divers Steve Hall, Ken Johns, Dave Wells, Jay Souza, Chris LaClair, Brett Bolton, Brian Degan, Jennifer Idol, and Henry J. Styron. We also thank J. ‘Trey’ Foscue for laboratory assistance.

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: DWFs work on this project was funded by NC SeaGrant, US National Science Foundation Grants DEB-0742437 and DEB-0743334, and the CMS DNA-Algal Trust.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.

  4. Ethical standards: The authors declare that no laws were willfully violated in the course of this research, only marine algae.

References

Bast, F., Bhushan, S., and John, A. (2014). Morphological and molecular assessment of native carrageenophyte Hypnea valentiae (Cystocloniace, Gigartinales) in Indian Subcontinent. Phykos 44: 52–88.Search in Google Scholar

Børgesen, F. (1920). The marine algae of the Danish West Indies. Part 3. Rhodophyceae (6) with addenda to chlorophyceae, phaeophyceae and rhodophyceae. Dan. Bot. Ark. 3: 396–498.Search in Google Scholar

Børgesen, F. (1943). Some marine algae from Mauritius. III. Rhodophyceae. Part 2. Gelidiales, cryptonemiales, gigartinales. Biol. Med. 19: 1–85.Search in Google Scholar

Cabrera, R., O’Shields, B., Diaz-Larrea, J., and López-Bautista, J. (2020). Molecular phylogenetic analyses of the genus Hypnea (cystoloniaceae, gigartinales) in Cuba. Caribb. J. Sci. 50: 74–85, https://doi.org/10.18475/cjos.v50i1.a10.Search in Google Scholar

Camacho, O., Fernández-García, C., Vieira, C., Gurgel, C.F.D., Norris, J.N., Freshwater, D.W., and Fredericq, S. (2019). The systematics of Lobophora (Dictyotales, Phaeophyceae) in the Western Atlantic and Eastern pacific oceans: Eight new species. J. Phycol. 55: 611–624, https://doi.org/10.1111/jpy.12850.Search in Google Scholar PubMed

Cribb, A.B. (1983). Marine algae of the southern Great Barrier Reef. Part 1. Rhodophyta. Brisbane, Australia: Australian Coral Reef Society.Search in Google Scholar

Díaz-Tapia, P., Boo, P.J.L., Geraldino, P.J.L., Maneiro, I., Barbara, I., and Hommersand, M.H. (2013). Morphology and systematics of Calliblepharis hypneoides sp. nov. (Cystocloniaceae, Rhodophyta) from the Atlantic Iberian peninsula. Eur. J. Phycol. 48: 380–397.10.1080/09670262.2013.844860Search in Google Scholar

Edgar, R.C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl. Acids Res. 32: 1792–1797, https://doi.org/10.1093/nar/gkh340.Search in Google Scholar PubMed PubMed Central

Fredericq, S., Cho, T.O., Earle, S.A., Gurgel, C.F., Krayesky, D.M., Mateo Cid, L.E., Mendoza Gonzáles, A.C., Norris, J.N., and Suárez, A.M. (2009). Seaweeds of the Gulf of Mexico. In: Felder, D.L., and Camp, D.K. (Eds.), Gulf of Mexico: origins, waters, and biota, Vol. 1. College Station, TX: Biodiversity. Texas A&M University Press, pp. 187–259.Search in Google Scholar

Freshwater, D.W. and Rueness, J. (1994). Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194, https://doi.org/10.2216/i0031-8884-33-3-187.1.Search in Google Scholar

Freshwater, D.W., Whitfield, P.E., Buckel, C.A., Muñoz, R.C., and Degan, B.P. (2016). Epibenthic community assessments indicate high spatial and temporal variability among continental shelf hard bottom sites in a marine transition zone. Reg. Stud. Mar. Sci. 5: 41–50, https://doi.org/10.1016/j.rsma.2016.01.005.Search in Google Scholar

Ganesan, M., Thiruppathi, S., and Jha, B. (2006). Mariculture of Hypnea musciformis (Wulfen) Lamouroux in South east coast of India. Aquaculture 256: 201–211, https://doi.org/10.1016/j.aquaculture.2006.01.039.Search in Google Scholar

Geraldino, P.J.L., Yang, E.C., Kim, M.S., and Boo, S.M. (2009). Systematics of Hypnea asiatica sp. nov. (Hypneaceae, Rhodophyta) based on morphology and nrDNA SSU, plastid rbcL, and mitochondrial cox1. Taxon 58: 606–616, https://doi.org/10.1002/tax.582023.Search in Google Scholar

Geraldino, P.J.L., Riosmena-Rodriguez, R., Liao, L.M., and Boo, S.M. (2010). Phylogenetic relationships within the genus Hypnea (Gigartinales, Rhodophyta), with a description of H. caespitosa sp. nov. J. Phycol. 46: 336–345, https://doi.org/10.1111/j.1529-8817.2009.00804.x.Search in Google Scholar

Hanisak, M.D. and Blair, S.M. (1988). The deep-water macroalgal community of the east Florida continental shelf (USA). Helgolander. Wiss. Meeresuntersuch. 42: 133–163.10.1007/BF02366040Search in Google Scholar

Hoffman, R., Wynne, M.J., and Saunders, G.W. (2018). Calliblepharis rammediorum sp. nov. (gigartinales, Rhodophyta) from the Israeli Levant Mediterranean sea. Cryptogam. Algol. 39: 109–121, https://doi.org/10.7872/crya/v39.iss1.2018.109.Search in Google Scholar

Holmes, E.M. (1895). Marine algae from Japan. J. Linn. Soc. Bot. 31: 248–260.10.1111/j.1095-8339.1896.tb00807.xSearch in Google Scholar

Hoyt, W.D. (1920). The marine algae of Beaufort, N.C., and adjacent regions. U.S. Bull. Bur. Fish. 36: 367–556.Search in Google Scholar

Huelsenbeck, J.P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755, https://doi.org/10.1093/bioinformatics/17.8.754.Search in Google Scholar PubMed

Huisman, J.M., D’Archino, R., Nelson, W., Boo, S.M., and Petrocelli, A. (2021). Cryptic cryptogam revealed: Hypnea corona (Gigartinales: Cystocloniaceae), a new red algal species described from the Hypnea cornuta complex. Pac. Sci. 75: 263–268, https://doi.org/10.2984/75.2.8.Search in Google Scholar

Iha, C., O’Shaughnessy, K.A., Guimaraes, S.M.P.B., Oliveira, M.C., and Freshwater, D.W. (2016). Taxonomic reappraisal of Gelidium coarctatum (Gelidiales, Rhodophyta) and Gelidium lineare sp. nov. from the tropical western Atlantic. Phycologia 55: 555–563, https://doi.org/10.2216/16-17.1.Search in Google Scholar

Jesus, P.B., Guimaraes, S.M.P.B., and Nunes, J.M.D. (2013). Hypnea platyclada, a new species of red alga (Rhodophyta, Cystocloniaceae) from Brazil. Phytotaxa 85: 26–34, https://doi.org/10.11646/phytotaxa.85.1.4.Search in Google Scholar

Jesus, P.B., Nauer, F., Lyra, G.D., Cassano, V., Oliveira, M.C., Nunes, J.M.D., and Schnadelbach, A.S. (2016). Species-delimitation and phylogenetic analyses of some cosmopolitan species of Hypnea (Rhodophyta) reveal synonyms and misapplied names to H. cervicornis, including a new species from Brazil. J. Phycol. 52: 774–792, https://doi.org/10.1111/jpy.12436.Search in Google Scholar PubMed

Jesus, P.B., Costa, A.L., Nunes, J.M.D., Manghisi, A., Genovese, G., Morabito, M., and Schnadelbach, A.S. (2019). Species delimitation methods reveal cryptic diversity in the Hypnea cornuta complex (Cystocloniaceae, Rhodophyta). Eur. J. Phycol. 54: 135–153, https://doi.org/10.1080/09670262.2018.1522454.Search in Google Scholar

Kang, P.J. and Nam, K.W. (2018). New record of three economic Hypnea species (Gigartinales) in Korea. Fish. Aquatic Sci. 21: 31, https://doi.org/10.1186/s41240-018-0108-x.Search in Google Scholar

Kapraun, D.F. (1980). An illustrated guide to the benthic marine algae of coastal North Carolina I. Rhodophyta. Chapel Hill, NC: The University of North Carolina Press.Search in Google Scholar

Lawson, G.W. and John, D.M. (1982). The marine algae and coastal environment of tropical West Africa. Nova Hedwigia Beih 70: 1–455.Search in Google Scholar

Lewmanomont, K. (1997). Species of Hypnea from Thailand. In: Abbott, I.A. (Ed.), Taxonomy of economic seaweeds, pp. 179–191, California Sea Grant College System, La Jolla, California.Search in Google Scholar

Littler, D.S., Littler, M.M., and Hanisak, M.D. (2008). Submersed Plants of the Indian River Lagoon. Washington, D.C.: Offshore Graphics.Search in Google Scholar

Nauer, F., Guimaraes, M.C., Cassano, V., Yokoya, N.S., and Oliveira, M.C. (2014). Hypnea species (Gigartinales, Rhodophyta) from the southeastern coast of Brazil based on molecular studies complemented with morphological analyses, including descriptions of Hypnea edeniana sp. nov. and H. flava sp. nov. Eur. J. Phycol. 49: 550–575, https://doi.org/10.1080/09670262.2014.981589.Search in Google Scholar

Nauer, F., Cassano, V., and Oliveira, M.C. (2015). Description of Hypnea pseudomusciformis sp. nov., a new species based on molecular and morphological analyses, in the context of the H. musciformis complex (Gigartinales, Rhodophyta). J. Appl. Phycol. 27: 2405–2417, https://doi.org/10.1007/s10811-014-0488-y.Search in Google Scholar

Nauer, F., Cassano, V., and Oliveira, M.C. (2016). Hypnea wynnei and Hypnea yokoyana (Cystocloniaceae, Rhodophyta), two new species revealed by a DNA barcoding survey on the Brazilian coast. Phytotaxa 268: 123–134, https://doi.org/10.11646/phytotaxa.268.2.3.Search in Google Scholar

Nauer, F., Ayres, L.M., Plastino, E.M., and Oliveira, M.C. (2017). Life history of two morphological variants of Hypnea pseudomusciformis (Gigartinales, Rodophyta). Phycologia 56: 134–135.Search in Google Scholar

Nauer, F., Cassano, V., and Oliveira, M.C. (2019a). Description of two new Caribbean species from the Hypnea musciformis complex (Cystocloniaceae, Rhodophyta). Phytotaxa 408: 85–98, https://doi.org/10.11646/phytotaxa.408.2.1.Search in Google Scholar

Nauer, F., Gurgel, C.F.D., Ayres-Ostrock, L.M., Plastino, E.M., and Oliveira, M.C. (2019b). Phylogeography of the Hypnea musciformis species complex (Gigartinales, Rhodophyta) with the recognition of cryptic species in the western Atlantic Ocean. J. Phycol. 55: 676–687, https://doi.org/10.1111/jpy.12848.Search in Google Scholar PubMed

Nauer, F., Jesus, P.B., Cassano, V., Nunes, J.M.C., Schnadelbach, A.S., and Oliveira, M.C. (2019c). A taxonomic review of the genus Hypnea (Gigartinales, Rhodophyta) in Brazil based on DNA barcode and morphology. Rev. Bras. Bot. 42: 561–574, https://doi.org/10.1007/s40415-019-00544-z.Search in Google Scholar

Oliveira, E.C. (1998). The seaweed resources of Brazil. In: Critchley, A.T. and Ohno, M. (Eds.), Seaweed resources of the world. Yokosuka, Japan: Japan International Cooperation Agency, pp. 366–371.Search in Google Scholar

Pearce, A.S. and Williams, L.G. (1951). The biota of the reefs off the Carolinas. J. Elisha Mitchell Sci. Soc. 67: 133–161, https://doi.org/10.1038/168133b0.Search in Google Scholar

Saunders, G.W. (2005). Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360: 1879–1888, https://doi.org/10.1098/rstb.2005.1719.Search in Google Scholar PubMed PubMed Central

Saunders, G.W. and McDevit, D.C. (2012). Acquiring DNA sequence data from dried archival red algae (Florideophyceae) for the purpose of applying available names to contemporary genetic species: a critical assessment. Botany 90: 191–203, https://doi.org/10.1139/b11-079.Search in Google Scholar

Schneider, C.W. (1976). Spatial and temporal distributions of benthic marine algae on the continental shelf of the Carolinas. Bull. Mar. Sci. 26: 133–151.Search in Google Scholar

Schneider, C.W. and Searles, R.B. (1976). North Carolina marine algae. VII. New species of Hypnea and Petroglossum (Rhodophyta, Gigartinales) and additional records of other Rhodophyta. Phycologia 15: 51–60, https://doi.org/10.2216/i0031-8884-15-1-51.1.Search in Google Scholar

Schneider, C.W. and Searles, R.B. (1991). Seaweeds of the southeastern United States: Cape Hatteras to Cape Canaveral. Durham and London: Duke University Press.Search in Google Scholar

Searles, R.B. and Schneider, C.W. (1980). Biogeographic affinities of the shallow and deep water benthic marine algae of North Carolina. Bull. Mar. Sci. 30: 732–736.Search in Google Scholar

Soares, L.P. and Fujii, M.T. (2020). Molecular assessment of flat Cystocloniaceae (Gigartinales, Rhodophyta) from Brazil with reinstatement of Calliblepharis jolyi and a new record of C. saidana for the Atlantic Ocean. Phytotaxa 439: 243–254, https://doi.org/10.11646/phytotaxa.439.3.6.Search in Google Scholar

Stamatakis, A., Ludwig, T., and Meier, H. (2005). RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456–463, https://doi.org/10.1093/bioinformatics/bti191.Search in Google Scholar PubMed

Taylor, W.R. (1960). Marine algae of the Eastern tropical and subtropical coast of the Americas. Ann Arbor, MI: The University of Michigan Press.Search in Google Scholar

Tsiamis, K. and Verlaque, M. (2011). A new contribution to the alien red macroalgal flora of Greece (Eastern Mediterranean) with emphasis on Hypnea species. Cryptogam. Algol. 32: 393–410, https://doi.org/10.7872/crya.v32.iss4.2011.393.Search in Google Scholar

Tsuda, R.T. and Abbott, I.A. (1985). Collecting, handling, preservation, and logistics. In: Littler, M.M. and Littler, D.S. (Eds.), Handbook of phycological methods: ecological field methods: Macroalgae. Cambridge: Cambridge University Press, pp. 67–86.Search in Google Scholar

Verlaque, M., Ruitton, S., Boudouresque, C.F., and Mineur, F. (2015). Macrophytes. In: Briand, F. (Ed.), CIESM Atlas of exotic species in the Mediterranean, Vol. 4. Monaco: CIESM Publishers, pp. 1–364.Search in Google Scholar

Womersley, H.B.S. (1994). The Marine Benthic Flora of Southern Australia, Part III A, Bangiophyceae and Florideo phyceae (Acrochaetiales, Nemaliales, Gelidiales, Hilden brandiales and Gigartinales sensu lato). Canberra: Australian Biological Resources Study.Search in Google Scholar

Wynne, M.J. (2011). A checklist of benthic marine algae of the tropical and subtropical western Atlantic: third revision. Nova Hedwigia Beih 140: 1–166.Search in Google Scholar

Yang, M.Y. and Kim, M.S. (2017). Molecular analyses and reproductive structure to verify the generic relationships of Hypnea and Calliblepharis (Cystocloniaceae, Gigartinales), with proposal of C. saidana comb. nov. Algae 32: 87–100, https://doi.org/10.4490/algae.2017.32.5.15.Search in Google Scholar

Zemke-White, W.L. and Ohno, M. (1999). World seaweed utilisation: an end-of-century summary. J. Appl. Phycol. 11: 369–376, https://doi.org/10.1023/a:1008197610793.10.1023/A:1008197610793Search in Google Scholar


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/bot-2021-0067).


Received: 2021-07-13
Accepted: 2021-11-24
Published Online: 2021-12-23
Published in Print: 2022-02-23

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