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Red algal parasites: a synopsis of described species, their hosts, distinguishing characters and areas for continued research

  • Maren Preuss

    Maren Preuss is interested in evolution, taxonomy and systematics of red algae and especially of red algal parasites. She is a PhD candidate at Victoria University of Wellington in New Zealand under the supervision of Dr. Giuseppe Zuccarello and Dr. Wendy Nelson.

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    , Wendy A. Nelson

    Wendy A. Nelson specialises in marine phycology, particularly the biosystematics of macroalgae of New Zealand, with research on floristics, evolution and phylogeny, as well as ecology and life history studies. Recently she has worked on the systematics and biology of red algae including corallines, distribution and diversity of seaweeds of the New Zealand region, including the Ross Sea and the Balleny Islands. Wendy leads NIWA’s biosystematics research team and holds a joint appointment as a Professor at the University of Auckland in the School of Biological Sciences.

    and Giuseppe C. Zuccarello

    Giuseppe C. Zuccarello is interested in the taxonomy, evolution and speciation of algae. His research has focussed on mangrove-associated red algae of the genus Bostrychia and Caloglossa. He received a PhD degree from the University of California Berkeley. He has been president of the International Phycological Society and is currently an Associate Professor at Victoria University of Wellington and has published over 120 peer-reviewed papers.

Published/Copyright: January 26, 2017

Abstract

Red algal parasites are diverse organisms that are unusual due to the fact that many are closely related to their hosts. Parasitism has developed many times within different red algal groups, but the full extent of parasite biodiversity is unknown, as parasites are easily overlooked due to their small size and often low abundance. Additionally, the literature on red algal parasites is dispersed and has not been compiled in over 30 years. Although criteria have been proposed to define what constitutes a red algal parasite, many parasites are poorly described, and the cellular interactions with their host are poorly known. A few studies have demonstrated that parasites transfer organelles to host cells, which can alter the physiology of the host to the benefit of the parasite. Here, we apply a set of defining criteria for parasites to a compiled list of all described red algal parasites. Our results highlight the lack of knowledge of many key parasitic processes including early parasite development, host cell “control”, and parasite origin. Until the biology of more parasites is studied, generalisations on the processes of parasitism in red algae may be premature. We hope this synopsis will stimulate research into this fascinating group.

About the authors

Maren Preuss

Maren Preuss is interested in evolution, taxonomy and systematics of red algae and especially of red algal parasites. She is a PhD candidate at Victoria University of Wellington in New Zealand under the supervision of Dr. Giuseppe Zuccarello and Dr. Wendy Nelson.

Wendy A. Nelson

Wendy A. Nelson specialises in marine phycology, particularly the biosystematics of macroalgae of New Zealand, with research on floristics, evolution and phylogeny, as well as ecology and life history studies. Recently she has worked on the systematics and biology of red algae including corallines, distribution and diversity of seaweeds of the New Zealand region, including the Ross Sea and the Balleny Islands. Wendy leads NIWA’s biosystematics research team and holds a joint appointment as a Professor at the University of Auckland in the School of Biological Sciences.

Giuseppe C. Zuccarello

Giuseppe C. Zuccarello is interested in the taxonomy, evolution and speciation of algae. His research has focussed on mangrove-associated red algae of the genus Bostrychia and Caloglossa. He received a PhD degree from the University of California Berkeley. He has been president of the International Phycological Society and is currently an Associate Professor at Victoria University of Wellington and has published over 120 peer-reviewed papers.

Acknowledgements

We thank E. K. Ganesan, Yuki Masuda, Narongrit Muangmai, Reinhard Schnetter, Marc Verlaque, and Michael Wynne for publications. We thank two anonymous reviewers and Matt Dring for helpful comments on the manuscript.

References

Abbott, I.A. and G.J. Hollenberg. 1992. Marine algae of California. Stanford University Press, Stanford, California. pp. 844.10.1515/9781503621053Search in Google Scholar

Adey, W.H. and C.P. Sperapani. 1971. The biology of Kvaleya epilaeve, a new parasitic genus and species of Corallinaceae. Phycologia10: 29–42.10.2216/i0031-8884-10-1-29.1Search in Google Scholar

Adey, W.H., T. Masaki and H. Akioka. 1974. Ezo epiyessoense, a new parasitic genus and species of Corallinaceae (Rhodophyta, Cryptonemiales). Phycologia13: 329–344.10.2216/i0031-8884-13-4-329.1Search in Google Scholar

Adey, W.H., J.J. Hernandez-Kantun, G. Johnson, P.W. Gabrielson and M. Vis. 2015. DNA sequencing, anatomy, and calcification patterns support a monophyletic, subarctic, carbonate reef-forming Clathromorphum (Hapalidiaceae, Corallinales, Rhodophyta). J. Phycol.51: 189–203.10.1111/jpy.12266Search in Google Scholar PubMed

Apt, K.E. 1984a. The morphology of Phaeocolax kajimurai (Rhodomelaceae, Rhodophyta), a host specific epiphyte on Lobophora variegata (Phaeophyta). Phycologia23: 239–247.10.2216/i0031-8884-23-2-239.1Search in Google Scholar

Apt, K.E. 1984b. Effects of the symbiotic red alga Hypneocolax stellaris on its host Hypnea musciformis (Hypneaceae, Gigartinales). J. Phycol.20: 148–150.10.1111/j.0022-3646.1984.00148.xSearch in Google Scholar

Apt, K.E. 1987. A new species of Janczewskia (Rhodomelaceae, Rhodophyta) from the Hawaiian Islands. Phycologia 26: 328–333.10.2216/i0031-8884-26-3-328.1Search in Google Scholar

Apt, K.E. and K.E. Schlech. 1998. Ululania stellata gen. et sp. nov. (Rhodomelaceae), a new genus and species of parasitic red algae from Hawaii. Phycologia37: 157–161.10.2216/i0031-8884-37-3-157.1Search in Google Scholar

Ashen, J.B. and L.J. Goff. 1998. Galls on the marine red alga Prionitis lanceolata (Halymeniaceae): Specific induction and subsequent development of an algal-bacterial symbiosis. Am. J. Bot. 85: 1710–1721.10.2307/2446505Search in Google Scholar

Baardseth, E. 1946. The marine algae of Tristan da Cunha. In: (E. Christophersen, ed) Results of the Norwegian scientific expedition to Tristan da Cunha 1937–1938. DetNorske Videnskaps-Akademi, Oslo. pp. 1–173.Search in Google Scholar

Batters, E.A.L. 1892. Gonimophyllum buffhami: a new marine alga. J. Bot.30: 65–67.Search in Google Scholar

Batters, E.A.L. 1895. On some new British marine algae. Ann. Bot.9: 307–321.10.1093/oxfordjournals.aob.a090740Search in Google Scholar

Blouin, N.A. and C.E. Lane. 2012. Red algal parasites: Models for a life history evolution that leaves photosynthesis behind again and again. Bioessays34: 226–235.10.1002/bies.201100139Search in Google Scholar PubMed

Blouin, N.A. and C.E. Lane. 2016. Red algae provide fertile ground for exploring parasite evolution. Perspect. Phycol.1: 11–19.10.1127/pip/2015/0027Search in Google Scholar

Boo, G-H., W.A. Nelson, M. Preuss, J-Y. Kim and S-M. Boo. 2015. Genetic segregation and differentiation of a common subtidal alga Pterocladia lucida (Gelidiales, Rhodophyta) between Australia and New Zealand. J. Appl. Phycol.28: 2027–2034.10.1007/s10811-015-0699-xSearch in Google Scholar

Børgesen, F. 1920. The marine algae of the Danish West Indies. Dansk Botanisk Arkiv, Copenhagen. pp. 520.Search in Google Scholar

Bula-Meyer, G. 1985. Champiocolax sarae gen. et sp. nov., an adelphohemiparasite of the Champiaceae (Rhodymeniales, Rhodophyta). Phycologia24: 429–435.10.2216/i0031-8884-24-4-429.1Search in Google Scholar

Chang, C.F. and B.M. Xia. 1978. Studies on the parasitic red algae of China (in Chinese). Studia Marina Sinica14: 119–127.Search in Google Scholar

Clayden, S.L. and G.W. Saunders. 2010. Recognition of Rubrointrusa membranacea gen. et comb. nov., Rhodonematella subimmersa gen. et comb. nov (with a reinterpretation of the life history) and the Meiodiscaceae fam. nov within the Palmariales (Rhodophyta). Phycologia49: 283–300.10.2216/PH09-43.1Search in Google Scholar

Cribb, T.H., R.A. Bray, T. Wright and S. Pichelin. 2002. The trematodes of groupers (Serranidae: Epinephelinae): knowledge, nature and evolution. Parasitology124: S23–S42.10.1017/S0031182002001671Search in Google Scholar

D’Archino, R., W.A. Nelson, M.Y. Yang and M.S. Kim. 2015. New record of Hypnea flexicaulis in New Zealand and description of Calliblepharis psammophilus sp. nov. Bot. Mar.58: 485–497.10.1515/bot-2015-0053Search in Google Scholar

D’Archino, R., S-M. Lin, P.W. Gabrielson and G.C. Zuccarello. 2016. How one species in New Zealand, Pugetia delicatissima (Kallymeniaceae, Rhodophyta), can become two new genera, Wendya gen. nov. and Judithia gen. nov. Eur. J. Phycol.51: 83–98.10.1080/09670262.2015.1104557Search in Google Scholar

Dalen, J. and W.A. Nelson. 2013. Te Papa’s list of New Zealand marine macroalgae Rhodophyta. Museum of New Zealand Te Papa Tongarewa, Wellington, New Zealand. https://collections.tepapa.govt.nz.Search in Google Scholar

Dawson, E.Y. 1945. Notes on pacific coast marine algae. III. Madroño8: 93–97.Search in Google Scholar

Delivopoulos, S.G. and B.E. Diannelidis. 1990. Ultrastructure of carposporophyte development in the red alga Caulacanthus ustulatus (Gigartinales: Caulacanthaceae). Mar. Bio.106: 145–152.10.1007/BF02114685Search in Google Scholar

De Oliveira-Filho, E.C. and Y. Ugadim. 1973. Levringiella polysiphoniae a new species of parasitic red algae (Rhodophyta, Rhodomelaceae). Bol. Inst. Bot.1: 95–99.10.11606/issn.2316-9052.v1i0p95-99Search in Google Scholar

Diaz-Tapia, P. and I. Bárbara. 2013. Seaweeds from sand-covered rocks of the Atlantic Iberian Peninsula. Part 1. The Rhodomelaceae (Ceramiales, Rhodophyta). Cryptogam., Algol. 34: 325–422.10.7872/crya.v34.iss4.2013.325Search in Google Scholar

Dixon, P.S. and L.M. Irvine. 1995. Seaweeds of the British Isles. Volume 1. Rhodophyta. Part 1. Introduction, Nemaliales, Gigartinales. London Natural History Museum, London.Search in Google Scholar

Dobson, A., K.D. Lafferty, A.M. Kuris, R.F. Hechinger and W. Jetz. 2008. Homage to Linnaeus: How many parasites? How many hosts? Proc. Natl. Acad. Sci. USA105: 11482–11489.10.1073/pnas.0803232105Search in Google Scholar PubMed PubMed Central

Edelstein, T. 1972. Halosacciocolax lundii, sp. nov., a new red alga parasitic on Rhodymenia palmata (L.) Grev. Brit. Phycol. J.7: 249–253.10.1080/00071617200650251Search in Google Scholar

Evans, L.V., J.A. Callow and M.E. Callow. 1973. Structural and physiological studies on the parasitic red alga Holmsella. New Phytol.72: 393–402.10.1111/j.1469-8137.1973.tb02047.xSearch in Google Scholar

Evans, L.V., J.A. Callow and M.E. Callow. 1978. Parasitic red algae: an appraisal. In: (D.E.G. Irvine and J.G. Price, eds) Modern approaches to the taxonomy of red and brown algae. Academic Press, London and New York. pp. 87–109.Search in Google Scholar

Fan, K.C. and G.F. Papenfuss. 1959. Red algal parasites occurring on members of the Gelidiales. Madroño15: 33–38.Search in Google Scholar

Feldmann, J. and G. Feldmann. 1961. Une nouvelle espèce de Delesseriacée adelphoparasite: gonimocolax roscoffensis nov. sp. Bull. Soc. Bot. France108: 18–24.10.1080/00378941.1961.10837987Search in Google Scholar

Feldmann, J. and G. Feldmann. 1963. Une nouvelle espèce de Floridée parasite du genre Gelidiocolax Gardner. Revue Générale de Botanique70: 557–571.Search in Google Scholar

Fredericq, S. and M.H. Hommersand. 1990. Morphology and Systematics of Holmsella pachyderma (Pterocladiophilaceae, Gracilariales). Brit. Phycol. J.25: 39–51.10.1080/00071619000650041Search in Google Scholar

Ganesan, E.K. 1970. A new species of Gelidiocolax Gardner (Choreocolacaceae, Rhodophyta) from the Caribbean Sea. Bol. Inst. Oceanogr. Univ. Oriente9: 93–102.Search in Google Scholar

Gerung, G.S. and H. Yamamoto. 2002. The taxonomy of parasitic genera growing on Gracilaria (Rhodophyta, Gracilariaceae). In: (I.A. Abbott and K.J. McDermid, eds) Taxonomy of economic seaweeds with reference to some Pacific species. Vol. VIII. California Sea Grant College, La Jolla. pp. 209–213.Search in Google Scholar

Goff, L.J. 1976. The biology of Harveyella mirabilis (Cryptonemiales; Rhodophyceae). V. Host responses to parasite infection. J. Phycol.12: 313–328.10.1111/j.0022-3646.1976.00313.xSearch in Google Scholar

Goff, L.J. 1982. The biology of parasitic red algae. In: (F.E. Round and D.J. Chapman, eds) Progress in phycological research. Elsevier Biomedical Press, Amsterdam. pp. 289–369.Search in Google Scholar

Goff, L.J. and A.W. Coleman. 1985. The role of secondary pit connections in red algal parasitism. J. Phycol.21: 483–508.10.1111/j.0022-3646.1985.00483.xSearch in Google Scholar

Goff, L.J. and A.W. Coleman. 1987. Nuclear transfer from parasite to host. A new regulatory mechanism. Endocytobiology503: 402–423.10.1111/j.1749-6632.1987.tb40626.xSearch in Google Scholar

Goff, L.J. and A.W. Coleman. 1995. Fate of parasite and host organelle DNA during cellular-transformation of red algae by their parasites. Plant Cell7: 1899–1911.10.2307/3870197Search in Google Scholar

Goff, L.J. and G.C. Zuccarello. 1994. The evolution of parasitism in red algae – Cellular interactions of adelphoparasites and their hosts. J. Phycol.30: 695–720.10.1111/j.0022-3646.1994.00695.xSearch in Google Scholar

Goff, L.J., D.A. Moon, P. Nyvall, B. Stache, K. Mangin and G.C. Zuccarello. 1996. The evolution of parasitism in the red algae: molecular comparisons of adelphoparasites and their hosts. J. Phycol. 32: 297–312.10.1111/j.0022-3646.1996.00297.xSearch in Google Scholar

Goff, L.J., J. Ashen and D. Moon. 1997. The evolution of parasites from their hosts: a case study in the parasitic red algae. Evolution51: 1068–1078.10.1111/j.1558-5646.1997.tb03954.xSearch in Google Scholar PubMed

Graham, L.E. and L.W. Wilcox. 2000. Algae. Upper Saddle River, Prentice-Hall Inc. pp. 640.Search in Google Scholar

Gregory, B.D. 1930. New light on the so-called parasitism of Accinococcus aggregatus, Kütz, and Sterrocolax decipiens, Schmitz. Ann. Bot.44: 767–769.10.1093/oxfordjournals.aob.a090246Search in Google Scholar

Guiry, M.D. 2012. How many species of algae are there? J. Phycol.48: 1057–1063.10.1111/j.1529-8817.2012.01222.xSearch in Google Scholar PubMed

Guiry, M.D. and G.M. Guiry. 2016. Algaebase. World-electronic publication, National University of Ireland, Galway. https://www.algaebase.org.Search in Google Scholar

Guiry, M.D. and O.N. Selivanova. 2007. Masakiella, nom. nov. pro Masakia N.G. Klochkova (Corallinaceae, Rhodophyta), non Masakia (Nakai) Nakai (Celastraceae, Tracheophyta). Phycologia46: 235–236.10.2216/06-37.1Search in Google Scholar

Hancock, L., L. Goff and C. Lane. 2010. Red algae lose key mitochondrial genes in response to becoming parasitic. Genome. Biol. Evol.2: 897–910.10.1093/gbe/evq075Search in Google Scholar PubMed PubMed Central

Harvey, W.H. and J.D. Hooker. 1845. Algae L. In: (J.D. Hooker, ed) The botany of the Antarctic voyage of H.M. discovery ships Erebus and Terror in the Years 1839–1843: under the command of Captain Sir James Clark Ross. Reeve Brothers, London. pp. 175–193.Search in Google Scholar

Harvey, A.S., S.T. Broadwater, W.J. Woelkerling and P.J. Mitrovski. 2003. Choreonema (Corallinales, Rhodophyta): 18s rDNA phylogeny and resurrection of the Hapalidiaceae for the subfamilies Choreonematoideae, Austrolithoideae, and Melobesioideae. J. Phycol.39: 988–998.10.1046/j.1529-8817.2003.02158.xSearch in Google Scholar

Hollenberg, G.J. 1970. Phycological notes IV, including new marine algae and new records for California. Phycologia9: 61–72.10.2216/i0031-8884-9-1-61.1Search in Google Scholar

Hudson, P.J., A.P. Dobson and D. Newborn. 1998. Prevention of population cycles by parasite removal. Science282: 2256–2258.10.1126/science.282.5397.2256Search in Google Scholar PubMed

Joly, A.B. 1966. Centrocerocolax, a new parasitic genus of Rhodophyta. Rickia2: 73–77.Search in Google Scholar

Joly, A.B. and E.C. de Oliveira. 1966. Spyridiocolax and Heterodasya two new genera of the Rhodophyceae. Sellowia18: 115–125.Search in Google Scholar

Joly, A.B. and N. Yamaguishi-Tomita. 1969. Note on Dawsoniella Joly & Yamaguishi-Tomita. Rickia4: 209–210.Search in Google Scholar

Karvonen, A. and O. Seehausen. 2012. The role of parasitism in adaptive radiations- When might parasites promote and when might they constrain ecological speciation? Acta. Oecol.2012: 1–20.10.1155/2012/280169Search in Google Scholar

Keeling, P.J. and J.C. Rayner. 2015. The origins of malaria: there are more things in heaven and earth. Parasitology142: 16–25.10.1017/S0031182014000766Search in Google Scholar PubMed PubMed Central

Kim, M-S. and G-Y. Cho. 2010. A new red algal parasite, Symphycolax koreana gen. et. sp. nov. (Rhodomelaceae, Ceramiales), from Korea. Algae25: 105–113.10.4490/algae.2010.25.3.105Search in Google Scholar

Kraft, G.T. and I.A. Abbott. 2002. The anatomy of Neotenophycus ichthyosteus gen. et sp.nov. (Rhodomelaceae, Ceramiales), a bizarre red algal parasite from the central Pacific. Eur. J. Phycol.37: 269–278.10.1017/S0967026202003554Search in Google Scholar

Kraft, G.T. and P.W. Gabrielson. 1983. Tikvahiella candida gen. et sp. nov. (Solieriaceae, Rhodophyta), a new adelphoparasite from southern Australia. Phycologia22: 47–57.10.2216/i0031-8884-22-1-47.1Search in Google Scholar

Kugrens, P. 1982. Leachiella pacifica, gen. et sp. nov., a new parasitic red alga from Washington and California. Am. J. Bot.69: 306–319.10.1002/j.1537-2197.1982.tb13261.xSearch in Google Scholar

Kugrens, P. and S.G. Delivopoulos. 1985. Ultrastructure of auxiliary and gonimoblast cells during carposporophyte development in Faucheocolax attenuata (Rhodophyta). J.Phycol.21: 240–249.10.1111/j.0022-3646.1985.00240.xSearch in Google Scholar

Kurihara, A., T. Abe, M. Tani and A.R. Sherwood. 2010. Molecular phylogeny and evolution of red algal parasites: a case study of Benzaitenia, Janczewskia, and Ululania (Ceramiales). J. Phycol. 46: 580–590.10.1111/j.1529-8817.2010.00834.xSearch in Google Scholar

Kylin, H. 1941. Californische Rhodophyceen. Lunds Universitets Årsskrift, Lund. pp. 47.Search in Google Scholar

Kylin, H. 1956. Die Gattungen der Rhodophyceen. CWK Gleerups Förlag, Lund. pp. 673.Search in Google Scholar

Kylin, H. and C. Skottsberg. 1919. Zur Kenntnis der subantarktischen und antarktischen Meeresalgen. II. Rhodophyceen. PA Norstedt, Stockholm. pp. 1–88.Search in Google Scholar

Lee, I.K. and M. Kurogi. 1978. Neohalosacciocolax aleutica gen. et sp. nov. (Rhodophyta), parasitic on Halosaccion minjaii I. K. Lee from the North Pacific. Brit. Phycol. J.13: 131–139.10.1080/00071617800650141Search in Google Scholar

Le Gall, L. and G.W. Saunders. 2010. DNA barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J. Phycol. 46: 374–389.10.1111/j.1529-8817.2010.00807.xSearch in Google Scholar

Le Roux, L.E. and A. Avenant-Oldewage. 2010. Checklist of the fish parasitic genus Cichlidogyrus (Monogenea), including its cosmopolitan distribution and host species Afr. J. Aquat. Sci.35: 21–36.10.2989/16085914.2010.466632Search in Google Scholar

Levring, T. 1941. Die Meeresalgen der Juan Fernandez-Inseln. Die Corallinaceen der Juan Fernandez-Inseln. In: (C. Skottsberg, ed) The natural history of Juan Fernandez and Easter Island. Almqvist & Wiksells Boktryckeri, Uppsala. pp. 601–670.Search in Google Scholar

Maggs, C.A. and M.H. Hommersand. 1993. Seaweeds of the British Isles. Volume 1. Rhodophyta. Part 3A. Ceramiales. Pelagic Publishing Ltd., London. pp. 464.Search in Google Scholar

Martin, M.T. and M.A. Pocock. 1953. South African parasitic Florideae and their hosts. 2. Some South African parasitic Florideae. J. Linn. Soc. Bot.55: 48–64.10.1111/j.1095-8339.1953.tb00003.xSearch in Google Scholar

McBride, D.L., P. Kugrens and J.A. West. 1974. Light and electron microscopic observations on red algal galls. Protoplasma79: 249–264.10.1007/BF01276605Search in Google Scholar PubMed

McCandless, E.L. and C.M. Vollmer. 1984. The nemathecium of Gymnogongrus chiton (Rhodophyceae, Gigartinales): immunochemical evidence of meiosis. Phycologia23: 119–123.10.2216/i0031-8884-23-2-119.1Search in Google Scholar

McFadden, M.E. 1911. On a Colacodasya from southern California. Univ. Calif.Publ. Bot.4: 143–150.Search in Google Scholar

Melchionna, M. and F. De Masi. 1977. The fine structure of the vegetative cells of Erythrocystis montagnei, a symbiotic red alga. Cytobios20: 113–119.Search in Google Scholar

Morrill, J. 1976a. Notes on parasitic Rhodomelaceae, III: Meridiocolax narcissus, a new red alga parasitic on Polysiphonia ferulacea Suhr from the Florida Keys. Proc. Acad. Nat. Sci. Philadelphia127: 233–248.Search in Google Scholar

Morrill, J. 1976b. Notes on parasitic Rhodomelaceae, II: The morphology and systematic position of the parasitic red alga Jantinella verrucaeformis (Setchell and McFadden) Kylin. Proc. Acad. Nat. Sci. Philadelphia127: 217–231.Search in Google Scholar

Morrill, J. 1977. Notes on parasitic Rhodomelaceae, IV: Dipterocolax fernandezianum, a new genus parasitizing Dipterosiphonia parva from the Juan Fernández Islands. Proc. Acad. Nat. Sci. Philadelphia128: 133–146.Search in Google Scholar

Nelson, W.A., J.E. Sutherland, T.J. Farr, D.R. Hart, K.F. Neill, H.J. Kim, H.S. Yoon and P.W. Gabrielson. 2015. Multi-gene phylogenetic analyses of New Zealand coralline algae: Corallinapetra novaezelandiae gen. et sp. nov. and recognition of the Hapalidiales ord. nov. J. Phycol.51: 454–468.10.1111/jpy.12288Search in Google Scholar PubMed

Ng, P-K., P-E. Lim, A. Kato and S-M. Phang. 2013. Molecular evidence confirms the parasite Congracilaria babae (Gracilariaceae, Rhodophyta) from Malaysia. J. Appl. Phycol.26: 1287–1300.10.1007/s10811-013-0166-5Search in Google Scholar

Ng, P-K., P-E. Lim and S-M. Phang. 2014. Radiation of the red algal parasite Congracilaria babae onto a secondary host species, Hydropuntia sp. (Gracilariaceae, Rhodophyta). PLoS One9: e97450.10.1371/journal.pone.0097450Search in Google Scholar PubMed PubMed Central

Ng, P-K., P-E. Lim and S-M. Phang. 2015. Small-scale genetic structure of Gracilaria salicornia and its red algal parasite, G. babae (Gracilariaceae, Rhodophyta), in Malaysia. Bot. Mar.58: 175–187.10.1515/bot-2014-0071Search in Google Scholar

Noble, J.M. and G.T. Kraft. 1983. Three new species of parasitic red algae (Rhodophyta) from Australia: Holmsella australis sp. nov., Meridiocolax bracteata sp. nov. and Trichidium pedicellatum gen. et sp. nov. Brit. Phycol. J.18: 391–413.10.1080/00071618300650381Search in Google Scholar

Nonomura, A.M. 1979. Development of Janczewskia morimotoi (Ceramiales) on its host Laurencia nipponica (Ceramiales, Rhodophyceae). J. Phycol.15: 154–162.10.1111/j.1529-8817.1979.tb02979.xSearch in Google Scholar

Nonomura, A.M. and J.A. West. 1979. Development of Janczewskia morimotoi (Ceramiales) on its host Laurencia nipponica (Ceramiales, Rhodopyceae). J. Phycol.15: 154–162.10.1111/j.1529-8817.1979.tb02979.xSearch in Google Scholar

Norris, R.E. 1988. Two new red algal parasites on Kuetzingia natalensis (Rhodomelaceae, Rhodophyta). Bot. Mar.31: 345–352.10.1515/botm.1988.31.4.345Search in Google Scholar

Norris, R.E. and M.J. Wynne. 1969. Notes on marine algae of Washington and southern British Columbia. III. Madroño1: 133–146.Search in Google Scholar

Ouahi, M. 1993. Contribution à l’étude biologique, systématique, phénologique et écologique du Gelidiocolax verruculata sp. nov., parasite des Gélidiacées du littoral marocain: station de Mohammedia (unpublished doctoral thesis) Université Mohammed V, Rabat, Morocco. pp. 101.Search in Google Scholar

Phillips, L.E. 2000. Taxonomy of the New Zealand-endemic genus Pleurostichidium (Rhodomelaceae, Rhodophyta). J. Phycol.36: 773–786.10.1046/j.1529-8817.2000.99134.xSearch in Google Scholar

Pocock, M.A. 1953. South African parasitic Florideae and their hosts. 1. Four members of the Rhodomelaceae which act as hosts for parasitic Florideae. J. Linn. Soc. Bot. 55: 34–47.10.1111/j.1095-8339.1953.tb00002.xSearch in Google Scholar

Pocock, M.A. 1956. South African parasitic Florideae and their hosts: 3. Four minute parasitic Florideae. Proc. Linn. Soc. Lond.167: 11–41.10.1111/j.1095-8312.1956.tb00764.xSearch in Google Scholar

Poulin, R. 1995. “Adaptive” changes in the behaviour of parasitized animals: a critical review. Int. J. Parasitol.25: 1371–1383.10.1016/0020-7519(95)00100-XSearch in Google Scholar

Preuss, M. and G.C. Zuccarello. 2014. What’s in a name? Monophyly of genera in the red algae: Rhodophyllis parasitica sp. nov. (Gigartinales, Rhodophyta); a new red algal parasite from New Zealand. Algae29: 279–288.10.4490/algae.2014.29.4.279Search in Google Scholar

Quandt, C.A., K.E. Bushley and J.W. Spatafora. 2015. The genome of the truffle-parasite Tolypocladium ophioglossoides and the evolution of antifungal peptaibiotics. BMC Genomics16: 553.10.1186/s12864-015-1777-9Search in Google Scholar PubMed PubMed Central

Reinsch, P.F. 1875. Contributiones ad algologiam et fungologiam. Vol. 1. Lipsiae, T.OWeigel. pp. 422.10.5962/bhl.title.49697Search in Google Scholar

Reinsch, P.F. 1890. Zur Meeresalgenflora von Süd-Georgien. In: (G. Neumayer, ed) Die internationale Polarforschung 18821883: Geschichtlicher Theil und in einem Anhange mehrere einzelne Abhandlungen physikalischen und sonstigen Inhalts. Verlag von A. Asher, Berlin. pp. 366–449.10.5962/bhl.title.64271Search in Google Scholar

Rosenvinge, L.K. 1931. The marine algae of Denmark; contributions to their natural history. Part IV. Rhodophyceae IV. (Gigartinales, Rhodymeniales, Nemastomatales). Det Kongelige Danske Videnskabernes Selskabs sjrifter, Naturvidenskabelig og., Kopenhagen. pp. 487–568.Search in Google Scholar

Salomaki, E.D. and C.E. Lane. 2014. Are all red algal parasites cut from the same cloth? Acta Soc. Bot. Pol. 83: 369–375.10.5586/asbp.2014.047Search in Google Scholar

Salomaki, E.D., K.R. Nickles and C.E. Lane. 2015. The ghost plastid of Choreocolax polysiphoniae. J. Phycol. 51: 217–221.10.1111/jpy.12283Search in Google Scholar PubMed

Saunders, G.W. and S.L. Clayden. 2010. Providing a valid epithet for the species widely known as Halosacciocolax kjellmanii S. Lund (Palmariales, Rhodophyta) – Rhodophysema kjellmanii sp. nov. Phycologia49: 628–628.10.2216/0031-8884-49.6.628Search in Google Scholar

Saunders, G.W. and B. McDonald. 2010. DNA barcoding reveals multiple overlooked Australian species of the red algal order Rhodymeniales (Florideophyceae), with resurrection of Halopeltis J. Agardh and description of Pseudohalopeltis gen. nov. Botany88: 639–667.10.1139/B10-038Search in Google Scholar

Saunders, G.W., A. Chiovitti and G.T. Kraft. 2004. Small-subunit rDNA sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 3. Delineating the Gigartinales sensu stricto. Can. J. Bot. 82: 43–74.10.1139/b03-110Search in Google Scholar

Schmitz, F. and P. Falkenberg. 1897. Rhodomelaceae. In: (A. Engler and K. Prantl, eds) Die natürlichen Pflanzenfamilien nebst ihren Gattungen und wichtigeren Arten insbesondere den Nutzpflanzen unter Mitwirkung zahlreicher hervorragender Fachgelehrten. Verlag von Wilhelm Engelmann, Leipzig. pp. 421–480.Search in Google Scholar

Schneider, C.W. and M.J. Wynne. 2007. A synoptic review of the classification of red algal genera a half century after Kylin’s “Die Gattungen der Rhodophyceen”. Bot. Mar.50: 197–249.10.1515/BOT.2007.025Search in Google Scholar

Schneider, C.W. and M.J. Wynne. 2013. Second addendum to the synoptic review of red algal genera. Bot. Mar.56: 111–118.10.1515/bot-2012-0235Search in Google Scholar

Schnetter, R., U. Richter, A. Schmesmer and G. Bula-Meyer. 1983. Licht- und elektronenmikroskopische Untersuchungen an Grateloupiocolax colombiana gen. et spec. nov. (Halymeniaceae, Rhodophyceae). Beitr. Biol. Pflanzen58: 77–94.Search in Google Scholar

Seoane-Camba, J.A. 1982. Sobre una rodofícea parásita de Gelidiáceas. Collect. Bot.13: 911–918.Search in Google Scholar

Setchell, W.A. 1914. Parasitic Florideae, I. Univ.Calif. Publ. Bot.6: 1–34.Search in Google Scholar

Setchell, W.A. 1918. Parasitism among the red algae. P. Am. Philos. Soc.57: 155–172.Search in Google Scholar

Setchell, W.A. 1923. Parasitic Florideae, II. Univ. Calif. Publ. Bot.10: 393–401.Search in Google Scholar

Setchell, W.A. and N.L. Gardner. 1924. New marine algae from the Gulf of California. Proc.Calif. Acad. Sci.12: 695–949.Search in Google Scholar

Setchell, W.A. and N.L. Gardner. 1930. Marine algae of the Revillagigedo Islands Expedition in 1925. Proc. Calif. Acad. Sci.4: 109–215.Search in Google Scholar

Sherwood, A.R., A. Kurihara, K.Y. Conklin, T. Sauvage and G.G. Presting. 2010. The Hawaiian Rhodophyta Biodiversity Survey (2006–2010): a summary of principal findings. BMC Plant Biol. 10: 258.10.1186/1471-2229-10-258Search in Google Scholar

Silva, P.C., P.W. Basson and R.L. Moe. 1996. Catalogue of the benthic marine algae of the Indian Ocean. University of California Press.Search in Google Scholar

Skottsberg, C. 1953. On two collections of Antarctic marine algae. Arkiv für Botanik2: 531–566.Search in Google Scholar

Sparling, S.R. 1957. The structure and reproduction of some members of the Rhodymeniaceae (doctoral thesis). Univ. Calif. Publ. Bot. Berkeley, USA. 29: 319–396.Search in Google Scholar

Tanaka, T. and Y. Nozawa. 1960. One red algal parasite from Japan. Mem. Fac. Fish. Kagoshima Univ. 9: 107–112.Search in Google Scholar

Tokida, J. 1934. Phycological observations. I. Trans Sapporo Nat. Hist. Soc.13: 196–202.Search in Google Scholar

Tokida, J. 1947. Notes on some new or little known marine algae. J. Jpn. Bot.21: 127–130.Search in Google Scholar

Townsend, R.A. and J.M. Huisman. 2004. Epulo multipedes gen. et sp. nov. (Corallinaceae, Rhodophyta), a coralline parasite from Australia. Phycologia43: 288–295.10.2216/i0031-8884-43-3-288.1Search in Google Scholar

Vergés, A., C. Izquierdo and M. Verlaque. 2005. Rhodymeniocolax mediterraneus sp. nov. (Rhodymeniales, Rhodophyta), parasitic on Rhodymenia ardissonei from the western Mediterranean Sea. Phycologia44: 510–516.10.2216/0031-8884(2005)44[510:RMSNRR]2.0.CO;2Search in Google Scholar

Wagner, F.S. 1954. Contributions to the morphology of the Delesseriaceae. Univ. Calif. Publ. Bot.27: 279–346.Search in Google Scholar

Weber-van Bosse, A. 1923. Liste des algues du Siboga. III. Rhodophyceae. Seconde partie. Ceramiales. Siboga-Expeditie Monographie 59d, Leiden. pp. 311–392.Search in Google Scholar

Weber-van Bosse, A. 1928. Liste des algues du Siboga, IV. Rhodophyceae. Troisème partie. Gigartinales et Rhodymeniales et tableau de la distribution des Chlorophycées, Phaeophycées et Rhodophycées de l’Archipel Malaisien. Siboga-Expeditie Monographie 59d, Leiden. pp. 393–533.Search in Google Scholar

Westwood, J.H., J.I. Yoder, M.P. Timko and C.W. dePamphilis. 2010. The evolution of parasitism in plants. Trends Plant. Sci.15: 227–235.10.1016/j.tplants.2010.01.004Search in Google Scholar

Wilson, H.L. 1990. Gracilariophila a new parasite on Gracilaria confervoides. Univ. Calif. Publ. Bot.4: 75–85.Search in Google Scholar

Womersley, H.B.S. 1994. The marine benthic flora of southern Australia. Rhodophyta. Part IIIA, Bangiophyceae and Florideophyceae. Australian Biological Resources Study, Canberra and the State Herbarium of South Australia, Canberra. pp. 508.Search in Google Scholar

Womersley, H.B.S. 1996. The marine benthic flora of southern Australia. Rhodophyta. Part IIIB, Gracilariales, Rhodymeniales, Corallinales and Bonnemaisoniales. Australian Biological Resources Study, Canberra and the State Herbarium of South Australia, Canberra. pp. 392.Search in Google Scholar

Womersley, H.B.S. 1998. The marine benthic flora of southern Australia. Rhodophyta. Part IIIC, Ceramiales – Ceramiaceae, Dasyaceae. Australian Biological Resources Study, Canberra and the State Herbarium of South Australia, Canberra. pp. 535.Search in Google Scholar

Womersley, H.B.S. 2003. The marine benthic flora of Southern Australia, Rhodophyta, Part IIID, Ceramiales-Delesseriaceae, Sarcomeniaceae, Rhodomelaceae. Australian Biological Resources Study/State Herbarium of South Australia, Canberra. pp. 533.Search in Google Scholar

Wynne, M.J. 1970. Marine algae of Amchitka Island (Aleutian Islands). I. Delesseriaceae. Syesis 3: 95–144.Search in Google Scholar

Wynne, M.J. 2013. The red algal families Delesseriaceae and Sarcomeniaceae. Koeltz Scientific Books, Königsstein, Germany. pp. 326.Search in Google Scholar

Wynne, M.J. and J.N. Heine. 1992. Collections of marine red algae from St. Matthew and St. Lawrence Islands, the Bering Sea. Nova Hedwigia55: 55–97.Search in Google Scholar

Wynne, M.J. and C.W. Schneider. 2010. Addendum to the synoptic review of red algal genera. Bot. Mar. 53: 291–299.10.1515/BOT.2010.039Search in Google Scholar

Wynne, M.J. and C.W. Schneider. 2016. Third addendum to the synoptic review of red algal genera. Bot. Mar. 59: 397–404.10.1515/bot-2016-0096Search in Google Scholar

Wynne, M.J. and F. Scott. 1989. Pitycolax, a new genus of Adelphoparasitic red algae from Ile Amsterdam, Southern Indian Ocean. Cryptogam., Algol. 10: 23–32.Search in Google Scholar

Yamamoto, H. 1986. Congracilaria babae gen. et sp. nov. (Gracilariaceae), an adelphoparasite growing on Gracilaria salicornia of Japan. Bull. Fac. Fish. Hokkaido Univ.37: 281–290.Search in Google Scholar

Yang, M-Y. and M-S. Kim. 2015. Taxonomy of Grateloupia (Halymeniales, Rhodophyta) by DNA barcode marker analysis and a description of Pachymeniopsis volvita sp nov. J. Appl. Phycol. 27: 1373–1384.10.1007/s10811-014-0432-1Search in Google Scholar

Yoneshigue, Y. and E.C. de Oliveira 1984. Algae from Cabo-Frio upwelling area 2. Gelidiocolax pustulata (Gelidiaceae, Rhodophyta) – an unusual new putative parasitic species. J. Phycol.20: 440–443.10.1111/j.0022-3646.1984.00440.xSearch in Google Scholar

Yoshida, T. and H. Mikami. 1996. Sorellocolax stellaris gen. et sp. nov., a hemiparasitic alga (Delesseriaceae, Rhodophyta) from the east coast of Honshu, Japan. Phycol. Res.44: 125–128.10.1111/j.1440-1835.1996.tb00041.xSearch in Google Scholar

Zinova, A.D. 1963. Delesseriaceae apud Insulas Kerguelen et Macquarie. Academia Nauk. USSR, Leningrad.16: 52–67.Search in Google Scholar

Zinova, A.D. 1967. Opredelitel zelenikh, burikh i krasnich odoroslei juzhnikh morei SSSR. Academia Nauk. USSR, Leningrad. pp. 398.Search in Google Scholar

Zuccarello, G.C. 2008. A fungal gall of Catenella nipae (Caulacanthaceae, Rhodophyta) and a review of Catenellocolax leeuweni. Bot. Mar.51: 436–440.10.1515/BOT.2008.045Search in Google Scholar

Zuccarello, G.C. and J.A. West. 1994a. Comparative development of the red algal parasites Bostrychiocolax australis gen. et sp. nov. and Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). J. Phycol.30: 137–146.10.1111/j.0022-3646.1994.00137.xSearch in Google Scholar

Zuccarello, G.C. and J.A. West. 1994b. Genus and race specificity in the red algal parasite Leachiella pacifica (Choreocolacaceae, Rhodophyta). Phycologia33: 213–218.10.2216/i0031-8884-33-3-213.1Search in Google Scholar

Zuccarello, G.C. and J.A. West. 1994c. Host specificity on the red algal parasites Bostrychioclax australis and Dawsoniocolax bostrychiae (Choreocolacaceae, Rhodophyta). J. Phycol.30: 762–473.10.1111/j.0022-3646.1994.00462.xSearch in Google Scholar

Zuccarello, G.C. and J.A. West. 2006. Molecular phylogeny of the subfamily Bostrychioideae (Ceramiales, Rhodophyta): Subsuming Stictosiphonia and highlighting polyphyly in species of Bostrychia. Phycologica. 45: 24–36.10.2216/05-07.1Search in Google Scholar

Zuccarello, G.C., D. Moon and L.J. Goff. 2004. A phylogenetic study of parasitic genera placed in the family Choreocolacaceae (Rhodophyta). J. Phycol.40: 937–945.10.1111/j.1529-8817.2004.04029.xSearch in Google Scholar


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The online version of this article (DOI: 10.1515/bot-2016-0044) offers supplementary material, available to authorized users.


Received: 2016-5-25
Accepted: 2016-12-20
Published Online: 2017-1-26
Published in Print: 2017-2-1

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