Climate change confers a potential advantage to fleshy Antarctic crustose macroalgae over calcified species.

Journal of Experimental Marine Biology and Ecology

Volumn 474, Issue , 2016, Pages 58-66

  Schoenrock, Kathryn M ^a   Schram, Julie B ^a   Amsler, Charles D ^a   McClintock, James B ^a   Angus, Robert A ^a   Vohra, Yogesh K ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Antarctica; Climate change; Coralline algae; Hildenbrandia sp.; Ocean acidification; Warming

Indexed keywords

ACIDIFICATION; BENTHOS; CALCIUM CARBONATE; CARBON DIOXIDE; CHLOROPHYLL A; CLIMATE CHANGE; HIGH TEMPERATURE; MACROALGA; MICROCOSM; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE;

ANTARCTICA;

ALGAE; CLATHROMORPHUM; HILDENBRANDIA SP.; RHODOPHYTA;

EID: 84943797769     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2015.09.009     Document Type: Article

References (118)

1. Adey W.H., Halfar J., Williams B. The Coralline Genus Clathromorphum Foslie emend. Adey: Biological, Physiological, and Ecological Factors Controlling Carbonate Production in an Arctic-Subarctic Climate Archive. Smithsonian Contr. to the Mar. Sci. 2013, 40:1-41.
2. Amsler C.D., Rowley R.J., Laur D.R., Quetin L.B., Ross R.M. Vertical distribution of Antarctic peninsular macroalgae: cover, biomass, and species composition. Phycologia 1995, 34(5):424-430.
3. Andersson A.J., Mackenzie F.T., Bates N.R. Life on the margin: implications of ocean acidification on Mg-calcite, high latitude ad cold-water marine calcifiers. Mar. Ecol. Prog. Ser. 2008, 373:265-273.
4. Baggini C., Salomidi M., Voutsinas E., Bray L., Krasakopoulou E., Hall-Spencer J.M. Seasonality Affects Macroalgal Community Response to Increases in pCO2. PLoS One 2014, 9(9). 10.1371/journal.pone.0106520.
5. Bender D., Diaz-Pulido G., Dove S. Warming and acidification promote cyanobacterial dominance in turf algal assemblages. Mar. Ecol. Prog. Ser. 2014, 517:271-284.
6. Bjork M.M., Fransson A., Chierici M. Ocean acidification state in western Antarctic surface waters: drivers and interannual variability. Biogeosci. Discuss. 2013, 10:7879-7916.
7. Borowitzka M.A. Mechanisms in algal calcification. Prog. Phycol. Res. 1982, 1:137-177.
8. 2 world. Ecol. Evol. 2014, 4(13):2787-2798.
9. 2. Mar. Ecol. Prog. Ser. 2011, 441:79-87.
10. Burdett H.L., Keddie V., MacArthur N., McDowall L., McLeish J., Spielvogel E., Hatton A.D., Kamenos N.A. Dynamic photoinhibition exhibited by red coralline algae in the Red Sea. BMC Plant biology 2014, 14(1):139.
11. Caldeira K., Wickett M.E. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J. Geophys. Res. 2005, 110(C9):C09S04.
12. Chave K.E. Aspects of the biogeochemistry of magnesium 1. Calcareous marine organisms. J. Geol. 1954, (62):266-283.
13. Chenelot H., Jewett S.C., Hoberg M.K. Macrobenthos of the nearshore Aleutian Archipelago, with emphasis on invertebrates associated with Clathromorphum nereostratum (Rhodophyta, Corallinaceae). Mar. Biodivers. 2011, 41(3):413-424.
14. Clarke A., Murphy E., Meredith M., King J., Peck L., Barnes D., Smith R. Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2007, 367(1477):149-166.
15. 2 as a resource among competitors for ecosystem dominance. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 2013, 362:20120442.
16. Dayton P., Robilliard G., Paine R., Dayton L. Biological accommodation in the benthic community at McMurdo Sound. Antarctic. Ecol. Mon. 1974, 44(1):105-128.
17. Denman K., Christian J.R., Steiner N., Portner H., Nojiri Y. Potential impacts of future ocean acidification on marine ecosystems and fisheries: current knowledge and recommendation for future research. ICES J. Mar. Sci. 2011, 68(6):1019-1029.
18. 2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 2011, 14:156-162.
19. Diaz-Pulido G., Nash M.C., Anthony K.R.N., Bender D., Opdyke B.N., Reyes-Nivia C., Troitzsch U. Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs. Nat. Commun. 2014, 5. 10.1038/ncomms4310.
20. 4 in synthetic sea water from 273.15 to 318.15K. J. Chem. Thermodyn. 1990, 22(2):113-127.
21. 2 Measurements 2007, PICES Special Publications, (191pp.).
22. Dixson D.L., Munday P.L., Jones G.P. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 2010, 13(1):68-75.
23. 2 problem. Mark. Sci. 2009, 1:169-192.
24. Drew E.A., Hastings R.M. A year-round ecophysiological study of Himantothallus gradifolius (Desmarestiales, Phaeophyta) at Signy Island, Antarctica. Phycologia 1992, 31(3-4):262-277.
25. Ducklow H.W., Fraser W.R., Meredtih M.P., Stammerjohn S.E., Doney S.C., Martinson D.G., Sailley S.F., Schofield O.M., Steinberg D.K., Venables H.J., Amsler C.D. West Antarctic Peninsula: an ice-dependent coastal marine ecosystem in transition. Oceanography 2013, 26(3):190-203.
26. Dupont S., Portner H. Marine science: get ready for ocean acidification. Nature 2013, 498:429.
27. Elettra L., Storch D., Poertner H.O., Mark C.F. Effects of ocean acidification and warming on the mitochondrial physiology of Atlantic cod. Bioch. Biophys. Acta (BBA) - Bioenerg. (Suppl.) 2014, 1837.
28. Fabry V.J., McClintock J.B., Mathis J.T., Grebmeir J.M. Ocean acidification at high latitudes; the bellweather. Oceanography 2009, 22:160-171.
29. Fabry V.J., Seible B.A., Feely R.A., Orr R.A., Orr J.C. Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J. Mar. Sci. 2008, 65:414-432.
30. 2 and nutrient regimes. Oecologia 2013, 172:575-583.
31. 3 system in the oceans. Science 2004, 305(5682):362-366.
32. Gao K., Zheng Y. Combined effects of ocean acidification and solar UV radiation on photosynthesis, growth, pigmentation and calcification of the coralline alga Corallina sessilis (Rhodophyta). Glob. Chang. Biol. 2010, 16:2388-2398.
33. Gao K., Hebling W., Hader D., Hutchins D. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 2012, 470:167-189.
34. Gattuso J.P., Allemand D., Frankignoulle M. Photosynthesis and calcification at cellular, organismal and community levels in coral reefs: a review on interactions and control by carbonate chemistry. Am. Zool. 1999, 39(1):160-183.
35. Gaylord B., Kroeker K.J., Sunday J.M., Anderson K.M., Barry J.P., Brown N.E., Connell S.D., Dupont S., Fabricius K.E., Hall-Spencer J.M., Thiyagarajan T.V., Vaughan M.L.H., Widdicombe S., Harley C.D.G. Ocean acidification through the lens of ecological theory. Ecology 2015, 96(1):3-15.
36. Gil-Diaz T., Haroun R., Tuya F., Betancor S., Viera-Rodriguez M.A. Effects of ocean acidification on the brown alga Padina pavonica: decalcification due to acute and chronic events. PLoS One 2014, 9(9).
37. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu. Rev. Plant Biol. 2005, 56:99-131.
38. Gomez I., Wulff A., Roleda M.Y., Huovinen P., Karsten U., Quartino M.L., Dunton K., Wiencke C. Light and temperature demands of marine benthic microalgae and seaweeds in polar regions. Bot. Mar. 2009, 52:593-608.
39. Guinotte J.M., Fabry V.J. Ocean acidification and its potential effects on marine organisms. Ann. N.Y. Acad. Sci. 2008, 1134:320-342.
40. Harley C.D.G., Anderson K.M., Demes K.W., Jorve J.P., Kordas R.L., Coyle T.A., Graham M.H. Effects of climate change on global seaweed communities. J. Phycol. 2012, 48(5):1064-1078.
41. 2 ocean. Glob. Chang. Biol. 2011, 17:2488-2497.
42. Hillebrand H., Burgmer T., Biermann E. Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics. Mar. Biol. 2012, 159:2415-2422.
43. Hofmann L.C., Bischof K. Ocean acidification effects on calcifying macroalgae. Aquat. Biol. 2014, 22:261-279.
44. 2 levels. Mar. Ecol. Prog. Ser. 2012, 464:89-105.
45. Hommersand M., Moe R.L., Amsler C.D., Fredericq S. Notes on the systematics and biogeographical relationships of Antarctic and sub-Antarctic Rhodophyta with descriptions of four new genera and five new species. Biology of Polar Benthic Algae 2011, 51-98. Walter de Gruyter GmbH & Co. KH, Gottingen. C. Weincke (Ed.).
46. +-dependant acid-base transport mechanisms and energy metabolism of squid (Sepioteuthis lessoniana) affected by seawater acidification. Front. Zool. 2014, 11(1):55.
47. Hurd C., Hepburn C.D., Currie K.I., Raven J.A., Hunter K.A. Testing the effects of ocean acidification on algal metabolism considerations for experimental designs. J. Phycol. 2009, 45:1236-1251.
48. IPCC Summary for Policymakers. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change 2013, Cambridge University Press, New York, NY USA. T.F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S.K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, P.M. Midgley (Eds.).
49. Irving A.D., Connell S.D., Johnston E.L., Pile A.J., Gillanders B.M. The response of encrusting coralline algae to canopy loss: an independent test of predictions on an Antarctic coast. Mar. Biol. 2005, 147(5):1075-1083.
50. Jassby A.D., Platt T. Mathematical formulation of the relationship between photosynthesis and light for pytoplankton. Limnol. Oceanogr. 1976, 21(4):540-547.
51. Johnson M.D., Carpenter R.C. Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J. Exp. Mar. Biol. Ecol. 2012, 434:94-101.
52. 2. PLoS One 2014, 9(2).
53. 2 gradients. Glob. Chang. Biol. 2012, 18:2792-2803.
54. Kamenos N.A. Coralline algal Mg-O bond strength as a marine pCO2 proxy. Geology 2015, 10.1130/G36386.1.
55. Kamenos N.A., Burdett H.L., Aloisio E., Findlay H.S., Martin S., Longbone C., Dunn J., Widdicombe S., Calosi P. Coralline algal structure is more sensitive to rate, rather than the magnitude, of ocean acidification. Glob. Chang. Biol. 2013, 19(12):3621-3628.
56. Kamenos N.A., Cusack M., Huthwelker T., Lagarde P., Scheibling R.E. Mg-lattice associations in red coralline algae. Geochim. Cosmochim. Acta 2009, 73:1901-1907.
57. Kelley M., Hofmann G. Adaptation and the physiology of ocean acidification. Fuct. Ecol. 2013, 27(4):980-990.
58. Koch M., Bowes G., Ross C., Zhang X. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Chang. Biol. 2013, 19(1):103-132.
59. Kohler K.E., Gill S.M. Coral Point Count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput. Geosci. 2006, 32(9):1259-1269.
60. 2 ocean. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(31):12721-12726.
61. Kroeker K.J., Micheli F., Gambi M.C., Martz T.R. Divergent ecosystem responses within a benthic marine community to ocean acidification. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(35):14515-14520.
62. Kuffner I., Andersson A., Jokiel P., Rodgers K., Mackenzie F. Decreased abundance of crustose coralline algae due to ocean acidification. Nat. Geosci. 2008, 1(2):114-117.
63. 2-driven ocean acidification on the early developmental stages of invertebrates. Mar. Ecol. Prog. Ser. 2008, 373:275-284.
64. Lobban C.S., Harrison P.J. Seaweed Ecology and Physiology 1997, Cambridge University Press, Cambridge, (1-366 pp.).
65. Martin S., Gattuso J. Response of Mediterranean coralline algae to ocean acidification and elevated temperature. Glob. Chang. Biol. 2009, 15(8):2089-2100.
66. McCoy S.J., Kamenos N.A. Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J. Phycol. 2015, 51(1):6-24.
67. McCoy S.J., Pfister C.A. Historical comparisons reveal altered competitive interactions in a guild of crustose coralline algae. Ecol. Lett. 2014, 17(4):475-483.
68. Meredith M., King J.C. Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century. Geophys. Res. Lett. 2005, 32(19):L19604.
69. Miller K.A., Pearse J.S. Ecological studies of seaweeds in McMurdo Sound, Antarctica. Am. Zool. 1991, 31(1):35-48.
70. Nash M.C., Opdyke B.N., Wu Z., Xu H., Trafford J.M. Simple X-ray diffraction techniques to identify Mg calcite, dolomite, and magnesite in tropical coralline algae and assess peak asymmetry. J. Sediment. Res. 2013, 83:1085-1099.
71. NOAA National Climatic Data Center State of the Climate: Global Analysis for December 2014 2014, http://www.ncdc.noaa.gov/sotc/global/2014/13.
72. 2. Oikos 2012, 001-015.
73. Olischläger M., Wiencke C. Ocean acidification alleviates low-temperature effects on growth and photosynthesis of the red alga Neosiphonia harveyi (Rhodophyta). J. Exp. Bot. 2013, 64(18):5587-5597.
74. Ordonez A., Doropoulos C., Diaz-Pulido G. Effects of ocean acidification on population dynamics and community structure of crutose coralline algae. Biol. Bull. 2014, 226:255-268.
75. Orr J.C., Fabry V.J., Aumont O., Bopp L., Doney S.C., Feely R.A., Gnanadesikan A., Gruber N., Ishida A., Joos F., Key R.M., Lindsay K., Maier-Reimer E., Mattear R., Monfray P., Mouchet A., Najjar R.G., Plattner G.K., Rodgers K.B., Sabine C.L., Sarmiento J.L., Schlitzer R., Slater R.D., Totterdell I.J., Weirig M.F., Yamanaka Y., Yool A. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 2005, 437:681-686.
76. Peck L.S. Prospects for survival in the Southern Ocean: vulnerability of benthic species to temperature change. Antarct. Sci. 2005, 17(4):497-507.
77. Pesce A.S. The Physiological Response of Non-calcifying Benthic Macroalgae to Ocean Acidification 2012, San Diego State University.
78. 2 vents. Mar. Biol. 2013, 160:2247-2259.
79. Quartino M.L., Deregibus D., Campana G.L., Latorre G.E.J., Momo F. Evidence of macroalgal colonization on newly ice-free areas following glacial retreat in Potter Cove (South Shetland Islands), Antarctica. PLoS One 2013, 8(3).
80. Ragazzola F., Foster L.C., Form A., Anderson P.S.L., Hansteen T.H., Fietske J. Ocean acidification weakens the structural integrity of coralline algae. Glob. Chang. Biol. 2013, 18(9):2804-2812.
81. Rautenberger R., Fernandez P.A., Strittmatter M., Heesch S., Cornwall C.E., Hurd C.L., Roleda M.Y. Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). Ecol. Evol. 2015, 5(4):874-888.
82. Rautenberger R., Huovinen P., Gomez I. Effects of increased seawater temperature on UV tolerance of Antarctic marine macroalgae. Mar. Biol. 2015, 162(5):1087-1097.
83. 2 perturbation studies: from organism to community level. Biogeosciences 2008, 5:1157-1164.
84. Riebesell U., Fabry V.J., Hansson L., Gattuso J.P. Guide to Best Practices for Ocean Acidification Research and Data Reporting 2010, Publications Office of the European Union, Luxembourg.
85. Ries J. Mg fractionation in crustose coralline algae: geochemical, biological, and sedimentological implications of secular variation in the Mg/Ca ratio of seawater. Geochim. Cosmochim. Acta 2006, 70:891-900.
86. Ries J. Effects of secular variation in seawater Mg/Ca ratio (calcite-aragonite seas) on CaCO3 sediment production by the calcareous algae Halimeda, Penicillus and Udotea- evidence from recent experiments and the geological record. Terra Nova 2009, 21(5):323-339.
87. Ries J.B. Review: geological and experimental evidence for secular variation in seawater Mg/Ca (calcite-aragonite seas) and its effect on marine biological calcification. Biogeosciences 2010, 7:2795-2849.
88. 2 world. J. Exp. Mar. Biol. Ecol. 2011, 408:54-64.
89. 2calc: A User-Friendly Seawater Carbon Calculator for Windows, Mac OS X, and iOS (iPhone). U.S. Geological Survey, Virginia 2010, U.S. Department of the Interior, U. (Ed.).
90. Roleda M.Y., Hurd C. Seaweed Responses to Ocean Acidification. Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization 2012, 407-431. Springer, New York. C. Bischof (Ed.).
91. Roleda M.Y., Boyd P.W., Hurd C.L. Before ocean acidification: calcifier chemistry lessons. J. Phycol. 2012, 48(4):840-843.
92. Roy R.N., Roy L.N., Vogel K.M., Porter-Moore C., Pearson T., Good C.E., Millero F.J., Campbel D.M. The dissociation constants of carbonic acid in seawater at salinities 5 to 45 and temperatures 0 to 45°C. Mar. Chem. 1993, 44(2):249-267.
93. 2 modifies the influence of light in shaping subtidal habitat. J. Phycol. 2011, 47:744-752.
94. 2. Science 2004, 305(5682):367-371.
95. Schloss I.R., Abele D., Moreau S., Demers S., Bers A.V., Gonzalez O., Ferreyra G.A. Response of phytoplankton dynamics to 19-year (1991-2009) climate trends in Potter Cove (Antarctica). J. Mar. Syst. 2012, 92(1):53-66.
96. Schoenrock K. Ecology and Physiology of Antarctic Macrophytes Under the Influence of Abiotic and Biotic Stressors 2014, 177. University of Alabama at Birmingham.
97. Schoenrock K., Amsler C.D., McClintock J.B., Baker B.J. Life history bias in endophyte infection of the Antarctic rhodophyte Iridaea cordata. Bot. Mar. 2015, 58(1):1-8.
98. Schoenrock K., Amsler C.D., McClintock J.B., Baker B.J. A comprehensive study of Antarctic algal symbioses: minimal impacts of endophyte presence in most species of macroalgal hosts. Eur. J. Phycol. 2015, 50(3):271-278.
99. Schoenrock K., Schram J.B., Amsler C.D., McClintock J.B., Angus R.A. Climate change impacts on overstory Desmarestia spp. from the western Antarctic Peninsula. Mar. Biol. 2015, 162(2):377-389.
100. Schram J.B., Schoenrock K.M., McClintock J.B., Amsler C.D., Angus R.A. Multiple stressor effects of near future elevated seawater temperature and decreased pH on righting and escape behaviors of two common Antarctic gastropods. J. Exp. Mar. Biol. Ecol. 2014, 457:90-96.
101. Schram J.B., Schoenrock K.M., McClintock J.B., Amsler C.D., Angus R.A. Multi-Frequency Observations of Seawater Carbonate Chemistry on the Central Coast of the Western Antarctic Peninsula. Polar Res 2015, 34.
102. Schwarz A.M., Hawes I., Andrew N., Norkko A. Macroalgal photosynthesis near the southern global limit for growth; Cape Evans, Ross Sea, Antarctica. Polar Biol. 2003, 26(12):789-799.
103. Short J.A., Kendrick G.A., Falter J., McCulloch M.T. Interactions between filamentous turf algae and coralline algae are modified under ocean acidification. J. Exp. Mar. Biol. Ecol. 2014, 456:70-77.
104. Silbiger N.J., Donahue M.J. Secondary calcification and dissolution respond differently to future ocean conditions. Biogeosciences 2015, 12:567-578.
105. Steig E.J., Schneider D.P., Rutherford S.D., Mann M.E., Comiso J.C., Shindell D.T. Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Nature 2009, 457(7228):459-462.
106. 2 difference. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(16):8292-8299.
107. Tans P., Keeling R. Trends in atmospheric cardon dioxide 2013, http://noaa.gov.
108. 3-production rates correspond to intensity and duration of the solar radiation. Biogeosciences 2014, 11:833-842.
109. Thompson D.W.J., Solomon S., Kushner P.J., England M.H., Grise K.M., Karoly D.J. Signatures of the Antarctic ozone hole in Southern Hemisphere surface climate change. Nat. Geosci. 2011, 4:741-749.
110. 2/Ar measurements. Geophys. Res. Lett. 2014, 41(19):6803-6810.
111. Vaughan D.G., Marshall G.J., Connolley W.M., Parkinson C., Mulvaney R., Hodgson D.A., King J.C., Pudsey C.J., Turner J. Recent rapid regional climate warming on the Antarctic Peninsula. Clim. Chang. 2003, 60(3):243-274.
112. Wanninkhof R.H. Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res.: Oceans (1978-2012) 1992, 97(C5):7373-7382.
113. Wiencke C., tom Dieck I. Temperature requirements for growth and survival of macroalgae from Antarctica and Southern Chile. Mar. Ecol. Prog. Ser. 1990, 59:157-170.
114. Wiencke C., Amsler C.D. Seaweeds and their communities in Polar Regions. Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization 2012, 265-294. Springer-Verlag, Berlin. C. Wiencke, K. Bischof (Eds.).
115. Wiencke C., Clayton M.N. Biology of Antarctic Seaweeds 2002, 239. A.R.G. Ganter Verlag KG, Liechtenstein.
116. Wiencke C., Amsler C.D., Clayton M.N. Macroalgae. Biogeographic Atlas of the Southern Ocean, 2014 2014, 66-73. Scientific Committee on Antarctic Research, Cambridge, UK. C. De Broyer, P. Koubbi, H.J. Griffiths, B. Raymond, C. d'Udekem d'Acoz, A.P. Van de Putte, B. Danis, B. David, S. Grant, J. Gutt, C. Held, G. Hosie, F. Huettmann, A. Post, Y. Ropert-Coudert (Eds.).
117. Wiencke C., Clayton M.N., Gomez I., Iken K., Luder U.H., Amsler C.D., Karsten U., Hanelt D., Bischof K., Dunton K. Life strategy, ecophysiology and ecology of seaweeds in polar waters. Rev. Environ. Sci. Biotechnol. 2007, 6:95-126.
118. Zou D., Gao K. Temperature response of photosynthetic light- and carbon-use characteristics in the red seaweed Gracilariopsis lemaneiformis (Gracialiales, Rhodophyta). J. Phycol. 2014, 50:366-375.