High diversity of coralline algae in New Zealand revealed: Knowledge gaps and implications for future research

English version

Autoři: Brenton A. Twist ^aff001; Kate F. Neill ^aff002; Jaret Bilewitch ^aff002; So Young Jeong ^aff004; Judy E. Sutherland ^aff002; Wendy A. Nelson ^aff002
Působiště autorů: Institute of Marine Sciences, University of Auckland, Auckland, New Zealand ^aff001; National Institute of Water & Atmospheric Research, Wellington, New Zealand ^aff002; Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada ^aff003; Department of Life Science, Chosun University, Dong-gu, Gwangju, Korea ^aff004; Griffith School of Environment and Australian Rivers Institute–Coast & Estuaries, Nathan Campus, Griffith University, Brisbane, Nathan, Queensland, Australia ^aff005; School of Biological Sciences, University of Auckland, Auckland, New Zealand ^aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225645

Souhrn

Coralline algae (Corallinophycideae) are calcifying red algae that are foundation species in euphotic marine habitats globally. In recent years, corallines have received increasing attention due to their vulnerability to global climate change, in particular ocean acidification and warming, and because of the range of ecological functions that coralline algae provide, including provisioning habitat, influencing settlement of invertebrate and other algal species, and stabilising reef structures. Many of the ecological roles corallines perform, as well as their responses to stressors, have been demonstrated to be species-specific. In order to understand the roles and responses of coralline algae, it is essential to be able to reliably distinguish individual species, which are frequently morphologically cryptic. The aim of this study was to document the diversity and distribution of coralline algae in the New Zealand region using DNA based phylogenetic methods, and examine this diversity in a broader global context, discussing the implications and direction for future coralline algal research. Using three independent species delimitation methods, a total of 122 species of coralline algae were identified across the New Zealand region with high diversity found both regionally and also when sampling at small local spatial scales. While high diversity identified using molecular methods mirrors recent global discoveries, what distinguishes the results reported here is the large number of taxa (115) that do not resolve with type material from any genus and/or species. The ability to consistently and accurately distinguish species, and the application of authoritative names, are essential to ensure reproducible science in all areas of research into ecologically important yet vulnerable coralline algae taxa.

Klíčová slova:

Algae – Biodiversity – New Zealand – Phylogenetic analysis – Phylogenetics – Phylogeography – Species delimitation – Species diversity

Zdroje

1. Nelson WA. Calcified macroalgae–critical to coastal ecosystems and vulnerable to change: a review. Mar Freshw Res. 2009;60: 787–801.

2. Ellison AM. Foundation Species, Non-trophic Interactions, and the Value of Being Common. iScience. Elsevier Inc.; 2019;13: 254–268. doi: 10.1016/j.isci.2019.02.020 30870783

3. Kuffner IB, Andersson AJ, Jokiel PL, Ku‘ulei SR, Mackenzie FT. Decreased abundance of crustose coralline algae due to ocean acidification. Nat Geosci. 2008;1: 114–117.

4. McCoy SJ, Kamenos NA. Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J Phycol. 2015;51: 6–24. doi: 10.1111/jpy.12262 26986255

5. Cornwall CE, Diaz-Pulido G, Comeau S. Impacts of Ocean Warming on Coralline Algal Calcification: Meta-Analysis, Knowledge Gaps, and Key Recommendations for Future Research. Front Mar Sci. 2019;6: 1–10. doi: 10.3389/fmars.2019.00186

6. Cowles A, Hewitt JE, Taylor RB. Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats. Mar Ecol Prog Ser. 2009;384: 175–185.

7. Chenelot H, Jewett SC, Hoberg MK. Macrobenthos of the nearshore Aleutian Archipelago, with emphasis on invertebrates associated with Clathromorphum nereostratum (Rhodophyta, Corallinaceae). Mar Biodivers. 2011;41: 413–424. doi: 10.1007/s12526-010-0071-y

8. Asnaghi V, Thrush SF, Hewitt JE, Mangialajo L, Cattaneo-Vietti R, Chiantore M. Colonisation processes and the role of coralline algae in rocky shore community dynamics. J Sea Res. 2015;95: 132–138. http://dx.doi.org/10.1016/j.seares.2014.07.012

9. Parada GM, Martínez EA, Aguilera MA, Oróstica MH, Broitman BR. Interactions between kelp spores and encrusting and articulated corallines: recruitment challenges for Lessonia spicata. Bot Mar. 2017;60: 619–625.

10. Pearce CM, Scheibling RE. Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. Biol Bull. 1990;179: 304–311. doi: 10.2307/1542322 29314958

11. O’Leary JK, Barry JP, Gabrielson PW, Rogers-Bennett L, Potts DC, Palumbi SR, et al. Calcifying algae maintain settlement cues to larval abalone following algal exposure to extreme ocean acidification. Sci Rep. 2017;7: 1–10.

12. Spotorno-Oliveira P, Figueiredo MAO, Tâmega FTS. Coralline algae enhance the settlement of the vermetid gastropod Dendropoma irregulare (d’Orbigny, 1842) in the southwestern Atlantic. J Exp Mar Bio Ecol. 2015;471: 137–145. doi: 10.1016/j.jembe.2015.05.021

13. Fredericq S, Krayesky-Self S, Sauvage T, Richards J, Kittle R, Arakaki N, et al. The critical importance of rhodoliths in the life cycle completion of both macro-and microalgae, and as holobionts for the establishment and maintenance of marine biodiversity. Front Mar Sci. 2019;5: 1–17.

14. Mallela J. Calcification by Reef-Building Sclerobionts. PLoS One. Public Library of Science; 2013;8: e60010.

15. Bracchi VA, Basso D, Marchese F, Corselli C, Savini A. Coralligenous morphotypes on subhorizontal substrate: A new categorization. Cont Shelf Res. Elsevier; 2017;144: 10–20.

16. Le Gall L, Saunders GW. A nuclear phylogeny of the Florideophyceae (Rhodophyta) inferred from combined EF2, small subunit and large subunit ribosomal DNA: establishing the new red algal subclass Corallinophycidae. Mol Phylogenet Evol. 2007;43: 1118–1130. doi: 10.1016/j.ympev.2006.11.012 17197199

17. Nelson WA, Sutherland JE, Farr TJ, Hart DR, Neill KF, Kim HJ, et al. Multi‐gene phylogenetic analyses of New Zealand coralline algae: Corallinapetra novaezelandiae gen. et sp. nov. and recognition of the Hapalidiales ord. nov. J Phycol. 2015;51: 454–468. doi: 10.1111/jpy.12288 26986662

18. Le Gall L, Payri CE, Bittner L, Saunders GW. Multigene phylogenetic analyses support recognition of the Sporolithales ord. nov. Mol Phylogenet Evol. 2010;54: 302–305. http://dx.doi.org/10.1016/j.ympev.2009.05.026 19490946

19. Caragnano A, Foetisch A, Maneveldt GW, Millet L, Liu L, Lin S, et al. Revision of Corallinaceae (Corallinales, Rhodophyta): recognizing Dawsoniolithon gen. nov., Parvicellularium gen. nov. and Chamberlainoideae subfam. nov. containing Chamberlainium gen. nov. and Pneophyllum. J Phycol. 2018;54: 391–409. doi: 10.1111/jpy.12644 29574890

20. Hernandez-Kantun JJ, Gabrielson P, Hughey JR, Pezzolesi L, Rindi F, Robinson NM, et al. Reassessment of branched Lithophyllum spp.(Corallinales, Rhodophyta) in the Caribbean Sea with global implications. Phycologia. 2016;55: 619–639.

21. Maneveldt GW, Gabrielson PW, Kangwe J. Sporolithon indopacificum sp. nov. (Sporolithales, Rhodophyta) from tropical western Indian and western Pacific oceans: First report, confirmed by DNA sequence data, of a widely distributed species of Sporolithon. Phytotaxa. 2017;326: 115–128.

22. Kato A, Baba M, Suda S. Revision of the Mastophorideae (Corallinales, Rhodophyta) and polyphyly in nongeniculate species widely distributed on pacific coral reefs. J Phycol. 2011;47: 662–672. doi: 10.1111/j.1529-8817.2011.00996.x 27021995

23. Basso D, Caragnano A, Le Gal L, Rodondi G. The genus Lithophyllum in the north-western Indian Ocean, with description of L. yemenense sp. nov., L. socotraense sp. nov., L. subplicatum comb. et stat. nov., and the resumed L. affine, L. kaiseri, and L. subreduncum. Phytotaxa. 2015;208: 183–200.

24. Gabrielson PW, Hughey JR, Diaz‐Pulido G. Genomics reveals abundant speciation in the coral reef building alga Porolithon onkodes (Corallinales, Rhodophyta). J Phycol. 2018;54: 429–434. doi: 10.1111/jpy.12761 29920669

25. Torrano-Silva BN, Vieira BR, Riosmena-Rodríguez R, Oliveira MC. Guidelines for DNA barcoding of coralline algae, focusing on Lithophylloideae (Corallinales) from Brazil. Bot Mar. 2018;61: 127–140.

26. Richards JL, Gabrielson PW, Hughey JR, Freshwater DW. A re-evaluation of subtidal Lithophyllum species (Corallinales, Rhodophyta) from North Carolina, USA, and the proposal of L. searlesii sp. nov. Phycologia. 2018;57: 318–330.

27. Richards JL, Sauvage T, Schmidt WE, Fredericq S, Hughey JR, Gabrielson PW. The coralline genera Sporolithon and Heydrichia (Sporolithales, Rhodophyta) clarified by sequencing type material of their generitypes and other species. J Phycol. 2017;53: 1044–1059. doi: 10.1111/jpy.12562 28681431

28. Hind KR, Gabrielson PW, Jensen CP, Martone PT. Crusticorallina gen. nov., a nongeniculate genus in the subfamily Corallinoideae (Corallinales, Rhodophyta). J Phycol. 2016;52: 929–941. doi: 10.1111/jpy.12449 27434825

29. Sissini MN, Oliveira MC, Gabrielson PW, Robinson NM, Okolodkov YB, Rodríguez RR, et al. Mesophyllum erubescens (Corallinales, Rhodophyta)—so many species in one epithet. Phytotaxa. 2014;190: 299–319.

30. Pezzolesi L, Peña V, Le Gall L, Gabrielson PW, Kaleb S, Hughey JR, et al. Mediterranean Lithophyllum stictiforme (Corallinales, Rhodophyta) is a genetically diverse species complex: implications for species circumscription, biogeography and conservation of coralligenous habitats. J Phycol. 2019;55: 473–492. doi: 10.1111/jpy.12837 30657167

31. Adey WH, Hernandez-Kantun JJ, Gabrielson PW, Nash MC, Hayek LC. Phymatolithon (Melobesioideae, Hapalidiales) in the boreal-subarctic transition zone of the North Atlantic. Smithson Inst Sch Press. 2018;40: 1–90.

32. Hind KR, Gabrielson PW, Saunders GW. Molecular-assisted alpha taxonomy reveals pseudocryptic diversity among species of Bossiella (Corallinales, Rhodophyta) in the eastern Pacific Ocean. Phycologia. 2014;53: 443–456. doi: 10.2216/13-239.1

33. Adey WH. The effects of light and temperature on growth rates in boreal-subarctic crustose corallines. J Phycol. 1970;6: 269–276.

34. Paine RT. Ecological determinism in the competition for space: the Robert H. MacArthur Award Lecture. Ecology. 1984;65: 1339–1348.

35. McCoy SJ, Pfister CA. Historical comparisons reveal altered competitive interactions in a guild of crustose coralline algae. Ecol Lett. 2014;17: 475–483. doi: 10.1111/ele.12247 24422586

36. Hofmann LC, Straub S, Bischof K. Competition between calcifying and noncalcifying temperate marine macroalgae under elevated CO2 levels. Mar Ecol Prog Ser. 2012;464: 89–105.

37. Egilsdottir H, Noisette F, Noël LM-LJ, Olafsson J, Martin S. Effects of pCO2 on physiology and skeletal mineralogy in a tidal pool coralline alga Corallina elongata. Mar Biol. 2013;160: 2103–2112. doi: 10.1007/s00227-012-2090-7

38. Noisette F, Egilsdottir H, Davoult D, Martin S. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J Exp Mar Bio Ecol. 2013;448: 179–187.

39. van der Merwe E, Miklasz K, Channing A, Maneveldt GW, Gabrielson PW. DNA sequencing resolves species of Spongites (Corallinales, Rhodophyta) in the Northeast Pacific and South Africa, including S. agulhensis sp. nov. Phycologia. 2015;54: 471–490.

40. Rösler A, Perfectti F, Peña V, Braga JC. Phylogenetic relationships of corallinaceae (Corallinales, Rhodophyta): taxonomic implications for reef-building corallines. J Phycol. 2016;

41. Harvey A, Farr T, Neill K, Woelkerling W, Nelson WA. Coralline algae of central New Zealand: An identification guide to common “crustose” species. NIWA Information Series 57. Wellington, New Zealand: NIWA; 2005.

42. Farr T, Broom J, Hart D, Neill K, Nelson WA. Common coralline algae of northern New Zealand: an identification guide. NIWA Information Series 70. Wellington, New Zealand: NIWA; 2009.

43. Thiers B. Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. 2019.

44. Canfield RH. Application of the line interception method in sampling range vegetation. J For. 1941;39: 388–394.

45. QGIS Development Team. QGIS geographic information system. Open Source Geospatial Foundation Project. 2019.

46. Yoon HS, Hackett JD, Bhattacharya D. A single origin of the peridinin-and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc Natl Acad Sci. 2002;99: 11724–11729. doi: 10.1073/pnas.172234799 12172008

47. Freshwater DW, Rueness J. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia. 1994;33: 187–194.

48. Broom JE, Hart DR, Farr TJ, Nelson WA, Neill KF, Harvey AS, et al. Utility of psbA and nSSU for phylogenetic reconstruction in the Corallinales based on New Zealand taxa. Mol Phylogenet Evol. 2008;46: 958–973. http://dx.doi.org/10.1016/j.ympev.2007.12.016 18243019

49. Blair C, Bryson RW. Cryptic diversity and discordance in single-locus species delimitation methods within horned lizards (Phrynosomatidae: Phrynosoma). Mol Ecol Resour. 2017;17: 1168–1182. doi: 10.1111/1755-0998.12658 28161911

50. Puillandre N, Lambert A, Brouillet S, Achaz G. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol. 2012;21: 1864–1877. doi: 10.1111/j.1365-294X.2011.05239.x 21883587

51. Zhang J, Kapli P, Pavlidis P, Stamatakis A. A general species delimitation method with applications to phylogenetic placements. Bioinformatics. 2013;29: 2869–2876. doi: 10.1093/bioinformatics/btt499 23990417

52. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, et al. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol. 2006;55: 595–609. doi: 10.1080/10635150600852011 16967577

53. Fujisawa T, Barraclough TG. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol. 2013;62: 707–724. doi: 10.1093/sysbio/syt033 23681854

54. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59: 307–321. doi: 10.1093/sysbio/syq010 20525638

55. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lect Math life Sci. 1986;17: 57–86.

56. Yang Z. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol. 1996;11: 367–372. doi: 10.1016/0169-5347(96)10041-0 21237881

57. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9: 772.

58. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29: 1969–1973. doi: 10.1093/molbev/mss075 22367748

59. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006;4: e88. doi: 10.1371/journal.pbio.0040088 16683862

60. Hoshino M, Ishikawa S, Kogame K. Concordance between DNA-based species boundaries and reproductive isolating barriers in the Scytosiphon lomentaria species complex (Ectocarpales, Phaeophyceae). Phycologia. 2018;57: 232–242.

61. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2014;32: 268–274. doi: 10.1093/molbev/msu300 25371430

62. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14: 587. doi: 10.1038/nmeth.4285 28481363

63. Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol. 2006;55: 539–552. doi: 10.1080/10635150600755453 16785212

64. Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19: 1572–1574. doi: 10.1093/bioinformatics/btg180 12912839

65. Rambaut A, Suchard M, Xie W, Drummond A. Tracer version 1.6. http://beast.bio.ed.ac.uk/. 2014;

66. Rambaut A. FigTree version 1. 4. http://tree.bio.ed.ac.uk/software/figtree/. 2012;

67. Chao A, Colwell RK, Lin C-W, Gotelli NJ. Sufficient sampling for asymptotic minimum species richness estimators. Ecology. 2009;90: 1125–1133. doi: 10.1890/07-2147.1 19449706

68. Chao A. Estimating the population size for capture-recapture data with unequal catchability. Biometrics. 1987;43: 783–791. 3427163

69. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, et al. vegan: Community Ecology Package. R package version 2.4–3. https://CRANR-project.org/package=vegan. 2017;

70. Twist BA. Diversity and distribution of coralline algae in southern New Zealand. PhD Thesis, University of Auckland. 2019.

71. Woelkerling WJ, Nelson WA. A baseline summary and analysis of the taxonomic biodiversity of coralline red algae (Corallinales, Rhodophyta) recorded from the New Zealand region. Cryptogam Algol. 2004;25: 39–106.

72. Melbourne LA, Hernández-Kantún JJ, Russell S, Brodie J. There is more to maerl than meets the eye: DNA barcoding reveals a new species in Britain, Lithothamnion erinaceum sp. nov. (Hapalidiales, Rhodophyta). Eur J Phycol. 2017;52: 166–178.

73. Kogame K, Uwai S, Anderson RJ, Choi HG, Bolton JJ. DNA barcoding of South African geniculate coralline red algae (Corallinales, Rhodophyta). South African J Bot. 2017;108: 337–341. https://doi.org/10.1016/j.sajb.2016.08.013

74. Rindi F, Peña V, Le Gall L, Braga JC, Falace A, Hernandez-Kantun JJ, et al. Evolutionary history and diversity of Mediterranean coralline algae: how much do we know? Phycologia. 2017;56: 158.

75. Peña V, Hernandez-Kantun JJ, Adey WH, Le Gall L. Assessment of coralline species diversity in the European coasts supported by sequencing of type material: the case study of Lithophyllum nitorum (Corallinales, Rhodophyta). Cryptogam Algol. 2018;

76. Maneveldt GW, Puckree-Padua C, Gabrielson PW. Inspired by the joy of new discoveries—uncovering cryptic coralline algal diversity. SANCOR Newsl. 2018; 4–6.

77. Keith SA, Kerswell AP, Connolly SR. Global diversity of marine macroalgae: environmental conditions explain less variation in the tropics. Glob Ecol Biogeogr. 2014;23: 517–529.

78. Kerswell AP. Global biodiversity patterns of benthic marine algae. Ecology. 2006;87: 2479–2488. doi: 10.1890/0012-9658(2006)87[2479:gbpobm]2.0.co;2 17089657

79. Bolton JJ. Global seaweed diversity: patterns and anomalies. Bot Mar. 1994;37: 241–246.

80. Mortimer N, Campbell HJ, Tulloch AJ, King PR, Stagpoole VM, Wood RA, et al. Zealandia: Earth’s hidden continent. GSA today. 2017;27: 27–35.

81. Hooper DU, Adair EC, Cardinale BJ, Byrnes JEK, Hungate BA, Matulich KL, et al. A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature. 2012;486: 105. doi: 10.1038/nature11118 22678289

82. Fanin N, Gundale MJ, Farrell M, Ciobanu M, Baldock JA, Nilsson M-C, et al. Consistent effects of biodiversity loss on multifunctionality across contrasting ecosystems. Nat Ecol Evol. 2018;2: 269. doi: 10.1038/s41559-017-0415-0 29255299

83. Benedetti-Cecchi L, Bertocci I, Vaselli S, Maggi E, Bulleri F. Neutrality and the response of rare species to environmental variance. PLoS One. 2008;3: e2777. doi: 10.1371/journal.pone.0002777 18648545

84. Connell SD. The monopolization of understorey habitat by subtidal encrusting coralline algae: A test of the combined effects of canopy-mediated light and sedimentation. Mar Biol. 2003;142: 1065–1071. doi: 10.1007/s00227-003-1021-z

85. Cornwall CE, Comeau S, McCulloch MT. Coralline algae elevate pH at the site of calcification under ocean acidification. Glob Chang Biol. 2017;23: 4245–4256. doi: 10.1111/gcb.13673 28370806

86. Comeau S, Carpenter RC, Nojiri Y, Putnam HM, Sakai K, Edmunds PJ. Pacific-wide contrast highlights resistance of reef calcifiers to ocean acidification. Proc R Soc London B Biol Sci. 2014;281: 20141339.

87. Cornwall CE, Hurd CL. Experimental design in ocean acidification research: problems and solutions. ICES J Mar Sci. 2015;73: 572–581. doi: 10.1093/icesjms/fsv118

88. Guenther RJ, Martone PT. Physiological performance of intertidal coralline algae during a simulated tidal cycle. J Phycol. 2014;50: 310–321. doi: 10.1111/jpy.12161 26988188

89. Johnson CR, Mann KH. The crustose coralline alga, Phymatolithon Foslie, inhibits the overgrowth of seaweeds without relying on herbivores. J Exp Mar Bio Ecol. 1986;96: 127–146.

90. Hind K, Starko S, Burt J, Lemay M, Salomon A, Martone PT. Trophic control of coralline species diversity. Proc Natl Acad Sci. 2019;116: 15080–15085.

91. Woelkerling WJ. Subfamily Mastophorideae (excluding Hydrolithon, Pneophyllum, Spongites & Neogoniolithon). In: Womersley HBS, editor. The Marine Benthic Flora of Southern Australia Rhodophyta Part IIIB, Gracilariales, Rhodymeniales, Corallinales and Bonnemaisoniales. Canberra, Australia: Australian Biological Resources Study; 1996. pp. 237–255.

92. Nelson WA, Dalen J, Neill KF. Insights from natural history collections: analysing the New Zealand macroalgal flora using herbarium data. PhytoKeys. 2013; 1–21.

93. Guiry MD, Guiry GM. AlgaeBase. Worldwide electronic publication, National University of Ireland, Galway. 2019.

94. Rösler A, Perfectti F, Peña V, Aguirre J, Braga JC. Timing of the evolutionary history of Corallinaceae (Corallinales, Rhodophyta). J Phycol. Wiley Online Library; 2017;53: 567–576.

High diversity of coralline algae in New Zealand revealed: Knowledge gaps and implications for future research

Souhrn

Klíčová slova:

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