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Phylogenetic relationship of Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta) in Malaysia

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Abstract

The genera Kappaphycus Doty and Eucheuma J. Agardh are important sources of carrageenan in Malaysia, offering lucrative revenues to the carrageenan industry, economy, and the local community. The extensive range of morphotypes and the lack of distinct morphological characteristics led to the application of molecular systematics in elucidating this taxonomic confusion. Local varieties of Kappaphycus and Eucheuma, identified using putative external morphology, were analyzed using the mitochondrial cox2–3 spacer and plastid RuBisCO spacer molecular markers. Phylogenetic analysis of these and non-local specimens indicate that Kappaphycus and Eucheuma are genetically distinct. Three main genotypes of Kappaphycus alvarezii were identified, of which two are extant in Hawaii. Morphological and color variations are not supported by molecular data, indicating that most of the local names are not genetically based. Both the cox2–3 spacer and RuBisCO spacer generated phylogenetic trees with similar topology except in variation of nodal supports. The two markers showed clear separation between Kappaphycus and Eucheuma and the existence of three Malaysian Kappaphycus cultivars. Cox2–3 spacer data is more variable and provides better resolution than the RuBisCO spacer, showing that Kappaphycus is more diversified with a larger number of genotypes, strains, and species which are unique to Southeast Asia. Kappaphycus sp. “Aring-aring” appeared to be phenotypically and genotypically different from other Kappaphycus congeners, whereas Kappaphycus striatum exhibited two different genotypes. Our data indicate that Eucheuma denticulatum is the dominant species in Malaysian waters and also suggested paraphyly in Eucheuma which will require further studies. The application of molecular taxonomy on Malaysian Kappaphycus and Eucheuma proves useful, offering valuable insights into the taxonomy and distribution of these commercially important Rhodophytes.

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References

  • Akaike H (1973) Information theory and an extension of the maximum likelihood principle. In: Petrov BN, Csaki F (eds) Second International Symposium Information Theory. Akademia Kiado, Budapest, pp 267–281

    Google Scholar 

  • Ask EI, Azanza RV (2002) Advances in cultivation technology of commercial eucheumatoid species:a review with suggestions for future research. Aquaculture 206:257–277

    Article  Google Scholar 

  • Azanza RV, Ask EI (2001) Kappaphycus alvarezii (Doty) Doty carposporeling growth and development in the laboratory. Paper presented at the 17th International Seaweed Symposium, Cape Town, South Africa,

  • Bindu MS (2010) Empowerment of coastal communities in cultivation and processing of Kappaphycus alvarezii—a case study at Vizhinjam village, Kerala, India. J Appl Phycol 23:157–163

    Article  Google Scholar 

  • Bindu MS, Levine IA (2010) The commercial red seaweed Kappaphycus alvarezii—an overview on farming and environment. J Appl Phycol 23:789–796

    Article  Google Scholar 

  • Bixler HJ, Porse H (2010) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335

    Article  Google Scholar 

  • Bulboa C, de Paula EJ, Chow F (2008) Germination and survival of tetraspores of Kappaphycus alvarezii var. alvarezii (Solieriaceae, Rhodophyta) introduced in subtropical waters of Brazil. Phycol Res 56:39–45

    Article  Google Scholar 

  • Bulboa CR, Paula EJ, Chow F (2007) Laboratory germination and sea out-planting of tetraspore progeny from Kappaphycus striatum (Rhodophyta) in subtropical waters of Brazil. J Appl Phycol 19:357–363

    Article  Google Scholar 

  • Cheney D, Rudolph B, Wang LZ, Metz B, Watson K, Roberts K, Levine I (1998) Genetic manipulation and strain improvement in commercially valuable red seaweeds. In: Le Gal H, Halvorson O (eds) New developments in marine biotechnology. Plenum Press, New York, pp 101–104

    Google Scholar 

  • Conklin KY, Kurihara A, Sherwood AR (2009) A molecular method for identification of the morphologically plastic invasive algal genera Eucheuma and Kappaphycus (Rhodophyta, Gigartinales) in Hawaii. J Appl Phycol 21:691–699

    Article  CAS  Google Scholar 

  • Dang DH, Hoang MH, Ngo HT, Hoang SN, Huynh QN, Tran MD (2008) Analysis of the genetic variation of Eucheuma and Kappaphycus strains in Vietnam using RAPD markers. In: Phang SM, Lewmanomont K, Lim PE (eds) Taxonomy of Southeast Asian seaweeds. Institute of Ocean and Earth Sciences University of Malaya, Kuala Lumpur

    Google Scholar 

  • Doty MS (1985) Eucheuma alvarezii, sp. Nov. (Gigartinales, Rhodophyta) from Malaysia. In: Abbott IA, Norris JN (eds) Taxonomy of economic seaweeds: with reference to some Pacific and Caribbean spcies. California Sea Grant College Program, La Jolla, California, pp 37–45

    Google Scholar 

  • Doty MS, Norris JN (1985) Eucheuma species (Solieriaceae, Rhodophyta) that are major sources of carrageenan. In: Abott IA, Norris JN (eds) Taxonomy of economic seaweeds: with reference to some Pacific and Caribbean species. California Sea Grant College Program, La Jolla, California, pp 47–61

    Google Scholar 

  • Fredericq S, Freshwater DW, Hommersand MH (1999) Observations on the phylogenetic systematics and biogeography of the Solieriaceae (Gigartinales, Rhodophyta) inferred from rbcL sequences and morphological evidence. Hydrobiologia 398/399:25–38

    Article  Google Scholar 

  • Gerung GS, Ohno M (1997) Growth rates of Eucheuma denticulatum (Burman) Collins et Harvey and Kappaphycus striatum (Schmitz) Doty under different conditions in warm waters of Southern Japan. J Appl Phycol 9:413–415

    Article  Google Scholar 

  • Góes HG, Reis RP (2011) Temporal variation of the growth, carrageenan yield and quality of Kappaphycus alvarezii (Rhodophyta, Gigartinales) cultivated at Sepetiba Bay, southeastern Brazilian coast. J Appl Phycol. doi:10.1007/s10811-011-9665-4

  • Hayashi L, Oliveira EC, Bleicher-Lhonneur G, Boulenguer P, Pereira RTL, Seckendorff R, Shimoda VT, Leflamand A, Vallée P, Critchley AT (2007) The effects of selected cultivation conditions on the carrageenan characteristics of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in Ubatuba Bay, São Paulo, Brazil. J Appl Phycol 19:505–511

    Article  CAS  Google Scholar 

  • Huelsenback JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–23114

    Article  Google Scholar 

  • Hurtado AQ, Agbayani RF, Chavoso EAJ (1996) Economics of cultivating Kappaphycus alvarezii using the fixed-bottom line and hanging-long line methods in Pangatan Cays, Caluya, Antique, Philippines. J Appl Phycol 105:105–109

    Article  Google Scholar 

  • Hurtado AQ, Agbayani RF, Sanares R, Castro-Mallare MTR (2001) The seasonality and economic feasibility of cultivating Kappaphycus alvarezii in Panagatan Cays, Caluya, Antique, Philippines. Aquaculture 199:295–310

    Article  Google Scholar 

  • Hurtado AQ, Critchley AT, Trespoey A, Bleicher-Lhonneur G (2008) Growth and carrageenan quality of Kappaphycus striatum var. sacol grown at different stocking densities, duration of culture and depth. J Appl Phycol 20:551–555

    Article  Google Scholar 

  • Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol, 4:18–26

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lim PE, Sakaguci M, Hayunda T, Kogame K, Phang SM, Kawai H (2007) Molecular phylogeny of crustose brown seaweeds (Ralfsiales, Phaeophyceae) inferred from rbcL sequences resulting in proposal for Neoralfsiaceae fam. nov. Phycologia 46:456–466

    Article  Google Scholar 

  • Lluisma AO, Ragan MA (1995) Relationships among Eucheuma denticulatum, Eucheuma isiforme and Kappaphycus alvarezii (Gigartinales, Rhodophyta) based on nuclear ssu-rRNA gene sequences. J Appl Phycol 7:471–477

    Article  Google Scholar 

  • Luhan MRJ, Sollesta H (2010) Growing the reproductive cells (carpospores) of the seaweed, Kappaphycus striatum, in the laboratory until outplanting in the field and maturation to tetrasporophyte. J Appl Phycol 22:579–585

    Article  Google Scholar 

  • Montes HRJ, Pobre KFR, Lluisma AO (2008) Phylogenetic affiliation of the ‘Endong’/‘Spaghetti’ variety of Eucheuma as revealed by molecular data. Philippine Agricultural Scientist 91:86–93

    Google Scholar 

  • Munoz J, Freilepelegrin Y, Robledo D (2004) Mariculture of Kappaphycus alvarezii (Rhodophyta, Solieriaceae) color strains in tropical waters of Yucatán, México. Aquaculture 239:161–177

    Article  Google Scholar 

  • Neish IC (2008) Good argonomy practices for Kappaphycus and Eucheuma: Including an overview of basic biology. SEAPlant.net Monograph HB2F 1008 V3 GAP. 72 pp

  • Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Computer Appl iBiosc 12:357–358

    CAS  Google Scholar 

  • Paula EJ, Pereira R, Ohno M (1999) Strain selection in Kappaphycus alvarezii var. alvarezii (Solieriaceae, Rhodophyta) using tetraspore progeny. J Appl Phycol 11:111–121

    Article  Google Scholar 

  • Phang SM (2006) Seaweed resources in Malaysia: current status and future prospects. Aquat Ecosyst Health Management 9:185–202

    Article  Google Scholar 

  • Phang SM, Yeong HY, Lim PE, Adibi Rahiman MN, Gan KT (2010) Commercial varieties of Kappaphycus and Eucheuma in Malaysia. Malaysian J Sci 29:214–223

    Google Scholar 

  • Pickering T (2006) Advances in seaweed aquaculture among Pacific Island countries. J Appl Phycol 18:227–234

    Article  Google Scholar 

  • Ridley M (2000) Species. In: Genome: the autobiography of a species in 23 chapters. Harper Collins, New York, pp 23–37

  • Russell DJ (1983) Ecology of imported red seaweed Kappaphycus alvarezii (E. striatum Schmitz) on Coconut Island, Oahu, Hawaii. Pac Sci 37:87–107

    Google Scholar 

  • Santelices B (1999) A conceptual framework for marine argonomy. Hydrobiologia 398/399:15–23

    Article  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Shimodaira H, Hasegawa H (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    Article  CAS  Google Scholar 

  • Swofford DL (2003) PAUP*. Phylogenetic Analysis Using Parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.

  • Tanabe AS (2007) Kakusan: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mol Ecol 7:962–964

    Article  CAS  Google Scholar 

  • Thirumaran G, Anantharaman P (2009) Daily growth rate of field farming seaweed Kappaphycus alvarezii (Doty) Doty ex P. Silva in Vellar Estuary. World J Fish Mar Sci 1:144–153

    Google Scholar 

  • Villanueva RD, Romero JB, Montaño MNE, de la Peña PO (2011) Harvest optimization of four Kappaphycus species from the Philippines. Biomass Bioenergy 35:1311–1316

    Article  CAS  Google Scholar 

  • Weiss KM, Buchanan A (2004) Understanding biological complexity: basic concepts and principles. In: Genetics and the logic of evolution. Wiley-LISS, New York, pp 1–43

    Google Scholar 

  • Zhao S, He P (2011) Molecular identification based on ITS sequences for Kappaphycus and Eucheuma cultivated in China. Chinese Oceanol Limnol 29:1287–1296

    Article  CAS  Google Scholar 

  • Zuccarello GC, West JA (2006) Molecular phylogeny of the subfamily Bostrychioideae (Ceramiales, Rhodophyta): subsuming Stictosiphonia and highlighting polyphyly in species of Bostrychia. Phycologia 45:24–36

    Article  Google Scholar 

  • Zuccarello GC, Burger G, West JA, King RJ (1999a) A mitochondrial marker for red algal intraspecific relationships. Mol Ecol 8:1443–1447

    Article  PubMed  CAS  Google Scholar 

  • Zuccarello GC, Critchley AT, Smith J, Sieber V, Lhonneur GB, West JA (2006) Systematics and genetic variation in commercial shape Kappaphycus and shape Eucheuma (Solieriaceae, Rhodophyta). J Appl Phycol 18:643–651

    Article  Google Scholar 

  • Zuccarello GC, West JA, Kamiya M, King RJ (1999b) A rapid method to score plastid haplotypes in red seaweeds and its use in determining parental inheritance of plastids in the red alga Bostrychia (Ceramiales). Hydrobiologia 401:207–214

    Article  CAS  Google Scholar 

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Acknowledgments

We would like to express our sincerest gratitude to the Department of Fisheries Sabah, Associate Prof. Dr. Suhaimi Md. Yasir, En. Adibi Rahiman bin Md. Nor, Japson Wong, and Mr Beh Wong King for their extensive help in seaweed collection. We are grateful to the University of Malaya and the Institute of Earth and Ocean Sciences (IOES) for providing research facilities. Special thanks to IOES members Song Sze Looi, Fiona Keng Seh Lin, Yu Chew Hock, Ng Poh Kheng, and Poong Sze Wan for technical support and advice. This project is funded by the Department of Fisheries Malaysia (Grant Number: 53-02-03-1062) and University of Malaya, PPP (Phylogenetic analysis of Kappaphycus spp. and Eucheuma spp. with the application of various molecular markers; grant number: PV014/2011A).

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Authors and Affiliations

  1. Institute of Ocean and Earth Sciences (IOES), University of Malaya, 50603, Kuala Lumpur, Malaysia

    Ji Tan, Phaik-Eem Lim & Siew-Moi Phang

  2. Institute of Biological Sciences, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Ji Tan, Phaik-Eem Lim & Siew-Moi Phang

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  1. Ji Tan
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Correspondence to Phaik-Eem Lim.

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Tan, J., Lim, PE. & Phang, SM. Phylogenetic relationship of Kappaphycus Doty and Eucheuma J. Agardh (Solieriaceae, Rhodophyta) in Malaysia. J Appl Phycol 25, 13–29 (2013). https://doi.org/10.1007/s10811-012-9833-1

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