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Reproductive output and productivity of filamentous tropical Ulva over time

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Abstract

The production of macroalgae in the tropics requires robust species that tolerate temperature and salinity fluctuations. The widely distributed macroalga Ulva sp. 3 is tolerant of these environmental challenges; however, a reliable source of seedlings and a consistent production of biomass are critical for the sustainable long-term cultivation of this species. Therefore, the objective of this study was to quantify the reproductive output and productivity of multiple cultivation cycles of the asexually reproducing Ulva sp. 3 seeded onto ropes using the harvested biomass of each cycle as the seedstock for each successive generation. The seedstock of three independent collections was assessed across multiple asexual generations in outdoor culture to investigate generational and environmental effects. This study, for the first time, has demonstrated that Ulva sp. 3 can be cultivated successfully over multiple (up to seven) successive generations and highlighted the importance of generational and environmental effects. Notably, there was an order of a magnitude decrease in reproductive output and greater than 4-fold decrease in biomass productivity across generations, while the decrease across cultivation cycles was more pronounced with a greater than 20-fold decrease in reproductive output and an order of a magnitude decrease in biomass productivity. The marked decrease in reproduction and productivity was driven by a generational effect in combination with environmental effect across the multi-generational study and both require consideration for the intensive production of biomass.

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References

  • Alström-Rapaport C, Leskinen E, Pamilo P (2010) Seasonal variation in the mode of reproduction of Ulva intestinalis in a brackish water environment. Aquat Bot 93:244–249

    Article  Google Scholar 

  • Aragón CF, Escudero A, Valladares F (2008) Stress-induced dynamic adjustments of reproduction differentially affect fitness components of a semi-arid plant. J Ecol 96:222–229

    Google Scholar 

  • Bonduriansky R (2012) Rethinking heredity, again. Trends Ecol Evol 27:330–336

    Article  CAS  PubMed  Google Scholar 

  • Bonduriansky R, Day T (2009) Nongenetic inheritance and its evolutionary implications. Annu Rev Ecol Evol Syst 40:103–125

    Article  Google Scholar 

  • Carl C, de Nys R, Paul NA (2014a) The seeding and cultivation of a tropical species of filamentous Ulva for algal biomass production. PLoS One 9(6):e98700

    Article  PubMed  PubMed Central  Google Scholar 

  • Carl C, de Nys R, Lawton RJ, Paul NA (2014b) Methods for the induction of reproduction in a tropical species of filamentous Ulva. PLoS One 9(5):e97396

    Article  PubMed  PubMed Central  Google Scholar 

  • Charrier B, Rolland E, Gupta V, Reddy CRK (2015) Production of genetically and developmentally modified seaweeds: exploiting the potential of artificial selection techniques. Front Plant Sci 6:127

    PubMed  PubMed Central  Google Scholar 

  • Clarke K, Gorley R (2006) PRIMER v6: user manual/tutorial. Primer-E, Plymouth

    Google Scholar 

  • Dan A, Hiraoka M, Ohno M, Critchley AT (2002) Observations on the effect of salinity and photon fluence rate on the induction of sporulation and rhizoid formation in the green alga Enteromorpha prolifera (Müller) J. Agardh (Chlorophyta, Ulvales). Fish Sci 68:1182–1188

    Article  CAS  Google Scholar 

  • de Paula Silva P, de Nys R, Paul NA (2012) Seasonal growth dynamics and resilience of the green tide alga Cladophora coelothrix in high-nutrient tropical aquaculture. Aquac Environ Interact 2:253–266

    Article  Google Scholar 

  • Donohue K, Schmitt J (1998) Maternal environmental effects in plants: adaptive plasticity? In: Mousseau T, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, New York, pp 152–173

    Google Scholar 

  • Edwards MD, Dring MJ (2011) Open-sea cultivation trial of the red alga, Palmaria palmata from seeded tetraspores in Strangford Lough, Northern Ireland. Aquaculture 317:203–209

    Article  Google Scholar 

  • Fletcher RL (1989) A bioassay technique using the marine fouling green alga Enteromorpha. Int Biodeterior 25:407–422

    Article  Google Scholar 

  • Han T, Han Y-S, Kim K-Y, Kim J-H, Shin H-W, Kain JM, Callow JA, Callow ME (2003) Influences of light and UV-B on growth and sporulation of the green alga Ulva pertusa Kjellman. J Exp Mar Biol Ecol 290:115–131

    Article  Google Scholar 

  • Handå A, Forbord S, Wang X, Broch OJ, Dahle SW, Størseth TR, Reitan KI, Olsen Y, Skjermo J (2013) Seasonal- and depth-dependent growth of cultivated kelp (Saccharina latissima) in close proximity to salmon (Salmo salar) aquaculture in Norway. Aquaculture 414–415:191–201

    Article  Google Scholar 

  • Hayden HS, Blomster J, Maggs CA, Silva PC, Stanhope MJ, Waaland JR (2003) Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol 38:277–294

    Article  Google Scholar 

  • Hiraoka M, Shimada S, Ohno M, Serisawa Y (2003a) Asexual life history by quadriflagellate swarmers of Ulva spinulosa (Ulvales, Ulvophyceae). Phycol Res 51:29–34

    Article  Google Scholar 

  • Hiraoka M, Dan A, Shimada S, Hagihira M, Migita M, Ohno M (2003b) Different life histories of Enteromorpha prolifera (Ulvales, Chlorophyta) from four rivers on Shikoku Island, Japan. Phycologia 42:275–284

    Article  Google Scholar 

  • Hiraoka M, Ichihara K, Zhu W, Ma J, Shimada S (2011) Culture and hybridization experiments on an Ulva clade including the Qingdao strain blooming in the Yellow Sea. PLoS One 6(5):e19371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang EK, Baek JM, Park CS (2007) Assessment of optimal depth and photon irradiance for cultivation of the brown alga, Sargassum fulvellum (Turner) C. Agardh. J Appl Phycol 19:787–793

    Article  Google Scholar 

  • Innes DJ, Yarish C (1984) Genetic evidence for the occurrence of asexual reproduction in populations of Enteromorpha linza (L.) J. Ag. (Chlorophyta, Ulvales) from Long Island Sound. Phycologia 23:311–320

    Article  Google Scholar 

  • Kalita TL, Titlyanov EA (2011) The effect of temperature on infradian rhythms of reproduction in Ulva fenestrata Postels et Ruprecht, 1840 (Chlorophyta: Ulvales). Russ J Mar Biol 37:52–61

    Article  Google Scholar 

  • Kalita TL, Tytlianov EA (2003) Effect of temperature and illumination on growth and reproduction of the green alga Ulva fenestrata. Russ J Mar Biol 29:316–322

    Article  Google Scholar 

  • Lawton RJ, Mata L, de Nys R, Paul NA (2013) Algal bioremediation of waste waters from land-based aquaculture using Ulva: selecting target species and strains. PLoS One 8(10):e77344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lüning K, Kadel P, Pang S (2008) Control of reproduction rhythmicity by environmental and endogenous signals in Ulva pseudocurvata (Chlorophyta). J Phycol 44:866–873

    Article  PubMed  Google Scholar 

  • Luo MB, Liu F (2011) Salinity-induced oxidative stress and regulation of antioxidant defense system in the marine macroalga Ulva prolifera. J Exp Mar Bio Ecol 409:223–228

    Article  CAS  Google Scholar 

  • Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24

    Article  CAS  Google Scholar 

  • Makarov MV, Voskoboinikov GM (2001) The influence of ultraviolet-B radiation on spore release and growth of the kelp Laminaria saccharina. Bot Mar 44:89–94

    Article  Google Scholar 

  • Moll B, Deikman J (1995) Enteromorpha clathrata: a potential seawater-irrigated crop. Bioresour Technol 52:255–260

    Article  Google Scholar 

  • Monro K, Poore AGB (2004) Selection in modular organisms: is intraclonal variation in macroalgae evolutionarily important? Am Nat 163:564–578

    Article  PubMed  Google Scholar 

  • Ohno M (1993) Cultivation of the green algae, Monostroma and Enteromorpha “Aonori.”. In: Ohno M, Critchley AT (eds) Seaweed cultivation and marine ranching. Japan International Cooperation Agency, Jokosuka, pp 7–16

    Google Scholar 

  • Ohno M (2006) Recent developments in the seaweed cultivation and industry in Japan. In: Phang SM, Critchley AT, Ang PO (eds) Advances in seaweed cultivation and utilisation in Asia: proceedings of a workshop held in conjunction with the 7th Asian Fisheries Forum. Penang. University of Malaya, Kuala Lumpur, pp 1–20

    Google Scholar 

  • Pang S, Lüning K (2004a) Tank cultivation of the red alga Palmaria palmata: effects of intermittent light on growth rate, yield and growth kinetics. J Appl Phycol 16:93–99

    Article  Google Scholar 

  • Pang SJ, Lüning K (2004b) Breaking seasonal limitation: year-round sporogenesis in the brown alga Laminaria saccharina by blocking the transport of putative sporulation inhibitors. Aquaculture 240:531–541

    Article  Google Scholar 

  • Patwary MU, van der Meer JP (1992) Genetics and breeding of cultivated seaweeds. Korean J Phycol 7:281–318

    Google Scholar 

  • Pearson EA, Murray SN (1997) Patterns of reproduction, genetic diversity, and genetic differentiation in California populations of the geniculate coralline alga Lithothrix aspergillum (Rhodophyta). J Phycol 33:753–763

    Article  Google Scholar 

  • Reddy CRK, Gupta MK, Mantri VA, Jha B (2008a) Seaweed protoplasts: status, biotechnological perspectives and needs. J Appl Phycol 20:619–632

    Article  CAS  Google Scholar 

  • Reddy CRK, Jha B, Fujita Y, Ohno M (2008b) Seaweed micropropagation techniques and their potentials: an overview. J Appl Phycol 20:609–617

    Article  Google Scholar 

  • Riginos C, Heschel MS, Schmitt J (2007) Maternal effects of drought stress and inbreeding in Impatiens capensis (Balsaminaceae). Am J Bot 94:1984–1991

    Article  PubMed  Google Scholar 

  • Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

    Article  Google Scholar 

  • Shan TF, Pang SJ, Gao SQ (2013) Novel means for variety breeding and sporeling production in the brown seaweed Undaria pinnatifida (Phaeophyceae): crossing female gametophytes from parthenosporophytes with male gametophyte clones. Phycol Res 61:154–161

    Article  Google Scholar 

  • Shimada S, Yokoyama N, Arai S, Hiraoka M (2008) Phylogeography of the genus Ulva (Ulvophyceae, Chlorophyta), with special reference to the Japanese freshwater and brackish taxa. J Appl Phycol 20:979–989

    Article  Google Scholar 

  • Sletvold N (2002) Effects of plant size on reproductive output and offspring performance in the facultative biennial Digitalis purpurea. J Ecol 90:958–966

    Article  Google Scholar 

  • Sultan SE (1996) Phenotypic plasticity for offspring traits in Polygonum persicaria. Ecology 77:1791–1807

    Article  Google Scholar 

  • Sultan SE (2001) Phenotypic plasticity for fitness components in Polygonum species of contrasting ecological breadth. Ecology 82:328–343

    Article  Google Scholar 

  • Taylor R, Fletcher RL, Raven JA (2001) Preliminary studies on the growth of selected “green tide” algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Bot Mar 44:327–336

    Article  Google Scholar 

  • Weiner J, Martinez S, Müller-Schärer H, Stoll P, Schmid B (1997) How important are environmental maternal effects in plants? A study with Centaurea maculosa. J Ecol 85:133–142

    Article  Google Scholar 

  • Xu Y, Xie C, Chen C, Ji D, Gao Y (2012) Genetic analyses of six quantitative traits of a doubled haploid population of Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). J Appl Phycol 24:89–96

    Article  Google Scholar 

  • Zhang Q-S, Tang X-X, Cong Y-Z, Qu S-C, Luo S-J, Yang G-P (2007) Breeding of an elite Laminaria variety 90–1 through inter-specific gametophyte crossing. J Appl Phycol 19:303–311

    Article  Google Scholar 

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Acknowledgments

This research is part of the MBD Energy Research and Development program for Biological Carbon Capture and Storage. The project is supported by the Australian Government through the Australian Renewable Energy Agency (ARENA) and the Advanced Manufacturing Cooperative Research Centre (AMCRC), funded through the Australian Government’s Cooperative Research Centre Scheme. We thank M. Martinez, A. Ricketts, B. Bao, Z. Loffler and K. Darlington for assistance with experiments and two anonymous reviewers for their comments on the manuscript.

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Authors and Affiliations

  1. MACRO—the Centre for Macroalgal Resources and Biotechnology, James Cook University, Townsville, Queensland, Australia

    Christina Carl, Rebecca J. Lawton, Nicholas A. Paul & Rocky de Nys

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  1. Christina Carl
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  2. Rebecca J. Lawton
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  3. Nicholas A. Paul
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  4. Rocky de Nys
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Correspondence to Christina Carl.

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Carl, C., Lawton, R.J., Paul, N.A. et al. Reproductive output and productivity of filamentous tropical Ulva over time. J Appl Phycol 28, 429–438 (2016). https://doi.org/10.1007/s10811-015-0589-2

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  • DOI: https://doi.org/10.1007/s10811-015-0589-2

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