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Journal of Applied Phycology

, Volume 31, Issue 1, pp 547–560 | Cite as

Porphyra umbilicalis in applied and basic research: reproductive phenology, development, seed stock culture, and a field trial for aquaculture

  • Charlotte J. RoyerEmail author
  • Sarah Redmond
  • Chu Shing Lai
  • Susan H. Brawley
Article

Abstract

Porphyra umbilicalis is being developed in the North Atlantic for aquaculture; however, information on nursery stock establishment and maintenance is needed, including when to collect spores (phenology), how to maintain healthy seed stock over multiple generations, and whether reproductively mature blades can be stored at low temperature (− 20 °C) for immediate use “on demand” to seed lines and nets. We evaluated whether spore damage would occur by documenting early developmental patterns of germlings from cold-stored parent blades to control blades. Phenological studies over 300 km of Maine, USA, shore indicated that successful NS production by P. umbilicalis peaks in winter, is greatly reduced in summer, and may be affected by amphipod (Apohyale prevostii) grazers in fall and spring. The pattern of early cell division in germinating neutral spores was affected by donor parent (blade) for a few minor patterns of cell division, but not by cold storage (− 20 °C) of reproductive blades for 6 weeks. Linear development was about four times more common in neutral spore germlings than bilateral development, but variations in pattern of cell division were observed, and these may help to explain the variable morphology of the adult blade. The minimal time required to grow neutral spores to reproductively mature blades in laboratory culture was 62 days; vigorous water motion provided by aeration and immobilization of blades by holdfast clips (versus tumbling) were essential to spore production. Seeded lines produced blades of harvestable size with a substantial understory in a preliminary field trial.

Keywords

Algal culture Macroalgal aquaculture Linear germlings Neutral spores Phenology Porphyra umbilicalis 

Notes

Acknowledgements

We gratefully acknowledge Maine Sea Grant (NOAA Contract NA14OAR4170072) and the NSF (RCN 0741907) for the support of this work. We especially appreciate strong contributions by Charlotte C. T. Quigley (UMaine) to the phenology collections; Rob Cushman for the multiple contributions to the field work, including on the pilot farm; Shepard Erhart (Maine Coast Sea Vegetables, LLC) for the assistance in the field and vision for the development of macroalgal aquaculture; and Luz Kogson (UMaine) for the assistance at CCAR. Other valuable assistance was provided by UMaine undergraduates Margaret Aydlett, Alexandra Pergerson, Eleanor McCarthy, Katlyn Buda, Chad Flickstrom, and Kyle Capistrant-Fossa. Dr. Les Watling (University of Hawaii) helped us identify the amphipods. We are grateful to two anonymous reviewers whose comments improved the manuscript. A portion of this research contributed to Royer’s M.S. thesis at the University of Maine (Royer 2017).

Funders

This work was supported by Maine Sea Grant (National Ocean and Atmospheric Agency [NOAA] Contract NA14OAR4170072) (SHB, PI) and a National Science Foundation Research Collaboration Network 0741907 (SHB, PI).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10811_2018_1538_MOESM1_ESM.docx (3.3 mb)
ESM 1 (DOCX 3332 kb)

References

  1. Andersen RA (ed) (2005) Algal culturing techniques. Elsevier, LondonGoogle Scholar
  2. Andersen RA, Berges JA, Harrisson PJ, Watanabe MM (2005) Recipies for freshwater and seawater media. In: Andersen RA (ed) Algal Culturing Techniques. Elsevier Academic Press, Amsterdam, pp 429–538Google Scholar
  3. Blouin NA, Brawley SH (2012) An AFLP analysis of clonality in widespread asexual populations of Porphyra umbilicalis (Rhodophyta) with a sensitivity analysis for bacterial contamination. Mar Biol 159:2723–2729CrossRefGoogle Scholar
  4. Blouin NA, Fei XG, Peng J, Yarish C, Brawley SH (2007) Seeding nets with neutral spores of the red alga Porphyra umbilicalis (L.) Kützing for use in integrated multi-trophic aquaculture (IMTA). Aquaculture 270:77–91CrossRefGoogle Scholar
  5. Blouin NA, Brodie JA, Grossman AC, Xu P, Brawley SH (2011) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37CrossRefGoogle Scholar
  6. Bousfield EL (1973) Shallow-water gammaridean Amphipoda of New England. Comstock Pub Assoc, IthacaGoogle Scholar
  7. Brawley SH, Fei XG (1987) Studies of mesoherbivory in aquaria and in an unbarricaded mariculture farm on the Chinese coast. J Phycol 23:614–623CrossRefGoogle Scholar
  8. Brawley SH, Blouin NA, Ficko-Blean E, Wheeler GL, Lohr M, Goodson HV, Jenkins JW, Blaby-Haas CE, Helliwell KE, Chan CX, Marriage TN, Bhattacharya D, Klein AS, Badis Y, Brodie J, Cao Y, Collén J, Dittami SM, Gachon CMM, Green BR, Karpowicz SJ, Kim JW, Kudahl UJ, Lin S, Michel G, Mittag M, Olson BJSC, Pangilinan JL, Peng Y, Qiu H, Shu S, Singer JT, Smith AG, Sprecher BN, Wagner V, Wang W, Wang ZY, Yan J, Yarish C, Zäuner-Riek S, Zhuang Y, Zou Y, Lindquist EA, Grimwood J, Barry KW, Rokhsar DS, Schmutz J, Stiller JW, Grossman AR, Prochnik SE (2017) Insights into the red algae and eukaryotic evolution from the genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta). Proc Natl Acad Sci U S A 114(31):E6361–E6370 Includes 106 page SI Appendix CrossRefGoogle Scholar
  9. Brodie J, Irvine L, Neefus CD, Russell S (2008) Ulva umbilicalis L. and Porphyra umbilicalis Kutz. (Rhodophyta, Bangiaceae): a molecular and morphological redescription of the species, with a typification update. Taxon 57:1328–1331CrossRefGoogle Scholar
  10. Carmona R, Kraemer GP, Yarish C (2006) Exploring northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture 252:54–65CrossRefGoogle Scholar
  11. Chapman VJ, Chapman DJ (1980) Seaweeds and their uses, 3rd edn. Chapman and Hall, LondonCrossRefGoogle Scholar
  12. Eriksen RL, Green LA, Klein AS (2016) Genetic variation within and among asexual populations of Porphyra umbilicalis Kützing (Bangiales, Rhodophyta) in the Gulf of Maine, USA. Bot Mar 59:1–12CrossRefGoogle Scholar
  13. Gordon R, Brawley SH (2004) Effects of water motion on propagule release from algae with complex life histories. Mar Biol 145:21–29CrossRefGoogle Scholar
  14. Green LA, Neefus CD (2014) The effects of short- and long-term freezing on Porphyra umbilicalis Kützing (Bangiales, Rhodophyta) blade viability. J Exp Mar Biol Ecol 461:499–503CrossRefGoogle Scholar
  15. Green LA, Neefus CD (2016) Effects of temperature, light level, and photoperiod on the physiology of Porphyra umbilicalis Kützing from the Northwest Atlantic, a candidate for aquaculture. J Appl Phycol 28:1815–1826CrossRefGoogle Scholar
  16. Hannach G, Waaland JR (1989) Growth and morphology of young gametophytes of Porphyra abbottae (Rhodophyta): effects of environmental factors in culture. J Phycol 25:247–254CrossRefGoogle Scholar
  17. Israel A, Levy I, Friedlander M (2006) Experimental tank cultivation of Porphyra in Israel. J Appl Phycol 18:235–240CrossRefGoogle Scholar
  18. Kikuchi N, Arai S, Yoshida G, Shin J-A, Broom JE, Nelson WA, Miyata M (2010) Porphyra migitae sp. nov. (Bangiales, Rhodophyta) from Japan. Phycologia 49:345–354CrossRefGoogle Scholar
  19. Kim JK, Kraemer GP, Neefus CD, Chung IK, Yarish C (2007) Effects of temperature and ammonium on growth, pigment production and nitrogen uptake by four species of Porphyra (Bangiales, Rhodophyta) native to the New England coast. J Appl Phycol 19:431–440CrossRefGoogle Scholar
  20. Kim JK, Yarish C, Hwang EK, Park M, Kim Y (2017) Seaweed aquaculture: cultivation technologies, challenges, and its ecosystem services. Algae 32:1–13CrossRefGoogle Scholar
  21. Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69:1–33CrossRefGoogle Scholar
  22. McBane CD, Croker RA (1983) Animal-algal relationships of the amphipod Hyale nilssoni (Rathke) in the rocky intertidal. J Crustac Biol 3:592–601CrossRefGoogle Scholar
  23. Miranda L, Hutchison K, Grossman A, Brawley SH (2013) Diversity and abundance of the bacterial community of the red macroalga Porphyra umbilicalis: did bacterial farmers produce macroalgae? PLoS One 8(3):e58269CrossRefGoogle Scholar
  24. Mitman GG, van der Meer JP (1994) Meiosis, blade development, and sex determination in Porphyra purpurea (Rhodophyta). J Phycol 30:147–159CrossRefGoogle Scholar
  25. Niwa K, Kato A, Kobiyama A, Kawai H, Aruga Y (2008) Comparative study of wild and cultivated Porphyra yezoensis (Bangiales, Rhodophyta) based on molecular and morphological data. J Appl Phycol 20:261–270CrossRefGoogle Scholar
  26. Niwa K, Kobiyama A, Sakamoto T (2010) Interspecific hybridization in the haploid blade-forming marine crop Porphyra (Bangiales, Rhodophyta): occurrence of allodiploidy in surviving F1 gametophytic blades. J Phycol 46:693–702CrossRefGoogle Scholar
  27. Noda H, Iwata S (1978) Nori Seihin Kojo no Tebiki (A Guide to the Improvement of Nori Products. translators: Mottet, M, Mottet L, Japanese Scientific Liaison, Friday Harbor, WA, 1983, available from Dr. Thomas Mumford in English). National Federation of Nori and Shellfish Fisheries Cooperative Associations, 234 ppGoogle Scholar
  28. Ohme M, Miura A (1988) Tetrad analysis in conchospore germlings of Porphyra yezoensis (Rhodophyta, Bangiales). Plant Sci 57:135–140CrossRefGoogle Scholar
  29. Polne-Fuller M, Gibor A (1984) Developmental studies in Porphyra perforata I. Blade differentiation in Porphyra perforata as expressed by morphology, enzymatic digestion, and protoplast regeneration. J Phycol 20:609–616CrossRefGoogle Scholar
  30. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical computing, ViennaGoogle Scholar
  31. Rhatigan P (2011) Irish seaweed kitchen: the comprehensive guide to healthy everyday cooking with seaweeds. Booklink, NorthamptonGoogle Scholar
  32. Royer, CJ (2017) Advancing development of Porphyra umbilicalis as a red algal model system and aquaculture crop. Master’s Thesis. University of Maine, School of Marine Sciences, USA http://digitalcommons.library.umaine.edu/etd/2683
  33. Sahoo D, Yarish C (2005) Mariculture of seaweeds. In: Andersen RA (ed) Algal culturing techniques. Elsevier, London, pp 219-237Google Scholar
  34. Shearman RK, Lentz SJ (2010) Long-term sea surface temperature variability along the US east coast. J Phys Oceanogr 40:1004–1017CrossRefGoogle Scholar
  35. Stein JR (ed) (1973) Handbook of Phycological Methods. University Press, CambridgeGoogle Scholar
  36. Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi H-G, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151CrossRefGoogle Scholar
  37. Thomas AC, Pershing AJ, Friedland KD, Nye JA, Mills KE, Alexander MA, Record NR, Weatherbee R, Henderson ME (2017) Seasonal trends and phenology shifts in sea surface temperature on the north American northeastern continental shelf. Elem Sci Anth 5:48CrossRefGoogle Scholar
  38. Wang J, Zhu J, Zhou W, Jiang P, Qin S, Xu P (2010) Early development patterns and morphogenesis of blades in four species of Porphyra (Bangiales, Rhodophyta). J Appl Phycol 22:297–303CrossRefGoogle Scholar
  39. Wells ML, Potin P, Craigie JS, Raven JA, Merchant SS, Helliwell KE, Smith AG, Camire ME, Brawley SH (2017) Algae as nutritional and functional food sources: revisiting our understanding. J Appl Phycol 29:949–982CrossRefGoogle Scholar
  40. Yan XH, Li L, Aruga Y (2005) Genetic analysis of the position of meiosis in Porphyra haitanensis Cheng et Zheng (Bangiales, Rhodophyta). J Appl Phycol 17:467–473CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Charlotte J. Royer
    • 1
    • 2
    Email author
  • Sarah Redmond
    • 1
    • 3
  • Chu Shing Lai
    • 4
  • Susan H. Brawley
    • 1
  1. 1.School of Marine SciencesUniversity of MaineOronoUSA
  2. 2.Davis Heart and Lung Research InstituteOhio State UniversityColumbusUSA
  3. 3.Springtide Seaweed LLCSullivanUSA
  4. 4.Department of Mathematics and StatisticsUniversity of MaineOronoUSA

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