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Narrow range of temperature and irradiance supports optimal development of Lessonia corrugata (Ochrophyta) gametophytes: implications for kelp aquaculture and responses to climate change

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Abstract

The kelp Lessonia corrugata (Ochrophyta, Laminariales) is being developed for integrated multi-trophic aquaculture (IMTA) trials in the vicinity of salmon cages in Tasmania, Australia. Gametophytes are vegetally maintained before seeding on hatchery twine; however, the optimal temperature and light conditions for growth and sexual development are unknown. We measured vegetative size of female and male gametophytes and sexual development of females over a range of temperatures and irradiances using a temperature gradient table and neutral density light filters. Over a 4-week experiment, gametophytes were exposed to a combination of thermal (5.7–24.9 °C) and irradiance (10–100 μmol photons m−2 s−1) gradients, to assess biological performance. At the temperature extremes (hottest = 24.9 °C, coldest = 5.7 °C), we observed the critical thermal limits for this species and the results reveal a narrow optimal temperature range for growth and sexual development between 15.7 and 17.9 °C, with irradiances between 40 and 100 μmol photons m−2 s−1 resulting in fertile female gametophytes. Lessonia corrugata inhabits a small geographic range, found only around Tasmania, south of the Australian mainland, hence oceanic changes such as ongoing increases in sea surface temperatures (SSTs), and altered irradiance regimes may limit recruitment of the early microscopic life stages in the future. Our findings provide optimised culture conditions for aquaculture and information to predict the future geographic range of L. corrugata under ocean global change.

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References

  • Allen MR, Dube OP, Solecki W, Aragón-Durand F, Cramer W, Kainuma M, Kala J, Mahowald N, Mulugetta Y, Perez R, Wairiu M, Zickfeld K (2018) Framing and context. In: Global Warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. https://www.ipcc.ch/site/assets/uploads/sites/2/2019/05/SR15_Chapter1_Low_Res.pdf

  • Andrews S, Bennett S, Wernberg T (2014) Reproductive seasonality and early life temperature sensitivity reflect vulnerability of a seaweed undergoing range reduction. Mar Ecol Prog Ser 495:119–129

    Article  Google Scholar 

  • Angilletta MJ (2006) Estimating and comparing thermal performance curves. J Therm Biol 31:541–545

    Article  Google Scholar 

  • Angilletta MJ Jr, Niewiarowski PH, Navas CA (2002) The evolution of thermal physiology in ectotherms. J Therm Biol 27:249–268

    Article  Google Scholar 

  • Arnhold E (2017) easynls: easy nonlinear model. vol R package version. https://cran.r-project.org/web/packages/easynls/easynls.pdf

  • Augyte S, Yarish C, Neefus CD (2019) Thermal and light impacts on the early growth stages of the kelp Saccharina angustissima (Laminariales, Phaeophyceae). Algae 34:153–162

    Article  CAS  Google Scholar 

  • Barrington K, Chopin T, Robinson S (2009) Integrated multi-trophic aquaculture (IMTA) in marine temperate waters. Integrated mariculture: a global review. FAO Fisheries and Aquaculture Technical Paper., vol 529. FAO, Rome

  • Bennett S, Wernberg T (2014) Canopy facilitates seaweed recruitment on subtidal temperate reefs. J Ecol 102:1462–1470

    Article  Google Scholar 

  • Bennett S, Wernberg T, de Bettignies T, Kendrick G, Anderson R, Bolton J, Rodgers K, Shears N, Leclerc J, Lévêque L, Davoult D, Christie H (2015) Canopy interactions and physical stress gradients in subtidal communities. Ecol Lett 18:677–686

    Article  PubMed  Google Scholar 

  • Bennett S, Wernberg T, Connell SD, Hobday AJ, Johnson CR, Poloczanska ES (2016) The 'Great Southern Reef': social, ecological and economic value of Australia's neglected kelp forests. Mar Freshw Res 67:47–56

    Article  Google Scholar 

  • Bennett S, Duarte CM, Marbà N, Wernberg T (2019) Integrating within-species variation in thermal physiology into climate change ecology. Phil Trans Roy Soc B 364:0550

  • Blain C, Shears N (2020) Differential response of forest-forming seaweeds to elevated turbidity may facilitate ecosystem shifts on temperate reefs. Mar Ecol Prog Ser 641:63–77

    Article  Google Scholar 

  • Bolton J (2010) The biogeography of kelps (Laminariales, Phaeophyceae): a global analysis with new insights from recent advances in molecular phylogenetics. Helgol Mar Res 64:263–279

    Article  Google Scholar 

  • Bringloe TT, Bartlett CAB, Bergeron ES, Cripps KSA, Daigle NJ, Gallagher PO, Gallant AD, Giberson ROJ, Greenough SJ, Lamb JM, Leonard TW, Mackay JA, McKenzie AD, Persaud SM, Sheng T, Stack Mills AME, Moore TE, Saunders GW (2018) Detecting Alaria esculenta and Laminaria digitata (Laminariales, Phaeophyceae) gametophytes in red algae, with consideration of distribution patterns in the intertidal zone. Phycologia 57:1–8

    Article  Google Scholar 

  • Buck BH, Nevejan N, Wille M, Chambers MD, Chopin T (2017) Offshore and multi-use aquaculture with extractive species: seaweeds and bivalves. In: Buck B, Langan R (eds) Aquaculture perspective of multi-use sites in the open ocean: the untapped potential for marine resources in the Anthropocene. Springer, Cham, pp 23–69

    Chapter  Google Scholar 

  • Buschmann AH, Troell M, Kautsky N (2001) Integrated algal farming: a review. Cah Biol Mar 42:83–90

    Google Scholar 

  • Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-González JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986

    Article  Google Scholar 

  • Cie DK, Edwards MS (2008) The effects of high irradiance on the settlement competency and viability of kelp zoospores. J Phycol 44:495–500

    Article  PubMed  Google Scholar 

  • de Bettignies T, Wernberg T, Gurgel C (2018) Exploring the influence of temperature on aspects of the reproductive phenology of temperate seaweeds. Front Mar Sci 5:218

    Article  Google Scholar 

  • Deysher LE, Dean TA (1986) In situ recruitment of sporophytes of the giant kelp, Macrocystis pyrifera (L.) C.A. Agardh: Effects of physical factors. J Exp Mar Biol Ecol 103:41–63

    Article  Google Scholar 

  • Durrant HMS, Barrett NS, Edgar GJ, Coleman MA, Burridge CP (2015) Shallow phylogeographic histories of key species in a biodiversity hotspot. Phycologia 54:556–565

    Article  Google Scholar 

  • Edwards MS (2000) The role of alternate life-history stages of a marine macroalga: a seed bank analogue? Ecology 81:2404–2415

    Article  Google Scholar 

  • Edwards P, van Baalen C (1970) An apparatus for the culture of benthic marine algae under varying regimes of temperature and light-intensity. Bot Mar 13:42

    Article  Google Scholar 

  • Edwards and Watson (2011) Aquaculture explained. Cultivating Laminaria digitata. BIM Bord Iascaigh Mhara, Irish Sea Fisheries Board, Dublin, Ireland

  • Fernández PA, Gaitán-Espitia JD, Leal PP, Schmid M, Revill AT, Hurd CL (2020) Nitrogen sufficiency enhances thermal tolerance in habitat-forming kelp: implications for acclimation under thermal stress. Sci Rep 10:3186

    Article  PubMed  PubMed Central  Google Scholar 

  • Flavin K, Flavin N, Flahive B (2013) Kelp farming manual: a guide to the processes, techniques, and equipment for farming kelp in New England waters. Ocean Approved, New England

    Google Scholar 

  • Gaitán-Espitia J, Belén Arias M, Lardies M, Nespolo R (2013) Variation in thermal sensitivity and thermal tolerances in an invasive species across a climatic gradient: lessons from the land snail Cornu aspersum. PLoS One 8:e70662

    Article  PubMed  PubMed Central  Google Scholar 

  • Gaitán-Espitia JD, Bacigalupe LD, Opitz T, Lagos NA, Timmermann T, Lardies MA (2014a) Geographic variation in thermal physiological performance of the intertidal crab Petrolisthes violaceus along a latitudinal gradient. J Exp Biol 217:4379–4386

    PubMed  Google Scholar 

  • Gaitán-Espitia JD, Hancock JR, Padilla-Gamiño JL, Rivest EB, Blanchette CA, Reed DC, Hofmann GE (2014b) Interactive effects of elevated temperature and pCO2 on early-life-history stages of the giant kelp Macrocystis pyrifera. J Exp Mar Biol Ecol 457:51–58

    Article  Google Scholar 

  • Gerard VA (1990) Ecotypic differentiation in the kelp Laminaria saccharina: phase-specific adaptation in a complex life cycle. Mar Biol 107:519–528

    Article  Google Scholar 

  • Harley CDG, Anderson KM, Demes KW, Jorve JP, Kordas RL, Coyle TA, Graham MH (2012) Effects of climate change on global seaweed communities. J Phycol 48:1064–1078

    Article  CAS  PubMed  Google Scholar 

  • Henkel SK, Hofmann GE (2008) Thermal ecophysiology of gametophytes cultured from invasive Undaria pinnatifida (Harvey) Suringar in coastal California harbors. J Exp Mar Biol Ecol 367:164–173

    Article  Google Scholar 

  • Hurd CL, Harrison PJ, Bischof K, Lobban CS (2014) Seaweed ecology and physiology, 2nd edn. Cambridge University Press, UK

    Book  Google Scholar 

  • IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland

  • Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F, Hill KL, Holbrook NJ, Hosie GW, Last PR, Ling SD, Melbourne-Thomas J, Miller K, Pecl GT, Richardson AJ, Ridgway KR, Rintoul SR, Ritz DA, Ross DJ, Sanderson JC, Shepherd SA, Slotwinski A, Swadling KM, Taw N (2011) Climate change cascades: shifts in oceanography, species' ranges and subtidal marine community dynamics in eastern Tasmania. J Exp Mar Biol Ecol 400:17–32

    Article  Google Scholar 

  • Jorda G, Marbà N, Bennett S, Santana-Garcon J, Agusti S, Duarte CM (2020) Ocean warming compresses the three-dimensional habitat of marine life. Nat Ecol Evol 4:109–114

    Article  PubMed  Google Scholar 

  • Krumhansl KA, Okamoto DK, Rassweiler A, Novak M, Bolton JJ, Cavanaugh KC, Connell SD, Johnson CR, Konar B, Ling SD, Micheli F, Norderhaug KM, Pérez-Matus A, Sousa-Pinto I, Reed DC, Salomon AK, Shears NT, Wernberg T, Anderson RJ, Barrett NS, Buschmann AH, Carr MH, Caselle JE, Derrien-Courtel S, Edgar GJ, Edwards M, Estes JA, Goodwin C, Kenner MC, Kushner DJ, Moy FE, Nunn J, Steneck RS, Vásquez J, Watson J, Witman JD, Byrnes JEK (2016) Global patterns of kelp forest change over the past half-century. Proc Natl Acad Sci U S A 113:13785–13790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JA, Brinkhuis BH (1988) Seasonal light and temperature interaction effects on development of Laminaria saccharina (Phaeophyta) gametophytes and juvenile sporophytes. J Phycol 24:181–191

    Article  Google Scholar 

  • Ling SD, Johnson CR, Frusher S, King CK (2008) Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Glob Change Biol 14:907–915

    Article  Google Scholar 

  • Lüning K, Dring MJ (1975) Reproduction, growth and photosynthesis of gametophytes of Laminaria saccharina grown in blue and red light. Mar Biol 29:195–200

    Article  Google Scholar 

  • Lüning K, Neushul M (1978) Light and temperature demands for growth and reproduction of laminarian gametophytes in southern and central California. Mar Biol 45:297–309

    Article  Google Scholar 

  • Mabin CJT, Johnson CR, Wright JT (2019) Family-level variation in early life-cycle traits of kelp. J Phycol 55:380–392

    Article  PubMed  Google Scholar 

  • Maier I, Müller DG, Gassmann G, Boland W, Jaenicke L (1987) Sexual pheromones and related egg secretions in Laminariales (Phaeophyta). Z Naturforsch C 42:948–954

    Article  CAS  Google Scholar 

  • Martínez EA (1999) Latitudinal differences in thermal tolerance among microscopic sporophytes of the kelp Lessonia nigrescens (Phaeophyta: Laminariales). Pac Sci 53:74–81

    Google Scholar 

  • Matson PG, Edwards MS (2007) Effects of ocean temperature on the southern range limits of two understory kelps, Pterygophora californica and Eisenia arborea, at multiple life-stages. Mar Biol 151:1941–1949

    Article  Google Scholar 

  • Mohring MB, Wernberg T, Kendrick GA, Rule MJ (2013) Reproductive synchrony in a habitat-forming kelp and its relationship with environmental conditions. Mar Biol 160:119–126

    Article  Google Scholar 

  • Mohring MB, Wernberg T, Wright JT, Connell SD, Russell BD (2014) Biogeographic variation in temperature drives performance of kelp gametophytes during warming. Mar Ecol Prog Ser 513:85–96

    Article  Google Scholar 

  • Morita T, Kurashima A, Maegawa M (2003) Temperature requirements for the growth and maturation of the gametophytes of Undaria pinnatifida and U. undarioides (Laminariales, Phaeophyceae). Phycol Res 51:154–160

    Google Scholar 

  • Müller DG, Gassmann G, Lüning K (1979) Isolation of a spermatozoid-releasing and -attracting substance from female gametophytes of Laminaria digitata. Nature 279:430–431

    Article  PubMed  Google Scholar 

  • Müller DG, Murúa P, Westermeier R (2019) Reproductive strategies of Lessonia berteroana (Laminariales, Phaeophyceae) gametophytes from Chile: apogamy, parthenogenesis and cross-fertility with L. spicata. J Appl Phycol 31:1475–1481

    Article  Google Scholar 

  • Murúa P, Westermeier R, Patiño DJ, Müller DG (2013) Culture studies on early development of Lessonia trabeculata (Phaeophyceae, Laminariales): seasonality and acclimation to light and temperature. Phycol Res 61:145–153

    Article  Google Scholar 

  • Nelson WA (2005) Life history and growth in culture of the endemic New Zealand kelp Lessonia variegata J. Agardh in response to differing regimes of temperature, photoperiod and light. J App Phycol 17:23–28

    Article  Google Scholar 

  • Oppliger LV, Correa JA, Engelen AH, Tellier F, Vieira V, Faugeron S, Valero M, Gomez G, Destombe C (2012) Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species. PLoS One 7:e39289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ratcliff JJ, Soler-Vila A, Hanniffy D, Johnson MP, Edwards MD (2017) Optimisation of kelp (Laminaria digitata) gametophyte growth and gametogenesis: effects of photoperiod and culture media. J Appl Phycol 29:1957–1966

    Article  CAS  Google Scholar 

  • Ridgeway KR (2007) Long-term trend and decadal variability of the southward penetration of the Eastern Australian Current. Geophys Res Lett 34:L12613

  • Roleda MY (2016) Stress physiology and reproductive phenology of Arctic endemic kelp Laminaria solidungula J. Agardh. Polar Biol 39:1967–1977

    Article  Google Scholar 

  • Roleda MY, Hurd CL (2019) Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation. Phycologia 58:552–562

    Article  CAS  Google Scholar 

  • Sato Y, Endo H, Oikawa H, Kanematsu K, Naka H, Mogamiya M, Kawano S, Kazama Y (2020) Sexual difference in the optimum environmental conditions for growth and maturation of the brown alga Undaria pinnatifida in the gametophyte stage. Genes 11:1–18

    Article  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Meth 9:676–682

    Article  CAS  Google Scholar 

  • Scott FJ (2017) Marine plants of Tasmania. Tasmanian Museum and Art Gallery, Hobart

    Google Scholar 

  • Sievert C (2020) Interactive web-based data visualization with R, plotly, and shiny. https://plotly-r.com/

  • Smale DA (2020) Impacts of ocean warming on kelp forest ecosystems. New Phytol 225:1447–1454

    Article  PubMed  Google Scholar 

  • Smale DA, Burrows MT, Moore P, O'Connor N, Hawkins SJ (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecol Evol 3:4016–4038

    Article  PubMed  PubMed Central  Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Article  Google Scholar 

  • Tait LW (2019) Giant kelp forests at critical light thresholds show compromised ecological resilience to environmental and biological drivers. Estuar Coast Shelf Sci 219:231–241

    Article  Google Scholar 

  • Tatsumi M, Wright JT (2016) Understory algae and low light reduce recruitment of the habitat-forming kelp Ecklonia radiata. Mar Ecol Prog Ser 552:131–143

    Article  CAS  Google Scholar 

  • Thomsen M, Mondardini L, Alestra T, Gerrity S, Tait L, South P, Lilley S, Schiel D (2019) Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front Mar Sci 6:84

  • tom Dieck I (1987) Temperature tolerance and daylength effects in isolates of Scytosiphon lomentaria (Phaeophyceae) of the North Atlantic and Pacific Ocean. Helgol Meeresunters 41:307–321

    Article  Google Scholar 

  • tom Dieck I (1993) Temperature tolerance and survival in darkness of kelp gamtetophytes (Laminariales, Phaeophyta): ecological and biogeographical implications. Mar Ecol Prog Ser 100:253–264

    Article  Google Scholar 

  • Wade R, Augyte S, Harden M, Nuzhdin S, Yarish C, Alberto F (2020) Macroalgal germplasm banking for conservation, food security, and industry. PLoS Biol 18:e3000641

    Article  PubMed  PubMed Central  Google Scholar 

  • Wernberg T, Thomsen MS, Tuya F, Kendrick GA, Staehr PA, Toohey BD (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecol Lett 13:685–694

    Article  PubMed  Google Scholar 

  • Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832

    Article  CAS  PubMed  Google Scholar 

  • Wiencke C (1990) Seasonality of brown macroalgae from Antarctica-a long-term culture study under fluctuating Antarctic daylengths. Polar Biol 10:589–600

    Article  Google Scholar 

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Acknowledgements

We thank Damon Britton, Fanny Noisette and Abigail Smith for the help in both the field and IMAS laboratories and Cathy Johnston, Ros Watson and Kim Lee Chang (CSIRO algal laboratory) for use of their temperature gradient table and laboratory support. We also thank Wouter Visch and Bradley Evans for their feedback on the manuscript.

Funding

The project was funded by Tassal Pty Ltd. and the FRDC project ID: 2017-177. MS was supported by funding from Deutsche Forschungsgemeinschaft (DFG, grant ID: SCHM 3335/1-1). JDGE was supported by the Research Grants Council (ECS 27124318) of Hong Kong.

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Authors and Affiliations

  1. Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS 7001, Australia

    Ellie R. Paine, Matthias Schmid, Joshua Castle & Catriona L. Hurd

  2. SWIRE Institute of Marine Sciences & School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, SAR, China

    Juan Diego Gaitán-Espitia

  3. CSIRO Oceans and Atmosphere, Castray Esplanade, Hobart, TAS 7001, Australia

    Ian Jameson

  4. Tassal Group Limited, Hobart, TAS 7001, Australia

    John C. Sanderson

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  1. Ellie R. Paine
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Contributions

E. Paine: experimental design, conducted experiments, drafting and editing of manuscript; M. Schmid: experimental design, laboratory assistance, editing manuscript; J. D. Gaitán-Espitia: data analysis and graph creation; J. Castle: analysis of images; Ian Jameson: laboratory facilities and assistance; J. C. Sanderson: original concept, experimental design; C. Hurd: original concept, experimental design, editing manuscript.

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Paine, E.R., Schmid, M., Gaitán-Espitia, J.D. et al. Narrow range of temperature and irradiance supports optimal development of Lessonia corrugata (Ochrophyta) gametophytes: implications for kelp aquaculture and responses to climate change. J Appl Phycol 33, 1721–1730 (2021). https://doi.org/10.1007/s10811-021-02382-7

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