Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests

Phenotypic plasticity (genotype × environment interaction) is an especially important means for sessile organisms to cope with environmental variation. While kelps, the globally most productive group of seaweeds, generally possess a wide thermal performance range, kelp populations at their warm dist...

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Published in:Frontiers in Marine Science
Main Authors: Liesner, Daniel, Shama, Lisa N. S., Diehl, Nora, Valentin, Klaus-Ulrich, Bartsch, Inka
Format: Article in Journal/Newspaper
Language:unknown
Published: 2020
Subjects:
Online Access:https://epic.awi.de/id/eprint/52352/
https://epic.awi.de/id/eprint/52352/1/Liesner_etal_2020_FMarS.pdf
https://doi.org/10.3389/fmars.2020.00456
https://hdl.handle.net/10013/epic.35041996-dded-4623-bc0c-5c49167d8e98
https://hdl.handle.net/
id ftawi:oai:epic.awi.de:52352
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spelling ftawi:oai:epic.awi.de:52352 2023-05-15T15:17:38+02:00 Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests Liesner, Daniel Shama, Lisa N. S. Diehl, Nora Valentin, Klaus-Ulrich Bartsch, Inka 2020-06-17 application/pdf https://epic.awi.de/id/eprint/52352/ https://epic.awi.de/id/eprint/52352/1/Liesner_etal_2020_FMarS.pdf https://doi.org/10.3389/fmars.2020.00456 https://hdl.handle.net/10013/epic.35041996-dded-4623-bc0c-5c49167d8e98 https://hdl.handle.net/ unknown https://epic.awi.de/id/eprint/52352/1/Liesner_etal_2020_FMarS.pdf https://hdl.handle.net/ Liesner, D. orcid:0000-0002-2125-9498 , Shama, L. N. S. orcid:0000-0002-9017-9950 , Diehl, N. orcid:0000-0002-7245-340X , Valentin, K. U. orcid:0000-0001-7401-9423 and Bartsch, I. orcid:0000-0001-7609-2149 (2020) Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests , Frontiers in Marine Science, 7 , p. 456 . doi:10.3389/fmars.2020.00456 <https://doi.org/10.3389/fmars.2020.00456> , hdl:10013/epic.35041996-dded-4623-bc0c-5c49167d8e98 EPIC3Frontiers in Marine Science, 7, pp. 456 Article isiRev 2020 ftawi https://doi.org/10.3389/fmars.2020.00456 2021-12-24T15:45:41Z Phenotypic plasticity (genotype × environment interaction) is an especially important means for sessile organisms to cope with environmental variation. While kelps, the globally most productive group of seaweeds, generally possess a wide thermal performance range, kelp populations at their warm distribution limits are threatened by ocean warming. Here, we investigated effects of temperature during ontogeny of the kelp Laminaria digitata across haploid gametophyte and diploid sporophyte life cycle stages in five distinct genetic lines. We hypothesized that thermal plasticity increases trait performance of juvenile sporophytes in experimental temperatures that match the temperature experienced during gametogenesis and recruitment, and that plasticity differs among genetic lines (genetic variation for plasticity). We applied a full-factorial experimental design to generate different temperature histories by applying 5 and 15°C during meiospore germination, gametogenesis of parental gametophytes and recruitment of offspring sporophytes (19–26 days), and juvenile sporophyte rearing (91–122 days). We then tested for thermal plasticity among temperature history treatments at 5 and 15°C in a final 12-day experiment assessing growth, the storage compound mannitol, carbon and nitrogen contents, and fluorometric responses in 3–4 month old sporophytes for five genetic lines. Our study provides evidence for the importance of cold temperatures at early development on later sporophyte performance of L. digitata. Gametogenesis and recruitment at 5°C promoted higher growth of offspring sporophytes across experimental temperatures. While photosynthetic capacity was higher at 15°C, carbon and nitrogen storage were higher at 5°C, both showing fast acclimation responses. We identified an important role of genetic variation for plasticity in shaping L. digitata’s thermal plasticity. Trait performance at 5 or 15°C (reaction norm slopes) differed among genetic lines, even showing opposite response patterns. Interestingly, genetic variation for plasticity was only significant when sporophytes were reared at 5°C. Thus, we provide evidence that the cold-temperate to Arctic kelp species, L. digitata, which possesses a wide temperature tolerance between 0 and 23°C, is impaired by warm temperature during gametogenesis and recruitment, reducing growth of juvenile sporophytes and expression of variable thermal plasticity in the wild. Article in Journal/Newspaper Arctic Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center) Arctic Frontiers in Marine Science 7
institution Open Polar
collection Alfred Wegener Institute for Polar- and Marine Research (AWI): ePIC (electronic Publication Information Center)
op_collection_id ftawi
language unknown
description Phenotypic plasticity (genotype × environment interaction) is an especially important means for sessile organisms to cope with environmental variation. While kelps, the globally most productive group of seaweeds, generally possess a wide thermal performance range, kelp populations at their warm distribution limits are threatened by ocean warming. Here, we investigated effects of temperature during ontogeny of the kelp Laminaria digitata across haploid gametophyte and diploid sporophyte life cycle stages in five distinct genetic lines. We hypothesized that thermal plasticity increases trait performance of juvenile sporophytes in experimental temperatures that match the temperature experienced during gametogenesis and recruitment, and that plasticity differs among genetic lines (genetic variation for plasticity). We applied a full-factorial experimental design to generate different temperature histories by applying 5 and 15°C during meiospore germination, gametogenesis of parental gametophytes and recruitment of offspring sporophytes (19–26 days), and juvenile sporophyte rearing (91–122 days). We then tested for thermal plasticity among temperature history treatments at 5 and 15°C in a final 12-day experiment assessing growth, the storage compound mannitol, carbon and nitrogen contents, and fluorometric responses in 3–4 month old sporophytes for five genetic lines. Our study provides evidence for the importance of cold temperatures at early development on later sporophyte performance of L. digitata. Gametogenesis and recruitment at 5°C promoted higher growth of offspring sporophytes across experimental temperatures. While photosynthetic capacity was higher at 15°C, carbon and nitrogen storage were higher at 5°C, both showing fast acclimation responses. We identified an important role of genetic variation for plasticity in shaping L. digitata’s thermal plasticity. Trait performance at 5 or 15°C (reaction norm slopes) differed among genetic lines, even showing opposite response patterns. Interestingly, genetic variation for plasticity was only significant when sporophytes were reared at 5°C. Thus, we provide evidence that the cold-temperate to Arctic kelp species, L. digitata, which possesses a wide temperature tolerance between 0 and 23°C, is impaired by warm temperature during gametogenesis and recruitment, reducing growth of juvenile sporophytes and expression of variable thermal plasticity in the wild.
format Article in Journal/Newspaper
author Liesner, Daniel
Shama, Lisa N. S.
Diehl, Nora
Valentin, Klaus-Ulrich
Bartsch, Inka
spellingShingle Liesner, Daniel
Shama, Lisa N. S.
Diehl, Nora
Valentin, Klaus-Ulrich
Bartsch, Inka
Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
author_facet Liesner, Daniel
Shama, Lisa N. S.
Diehl, Nora
Valentin, Klaus-Ulrich
Bartsch, Inka
author_sort Liesner, Daniel
title Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
title_short Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
title_full Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
title_fullStr Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
title_full_unstemmed Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests
title_sort thermal plasticity of the kelp laminaria digitata (phaeophyceae) across life cycle stages reveals the importance of cold seasons for marine forests
publishDate 2020
url https://epic.awi.de/id/eprint/52352/
https://epic.awi.de/id/eprint/52352/1/Liesner_etal_2020_FMarS.pdf
https://doi.org/10.3389/fmars.2020.00456
https://hdl.handle.net/10013/epic.35041996-dded-4623-bc0c-5c49167d8e98
https://hdl.handle.net/
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source EPIC3Frontiers in Marine Science, 7, pp. 456
op_relation https://epic.awi.de/id/eprint/52352/1/Liesner_etal_2020_FMarS.pdf
https://hdl.handle.net/
Liesner, D. orcid:0000-0002-2125-9498 , Shama, L. N. S. orcid:0000-0002-9017-9950 , Diehl, N. orcid:0000-0002-7245-340X , Valentin, K. U. orcid:0000-0001-7401-9423 and Bartsch, I. orcid:0000-0001-7609-2149 (2020) Thermal Plasticity of the Kelp Laminaria digitata (Phaeophyceae) Across Life Cycle Stages Reveals the Importance of Cold Seasons for Marine Forests , Frontiers in Marine Science, 7 , p. 456 . doi:10.3389/fmars.2020.00456 <https://doi.org/10.3389/fmars.2020.00456> , hdl:10013/epic.35041996-dded-4623-bc0c-5c49167d8e98
op_doi https://doi.org/10.3389/fmars.2020.00456
container_title Frontiers in Marine Science
container_volume 7
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