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Variation of isotope composition in kelps from Kongsfjorden (Svalbard)

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Abstract

Kelp-derived detritus is a potential food item at the base level of marine food webs. A good knowledge of the factors that influence stable isotope composition in kelps is essential for reliable food web models. The variation of stable isotope signatures was analysed in three species of kelp in Kongsfjorden, Svalbard. Between 15 and 2.5 m depth, towards higher photon fluence rate, Alaria esculenta was gradually enriched in 13C while 15N did not change. The carbon/nitrogen ratio decreased with depth. 2- and 3-year-old kelp individuals had significantly higher δ15N values in their blades than 5- and 6-year-old ones. C/N ratio in blades remained statistically the same over the range of 2–6 years old plants. A two-way ANOVA did not show any interactive effects between depth and age group. A. esculenta as well as Saccharina latissima and Laminaria digitata exhibited enrichment in heavy carbon isotopes in the blades compared to the stipes, while within each species, δ15N values remained the same between blades and stipes. A more detailed analysis of kelp blades showed that independent of location in the fjord, year or season, and species, young tissue was more enriched in 13C than meristem and that decaying apical tissue was depleted relative to young tissue. The degree of this 13C depletion varied with kelp species. Meristem tissue appeared most uniform in the blades compared to young and decaying tissues and its δ13C signature was characteristic for each species with no significant difference in δ15N values. Decaying tissue showed no difference in δ13C between species. Carbon and nitrogen contents along the blades were species-specific and varied with growing location and year or season. Some advice is given on the temporal, spatial, and tissue-related choice of samples for different research objectives.

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Notes

  1. Ribulose 1,5-biphosphate carboxylase-oxygenase.

  2. Phosphoenolpyruvate carboxykinase.

References

  • Bartsch I, Paar M, Fredriksen S, Schwanitz M, Daniel C, Hop H, Wiencke C (2016) Changes in kelp forest biomass and depth distribution in Kongsfjorden, Svalbard, between 1996–1998 and 2012–2014 reflect Arctic warming. Polar Biol 39:2021–2036. https://doi.org/10.1007/s00300-015-1870-1

    Article  Google Scholar 

  • Bengtsson MM, Sjøtun K, Storesund JE, Øvreås L (2011) Utilization of kelp-derived carbon sources by kelp surface-associated bacteria. Aquat MicrobEcol 62:191–199

    Article  Google Scholar 

  • Black WAP (1950) The seasonal variation in weight and chemical composition of the common British Laminariaceae. J Mar Biol Assoc UK 29:45–72

    Article  CAS  Google Scholar 

  • Bode A, Alvarez-Ossorio MT, Varela M (2006) Phytoplankton and macrophyte contributions to littoral food webs in the Galician upwelling estimated from stable isotopes. Mar Ecol Prog Ser 318:89–102

    Article  CAS  Google Scholar 

  • Buchholz C, Wiencke C (2016) Working on a baseline for the Kongsfjorden food web: production and properties of macroalgal particulate organic matter (POM). Polar Biol 39:2053–2064. https://doi.org/10.1007/s00300-015-1828-3

    Article  Google Scholar 

  • Bustamante RH, Branch GM (1996) The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. J Exp Mar Biol Ecol 196:1–28

    Article  Google Scholar 

  • Cabello-Pasini A, Alberte RS (2001) Expression of carboxylating enzymes in Laminaria setchellii (Phaeophyceae). Phycologia 40:351–358

    Article  Google Scholar 

  • Conover J, Green LA, Thornber CS (2016) Biomass decay rates and tissue nutrient loss in bloom and non-bloom-forming macroalgal species. Estuar Coast Shelf Sci 178:58–64

    Article  CAS  Google Scholar 

  • Corre S, Prieur D, Chamroux S, Floch J-Y, Hourmant A (1989) Étude préliminaire des communautés bactériennes épiphytes de Laminaria digitata. Can J Microbiol 35:740–743. https://doi.org/10.1139/m89-121

    Article  Google Scholar 

  • Dankworth M, Heinrich S, Fredriksen S, Bartsch I (2019) DNA barcoding and mucilage ducts in the stipe reveal the presence of Saccharina nigripes (Laminariales, Phaeophyceae) in Kongsfjorden (Spitsbergen). J Phycol (in press)

  • Davison IR, Stewart WDP (1983) Occurrence and significance of nitrogen transport in the brown alga Laminaria digitata. Mar Biol 77:107–112

    Article  CAS  Google Scholar 

  • Dethier MN, Sosik EA, Galloway AWE, Duggins DO, Simenstad CA (2013) Addressing assumptions: variation in stable isotopes and fatty acids of marine macrophytes can confound conclusions of food web studies. Mar Ecol Prog Ser 478:1–14

    Article  CAS  Google Scholar 

  • Drobnitch ST, Nickols KJ, Edwards MS, Bay M (2016) Abiotic influences on bicarbonate use in the giant kelp, Macrocystis pyrifera, in the Monterey Bay. J Phycol 53:85–94. https://doi.org/10.1111/jpy.12480

    Article  CAS  PubMed  Google Scholar 

  • Drobnitch ST, Pochron T, Miranda C (2018) Patterns and drivers of δ13C variation in the giant kelp, Macrocystis pyrifera. Limnol Oceanogr 63:871–885. https://doi.org/10.1002/lno.10675

    Article  Google Scholar 

  • Dunton KH (2001) δ13C and δ15N measurements of Antarctic Peninsula Fauna: trophic relationships and assimilation of benthic seaweeds. Am Zool 41:99–112

    Google Scholar 

  • Dunton KH, Dayton PK (1995) The biology of high latitude kelp. Ecology of Fjords and Coastal Waters. In: Skoldal HR (ed) Proceedings of the Mare Nor Symposium on the Ecology of Fjords and Coastal Waters, Tromsoe, Norway, 5–9 Dec 1994, pp. 499–508

  • Filbee-Dexter K, Wernberg T, Norderhaug KM, Ramirez-Llodra E, Pedersen MF (2018) Movement of pulsed resource subsidies from kelp forests to deep fjords. Oecologia 187:291–304. https://doi.org/10.1007/s00442-018-4121-7

    Article  PubMed  Google Scholar 

  • Filbee-Dexter K, Wernberg T, Fredriksen S, Norderhaug KM, Pedersen MF (2019) Arctic kelp forests: diversity, resilience and future. Glob Planet Chang 172:1–14

    Article  Google Scholar 

  • Finlay JC, Power ME, Cabana G (1999) Effects of water velocity on algal carbon isotope ratios: implications for river food web studies. Limnol Oceanogr 44:1198–1203

    Article  Google Scholar 

  • Fischer G, Wiencke C (1992) Stable carbon isotope composition, depth distribution and fate of macroalgae from the Antarctic Peninsula region. Polar Biol 12:341–348

    Article  Google Scholar 

  • Flynn KJ, Mitra A, Bode A (2018) Toward a mechanistic understanding of trophic structure: inferences from simulating stable isotope ratios. Mar Biol 165:147. https://doi.org/10.1007/s00227-018-3405-0

    Article  PubMed  PubMed Central  Google Scholar 

  • Fox MD (2013) Resource translocation drives δ13C fractionation during recovery from disturbance in giant kelp, Macrocystis pyrifera. J Phycol 49:811–815. https://doi.org/10.1111/jpy.12099

    Article  CAS  PubMed  Google Scholar 

  • Fredriksen S (2003) Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Mar Ecol Prog Ser 260:71–81

    Article  CAS  Google Scholar 

  • Fry B (2002) Conservative mixing of stable isotopes across estuarine salinity gradients: a conceptual framework for monitoring watershed influences on downstream fisheries production. Estuaries 25:264–271

    Article  Google Scholar 

  • Germann I (1989) Aspects of carbon metabolism in relation to autumnal blade abscission in the kelp Pleurophycus gardneri (Phaeophyceae, Laminariales). Mar Ecol Prog Ser 54:179–188

    Article  CAS  Google Scholar 

  • Goecke F, Labes A, Wiese J, Imhoff J (2010) Chemical interactions between marine macroalgae and bacteria. Mar Ecol Prog Ser 409:267–300

    Article  CAS  Google Scholar 

  • Hardison AK, Canuel EA, Anderson IC, Veuger B (2010) Fate of macroalgae in benthic systems: carbon and nitrogen cycling within the microbial community. Mar Ecol Prog Ser 414:41–55

    Article  CAS  Google Scholar 

  • Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Cah Biol Mar 42:71–82

    Google Scholar 

  • Harrison PJ, Druehl LD, Lloyd KE, Thompson PA (1986) Nitrogen uptake kinetics in three year-classes of Laminaria groenlandica (Laminariales: Phaeophyta). Mar Biol 93:29–35

    Article  CAS  Google Scholar 

  • Haug A, Jensen A (1954) Seasonal variations in chemical composition of Alaria esculenta, Laminaria saccharina. Laminaria hyperborea and Laminaria digitata from northern Norway, Nor Inst Seaweed Res Rep No, p 4

    Google Scholar 

  • Hegseth EN, Tverberg V (2013) Effect of Atlantic water inflow on timing of the phytoplankton spring bloom in a high Arctic fjord (Kongsfjorden, Svalbard). J Mar Sys 113:94–105

    Article  Google Scholar 

  • Hill JM, McQuaid CD (2008) δ13C and δ15N biogeographic trends in rocky intertidal communities along the coast of South Africa: evidence of strong environmental signatures. Estuar Coast Shelf Sci 80:261–268

    Article  Google Scholar 

  • Hollohan BT, Dabinett PE, Gow JA (1986) Bacterial succession during biodegradation of the kelp Alaria esculenta (L.) Greville. Can J Microbiol 32:505–512

    Article  Google Scholar 

  • Holst Hansen J, Berg Hedeholm R, Sünksen K, Tang Christensen J, Grønkjær P (2012) Spatial variability of carbon (δ13C) and nitrogen (δ15N) stable isotope ratios in an Arctic marine food web. Mar Ecol Prog Ser 467:47–59

    Article  Google Scholar 

  • Hunter RD (1976) Changes in carbon and nitrogen content during decomposition of three macrophytes in freshwater and marine environments. Hydrobiologia 51:119–128

    Article  Google Scholar 

  • Jain A, Krishnan KP (2017) A glimpse of the diversity of complex polysaccharide-degrading culturable bacteria from Kongsfjorden, Arctic Ocean. Ann Microbiol 67:203–214

    Article  CAS  Google Scholar 

  • Kaehler S, Pakhomov EA, McQuaid CD (2000) Trophic structure of the marine food web at the Prince Edward Islands (Southern Ocean) determined by δ13C and δ15N analysis. Mar Ecol Prog Ser 208:13–20

    Article  Google Scholar 

  • Kaehler S, Pakhomov EA, Kalin RM, Davis S (2006) Trophic importance of kelp-derived suspended particulate matter in a through-flow sub-Antarctic system. Mar Ecol Prog Ser 316:17–22

    Article  CAS  Google Scholar 

  • Krause-Jensen D, Duarte CM (2016) Substantial role of macroalgae in marine carbon sequestration. Nat Geosci 9:737–742

    Article  CAS  Google Scholar 

  • Krumhansl KA, Scheibling RE (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302

    Article  Google Scholar 

  • Küppers U, Kremer BP (1978) Longitudinal profiles of carbon dioxide fixation capacities in marine macroalgae. Plant Physiol 62:49–53

    Article  Google Scholar 

  • Lawrence JM, McClintock JB (1988) Allocation of organic material and energy to the holdfast, stipe, and fronds in Postelsia palmaeformis (Phaeophyta: Laminariales) on the California coast. Mar Biol 99:151–155

    Article  CAS  Google Scholar 

  • Laycock RA (1974) The detrital food chain based on seaweeds. I. Bacteria associated with the surface of Laminaria fronds. Mar Biol 25:223–231

    Article  Google Scholar 

  • Leclerc JC, Riera P, Leroux C, Lévêque L, Laurans M, Schaal G, Davoult D (2013a) Trophic significance of kelps in kelp communities in Brittany (France) inferred from isotopic comparisons. Mar Biol 160:3249–3258

    Article  Google Scholar 

  • Leclerc JC, Riera P, Leroux C, Lévêque L, Davoult D (2013b) Temporal variation in organic matter supply in kelp forests: linking structure to trophic functioning. Mar Ecol Prog Ser 494:87–105

    Article  CAS  Google Scholar 

  • Lund L (2014) Morphological diversity in Laminaria digitata: different species or different phenotypes? Master thesis, Norwegian University of Science and Technology, Trondheim, Norway

  • Martin M, Portelle D, Michel G, Vandenbol M (2014) Microorganisms living on macroalgae: diversity, interactions, and biotechnological applications. Appl Microbiol Biotechnol 98:2917–2935

    Article  CAS  Google Scholar 

  • Mizuta H, Maita Y, Yanada M (1992) Seasonal changes of nitrogen in the sporophyte of Laminaria japonica (Phaeophyceae). Nippon Suisan Gakk 58:2345–2350

    Article  CAS  Google Scholar 

  • Mizuta H, Maita Y, Kuwada K (1994) Nitrogen recycling mechanism within the thallus of Laminaria japonica (Phaeophyceae) under nitrogen limitation. Fish Sci 60:763–767

    Article  CAS  Google Scholar 

  • Norderhaug KM, Fredriksen S, Nygaard K (2003) Trophic importance of Laminaria hyperborea to kelp forest consumers and the importance of bacterial degradation to food quality. Mar Ecol Prog Ser 255:135–144

    Article  CAS  Google Scholar 

  • Norderhaug KM, Nygaard K, Fredriksen S (2006) Importance of phlorotannin content and C:N ratio of Laminaria hyperborea in determining its palatability as food for consumers. Mar Biol Res 2:367–371

    Article  Google Scholar 

  • O’Leary MH (1988) Carbon Isotopes in photosynthesis: fractionation techniques may reveal new aspects of carbon dynamics in plants. BioScience 38(5):328–336

    Article  CAS  Google Scholar 

  • Ramshaw BC, Pakhomov EA, Markel RW, Kaehler S (2017) Quantifying spatial and temporal variations in phytoplankton and kelp isotopic signatures to estimate the distribution of kelp-derived detritus off the west coast of Vancouver Island, Canada. Limnol Oceanogr 62:2133–2153. https://doi.org/10.1002/lno.10555

    Article  Google Scholar 

  • Renaud PE, Løkken TS, Jørgensen LL, Berge J, Johnson BJ (2015) Macroalgal detritus and food-web subsidies along an Arctic fjord depth-gradient. Front Mar Sci 2:31

    Article  Google Scholar 

  • Schaal G, Riera P, Leroux C (2010) Trophic ecology in a Northern Brittany (Batz Island, France) kelp (Laminaria digitata) forest, as investigated through stable isotopes and chemical assays. J Sea Res 63:24–35

    Article  CAS  Google Scholar 

  • Schiener P, Black KD, Ms S, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373

    Article  CAS  Google Scholar 

  • Schmid M, Stengel DB (2015) Intra-thallus differentiation of fatty acid and pigment profiles in some temperate Fucales and Laminariales. J Phycol 51:25–36

    Article  CAS  Google Scholar 

  • Schmitz K, Lobban CS (1976) A survey of translocation in Laminariales (Phaeophyceae). Mar Biol 36:207–2016

    Article  Google Scholar 

  • Simenstad CA, Duggins DO, Quay PD (1993) High turnover of inorganic carbon in kelp habitats as a cause of δ13C variability in marine food webs. Mar Biol 116:147–160

    Article  CAS  Google Scholar 

  • Sjøtun K, Fredriksen S, Rueness J (1996) Seasonal growth and carbon and nitrogen content in canopy and first-year plants of Laminaria hyperborea (Laminariales, Phaeophyceae). Phycologia 35:1–8

    Article  Google Scholar 

  • Smith BD, Foreman RE (1984) An assessment of seaweed decomposition within a southern Strait of Georgia seaweed community. Mar Biol 84:197–205

    Article  Google Scholar 

  • Sokołowski A, Szczepańska A, Richard P, Kędra M, Wołowicz M, Węsławski JM (2014) Trophic structure of the macrobenthic community of Hornsund, Spitsbergen, based on the determination of stable carbon and nitrogen isotopic signatures. Polar Biol 37(9):1247–1260. https://doi.org/10.1007/s00300-014-1517-7

    Article  Google Scholar 

  • Stephenson RL, Tan FC, Mann KH (1984) Stable carbon isotope variability in marine macrophytes and its implications for food web studies. Mar Biol 81:223–230

    Article  CAS  Google Scholar 

  • Surif MB, Raven JA (1990) Photosynthetic gas exchange under emersed conditions in eulittoral and normally submersed members of the Fucales and the Laminariales: interpretation in relation to C isotope ratio and N and water use efficiency. Oecologia 82:68–80. https://doi.org/10.1007/BF00318535

    Article  PubMed  Google Scholar 

  • Svendsen H, Beszczynska-Møller A, Hagen JO, Lefauconnier B, Tverberg V, Gerland S, Ørbæk JB, Bischof K, Papucci C, Zajaczkowski M, Azzolini R, Brunland O, Wiencke C, Winther J-G, Dallmann W (2002) The physical environment of Kongsfjorden-Krossfjorden, an Arctic fjord system in Svalbard. Polar Res 21:133–166

    Google Scholar 

  • Tallis H (2009) Kelp and rivers subsidize rocky intertidal communities in the Pacific Northwest (USA). Mar Ecol Prog Ser 389:85–96

    Article  Google Scholar 

  • Teagle H, Hawkins SJ, Moore PJ, Smale DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. J Exp Mar Biol Ecol 492:81–98. https://doi.org/10.1016/j.jembe.2017.01.017

    Article  Google Scholar 

  • von Biela VR, Newsome SD, Bodkin JL, Kruse GH, Zimmerman CE (2016) Widespread kelp-derived carbon in pelagic and benthic nearshore fishes suggested by stable isotope analysis. Estuar Coast Shelf Sci 181:364–374. https://doi.org/10.1016/j.ecss.2016.08.039

    Article  CAS  Google Scholar 

  • Wernberg T, Krumhansl K, Filbee-Dexter K, Pedersen F (2019) Status and trends for the world’s kelp forests. In: Sheppard C (ed) World seas: an environmental evaluation, 2nd edn. Academic Press, New York, pp 57–78

    Chapter  Google Scholar 

  • Wiencke C, Fischer G (1990) Growth and stable carbon isotope composition of cold-water macroalgae in relation to light and temperature. Mar Ecol Prog Ser 65:283–292

    Article  Google Scholar 

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Acknowledgements

This research was performed at the Ny-Ålesund International Research and Monitoring Facility on Spitsbergen (Svalbard) as part of the KOL06 long term project. We are grateful for the logistic support from all AWIPEV teams. We wish to thank Max Schwanitz and several AWI diving teams as well as Ines Stuhldreier and Claudia Daniel for their reliable and diligent help with sampling. Thanks to Gaël Guillou, stable isotope analysis was conducted with utmost precision. We greatly appreciate the time two anonymous reviewers and the editor spent on reading the manuscript and their constructive criticism!

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  1. Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany

    Cornelia M. Buchholz, Inka Bartsch & Christian Wiencke

  2. UMR Littoral, Environment and Societies, CNRS, University of La Rochelle, Institut du Littoral et de l’Environnement, 2 Rue Olympe de Gouges, 17000, La Rochelle, France

    Benoit Lebreton

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  1. Cornelia M. Buchholz
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Buchholz, C.M., Lebreton, B., Bartsch, I. et al. Variation of isotope composition in kelps from Kongsfjorden (Svalbard). Mar Biol 166, 71 (2019). https://doi.org/10.1007/s00227-019-3513-5

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