Differential acclimation responses to irradiance and temperature in two co-occurring seaweed species in Arctic fjords

  • Johanna Marambio Marine Botany, University of Bremen, Bremen, Germany; Laboratory of Antarctic and Sub-Antarctic Marine Ecosystems, Department of Sciences, University of Magallanes, Punta Arenas, Chile; and Functional Ecology, Alfred Wegener Institute for Polar and Marine Research, Bremerhaven, Germany
  • Kai Bischof Marine Botany, University of Bremen, Bremen, Germany; and Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany
Keywords: Arctic, Desmarestia aculeata, Palmaria palmata, photosynthesis, temperature, irradiance

Abstract

Arctic fjord systems experience large amplitudes of change in temperature and radiation regime due to climate warming and the related decrease in sea ice. The resultant increase in irradiance entering the water column influences photosynthetic activity of benthic and pelagic primary producers. The subtidal brown alga Desmarestia aculeata and the intertidal red alga Palmaria palmata populate the cold-temperate coasts of the North Atlantic, reaching the polar zone. To evaluate their acclimation potential, we collected both species in Kongsfjorden, Svalbard (78.9°N, 11.9°E), during the Arctic summer and exposed specimens to two different PAR levels (50 and 500 μmol photons m−2 s−1) and temperatures (0, 4 and 8 °C) for 21 days. Photosynthetic parameters and biochemical features (pigment concentration and antioxidants) were assessed. In general, high irradiance was the factor that generated a negative effect for D. aculeata and P. palmata in the photosynthetic parameters of the photosynthesis–irradiance curve and Fv/Fm. The pigment concentration in both species tended to decrease with increasing irradiance. Antioxidant level showed different trends for both species: in D. aculeata, antioxidant potential increased with high irradiance and temperature, while in P. palmata, it only increased with high irradiance. Both species showed responses to the interaction of irradiance and temperature, although D. aculeata was more sensitive to high irradiance than P. palmata. Our study shows how these species, which have similar geographical distribution in the North Atlantic and the Arctic but belong to different taxonomic lineages, have similar strategies of acclimation, although they respond differently to ecophysiological parameters.

Downloads

Download data is not yet available.

References


Abdala R.T., Cabello A., Pérez E., Conde R.M. & Figueroa F.L. 2006. Daily and seasonal variations of optimum quantum yield and phenolic compounds in Cystoseira tamariscifolia (Phaeophyta). Marine Biology 148, 459–465, doi: 10.1007/s00227005-0102-6.


Aguilera J., Bischof K., Karsten U., Hanelt D. & Wiencke C. 2002. Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. II. Pigment accumulation and biochemical defence systems against high light stress. Marine Biology 140, 1087–1095, doi: 10.1007/s00227-002-0792-y.


Aro E.M., Virgin I. & Andersson B. 1993. Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113–134, doi: 10.1016/0005-2728(93)90134-2.


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 Biology 39, 2021–2036, doi: 10.1007/s00300-015-1870-1.


Becker S., Walter B. & Bischof K. 2009. Freezing tolerance and photosynthetic performance of polar seaweeds at low temperatures. Botanica Marina 52, 609–616, doi: 10.1515/BOT.2009.079.


Bischof K., Convey P., Duarte P., Gattuso J.P., Granberg M., Hop H., Hoppe C., Jiménez C., Lisitsyn L., Martinez B., Roleda M.Y., Thor P., Wiktor J.M. & Gabrielsen G.W. 2019. Kongsfjorden as harbinger of the future Arctic: knowns, unknowns and research priorities. In H. Hop & C. Wiencke (eds.): The ecosystem of Kongsfjorden, Svalbard. Pp 537–562. Cham, Switzerland: Springer.


Bischof K., Hanelt D., Aguilera J., Karsten U., Vögele B., Sawall T. & Wiencke C. 2002. Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord. I. Sensitivity of photosynthesis to ultraviolet radiation. Marine Biology 140, 1097–1106, doi: 10.1007/s00227-002-0795-8.


Bischof K., Hanelt D. & Wiencke C. 1999. Acclimation of maximal quantum yield of photosynthesis in the brown alga Alaria esculenta und high light and UV radiation. Plant Biology 1, 435–444, doi: 10.1111/j.1438-8677.1999.tb00726.x.


Bjarnadóttir M., Aðalbjörnsson B.V., Nilsson A., Slizyte R., Roleda M.Y., Hreggviðsson G.Ó., Friðjónsson O.H. & Jónsdóttir R. 2018. Palmaria palmata as an alternative protein source: enzymatic protein extraction, amino acid composition, and nitrogen-to-protein conversion factor. Journal of Applied Phycology 30, 2061–2070, doi: 10.1007/s10811-017-1351-8.


Brand-Williams W., Cuvelier M.E. & Berset C. 1995. Use of a free radical method to evaluate antioxidant activity. LWT Food Science and Technology 28, 25–30, doi: 10.1016/S0023-6438(95)80008-5.


Bringloe B., Verbruggenb H., & Saundersa G.W. 2020. Unique biodiversity in Arctic marine forests is shaped by diverse recolonization pathways and far northern glacial refugia. Proceedings of the National Academy of Science of the United States of America 117, 22590–22596, doi: 10.1073/pnas.2002753117.


Chapman A.R.O. & Burrows E.M. 1970. Experimental investigations into the controlling effects of light conditions on the development and growth of Desmarestia aculeata (L.) Lamour. Phycology 9, 103–108, doi: 10.2216/i0031-8884-9-1-103.1.


Colombo-Pallotta M., García E. & Ladah L. 2006. Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. Journal of Phycology 42, 1225–1234, doi: 10.1111/j.1529-8817.2006.00287.x.


Cruces E., Huovinen P. & Gómez I. 2012. Phlorotannin and antioxidant responses upon short-term exposure to UV radiation and elevated temperature in three South Pacific kelps. Photochemistry and Photobiology 88, 58–66, doi: 10.1111/j.1751-1097.2011.01013.x.


Diehl N., Karsten U. & Bischof K. 2020. Impacts of combined temperature and salinity stress on the endemic Arctic brown seaweed Laminaria solidungula J. Agardh. Polar Biology 43, 647–656, doi: 10.1007/s00300-020-02668-5.


Dunton K.H. & Dayton P.K. 1995. The biology of high latitude kelp. In H.R. Skjoldal et al. (eds.): Ecology of fjords and coastal waters. Pp. 499–507. Amsterdam: Elsevier.


Falkowsi P. & La Roche J. 1991. Acclimation to spectral irradiance in algae. Journal of Phycology 27, 8–14, doi: 10.1111/j.0022-3646.1991.00008.x.


Filbee-Dexter K., Wernberg T., Fredriksen S., Norderhaug K.M. & Pedersen M.F. 2019. Arctic kelp forests: diversity, resilience and future. Global and Planetary Change 172, 1–14, doi: 10.1016/j.gloplacha.2018.09.005.


Francis J.A. & Hunter E. 2006. New insight into the disappearing Arctic sea ice. Eos, Transactions American Geophysical Union 87, 509–524, doi: 10.1029/2006EO460001.


Fredriksen S., Karsten U., Bartsch I., Woelfel J., Koblowsky M., Schumann R., Moy S.R., Steneck R.S., Wiktor J.M., Hop H. & Wiencke C. 2019. Biodiversity of benthic macro- and microalgae from Svalbard with special focus on Kongsfjorden. In H. Hop & C. Wiencke (eds.): The ecosystem of Kongsfjorden, Svalbard. Pp. 331–371. Cham, Switzerland: Springer.


Galindo V., Gosselin M., Lavaud J., Mundy C.J., Else B., Ehn J., Babin M. & Rysgaard S. 2017. Pigment composition and photoprotection of Arctic sea ice algae during spring. Marine Ecology Progress Series 585, 49–69, doi: 10.3354/meps1239.


Gordillo F., Carmona R., Viñegla V., Wiencke C. & Jimenez C. 2016. Effects of simultaneous increase in temperature and ocean acidification on biochemical composition and photosynthetic performance of common macroalgae from Kongsfjorden (Svalbard). Polar Biology 39, 1993–2007, doi: 10.1007/s00300-016-1897-y.


Hallerud C.B. 2014. Pigment composition of macroalgae from a Norwegian kelp forest. MSc thesis, Dept. of Biology, Norwegian University of Science and Technology.


Hanelt D. 1998. Capability of dynamic photoinhibition in Arctic macroalgae is related to their depth distribution. Marine Biology 131, 361–369, doi: 10.1007/s002270050329.


Hanelt D. & Nultsch W. 1995. Field studies of photoinhibition show non-correlations between oxygen and fluorescence measurements in the Arctic red alga Palmaria palmata. Journal of Plant Physiology 145, 31–38, doi: 10.1016/S0176-1617(11)81842-0.


Hanelt D., Tüg H., Bischof K., Groß C., Lippert H., Sawall T. & Wiencke C. 2001. Light regime in an Arctic fjord: a study related to stratospheric ozone depletion as a basis for determination of UV effects on algal growth. Marine Biology 138, 649–658, doi: 10.1007/s002270000481.


Hanelt D., Wiencke C. & Bischof K. 2003. Photosynthesis in marine macroalgae. In W.A. Larkum et al. (eds.): Photosynthesis in algae. Vol. 14. Pp. 413–435. Dordrecht, the Netherlands: Kluwer Academic Publishers.


Hashimoto H., Uragami C. & Cogdell R.J. 2016. Carotenoids and photosynthesis. In C. Stange (ed.): Carotenoids in nature: biosynthesis, regulation and function. Pp. 111–139. Cham, Switzerland: Springer.


He M., Hu Y., Chen N., Wang D., Huang J. & Stamnes K. 2019. High cloud coverage over melted areas dominates the impact of clouds on the albedo feedback in the Arctic. Scientific Reports 9, article no. 9529, doi: 10.1038/s41598-019-44155-w.


Heriyanto H., Juliadiningtyas A.D., Shioi Y., Limantara L. & Brotosudarmo T.H.P. 2017. Analysis of pigment composition of brown seaweeds collected from Panjang Island, central Java, Indonesia. Philippine Journal of Science 146, 323–330.


Higgins M.E. & Cassano J.J. 2009. Impacts of reduced sea ice on winter Arctic atmospheric circulation, precipitation, and temperature. Journal of Geophysical ResearchAtmospheres 114, D16107, doi: 10.1029/2009JD011884.


Holzinger A., Lütz C., Karsten U., & Wiencke C. 2004. The effect of ultraviolet radiation on ultrastructure and photosynthesis in the red macroalgae Palmaria palmata and Odonthalia dentata from Arctic waters. Plant Biology 6, 568–577, doi: 10.1055/s-2004-821003.


Hop H., Pearson T., Hegseth E.N., Kovacs K.M., Wiencke C., Kwasniewski S., Eiane K, Mehlum F., Gulliksen B., Kowalczuk M.W., Lydersen C., Weslawski J.M., Cochrane S., Gabrielsen G.W., Leakey R., Lönne O.J., Zajaczkowski M., Petersen S.F., Kendall M., Wängberg S.A., Bischof K., Voronkov Y., Kovaltchouk N.A., Wiktor J., Poltermann M., Prisco G., Papucci C. & Gerland S. 2002. The marine ecosystem of Kongsfjorden, Svalbard. Polar Research 21, 167–208, doi: 10.3402/polar.v21i1.6480.


Hurd C.L., Harrison P.J., Bishof K. & Lobban C.S. (eds.) 2014. Seaweed ecology and physiology. Cambridge: Cambridge University Press.


Iñiguez C., Carmona R., Lorenzo M.R., Niell F.X., Wiencke C. & Gordillo F.J.L. 2015. Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta. Polar Biology 39, 1979–1991, doi: 10.1007/s00300-015-1724-x.


Kain J. & Jones S. 1975. Algal recolonization of some cleared subtidal areas. Journal of Ecology 63, 739–765, doi: 10.2307/2258599.


Karsten U., Bischof K. & Wiencke C. 2001. Photosynthetic performance of Arctic macroalgae after transplantation from deep to shallow waters followed by exposure to natural solar radiation. Oecologia 127, 11–20, doi: 10.1007/s004420000553.


Karsten U., Dummermuth A., Hoyer K. & Wiencke C. 2003. Interactive effects of ultraviolet radiation and salinity on the ecophysiology of two Arctic red algae from shallow waters. Polar Biology 26, 249–258, doi: 10.1007/s00300-002-0462-z.


Karsten U. & Wiencke C. 1999. Factors controlling the formation of UV-absorbing mycosporine-like amino acids in the marine red alga Palmaria palmata from Spitsbergen (Norway). Journal of Plant Physiology 155, 407–415, doi: 10.1016/S0176-1617(99)80124-2.


Koch K., Thiel M., Hagen W., Graeve M., Gómez I., Jofre D., Hoffman L., Tala F. & Bischof K. 2016. Short- and long-term acclimation patterns of the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) along a depth gradient. Journal of Phycology 52, 260–273, doi: 10.1111/jpy.12394.


Koch K., Thiel M., Tellier F., Hagen W., Graeve M., Tala F., Laesecke P. & Bischof K. 2015. Species separation within the Lessonia nigrescens complex (Phaeophyceae, Laminariales) is mirrored by ecophysiological traits. Botanica Marina 58, 81–92, doi: 10.1515/bot-2014-0086.


Koivikko R., Loponen J., Honkanen T. & Jormalainen V. 2005. Contents of soluble, cell-wall-bound and exuded phlorotannins in the brown alga Fucus vesiculosus, with implications on their ecological aspects. Journal of Chemical Ecology 31, 195–212, doi: 10.1007/s10886-005-0984-2.


Krause-Jensen D., Duarte C.M., Hendriks I.E., Meire L., Blicher M.E., Marbà N. & Sejr M.K. 2015. Macroalgae contribute to nested mosaics of pH variability in a Subarctic fjord. Biogeosciences 12, 4895–4911, doi: 10.5194/bg-12-4895-2015.


Kursar T.A., Van der Meer J.P. & Aberte R.S. 1983. Light harvesting system of the red alga Gracilaria tikvahiae. I. Biochemical analyses of pigment mutations. Plant Physiology 73, 353–360, doi: 10.1104/pp.73.2.353


Lahaye M., Michel C. & Barry J.L. 1993. Chemical, physicochemical and in-vitro fermentation characteristics of dietary fibres from Palmaria palmata (L.) Kuntze. Food Chemistry 47, 29–36, doi: 10.1016/0308-8146(93)90298-T.


Lalegerie F., Stiger-Pouvreau V. & Connan S. 2020. Temporal variation in pigment and mycosporine-like amino acid composition of the red macroalga Palmaria palmata from Brittany (France): hypothesis on the MAA biosynthesis pathway under high irradiance. Journal of Applied Phycology 32, 2641–2656, doi: 10.1007/s10811-020-02075-7.


Lee D., Nishizawa M., Shimizu Y. & Saeki H. 2017. Anti-inflammatory effects of dulse (Palmaria palmata) resulting from the simultaneous water-extraction of phycobiliproteins and chlorophyll a. Food Research International 100, 514–521, doi: 10.1016/j.foodres.2017.06.040.


Le Gall L., Pien S. & Rusig A.M. 2004. Cultivation of Palmaria palmata (Palmariales, Rhodophyta) from isolated spores in semi-controlled conditions. Aquaculture 229, 181–191, doi: 10.1016/S0044-8486(03)00390-9.


Li H., Monteiro C., Heinrich S., Bartsch I., Valentin K., Harms L., Glöckner G., Corre E. & Bischof K. 2019. Responses of the kelp Saccharina latissima (Phaeophyceae) to the warming Arctic: from physiology to transcriptomics. Physiologia Plantarum 168, 5–26, doi: 10.1111/ppl.13009.


Lippert H., Iken K., Rachor E. & Wiencke C. 2001. Macrofauna associated with macroalgae in the Kongsfjord (Spitsbergen). Polar Biology 24, 512–522, doi: 10.1007/s003000100250.


Lüder U.H., Wiencke C. & Knoetzel J. 2002. Acclimation of photosynthesis and pigments during and after six months of darkness in Palmaria decipiens (Rhodophyta): a study to stimulate Antarctic winter sea ice cover. Journal of Phycology 38, 904–913, doi: 10.1046/j.1529-8817.2002.t01-1-01071.x.


Lüning K. (ed.) 1990. Seaweeds: their environment, biogeography, and ecophysiology. New York: Wiley.


MacArtain P., Gill C.I.R., Brooks M., Campbell R. & Rowland I.R. 2007. Nutritional value of edible seaweeds. Nutritional Reviews 65, 535–543, doi: 10.1301/nr.2007.dec.535-543.


Mathieson A.C. & Dawes C.J. (eds.) 2017. Seaweeds of the northwest Atlantic. Amherst: University of Massachusetts Press.


Miller G.H., Brigham-Grette J., Anderson L., Henning B., Douglas M. A., Edwards M.E., Elias S., Finney B., Funder S., Herbert T., Hinzman L., Kaufman D. K., MacDonald G., Robock A., Serreze M., Smol J., Spielhagen R., Wolfe A.P. & Wolff E. 2009. Temperature and precipitation history of the Arctic. In Alley R.B. et al. (eds.): Past climate variability and change in the Arctic and at high latitudes. Pp. 77–246. Washington, DC: US Climate Change Science Program.


Müller R., Wiencke C. & Bischof K. 2008. Interactive effects of UV radiation and temperature on microstages of Laminariales (Paheophyceae) from the Arctic and North Sea. Climate Research 37, 203–213, doi: 10.3354/cr00762.


Nielsen R. & Lundsteen S. 2019. Danmarks havalger. Bind 2. Brunalger (Phaeophyceae) og grønalger (Chlorophyta). (Denmark’s sea algae. Vol. 2. Brown algae [Phaeophyceae] and green algae [Chlorophyta].) Scientia Danica. Series B, Biologica 8. Copenhagen: The Royal Danish Academy of Sciences and Letters.


Olischläger M., Iñiguez C., Koch K., Wiencke C. & Gordillo F.J.L. 2017. Increases in pCO2 and temperature reveal ecotypic differences in growth and photosynthetic yield of temperate and Arctic Saccharina latissima. Planta 245, 119–136, doi: 10.1007/s00425-016-2594-3.


Osmond C.B. 1994. What is photoinhibition? Some insights from comparisons of shade and sun plants. In N.R. Baker & J.R. Bowyer (eds.): Photoinhibition of photosynthesis. From the molecular mechanisms to the field. Pp. 1–24. Oxford: BIOS Scientific Publications.


Pehlke C. & Bartsch I. 2008. Changes in depth distribution and biomass of sublittoral seaweeds at Helgoland (North Sea) between 1970 and 2005. Climate Research 37, 135–147, doi: 10.3354/cr00767.


Platt T., Gallegos C.L. & Harrison W.G. 1980. Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal Marine Research 38, 687–701.


Raven J.A. & Hurd C.L. 2012. Ecophysiology of photosynthesis in macroalgae. Photosynthesis Research 113, 105–125, doi: 10.1007/s11120-012-9768-z.


Sagert S. & Schubert H. 2000. Acclimation of Palmaria palmata (Rhodophyta) to light intensity: comparison between artificial and natural light fields. Journal of Phycology 36, 1119–1128, doi: 10.1046/j.1529-8817.2000.99156.x.


Schreiber U., Bilger W. & Neubauer C. 1995. Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. In E.D. Schulze & M.M. Caldwell (eds.): Ecophysiology of photosynthesis. Vol. 100. Pp. 49–70. Berlin: Springer.


Serreze M.C. & Francis J.A. 2006. The Arctic amplification debate. Climatic Change 76, 241–264, doi: 10.1007/s10584-005-9017-y.


Springer K., Lütz C., Lütz-Meindl U., Wendt A. & Bischof K. 2017. Hyposaline conditions affect UV susceptibility in the Arctic kelp Alaria esculenta (Phaeophyceae)—results of laboratory experiments at Kongsfjorden. Phycologia 56, 675–685, doi: 10.2216/16-122.1.


Van De Poll W., Eggert A., Buma A. & Breeman A. 2002. Temperature dependence of UV radiation effects in Arctic and temperate isolates of three red macrophytes. European Journal of Phycology 37, 59–68, doi: 10.1017/S0967026201003407.


Wang T., Jónsdóttir R., Kristinsson H.G., Hreggvidsson G.O., Jónsson J.Ó., Thorkelsson G. & Ólafsdóttir G. 2010. Enzyme-enhanced extraction of antioxidant ingredients from red alga Palmaria palmata. LWT Food Science and Technology 43, 1387–1393, doi: 10.1016/j.lwt.2010.05.010.


Weykam G., Gómez I., Wiencke C., Iken K. & Klöser H. 1996. Photosynthetic characteristics and C:N ratios of macroalgae from King George Island (Antarctica). Journal of Experimental Marine Biology and Ecology 204, 1–22, doi: 10.1016/0022-0981(96)02576-2


Wiencke C. & Amsler C. 2012. Seaweeds and their communities in polar regions. In C. Wiencke & K. Bischof (eds.): Seaweed biology. Novel insights into ecophysiology, ecology and utilization. Pp. 265–291. Berlin: Springer.


Wiencke C., Clayton M.N., Goméz I., Iken K., Lüder U.H., Amsler C.D., Karsten U., Hanelt D., Bischof K. & Dunton K. 2006. Life strategy, ecophysiology and ecology of algae in polar waters. Reviews in Environmental Science and Biotechnology 6, 95–126, doi: 10.1007/s11157-006-9106-z.


Wiencke C., Gómez I. & Dunton K. 2011. Phenology and seasonal physiological performance of polar seaweeds. In C. Wiencke (ed.): Biology of polar benthic algae. Pp. 181–194. Berlin: De Gruyter.


Wiencke C. & Hop H. 2016. Ecosystem Kongsfjorden: new views after more than a decade of research. Polar Biology 39, 1679–1687, doi: 10.1007/s00300-016-2032-9.


Wright S.W., Jeffrey S.W., Mantoura R.F.C., Llewellyn C.A., Bjørnland T., Repeta D. & Welschmeyer N. 1991. Improved HPLC method for the analysis of chlorophylls and carotenoids from marine phytoplankton. Marine Ecology Progress Series 77, 183–96, doi: 10.3354/meps077183.


Wulff A., Iken K., Quartino M.L., Al-Handal A., Wiencke C. & Clayton M.N. 2011. Biodiversity, biogeography and zonation of marine benthic micro- and macroalgae in the Arctic and Antarctic. In C. Wiencke (ed.): Biology of polar benthic algae. Pp. 23–52. Berlin: De Gruyter.


Yuan Y., Westcott N., Gu J. & Kitts D. 2009. Mycosporine-like amino acid composition of the edible red alga, Palmaria palmata (Dulse) harvested from the west and east coasts of Grand Manan Island, New Brunswick. Food Chemistry 112, 321–328, doi: 10.1016/j.foodchem.2008.05.066.


Zacher K., Rautenberger R., Hanelt D., Wulff A. & Wiencke C. 2011. The abiotic environment of polar benthic algae. In C. Wiencke (ed.): Biology of polar benthic algae. Pp. 9–22. Berlin: De Gruyter.
Published
2021-12-21
How to Cite
MarambioJ., & BischofK. (2021). Differential acclimation responses to irradiance and temperature in two co-occurring seaweed species in Arctic fjords. Polar Research, 40. https://doi.org/10.33265/polar.v40.5702
Section
Research Articles