Marine Biology

, Volume 161, Issue 8, pp 1895–1904 | Cite as

Juvenile life stages of the brown alga Fucus serratus L. are more sensitive to combined stress from high copper concentration and temperature than adults

  • Søren Laurentius NielsenEmail author
  • Hanne Dalsgaard Nielsen
  • Morten Foldager Pedersen
Original Paper


The combined effects of exposure to copper and temperature were investigated in adult specimens and germlings of the canopy-forming brown alga Fucus serratus. A matrix of four temperatures, 6, 12, 17 and 22 °C, and three concentrations of copper, 0, 100 and 1,000 nM total copper were used. Measured endpoints were growth rate, chlorophyll fluorescence parameters and for germlings also survival. The growth rate of adult specimens of F. serratus changed with increasing temperature. Growth tended to be negatively affected by high concentrations of copper when exposed to heat (22 °C) though not significantly so. The photosynthetic performance (i.e., chlorophyll fluorescence parameters: F v/F m, maximum electron transport rate (ETRmax) and maximum non-photosynthetic quenching (NPQmax) of adults was largely unaffected by both copper and temperature. Germling survival, growth rate and chlorophyll fluorescence parameters were affected by the combination of copper concentration and temperature. Increasing temperature led to reduced survival, increased rhizoid growth and higher F v/F m and ETRmax, whereas high copper concentration had a negative effect on the latter three endpoints. The negative effect of high copper concentration was amplified by high temperature. We conclude that juveniles of F. serratus are more susceptible to environmental stressors than adult specimens and recommend therefore including early life stages when assessing the risk of exposure to toxic compounds. Considering the response of adult specimens only may lead to false conclusions regarding the ecological impact of environmental stress.


Light Emit Diode Chlorophyll Fluorescence Relative Growth Rate Copper Concentration Brown Alga 
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HDN was supported by a grant from the Danish Natural Science Research Council. The council had no involvement in study design, data collection and interpretation, or writing and submitting the paper. We thank Theresa Fernandes and Paul Tett at Napier University, Edinburgh, for housing and supporting HDN during work on this project. We thank Dr. Gary T. Banta for advice on statistical methods.


  1. Adey WH, Steneck RS (2001) Thermogeography over time creates biogeographic regions: a temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae. J Phycol 37:677–698CrossRefGoogle Scholar
  2. Altamirano M, Flores-Moya A, Figueroa FL (2003) Effects of UV radiation and temperature on growth of germlings of three species of Fucus (Phaeophyceae). Aquat Bot 75:9–20CrossRefGoogle Scholar
  3. Andersen GS, Pedersen MF, Nielsen SL (2013) Temperature acclimation and heat tolerance of photosynthesis in Norwegian Saccharina latissima (Laminariales, Phaeophyceae). J Phycol 49:689–700CrossRefGoogle Scholar
  4. Anderson WH, Gorley RN, Clarke KR (2008) Permanova + for Primer. Guide to software and statistical methods. PRIMER-E Ltd., PlymouthGoogle Scholar
  5. Andersson S, Kautsky L (1996) Copper effects on reproductive stages of Baltic Sea fucus vesiculosus. Mar Biol 125:171–176CrossRefGoogle Scholar
  6. Baumann HA, Morrison L, Stengel DB (2009) Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol Environ Saf 72:1063–1075CrossRefGoogle Scholar
  7. Begin C, Johnson LE, Himmelman JH (2004) Macroalgal canopies: distribution and diversity of associated invertebrates and effects on the recruitment and growth of mussels. Mar Ecol Prog Ser 271:121–132CrossRefGoogle Scholar
  8. Bond PR, Brown MT, Moate RM, Gledhill M, Hill SJ, Nimmo M (1999) Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper. Eur J Phycol 34:513–521CrossRefGoogle Scholar
  9. Brownlee C, Bouget FY (1998) Polarity determination in fucus: from zygote to multicellular embryo. Semin Cell Dev Biol 9:179–185CrossRefGoogle Scholar
  10. Connan S, Stengel DB (2011) Impacts of ambient salinity and copper on brown algae: 1. Interactive effects on photosynthesis, growth, and copper accumulation. Aquat Toxicol 104:94–107CrossRefGoogle Scholar
  11. Dethier MN, Williams SL (2009) Seasonal stresses shift optimal intertidal algal habitats. Mar Biol 156:555–567CrossRefGoogle Scholar
  12. Diez I, Muguerza N, Santolaria A, Ganzedo U, Gorostiaga JM (2012) Seaweed assemblage changes in the eastern Cantabrian Sea and their potential relationship to climate change. Estuar Coast Shelf Sci 99:108–120CrossRefGoogle Scholar
  13. Eklund BT, Kautsky L (2003) Review on toxicity testing with marine macroalgae and the need for method standardization—exemplified with copper and phenol. Mar Pollut Bull 46:171–181CrossRefGoogle Scholar
  14. Fredersdorf J, Muller R, Becker S, Wiencke C, Bischof K (2009) Interactive effects of radiation, temperature and salinity on different life history stages of the Arctic kelp Alaria esculenta (Phaeophyceae). Oecologia 160:483–492CrossRefGoogle Scholar
  15. 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 48:1064–1078CrossRefGoogle Scholar
  16. Kevekordes K (2000) The effects of secondary-treated sewage effluent and reduced salinity on specific events in the early life stages of Hormosira banksii (Phaeophyceae). Eur J Phycol 35:365–371CrossRefGoogle Scholar
  17. Kevekordes K, Clayton MN (2000) Development of Hormosira banksii (Phaeophyceae) embryos in selected components of secondarily-treated sewage effluent. J Phycol 36:25–32CrossRefGoogle Scholar
  18. Knight M, Parke M (1950) A biological study of Fucus vesiculosus and F. serratus. J Mar Biol Assoc UK 29:87–90CrossRefGoogle Scholar
  19. La Rocca N, Andreoli C, Giacometti GM, Rascio N, Moro I (2009) Responses of the Antarctic microalga Koliella antarctica (Trebouxiophyceae, Chlorophyta) to cadmium contamination. Photosynthetica 47:471–479CrossRefGoogle Scholar
  20. Larcher W (2001) Physiological plant ecology. Ecophysiology and stress physiology of functional groups. Springer, BerlinGoogle Scholar
  21. Lüning K (1984) Temperature tolerance and biogeography of seaweeds—the marine algal flora of Helgoland (North Sea) as an example. Helgolander Meeresuntersuchungen 38:305–317CrossRefGoogle Scholar
  22. Malm T, Kautsky L, Engkvist R (2001) Reproduction, recruitment and geographical distribution of Fucus serratus L. in the Baltic Sea. Bot Mar 44:101–108CrossRefGoogle Scholar
  23. Martinez B, Arenas F, Rubal M, Burgues S, Esteban R, Garcia-Plazaola I, Figueroa FL, Pereira R, Saldana L, Sousa-Pinto I, Trilla A, Viejo RM (2012) Physical factors driving intertidal macroalgae distribution: physiological stress of a dominant fucoid at its southern limit. Oecologia 170:341–353CrossRefGoogle Scholar
  24. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668CrossRefGoogle Scholar
  25. Morel FMM, Rueter JG, Anderson DM, Guillard RRL (1979) Aquil: a chemically defined phytoplankton culture medium for trace metal studies. J Phycol 15:135–141CrossRefGoogle Scholar
  26. Muller R, Laepple T, Bartsch I, Wiencke C (2009) Impact of oceanic warming on the distribution of seaweeds in polar and cold-temperate waters. Bot Mar 52:617–638CrossRefGoogle Scholar
  27. Nielsen HD, Nielsen SL (2005) Photosynthetic responses to Cu2+ exposure are independent of light acclimation and uncoupled from growth inhibition in Fucus serratus (Phaeophyceae). Mar Pollut Bull 51:715–721CrossRefGoogle Scholar
  28. Nielsen HD, Nielsen SL (2008) Evaluation of imaging and conventional PAM as a measure of photosynthesis in thin- and thick-leaved marine macroalgae. Aquat Biol 3:121–131CrossRefGoogle Scholar
  29. Nielsen HD, Nielsen SL (2010) Adaptation to high light irradiances enhances the photosynthetic Cu2+ resistance in Cu2+ tolerant and non-tolerant populations of the brown macroalgae Fucus serratus. Mar Pollut Bull 60:710–717CrossRefGoogle Scholar
  30. Nielsen HD, Brown MT, Brownlee C (2003a) Cellular responses of developing Fucus serratus embryos exposed to elevated concentrations of Cu2+. Plant Cell Environ 26:1737–1747CrossRefGoogle Scholar
  31. Nielsen HD, Brownlee C, Coelho SM, Brown MT (2003b) Inter-population differences in inherited copper tolerance involve photosynthetic adaptation and exclusion mechanisms in Fucus serratus. New Phytol 160:157–165CrossRefGoogle Scholar
  32. Nielsen HD, Burridge TR, Brownlee C, Brown MT (2005) Prior exposure to Cu contamination influences the outcome of toxicological testing of Fucus serratus embryos. Mar Pollut Bull 50:1675–1680CrossRefGoogle Scholar
  33. Nygard CA, Dring MJ (2008) Influence of salinity, temperature, dissolved inorganic carbon and nutrient concentration on the photosynthesis and growth of Fucus vesiculosus from the Baltic and Irish Seas. Eur J Phycol 43:253–262CrossRefGoogle Scholar
  34. Pohl C, Hennings U (1999) Bericht zum Ostsee-Monitoring: die Schwermetall-Situation in der Ostsee im Jahre 1999. Institut für OstseeforschungGoogle Scholar
  35. Pohl C, Kattner G, Schulzbaldes M (1993) Cadmium, copper, lead and zinc on transects through arctic and eastern Atlantic surface and deep waters. J Mar Syst 4:17–29CrossRefGoogle Scholar
  36. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  37. Roberts SK, Berger F, Brownlee C (1993) The role of Ca2+ in signal-transduction following fertilization in Fucus serratus. J Exp Biol 184:197–212Google Scholar
  38. Steen H (2004a) Effects of reduced salinity on reproduction and germling development in Sargassum muticum (Phaeophyceae, Fucales). Eur J Phycol 39:293–299CrossRefGoogle Scholar
  39. Steen H (2004b) Interspecific competition between Enteromorpha (Ulvales: chlorophyceae) and Fucus (Fucales : phaeophyceae) germlings: effects of nutrient concentration, temperature, and settlement density. Mar Ecol Prog Ser 278:89–101CrossRefGoogle Scholar
  40. Steen H, Rueness J (2004) Comparison of survival and growth in germlings of six fucoid species (fucales, Phaeophyceae) at two different temperature and nutrient levels. Sarsia 89:175–183CrossRefGoogle Scholar
  41. Steen H, Scrosati R (2004) Intraspecific competition in Fucus serratus and F. evanescens (phaeophyceae : fucales) germlings: effects of settlement density, nutrient concentration, and temperature. Mar Biol 144:61–70CrossRefGoogle Scholar
  42. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51CrossRefGoogle Scholar
  43. Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJA, Poloczanska ES, Connell SD (2011) Seaweed communities in retreat from Ocean warming. Curr Biol 21:1828–1832CrossRefGoogle Scholar
  44. Wiencke C, Bartsch I, Bischoff B, Peters AF, Breeman AM (1994) Temperature requirements and biogeography of antarctic, arctic and amphiequatorial seaweeds. Bot Mar 37:247–259CrossRefGoogle Scholar
  45. Xylander M, Fischer W, Braune W (1998) Influence of mercury on the green alga Haemotococcus lacustris. Inhibition effects and recovery of impact. Botanica Acta 111:467–473CrossRefGoogle Scholar
  46. Zou DH, Liu SX, Du H, Xu JT (2012) Growth and photosynthesis in seedlings of Hizikia fusiformis (Harvey) Okamura (Sargassaceae, Phaeophyta) cultured at two different temperatures. J Appl Phycol 24:1321–1327CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Søren Laurentius Nielsen
    • 1
    Email author
  • Hanne Dalsgaard Nielsen
    • 2
  • Morten Foldager Pedersen
    • 1
  1. 1.Department of Environmental, Social and Spatial ChangeRoskilde UniversityRoskildeDenmark
  2. 2.School of Life SciencesNapier UniversityEdinburghUK

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