Marine Biology

, Volume 157, Issue 5, pp 1151–1159 | Cite as

Stressed, but not defenceless: no obvious influence of irradiation levels on antifeeding and antifouling defences of tropical macroalgae

  • Yasmin Shirin Appelhans
  • Mark Lenz
  • Heloisa Elias Medeiros
  • Bernardo Antonio Perez da Gama
  • Renato Crespo Pereira
  • Martin Wahl
Original Paper

Abstract

The production of defence metabolites is assumed to be costly in metabolic terms. If this holds true, low-light stress should reduce the ability of seaweeds to defend themselves chemically against herbivory and fouling. We investigated the effect of energy limitation on the defensive status of seaweeds by assessing their attractiveness to mesograzers and their activity against a bivalve macrofouler in comparison with non-stressed conspecifics. The macroalgae Codium decorticatum (Woodw.) M. Howe, Osmundaria obtusiloba (C. Agardh) R. E. Norris, Pterocladiella capillacea (S. G. Gmel.) Santel. and Hommer., Sargassum vulgare C. Agardh and Stypopodium zonale (Lamour.) Papenf. collected at the southeastern Brazilian coast were exposed to six levels of irradiation (between 1 and 180 μmol photons m−2 s−1) for 10–14 days. After this period, algae from all treatment levels were: (a) processed as artificial food and offered to an amphipod community dominated by Elasmopus brasiliensis Dana and (b) extracted to test for differences in settlement rates of the fouling mussel Perna perna L. on filter paper loaded with the crude extracts. Generally, photosynthesis rates and growth were reduced under low light conditions. Attractiveness to herbivores and macrofoulers, however, was insensitive to energy limitation. We discuss possible explanations for the observed absence of a relationship between light availability and algal defence including the change in nutritional value of the algal tissue, the allocation of resources towards defence instead of growth and the absence of costs for defence.

References

  1. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91CrossRefGoogle Scholar
  2. Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558CrossRefGoogle Scholar
  3. Bolser RC, Hay ME (1996) Are tropical plants better defended? Palatability and defenses of temperate vs. tropical seaweeds. Ecology 77:2269–2286CrossRefGoogle Scholar
  4. Ceh J, Molis M, Dzeha TM, Wahl M (2005) Induction and reduction of anti-herbivore defenses in brown and red macroalgae off the Kenyan coast. J Phycol 41:726–731CrossRefGoogle Scholar
  5. Clare AS (1996) Natural product antifoulants: status and potential. Biofouling 9:211–229CrossRefGoogle Scholar
  6. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: Mc Clintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 325–353Google Scholar
  7. Cronin G, Hay ME (1996a) Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93–106CrossRefGoogle Scholar
  8. Cronin G, Hay ME (1996b) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531–1543CrossRefGoogle Scholar
  9. Cronin G, Lodge DM (2003) Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes. Oecologia 137:32–41CrossRefPubMedGoogle Scholar
  10. Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506CrossRefGoogle Scholar
  11. da Gama BAP, Pereira RC, Soares AR, Teixeira VL, Yoneshigue-Valentin Y (2003) Is the mussel test a good indicator of antifouling activity? a comparison between laboratory and field assays. Biofouling 19:161–169CrossRefPubMedGoogle Scholar
  12. da Gama BAP, Santos RPD, Pereira RC (2008) The effect of epibionts on the susceptibility of the red seaweed Cryptonemia seminervis to herbivory and fouling. Biofouling 24:209–218CrossRefPubMedGoogle Scholar
  13. de Carvalho LR, Guimaraes SMPB, Roque NF (2006) Sulfated bromphenols from Osmundaria obtusiloba (C. Agardh) R. E. Norris (Rhodophyta, Ceramiales). Rev Bras Bot 29:453–459Google Scholar
  14. Dethier MN, Williams SL, Freeman A (2005) Seaweeds under stress: manipulated stress and herbivory affect critical life-history functions. Ecol Monogr 75:403–418CrossRefGoogle Scholar
  15. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263CrossRefGoogle Scholar
  16. Dworjanyn SA, Wright JT, Paul NA, de Nys R, Steinberg PD (2006) Cost of chemical defence in the red alga Delisea pulchra. Oikos 113:13–22CrossRefGoogle Scholar
  17. Edwards KF, Pfister CA, Van Alstyne KL (2006) Nitrogen content in the brown alga Fucus gardneri and its relation to light, herbivory and wave exposure. J Exp Mar Biol Ecol 336:99–109CrossRefGoogle Scholar
  18. Erftemeijer PLA, Lewis RRR (2006) Environmental impacts of dredging on seagrasses: a review. Mar Pollut Bull 52:1553–1572CrossRefPubMedGoogle Scholar
  19. Fowler AM, Henessy KJ (1995) Potential impacts of global warming on the frequency and magnitude of heavy precipitation. Nat Hazards 11:283–303CrossRefGoogle Scholar
  20. Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134CrossRefGoogle Scholar
  21. Hay ME, Fenical W (1988) Marine plant-herbivore interactions—the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145CrossRefGoogle Scholar
  22. Heaven C, Scrosati R (2004) Feeding preference of Littorina snails (Gastropoda) for bleached and photosynthetic tissues of the seaweed Mazzaella parksii (Rhodophyta). Hydrobiologia 513:239–243CrossRefGoogle Scholar
  23. Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  24. Jormalainen V, Honkanen T, Koivikko R, Eranen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650CrossRefGoogle Scholar
  25. Kavanaugh MT, Nielsen KJ, Chan FT, Menge BA, Letelier RM, Goodrich LM (2009) Experimental assessment of the effects of shade on an intertidal kelp: do phytoplankton blooms inhibit growth of open-coast macroalgae? Limnol Oceanogr 54:276–288Google Scholar
  26. Khan FA, Ansari AA (2005) Eutrophication: an ecological vision. Bot Rev 71:449–482CrossRefGoogle Scholar
  27. Kjerfve B, Ribeiro CHA, Dias GTM, Filippo AM, Quaresma VD (1997) Oceanographic characteristics of an impacted coastal bay: Baia de Guanabara, Rio de Janeiro, Brazil. Cont Shelf Res 17:1609–1643CrossRefGoogle Scholar
  28. Lehvo A, Back S, Kiirikki M (2001) Growth of Fucus vesiculosus L. (Phaeophyta) in the northern Baltic proper: energy and nitrogen storage in seasonal environment. Bot Mar 44:345–350CrossRefGoogle Scholar
  29. Manly BFJ (1993) Comments on design and analysis of multiple-choice feeding-preference experiments. Oecologia 93:149–152Google Scholar
  30. Mole S (1994) Trade-offs and constraints in plant-herbivore defense theory—a life-history perspective. Oikos 71:3–12CrossRefGoogle Scholar
  31. Pansch C, Cerda O, Lenz M, Wahl M, Thiel M (2009) Consequences of light reduction for anti-herbivore defense and bioactivity against mussels in four seaweed species from northern-central Chile. Mar Ecol Prog Ser 381:83–97CrossRefGoogle Scholar
  32. Paul VJ, Ritson-Williams R (2008) Marine chemical ecology. Nat Prod Rep 25:662–695CrossRefPubMedGoogle Scholar
  33. Pavia H, Toth GB (2000) Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299–305CrossRefGoogle Scholar
  34. Pavia H, Toth G (2008) Macroalgal models in testing and extending defense theories. In: Amsler CD (ed) Algal Chemical Ecology. Springer, Berlin, pp 147–172CrossRefGoogle Scholar
  35. Pereira RC, Yoneshigue-Valentin Y (1999) The role of polyphenols from the tropical brown alga Sargassum furcatum on the feeding by amphipod herbivores. Bot Mar 42:441–448CrossRefGoogle Scholar
  36. Peterson CH, Renaud PE (1989) Analysys of feeding preference experiments. Oecologia 80:82–86CrossRefGoogle Scholar
  37. Purrington CB (2000) Costs of resistance. Curr Opin Plant Biol 3:305–308CrossRefPubMedGoogle Scholar
  38. Renaud PE, Hay ME, Schmitt TM (1990) Interactions of plant stress and herbivory—intraspecific variation in the susceptibility of a palatable versus an unpalatable seaweed to sea urchin grazing. Oecologia 82:217–226CrossRefGoogle Scholar
  39. Rhoades DF (1985) Offensive-defensive interactions between herbivores and plants—their relevance in herbivore population-dynamics and ecological theory. Am Nat 125:205–238CrossRefGoogle Scholar
  40. Rohde S, Molis M, Wahl M (2004) Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. J Ecol 92:1011–1018CrossRefGoogle Scholar
  41. Rohde S, Hiebenthal C, Wahl M, Karez R, Bischof K (2008) Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: effects of light deficiency and epibionts on growth and photosynthesis. Eur J Phycol 43:143–150CrossRefGoogle Scholar
  42. Scheibling RE, Hennigar AW, Balch T (1999) Destructive grazing, epiphytism, and disease: the dynamics of sea urchin—kelp interactions in Nova Scotia. Can J Fish Aquat Sci 56:2300–2314CrossRefGoogle Scholar
  43. Scheibling RE, Lyons DA, Sumi CBT (2008) Grazing of the invasive alga Codium fragile ssp tomentosoides by the common periwinkle Littorina littorea: effects of thallus size, age and condition. J Exp Mar Biol Ecol 355:103–113CrossRefGoogle Scholar
  44. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55CrossRefPubMedGoogle Scholar
  45. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285CrossRefGoogle Scholar
  46. Tauiol A, Yoneshigue-Valentin Y (2002) Alteraçãoes na composição floristica das algas da Praia de Boa Viagem (Niterói, RJ). Rev Bras Bot 25:405–412Google Scholar
  47. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76CrossRefGoogle Scholar
  48. Thomas TE, Harrison PJ, Turpin DH (1987) Adaptations of Gracilaria pacifica (Rhodophyta) to nitrogen procurement at different intertidal locations. Mar Biol 93:569–580CrossRefGoogle Scholar
  49. Wahl M (1989) Marine epibiosis.1. Fouling and antifouling—some basic aspects. Mar Ecol-Prog Ser 58:175–189CrossRefGoogle Scholar
  50. Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438CrossRefPubMedGoogle Scholar
  51. Webster PJ, Holland GJ, Curry JA, Chang H-R (2005) Changes in tropical cyclone number, duration and intensity in a warming environment. Science 309:1844–1846CrossRefPubMedGoogle Scholar
  52. Weidner K, Lages BG, da Gama BAP, Molis M, Wahl M, Pereira RC (2004) Effect of mesograzers and nutrient levels on induction of defenses in several Brazilian macroalgae. Mar Ecol-Prog Ser 283:113–125CrossRefGoogle Scholar
  53. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105CrossRefGoogle Scholar
  54. Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Yasmin Shirin Appelhans
    • 1
  • Mark Lenz
    • 1
  • Heloisa Elias Medeiros
    • 2
  • Bernardo Antonio Perez da Gama
    • 2
  • Renato Crespo Pereira
    • 2
  • Martin Wahl
    • 1
  1. 1.Leibniz Institute of Marine Sciences at the University of Kiel (IFM-GEOMAR)KielGermany
  2. 2.Departamento de Biologia MarinhaUniversidade Federal Fluminense (UFF)Niterói, Rio de JaneiroBrazil

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