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

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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.

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References

  • Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91

    Article  CAS  Google Scholar 

  • Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558

    Article  Google Scholar 

  • Bolser RC, Hay ME (1996) Are tropical plants better defended? Palatability and defenses of temperate vs. tropical seaweeds. Ecology 77:2269–2286

    Article  Google Scholar 

  • 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 41:726–731

    Article  Google Scholar 

  • Clare AS (1996) Natural product antifoulants: status and potential. Biofouling 9:211–229

    Article  CAS  Google Scholar 

  • 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 325–353

    Google Scholar 

  • 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 77:93–106

    Article  CAS  Google Scholar 

  • Cronin G, Hay ME (1996b) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531–1543

    Article  Google Scholar 

  • 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 137:32–41

    Article  PubMed  Google Scholar 

  • Cruz-Rivera E, Hay ME (2003) Prey nutritional quality interacts with chemical defenses to affect consumer feeding and fitness. Ecol Monogr 73:483–506

    Article  Google Scholar 

  • 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 19:161–169

    Article  CAS  PubMed  Google Scholar 

  • 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 24:209–218

    Article  PubMed  Google Scholar 

  • de Carvalho LR, Guimaraes SMPB, Roque NF (2006) Sulfated bromphenols from Osmundaria obtusiloba (C. Agardh) R. E. Norris (Rhodophyta, Ceramiales). Rev Bras Bot 29:453–459

    Google Scholar 

  • Dethier MN, Williams SL, Freeman A (2005) Seaweeds under stress: manipulated stress and herbivory affect critical life-history functions. Ecol Monogr 75:403–418

    Article  Google Scholar 

  • Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263

    Article  Google Scholar 

  • Dworjanyn SA, Wright JT, Paul NA, de Nys R, Steinberg PD (2006) Cost of chemical defence in the red alga Delisea pulchra. Oikos 113:13–22

    Article  CAS  Google Scholar 

  • 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 336:99–109

    Article  CAS  Google Scholar 

  • Erftemeijer PLA, Lewis RRR (2006) Environmental impacts of dredging on seagrasses: a review. Mar Pollut Bull 52:1553–1572

    Article  CAS  PubMed  Google Scholar 

  • Fowler AM, Henessy KJ (1995) Potential impacts of global warming on the frequency and magnitude of heavy precipitation. Nat Hazards 11:283–303

    Article  Google Scholar 

  • Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134

    Article  CAS  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions—the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Article  Google Scholar 

  • Heaven C, Scrosati R (2004) Feeding preference of Littorina snails (Gastropoda) for bleached and photosynthetic tissues of the seaweed Mazzaella parksii (Rhodophyta). Hydrobiologia 513:239–243

    Article  Google Scholar 

  • Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335

    Article  Google Scholar 

  • Jormalainen V, Honkanen T, Koivikko R, Eranen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650

    Article  CAS  Google Scholar 

  • 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 54:276–288

    Google Scholar 

  • Khan FA, Ansari AA (2005) Eutrophication: an ecological vision. Bot Rev 71:449–482

    Article  Google Scholar 

  • 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 17:1609–1643

    Article  Google Scholar 

  • 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 44:345–350

    Article  Google Scholar 

  • Manly BFJ (1993) Comments on design and analysis of multiple-choice feeding-preference experiments. Oecologia 93:149–152

    Google Scholar 

  • Mole S (1994) Trade-offs and constraints in plant-herbivore defense theory—a life-history perspective. Oikos 71:3–12

    Article  Google Scholar 

  • 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 381:83–97

    Article  Google Scholar 

  • Paul VJ, Ritson-Williams R (2008) Marine chemical ecology. Nat Prod Rep 25:662–695

    Article  CAS  PubMed  Google Scholar 

  • Pavia H, Toth GB (2000) Influence of light and nitrogen on the phlorotannin content of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299–305

    Article  CAS  Google Scholar 

  • Pavia H, Toth G (2008) Macroalgal models in testing and extending defense theories. In: Amsler CD (ed) Algal Chemical Ecology. Springer, Berlin, pp 147–172

    Chapter  Google Scholar 

  • 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 42:441–448

    Article  CAS  Google Scholar 

  • Peterson CH, Renaud PE (1989) Analysys of feeding preference experiments. Oecologia 80:82–86

    Article  Google Scholar 

  • Purrington CB (2000) Costs of resistance. Curr Opin Plant Biol 3:305–308

    Article  CAS  PubMed  Google Scholar 

  • 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 82:217–226

    Article  Google Scholar 

  • Rhoades DF (1985) Offensive-defensive interactions between herbivores and plants—their relevance in herbivore population-dynamics and ecological theory. Am Nat 125:205–238

    Article  Google Scholar 

  • Rohde S, Molis M, Wahl M (2004) Regulation of anti-herbivore defence by Fucus vesiculosus in response to various cues. J Ecol 92:1011–1018

    Article  Google Scholar 

  • 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 43:143–150

    Article  Google Scholar 

  • 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 56:2300–2314

    Article  Google Scholar 

  • 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 355:103–113

    Article  Google Scholar 

  • Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55

    Article  PubMed  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Tauiol A, Yoneshigue-Valentin Y (2002) Alteraçãoes na composição floristica das algas da Praia de Boa Viagem (Niterói, RJ). Rev Bras Bot 25:405–412

    Google Scholar 

  • Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76

    Article  Google Scholar 

  • Thomas TE, Harrison PJ, Turpin DH (1987) Adaptations of Gracilaria pacifica (Rhodophyta) to nitrogen procurement at different intertidal locations. Mar Biol 93:569–580

    Article  Google Scholar 

  • Wahl M (1989) Marine epibiosis.1. Fouling and antifouling—some basic aspects. Mar Ecol-Prog Ser 58:175–189

    Article  Google Scholar 

  • Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438

    Article  PubMed  Google Scholar 

  • Webster PJ, Holland GJ, Curry JA, Chang H-R (2005) Changes in tropical cyclone number, duration and intensity in a warming environment. Science 309:1844–1846

    Article  CAS  PubMed  Google Scholar 

  • 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 283:113–125

    Article  Google Scholar 

  • White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105

    Article  Google Scholar 

  • Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Mercator Foundation for funding this study. Moreover, we thank Florian Weinberger for advice on the manuscript and two anonymous reviewers as well as the editor for substantially helpful comments and critique. Further, we recognize valuable help in field and laboratory work: Camille Alves, Glaucia Ank, Bruno Antunes, Éverson Bianco, Juliana Ferrari, Suzana Guimarães, Ricardo Rogers, Rodrigo Santos, Camilla Souza, Daniela Sudatti, Frauke Symanowski, Phillipe Vieira and Eduardo Xavier for great support. The experiments comply with the current laws of Brazil, where they were performed.

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Correspondence to Yasmin Shirin Appelhans.

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Communicated by T. Reusch.

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Appelhans, Y.S., Lenz, M., Medeiros, H.E. et al. Stressed, but not defenceless: no obvious influence of irradiation levels on antifeeding and antifouling defences of tropical macroalgae. Mar Biol 157, 1151–1159 (2010). https://doi.org/10.1007/s00227-010-1396-6

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