Abstract
In the marine littoral, strong grazing pressure selects for macroalgal defenses such as the constitutive and inductive production of defense metabolites. Induced defenses are expected under spatiotemporally varying grazing pressure and should be triggered by a reliable cue from herbivory, thereby reducing grazing pressure via decreased herbivore preference and/or performance. Although induced resistance has frequently been demonstrated in brown macroalgae, it is yet to be investigated whether induced macroalgal resistance shows genetic variation, a prerequisite for evolutionary responses to selection. In addition, consequences of induced resistance on herbivore performance have rarely been tested while the role of brown algal phlorotannins as inducible defense metabolites remains ambiguous. Using preference bioassays, we tested various cues, e.g., natural grazing, waterborne cues or simulated grazing to induce resistance in the brown alga Fucus vesiculosus. Further, we investigated whether there are induced responses in phlorotannin content, genetic variation in induced resistance or incurred performance costs to the mesoherbivore isopod, Idotea baltica. We found that both direct grazing and waterborne grazing cues decreased the palatability of F. vesiculosus, while increasing the total phlorotannin content. Since the sole presence of the herbivore also increased the total soluble phlorotannins, yet failed to stimulate deterrence, we concluded that phlorotannins alone do not explain increased resistance. Induced resistance varied between algal genotypes and thus showed potential for evolutionary responses to variation in grazing pressure. Induced resistance also incurred performance costs for female I. baltica via reduced egg production. Our results show that the induced resistance of F. vesiculosus decreases grazing pressure by deterring herbivores as well as impairing their performance. Resistance may be induced in advance by waterborne cues and spread effectively throughout the F. vesiculosus belt. Through lowering herbivore performance, induced resistance may also reduce future grazing pressure by decreasing the population growth rate of I. baltica.
Similar content being viewed by others
References
Amsler CD (2001) Induced defenses in macroalgae: the herbivore makes a difference. J Phycol 37:353–356. 10.1046/j.1529-8817.2001.037003353.x
Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91
Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279. doi:10.1126/science.221.4607.277
Borell EM, Foggo A, Coleman RA (2004) Induced resistance in intertidal macroalgae modifies feeding behaviour of herbivorous snails. Oecologia 140:328–334. doi:10.1007/s00442-004-1589-0
Cyr H, Pace M (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150. doi:10.1038/361148a0
Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114. doi:10.1007/s00442-003-1242-3
Díaz E, Güldenzoph C, Molis M, McQuaid C, Wahl M (2006) Variability in grazer-mediated defensive responses of green and red macroalgae on the south coast of South Africa. Mar Biol 149:1301–1311. doi:10.1007/s00227-006-0320-6
Dicke M, Agrawal AA, Bruin J (2003) Plants talk, but are they deaf? Trends Plant Sci 8:403–405. doi:10.1016/S1360-1385(03)00183-3
Engkvist R, Malm T, Tobiasson S (2000) Density dependent grazing effects of the isopod Idotea baltica Pallas on Fucus vesiculosus L. in the Baltic Sea. Aquat Ecol 34:253–260. doi:10.1023/A:1009919526259
Gruner DS, Smith JE, Seabloom EW, Sandin SA, Ngai JT, Hillebrand H, Harpole WS, Elser JJ, Cleland EE, Bracken MES, Borer ET, Bolker BM (2008) A cross-system synthesis of consumer and nutrient resource control on producer biomass. Ecol Lett 11:740–755. doi:10.1111/j.1461-0248.2008.01192.x
Haahtela I (1978) Morphology as evidence of maturity in isopod Crustacean, as exemplified by Mesidotea entomon (L.). Ann Zool Fenn 15:186–190
Hay ME (1991) Marine-terrestrial contrasts in the ecology of plant chemical defences against herbivores. Trends Ecol Evol 6:362–365. doi:10.1016/0169-5347(91)90227-O
Hemmi A, Jormalainen V (2002) Nutrient enhancement increases fecundity and growth of a marine herbivore via quality of its food alga. Ecology 83:1052–1064. doi:10.1890/0012-9658(2002)083[1052:NEIPOA]2.0.CO;2
Hemmi A, Jormalainen V (2004) Geographic covariation of chemical quality of the host alga Fucus vesiculosus with fitness of the herbivorous isopod Idotea baltica. Mar Biol 145:759–768. doi:10.1007/s00227-004-1360-4
Hemmi A, Honkanen T, Jormalainen V (2004) Inducible resistance to herbivory in Fucus vesiculosus–duration, spreading and variation with nutrient availability. Mar Ecol Prog Ser 273:109–120. doi:10.3354/meps273109
Honkanen T, Jormalainen V (2005) Genotypic variation in tolerance and resistance to fouling in the brown alga Fucus vesiculosus. Oecologia 144:196–205. doi:10.1007/s00442-005-0053-0
Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown alga Fucus vesiculosus. Mar Biol 101:115–119. doi:10.1007/BF00393484
Jormalainen V, Honkanen T (2004) Variation in natural selection for growth and phlorotannins in the brown alga Fucus vesiculosus. J Evol Biol 17:807-820. doi:10.1111/j.1420-9101.2004.00715.x
Jormalainen V, Honkanen T (2008) Macroalgal chemical defenses and their roles in structuring temperate marine communities. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 57–81
Jormalainen V, Ramsay T (2009) Resistance of the brown alga Fucus vesiculosus to herbivory. Oikos 118:713–722. doi:10.1111/j.1600-0706.2008.17178.x
Jormalainen V, Honkanen T, Koivikko R, Eränen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650. doi:10.1034/j.1600-0706.2003.12635.x
Jormalainen V, Wikström SA, Honkanen T (2008) Fouling mediates grazing: intertwining of resistances to multiple enemies in the brown alga Fucus vesiculosus. Oecologia 155:559–569. doi:10.1007/s00442-007-0939-0
Karban R, Baldwin IT (1997) Induced responses to herbivory. University Chicago Press, Illinois
Karban R, Myers J (1989) Induced plant responses to herbivory. Annu Rev Ecol Syst 20:331–348
Koivikko R, Loponen J, Honkanen T, Jormalainen V (2005) Contents of soluble, cell-wall-bound and exuded phlorotannnins in the brown alga Fucus vesiculosus, with implications on their ecological functions. J Chem Ecol 31:195–212. doi:10.1007/s10886-005-0984-2
Koivikko R, Eränen J, Loponen J, Jormalainen V (2008) Variation of phlorotannins among three populations of Fucus vesiculosus as revealed by HPLC and colorimetric quantification. J Chem Ecol 34:57–64. doi:10.1007/s10886-007-9410-2
Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628. doi:10.1111/j.1365-2745.2006.01120.x
Kotta J, Orav-Kotta H, Paalme T, Kotta I, Kukk H (2006) Seasonal changes in situ grazing of the mesoherbivores Idotea baltica and Gammarus oceanicus on the brown algae Fucus vesiculosus and Pylaiella littoralis in the central Gulf of Finland, Baltic Sea. Hydrobiologia 554:117–125. doi:10.1007/s10750-005-1011-x
Kubanek J, Lester SE, Fenical W, Hay ME (2004) Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus. Mar Ecol Prog Ser 277:79–93. doi:10.3354/meps277079
Littell RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute, Cary
Long JD, Hamilton RS, Mitchell JL (2007) Asymmetric competition via induced resistance: specialist herbivores indirectly suppress generalist preference and populations. Ecology 88:1232–1240. doi:10.1890/06-1585
Macaya EC, Thiel M (2008) In situ tests on inducible defenses in Dictyota kunthii and Macrocystis integrifolia (Phaeophyceae) from the Chilean coast. J Exp Mar Biol Ecol 354:28–38. doi:10.1016/j.jembe.2005
Macaya EC, Rothäusler E, Thiel M, Molis M, Wahl M (2005) Induction of defenses and within-alga variation of palatability in two brown algae from the northern-central coast of Chile: effects of mesograzers and UV radiation. J Exp Mar Biol Ecol 325:214–227. doi:10.1016/j.jembe.2007.10.005
Milliken GA, Johnson DE (2002) Analysis of messy data, vol III. Analysis of covariance. Chapman & Hall, New York
Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268. doi:10.1111/j.0030-1299.2004.12768.x
Pavia H, Brock E (2000) Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 193:285–294. doi:10.3354/meps193285
Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3223–3225. doi:10.1890/00129658(2000)081[3212:ICRTHI]2.0.CO;2
Pavia H, Toth GB (2008) Macroalgal models in testing and extending defense theories. In: Amsler CD (ed) Algal chemical ecology. Springer, Berlin, pp 147–172
Peckol P, Krane JM, Yates JL (1996) Interactive effects of inducible defense and resource availability on phlorotannins in the North Atlantic brown alga Fucus vesiculosus. Mar Ecol Prog Ser 138:209–217. doi:10.3354/meps138209
Pettay E (2001) The responses of Fucus-inhabiting animal species to nutrient enrichment caused by fish farming. M.Sc. thesis, Department of Biology, University of Turku, Finland
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists, 1st edn. Cambridge University Press, Cambridge
Rapport DJ, Turner JE (1970) Determination of predator food preference. J Theor Biol 26:365–372. doi:10.1016/0022-5193(70)90089-5
Rhoades DF (1983) Responses of alder and willow to attack by ten caterpillars and webworms: evidence of pheromonal sensitivity of willows. In: Hedin PA (ed) Plant resistance to insects. symposium series 208. American Chemical Society, Washington, DC, pp 55–68
Rohde S, Wahl M (2008) Antifeeding defense in Baltic macroalgae: induction by direct versus waterborne cues. J Phycol 44:85–90. doi:10.1111/j.1529-8817.2007.00451.x
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. doi:10.1111/j.0022-0477.2004.00936.x
SAS Institute (1999) SAS/STAT user′s guide, version 8. SAS Institute, Cary
Simms EL (1992) Costs of plant resistance to herbivory. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, Chicago, pp 392–425
Simms EL, Rausher MD (1992) Use of quantitative genetics for studying the evolution of plant resistance. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology evolution and genetics. University of Chicago Press, Chicago, pp 42–68
Sotka EE, Taylor RB, Hay ME (2002) Tissue-specific induction of resistance to herbivores in a brown seaweed: the importance of direct grazing versus waterborne signals from grazed neighbors. J Exp Mar Biol Ecol 277:1–12. doi:10.1016/S0022-0981(02)00128-4
Strong KW, Daborn GR (1979) Growth and energy utilisation of the intertidal isopod Idotea baltica (Pallas) (Crustacea: Isopoda). J Exp Mar Biol Ecol 41:101–123. doi:10.1016/0022-0981(79)90046-7
Targett NM, Arnold TM (2001) Effects of secondary metabolites on digestion in marine herbivores. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, pp 391–412
Tollrian R, Harvell CD (1999) Why inducible defenses? In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, New Jersey, pp 3–9
Toth GB, Pavia H (2000) Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). PNAS 97:14418–14420. doi:10.1073/pnas.250226997
Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434. doi:10.1111/j.1365-2745.2007.01224.x
Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defenses of valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612–618. doi:10.1890/04-0484
Toth GB, Karlsson M, Pavia H (2007) Mesoherbivore reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia 152:245–255. doi:10.1007/s00442-006-0643-5
Underwood AJ, Clarke KR (2005) Solving some statistical problems in analyses of experiments on choices of food and on associations with habitat. J Exp Mar Biol Ecol 318:227–237. doi:10.1016/j.jembe.2004.12.014
Underwood AJ, Chapman MG, Crowe TP (2004) Identifying and understanding ecological preferences for habitat of prey. J Exp Mar Biol Ecol 300:161–187. doi:10.1016/j.jembe.2003.12.006
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. doi:10.3354/meps283127
Wright JT, de Nys R, Poore AGB, Steinberg PD (2004) Chemical defense in a marine alga: heritability and the potential for selection by herbivore. Ecology 85:2946–2959. doi:10.1890/03-4041
Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766. doi:10.2307/1939934
Yun HY, Cruz J, Treitschke M, Wahl M, Molis M (2007) Testing for the induction of anti-herbivory defences in four Portuguese macroalgae by direct and water-borne cues of grazing amphipods. Helgol Mar Res 61:203–209. doi:10.1007/s10152-007-0067-6
Acknowledgments
We are grateful to Elina Salo, Tiina Sojakka and Janika Ulenius for help in executing the experiments, Riitta Koivikko for analyzing the phlorotannins and the Archipelago Research Institute for use of their facilities. Comments by Hans Helenius, Lauri Oksanen, Kai Ruohomäki, Outi Vesakoski and two anonymous reviewers helped to improve the manuscript. The study was financed by the Academy of Finland (decision no. 213966 to V. J.). All the experiments conducted comply with the current laws of Finland.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Tony Underwood.
Rights and permissions
About this article
Cite this article
Haavisto, F., Välikangas, T. & Jormalainen, V. Induced resistance in a brown alga: phlorotannins, genotypic variation and fitness costs for the crustacean herbivore. Oecologia 162, 685–695 (2010). https://doi.org/10.1007/s00442-009-1494-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-009-1494-7