Macroalgal Models in Testing and Extending Defense Theories

  • Henrik Pavia
  • Gunilla B. Toth

The ecological roles of secondary metabolites have become one of the most expansive areas of research within plant ecology during the last two to three decades. They have also become one of the most theory-laden fields of plant ecology, if not ecology in general, with a number of general models (theories) seeking to explain and predict patterns of chemical defenses in plants. (We use the terms model or theory rather than hypothesis because we define the latter term in a more restricted way: a testable prediction that is logically derived from an explanatory model/ theory.) The discovery and characterization of tens of thousands of natural products in terrestrial plants and marine organisms during the last century called for models that could provide explanations and categorizations to this ample form of biodiversity. Suggestions that the primary function of these so-called secondary metabolites was as a defense against consumers (Dethier 1954; Fraenkel 1959) led ecologists to formulate a series of general defense models, especially during the 1970s and 1980s, to explain the distribution and variation of secondary metabolites. These defense models have allowed natural product chemists and chemical ecologists to put their specific work into a broader context and they have become a significant driving force for further studies of secondary metabolites and their ecological roles.

Keywords

Chemical Defense Brown Seaweed Defense Model Defense Theory Phlorotannin Content 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91CrossRefGoogle Scholar
  2. Amsler CD, Iken K, McClintock JB, Amsler MO, Peters KJ, Hubbard JM, Furrow FB, Baker BJ (2005) Comprehensive evaluation of the palatability and chemical defenses of subtidal macroalgae from the Antarctic Peninsula. Mar Ecol Prog Ser 294:141–159CrossRefGoogle Scholar
  3. Arnold TM, Tanner CE, Hatch WI (1995) Phenotypic variation in polyphenolic content of the tropical brown algae Lobophora variegata as a function of nitrogen availability. Mar Ecol Prog Ser 123:177–183CrossRefGoogle Scholar
  4. Arnold TM, Targett NM, Tanner CE, Hatch WI, Ferrari KE (2001) Evidence for methyl jasmonate-induced phlorotannin production in Fucus vesiculosus (Phaeophyceae). J Phycol 37:1026–1029CrossRefGoogle Scholar
  5. Bazzaz FA, Chiariello NR, Coley PD, Pitelka LF (1987) Allocating resources to reproduction and defence. BioScience 37:58–67CrossRefGoogle Scholar
  6. Berenbaum MR (1995) The chemistry of defense: theory and practice. Proc Natl Acad Sci USA 92:2–8PubMedCrossRefGoogle Scholar
  7. Borell EM, Foggo A, Coleman RA (2004) Induced resistance in intertidal macroalgae modifies feeding behaviour of herbivorous snails. Oecologia 140:328–334PubMedCrossRefGoogle Scholar
  8. Bryant JP, Chapin III FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368CrossRefGoogle Scholar
  9. Bryant JP, Chapin III FS, Reichardt PB, Clausen TP (1987) Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nutrient balance. Oecologia 72:510–514CrossRefGoogle Scholar
  10. Bryant JP, Kuropat PJ, Cooper SM, Frisby K, Owen-Smith N (1989) Resource availability hypothesis of plant antiherbivore defence tested in South African savanna ecosystem. Nature 340:227–228CrossRefGoogle Scholar
  11. 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
  12. Cetrulo GL, Hay ME (2000) Activated chemical defenses in tropical versus temperate seaweeds. Mar Ecol Prog Ser 207:243–253CrossRefGoogle Scholar
  13. Coleman RA, Ramchunder SJ, Moody AJ, Foggo A (2006) An enzyme in snail saliva induces herbivore-resistance in a marine alga. Func Ecol 21:101–106Google Scholar
  14. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899PubMedCrossRefGoogle Scholar
  15. Connan S, Goulard F, Stiger V, Deslandes E, Ar Gall E (2004) Phlorotannins in belt-forming brown algae of a sheltered shore. Bot Mar 47:410–416CrossRefGoogle Scholar
  16. Connan S, Delisle F, Deslandes E, Ar Gall E (2006) Intra-thallus phlorotannin content and antioxidant activity in Phaeophyceae of temperate waters. Bot Mar 49:39–46CrossRefGoogle Scholar
  17. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, FL, pp 325–353Google Scholar
  18. Cronin G, Hay ME (1996a) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301CrossRefGoogle Scholar
  19. Cronin G, Hay ME (1996b) Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis. Oecologia 195:361–368CrossRefGoogle Scholar
  20. Cronin G, Hay ME (1996c) Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93–106CrossRefGoogle Scholar
  21. 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
  22. Denton A, Chapman ARO, Markham J (1990) Size-specific concentrations of phlorotannins (anti-herbivore compounds) in three species of Fucus. Mar Ecol Prog Ser 65:103–104CrossRefGoogle Scholar
  23. 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
  24. Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8:33–54CrossRefGoogle Scholar
  25. 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 149:1301–1311CrossRefGoogle Scholar
  26. Fagerström T, Larsson S, Tenow O (1987) On optimal defence in plants. Func Ecol 1:73–81CrossRefGoogle Scholar
  27. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005a) Within-thallus variation in chemical and physical defences in two species of ecologically dominant macroalgae from the Antarctic Peninsula. J Exp Mar Biol Ecol 322:1–12CrossRefGoogle Scholar
  28. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2005b) Variation in phlorotannin content within two species of brown macroalgae (Desmarestia anceps and D. menziesii) from the Western Antarctic Peninsula. Polar Biol 28:680–686CrossRefGoogle Scholar
  29. Fairhead VA, Amsler CD, McClintock JB, Baker BJ (2006) Lack of defense or phlorotannin induction by UV radiation or mesograzers in Desmarestia anceps and D. menziesii. J Phycol 42:1174–1183CrossRefGoogle Scholar
  30. Feeny PP (1976) Plant apparency and chemical defense. Res Adv Phytochem 10:1–40Google Scholar
  31. Fraenkel GS (1959) The raison d’être of secondary plant substances. Science 129:1466–1470PubMedCrossRefGoogle Scholar
  32. Franklin LA, Yakovleva I, Karsten U, Lüning K (1999) Synthesis of mycosporine-like amino acids in Chondrus crispus (Florideophyceae) and the consequences for sensitivity to ultraviolet B radiation. J Phycol 35:682–693CrossRefGoogle Scholar
  33. Franklin LA, Kräbs G, Kuhlenkamp R (2001) Blue light and UV-A radiation control the synthesis of mycosporine-like amino acids in Chondrus crispus (Florideaphyceae). J Phycol 37:257–270CrossRefGoogle Scholar
  34. Hammerstrom K, Dethier MN, Duggins DO (1998) Rapid phlorotannin induction and relaxation in five Washington kelps. Mar Ecol Prog Ser 165:293–305CrossRefGoogle Scholar
  35. Haslam E (1985) Metabolites and metabolism. Clarendon, OxfordGoogle Scholar
  36. Hay ME (1996) Marine chemical ecology: what’s known and what’s next? J Exp Mar Biol Ecol 200:103–134CrossRefGoogle Scholar
  37. Hay ME, Steinberg PD (1992) The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites. Academic, New York, pp 371–413Google Scholar
  38. Hay ME, Paul VJ, Lewis SM, Gustavson K, Tucker J, Trindell RN (1988) Can tropical seaweeds reduce herbivory by growing at night? Diel patterns of growth, nitrogen content, herbivory, and chemical versus morphological defenses. Oecologia 75:233–245CrossRefGoogle Scholar
  39. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064CrossRefGoogle Scholar
  40. 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 273:109–120CrossRefGoogle Scholar
  41. Hemmi A, Mäkinen A, Jormalainen V, Honkanen T (2005) Responses of growth and phlorotannins in Fucus vesiculosus to nutrient enrichment and herbivory. Aquat Ecol 39:201–211CrossRefGoogle Scholar
  42. Henry BE, Van Alstyne KL (2004) Effects of UV radiation on growth and phlorotannins in Fucus gardneri (Phaeophyceae) juveniles and embryos. J Phycol 40:527–533CrossRefGoogle Scholar
  43. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or to defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  44. Honkanen T, Jormalainen V, Hemmi A, Mäkinen A, Heikkilä N (2002) Feeding and growth of the isopod Idotea baltica on the brown alga Fucus vesiculosus: roles of inter-population and within-plant variation in plant quality. Ecoscience 9:332–338Google Scholar
  45. Hoyer K, Karsten U, Wiencke C (2002) Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Mar Biol 141:619–627CrossRefGoogle Scholar
  46. Ilvessalo H, Tuomi J (1989) Nutrient availability and accumulation of phenolic compounds in the brown algae Fucus vesiculosus. Mar Biol 101:115–119CrossRefGoogle Scholar
  47. Jones CG, Firn RD (1991) On the evolution of plant chemical diversity. Phil Trans R Soc Lond B, Biol Sci 333:273–280CrossRefGoogle Scholar
  48. Jormalainen V, Honkanen T, Koivikko R, Eränen J (2003) Induction of phlorotannin production in a brown alga: defense or resource dynamics? Oikos 103:640–650CrossRefGoogle Scholar
  49. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, IllinoisGoogle Scholar
  50. Karsten U, Franklin LA, Lüning K, Wiencke C (1998) Natural ultraviolet radiation and photosynthetically active radiation induce formation of mycosporine-like amino acids in the marine macroalga Chondrus crispus (Rhodophyta). Planta 205:257–262CrossRefGoogle Scholar
  51. Karsten U, Bischof K, Hanelt D, Tüg H, Wiencke C (1999) The effect of ultraviolet radiation on photosynthesis and ultraviolet-absorbing substances in the endemic Arctic macroalga Devaleraea ramentacea (Rhodophyta). Physiol Plant 105:58–66CrossRefGoogle Scholar
  52. Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Ann Rev Plant Biol 53:299–328CrossRefGoogle Scholar
  53. 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 functions. J Chem Ecol 31:195–212PubMedCrossRefGoogle Scholar
  54. Koricheva J (2002) The carbon-nutrient balance hypothesis is dead; long live the carbon-nutrient balance hypothesis? Oikos 98:537–539CrossRefGoogle Scholar
  55. Kräbs G, Bischof K, Hanelt D, Karsten U, Wiencke C (2002) Wavelength-dependent induction of UV absorbing mycosporine-like amino acids in the red alga Chondrus crispus under natural solar radiation. J Exp Mar Biol Ecol 268:69–82CrossRefGoogle Scholar
  56. Lerdau M, Coley PD (2002) Benefits of the carbon-nutrient balance hypothesis. Oikos 98:534–536CrossRefGoogle Scholar
  57. Loomis WE (1932) Growth-differentiation balance vs carbohydrate-nitrogen ratio. Proc Am Soc Hort Sci 29:240–245Google Scholar
  58. Lüder UH, Clayton MN (2004) Induction of phlorotannins in the brown macroalga Ecklonia radiata (Laminariales, Phaeophyta) in response to simulated herbivory–the first microscopic study. Planta 218:928–937PubMedCrossRefGoogle Scholar
  59. 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 coasts of Chile: effects of mesograzers and UV radiation. J Exp Mar Biol Ecol 325:214–227CrossRefGoogle Scholar
  60. Martinez EA (1996) Micropopulation differentiation in phenol content and susceptibility to herbivory in the Chilean kelp Lessonia nigrescens (Phaeophyta, Laminariales). Hydrobiologia 326/327:205–211CrossRefGoogle Scholar
  61. McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320CrossRefGoogle Scholar
  62. McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with plant secondary metabolites. Academic, New York, pp 55–133Google Scholar
  63. Molis M, Körner J, Ko YW, Kim JH, Wahl M (2005) Inducible responses in the brown seaweed Ecklonia cava: the role of grazer identity and season. J Ecol 94:243–249CrossRefGoogle Scholar
  64. Nitao JK, Zangerl AR, Berenbaum MR (2002) CNB: requiescat in pace? Oikos 98:540–546CrossRefGoogle Scholar
  65. Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169CrossRefGoogle Scholar
  66. Paul VJ, Van Alstyne KL (1988) Chemical defense and chemical variation in some tropical Pacific species of Halimeda (Halimedaceae; Chlorophyta). Coral Reefs 6:263–269CrossRefGoogle Scholar
  67. Paul VJ, Puglisi MP, Ritson-Williams R (2006) Marine chemical ecology. Nat Prod Rep 23:153–180PubMedCrossRefGoogle Scholar
  68. Pavia H, Brock E (2000) Extrinsic factors influencing phlorotannin production in the brown seaweed Ascophyllum nodosum. Mar Ecol Prog Ser 193:285–294CrossRefGoogle Scholar
  69. Pavia H, Toth GB (2000a) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225Google Scholar
  70. Pavia H, Toth GB (2000b) Influence of light and nitrogen on the phlorotannin content. of the brown seaweeds Ascophyllum nodosum and Fucus vesiculosus. Hydrobiologia 440:299–305CrossRefGoogle Scholar
  71. Pavia H, Cervin G, Lindgren A, Åberg P (1997) Effects of UV-B radiation and simulated herbivory on phlorotannins in the brown alga Ascophyllum nodosum. Mar Ecol Prog Ser 157:139–146CrossRefGoogle Scholar
  72. Pavia H, Toth G, Åberg P (1999) Trade-offs between phlorotannin production and annual growth in the brown seaweed Ascophyllum nodosum. J Ecol 87:761–771CrossRefGoogle Scholar
  73. Pavia H, Toth GB, Åberg P (2002) Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891–897CrossRefGoogle Scholar
  74. Pavia H, Toth GB, Lindgren A, Åberg P (2003) Intraspecific variation in the phlorotannin content of the brown alga Ascophyllum nodosum. Phycologia 42:378–383CrossRefGoogle Scholar
  75. 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 138:209–217CrossRefGoogle Scholar
  76. Peinado NK, Diaz RTA, Figueroa FL, Helbling EW (2004) Ammonium and UV radiation stimulate the accumulation of mycosporine-like amino acids in Porphyra columbina (Rhodophyta) from Patagonia, Argentina. J Phycol 40:248–259CrossRefGoogle Scholar
  77. Plouguerné E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger-Pouvreau V (2006) Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquat Bot 85:337–344CrossRefGoogle Scholar
  78. Pohnert G (2004) Chemical defense strategies of marine organisms. Topics Curr Chem 239:179–219CrossRefGoogle Scholar
  79. Potin P, Bouarab K, Salaün J-P, Pohnert G, Kloareg B (2002) Biotic interactions off marine algae. Cur Opin Plant Biol 5:308–317CrossRefGoogle Scholar
  80. Puglisi MP, Paul VJ (1997) Intraspecific variation in the red alga Portieria hornemannii: monoterpene concentrations are not influenced by nitrogen or phosphorous enrichment. Mar Biol 128:161–170CrossRefGoogle Scholar
  81. Ragan MA, Glombitza K-W (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241Google Scholar
  82. Renaud PE, Hay ME, TM Schmitt (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
  83. Reichardt PB, Chapin III FS, Bryant JP, Mattes BR, Clausen TP (1991) Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: potential importance of metabolic turnover. Oecologia 88:401–406CrossRefGoogle Scholar
  84. Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 3–54Google Scholar
  85. Robinson T (1974) Metabolism and function of alkaloids in plants. Science 184:430–435PubMedCrossRefGoogle Scholar
  86. Roff DA (1992) Evolution of life histories: theory and analysis. Chapman & Hall, New YorkGoogle Scholar
  87. 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
  88. Roleda MY, Wiencke C, Lüder UH (2006) Impact of ultraviolet radiation on cell structure, UV-absorbing compounds, photosynthesis, DNA damage, and germination in zoospores of Arctic Saccorhiza dermatodea. J Exp Bot 57:3847–3856PubMedCrossRefGoogle Scholar
  89. Rothäusler E, Thiel M (2006) Effect of detachment on the palatability of two kelp species. J Appl Phycol 18:423–435CrossRefGoogle Scholar
  90. Rothäusler E, Macaya EC, Molis M, Wahl M, Thiel M (2005) Laboratory experiments examining inducible defence show variable responses of temperate brown and red macroalgae. Revista Chilena de Historia Natural 78:603–614CrossRefGoogle Scholar
  91. Simms EL (1992) Cost of plant resistance to herbivory. In: Fritz RS, Simms EL (eds) Plants resistance to herbivores and pathogens. University of Chicago Press, Chicago, pp 392–425Google Scholar
  92. Simms EL, Rausher MD (1987) Cost and benefits of plant resistance to herbivory. Am Nat 130:570–581CrossRefGoogle Scholar
  93. Sotka E, 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 277:1–12CrossRefGoogle Scholar
  94. Stamp N (2003) Out of the quagmire of plant defense hypotheses. Q Rev Biol 78:23–55PubMedCrossRefGoogle Scholar
  95. Stamp N (2004) Can the growth-differentiation balance hypothesis be tested rigorously? Oikos 107:439–448CrossRefGoogle Scholar
  96. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  97. Steinberg PD (1984) Algal chemical defense against herbivores: allocation of phenolic compounds in the kelp Alaria marginata. Science 223:405–407PubMedCrossRefGoogle Scholar
  98. Steinberg PD (1992) Geographical variation in the interaction between marine herbivores and brown algal secondary metabolites. In: Paul VJ (ed) Ecological roles of marine natural products. Cornell University, New York, pp 51–92Google Scholar
  99. Steinberg PD (1994) Lack of short-term induction of phlorotannins in the Australasian brown algae Ecklonia radiata and Sargassum vestitum. Mar Ecol Prog Ser 112:129–133CrossRefGoogle Scholar
  100. Steinberg PD (1995) Interaction between the canopy dwelling echinoid Holopneustes purpurescens and its host kelp Ecklonia radiata. Mar Ecol Prog Ser 127:169–181CrossRefGoogle Scholar
  101. Stiger V, Deslandes E, Payri CE (2004) Phenolic contents of two brown algae, Turbinaria ornata and Sargassum mangarevense on Tahiti (French Polynesia): interspecific, ontogenetic and spatio-temporal variations. Bot Mar 47:402–409CrossRefGoogle Scholar
  102. Svensson CJ, Pavia H, Toth GB (2007) Do plant density, nutrient availability, and herbivore grazing interact to affect phlorotannin plasticity in the brown seaweed Ascophyllum nodosum? Mar Biol 151:2177–2181CrossRefGoogle Scholar
  103. Swanson AK, Druehl LD (2002) Induction, exudation and the UV protective role of kelp phlorotannins. Aquat Bot 73:241–253CrossRefGoogle Scholar
  104. Tallamy DW, Raupp MJ (1991) Phytochemical induction by herbivores. Wiley, New YorkGoogle Scholar
  105. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76CrossRefGoogle Scholar
  106. Toth GB (2007) Screening for induced herbivore resistance in Swedish intertidal seaweeds. Mar Biol 151:1597–1604CrossRefGoogle Scholar
  107. Toth GB, Pavia H (2000a) Water-borne cues induce chemical defense in a marine alga (Ascophyllum nodosum). Proc Natl Acad Sci USA 97:14418–14420PubMedCrossRefGoogle Scholar
  108. Toth GB, Pavia H (2000b) Lack of phlorotannin induction in the brown seaweed Ascophyllum nodosum in response to increased copper concentrations. Mar Ecol Prog Ser 192:119–126CrossRefGoogle Scholar
  109. Toth GB, Pavia H (2002) Lack of phlorotannin induction in the kelp Laminaria hyperborea in response to grazing by two gastropod herbivores. Mar Biol 140:403–409CrossRefGoogle Scholar
  110. Toth GB, Pavia H (2007) Induced resistance in seaweeds: a meta-analysis. J Ecol 95:425–434CrossRefGoogle Scholar
  111. Toth GB, Langhamer O, Pavia H (2005) Inducible and constitutive defenses of valuable seaweed tissues: consequences for herbivore fitness. Ecology 86:612–618CrossRefGoogle Scholar
  112. Toth GB, Karlsson M, Pavia H (2007) Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia 152:245–255PubMedCrossRefGoogle Scholar
  113. Tugwell S, Branch GM (1992) Differential polyphenolic distribution among tissues in the kelps Ecklonia maxima, Laminaria pallida and Macrocystis angustifolia in relation to plant-defence theory. J Exp Mar Biol Ecol 129:219–230CrossRefGoogle Scholar
  114. Tuomi J (1992) Toward integration of plant defense theories. Trend Ecol Evol 7:365–367CrossRefGoogle Scholar
  115. Tuomi J, Ilvessalo H, Niemelä P, Sirén S, Jormalainen V (1989) Within-plant variation in phenolic content and toughness of the brown alga Fucus vesiculosus L. Bot Mar 32:505–509CrossRefGoogle Scholar
  116. Tuomi J, Niemelä P, Sirén S (1990) The Panglossian paradigm and delayed inducible accumulation of foliar phenolics in mountain birch. Oikos 59:399–410CrossRefGoogle Scholar
  117. Van Alstyne KL (1988) Herbivore grazing increases polyphenolic defenses in the intertidal brown alga Fucus distichus. Ecology 69:655–663CrossRefGoogle Scholar
  118. Van Alstyne KL (1989) Adventitious branching as a herbivore-induced defense in the intertidal brown alga Fucus distichus. Mar Ecol Prog Ser 56:169–176CrossRefGoogle Scholar
  119. Van Alstyne KL, Pelletreau KN (2000) Effects of nutrient enrichment on growth and phlorotannin production in Fucus gardneri embryos. Mar Ecol Prog Ser 206:33–43CrossRefGoogle Scholar
  120. Van Alstyne KL, McCarthy III JJ, Hystead CL, Kearns LJ (1999) Phlorotannin allocation among tissues of Northeastern Pacific kelps and rockweeds. J Phycol 35:483–492CrossRefGoogle Scholar
  121. Van Alstyne KL, Dethier MN, Duggins DO (2001a) Spatial patterns in macroalgal chemical defenses. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC, Boca Raton, FL, pp 301–324Google Scholar
  122. Van Alstyne KL, Whitman SL, Ehlig JM (2001b) Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Mar Biol 139:201–210CrossRefGoogle Scholar
  123. Waterman PG, Mole S (1989) Extrinsic factors influencing production of secondary metabolites in plants. In: Bernays EA (ed) Insect-plant interactions. CRC, Boca Raton, FL, pp 107–164Google Scholar
  124. 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
  125. Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766CrossRefGoogle Scholar
  126. Zangerl AR, Bazzaz FA (1992) Theory and pattern in plant defense allocation. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens. Chicago Press, Chicago, pp 363–391Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Henrik Pavia
    • 1
  • Gunilla B. Toth
    • 1
  1. 1.Department of Marine EcologyGöteborg UniversitySweden

Personalised recommendations