Oecologia

, 155:751 | Cite as

Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish

  • Adriana Vergés
  • Marta Pérez
  • Teresa Alcoverro
  • Javier Romero
Plant-Animal Interactions - Original Paper

Abstract

Herbivory can induce changes in plant traits that may involve both tolerance mechanisms that compensate for biomass loss and resistance traits that reduce herbivore preference. Seagrasses are marine vascular plants that possess many attributes that may favour tolerance and compensatory growth, and they are also defended with mechanisms of resistance such as toughness and secondary metabolites. We quantified phenotypic changes induced by herbivore damage on the temperate seagrass Posidonia oceanica in order to identify specific compensatory and resistance mechanisms in this plant, and to assess any potential trade-offs between these two strategies of defence. We simulated three natural levels of fish herbivory by repeatedly clipping seagrass leaves during the summer period of maximum herbivory. Compensatory responses were determined by measuring shoot-specific growth, photosynthetic rate, and the concentration of nitrogen and carbon resources in leaves and rhizomes. Induced resistance was determined by measuring the concentration of phenolic secondary metabolites and by assessing the long-term effects of continued clipping on herbivore feeding preferences using bioassays. Plants showed a significant ability to compensate for low and moderate losses of leaf biomass by increasing aboveground growth of damaged shoots, but this was not supported by an increase in photosynthetic capacity. Low levels of herbivory induced compensatory growth without any measurable effects on stored resources. In contrast, nitrogen reserves in the rhizomes played a crucial role in the plant’s ability to compensate and survive herbivore damage under moderate and high levels of herbivory, respectively. We found no evidence of inducibility of long-term resistance traits in response to herbivory. The concentration of phenolics decreased with increasing compensatory growth despite all treatments having similar carbon leaf content, suggesting reallocation of these compounds towards primary functions such as cell-wall construction.

Keywords

Compensatory growth Tolerance Resistance Defence Phenolic compounds Induced responses Plant–herbivore interactions Mediterranean sea 

References

  1. Abdulrazzak N et al (2006) A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growth. Plant Physiol 140:30–48PubMedCrossRefGoogle Scholar
  2. Agostini S, Desjobert J, Pergent G (1998) Distribution of phenolic compounds in the seagrass Posidonia oceanica. Phytochemistry 48:611–617CrossRefGoogle Scholar
  3. Alcoverro T, Duarte CM, Romero J (1995) Annual growth dynamics of Posidonia oceanica—contribution of large-scale versus local factors to seasonality. Mar Ecol Prog Ser 120:203–210CrossRefGoogle Scholar
  4. Alcoverro T, Manzanera M, Romero J (1998) Seasonal and age-dependent variability of Posidonia oceanica (L.) Delile photosynthetic parameters. J Exp Mar Biol Ecol 230:1–13CrossRefGoogle Scholar
  5. Alcoverro T, Zimmerman RC, Kohrs DG, Alberte RS (1999) Resource allocation and sucrose mobilization in light-limited eelgrass Zostera marina. Mar Ecol Prog Ser 187:121–131CrossRefGoogle Scholar
  6. Alcoverro T, Manzanera M, Romero J (2000) Nutrient mass balance of the seagrass Posidonia oceanica: the importance of nutrient retranslocation. Mar Ecol Prog Ser 194Google Scholar
  7. Alcoverro T, Cerbian E, Ballesteros E (2001a) The photosynthetic capacity of the seagrass Posidonia oceanica: influence of nitrogen and light. J Exp Mar Biol Ecol 261:107–120PubMedCrossRefGoogle Scholar
  8. Alcoverro T, Manzanera M, Romero J (2001b) Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Mar Ecol Prog Ser 211:105–116CrossRefGoogle Scholar
  9. Amsler CD, Fairhead VA (2006) Defensive and sensory chemical ecology of brown algae. Adv Bot Res 43:1–91CrossRefGoogle Scholar
  10. Aragones LV, Lawler IR, Foley WJ, Marsh H (2006) Dugong grazing and turtle cropping: grazing optimization in tropical seagrass systems?. Oecologia 149:635–647PubMedCrossRefGoogle Scholar
  11. Arnold TM, Targett NM (2003) To grow and defend: lack of tradeoffs for brown algal phlorotannins. Oikos 100:406–408CrossRefGoogle Scholar
  12. Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93CrossRefGoogle Scholar
  13. Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants—herbivore optimization or red herring. Evol Ecol 7:109–121CrossRefGoogle Scholar
  14. Bennett RN, Wallsgrove RM (1994) Secondary metabolites in plant defense mechanisms. New Phytol 127:617–633CrossRefGoogle Scholar
  15. Boege K (2005) Influence of plant ontogeny on compensation to leaf damage. Am J Bot 92:1632–1640CrossRefGoogle Scholar
  16. Bolser R, Hay M, Lindquist N, Fenical W, Wilson D (1998) Chemical defenses of freshwater macrophytes against crayfish herbivory. J Chem Ecol 24:1639–1658CrossRefGoogle Scholar
  17. Boudouresque CF, Meinesz A (1982) Découverte de l’herbier de Posidonies. Cahier du Parc National de Port-Cros 4:1–79Google Scholar
  18. Boudouresque C, Verlaque M (2001) Ecology of Paracentrotus lividus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 177–216Google Scholar
  19. Cebrian J, Duarte CM, Agawin NSR, Merino M (1998) Leaf growth response to simulated herbivory: a comparison among seagrass species. J Exp Mar Biol Ecol 220:67–81CrossRefGoogle Scholar
  20. Cuny P, Serve L, Jupin H, Boudouresque CF (1995) Water soluble phenolic compounds of the marine phanerogam Posidonia oceanica in a Mediterranean area colonised by the introduced chlorophyte Caulerpa taxifolia. Aquat Bot 52:237–242CrossRefGoogle Scholar
  21. Cyr H, Pace ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150CrossRefGoogle Scholar
  22. Dawes C, Guiry M (1992) Proximate constituents in the Seagrasses Zostera marina and Z. noltii in Ireland: seasonal changes and the effect of blade removal. Mar Ecol 13:307–315CrossRefGoogle Scholar
  23. Ferraro DO, Oesterheld M (2002) Effect of defoliation on grass growth. A quantitative review. Oikos 98:125–133CrossRefGoogle Scholar
  24. Fineblum WL, Rausher MD (1995) Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377:517–520CrossRefGoogle Scholar
  25. Fritz R, Simms E (1992) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, ChicagoGoogle Scholar
  26. Fry SC (2000) The growing plant cell wall: chemical and metabolic analysis. The Blackburn Press, CaldwellGoogle Scholar
  27. Heck KL, Valentine JF (1995) Sea-urchin herbivory—evidence for long-lasting effects in subtropical seagrass meadows. J Exp Mar Biol Ecol 189:205–217CrossRefGoogle Scholar
  28. Honkanen T, Jormalainen V (2002) Within-alga integration and compensation: Effects of simulated herbivory on growth and reproduction of the brown alga, Fucus vesiculosus. Int J Plant Sci 163:815–823CrossRefGoogle Scholar
  29. Hulme PE (1996) Herbivory, plant regeneration, and species coexistence. J Ecol 84:609–615CrossRefGoogle Scholar
  30. Invers O, Perez M, Romero J (2002) Seasonal nitrogen speciation in temperate seagrass Posidonia oceanica (L.) Delile. J Exp Mar Biol Ecol 273:219–240CrossRefGoogle Scholar
  31. Invers O, Kraemer GP, Perez M, Romero J (2004) Effects of nitrogen addition on nitrogen metabolism and carbon reserves in the temperate seagrass Posidonia oceanica. J Exp Mar Biol Ecol 303:97–114CrossRefGoogle Scholar
  32. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, ChicagoGoogle Scholar
  33. Leimu R, Koricheva J (2006) A meta-analysis of genetic correlations between plant resistances to multiple enemies. Am Nat 168:E15–E37PubMedCrossRefGoogle Scholar
  34. Littler MM, Littler DS, Taylor PR (1995) Selective herbivore increases biomass of its prey—a chiton-coralline reef-building association. Ecology 76:1666–1681CrossRefGoogle Scholar
  35. Lockwood JR (1998) On the statistical analysis of multiple-choice feeding preference experiments. Oecologia 116:475–481CrossRefGoogle Scholar
  36. Lubchenco J, Gaines SD (1981) A unified approach to marine plant-herbivore interactions. 1. Populations and communities. Ann Rev Ecol Syst 12:405–437CrossRefGoogle Scholar
  37. Macpherson E, Gordoa A, Garcia-Rubies A (2002) Biomass size spectra in littoral fishes in protected and unprotected areas in the NW Mediterranean. Estuar Coast Shelf Sci 55:777–788CrossRefGoogle Scholar
  38. Marbà N et al (2002) Carbon and nitrogen translocation between seagrass ramets. Mar Ecol Prog Ser 226:287–300CrossRefGoogle Scholar
  39. Marbà N, Hemminga MA, Duarte CM (2006) Resource translocation within seagrass clones: allometric scaling to plant size and productivity. Oecologia 150:362–372PubMedCrossRefGoogle Scholar
  40. McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca RatonGoogle Scholar
  41. McMillan C (1984) The condensed tannins (Proanthocyanidins) in seagrasses. Aquat Bot 20:351–357CrossRefGoogle Scholar
  42. McNaughton SJ, Oesterheld M, Frank DA, Williams KJ (1989) Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature 341:142–144PubMedCrossRefGoogle Scholar
  43. Moran KL, Bjorndal KA (2005) Simulated green turtle grazing affects structure and productivity of seagrass pastures. Mar Ecol Prog Ser 305:235–247CrossRefGoogle Scholar
  44. Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225Google Scholar
  45. Pellegrini L, Pellegrini M (1993) Ultrastructural differentiation of the tanniniferous cells in the marine phanerogam Posidonia oceanica (L.) Delile. Bot Mar 36:179–187CrossRefGoogle Scholar
  46. Pohnert G (2004) Chemical defense strategies of marine organisms. Chem Pheromones Other Semiochem I 239:179–219CrossRefGoogle Scholar
  47. Prado P, Tomas F, Alcoverro T, Romero J (2007a) New evidence of the importance of herbivory on seagrass food webs: extensive direct measurements of P. oceanica consumption in continental meadows. Mar Ecol Prog Ser 340:63–71CrossRefGoogle Scholar
  48. Prado P, Alcoverro T, Martínez-Crego B, Vergés A, Pérez M, Romero J (2007b) Macrograzers strongly influence patterns of epiphytic assemblages in seagrass meadows. J Exp Mar Biol Ecol 350:130–143CrossRefGoogle Scholar
  49. Procaccini G et al (2003) The seagrasses of the Western Mediterranean. In: Green EP, Short FT (eds) World Atlas of seagrasses. University of California Press, CaliforniaGoogle Scholar
  50. Prusak AC, O’Neal J, Kubanek J (2005) Prevalence of chemical defenses among freshwater plants. J Chem Ecol 31:1145–1160PubMedCrossRefGoogle Scholar
  51. Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeGoogle Scholar
  52. Romero J (1989) Primary production of Posidonia oceanica beds in the Medes Islands (Girona, NE Spain). In: Boudouresque CF, Meinesz A, Fresi E, Gravez V (eds) International Workshop on Posidonia oceanica beds 2, vol GIS Posidonie, Marseille, pp 85–91Google Scholar
  53. Romero J, Lee KS, Pérez M, Mateo MA, Alcoverro T (2006) Nutrient dynamics in seagrass ecosystems. In: Larkum A, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, HeidelbergGoogle Scholar
  54. Steneck RS (1982) A limpet-coralline alga association—adaptations and defenses between a selective herbivore and its prey. Ecology 63:507–522CrossRefGoogle Scholar
  55. Stowe KA (1998) Experimental evolution of resistance in Brassica rapa: correlated response of tolerance in lines selected for glucosinolate content. Evolution 52:703–712CrossRefGoogle Scholar
  56. Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Ann Rev Ecol Syst 31:565–595CrossRefGoogle Scholar
  57. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedCrossRefGoogle Scholar
  58. Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know?. Evol Ecol 14:523–536CrossRefGoogle Scholar
  59. Tomas F, Turon X, Romero J (2005) Seasonal and small-scale spatial variability of herbivory pressure on the temperate seagrass Posidonia oceanica. Mar Ecol Prog Ser 301:95–107CrossRefGoogle Scholar
  60. Tomasko DA, Dawes CJ (1989) Effects of partial defoliation on remaining intact leaves in the seagrass Thalassia testudinum Banks Ex Konig. Bot Mar 32:235–240Google Scholar
  61. Valentine J, Duffy J (2006) The central role of grazing in seagrasses ecosystems. In: Larkum A, Orth R, Duarte C (eds) Seagrasses: biology, ecology and conservation. Springer, HeidelbergGoogle Scholar
  62. Valentine JF, Heck KL, Busby J, Webb D (1997) Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum) meadow. Oecologia 112:193–200CrossRefGoogle Scholar
  63. Valentine JF, Heck KL, Kirsch KD, Webb D (2000) Role of sea urchin Lytechinus variegatus grazing in regulating subtropical turtlegrass Thalassia testudinum meadows in the Florida Keys (USA). Mar Ecol Prog Ser 200:213–228CrossRefGoogle Scholar
  64. Vandermeijden E, Wijn M, Verkaar HJ (1988) Defense and regrowth, alternative plant strategies in the struggle against herbivores. Oikos 51:355–363CrossRefGoogle Scholar
  65. Vergés A, Becerro MA, Alcoverro T, Romero J (2007a) Variation in multiple traits of vegetative and reproductive seagrass tissues influences plant-herbivore interactions. Oecologia 151:675–686PubMedCrossRefGoogle Scholar
  66. Vergés A, Becerro MA, Alcoverro T, Romero J (2007b) Experimental evidence of chemical deterrence against multiple herbivores in the seagrass Posidonia oceanica. Mar Ecol Prog Ser 343:107–114CrossRefGoogle Scholar
  67. Wai TC, Williams GA (2005) The relative importance of herbivore-induced effects on productivity of crustose coralline algae: Sea urchin grazing and nitrogen excretion. J Exp Mar Biol Ecol 324:141–156CrossRefGoogle Scholar
  68. Williams S (1988) Thalassia testudinum productivity and grazing by green turtles in a highly disturbed seagrass bed. Mar Biol 98:447–455CrossRefGoogle Scholar
  69. Zapata O, McMillan C (1979) Phenolic acids in seagrasses. Aquat Bot 7:307–317CrossRefGoogle Scholar
  70. Zimmerman RC, Kohrs DG, Alberte RS (1996) Top-down impact through a bottom-up mechanism: The effect of limpet grazing on growth, productivity and carbon allocation of Zostera marina L (eelgrass). Oecologia 107:560–567CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Adriana Vergés
    • 1
  • Marta Pérez
    • 2
  • Teresa Alcoverro
    • 1
  • Javier Romero
    • 2
  1. 1.Centre d’Estudis Avançats de BlanesCSICBlanes, GironaSpain
  2. 2.Departament d’EcologiaUniversitat de Barcelona BarcelonaSpain

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