, Volume 174, Issue 3, pp 789–801 | Cite as

Major consequences of minor damage: impacts of small grazers on fast-growing kelps

  • Alistair G. B. PooreEmail author
  • Lars Gutow
  • José F. Pantoja
  • Fadia Tala
  • David Jofré Madariaga
  • Martin Thiel
Plant-microbe-animal interactions - Original research


Damage by small herbivores can have disproportionately large effects on the fitness of individual plants if damage is concentrated on valuable tissues or on select individuals within a population. In marine systems, the impact of tissue loss on the growth rates of habitat-forming algae is poorly understood. We quantified the grazing damage by an isopod Amphoroidea typa on two species of large kelps, Lessonia spicata and Macrocystis pyrifera, in temperate Chile to test whether non-lethal grazing damage could reduce kelp growth rates and photosynthetic efficiency. For L. spicata, grazing damage was widespread in the field, unevenly distributed on several spatial scales (among individuals and among tissue types) and negatively correlated with blade growth rates. In field experiments, feeding by A. typa reduced the concentration of photosynthetic pigments and led to large reductions (~80 %) in blade growth rates despite limited loss of kelp biomass (0.5 % per day). For M. pyrifera, rates of damage in the field were lower and high densities of grazers were unable to reduce growth rates in field experiments. These results demonstrate that even low per capita grazing rates can result in large reductions in the growth of a kelp, due the spatial clustering of herbivores in the field and the selective removal of photosynthetically active tissues. The impacts of small herbivores on plant performance are thus not easily predicted from consumption rates or abundance in the field, and vary with plant species due to variation in their ability to compensate for damage.


Grazing Herbivory Isopods Lessonia Mesograzers Macroalgae Macrocystis Plant–herbivore interactions 



We thank L. Jorquera, L. Miranda and G. Penna for assistance with field and laboratory work, A. Letten for assistance with analyses and J. Shurin and two anonymous reviewers for comments that improved this manuscript. Research was supported by FONDECYT grant 1100749 to M.T. and BMBF-CONICYT grant 01DN12106 to M.T. and L.G.

Supplementary material

442_2013_2795_MOESM1_ESM.pdf (214 kb)
Supplementary material 1 (PDF 213 kb)


  1. Anderson MJ, Gorley RN, Clark KR (2006) PERMANOVA+ for PRIMER: guide to software and statistical methodsGoogle Scholar
  2. Black R (1976) The effects of grazing by the limpet, Acmaea insessa, on the kelp, Egregia laevigata, in the intertidal zone. Ecology 57:265–277CrossRefGoogle Scholar
  3. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448PubMedCrossRefGoogle Scholar
  4. Brawley SH (1992) Mesoherbivores. In: John DM, Hawkins SJ, Price JH (eds) Plant–animal interactions in the marine benthos. Clarendon, Oxford, pp 235–263Google Scholar
  5. Campbell AH, Vergés A, Steinberg PD (2013) Demographic consequences of disease in a habitat-forming seaweed and impacts on interactions between natural enemies. Ecology
  6. Cerda O, Karsten U, Rothäusler E, Tala F, Thiel M (2009) Compensatory growth of the kelp Macrocystis integrifolia (Phaeophyceae, Laminariales) against grazing of Peramphithoe femorata (Amphipoda, Ampithoidae) in northern-central Chile. J Exp Mar Biol Ecol 377:61–67CrossRefGoogle Scholar
  7. Chess JR (1993) Effects of the stipe-boring amphipod Peramphithoe stypotrupetes (Corophioidea: Ampithoidae) and grazing gastropods on the kelp Laminaria setchelli. J Crustac Biol 13:638–646CrossRefGoogle Scholar
  8. Cook K, Vanderklift MA, Poore AGB (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269CrossRefGoogle Scholar
  9. Crawley MJ (1985) Reduction of oak fecundity by low-density herbivore populations. Nature 314:163–164CrossRefGoogle Scholar
  10. Cyr H, Pace ML (1993) Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. Nature 361:148–150CrossRefGoogle Scholar
  11. Davenport AC, Anderson TW (2007) Positive indirect effects of reef fishes on kelp performance: the importance of mesograzers. Ecology 88:1548–1561PubMedCrossRefGoogle Scholar
  12. de Bettignies T, Thomsen MS, Wernberg T (2012) Wounded kelps: patterns and susceptibility to breakage. AquatiBiol 17:223–233CrossRefGoogle Scholar
  13. Dean TA, Schroeter SC, Dixon JD (1984) Effects of grazing by two species of sea urchins (Strongylocentrotus franciscanus and Lytechinus anamesus) on recruitment and survival of two species of kelp (Macrocystis pyrifera and Pterygophora californica). Mar Biol 78:301–313CrossRefGoogle Scholar
  14. Doak DF (1992) Lifetime impacts of herbivory for a perennial plant. Ecology 73:2086–2099Google 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. Duffy JE, Richardson JP, France KE (2005) Ecosystem consequences of diversity depend on food chain length in estuarine vegetation. Ecol Lett 8:301–309CrossRefGoogle Scholar
  17. Duggins D, Eckman JE, Siddon CE, Klinger T (2001) Interactive roles of mesograzers and current flow in survival of kelps. Mar Ecol Prog Ser 223:143–155CrossRefGoogle Scholar
  18. Gómez I, Ulloa N, Orostegui M (2005) Morpho-functional patterns of photosynthesis and UV sensitivity in the kelp Lessonia nigrescens (Laminariales, Phaeophyta). Mar Biol 148:231–240CrossRefGoogle Scholar
  19. González A, Beltrán J, Hiriart-Bertrand L, Flores V, de Reviers B, Correa JA, Santelices B (2012) Identification of cryptic species in the Lessonia nigrescens complex (Phaeophyceae, Laminariales). J Phycol 48:1153–1165CrossRefGoogle Scholar
  20. Graham MH (2002) Prolonged reproductive consequences of short-term biomass loss in seaweeds. Mar Biol 140:901–911CrossRefGoogle Scholar
  21. Graham MH, Vásquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol Annu Rev 45:39–88Google Scholar
  22. Gutow L, Long JD, Cerda O, Hinojosa IA, Rothäusler E, Tala F, Thiel M (2011) Herbivorous amphipods inhabit protective microhabitats within thalli of giant kelp Macrocystis pyrifera. Mar Biol 159:141–149CrossRefGoogle Scholar
  23. Hammons DL, Kurtural SK, Newman MC, Potter DA (2009) Invasive Japanese beetles facilitate aggregation and injury by a native scarab pest of ripening fruits. Proc Natl Acad Sci USA 106:3686–3691PubMedCrossRefGoogle Scholar
  24. Hay KB, Poore AGB, Lovelock CE (2011) Tolerance to herbivory in a brown seaweed and the effects of nutrient availability. J Ecol 99:1540–1550CrossRefGoogle Scholar
  25. Henley WJ, Dunton KH (1995) A seasonal comparison of carbon, nitrogen, and pigment content in Laminaria solidungula and L. saccharina (Phaeophyta) in the Alaskan Arctic. J Phycol 31:325–331CrossRefGoogle Scholar
  26. Henríquez LA, Buschmann AH, Maldonado MA, Graham MH, Hernández-González MC, Pereda SV, Bobadilla MI (2011) Grazing on giant kelp microscopic phases and the recruitment success of annual populations of Macrocystis pyrifera (Laminariales, Phaeophyta) in southern Chile. J Phycol 47:252–258CrossRefGoogle Scholar
  27. Hinojosa E, González P, Ugalde P, Valdivia N, Macaya E, Thiel M (2007) Distribución y abundancia de macroalgas flotando a la deriva y su fauna peracárida asociada en los canales de la XI región. Chile, Ciencia y Technologia del Mar 30Google Scholar
  28. Inskeep WP, Bloom PR (1985) Extinction coefficients of chlorophyll a and b in N, N-dimethyl-formamide and 80 % acetone. Plant Physiol 77:483–485PubMedCentralPubMedCrossRefGoogle Scholar
  29. Johnson CR, Mann KH (1986) The importance of plant defence abilities to the structure of subtidal seaweed communities: the kelp Laminaria longicruris de la Pylaie survives grazing by the snail Lacuna vincta (Montagu) at high population densities. J Exp Mar Biol Ecol 97:231–267CrossRefGoogle Scholar
  30. Krebs CJ (1999) Ecological methodology, 2nd edn. Benjamin/Cummings, Menlo ParkGoogle Scholar
  31. Krumhansl KA, Scheibling RE (2011) Spatial and temporal variation in grazing damage by the gastropod Lacuna vincta in Nova Scotian kelp beds. Aquat Biol 13:163–173CrossRefGoogle Scholar
  32. Krumhansl KA, Scheibling RE (2012) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302CrossRefGoogle Scholar
  33. Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80:135–149Google Scholar
  34. Lewis LS, Anderson TW (2012) Top-down control of epifauna by fishes enhances seagrass production. Ecology 93:2746–2757PubMedCrossRefGoogle Scholar
  35. Marquis RJ (1996) Plant architecture, sectoriality and plant tolerance to herbivores. Vegetation 127:85–97CrossRefGoogle Scholar
  36. Molis M, Enge A, Karsten U (2010) Grazing impact of, and indirect interactions between mesograzers associated with kelp (Laminaria digitata). J Phycol 46:76–84CrossRefGoogle Scholar
  37. Morris WF, Hufbauer RA, Agrawal AA, Bever JD, Borowicz VA, Gilbert GS, Maron JL, Mitchell CE, Parker IM, Power AG, Torchin ME, Vázquez DP (2007) Direct and interactive effects of enemies and mutualists on plant performance: a meta-analysis. Ecology 88:1021–1029PubMedCrossRefGoogle Scholar
  38. Muñoz M, Santelices B (1989) Determination of the distribution and abundance of the limpet Scurria scurra on the stipes of the kelp Lessonia nigrescens in Central Chile. Mar Ecol Prog Ser 54:277–285CrossRefGoogle Scholar
  39. Newcombe EM, Taylor RB (2010) Trophic cascade in a seaweed-epifauna-fish food chain. Mar Ecol Prog Ser 408:161–167CrossRefGoogle Scholar
  40. Pansch C, Gómez I, Rothäusler E, Véliz K, Thiel M (2008) Species-specific defences strategies of vegetative versus reproductive blades of the Pacific kelps Lessonia nigrescens and Macrocystis integrifolia. Mar Biol 155:51–52CrossRefGoogle Scholar
  41. Pavia H, Toth G, Åberg P (2002) Optimal defense theory: elasticity analysis as a tool to predict intraplant variation in defenses. Ecology 83:891–897CrossRefGoogle Scholar
  42. Pérez-Matus A, Shima JS (2010) Density- and trait-mediated effects of fish predators on amphipod grazers: potential indirect benefits for the giant kelp Macrocystis pyrifera. Mar Ecol Prog Ser 417:151–158CrossRefGoogle Scholar
  43. Poore AGB (1994) Selective herbivory by amphipods inhabiting the brown alga Zonaria angustata. Mar Ecol Prog Ser 107:113–122CrossRefGoogle Scholar
  44. Poore AGB, Campbell AH, Steinberg PD (2009) Natural densities of mesograzers fail to limit the growth of macroalgae or their epiphytes in a temperate algal bed. J Ecol 97:164–175CrossRefGoogle Scholar
  45. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA, Duffy JE (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922PubMedCrossRefGoogle Scholar
  46. Prado P, Collier CJ, Romero J, Alcoverro T (2011) Distinctive types of leaf tissue damage influence nutrient supply to growing tissues within seagrass shoots. Mar Biol 158:1473–1482CrossRefGoogle Scholar
  47. Puentes A, Ågren J (2012) Additive and non-additive effects of simulated leaf and inflorescence damage on survival, growth and reproduction of the perennial herb Arabidopsis lyrata. Oecologia 169:1033–1042PubMedCrossRefGoogle Scholar
  48. Rothäusler E, Thiel M (2006) Effect of detachment on the palatability of two kelp species. J Appl Phycol 18:423–435CrossRefGoogle Scholar
  49. Sala E, Graham MH (2002) Community-wide distribution of predator-prey interactions strength in kelp forests. Proc Natl Acad Sci USA 99:3683–3768CrossRefGoogle Scholar
  50. Santelices B, Castilla JC, Cancino J, Schmiede P (1980) Comparative ecology of Lessonia nigrescens and Durvillaea antarctica (Phaeophyta) in Central Chile. Mar Biol 59:119–132CrossRefGoogle Scholar
  51. 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
  52. Steneck RS, Graham MH, Borque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  53. Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689PubMedCrossRefGoogle Scholar
  54. Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Annu Rev Ecol Syst 565–595Google Scholar
  55. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedCrossRefGoogle Scholar
  56. Tala F, Edding M (2005) Growth and loss of distal tissue in blades of Lessonia nigrescens and Lessonia trabeculata (Laminariales). Aquat Bot 82:39–54CrossRefGoogle Scholar
  57. Tala F, Edding M, Vásquez JA (2004) Aspects of the reproductive phenology of Lessonia trabeculata (Laminariales: Phaeophyceae) from three populations in northern Chile. NZ J Mar Freshwat Res 38:255–266CrossRefGoogle Scholar
  58. Tegner MJ, Dayton PK (1987) El Niño effects on southern California kelp forest communities. Adv Ecol Res 17:243–279CrossRefGoogle Scholar
  59. Thiel M, Vásquez JA (2000) Are kelp holdfasts islands on the ocean floor?-indication for temporarily closed aggregations of peracarid crustaceans. Hydrobiologia 440:45–54CrossRefGoogle Scholar
  60. Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536CrossRefGoogle Scholar
  61. Toth G, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434CrossRefGoogle Scholar
  62. Toth G, Karlsson M, Pavia H (2007) Mesoherbivores reduce net growth and induce chemical resistance in natural seaweed populations. Oecologia 152:245–255PubMedCrossRefGoogle Scholar
  63. Underwood N, Anderson K, Inouye BD (2005) Induced vs. constitutive resistance and the spatial distribution of insect herbivores among plants. Ecology 86:594–602CrossRefGoogle Scholar
  64. Uthicke S, Schaffelke B, Byrne M (2009) A boom–bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24CrossRefGoogle Scholar
  65. Vásquez JA (2008) Production, use and fate of Chilean brown seaweeds: re-sources for a sustainable fishery. J Appl Phycol 20:457–467CrossRefGoogle Scholar
  66. Vergés A, Pérez M, Alcoverro T, Romero J (2008) Compensation and resistance to herbivory in seagrasses: induced responses to simulated consumption by fish. Oecologia 155:751–760PubMedCrossRefGoogle Scholar
  67. Whalen MA, Duffy JE, Grace JB (2013) Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94:510–520PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Alistair G. B. Poore
    • 1
    Email author
  • Lars Gutow
    • 2
  • José F. Pantoja
    • 3
  • Fadia Tala
    • 3
    • 4
  • David Jofré Madariaga
    • 3
  • Martin Thiel
    • 3
    • 5
  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Alfred Wegener Institute Helmholtz Centre for Polar and Marine ResearchBremerhavenGermany
  3. 3.Facultad Ciencias del MarUniversidad Católica del NorteCoquimboChile
  4. 4.Centro de Investigación y Desarrollo Tecnológico en Algas (CIDTA-UCN)Universidad Católica del NorteCoquimboChile
  5. 5.Centro de Estudios Avanzados en Zonas Áridas (CEAZA)CoquimboChile

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