Marine Biology

, Volume 162, Issue 12, pp 2521–2526 | Cite as

Do native subtidal grazers eat the invasive kelp Undaria pinnatifida?

  • Rocío Suárez JiménezEmail author
  • Christopher D. Hepburn
  • Glenn A. Hyndes
  • Rebecca J. McLeod
  • Richard B. Taylor
  • Catriona L. Hurd
Invasive Species - Short Note
Part of the following topical collections:
  1. Invasive Species


Key to understanding the impacts of invasive macroalgae on local food webs is determining the extent to which native herbivores consume the invasive macroalga. We used multiple-choice feeding assays to ascertain the relative feeding preferences of four subtidal grazers (the amphipod Aora typica, the isopod Batedotea elongata and the gastropods Cookia sulcata and Haliotis iris) for the invasive macroalga Undaria pinnatifida and six native macroalgae (Macrocystis pyrifera, Durvillaea antarctica, Carpophyllum flexuosum, Cystophora scalaris, Marginariella boryana and Ulva spp.) that are all abundant along the Otago coast of southern New Zealand. Multiple-choice feeding assays were run under laboratory conditions during the austral autumn (April and June) of 2013. The relative abundances of the macroalgae in the field were also determined. All of the grazers ate U. pinnatifida at rates comparable to most of the native macroalgae, except for B. elongata, which barely consumed it. This indicates that U. pinnatifida, which was shown to be more abundant than native macroalgae in subtidal habitats, has the potential to contribute organic matter to the local food web and may be an undesirable food for some group of grazers. We suggest that U. pinnatifida could potentially alter existing trophic relationships.


Macroalgae Macroalgal Species Feeding Assay Macrocystis Pyrifera Native Grazer 
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.



We thank S. Bell, R. Pooley, P. Jones, P. S. Fernández, M. Desmond and B. Flack for field and laboratory assistance. This study was funded by an Otago University Doctoral Scholarship to RSJ, Performance Based Research (PBRF) funding from the Department of Botany, University of Otago to CLH, a Foundation for Research, Science and Technology (FRST) subcontract to CLH from the National Institute of Water and Atmospheric Research Ltd., Biodiversity and Biosecurity OBI (C01X0502) and a FRST Science and Technology Postdoctoral Fellowship to RJM (UOOX0814).


  1. Boudouresque C (1996) The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aquatic Bot 53:245–250CrossRefGoogle Scholar
  2. Cabin RJ, Mitchell RJ (2000) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248Google Scholar
  3. Casas G, Scrosati R, Piriz ML (2004) The invasive kelp Undaria Pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in nuevo Gulf (Patagonia, Argentina). Biol Invasions 6:411–416CrossRefGoogle Scholar
  4. Cebrián E, Ballesteros E, Linares C, Tomas F (2011) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biol Invasions 13:1397–1408CrossRefGoogle Scholar
  5. Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New YorkGoogle Scholar
  6. Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219CrossRefGoogle Scholar
  7. Davis AR, Benkendorff K, Ward DW (2005) Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar Biol 146:859–868CrossRefGoogle Scholar
  8. Deudero S, Box A, Alós J, Arroyo NL, Marbà N (2011) Functional changes due to invasive species: food web shifts at shallow Posidonia oceanica seagrass beds colonized by the alien macroalga Caulerpa racemosa. Estuar Coast Shelf Sci 93:106–116CrossRefGoogle Scholar
  9. Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298CrossRefGoogle Scholar
  10. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263CrossRefGoogle Scholar
  11. Edgar GJ, Moore PG (1986) Macro-algae as habitat for motile macrofauna. Monogr Biol 4:255–277Google Scholar
  12. Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London, p 181CrossRefGoogle Scholar
  13. Floc’h JY, Pajot R, Wallentinus I (1991) The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. J Cons Int Explor Mer 47(47):379–390CrossRefGoogle Scholar
  14. Gollan JR, Wright JT (2006) Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary. Mar Freshw Res 57:685–694CrossRefGoogle Scholar
  15. Gribben PE, Byers JE, Wright JT, Glasby TM (2013) Positive versus negative effects of an invasive ecosystem engineer on different components of a marine ecosystem. Oikos 122:816–824CrossRefGoogle Scholar
  16. Hammann M, Wang G, Rickert E, Boo S, Weinberger F (2013) Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatability. Mar Ecol Progr Ser 486:93–103CrossRefGoogle Scholar
  17. Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbour. NZ J Bot 25:329–332CrossRefGoogle Scholar
  18. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  19. Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the World’s worst invasive alien species A selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN)Google Scholar
  20. Monteiro CA, Engelen AH, Santos ROP (2009) Macro- and mesoherbivores prefer native seaweeds over the invasive brown seaweed Sargassum muticum: a potential regulating role on invasions. Mar Biol 156:2505–2515CrossRefGoogle Scholar
  21. Nejrup LB, Pedersen MF, Vinzent J (2012) Grazer avoidance may explain the invasiveness of the red alga Gracilaria vermiculophylla in Scandinavian waters. Mar Biol 159:1703–1712CrossRefGoogle Scholar
  22. Newcombe EM, Taylor RB (2010) Trophic cascade in a seaweed-epifauna-fish food chain. Mar Ecol Progr Ser 408:161–167CrossRefGoogle Scholar
  23. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  24. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic. Science 311:1459–1461CrossRefGoogle Scholar
  25. Pennings CS, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619CrossRefGoogle Scholar
  26. Pennings SC, Masatomo TN, Paul VJ (1993) Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74:879–890CrossRefGoogle Scholar
  27. Peteiro C, Freire O (2012) Observations on fish grazing of the cultured kelps Undaria pinnatifida and Saccharina latissima (Phaeophycea, Laminariales) in Spanish Atlantic waters. AACL Bioflux 5:189–196Google Scholar
  28. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86CrossRefGoogle Scholar
  29. Piriz ML, Casas G (1994) Occurrence of Undaria pinnatifida in Golfo Nuevo, Argentina. Appl Phycol Forum 10:4Google Scholar
  30. 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 15:912–922CrossRefGoogle Scholar
  31. Raffo MP, Eyras MC, Iribarne OO (2009) The invasion of Undaria pinnatifida to a Macrocystis pyrifera kelp in Patagonia (Argentina, south-west Atlantic). J Mar Biol Assoc UK 89:1571CrossRefGoogle Scholar
  32. Richards DK (2009) Subtidal rocky reef communities of the East Otago Taiapure: community structure, succession and productivity. Master thesis, University of Otago, DunedinGoogle Scholar
  33. Russell LK, Hepburn CD, Hurd CL, Stuart MD (2008) The expanding range of Undaria pinnatifida in southern New Zealand: distribution, dispersal mechanisms and the invasion of wave-exposed environments. Biol Invasions 10:103–115CrossRefGoogle Scholar
  34. Salvaterra T, Green DS, Crowe TP, O’Gorman EJ (2013) Impacts of the invasive alga Sargassum muticum on ecosystem functioning and food web structure. Biol Invasions 15:2563–2576CrossRefGoogle Scholar
  35. Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417CrossRefGoogle Scholar
  36. Scheibling R, Anthony SX (2001) Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides. Mar Biol 139:139–146CrossRefGoogle Scholar
  37. Silva PC, Woodfield RA, Cohen AN, Harris LH, Goddard JHR (2002) First report of the Asian kelp Undaria pinnatifida in the northeastern Pacific Ocean. Biol Invasions 4:333–338CrossRefGoogle Scholar
  38. Suárez RJ (2015) The ecology of the invasive kelp Undaria pinnatifida: functioning at an ecosystem level. Ph.D. thesis, University of Otago, DunedinGoogle Scholar
  39. Suárez RJ, Hepburn CD, Hyndes GA, McLeod RJ, Hurd CL (2015) Contributions of an annual invasive kelp to native algal assemblages: algal resource allocation and seasonal connectivity across ecotones. Phycology 54:530–544CrossRefGoogle Scholar
  40. Sumi CBT, Scheibling RE (2005) Role of grazing by sea urchins Strongylocentrotus droebachiensis in regulating the invasive alga Codium fragile ssp. tomentosoides in Nova Scotia. Mar Ecol Progr Ser 292:203–212CrossRefGoogle Scholar
  41. Taylor RB (1998) Density, biomass and productivity of animals in four subtidal rocky reef habitats: the importance of small mobile invertebrates. Mar Ecol Progr Ser 172:37–51CrossRefGoogle Scholar
  42. Taylor RB, Brown PJ (2006) Herbivory in the gammarid amphipod Aora typica: relationships between consumption rates, performance and abundance across ten seaweed species. Mar Biol 149:455–463CrossRefGoogle Scholar
  43. Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Progr Ser 115:271–282CrossRefGoogle Scholar
  44. Taylor RB, Sotka EE, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76CrossRefGoogle Scholar
  45. Teso VS, Bigatti G, Casas GN, Piriz ML, Penchaszadeh PE (2009) Do native grazers from Patagonia, Argentina, consume the invasive kelp Undaria pinnatifida? Rev Mus Argentino Cienc Nat 11:7–14CrossRefGoogle Scholar
  46. Thornber C, Kinlan B, Graham M, Stachowicz J (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Mar Ecol Progr Ser 268:69–80CrossRefGoogle Scholar
  47. Tomas F, Box A, Terrados J (2011) Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol Invasions 13:1559–1570CrossRefGoogle Scholar
  48. Valentine JP, Johnson CR (2003) Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. J Exp Mar Biol Ecol 295:63–90CrossRefGoogle Scholar
  49. Valentine JP, Johnson CR (2005) Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar Ecol Prog Ser 285:43–55CrossRefGoogle Scholar
  50. Vergés A, Alcoverro T, Ballesteros E (2009) Role of fish herbivory in structuring the vertical distribution of canopy algae Cystoseira spp. in the Mediterranean Sea. Mar Ecol Progr Ser 375:1–11CrossRefGoogle Scholar
  51. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38:327–359CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Rocío Suárez Jiménez
    • 1
    Email author
  • Christopher D. Hepburn
    • 2
  • Glenn A. Hyndes
    • 3
  • Rebecca J. McLeod
    • 4
  • Richard B. Taylor
    • 5
  • Catriona L. Hurd
    • 1
    • 6
  1. 1.Department of BotanyUniversity of OtagoDunedinNew Zealand
  2. 2.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  3. 3.Centre for Marine Ecosystems Research, School of Natural SciencesEdith Cowan UniversityPerthAustralia
  4. 4.Department of ChemistryUniversity of OtagoDunedinNew Zealand
  5. 5.Leigh Marine LaboratoryUniversity of AucklandLeighNew Zealand
  6. 6.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia

Personalised recommendations