Skip to main content
Log in

Do native subtidal grazers eat the invasive kelp Undaria pinnatifida?

  • Invasive Species - Short Note
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

References

  • Boudouresque C (1996) The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aquatic Bot 53:245–250

    Article  Google Scholar 

  • Cabin RJ, Mitchell RJ (2000) To Bonferroni or not to Bonferroni: when and how are the questions. Bull Ecol Soc Am 81:246–248

    Google Scholar 

  • 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 6:411–416

    Article  Google Scholar 

  • Cebrián E, Ballesteros E, Linares C, Tomas F (2011) Do native herbivores provide resistance to Mediterranean marine bioinvasions? A seaweed example. Biol Invasions 13:1397–1408

    Article  Google Scholar 

  • Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New York

    Google Scholar 

  • Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219

    Article  Google Scholar 

  • Davis AR, Benkendorff K, Ward DW (2005) Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp. Mar Biol 146:859–868

    Article  Google Scholar 

  • 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 93:106–116

    Article  CAS  Google Scholar 

  • Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298

    Article  Google Scholar 

  • Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263

    Article  Google Scholar 

  • Edgar GJ, Moore PG (1986) Macro-algae as habitat for motile macrofauna. Monogr Biol 4:255–277

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London, p 181

    Book  Google Scholar 

  • 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):379–390

    Article  Google Scholar 

  • 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 57:685–694

    Article  Google Scholar 

  • 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 122:816–824

    Article  Google Scholar 

  • 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 486:93–103

    Article  Google Scholar 

  • Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbour. NZ J Bot 25:329–332

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • 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)

  • 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 156:2505–2515

    Article  Google Scholar 

  • Nejrup LB, Pedersen MF, Vinzent J (2012) Grazer avoidance may explain the invasiveness of the red alga Gracilaria vermiculophylla in Scandinavian waters. Mar Biol 159:1703–1712

    Article  Google Scholar 

  • Newcombe EM, Taylor RB (2010) Trophic cascade in a seaweed-epifauna-fish food chain. Mar Ecol Progr Ser 408:161–167

    Article  Google Scholar 

  • Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967

    Article  Google Scholar 

  • Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic. Science 311:1459–1461

    Article  CAS  Google Scholar 

  • Pennings CS, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619

    Article  Google Scholar 

  • Pennings SC, Masatomo TN, Paul VJ (1993) Selectivity and growth of the generalist herbivore Dolabella auricularia feeding upon complementary resources. Ecology 74:879–890

    Article  Google Scholar 

  • 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 5:189–196

    Google Scholar 

  • Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86

    Article  CAS  Google Scholar 

  • Piriz ML, Casas G (1994) Occurrence of Undaria pinnatifida in Golfo Nuevo, Argentina. Appl Phycol Forum 10:4

    Google Scholar 

  • 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 15:912–922

    Article  Google Scholar 

  • 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 89:1571

    Article  Google Scholar 

  • Richards DK (2009) Subtidal rocky reef communities of the East Otago Taiapure: community structure, succession and productivity. Master thesis, University of Otago, Dunedin

  • 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 10:103–115

    Article  Google Scholar 

  • 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 15:2563–2576

    Article  Google Scholar 

  • Schaffelke B, Hewitt CL (2007) Impacts of introduced seaweeds. Bot Mar 50:397–417

    Article  Google Scholar 

  • 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 139:139–146

    Article  Google Scholar 

  • 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 4:333–338

    Article  Google Scholar 

  • Suárez RJ (2015) The ecology of the invasive kelp Undaria pinnatifida: functioning at an ecosystem level. Ph.D. thesis, University of Otago, Dunedin

  • 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 54:530–544

    Article  Google Scholar 

  • 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 292:203–212

    Article  Google Scholar 

  • 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 172:37–51

    Article  Google Scholar 

  • 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 149:455–463

    Article  Google Scholar 

  • Taylor RB, Cole RG (1994) Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar Ecol Progr Ser 115:271–282

    Article  Google Scholar 

  • Taylor RB, Sotka EE, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76

    Article  Google Scholar 

  • 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 11:7–14

    Article  Google Scholar 

  • 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 268:69–80

    Article  Google Scholar 

  • Tomas F, Box A, Terrados J (2011) Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol Invasions 13:1559–1570

    Article  Google Scholar 

  • 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 295:63–90

    Article  Google Scholar 

  • Valentine JP, Johnson CR (2005) Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar Ecol Prog Ser 285:43–55

    Article  Google Scholar 

  • 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 375:1–11

    Article  Google Scholar 

  • Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Ann Rev Ecol Syst 38:327–359

    Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rocío Suárez Jiménez.

Additional information

Responsible Editor: F. Bulleri.

Reviewed by undisclosed experts.

This article is part of the Topical Collection on Invasive Species.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jiménez, R.S., Hepburn, C.D., Hyndes, G.A. et al. Do native subtidal grazers eat the invasive kelp Undaria pinnatifida?. Mar Biol 162, 2521–2526 (2015). https://doi.org/10.1007/s00227-015-2757-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-015-2757-y

Keywords

Navigation