Marine Biology

, 164:113 | Cite as

Importance of the invasive macroalga Undaria pinnatifida as trophic subsidy for a beach consumer

  • Rocío Suárez-Jiménez
  • Christopher D. Hepburn
  • Glenn A. Hyndes
  • Rebecca J. McLeod
  • Richard B. Taylor
  • Catriona L. Hurd
Original Paper

Abstract

Food webs on sandy beaches rely heavily on spatial subsidies of macroalgae and other detritus. Invasive macroalgal species are modifying many ecosystems worldwide, so the potential exists for them to alter the quantity and quality of food available to sandy beach consumers. We evaluated the suitability of the invasive kelp Undaria pinnatifida as a food for the talitrid amphipod Bellorchestia quoyana, an abundant consumer on sandy beaches in southern New Zealand. U. pinnatifida had similar gross nutritional and biomechanical properties to the three native macroalgal species (the kelps Macrocystis pyrifera and Durvillaea antarctica, and the green Ulva spp.). B. quoyana consumed U. pinnatifida at similar or higher rates than the native kelps in laboratory feeding assays (choice and no-choice assays with fresh tissues, and choice assays with tissue reconstituted into agar foods to remove structural properties). Our results indicate that U. pinnatifida is a usable alternative food source for B. quoyana and could, therefore, contribute to the local sandy beach food web. Understanding the role that invasive macroalgae play as a food source for beach consumers is essential to better comprehend how they may affect these subsidy-dependent ecosystems.

References

  1. Adin R, Riera P (2003) Preferential food source utilization among stranded macroalgae by Talitrus saltator (Amphipod, Talitridae): a stable isotopes study in the northern coast of Brittany (France). Estuar Coast Shelf Sci 56:91–98CrossRefGoogle 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. Catenazzi A, Donnelly M (2007) Role of supratidal invertebrates in the decomposition of beach-cast green algae Ulva spp. Mar Ecol Prog Ser 349:33–42CrossRefGoogle Scholar
  4. Conover WJ (1980) Practical nonparametric statistics, 2nd edn. Wiley, New YorkGoogle Scholar
  5. Cowles A, Hewitt JE, Taylor RB (2009) Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats. Mar Ecol Prog Ser 384:175–185CrossRefGoogle Scholar
  6. Crawley KR, Hyndes GA (2007) The role of different types of detached macrophytes in the food and habitat choice of a surf-zone inhabiting amphipod. Mar Biol 151:1433–1443CrossRefGoogle Scholar
  7. Crawley KR, Hyndes GA, Vanderklift MA, Revill AT, Nichols PD (2009) Allochthonous brown algae are the primary food source for consumers in a temperate, coastal environment. Mar Ecol Prog Ser 376:33–44CrossRefGoogle Scholar
  8. Cronin G, Hay ME (1996) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531–1543CrossRefGoogle Scholar
  9. Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219CrossRefGoogle Scholar
  10. Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114CrossRefGoogle Scholar
  11. Duarte C, Jaramillo E, Contreras H (2008) Macroalgas varadas sobre la superficie de una playa arenosa del sur de Chile: preferencias alimentarias y de habitat de juveniles y adultos de Orchestoidea tuberculata (Nicolet), (Amphipoda, Talitridae). Rev Chil His Nat 81:69–81Google Scholar
  12. Duarte C, Navarro JM, Acuña K, Gómez I (2010) Feeding preferences of the sandhopper Orchestoidea tuberculata: the importance of algal traits. Hydrobiologia 651:291–303CrossRefGoogle Scholar
  13. Duarte C, Acuña K, Navarro JM, Gómez I (2011) Intra-plant differences in seaweed nutritional quality and chemical defenses: importance for the feeding behavior of the intertidal amphipod Orchestoidea tuberculata. J Sea Res 66:215–221CrossRefGoogle Scholar
  14. Duarte C, Acuña K, Navarro JM, Gómez I, Jaramillo E, Quijón P (2014) Variable feeding behavior in Orchestoidea tuberculata (Nicolet 1849): exploring the relative importance of macroalgal traits. J Sea Res 87:1–7CrossRefGoogle Scholar
  15. Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298CrossRefGoogle Scholar
  16. Duffy JE, Paul VJ (1992) Prey nutritional quality and effectiveness of chemical defenses against tropical reef fishes. Oecologia 90:333–339CrossRefGoogle Scholar
  17. Dugan JE, Hubbard DM, McCrary MD, Pierson MO (2003) The response of macrofauna communities and shorebirds to macrophyte wrack subsidies on exposed sandy beaches of southern California. Estuar Coast Shelf Sci 58:25–40CrossRefGoogle Scholar
  18. Duggins DO, Eckman JE (1997) Is kelp detritus a good food for suspension feeders? Effects of kelp species, age and secondary metabolites. Mar Biol 128:489–495CrossRefGoogle Scholar
  19. 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 Mar Sci 47:379–390Google Scholar
  20. Griffiths CL, Stenton-Dozey JME, Koop K (1983) Kelp wrack and the flow of energy through a sandy beach ecosystem. In: McLachlan A, Erasmus T (eds) Sandy beaches as ecosystems. Junk, The Hague, pp 547–556CrossRefGoogle Scholar
  21. Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbour. N Z J Bot 25:329–332CrossRefGoogle Scholar
  22. Hay C, Villouta E (1993) Seasonality of Undaria pinnatifida in New Zealand. Bot Mar 36:461–476CrossRefGoogle Scholar
  23. Hay ME, Duffy JE, Pfister CA, Fenical W (1987) Chemical defense against different marine herbivores: are amphipods insect equivalents? Ecology 68:1567–1580CrossRefGoogle Scholar
  24. Hyndes GA, Nagelkerken I, McLeod RJ, Connolly RM, Lavery PS, Vanderklift MA (2014) Mechanisms and ecological role of carbon transfer within coastal seascapes. Biol Rev 89:232–254CrossRefGoogle Scholar
  25. Ince R, Hyndes G, Lavery P, Vanderklift M (2007) Marine macrophytes directly enhance abundances of sandy beach fauna through provision of food and habitat. Estuar Coast Shelf Sci 74:77–86CrossRefGoogle Scholar
  26. Jiménez RS, Hepburn CD, Hyndes GA, McLeod RJ, Hurd CL (2015a) Contributions of an annual invasive kelp to native algal assemblages: algal resource allocation and seasonal connectivity across ecotones. Phycologia 54:530–544CrossRefGoogle Scholar
  27. Jiménez RS, Hepburn CD, Hyndes GA, McLeod RJ, Hurd CL (2015b) Do native subtidal grazers eat the invasive kelp Undaria pinnatifida? Mar Biol 54:530–544Google Scholar
  28. Johnston M, Johnston D, Richardson A (2005) Digestive capabilities reflect the major food sources in three species of talitrid amphipods. Comp Biochem Phys B 140:251–257CrossRefGoogle Scholar
  29. Krumhansl K, Scheibling R (2012a) Production and fate of kelp detritus. Mar Ecol Prog Ser 467:281–302CrossRefGoogle Scholar
  30. Krumhansl K, Scheibling R (2012b) Detrital subsidy from subtidal kelp beds is altered by the invasive green alga Codium fragile ssp. fragile. Mar Ecol Prog Ser 456:73–85CrossRefGoogle Scholar
  31. Lastra M, Page HM, Dugan JE, Hubbard DM, Rodil IF (2008) Processing of allochthonous macrophyte subsidies by sandy beach consumers: estimates of feeding rates and impacts on food resources. Mar Biol 154:163–174CrossRefGoogle Scholar
  32. Lastra M, Rodil IF, Sánchez-Mata A, García-Gallego M, Mora J (2014) Fate and processing of macroalgal wrack subsidies in beaches of Deception Island, Antarctic Peninsula. J Sea Res 88:1–10CrossRefGoogle Scholar
  33. Lewis SM, Norris JN, Searles RB (1987) The regulation of morphological plasticity in tropical reef algae by herbivory. Ecology 68:636–641CrossRefGoogle Scholar
  34. Marsden ID (1991a) Kelp-sandhopper interactions on a sand beach in New Zealand. II. Population dynamics of Talorchestia quoyana (Milne-Edwards). J Exp Mar Biol Ecol 152:75–90CrossRefGoogle Scholar
  35. Marsden ID (1991b) Kelp-sandhopper interactions on a sand beach in New Zealand. I. Drift composition and distribution. J Exp Mar Biol Ecol 152:61–74CrossRefGoogle Scholar
  36. Martone PT, Denny MW (2008) To break a coralline: mechanical constraints on the size and survival of a wave-swept seaweed. J Exp Biol 211:3433–3441CrossRefGoogle Scholar
  37. Mayakun J, Kim JH, Lapointe BE, Prathep A (2013) Effects of nutrient enrichment and herbivory on morphology, reproduction and chemical content of Turbinaria conoides (Phaeophyceae). Phycol Res 61:270–276CrossRefGoogle Scholar
  38. Mellbrand K, Lavery PS, Hyndes G, Hambäck PA (2011) Linking land and sea: different pathways for marine subsidies. Ecosystems 14:732–744CrossRefGoogle Scholar
  39. 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
  40. Moore PG, Macalister HE, Taylor AC (1995) The environmental tolerances and behavioural ecology of the sub-Antarctic beach-hopper “Orchestiascutigerda Dana (Crustacea: Amphipoda) from Husvik, South Georgia. J Exp Mar Biol Ecol 189:159–182CrossRefGoogle Scholar
  41. Olabarria C, Incera M, Garrido J, Rodil IF, Rossi F (2009) Intraspecific diet shift in Talitrus saltator inhabiting exposed sandy beaches. Estuar Coast Shelf Sci 84:282–288CrossRefGoogle Scholar
  42. Olabarria C, Incera M, Garrido J, Rossi F (2010) The effect of wrack composition and diversity on macrofaunal assemblages in intertidal marine sediments. J Exp Mar Bio Ecol 396:18–26CrossRefGoogle Scholar
  43. Parker JD, Hay ME (2005) Biotic resistance to plant invasions? Native herbivores prefer non-native plants. Ecol Lett 8:959–967CrossRefGoogle Scholar
  44. Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic herbivores on plant invasions. Science 311:1459–1461CrossRefGoogle Scholar
  45. Pennings CS, Paul VJ (1992) Effect of plant toughness, calcification, and chemistry on herbivory by Dolabella auricularia. Ecology 73:1606–1619CrossRefGoogle Scholar
  46. Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86CrossRefGoogle Scholar
  47. Piovia-Scott J, Spiller DA, Schoener TW (2011) Effects of experimental seaweed deposition on lizard and ant predation in an island food web. Science 331:461–463CrossRefGoogle Scholar
  48. Piriz ML, Eyras MC, Rostagno CM (2003) Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia. J Appl Phycol 15:67–74CrossRefGoogle Scholar
  49. Poore AGB, Gallagher KM (2013) Strong consequences of diet choice in a talitrid amphipod consuming seagrass and algal wrack. Hydrobiologia 701:117–127CrossRefGoogle Scholar
  50. Prince JS, LeBlanc WG, Maciá S (2004) Design and analysis of multiple choice feeding preference data. Oecologia 138:1–4CrossRefGoogle Scholar
  51. Rodil IF, Olabarria C, Lastra M, López J (2008) Differential effects of native and invasive algal wrack on macrofaunal assemblages inhabiting exposed sandy beaches. J Exp Mar Biol Ecol 358:1–13CrossRefGoogle Scholar
  52. Rossi F, Olabarria C, Incera M, Garrido J (2010) The trophic significance of the invasive seaweed Sargassum muticum in sandy beaches. J Sea Res 63:52–61CrossRefGoogle Scholar
  53. 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 Invasion 10:103–115CrossRefGoogle Scholar
  54. 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
  55. Spiller DA, Piovia-Scott J, Wright AN, Yang LH, Takimoto G, Schoener TW, Iwata T (2010) Marine subsidies have multiple effects on coastal food webs. Ecology 91:1424–1434CrossRefGoogle Scholar
  56. Steinberg PD (1988) Effects of quantitative and qualitative variation in phenolic compounds on feeding in three species of marine invertebrate herbivores. J Exp Mar Biol Ecol 120:221–237CrossRefGoogle Scholar
  57. Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222CrossRefGoogle Scholar
  58. Stenton-Dozey JME, Griffiths CL (1983) The fauna associated with kelp stranded on a sandy beach. In: McLachlan A, Erasmus T (eds) Sandy beaches as ecosystems. Junk, The Hague, pp 557–568CrossRefGoogle Scholar
  59. 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
  60. 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
  61. Taylor RB, Sotka E, Hay ME (2002) Tissue-specific induction of herbivore resistance: seaweed response to amphipod grazing. Oecologia 132:68–76CrossRefGoogle Scholar
  62. Tomas F, Box A, Terrados J (2011) Effects of invasive seaweeds on feeding preference and performance of a keystone Mediterranean herbivore. Biol Inv 13:1559–1570CrossRefGoogle Scholar
  63. Williams SL, Smith JE (2007) A global review of the distribution, taxonomy, and impacts of introduced seaweeds. Annu Rev Ecol Evol Syst 38:327–359CrossRefGoogle Scholar
  64. Wright AN, Piovia-Scott J, Spiller DA, Takimoto G, Hang LH, Schoener TW (2013) Pulses of marine subsidies amplify reproductive potential of lizards by increasing individual growth rate. Oikos 122:1496–1504Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Rocío Suárez-Jiménez
    • 1
  • Christopher D. Hepburn
    • 2
  • Glenn A. Hyndes
    • 3
  • Rebecca J. McLeod
    • 4
  • Richard B. Taylor
    • 5
  • Catriona L. Hurd
    • 1
    • 6
  1. 1.Botany DepartmentUniversity of OtagoDunedinNew Zealand
  2. 2.Marine Science DepartmentUniversity of OtagoDunedinNew Zealand
  3. 3.Centre for Marine Ecosystems Research, School of Natural ScienceEdith Cowan UniversityJoondalupAustralia
  4. 4.Chemistry DepartmentUniversity of OtagoDunedinNew Zealand
  5. 5.Leigh Marine Laboratory and Institute of Marine ScienceUniversity of AucklandLeighNew Zealand
  6. 6.Institute for Marine and Antarctic StudiesUniversity of TasmaniaHobartAustralia

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