Marine Biology

, 166:139 | Cite as

Superior photosynthetic performance of the invasive kelp Undaria pinnatifida may contribute to continued range expansion in a wave-exposed kelp forest community

  • M. J. DesmondEmail author
  • D. W. Pritchard
  • C. L. Hurd
  • D. K. Richards
  • K. Schweikert
  • S. Wing
  • C. D. Hepburn
Original Paper


In New Zealand, the kelp Undaria pinnatifida has colonized nearly all major coastal ports and has spread to colonize diverse habitats over a range of hydrodynamic environments. We report one of the earliest surveys of the distribution of this species in Macrocystis pyrifera dominated kelp forest habitats in New Zealand alongside experiments comparing the photosynthetic physiology of U. pinnatifida to nine native co-occurring macroalgal species. Undaria pinnatifida was identified at four locations that had previously been reported to be uninvaded and was found throughout the depth range of the kelp forest. Highest densities were observed at shallow depths, reflecting the commonly accepted mode of invasion via sheltered rock pools. Photosynthesis versus Irradiance (P vs. E) curves were constructed for 10 dominant brown macroalgal species. Undaria pinnatifida exhibited greater photosynthetic ability than native macroalgae with maximal rates of photosynthesis at least 1.6-times higher than the habitat forming native kelp species Macrocystis pyrifera and Ecklonia radiata and more than 2.5 times higher than eight other native species. The photosynthetic efficiency of U. pinnatifida under low light was at least as high as macroalgae common on deeper sections of surveyed reefs (e.g. M. pyrifera and E. radiata). Collectively, this information shows that U. pinnatifida has superior photosynthetic performance across all ecologically relevant light intensities. Our data show that the photosynthetic physiology of U. pinnatifida is not likely to limit invasion into deeper sections of reef. This trend could continue, with the potential to fundamentally alter the structure of these wave-exposed kelp communities.



We thank April Brown, Rob Win, Stewart Bell and Christopher Cornwall for their support in the field. We also acknowledge the East Otago Taiāpure Committee for their continued support of research in this area.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

227_2019_3593_MOESM1_ESM.pdf (95 kb)
Supplementary material 1 Cluster dendrogram constructed from a Bray–Curtis dissimilarity matrix based on fitted photosynthetic parameters α and Pmax (PDF 94 kb)


  1. Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. In: Gibson RN, Atkinson RJA, Gordon JDM (eds) Oceanogr Mar Biol. CRC Press, London, pp 345–405Google Scholar
  2. Baty F, Ritz C, Charles S, Brutsche M, Flandrois JP, Delignette-Muller ML (2015) A toolbox for nonlinear regression in R: the package nlstools. J Stat Softw 66(5):1–21. CrossRefGoogle Scholar
  3. Brown SN (1999) Dispersal characteristics of the adventive seaweed Undaria pinnatifida in New Zealand. Masters Thesis, University of Otago, Dunedin, New ZealandGoogle Scholar
  4. Campbell SJ, Bité JS, Burridge TR (1999) Seasonal patterns in the photosynthetic capacity, tissue pigment and nutrient content of different developmental stages of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, South-Eastern Australia. Bot Mar 42:231–241.
  5. Casas G, Scrosati R, Luz Piriz M (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invasions 6:411–416. CrossRefGoogle Scholar
  6. Chiswell SM, Rickard GJ (2011) Larval connectivity of harbours via ocean currents: A New Zealand study. Cont Shelf Res 31:1057–1074. CrossRefGoogle Scholar
  7. Connell S (2005) Assembly and maintenance of subtidal habitat heterogeneity: synergistic effects of light penetration and sedimentation. Mar Ecol-Prog Ser 289:53–61. CrossRefGoogle Scholar
  8. Connell S, Russell B, Turner D, Shepherd S, Kildea T, Miller D, Airoldi L, Cheshire A (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol-Prog Ser 360:63–72. CrossRefGoogle Scholar
  9. Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  10. Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol S 34:183–211. CrossRefGoogle Scholar
  11. Dayton P (1985) Ecology of kelp communities. Annu Rev Ecol Evol S 16:215–245. CrossRefGoogle Scholar
  12. Dean PR, Hurd CL (2007) Seasonal growth, erosion rates, and nitrogen and photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in southern New Zealand. J Phycol 43:1138–1148. CrossRefGoogle Scholar
  13. Desmond MJ, Pritchard DW, Hepburn CD (2015) Light limitation within southern New Zealand kelp forest communities. PLoS One 10:1–18. CrossRefGoogle Scholar
  14. Desmond MJ, Pritchard W, Hepburn CD (2017) Light dose versus rate of delivery: implications for macroalgal productivity. Photosynth Res. CrossRefPubMedGoogle Scholar
  15. Desmond MJ, Pajusalu L, Pritchard DW, Stephens TA, Hepburn CD (2019) Whole community estimates of macroalgal pigment concentration within two southern New Zealand kelp forests. J Phycol. CrossRefPubMedGoogle Scholar
  16. Duggins DO, Eckman JE, Sewell AT (1990) Ecology of understory kelp environments. II. Effects of kelps on recruitment of benthic invertebrates. J Exp Mar Biol Ecol 143:27–45. CrossRefGoogle Scholar
  17. Dunton KH, Schell DM (1986) Seasonal carbon budget and growth of Laminaria solidungula in the Alaskan High Arctic. Mar Ecol-Prog Ser 31:57–66CrossRefGoogle Scholar
  18. Edgar GJ, Barrett NS, Morton AJ, Samson CR (2004) Effects of algal canopy clearance on plant, fish and macroinvertebrate communities on eastern Tasmanian reefs. J Exp Mar Biol Ecol 312:67–87. CrossRefGoogle Scholar
  19. Epstein G, Smale DA (2017) Undaria pinnatifida: a case study to highlight challenges in marine invasion ecology and management. Ecol Evol 7:8624–8642CrossRefGoogle Scholar
  20. Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia 39:547–553. CrossRefGoogle Scholar
  21. Fox J, Weisberg S (2011) An R companion to applied regression. Sage, Thousand Oaks CAGoogle Scholar
  22. Funk JL, McDaniel S (2010) Altering light availability to restore invaded forest: the predictive role of plant traits. Restor Ecol 18:865–872. CrossRefGoogle Scholar
  23. Garcia HE, Gordon LI (1992) Oxygen solubility in seawater: Better fitting equations. Limnol Oceanogr 37:1307–1312. CrossRefGoogle Scholar
  24. Gaylord B, Rosman J, Reed DC, Koseff J, Fram J, MacIntyre S, Arkema K, McDonald C, Brzezinski MA, Largier JL, Monismith SG, Raimondi PT, Mardian B (2007) Spatial patterns of flow and their modification within and around a giant kelp forest. Limnol Oceanogr 52:1838–1852CrossRefGoogle Scholar
  25. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194. CrossRefGoogle Scholar
  26. Hay CH, Luckens PA (1987) The Asian kelp Undaria pinnatifida (Phaeophyta: Laminariales) found in a New Zealand harbor. New Zeal J Bot 25:329–332. CrossRefGoogle Scholar
  27. Hay CH, Villouta E (1993) Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Bot Mar 36:461–476.
  28. Henkel SK, Hofmann GE (2008) Thermal ecophysiology of gametophytes cultured from invasive Undaria pinnatifida (Harvey) Suringar in coastal California harbors. J Exp Mar Biol Ecol 367:164–173. CrossRefGoogle Scholar
  29. Hepburn CD, Pritchard DW, Cornwall CE, McLeod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Chang Biol 17:2488–2497. CrossRefGoogle Scholar
  30. Irigoyen AJ, Eyras C, Parma AM (2010) Alien algae Undaria pinnatifida causes habitat loss for rocky reef fishes in north Patagonia. Biol Invas 13:17–24. CrossRefGoogle Scholar
  31. James K, Shears N (2012) Spatial distribution and seasonal variation in Undaria pinnatifida populations around the Coromandel Peninsula. Waikato Regional Council Technical Report 2013/15Google Scholar
  32. Jiménez R, 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. Phycologia 54:530–544. CrossRefGoogle Scholar
  33. Lees D, Heatley P (2009) Introduction of bladder kelp seaweed, Macrocystis pyrifera (KBB), in Fisheries Management Areas 3 and 4 into the Quota Management System on 1 October 2010. Final Position Paper, Ministry of Fisheries, New ZealandGoogle Scholar
  34. Lüning K (1990) Seaweeds: their environment, biogeography, and ecophysiology. Wiley, New YorkGoogle Scholar
  35. Millero FJ, Poisson A (1981) International one-atmosphere equation of state of seawater. Deep Sea Res 28A:625–629CrossRefGoogle Scholar
  36. Nickols K, Gaylord B, Largier J (2012) The coastal boundary layer: predictable current structure decreases alongshore transport and alters scales of dispersal. Mar Ecol-Prog Ser 464:17–35. CrossRefGoogle Scholar
  37. Oh S, Koh C (1996) Growth and Photosynthesis of Undaria pinnatifida (Laminariales, Phaeophyta) on a Cultivation Ground in Korea. Bot Mar 39:389–394.
  38. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: Community Ecology PackageGoogle Scholar
  39. Paerl HW, Piehler MF (2008) Nitrogen and marine eutrophication. In: Capone DG, Bronk DA, Mulholland MR, Carpenter EJ (eds) Nitrogen in the marine environment, 2nd edn. Academic Press, San Diego, pp 529–567CrossRefGoogle Scholar
  40. Pritchard DW, Hurd CL, Beardall J, Hepburn CD (2013) Survival in low light: photosynthesis and growth of a red alga in relation to measured in situ irradiance. J Phycol 49:867–879. CrossRefPubMedGoogle Scholar
  41. Raven JA, Hurd CL (2012) Ecophysiology of photosynthesis in macroalgae. Photosynth Res 113:105–125. CrossRefPubMedGoogle Scholar
  42. Richards DK, Hurd CL, Pritchard DW, Wing SR, Hepburn CD (2011) Photosynthetic response of monospecific macroalgal stands to density. Aquat Biol 13:41–49. CrossRefGoogle Scholar
  43. Rowley RJ (1989) Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes? Mar Biol 100:485–494. CrossRefGoogle Scholar
  44. 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. CrossRefGoogle Scholar
  45. Saito Y (1975) Undaria. In: Tokida J, Hirose H (eds) Advance of phycology in Japan. Dr. W. Junk Publishers, The Hague, pp 304–320Google Scholar
  46. Salinger MJ, Renwick J, Behrens E, Mullan AB, Diamond HJ, Sirguey P, Smith RO, Trought MCT, Alexander L, Cullen NJ, Fitzharris BB, Hepburn CD, Parker AK, Sutton PJ (2019) The unprecedented coupled ocean-atmosphere summer heatwave in the New Zealand region 2017/18: drivers, mechanisms and impacts. Environ Res Lett 14:044023. CrossRefGoogle Scholar
  47. Sanderson JC (1990) A preliminary survey of the distribution of the introduced macroalga, Undaria pinnatifida (Harvey) Suringer on the East Coast of Tasmania, Australia. Bot Mar 33:153–157.
  48. Schiel DR, Thompson GA (2012) Demography and population biology of the invasive kelp Undaria pinnatifida on shallow reefs in southern New Zealand. J Exp Mar Biol Ecol 434–435:25–33. CrossRefGoogle Scholar
  49. Shears NT, Babcock RC (2007) Quantitative description of mainland New Zealand’s shallow subtidal reef communities. Science for Conservation. 280. Department of Conservation, Wellington, New ZealandGoogle Scholar
  50. Siemann E, Rogers WE (2003) Changes in light and nitrogen availability under pioneer trees may indirectly facilitate tree invasions of grasslands. J Ecol 91:923–931. CrossRefGoogle Scholar
  51. 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. CrossRefGoogle Scholar
  52. Steneck R, Dethier M (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69(3):476–498. CrossRefGoogle Scholar
  53. Stuart MD, Hurd CL, Brown MT (1999) Effects of seasonal growth rate on morphological variation of Undaria pinnatifida (Alariaceae, Phaeophyceae). In: Kain JM, Brown MT, Lahaye M (eds) sixteenth international seaweed symposium: proceedings of the sixteenth international seaweed symposium held in Cebu City, Philippines, 12–17 April 1998. Springer, The Netherlands, pp 191–199Google Scholar
  54. Tait LW (2019) Giant kelp forests at critical light thresholds show compromised ecological resilience to environmental and biological drivers. Estuar Coast Shelf SciGoogle Scholar
  55. Tait LW, Schiel DR (2011) Legacy effects of canopy disturbance on ecosystem functioning in macroalgal assemblages. PLoS One 6:e26986. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Thompson G, Schiel D (2012) Resistance and facilitation by native algal communities in the invasion success of Undaria pinnatifida. Mar Ecol-Prog Ser 468:95–105. CrossRefGoogle Scholar
  57. 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. CrossRefGoogle Scholar
  58. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Mar Freshw Res 55:223. CrossRefGoogle Scholar
  59. Wallentinus I (1999) Undaria pinnatifida (Harvey) Suringar. In: Gollasch S, Minchin D, Rosenthal H, Voight M (eds) Case histories on introduced species: their general biology, distribution, range expansion and general impact. Department of Fishery Biology, Institute for Marine Science, University of Kiel, Germany, pp 13–19Google Scholar
  60. Webb WL, Newton M, Starr D (1974) Carbon dioxide exchange of Alnus rubra: a mathematical model. Oecologia 17:281–291CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • M. J. Desmond
    • 1
    Email author
  • D. W. Pritchard
    • 2
    • 4
  • C. L. Hurd
    • 2
    • 3
  • D. K. Richards
    • 2
  • K. Schweikert
    • 2
  • S. Wing
    • 1
  • C. D. Hepburn
    • 1
  1. 1.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  2. 2.Department of BotanyUniversity of OtagoDunedinNew Zealand
  3. 3.Institute for Marine and Antarctic Studies (IMAS)University of TasmaniaHobartAustralia
  4. 4.Te Ao TūroaTe Rūnanga o Ngāi TahuDunedinNew Zealand

Personalised recommendations