Skip to main content
SpringerLink
Log in

Population ecology of the invasive kelp Undaria pinnatifida towards the upper extreme of its temperature range

  • Invasive Species - Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Understanding how the growth and life cycle of an invasive species relate to temperature is fundamental to predicting potential distribution and impacts. This paper investigates how the population ecology of the invasive kelp Undaria pinnatifida relates to water temperature in the warm-temperate waters of north-eastern New Zealand, one of the warmest water populations in the world and a region previously thought to be suboptimal for U. pinnatifida colonisation. Monitoring of U. pinnatifida on artificial structures over three growth seasons revealed an annual growth cycle, with one main recruitment event in winter ~2 months after water temperatures dropped below ~15 °C. Sporophyte growth rates peaked in late winter, density and sporophyte length peaked in spring and declined rapidly in summer. Density was strongly negatively related to water temperatures 8 weeks prior to sampling, whereas relative change in density was most strongly related to water temperature on the day of sampling, with largest declines when temperatures exceeded 20 °C. Densities remained low for varying periods depending on how long temperatures remained above 20 °C. Overall, sporophyte size and growth rates were comparable to those of cooler water populations, but the seasonal cycle was compressed into a shorter period when temperatures were cool enough for recruitment and growth. In warm-temperate and subtropical regions summer temperatures limit the seasonal presence while winter temperatures will ultimately determine the distribution of U. pinnatifida. The strong coupling between U. pinnatifida density and water temperature provides a basis for predicting the future distribution and related impacts of this species under changing climatic conditions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aguilar-Rosas R, Galindo AM (1990) Ecological aspects of Sargassum muticum (Fucales, Phaeophyta) in Baja California, Mexico: reproductive phenology and epiphytes. In: Thirteenth international seaweed symposium. Springer Netherlands, pp 185–190

  • Aguilar-Rosas R, Aguilar-Rosas LE, Avila-Serrano G, Marcos-Ramirez R (2004) First record of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta) on the Pacific coast of Mexico. Bot Mar 47:255–258

    Article  Google Scholar 

  • Britton-Simmons KH (2004) Direct and indirect effects of the introduced alga Sargassum muticum on benthic, subtidal communities of Washington State, USA. Mar Ecol Prog Ser 277(6):61–78

    Article  Google Scholar 

  • Campbell SJ, Burridge TR (1998) Occurrence of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, Victoria, Australia. Mar Freshw Res 49(5):379–381

    Article  Google Scholar 

  • Campbell SJ, Bite JS, Burridge TR (1999) Seasonal patterns in photosynthetic capacity, tissue pigment and nutrient content developmental stages of Undaria pinnatifida (Phaeophyta: Laminariales) in Port Phillip Bay, South Eastern Australia. Bot Mar 42:231–241

    Article  CAS  Google Scholar 

  • Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologica 326(327):213–215

    Article  Google Scholar 

  • Casas GN, Piriz ML, Parodi ER (2008) Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). J Mar Biol Assoc UK 88(1):21–28

    Article  Google Scholar 

  • Castic-Fey A, Beaupoil C, Bouchain J, Pradier E, L’Hardy-Halos MT (1999) The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the rocky shore ecosystem of the St Malo area: growth rate and longevity of the sporophyte. Bot Mar 42:83–96

    Google Scholar 

  • Cecere E, Petrocelli A, Saracino OD (2000) Undaria pinnatifida (Fucophyceae, Laminariales) spread in the central Mediterranean: its occurrence in the Mar Piccolo of Taranto (Ionian Sea, southern Italy). Cryptogam Algol 21:305–309

    Article  Google Scholar 

  • Choi HG, Kim YS, Lee SJ, Nam KW (2007) Growth and reproductive patterns of Undaria pinnatifida sporophytes in a cultivation farm in Busan, Korea. J Appl Phycol 19:131–138

    Article  Google Scholar 

  • Curiel D, Guidetti P, Bellemo G, Scattolin M, Marzocchi M (2001) The introduced alga Undaria pinnatifida (Laminariales, Alariaceae) in the Lagoon of Venice. Hydrobiologica 477:209–219

    Article  Google Scholar 

  • Dean PR, Hurd CL (2007) Seasonal growth, erosion rates, and nitrogen and photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in southern New Zealand. J Phycol 46:1138–1148

    Article  Google Scholar 

  • Dieck I (1993) Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta): ecological and biogeographical implications. Mar Ecol Prog Ser 100:253–264

    Article  Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139

    Article  Google Scholar 

  • Fletcher RL, Farrell P (1999) Introduced brown algae in the northeast Atlantic, with particular respect to Undaria pinnatifida (Harvey) Suringar. Helgol Meeresunters 52:259–275

    Article  Google Scholar 

  • Floc’h YL, Pajot R, Wallentinus I (1991) The Japanese brown alga Undaria pinnatifida on the coast of France and its possible establishment in European waters. Conseil International pour l’Exploration de la Mer 47:379–390

    Article  Google Scholar 

  • Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia 39(6):547–553

    Article  Google Scholar 

  • Gerard VA, Du Bois KR (1988) Temperature ecotypes near the southern boundary of the kelp Laminaria saccharina. Mar Biol 97(4):575–580

    Article  Google Scholar 

  • Hatcher BG, Kirkman H, Wood WF (1987) Growth of the kelp Ecklonia radiata near the northern limit of its range in Western Australia. Mar Biol 95(1):63–73

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hay CH, Villouta E (1993) Seasonality of the adventive Asian kelp Undaria pinnatifida in New Zealand. Bot Mar 36:461–476

    Article  Google Scholar 

  • Hellmann JJ, Byers JE, Bierwagen BG, Dukes JS (2008) Five potential consequences of climate change for invasive species. Conserv Biol 22(3):534–543

    Article  Google Scholar 

  • Hewitt CL, Campbell ML, McEnnulty F, Moore KM, Murfet NB, Robertson B et al (2005) Efficacy of physical removal of a marine pest: the introduced kelp Undaria pinnatifida in a Tasmanian marine reserve. Biol Invasions 7:251–263

    Article  Google Scholar 

  • Hue JS, Gong YG, Lee DY, Nam KW (1995) Studies on the free living culture of gametophytes of Undaria pinnatifida. Bull Natl Fish Res Dev Agency 49:197–217

    Google Scholar 

  • James K, Shears NT (2016) Proliferation of the invasive kelp Undaria pinnatifida at aquaculture sites promotes spread to coastal reefs. Mar Biol 163(2):1–12

    Article  Google Scholar 

  • James K, Middleton I, Middleton C, Shears NT (2014) Discovery of Undaria pinnatifida (Harvey) Suringar, 1873 in northern New Zealand indicates increased invasion threat in subtropical regions. BioInvasions Rec 3(1):21–24

    Article  Google Scholar 

  • James K, Kibele J, Shears NT (2015) Using satellite-derived sea surface temperature to predict the potential global range and phenology of the invasive kelp Undaria pinnatifida. Biol Invasions 17(12):3393–3408

    Article  Google Scholar 

  • Johnson C (ed) (2008) Seaweed invasions: a synthesis of ecological, economic and legal imperatives. Walter de Gruyter, New York

    Google Scholar 

  • Kain JM (1979) A view of the genus Laminaria. Oceanogr Mar Biol Ann Rev 17:101–161

    Google Scholar 

  • Koh CH, Shin HC (1990) Growth and size distribution of some large brown algae in Ohori, east coast of Korea. Hydrobiologica 204(205):225–231

    Article  Google Scholar 

  • Kohtio D (2008) Population biology of Undaria pinnatifida in central California. Unpublished Master’s Thesis (Paper 3565), San Jose State University, California

  • Ladah LB, Zertuche-González JA, Hernández-Carmona G (1999) Giant kelp (Macrocystis pyrifera, Phaeophyceae) recruitment near its southern limit in Baja California after mass disappearance during ENSO 1997–1998. J Phycol 35(6):1106–1112

    Article  Google Scholar 

  • Lee JA, Brinkhuis BH (1986) Reproductive phenology of Laminaria saccharina Lamour (Phaeophyta) at the southern limit of its distribution in the northwestern Atlantic Ocean. J Phycol 22:276–285

    Article  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2007) Invasion ecology. Blackwell, Oxford

    Google Scholar 

  • Lüning K (1980) Critical levels of light and temperature regulating the gametogenesis of three Laminaria species (Phaeophyceae). J Phycol 16:1–15

    Article  Google Scholar 

  • Lüning K, Neushul M (1978) Light and temperature demands for growth and reproduction of laminarian gametophytes in southern and central California. Mar Biol 45:297–309

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10(3):689–710

    Article  Google Scholar 

  • Martin JP, Bastida R (2008) El alga invasora Undaria pinnatifida (Harvey) Suringar en la Ría Deseado (Patagonia austral, Argentina): ciclo del esporofito y factores ambientales determinantes de su distribución. Rev Biol Mar Oceangr 43(2):335–344

    Google Scholar 

  • Meretta PE, Matula CV, Casas G (2012) Occurrence of the alien kelp Undaria pinnatifida (Laminariales, Phaeophyceae) in Mar del Plata, Argentina. BioInvasions Rec 1(1):59–63

    Article  Google Scholar 

  • Minchin D, Nunn J (2014) The invasive brown alga Undaria pinnatifida (Harvey) Suringar, 1873 (Laminariales: Alariaceae), spreads northwards in Europe. BioInvasions Rec 3(2):57–63

    Article  Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6(9):485–492

    Article  Google Scholar 

  • Morelisson B, Dudley BD, Geange SW, Phillips NE (2013) Gametophyte reproduction and development of Undaria pinnatifida under varied nutrient and irradiance conditions. J Exp Mar Biol Ecol 448:197–206

    Article  Google Scholar 

  • Morita T, Kurashima A, Maegawa M (2003a) Temperature requirements for the growth and maturation of the gametophytes of Undaria pinnatifida and U. undarioides (Laminariales, Phaeophyceae). Phycol Res 51(3):154–160

    Google Scholar 

  • Morita T, Kurashima A, Maegawa M (2003b) Temperature requirements for the growth of young sporophytes of Undaria pinnatifida and U. undarioides (Laminariales, Phaeophyceae). Phycol Res 51:266–270

    Article  Google Scholar 

  • Nelson W (2013) New Zealand seaweeds: an illustrated guide. Te Papa Press, Wellington

    Google Scholar 

  • Nyberg CD, Wallentinus I (2005) Can species traits be used to predict marine macroalgal introductions? Biol Invasions 7(2):265–279

    Article  Google Scholar 

  • Oh SH, Koh CH (1996) Growth and photosynthesis of Undaria pinnatifida (Laminariales, Phaeophyta) on a cultivation ground in Korea. Bot Mar 39:389–393

    Article  CAS  Google Scholar 

  • Pang SJ, Shan TF, Zhang ZH (2008) Responses of vegetative gametophytes of Undaria pinnatifida to high irradiance in the process of gametogenesis. Phycol Res 56:280–287

    Article  Google Scholar 

  • Parke M (1948) Studies of British Laminariaceae. I. Growth in Laminaria saccharina (L.) Lamour. J Mar Biol Assoc UK 27:651–709

    Article  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • 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 

  • Saito Y (1975) Undaria. In: Tokida J, Hirose H (eds) Advance in phycology in Japan. W. Junk, The Hague, pp 304–320

    Google Scholar 

  • Sanderson JC (1990) A preliminary survey of the distribution of the introduced macroalga, Undaria pinnatifida (Harvey) Suringar on the east coast of Tasmania, Australia. Bot Mar 33:153–157

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schiel DR, Steinbeck JR, Foster MS (2005) Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. Ecology 85:1833–1839

    Article  Google Scholar 

  • Sfrisco A, Facca C (2013) Annual growth and environmental relationships of the invasive species Sargassum muticum and Undaria pinnatifida in the lagoon of Venice. Estuar Coast Shelf Sci 129:162–172

    Article  Google Scholar 

  • Sharples J (1997) Cross-shelf intrusion of subtropical water into the coastal zone of northeast New Zealand. Cont Shelf Res 17(7):835–857

    Article  Google Scholar 

  • Shibneva SY, Skriptsova AV, Shan TF, Pang SJ (2013) The different morphs of Undaria pinnatifida (Phaeophyceae, Laminariales) in Peter the Great Bay (Sea of Japan) are phenotypic variants: direct evidence. J Appl phycol 25(6):1909–1916

    Article  Google Scholar 

  • Simberloff D (2013) Invasive species: what everyone needs to know. Oxford University Press, New York (Kindle Edition)

    Google Scholar 

  • Sinner J, Forrest B, Taylor M (2000) A strategy for managing the Asian kelp Undaria: Final report. (Cawthron Report No. 578). Nelson, New Zealand: Prepared for the Ministry of Fisheries

  • South PM, Lilley SA, Tait LW, Alestra T, Hickford MJH, Thomsen MS, Schiel DR (2015) Transient effects of an invasive kelp on the community structure and primary productivity of an intertidal assemblage. Mar Freshw Res. doi:10.1071/MF14211

    Google Scholar 

  • Stuart M (1997) The seasonal ecophysiology of Undaria pinnatifida (Harvey) Suringar in Otago Harbour, New Zealand. Unpublished Ph.D. Thesis, University of Otago

  • Thornber CS, Kinlan BP, Graham MH, Stachowicz JJ (2004) Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography. Mar Ecol Prog Ser 268:69–80

    Article  Google Scholar 

  • Torres AI, Gil MN, Esteves JL (2004) Nutrient uptake rates by the alien alga Undaria pinnatifida (Phaeophyta) (Nuevo Gulf, Patagonia, Argentina) when exposed to diluted sewage effluent. Hydrobiologia 520(1–3):1–6

    Article  CAS  Google Scholar 

  • Uwai S, Nelson W, Neill K, Wang WD, Aquilar-Rosas LE, Boo SM, Kitayama T, Kawai H (2006) Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes—origins and succession of introduced populations. Phycologia 45(6):687–695

    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 

  • Verlaque M (2007) Ecology of Undaria pinnatifida. www.issg.org/database/species/ecology.asp?si=68andfr=1andsts=sss. Accessed 26 Apr 2015

  • Voisin M (2007) Le processus d’invasions biologiques en milieu cˆotier marin: le cas de l’algue brune Undaria pinnatifida, cultiv´ee et introduite `a l’´echelle mondiale. Ph.D. Thesis, L’Universit´e Pierre et Marie Curie

  • Watanabe Y, Nishihara GN, Tokunaga S, Terada R (2014) The effect of irradiance and temperature responses and the phenology of a native alga, Undaria pinnatifida (Laminariales), at the southern limit of its natural distribution in Japan. J Appl Phycol 26(6):2405–2415

    Article  CAS  Google Scholar 

  • Wernberg T, Thomsen MS, Tuya F, Kendrick GA, Staehr PA, Toohey BD (2010) Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecol Lett 13(6):685–694

    Article  Google Scholar 

  • Yoshikawa T, Takeuchi I, Furuya K (2001) Active erosion of Undaria pinnatifida Suringar (Laminariales, Phaeophyceae) mass-cultured in Otsuchi Bay in northeastern Japan. J Exp Mar Biol Ecol 266(1):51–65

    Article  Google Scholar 

  • Zabin CJ, Ashton GV, Brown CW, Ruiz GM (2009) Northern range expansion of the Asian kelp Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyceae) in western North America. Aquat Invasions 4(3):429–434

    Article  Google Scholar 

  • Zhang Z, Pang S (2007) Circadian rhythms in the growth and reproduction of the brown alga Undaria pinnatifida and gametogenesis under different photoperiods. Acta Oceanol Sin 26(4):104–111

    CAS  Google Scholar 

  • Zhang DM, Miao GR, Pei LO (1984) Studies on Undaria pinnatifida. Hydrobiologia 116(117):263–265

    Google Scholar 

Download references

Acknowledgments

Thank you to the management at Westhaven Marina for providing access to the marina and allowing the installation of research equipment. Thank you to Auckland Council and Waikato Regional Council for helping to fund this research and to everyone who helped with fieldwork including G. Braidwood, O. Brine, I. James, B. Patel, I. Ruza, B. Seers, L. Jones, E. Duder, J. James, N. White and K. Kenyon. Thank you to A. Rees for comments on the manuscript and to the anonymous reviewers of this manuscript.

Author information

Authors and Affiliations

  1. Institute of Marine Science, University of Auckland, Private Bag 92019, Auckland, New Zealand

    Kate James

  2. Leigh Marine Laboratory, Institute of Marine Science, University of Auckland, Box 349, Warkworth, Northland, New Zealand

    Nick T. Shears

Authors
  1. Kate James
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nick T. Shears
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kate James.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Human or animal rights

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Responsible Editor: K. Bischof.

Reviewed by undisclosed experts.

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

Appendix

Appendix

See Fig. 9.

Fig. 9
figure 9

Daily average water temperature at each monitoring site: Horizontal lines show 15 and 20 °C for reference. Temperature readings were made every 30 min 24 h a day using Hobo© temperature loggers suspended ~30 cm below the sea surface

Full size image

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

James, K., Shears, N.T. Population ecology of the invasive kelp Undaria pinnatifida towards the upper extreme of its temperature range. Mar Biol 163, 225 (2016). https://doi.org/10.1007/s00227-016-2993-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2993-9

Keywords

Search

Navigation