Journal of Applied Phycology

, Volume 26, Issue 2, pp 837–847 | Cite as

Ecophysiological plasticity of annual populations of giant kelp (Macrocystis pyrifera) in a seasonally variable coastal environment in the Northern Patagonian Inner Seas of Southern Chile

  • Alejandro H. Buschmann
  • Sandra V. Pereda
  • Daniel A. Varela
  • Juan Rodríguez-Maulén
  • Alejandra López
  • Luis González-Carvajal
  • Marcela Schilling
  • Eduardo A. Henríquez-Tejo
  • María C. Hernández-González


Annual populations of Macrocystis pyrifera in Southern Chile have been the main focus of studies intending to understand how these populations can couple consecutive sporophytic generations. Research has included studying the population dynamics and gametophytic responses to environmental conditions and the role of recruitment, grazing, and the use of benthic filter feeders as secondary substrate. Adult sporophytes undergo senescence due to changes in abiotic factors during summer and autumn producing 100 % mortality. This study provides evidence about the environmental factors driving the decline in sporophyte populations occurring in summer and fall by monitoring two independent kelp populations and also by running experiments using 400 L tubular photobioreactors with semicontrolled environmental factors for testing the capacity for new recruits to recover population levels under winter conditions. The study of natural populations of giant kelp indicates that high temperatures (>15–17 °C) explain the high mortality of adult plants in summer. On the other hand, the sporophytes established in late winter/early spring are able, under high nitrogen availability, to increase their chlorophyll content significantly, allowing the individuals to reduce their light saturation point and thus allow a higher productivity under the low light conditions that exist in late winter and early spring. These results, in addition to the recruitment facilitation produced by filter feeders, help to explain how giant kelp can deal with, and couple sporophytic generations, in variable environments. These results also emphasize the highly plastic physiology of giant kelp that enables this species to colonize diverse habitats across its large distributional range.


Giant kelp Macrocystis Phaeophyta Annual populations Ecophysiology Growth Photosynthesis Nitrate reductase Chlorophyll 



The authors acknowledge the financial support of FONDECYT 11100845 grant. The authors also acknowledge the field support of Miguel Maldonado, Robinson Altamirano, and Cristian Vera between many other students. English language usage was improved by Dr Matthew Lee.


  1. Brown MT, Nyman MA, Keogh JA, Chin NKM (1997) Seasonal growth of the giant kelp Macrocystis pyrifera in New Zealand. Mar Biol 129:417–424CrossRefGoogle Scholar
  2. Buschmann AH (1992) Algal communities of a wave-protected intertidal rocky shore in Southern Chile. In: Seeliger U (ed) Coastal plant communities of Latin America. Academic, San Diego, pp 91–104CrossRefGoogle Scholar
  3. Buschmann AH, Vásquez JA, Osorio P, Reyes E, Filún L, Hernández-González MC, Vega A (2004) The effect of water movement, temperature and salinity on abundance and reproductive patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile. Mar Biol 145:849–862CrossRefGoogle Scholar
  4. Buschmann AH, Moreno C, Vásquez JA, Hernández-González MC (2006) Reproduction strategies of Macrocystis pyrifera (Phaeophyta) in Southern Chile: the importance of population dynamics. J Appl Phycol 18:575–582CrossRefGoogle Scholar
  5. Cabello-Pasini A, Aguirre-von-Wobeser E, Figueroa FL (2000) Photoinhibition of photosynthesis in Macrocystis pyrifera (Phaeophyceae), Chondrus crispus (Rhodophyceae) and Ulva lactuca (Chlorophyceae) in outdoor culture systems. J Photochem Photobiol 57:169–178CrossRefGoogle Scholar
  6. Chapman ARO, Craigie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40:197–205CrossRefGoogle Scholar
  7. Chapman ARO, Markham JW, Lüning K (1978) Effects of nitrate concentration on the growth and physiology of Laminaria saccharina (Phaeophyta) in culture. J Phycol 14:195–198CrossRefGoogle Scholar
  8. Colombo-Pallotta MF, García-Mendoza E, Ladah LB (2006) Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234CrossRefGoogle Scholar
  9. Coyer JA, Smith GJ, Andersen RA (2001) Evolution of Macrocystis spp. (Phaeophyceae) as determined by ITS1 and ITS2 sequences. J Phycol 37:574–585CrossRefGoogle Scholar
  10. Dayton PK (1985a) Ecology of kelp communities. Ann Rev Ecol Syst 16:215–245CrossRefGoogle Scholar
  11. Dayton PK (1985b) The structure and regulation of some South American kelp communities. Ecol Monogr 55:447–468CrossRefGoogle Scholar
  12. Dayton PK, Tegner MJ, Edwards PB, Riser KL (1999) Temporal and spatial scales of kelp demography: the role of oceanographic climate. Ecol Monogr 69:219–250CrossRefGoogle Scholar
  13. Demes KW, Graham MH, Suskiewicz TS (2009) Phenotypic plasticity reconciles incongruous molecular and morphological taxonomies: the giant kelp, Macrocystis (Laminariales, Phaeophyceae), is a monospecific genus. J Phycol 45:1266–1269CrossRefGoogle Scholar
  14. Dean PR, Hurd CL (2007) Seasonal growth, erosion rates, and nitrogen and photosynthetic ecophysiology of Undaria pinnatifida (Heterokontophyta) in Southern New Zealand. J Phycol 43:1138–1148CrossRefGoogle Scholar
  15. Druehl LD, Wheeler WN (1986) Population biology of Macrocystis integrifolia from British Columbia, Canada. Mar Biol 90:173–179CrossRefGoogle Scholar
  16. Dunton KH (1990) Growth and production in Laminaria solidungula: relation to continuous underwater light levels in the Alaskan high Arctic. Mar Biol 106:297–304CrossRefGoogle Scholar
  17. Dunton KH, Jodwalis CM (1988) Photosynthetic performance of Laminaria solidungula measured in situ in the Alaskan high Arctic. Mar Biol 98:277–286CrossRefGoogle Scholar
  18. Edwards MS (2004) Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia 138:436–447PubMedCrossRefGoogle Scholar
  19. Edwards MS, Kim KY (2010) Diurnal variation in relative photosynthetic performance in giant kelp Macrocystis pyrifera (Phaeophyceae, Laminariales) at different depths as estimated using PAM fluorometry. Aquat Bot 92:119–128CrossRefGoogle Scholar
  20. Gao X, Endo H, Taniguchi K, Agatsuma Y (2013) Combined effects of seawater temperature and nutrient condition on growth and survival of juvenile sporophytes of the kelp Undaria pinnatifida (Laminariales; Phaeophyta) cultivated in northern Honshu, Japan. J Appl Phycol 25:269–275CrossRefGoogle Scholar
  21. Gagne JA, Mann KH, Chapman ARO (1982) Seasonal patterns of growth and storage in Laminaria longicruris in relation to differing patterns of availability of nitrogen in the water. Mar Biol 69:91–101CrossRefGoogle Scholar
  22. Genty B, Briantais J, Baker N (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92CrossRefGoogle Scholar
  23. Gerard VA (1997) The role of nitrogen nutrition in high-temperature tolerance of the kelp Laminaria saccharina (Chromophyta). J Phycol 33:800–810CrossRefGoogle Scholar
  24. Gerard VA (1982) Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar Biol 66:27–35CrossRefGoogle Scholar
  25. Gerard VA, Mann KH (1979) Growth and production of Laminaria longicruris (Phaeophyta) populations exposed to different intensities of water movement. J Phycol 14:195–198Google Scholar
  26. Gerard VA, DuBois K (1988) Temperature ecotypes near the Southern boundary of the kelp, Laminaria saccharina. Mar Biol 97:575–580CrossRefGoogle Scholar
  27. González-Fragoso J, Ibarra-Obando SE, North WJ (1991) Frond elongation rates of shallow water Macrocystis pyrifera (L.) Ag. in northern Baja California, México. J Appl Phycol 3:311–318CrossRefGoogle Scholar
  28. Graham MH (1996) Effect of high irradiance on recruitment of giant kelp Macrocystis (Phaeophyta) in shallow water. J Phycol 32:903–906CrossRefGoogle Scholar
  29. Graham MH (2002) Prolonged reproductive consequences of short-term biomass loss in seaweeds. Mar Biol 140:901–911CrossRefGoogle Scholar
  30. Graham MH, Harrold C, Lisin S, Light K, Watanabe JM, Foster MS (1997) Population dynamics of giant kelp Macrocystis pyrifera along a wave exposure gradient. Mar Ecol Prog Ser 148:269–279CrossRefGoogle Scholar
  31. Graham MH, Vásquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol Ann Rev 45:39–88Google Scholar
  32. Gutiérrez A, Correa T, Muñoz V, Santibañez A, Marcos T, Cáceres C, Buschmann AH (2006) Farming of the giant kelp Macrocystis pyrifera in Southern Chile for development of novel food products. J Appl Phycol 18:259–267CrossRefGoogle Scholar
  33. Henley W (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739CrossRefGoogle Scholar
  34. Henríquez LA, Buschmann AH, Maldonado MA, Graham MH, Hernández-González MC, Pereda SV, Bobadilla MI (2011) Grazing on giant kelp microscopic phases and the recruitment success of annual populations of Macrocystis pyrifera (Laminariales, Phaeophyta) in Southern Chile. J Phycol 47:252–258CrossRefGoogle Scholar
  35. Hernández-Carmona G (1996) Frond elongation rates of Macrocystis pinífera (L.) Ag. at Bahia Tortugas, Baja California sur, México. Ciencias Marinas 22:57–72Google Scholar
  36. Hurd C, Berges J, Osborne J, Harrison P (1995) An in vitro assay for marine macroalgae: optimization and characterization of the enzyme for Fucus gardneri (Phaeophyta). J Phycol 31:835–843CrossRefGoogle Scholar
  37. Jackson GA (1977) Nutrients and production of the giant kelp Macrocystis pyrifera off Southern California. Limnol Oceanogr 22:979–995CrossRefGoogle Scholar
  38. Jackson GA (1987) Modeling the growth and harvest yield of the giant kelp Macrocystis pyrifera. Mar Biol 95:611–624CrossRefGoogle Scholar
  39. Jassby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547CrossRefGoogle Scholar
  40. Lobban CS (1978) Growth of Macrocystis integrifolia in Barkley Sound, Vancouver Island, B.C. Can J Bot 56:2707–2711CrossRefGoogle Scholar
  41. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge, 384 ppCrossRefGoogle Scholar
  42. Macaya EC, Zucarello GC (2010a) DNA barcoding and genetic divergence in the giant kelp Macrocystis (Laminariales). J Phycol 46:736–742CrossRefGoogle Scholar
  43. Macaya EC, Zucarello GC (2010b) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112CrossRefGoogle Scholar
  44. Mizuta H, Torii K, Yamamoto H (1997) The relationship between nitrogen and carbon contents in the sporophytes of Laminaria japonica (Phaeophyceae). Fish Sci 63:553–556Google Scholar
  45. North WJ (1971) The biology of giant kelp beds (Macrocystis) in California: introduction and background. Nova Hedwigia 32:1–68Google Scholar
  46. North WJ (1994) Review of Macrocystis biology. In: Akatsuka I (ed) Biology of economic algae. Academic, The Hague, pp 447–527Google Scholar
  47. North WJ, Jackson GA, Manley SL (1986) Macrocystis and its environment: knowns and unknowns. Aquat Bot 26:9–26CrossRefGoogle Scholar
  48. Reed DC (1987) Factors affecting sporophyll production in the giant kelp Macrocystis pyrifera. J Exp Mar Biol Ecol 113:60–69CrossRefGoogle Scholar
  49. Reed DC, Ebeling AW, Anderson TW, Anghera M (1996) Differential reproductive responses to fluctuating resources in two seaweeds with different reproductive strategies. Ecology 77:300–316CrossRefGoogle Scholar
  50. Reed DC, Kinlan BP, Raimondi PT, Washburn L, Gaylord B, Drake PT (2006) A metapopulation perspective on patch dynamics and connectivity of giant kelp. In: Kritzer JP, Sale PF (eds) Marine metapopulations. Academic, San Diego, pp 352–386Google Scholar
  51. Reed DC, Rassweiler A, Arkema KK (2008) Biomass rather than growth rate determines variation in net primary production by giant kelp. Ecology 89:2493–2505PubMedCrossRefGoogle Scholar
  52. Russell G (1986) Variation and natural selection in marine macroalgae. Oceanogr Mar Biol Annu Rev 24:309–377Google Scholar
  53. Seely G, Duncan M, Vidaver W (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12:184–188CrossRefGoogle Scholar
  54. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99CrossRefGoogle Scholar
  55. Strickland J, Parsons T (1972) A practical handbook of seawater analysis. Bull Fish Res Board Can No 167, 2nd ed., 310 ppGoogle Scholar
  56. van Tüssenbroek BI (1989) Seasonal growth and composition of fronds of Macrocystis pyrifera in the Falkland Islands. Mar Biol 100:419–430CrossRefGoogle Scholar
  57. Vásquez JA, Alonso-Vega JM, Buschmann AH (2006) Long term variability in the structure of kelp communities in northern Chile and the 1997–98 ENSO. J Appl Phycol 18:505–519CrossRefGoogle Scholar
  58. Vega A, Vásquez JA, Buschmann AH (2005) Population biology of the subtidal kelps Macrocystis integrifolia and Lessonia trabeculata (Laminariales, Phaeophyceae) in an upwelling ecosystem of Northern Chile: interannual variability and EL Niño 1997–1998. Rev Chil Hist Nat 78:33–50Google Scholar
  59. Westermeier R, Möller P (1990) Population dynamics of Macrocystis pyrifera (L.) C. Agardh in the rocky intertidal of Southern Chile. Bot Mar 33:363–367CrossRefGoogle Scholar
  60. Westermeier R, Patiño D, Piel M, Maier I, Müller D (2006) A new approach to kelp mariculture in Chile: production of free-floating sporophyte seedlings from gametophyte cultures of Lessonia trabeculata and Macrocystis pyrifera. Aquacult Res 37:164–171CrossRefGoogle Scholar
  61. Wheeler PA, North WJ (1981) Nitrogen supply, tissue composition and frond growth rates for Macrocystis pyrifera off the coast of Southern California. Mar Biol 64:59–69CrossRefGoogle Scholar
  62. Wheeler WN, Druehl LD (1986) Seasonal growth and productivity of Macrocystis integrifolia in British Columbia, Canada. Mar Biol 90:181–186CrossRefGoogle Scholar
  63. Zimmerman RC, Kremer JN (1986) In situ growth and chemical composition of the giant kelp, Macrocystis pyrifera, response to temporal changes in ambient nutrient availability. Mar Ecol Prog Ser 27:277–285CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Alejandro H. Buschmann
    • 1
  • Sandra V. Pereda
    • 1
  • Daniel A. Varela
    • 1
  • Juan Rodríguez-Maulén
    • 1
  • Alejandra López
    • 1
  • Luis González-Carvajal
    • 1
  • Marcela Schilling
    • 3
  • Eduardo A. Henríquez-Tejo
    • 2
  • María C. Hernández-González
    • 1
  1. 1.Centro i-mar, Universidad de Los LagosPuerto MonttChile
  2. 2.Programa Magister en Ciencias, Dirección de Postgrado, Universidad de Los LagosOsornoChile
  3. 3.Universidad de La Frontera, Avenida Francisco SalazarTemucoChile

Personalised recommendations