Skip to main content
SpringerLink
Log in

A kelp with integrity: Macrocystis pyrifera prioritises tissue maintenance in response to nitrogen fertilisation

  • Physiological ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Our understanding of the response of vascular, terrestrial plants to nitrogen (N) addition is advanced and provides the foundation for modern agriculture. In comparison, information on responses of marine macroalgae to increased nitrogen is far less developed. We investigated how in situ pulses of nitrate (NO3 −) affected the growth and N physiology of Macrocystis pyrifera by adding N using potassium nitrate dissolution blocks during a period of low seawater N concentration. Multiple parameters (e.g. growth, pigments, soluble NO3 −) were measured in distinct tissues throughout entire fronds (apical meristem, stipe, adult blade, mature blade, sporophyll, and holdfast). Unexpectedly, N fertilisation did not enhance elongation rates within the frond, but instead thickness (biomass per unit area) increased in adult blades. Increased blade thickness may have enhanced tissue integrity as fertilised kelp had lower rates of blade erosion. Tissue chemistry also responded to enrichment; pigmentation, soluble NO3 −, and % N were higher throughout fertilised fronds. Labelled 15N traced N uptake and translocation from N sources in the kelp canopy to sinks in the holdfast, 10 m below. This is the first evidence of long-distance (>1 m) transport of N in macroalgae. Patterns in physiological parameters suggest that M. pyrifera displays functional differentiation between canopy and basal tissues that may aid in nutrient-tolerance strategies, similar to those seen in higher plants and unlike those seen in more simple algae (i.e. non-kelps). This study highlights how little we know about N additions and N-use strategies within kelp compared to the wealth of literature available for higher plants.

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.

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

Similar content being viewed by others

References

  • Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67

    Article  CAS  Google Scholar 

  • Anten NPR, Martínez-Ramos M, Ackerly DD (2003) Defoliation and growth in an understory palm: quantifying the contributions of compensatory responses. Ecology 84(11):2905–2918

    Article  Google Scholar 

  • Armitage AR, Frankovich TA, Fourqurean JW (2011) Long-term effects of adding nutrients to an oligotrophic coastal environment. Ecosystems 14(3):430–444

    Article  CAS  Google Scholar 

  • Barsanti L, Paolo G (2014) Algae: anatomy, biochemistry and biotechnology, 2nd edn., vol 1. CRC, New York

  • Beardall J, Roberts S, Millhouse J (1991) Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1,5-biphosphate carboxylase/oxygenase in green microalgae. Can J Bot 69(5):1146–1150

    Article  CAS  Google Scholar 

  • Brown MT, Nyman MA, Keogh JA, Chin NKM (1997) Seasonal growth of the giant kelp Macrocystis pyrifera in New Zealand. Mar Biol 129(3):417–424

    Article  Google Scholar 

  • Champan ARO, Craigie JS (1977) Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen. Mar Biol 40(3):197–205

    Article  Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Chapin FS III, Vitousek PM, Van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127(1):48–58

    Article  Google Scholar 

  • Clendenning K (1971) Photosynthesis and general development. In: North WJ (ed) The biology of the giant kelp beds (Macrocystis pyrifera) in California. Hedwigia, Von Cramer, pp 257–263

  • 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(6):1225–1234

    Article  CAS  Google Scholar 

  • Dean TA, Jacobsen FR (1986) Nutrient-limited growth of juvenile kelp, Macrocystis pyrifera, during the 1982–1984 “El Niño” in southern California. Mar Biol 90(4):597–601

    Article  Google Scholar 

  • Desmond MJ, Pritchard DW, Hepburn CD (2015) Light limitation within southern New Zealand kelp forest communities. PLoS One 10(4):e0123676. doi:10.1371/journal.pone.0123676

    Article  PubMed  PubMed Central  Google Scholar 

  • Drobnitch ST, Jensen KH, Prentice P, Pittermann J (2015) Convergent evolution of vascular optimization in kelp (Laminariales). Proc R Soc B 282:20151667. doi:10.1098/rspb.2015.1667

    Article  PubMed  Google Scholar 

  • Duncan MJ, Harrison PJ (1982) Comparison of solvente for extracting chlorophylls from marine Macrophytes. Bot Mar 25(9):445–447

    Article  CAS  Google Scholar 

  • Evans G (1972) The quantitative analysis of plant growth. Blackwell Scientific, Oxford

    Google Scholar 

  • Ferdie M, Fourqurean JW (2004) Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment. Limnol Oceanogr 49(6):1–14

    Article  Google Scholar 

  • Fox MD (2013) Resource translocation drives δ13C fractionation during recovery from disturbance in giant kelp, Macrocystis pyrifera. J Phycol 49(5):811–815

    CAS  PubMed  Google Scholar 

  • Foyer CH, Ferrario-Méry S, Noctor G (2001) Interactions between carbon and nitrogen metabolism. In: Plant nitrogen. Springer Berlin Heidelberg,  pp 237–254

  • Fry B (2007) Stable isotope ecology. Springer Science & Business Media

  • Gao X, Agatsuma Y, Taniguchi K (2013) Effect of nitrate fertilization of gametophytes of the kelp Undaria pinnatifida on growth and maturation of the sporophytes cultivated in Matsushima Bay, northern Honshu, Japan. Aquacult Int 21(1):53–64

    Article  Google Scholar 

  • Gerard GA (1982a) In situ rates of nitrate uptake by giant kelp, Macrocystis pyrifera (L.) C. Agardh: tissue differences, environmental effects, and predictions of nitrogen-limited growth. J Exp Biol 62(3):211–224

    Article  CAS  Google Scholar 

  • Gerard VA (1982b) Growth and utilization of internal nitrogen reserves by the giant kelp Macrocystis pyrifera in a low-nitrogen environment. Mar Biol 66(1):27–35

    Article  CAS  Google Scholar 

  • Graham MH, Vasquez JA, Buschmann AH (2007) Global ecology of the giant kelp Macrocystis pyrifera: from ecotypes to ecosystems. In: Gibson RN, Atkinson RJA, Gordon JM (eds) Oceanography and marine biology: an annual review. CRC Press, Boca Raton, pp 50–62

    Google Scholar 

  • Graneli E, Sündback K (1985) The response of planktonic and microbenthic algal assemblages to nutrient enrichment in shallow coastal waters, southwest Sweden. J Exp Mar Biol Ecol 85:253–268

    Article  CAS  Google Scholar 

  • Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 222:1169–1194

    Article  Google Scholar 

  • Hepburn CD (2003) Macrocystis and associated epifauana. PhD thesis, University of Otago, Dunedin

  • Hepburn CD, Holborow JD, Wing SR, Frew RD, Hurd CL (2007) Exposure to waves enhances the growth rate and nitrogen status of the giant kelp Macrocystis pyrifera. Mar Ecol Prog Ser 339:99–108

    Article  CAS  Google Scholar 

  • Hepburn CD, Frew RD, Hurd CL (2011) Uptake and transport of nitrogen derived from sessile epifauna in the giant kelp Macrocystis pyrifera. Aquat Biol 14:121–128

    Article  Google Scholar 

  • Hernández I, Peralta G, Pérez-Lloréns L, Vergara JJ (1997) Biomass and dynamics of growth of Ulva species in Palmones River estuary. J Phycol 33:764–772

    Article  Google Scholar 

  • Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Annu Rev Ecol 19(1):1–22

    Article  Google Scholar 

  • Howarth RW, Billen G, Swaney D, Townsend A, Jaworski N, Lajtha K, Downing JA, Elmgren R, Caraco N, Jordan T, Berendse R, Freney J, Kudeyarov V, Murdoch P, Zhao-Liang Z (1996) Regional nitrogen budgets and riverine N and P fluxes for the drainages to the North Atlantic Ocean: natural and human influences. In: Nitrogen cycling in the North Atlantic Ocean and its watersheds. Springer, Dordrecht,  pp 75–139

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Biol 45(1):577–607

    Article  CAS  Google Scholar 

  • Kain JM (1989) The seasons in the subtidal. Brit Phycol J 24:203–215

    Article  Google Scholar 

  • Konotchick T, Parnell PE, Dayton P, Leichter JJ (2012) Vertical distribution of Macrocystis pyrifera nutrient exposure in southern California. Estuar Coast Shelf Sci 106:85–92

    Article  CAS  Google Scholar 

  • Konotchick T, Dupont CL, Valas R, Badger JH, Allen AE (2013) Transcriptomic analysis of metabolic function in the giant kelp, Macrocystis pyrifera, across depth and season. New Phytol. doi:10.1111/nph.12160

    PubMed  PubMed Central  Google Scholar 

  • Lamport DTA (1965) The protein component of primary cell walls. In: Preston RD (ed) Advances in botanical research.. Academic Press, Orlando

  • Maloney B, Iliffe TM, Gelwick F, Quigg A (2011) Effect of nutrient enrichment on naturally occurring macroalgal species in six cave pools in Bermuda. Phycologia 50(2):132–143

    Article  Google Scholar 

  • Manley SL (1983) Composition of sieve tube sap from Macrocystis pyrifera (Phaeophyta) with emphasis on the inorganic constituents. J Phycol 19:118–121

    Article  CAS  Google Scholar 

  • Mann K (1973) Seaweeds—their productivity and strategy for growth. Science 182:975–981

    Article  CAS  PubMed  Google Scholar 

  • Martínez B, Pato LS, Rico JM (2012) Nutrient uptake and growth responses of three intertidal macroalgae with perennial, opportunistic and summer-annual strategies. Aquat Bot 96:14–22

    Article  Google Scholar 

  • McGlathery KJ, Pedersen MF (1999) The effect of growth irradiance on the coupling of carbon and nitrogen metabolism in Chaetomorpha linum (Chlorophyta). J Phycol 35:721–731

    Article  CAS  Google Scholar 

  • McGlathery KJ, Pedersen MF, Borum J (1996) Changes in intracellular nitrogen pools and feedback controls on nitrogen uptake in Chaetomorpha linum (Chlorophyta). J Phycol 32(3):393–401

    Article  CAS  Google Scholar 

  • Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11(5):470–480

    Article  PubMed  Google Scholar 

  • Neushul M (1971) Species of Macrocystis pyrifera with particular reference to those of North and South America. Nova Hedw 32:211–222

    Google Scholar 

  • North WJ (1971) The biology of giant kelp beds (Macrocystis pyrifera) in California: introduction and background. Nova Hedw 32:1–68

    Google Scholar 

  • North WJ, Zimmerman RC (1984) Influences of macronutrients and water temperatures on summertime survival of Macrocystis pyrifera canopies. Hydrobiologia 116–117(1):419–424

    Article  Google Scholar 

  • Pastor J, Aber JD, McClaugherty CA, Melillo JM (1984) Aboveground production and N and P cycling along a nitrogen mineralization gradient on Blackhawk Island, Wisconsin. Ecology 65:265–268

    Google Scholar 

  • Pedersen MF, Borum J (1996) Nutrient control of algal growth in estuarine waters. Nutrient limitation and the importance of nitrogen requirements and nitrogen storage among phytoplankton and species of macroalgae. Mar Ecol Prog Ser 142:261–272

    Article  CAS  Google Scholar 

  • Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161:155–163

    Article  Google Scholar 

  • Perissinotto R, McQuaid CD (1992) Deep occurrence of the giant kelp Macrocystis laevis in the Southern Ocean. Mar Ecol Prog Ser 81:89–95

    Article  Google Scholar 

  • Pfister CA, Van Alstyne KL (2003) An experimental assessment of the effects of nutrient enhancement on the intertidal kelp Hedophyllum sessile (Laminariales, Phaeophyceae). J Phycol 39(2):285–290

    Article  Google Scholar 

  • Poorter H, Remkes C, Lambers H (1990) Carbon and nitrogen economy of 24 wild species differing in relative growth rate. Plant Physiol 94:621–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raven JA (2003) Long-distance transport in non-vascular plants. Plant Cell Environ 26(1):73–85

    Article  Google Scholar 

  • Raven JA, Wollenweber B, Handley LL (1992) A comparison of ammonium and nitrate as nitrogen sources for photolithotrophs. New Phytol 19–32

  • Reich PB, Walters MB, Ellsworth DS (1991) Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in maple and oak trees. Plant Cell Environ 14(3):251–259

    Article  Google Scholar 

  • Reiter WD (1998) Arabidopsis thaliana as a model system to study synthesis, structure, and function of the plant cell wall. Plant Physiol Biochem 36(1–2):167–176

    Article  CAS  Google Scholar 

  • Schilling G, Adgo E, Schulze J (2006) Carbon costs of nitrate reduction in broad bean (Vicia faba L.) and pea (Pisum sativum L.) plants. J Plant Nutr Soil Sci 169(5):691–698

    Article  CAS  Google Scholar 

  • Schmitz K, Srivastava LM (1979) Long distance transport in Macrocystis integrifolia. I. Translocation of 14C-labeled assimilates. Plant Physiol 63(6):995–1002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seely GR, Duncan MJ, Vidaver WE (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12(2):184–188

    Article  CAS  Google Scholar 

  • Shemesh A, Macko SA, Charles CD, Rau GH (1993) Isotopic evidence for reduced productivity in the glacial Southern Ocean. Science 262(5132):407–410

    Article  CAS  PubMed  Google Scholar 

  • Shivji MS (1985) Interactive effects of light and nitrogen on growth and chemical composition of juvenile Macrocystis pyrifera (L.) C. Ag. (Phaeophyta) sporophytes. J Exp Biol 89(1):81–96

    Article  CAS  Google Scholar 

  • Stephens TA, Hepburn CD (2014) Mass-transfer gradients across kelp beds influence Macrocystis pyrifera growth over small spatial scales. Mar Ecol Prog Ser 515:97–109

    Article  Google Scholar 

  • Syrett P (1981) Nitrogen metabolism of microalgae. Can Bull Fish Aquat Sci 1(1):12

    Google Scholar 

  • Teichberg M, Heffner LR, Fox S, Valiela I (2007) Nitrate reductase and glutamine synthetase activity, internal N pools, and growth of Ulva lactuca: responses to long and short-term N supply. Mar Biol 151(4):1249–1259

    Article  CAS  Google Scholar 

  • Tilman D (1984) Plant dominance along an experimental nutrient gradient. Ecology 65:1445–1453

    Article  Google Scholar 

  • Wright IJ, Cannon K (2001) Relationships between leaf lifespan and structural defences in a low-nutrient, sclerophyll flora. Funct Ecol 15:351–359

    Article  Google Scholar 

  • Zimmerman RC, Kremer JN (1984) Episodic nutrient supply to a kelp forest ecosystem in Southern California. J Mar Res 42(3):591–604

    Article  Google Scholar 

  • 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 27:277–285

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the staff and students of the University of Otago Marine Science Department, the Portobello Marine Laboratory, and Liina Pajusalu for providing assistance in the field. David Duggins provided useful comments during the final stages of preparation of this manuscript, and input from reviewers on its first submission improved the clarity. This work was funded by a University of Otago International Postgraduate Scholarship and postgraduate research funding to T. A. S., and was supplemented by Departmental Funding from C. D. H.

Author contribution statement

T. A. S. and C. D. H. conceived the experiment. T. A. S. was responsible for the experimental design, performed the lab and field experiments and did the chemical and data analyses. T. A. S. wrote the manuscript with editorial advice from C. D. H.

Author information

Authors and Affiliations

  1. Department of Marine Science, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand

    Tiffany A. Stephens & Christopher D. Hepburn

Authors
  1. Tiffany A. Stephens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher D. Hepburn
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tiffany A. Stephens.

Ethics declarations

Funding

This research was not funded by any body independent of the University of Otago. It was funded through the Marine Science Department at the University of Otago via postgraduate research funding to T. A. S. and personal research funds given to C. D. H. as part of his professorship.

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by James Fourqurean.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stephens, T.A., Hepburn, C.D. A kelp with integrity: Macrocystis pyrifera prioritises tissue maintenance in response to nitrogen fertilisation. Oecologia 182, 71–84 (2016). https://doi.org/10.1007/s00442-016-3641-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3641-2

Keywords

Search

Navigation