, Volume 172, Issue 2, pp 575–583 | Cite as

Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes

  • Laura J. Falkenberg
  • Bayden D. Russell
  • Sean D. ConnellEmail author
Global change ecology - Original research


Primary producers rarely exist under their ideal conditions, with key processes often limited by resource availability. As human activities modify environmental conditions, and therefore resource availability, some species may be released from these limitations while others are not, potentially disrupting community structure. In order to examine the limitations experienced by algal functional groups that characterise alternate community structures (i.e. turf-forming algae and canopy-forming kelp), we exposed these groups to contemporary and enriched levels of carbon dioxide (CO2) and nutrients. Turfs responded to the individual enrichment of both CO2 and nutrients, with the greatest shift in the biomass and carbon:nitrogen (C:N) ratios observed under their combined enrichment. In contrast, kelp responded to enriched nutrients, but not enriched CO2. We hypothesise that the differing limitations reflect the contrasting physiologies of these functional groups, specifically their methods of C acquisition, such as the possession and/or efficiency of a carbon concentrating mechanism (CCM). Importantly, our results reveal that these functional groups, whose interactions structure entire communities, experience distinct resource limitations, with some potentially limited by a single type of resource (i.e. kelp by nutrients), while others may be co-limited (i.e. turf by CO2 and nutrients). Consequently, the identification of how alternate conditions modify resource availability and limitations may facilitate anticipation of the future sustainability of major ecosystem components and the communities they support.


Carbon dioxide Co-limitation Kelp Nutrients Turf-forming algae 



We thank the many volunteers, including members of the Southern Seas Ecology Laboratories, for assistance with the assembly of the experimental mesocosms, collection of algae and maintenance of experimental conditions. Financial support for this research was provided by an ARC grant to S.D.C. and B.D.R. and an APA grant to L.J.F.

Supplementary material

442_2012_2507_MOESM1_ESM.doc (152 kb)
Supplementary material 1 (DOC 151 kb)


  1. Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Oceanogr Mar Biol Annu Rev 45:345–405Google Scholar
  2. Airoldi L, Balata D, Beck MW (2008) The gray zone: relationships between habitat loss and marine diversity and their applications in conservation. J Exp Mar Biol Ecol 366:8–15CrossRefGoogle Scholar
  3. Allgeier JE, Rosemond AD, Layman CA (2011) The frequency and magnitude of non-additive responses to multiple nutrient enrichment. J Appl Ecol 48:96–101CrossRefGoogle Scholar
  4. Andersen T, Pedersen O (2002) Interactions between light and CO2 enhance the growth of Riccia fluitans. Hydrobiologia 477:163–170CrossRefGoogle Scholar
  5. Beardall J, Giordano M (2002) Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms, and their regulation. Funct Plant Biol 29:335–347CrossRefGoogle Scholar
  6. Beardall J, Raven JA (2004) The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43:26–40CrossRefGoogle Scholar
  7. Benedetti-Cecchi L et al (2001) Predicting the consequences of anthropogenic disturbance: large-scale effects of loss of canopy algae on rocky shores. Mar Ecol Progr Ser 214:137–150CrossRefGoogle Scholar
  8. Bryars S, Rowling K (2009) Benthic habitats of eastern Gulf St Vincent: major changes in benthic cover and composition following European settlement of Adelaide. Trans R Soc South Aust 133:318–338Google Scholar
  9. Caldeira K, Wickett ME (2003) Anthropogenic carbon and ocean pH. Nature 425:365PubMedCrossRefGoogle Scholar
  10. Coleman MA (2002) Small-scale spatial variability in intertidal and subtidal turfing algal assemblages and the temporal generality of these patterns. J Exp Mar Biol Ecol 267:53–74CrossRefGoogle Scholar
  11. Connell SD (2003) The monopolization of understorey habitat by subtidal encrusting coralline algae: a test of the combined effects of canopy-mediated light and sedimentation. Mar Biol 142:1065–1071Google Scholar
  12. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B 277:1409–1415PubMedCrossRefGoogle Scholar
  13. Connell SD et al (2008) Recovering a lost baseline: missing kelp forests from a metropolitan coast. Mar Ecol Progr Ser 360:63–72CrossRefGoogle Scholar
  14. Craine JM, Morrow C, Stock WD (2008) Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol 179:829–836PubMedCrossRefGoogle Scholar
  15. Davidson EA, Howarth RW (2007) Nutrients in synergy. Nature 449:1000–1001PubMedCrossRefGoogle Scholar
  16. Dickson AG, Millero FJ (1987) A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep Sea Research Part A. Oceanogr Res Pap 34:1733–1743CrossRefGoogle Scholar
  17. Duarte CM (2002) The future of seagrass meadows. Environ Conserv 29:192–206CrossRefGoogle Scholar
  18. Elser JJ et al (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142PubMedCrossRefGoogle Scholar
  19. Eriksson BK, Johansson G, Snoeijs P (2002) Long-term changes in the macroalgal vegetation of the inner Gullmar Fjord, Swedish Skagerrak coast. J Phycol 38:284–296CrossRefGoogle Scholar
  20. Falkenberg LJ, Burnell OW, Connell SD, Russell BD (2010) Sustainability in near-shore marine systems: promoting natural resilience. Sustainability 2:2593–2600CrossRefGoogle Scholar
  21. Falkowski PG, Raven JA (2007) Aquatic photosyntesis, 2nd edn. Princeton University Press, PrincetonGoogle Scholar
  22. Feely RA et al (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305:362–366PubMedCrossRefGoogle Scholar
  23. Fowler-Walker MJ, Connell SD (2002) Opposing states of subtidal habitat across temperate Australia: consistency and predictability in kelp canopy-benthic associations. Mar Ecol Progr Ser 240:49–56CrossRefGoogle Scholar
  24. Gattuso JP, Buddemeier RW (2000) Ocean biogeochemistry: calcification and CO2. Nature 407:311–313PubMedCrossRefGoogle Scholar
  25. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annu Rev Plant Biol 56:99–131PubMedCrossRefGoogle Scholar
  26. Gorgula SK, Connell SD (2004) Expansive covers of turf-forming algae on human-dominated coast: the relative effects of increasing nutrient and sediment loads. Mar Biol 145:613–619CrossRefGoogle Scholar
  27. Gorman D, Connell SD (2009) Recovering subtidal forests in human-dominated landscapes. J Appl Ecol 46:1258–1265CrossRefGoogle Scholar
  28. Gorman D, Russell BD, Connell SD (2009) Land-to-sea connectivity: linking human-derived terrestrial subsidies to subtidal habitat change on open rocky coasts. Ecol Appl 19:1114–1126PubMedCrossRefGoogle Scholar
  29. Hamilton JG, Zangerl AR, DeLucia EH, Berenbaum MR (2001) The carbon–nutrient balance hypothesis: its rise and fall. Ecol Lett 4:86–95CrossRefGoogle Scholar
  30. Harpole WS et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862PubMedCrossRefGoogle Scholar
  31. Hein M, Pedersen MF, Sandjensen K (1995) Size-dependent nitrogen uptake in micro- and macroalgae. Mar Ecol Progr Ser 118:247–253CrossRefGoogle Scholar
  32. Hepburn CD et al (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Change Biol 17:2488–2497CrossRefGoogle Scholar
  33. Hurd CL, Hepburn CD, Currie KI, Raven JA, Hunter KA (2009) Testing the effects of ocean acidification on algal metabolism: considerations for experimental designs. J Phycol 45:1236–1251CrossRefGoogle Scholar
  34. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  35. Kraufvelin P (2007) Responses to nutrient enrichment, wave action and disturbance in rocky shore communities. Aquat Bot 87:262–274CrossRefGoogle Scholar
  36. Kraufvelin P, Moy FE, Christie H, Bokn TL (2006) Nutrient addition to experimental rocky shore communities revisited: delayed responses, rapid recovery. Ecosystems 9:1076–1093CrossRefGoogle Scholar
  37. Kraufvelin P, Lindholm A, Pedersen M, Kirkerud L, Bonsdorff E (2010) Biomass, diversity and production of rocky shore macroalgae at two nutrient enrichment and wave action levels. Mar Biol 157:29–47CrossRefGoogle Scholar
  38. Kübler JE, Johnston AM, Raven JA (1999) The effects of reduced and elevated CO2 and O2 on the seaweed Lomentaria articulata. Plant Cell Environ 22:1303–1310CrossRefGoogle Scholar
  39. Liebig J (1842) Animal chemistry or organic chemistry and its application to physiology and pathology. Johnson Reprint, New YorkGoogle Scholar
  40. Lobban CS, Harrison PJ (1994) Seaweed ecology and physiology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  41. Maberly S, Raven J, Johnston A (1992) Discrimination between 12C and 13C by marine plants. Oecologia 91:481–492CrossRefGoogle Scholar
  42. Mehrbach C, Culberson CH, Hawley JE, Pytkowicz RM (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol Oceanogr 18:897–907CrossRefGoogle Scholar
  43. Miller RJ, Reed DC, Brzezinski MA (2009) Community structure and productivity of subtidal turf and foliose algal assemblages. Mar Ecol Prog Ser 388:1–11CrossRefGoogle Scholar
  44. Nielsen KJ (2001) Bottom-up and top-down forces in tide pools: test of a food chain model in an intertidal community. Ecol Monogr 71:187–217CrossRefGoogle Scholar
  45. Orth RJ et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996CrossRefGoogle Scholar
  46. 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 Progr Ser 142:261–272CrossRefGoogle Scholar
  47. Pedersen MF, Borum J (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Mar Ecol Prog Ser 161:155–163CrossRefGoogle Scholar
  48. Pedersen MF, Borum J, Leck Fotel F (2010) Phosphorus dynamics and limitation of fast- and slow-growing temperate seaweeds in Oslofjord, Norway. Mar Ecol Prog Ser 399:103–115CrossRefGoogle Scholar
  49. 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 39:285–290CrossRefGoogle Scholar
  50. Pierrot D, Lewis E, Wallace DWR (2006) MS Excel program developed for CO2 system calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak RidgeGoogle Scholar
  51. Raven JA, Beardall J (2003) Carbon acquisition mechanisms of algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In: Larkum AWD, Douglas S, Raven JA (eds) Photosynthesis in algae, vol 14. Kluwer Academic, Dordrecht, pp 225–244CrossRefGoogle Scholar
  52. Raven JA et al (2002) Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct Plant Biol 29:355–378CrossRefGoogle Scholar
  53. Raven J, Giordano M, Beardall J, Maberly S (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynth Res 109:281–296PubMedCrossRefGoogle Scholar
  54. Rost B, Riebesell U, Burkhardt S, Sültemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnol Oceanogr 48:55–67CrossRefGoogle Scholar
  55. Russell BD (2007) Effects of canopy-mediated abrasion and water flow on the early colonisation of turf-forming algae. Mar Freshw Res 58:657–665CrossRefGoogle Scholar
  56. Russell BD, Thompson JI, Falkenberg LJ, Connell SD (2009) Synergistic effects of climate change and local stressors: CO2 and nutrient-driven change in subtidal rocky habitats. Glob Change Biol 15:2153–2162CrossRefGoogle Scholar
  57. Russell BD, Passarelli CA, Connell SD (2011) Forecasted CO2 modifies the influence of light in shaping subtidal habitat. J Phycol 47:744–752CrossRefGoogle Scholar
  58. Steneck RS et al (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  59. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, PrincetonGoogle Scholar
  60. Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci 57:579–589CrossRefGoogle Scholar
  61. Vitousek PM et al (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750Google Scholar
  62. Worm B, Lotze HK, Bostrom C, Engkvist R, Labanauskas V, Sommer U (1999) Marine diversity shift linked to interactions among grazers, nutrients and propagule banks. Mar Ecol Progr Ser 185:309–314CrossRefGoogle Scholar
  63. Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: methods for marine benthic ecology. Int Rev Hydrobiol 85:359–375CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Laura J. Falkenberg
    • 1
  • Bayden D. Russell
    • 1
  • Sean D. Connell
    • 1
    Email author
  1. 1.Southern Seas Ecology Laboratories, School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia

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