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Oecologia

, Volume 176, Issue 3, pp 871–882 | Cite as

Seagrass response to CO2 contingent on epiphytic algae: indirect effects can overwhelm direct effects

  • Owen W. BurnellEmail author
  • Bayden D. Russell
  • Andrew D. Irving
  • Sean D. Connell
Global change ecology - Original research

Abstract

Increased availability of dissolved CO2 in the ocean can enhance the productivity and growth of marine plants such as seagrasses and algae, but realised benefits may be contingent on additional conditions (e.g. light) that modify biotic interactions between these plant groups. The combined effects of future CO2 and differing light on the growth of seagrass and their algal epiphytes were tested by maintaining juvenile seagrasses Amphibolis antarctica under three different CO2 concentrations representing ambient, moderate future and high future forecasts (i.e. 390, 650 vs. 900 µl l−1) and two light levels representing low and high PAR (i.e. 43 vs. 167 µmol m−2 s−1). Aboveground and belowground biomass, leaf growth, epiphyte cover, tissue chemistry and photosynthetic parameters of seagrasses were measured. At low light, there was a neutral to positive effect of elevated CO2 on seagrass biomass and growth; at high light, this effect of CO2 switched toward negative, as growth and biomass decreased at the highest CO2 level. These opposing responses to CO2 appeared to be closely linked to the overgrowth of seagrass by filamentous algal epiphytes when high light and CO2 were combined. Importantly, all seagrass plants maintained positive leaf growth throughout the experiment, indicating that growth was inhibited by some experimental conditions but not arrested entirely. Therefore, while greater light or elevated CO2 provided direct physiological benefits for seagrasses, such benefits were likely negated by overgrowth of epiphytic algae when greater light and CO2 were combined. This result demonstrates how indirect ecological effects from epiphytes can modify independent physiological predictions for seagrass associated with global change.

Keywords

Amphibolis antarctica Biotic interactions Filamentous epiphytes Global change Photosynthesis 

Notes

Acknowledgments

We would like to thank Nenah Mackenzie from The University of Adelaide for operating the mass spectrometer. S.D.C. and B.D.R. were funded by an ARC grant and S.D.C. received an ARC Future Fellowship. We would also like to thank two anonymous reviewers and the Associate Editor, whose comments improved an early draft of the manuscript.

Conflict of interest

The authors have no conflicts of interest to declare.

Supplementary material

442_2014_3054_MOESM1_ESM.docx (38 kb)
Table S1 ANOVA comparing the effects of CO2 and light on the biomass of calcified epiphytic algae on juvenile seagrass Amphibolis antarctica after 12 weeks. ACO 2  ambient CO2, MCO 2  moderate CO2, HCO 2  high CO2. Significant effects from ANOVA are highlighted in bold Fig. S1 Average hourly photosynthetically active radiation (PAR in µmol m−2 s−1) over 24 h for 12 weeks at different light treatments. Closed circles low light, open circles high light. Data points represent the mean ± SE (n = 84) Fig. S2a–b Calcified epiphytic algae on a shed leaves and b living plants of juvenile seagrass grown at different CO2 and light levels for 12 weeks. ACO 2  ambient CO2, MCO 2  moderate CO2, HCO 2  high CO2, LL low light, HL high light. Bars represent the mean ± SE (n = 6). Fig. S3a–b Regression analysis showing a total seagrass biomass (aboveground + belowground) vs.  % N in seagrass tissue, and b total epiphyte biomass (filamentous algae + calcified algae) vs.  % N in seagrass tissue. Linear regression analysis for total seagrass biomass (r 2 = 0.280, F 1,35 = 13.24, P < 0.001) and total epiphyte biomass (r 2 = 0.378, F 1,35 = 20.70, P < 0.001) (DOCX 38 kb)

References

  1. Alexandre A, Silva J, Buapet P, Bjork M, Santos R (2012) Effects of CO2 enrichment on photosynthesis, growth, and nitrogen metabolism of the seagrass Zostera noltii. Ecol Evol 2:2620–2630CrossRefGoogle Scholar
  2. Beardall J, Beer S, Raven JA (1998) Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot Mar 41:113–123CrossRefGoogle Scholar
  3. Beer S, Koch E (1996) Photosynthesis of marine macroalgae and seagrasses in globally changing CO2 environments. Mar Ecol Prog Ser 141:199–204CrossRefGoogle Scholar
  4. Beer S, Bjork M, Gademann R, Ralph PJ (2001) Measurements of photosynthetic rates in seagrasses. In: Short FT, Coles RG (eds) Global seagrass research methods. Elsevier, Amsterdam, pp 183–198CrossRefGoogle Scholar
  5. Borowitzka MA, Lavery PS, van Keulen M (2006) Epiphytes of seagrasses. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Dordrecht, pp 441–461Google Scholar
  6. Bryars S (2009) Can regional nutrient status be used to predict plant biomass, canopy structure and epiphyte biomass in the temperate seagrass Amphibolis antarctica? Mar Freshw Res 60:1054–1067CrossRefGoogle Scholar
  7. Bryars S, Neverauskas V (2004) Natural recolonisation of seagrasses at a disused sewage sludge outfall. Aquat Bot 80:283–289CrossRefGoogle Scholar
  8. Bryars S, Wear R, Collings G (2008) Seagrasses of Gulf St Vincent and Investigator Strait. In: Shepherd SA, Bryars S, Kirkegaard I, Harbison P, Jennings JT (eds) Natural history of Gulf St Vincent, vol 8. R Soc S Aust, Adelaide, pp 132–147Google Scholar
  9. Bryars S, Collings G, Miller D (2011) Nutrient exposure causes epiphytic changes and coincident declines in two temperate Australian seagrasses. Mar Ecol Prog Ser 441:89–103CrossRefGoogle Scholar
  10. Bulthuis DA, Woelkerling WJ (1983) Biomass accumulation and shading effects of epiphytes on leaves of the seagrass, Heterozostera tasmanica, in Victoria, Australia. Aquat Bot 16:137–148CrossRefGoogle Scholar
  11. Burkholder DA, Fourqurean JW, Heithaus MR (2013) Spatial pattern in seagrass stoichiometry indicates both N-limited and P-limited regions of an iconic P-limited subtropical bay. Mar Ecol Prog Ser 472:101–115CrossRefGoogle Scholar
  12. Burnell OW, Connell SD, Irving AD, Russell BD (2013a) Asymmetric patterns of recovery in two habitat forming seagrass species following simulated overgrazing by urchins. J Exp Mar Biol Ecol 448:114–120CrossRefGoogle Scholar
  13. Burnell OW, Russell BD, Irving AD, Connell SD (2013b) Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Mar Ecol Prog Ser 485:37–46CrossRefGoogle Scholar
  14. Calosi P et al (2013) Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acid-base and ion-regulatory abilities. Mar Pollut Bull 73:470–484PubMedCrossRefGoogle Scholar
  15. Campbell JE, Fourqurean JW (2013) Effects of in situ CO2 enrichment on the structural and chemical characteristics of the seagrass Thalassia testudinum. Mar Biol 160:1465–1475CrossRefGoogle Scholar
  16. Collings G, Bryars S, Nayar S, Miller D, Lill J, O’Loughlin E (2006) Elevated nutrient responses of the meadow forming seagrasses, Amphibolis and Posidonia, from the Adelaide metropolitan coastline. ACWS Technical Report No. 11 prepared for the Adelaide Coastal Waters Study Steering Committee. SARDI publication no. RD01/0208-16. South Australian Research and Development Institute (Aquatic Sciences), AdelaideGoogle Scholar
  17. 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 Biol Sci 277:1409–1415CrossRefGoogle Scholar
  18. Connell SD, Russell BD, Irving AD (2011) Can strong consumer and producer effects be reconciled to better forecast ‘catastrophic’ phase-shifts in marine ecosystems? J Exp Mar Biol Ecol 400:296–301CrossRefGoogle Scholar
  19. Connell SD, Kroeker KJ, Fabricius KE, Kline DI, Russell BD (2013) The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance. Philos Trans R Soc B 368(1627):20120442CrossRefGoogle Scholar
  20. Cook K, Vanderklift MA, Poore AGB (2011) Strong effects of herbivorous amphipods on epiphyte biomass in a temperate seagrass meadow. Mar Ecol Prog Ser 442:263–269CrossRefGoogle Scholar
  21. Copertino MS, Cheshire A, Kildea T (2009) Photophysiology of a turf algal community: integrated responses to ambient light and standing biomass. J Phycol 45:324–336CrossRefGoogle Scholar
  22. Curtis PS, Wang XZ (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313CrossRefGoogle Scholar
  23. DeLucia EH et al (1999) Net primary production of a forest ecosystem with experimental CO2 enrichment. Science 284:1177–1179PubMedCrossRefGoogle Scholar
  24. Duarte CM (1991) Seagrass depth limits. Aquat Bot 40:363–377CrossRefGoogle Scholar
  25. Ducker SC, Foord NJ, Knox RB (1977) Biology of Australian seagrasses: genus Amphibolis C Agardh (Cymodoceaceae). Aust J Bot 25:67–95CrossRefGoogle Scholar
  26. Eklof JS, Alsterberg C, Havenhand JN, Sundback K, Wood HL, Gamfeldt L (2012) Experimental climate change weakens the insurance effect of biodiversity. Ecol Lett 15:864–872PubMedCrossRefGoogle Scholar
  27. Falkenberg LJ, Russell BD, Connell SD (2012) Stability of strong species interactions resist the synergistic effects of local and global pollution in kelp forests. PLoS One 7:e33841PubMedCrossRefPubMedCentralGoogle Scholar
  28. Falkenberg LJ, Russell BD, Connell SD (2013) Contrasting resource limitations of marine primary producers: implications for competitive interactions under enriched CO2 and nutrient regimes. Oecologia 172:575–583PubMedCrossRefGoogle Scholar
  29. Gifford RM, Barrett DJ, Lutze JL (2000) The effects of elevated CO2 on the C:N and C:P mass ratios of plant tissues. Plant Soil 224:1–14CrossRefGoogle Scholar
  30. Hall-Spencer JM et al (2008) Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454:96–99PubMedCrossRefGoogle Scholar
  31. 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
  32. Irving AD (2009) Seagrass rehabilitation in Adelaide’s coastal waters VI. Refining techniques for the rehabilitation of Amphibolis spp. Final report prepared for the Coastal Management Branch of the Department for Environment and Heritage SA. South Australian Research and Development Institute (Aquatic Sciences), AdelaideGoogle Scholar
  33. Israel A, Hophy M (2002) Growth, photosynthetic properties and Rubisco activities and amounts of marine macroalgae grown under current and elevated seawater CO2 concentrations. Glob Change Biol 8:831–840CrossRefGoogle Scholar
  34. James NP, Bone Y, Brown KM, Cheshire A (2009) Calcareous epiphyte production in cool-water carbonate seagrass depositional environments—Southern Australia. In: Swart PK, Eberli GP, McKenzie JA (eds) Perspectives in carbonate geology: a tribute to the career of Robert Nathan Ginsburg, vol 41. Wiley, New York, pp 123–148. doi: 10.1002/9781444312065.ch9 Google Scholar
  35. Jiang ZJ, Huang XP, Zhang JP (2010) Effects of CO2 enrichment on photosynthesis, growth, and biochemical composition of seagrass Thalassia hemprichii (Ehrenb.) Aschers. J Integr Plant Biol 52:904–913PubMedCrossRefGoogle Scholar
  36. Kelaher BP, Van Den Broek J, York PH, Bishop MJ, Booth DJ (2013) Positive responses of a seagrass ecosystem to experimental nutrient enrichment. Mar Ecol Prog Ser 487:15–25CrossRefGoogle Scholar
  37. Kendrick GA, Burt JS (1997) Seasonal changes in epiphytic macro-algae assemblages between offshore exposed and inshore protected Posidonia sinuosa Cambridge et Kuo seagrass meadows, Western Australia. Bot Mar 40:77–85Google Scholar
  38. Kendrick GA, Lavery PS (2001) Assessing biomass, assemblage structure and productivity of algal epiphytes on seagrasses. In: Short FT, Coles RG (eds) Global seagrass research methods. Elsevier, Amsterdam, pp 199–222Google Scholar
  39. Keuskamp D (2004) Limited effects of grazer exclusion on the epiphytes of Posidonia sinuosa in South Australia. Aquat Bot 78:3–14CrossRefGoogle Scholar
  40. Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Change Biol 19:103–132CrossRefGoogle Scholar
  41. Kubler JE, Raven JA (1995) The interaction between inorganic carbon acquisition and light supply in Palmaria palmata (Rhodophyta). J Phycol 31:369–375CrossRefGoogle Scholar
  42. Lavery PS, Vanderklift MA (2002) A comparison of spatial and temporal patterns in epiphytic macroalgal assemblages of the seagrasses Amphibolis griffithii and Posidonia coriacea. Mar Ecol Prog Ser 236:99–112CrossRefGoogle Scholar
  43. Lavery PS, Reid T, Hyndes GA, Van Elven BR (2007) Effect of leaf movement on epiphytic algal biomass of seagrass leaves. Mar Ecol Prog Ser 338:97–106CrossRefGoogle Scholar
  44. Mabrouk L, Hamza A, Ben Brahim M, Bradai M-N (2013) Variability in the structure of epiphyte assemblages on leaves and rhizomes of Posidonia oceanica in relation to human disturbances in a seagrass meadow off Tunisia. Aquat Bot 108:33–40CrossRefGoogle Scholar
  45. Marba N, Walker DI (1999) Growth, flowering, and population dynamics of temperate Western Australian seagrasses. Mar Ecol Prog Ser 184:105–118CrossRefGoogle Scholar
  46. Martin S et al (2008) Effects of naturally acidified seawater on seagrass calcareous epibionts. Biol Lett 4:689–692PubMedCrossRefPubMedCentralGoogle Scholar
  47. Meehl GA et al (2007) Global climate projections. In: Soloman S et al (eds) Climate change 2007: the physical science basis. Contribution of the Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  48. Nayar S, Collings GJ, Miller DJ, Bryars S, Cheshire AC (2009) Uptake and resource allocation of inorganic carbon by the temperate seagrasses Posidonia and Amphibolis. J Exp Mar Biol Ecol 373:87–95CrossRefGoogle Scholar
  49. Nayar S, Collings GJ, Miller DJ, Bryars S, Cheshire AC (2010) Uptake and resource allocation of ammonium and nitrate in temperate seagrasses Posidonia and Amphibolis. Mar Pollut Bull 60:1502–1511PubMedCrossRefGoogle Scholar
  50. Orr JC et al (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686PubMedCrossRefGoogle Scholar
  51. Orth RJ, Moore KA (1983) Chesapeake Bay—an unprecedented decline in submerged aquatic vegetation. Science 222:51–53Google Scholar
  52. Orth RJ et al (2006) A global crisis for seagrass ecosystems. Bioscience 56:987–996CrossRefGoogle Scholar
  53. Palacios SL, Zimmerman RC (2007) Response of eelgrass Zostera marina to CO2 enrichment: possible impacts of climate change and potential for remediation of coastal habitats. Mar Ecol Prog Ser 344:1–13CrossRefGoogle Scholar
  54. Peralta G, Perez-Llorens JL, Hernandez I, Vergara JJ (2002) Effects of light availability on growth, architecture and nutrient content of the seagrass Zostera noltii Hornem. J Exp Mar Biol Ecol 269:9–26CrossRefGoogle Scholar
  55. Raven JA (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant Cell Environ 14:779–794CrossRefGoogle Scholar
  56. Reekie EG, Bazzaz FA (1989) Competition and patterns of resource use among seedlings of 5 tropical trees grown at ambient and elevated CO2. Oecologia 79:212–222CrossRefGoogle Scholar
  57. Russell BD, Connell SD (2005) A novel interaction between nutrients and grazers alters relative dominance of marine habitats. Mar Ecol Prog Ser 289:5–11CrossRefGoogle Scholar
  58. Russell BD, Passarelli CA, Connell SD (2011) Forecasted CO2 modifies the influence of light in shaping subtidal habitat. J Phycol 47:744–752CrossRefGoogle Scholar
  59. Russell BD et al (2012) Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems. Biol Lett 8:164–166PubMedCrossRefPubMedCentralGoogle Scholar
  60. Russell BD, Connell SD, Uthicke S, Muehllehner N, Fabricius KE, Hall-Spencer JM (2013) Future seagrass beds: can increased productivity lead to increased carbon storage? Mar Pollut Bull 73:463–469PubMedCrossRefGoogle Scholar
  61. Sand-Jensen K (1977) Effect of epiphytes on eelgrass photosynthesis. Aquat Bot 3:55–63Google Scholar
  62. Sand-Jensen K (1989) Environmental variables and their effect on photosynthesis of aquatic plant communities. Aquat Bot 34:5–25CrossRefGoogle Scholar
  63. Sand-Jensen K, Revsbech NP, Jorgensen BB (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89:55–62CrossRefGoogle Scholar
  64. Sarker YM, Bartsch I, Olischlager M, Gutow L, Wiencke C (2013) Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot Mar 56:63–74CrossRefGoogle Scholar
  65. Schwarz AM, Hellblom F (2002) The photosynthetic light response of Halophila stipulacea growing along a depth gradient in the Gulf of Aqaba, the Red Sea. Aquat Bot 74:263–272CrossRefGoogle Scholar
  66. Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196CrossRefGoogle Scholar
  67. Short FT, Wyllie-Echeverria S (1996) Natural and human-induced disturbance of seagrasses. Environ Conserv 23:17–27CrossRefGoogle Scholar
  68. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  69. Thimijan RW, Heins RD (1983) Photometric, radiometric, and quantum light units of measure: a review of procedures for interconversion. Hortscience 18:818–822Google Scholar
  70. Thomas CD et al (2004) Extinction risk from climate change. Nature 427:145–148PubMedCrossRefGoogle Scholar
  71. Thomsen MS et al (2012) A meta-analysis of seaweed impacts on seagrasses: generalities and knowledge gaps. PLoS One 7:21–28Google Scholar
  72. Thuiller W, Lavorel S, Araujo MB, Sykes MT, Prentice IC (2005) Climate change threats to plant diversity in Europe. Proc Natl Acad Sci USA 102:8245–8250PubMedCrossRefPubMedCentralGoogle Scholar
  73. Tomasko DA, Lapointe BE (1991) Productivity and biomass of Thalassia testudinum as related to water column nutrient availability and epiphyte levels: field observations and experimental studies. Mar Ecol Prog Ser 75:9–17CrossRefGoogle Scholar
  74. Touchette BW, Burkholder JM (2000) Overview of the physiological ecology of carbon metabolism in seagrasses. J Exp Mar Biol Ecol 250:169–205PubMedCrossRefGoogle Scholar
  75. Walker DI (1985) Correlations between salinity and growth of the seagrass Amphibolis antarctica (Labill) Sonder and Aschers. in Shark Bay, Western Australia, using a new method for measuring production-rate. Aquat Bot 23:13–26Google Scholar
  76. Walker DI, McComb AJ (1992) Seagrass degradation in Australian coastal waters. Mar Pollut Bull 25:191–195CrossRefGoogle Scholar
  77. Wand SJE, Midgley GF, Jones MH, Curtis PS (1999) Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Glob Change Biol 5:723–741CrossRefGoogle Scholar
  78. Waycott M et al (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381PubMedCrossRefPubMedCentralGoogle Scholar
  79. Williams WE, Garbutt K, Bazzaz FA, Vitousek PM (1986) The response of plants to elevated CO2.. IV. Two deciduous-forest tree communities. Oecologia 69:454–459Google Scholar
  80. Zou DH, Gao KS (2009) Effects of elevated CO2 on the red seaweed Gracilaria lemaneiformis (Gigartinales, Rhodophyta) grown at different irradiance levels. Phycologia 48:510–517Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Owen W. Burnell
    • 1
    Email author
  • Bayden D. Russell
    • 1
  • Andrew D. Irving
    • 2
  • Sean D. Connell
    • 1
  1. 1.Southern Seas Ecology Laboratories, Darling Building (DP418), School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia
  2. 2.School of Medical and Applied SciencesCentral Queensland UniversityRockhamptonAustralia

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