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Oecologia

, Volume 175, Issue 1, pp 409–416 | Cite as

Spatially variable synergistic effects of disturbance and additional nutrients on kelp recruitment and recovery

  • Paul E. Carnell
  • Michael J. Keough
Ecosystem ecology - Original research

Abstract

Understanding the impact of multiple stressors on ecosystems is of pronounced importance, particularly when one or more of those stressors is anthropogenic. Here we investigated the role of physical disturbance and increased nutrients on reefs dominated by the canopy-forming kelp Ecklonia radiata. We combined experimental kelp canopy removals and additional nutrient at three different locations in a large embayment in temperate southeastern Australia. Over the following winter recruitment season, Ecklonia recruitment was unaffected by increased nutrients alone, but tripled at all sites where the canopy had been removed. At one site, the combination of disturbance and increased nutrients resulted in more than four times the recruitment of the introduced kelp Undaria pinnatifida. Six months after disturbance, the proliferation of the Undaria canopy in the canopy-removal and nutrient-addition treatment negatively influenced the recovery of the native kelp Ecklonia. Given the otherwise competitive dominance of adult Ecklonia, this provides a mechanism whereby Undaria could maintain open space for the following recruitment season. This interplay between disturbance, nutrients and the response of native and invasive species makes a compelling case for how a combination of factors can influence species dynamics.

Keywords

Multiple stressors Invasive species Resilience Ecklonia radiata Undaria pinnatifida 

Notes

Acknowledgments

We thank R. Saaristo, P. Crockett, P. Gilmour, C. Jung, R. Chisholm, C. Taylor, H. Wooton and B. Hull for their invaluable field assistance. We also thank K. Mossop, A. O’Brien and three anonymous reviewers for comments that greatly improved the manuscript. This study was funded by an Australian Research Council Grant to M. J. K., a Holsworth Wildlife Research Endowment to P. E. C., the Jasper Loftus-Hills award to P. E. C. and an Australian Postgraduate Award to P. E. C.

References

  1. Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. J Biophotonics 11:36–42Google Scholar
  2. Bellgrove A, Clayton MN, Quinn GP (1997) Effects of secondarily treated sewage effluent on intertidal macroalgae recruitment processes. Mar Freshwater Res 48:137–146CrossRefGoogle Scholar
  3. Berger R, Bergstrom L, Graneli E, Kautsky L (2004) How does eutrophication affect different life stages of Fucus vesiculosus in the Baltic Sea? A conceptual model. Hydrobiologia 514:243–248CrossRefGoogle Scholar
  4. Brown VB, Davies SA, Synnot RN (1990) Long-term monitoring of the effects of treated sewage effluent on the intertidal macroalgal community near Cape Schanck, Victoria, Australia. Bot Mar 33:85–98CrossRefGoogle Scholar
  5. Bulleri F, Russell BD, Connell SD (2012) Context-dependency in the effects of nutrient loading and consumers on the availability of space in marine rocky environments. PLoS One 7:1–9CrossRefGoogle Scholar
  6. Campbell SJ (1999) Uptake of ammonium by four species of macroalgae in Port Phillip Bay, Victoria Australia. Mar Freshwater Res 50:515–522CrossRefGoogle Scholar
  7. Clark GF, Johnston EL (2009) Propagule pressure and disturbance interact to overcome biotic resistance of marine invertebrate communities. Oikos 118:1679–1686CrossRefGoogle Scholar
  8. Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310PubMedCrossRefGoogle Scholar
  9. 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 277:1409–1415PubMedCentralPubMedCrossRefGoogle Scholar
  10. Connell JH, Hughes TP, Wallace CC (1997) A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecol Monogr 67:461–488CrossRefGoogle Scholar
  11. Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315PubMedCrossRefGoogle Scholar
  12. Dayton PK, Tegner MJ (1984) Catastrophic storms, El Niño, and patch stability in a Southern California kelp community. Science 224:283–285PubMedCrossRefGoogle Scholar
  13. Dayton PK, Tegner MJ, Parnell PE, Edwards PB (1992) Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol Monogr 62:421–445CrossRefGoogle Scholar
  14. Doblin M, Clayton MN (1995) Effects of secondarily treated sewage effluent on the early life history stages of two species of brown macroalgae: Hormosira banksii and Durvillaea potatorum. Mar Biol 122:689–698CrossRefGoogle Scholar
  15. Eckman JE, Duggins DO, Sewell AT (1989) Ecology of understory kelp environments. I. Effects of kelps on flow and particle transport near the bottom. J Exp Mar Biol Ecol 129:173–188CrossRefGoogle Scholar
  16. Eriksson BK, Rubach A, Hillebrand H (2007) Dominance by a canopy forming seaweed modifies resource and consumer control of bloom-forming macroalgae. Oikos 116:1211–1219CrossRefGoogle Scholar
  17. 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 7:1–7Google Scholar
  18. 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
  19. Forrest BM, Brown SN, Taylor MD, Hurd CL, Hay CH (2000) The role of natural dispersal mechanisms in the spread of Undaria pinnatifida (Laminariales, Phaeophyceae). Phycologia 39:547–553CrossRefGoogle Scholar
  20. Gorman D, Connell SD (2009) Recovering subtidal forests in human dominated landscapes. J App Ecol 46:1258–1265CrossRefGoogle Scholar
  21. Gross KL, Mittelbach GG, Reynolds HL (2005) Grassland invasibility and diversity: responses to nutrients, seed input, and disturbance. Ecology 86:476–486CrossRefGoogle Scholar
  22. Heggie DT, Skyring GW, Orchardo J, Longmore AR, Nicholson GJ, Berelson WM (1999) Denitrification and denitrifying efficiencies in sediments of Port Phillip Bay: direct determinations of biogenic N2 and N-metabolite fluxes with implications for water quality. Mar Freshwater Res 50:589–596CrossRefGoogle Scholar
  23. Hemmi A, Jormalainen V (2002) Nutrient enhancement increases performance of a marine herbivore via quality of its food alga. Ecology 83:1052–1064CrossRefGoogle Scholar
  24. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nyström M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933PubMedCrossRefGoogle Scholar
  25. Irving AD, Connell SD (2006) Physical disturbance by kelp abrades erect algae from the understorey. Mar Ecol Prog Ser 324:127–137CrossRefGoogle Scholar
  26. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  27. Kennelly SJ (1987a) Physical disturbances in an Australian kelp community. 1. Temporal effects. Mar Ecol Prog Ser 40:145–153CrossRefGoogle Scholar
  28. Kennelly SJ (1987b) Physical disturbances in an Australian kelp community. 2. Effects on understorey species due to differences in kelp cover. Mar Ecol Prog Ser 40:155–165CrossRefGoogle Scholar
  29. Kennelly SJ (1989) Effects of kelp canopies on understorey species due to shade and scour. Mar Ecol Prog Ser 50:215–224CrossRefGoogle Scholar
  30. Kennelly SJ, Underwood AJ (1993) Geographic consistencies of effects of experimental physical disturbance on understorey species in sublittoral kelp forests in central New South Wales. J Exp Mar Biol Ecol 168:35–58CrossRefGoogle Scholar
  31. Kirkman H (1981) The first year in the life history and the survival of the juvenile marine macrophyte, Ecklonia radiata (Turn.). J. Agardh. J Exp Mar Biol Ecol 55:243–254CrossRefGoogle Scholar
  32. Kirkman H (1984) Standing stock and production of Ecklonia radiata (C.Ag.). J. Agardh. J Exp Mar Biol Ecol 76:119–130CrossRefGoogle Scholar
  33. Korpinen S, Jormalainen V (2008) Grazing and nutrients reduce recruitment success of Fucus vesiculosus L. (Fucales: Phaeophyceae). Estuar Coast Shelf Sci 78:437–444CrossRefGoogle Scholar
  34. Korpinen S, Honkanen T, Vesakoski O, Hemmi A, Koivikko R, Loponen J, Jormalainen V (2007a) Macroalgal communities face the challenge of changing biotic interactions: review with focus on the Baltic Sea. Ambio 36:203–211PubMedCrossRefGoogle Scholar
  35. Korpinen S, Jormalainen V, Honkanen T (2007b) Effects of nutrients, herbivory, and depth on the macroalgal community in the rocky sublittoral. Ecology 88:839–852PubMedCrossRefGoogle Scholar
  36. Korpinen S, Jormalainen V, Honkanen T (2007c) Bottom-up and cascading top-down control of macroalgae along a depth gradient. J Exp Mar Biol Ecol 343:52–63CrossRefGoogle Scholar
  37. Korpinen S, Jormalainen V, Pettay E (2010) Nutrient availability modifies species abundance and community structure of Fucus-associated littoral benthic fauna. Mar Environ Res 70:283–292PubMedCrossRefGoogle Scholar
  38. Kraufvelin P, Salovius S, Christie H, Moy FE, Karez R (2006) Eutrophication induced changes in benthic algae affect the behaviour and fitness of the marine amphipod Gammarus locusta. Aquat Bot 84:199–209CrossRefGoogle Scholar
  39. Lee RS, Black KP, Bosserel C, Greer D (2012) Present and future prolonged drought impacts on a large temperate embayment: Port Phillip Bay, Australia. Ocean Dynam 62:907–922CrossRefGoogle Scholar
  40. Littler MM, Murray SN (1975) Impact of sewage on the distribution, abundance and community structure of rocky intertidal macro-organisms. Mar Biol 30:277–291CrossRefGoogle Scholar
  41. Lotze HK, Worm B (2002) Complex interaction of ecological and climatic controls on macroalgal recruitment. Limnol Oceanogr 47:1734–1741CrossRefGoogle Scholar
  42. Luning K (1980) Critical light levels and temperature regulating the gametogenesis of three Laminaria species (Phaeophyceae). J Phycol 16:1–15CrossRefGoogle Scholar
  43. Luning K, Neushul M (1978) Light and temperature demands for growth and reproduction for Laminaria gametophytes in southern and central California. Mar Biol 45:297–309CrossRefGoogle Scholar
  44. Massad TJ, Balch JK, Davidson EA, Brando PM, Mews CL, Porto P, Quintino RM, Vieira SA, Marimon BH Jr, Trumbore SE (2013) Interactions between repeated fire, nutrients, and insect herbivores affect the recovery of diversity in the southern Amazon. Oecologia 172:219–229PubMedCrossRefGoogle Scholar
  45. McKenzie LA, Brooks RC, Johnston EL (2012) A widespread contaminant enhances invasion success of a marine invader. J App Ecol 49:767–773CrossRefGoogle Scholar
  46. Mora C, Metzger R, Rollo A, Myers RA (2007) Experimental simulations about the effects of overexploitation and habitat fragmentation on populations facing environmental warming. Proc R Soc B Biol Sci 274:1023–1028CrossRefGoogle Scholar
  47. Morelissen 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 448:197–206CrossRefGoogle Scholar
  48. Morris L, Keough MJ (2003) Variation in the response of intertidal infaunal invertebrates to nutrient additions: field manipulations at two sites within Port Phillip Bay, Australia. Mar Ecol Prog Ser 250:35–49CrossRefGoogle Scholar
  49. Morris L, Jenkins G, Hatton D, Smith T (2007) Effects of nutrient additions on intertidal seagrass (Zostera muelleri) habitat in Western Port, Victoria, Australia. Mar Freshwater Res 58:666–674CrossRefGoogle Scholar
  50. Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101PubMedCrossRefGoogle Scholar
  51. Murray AG, Parslow JS (1999) Modelling of nutrient impacts in Port Phillip Bay—a semi-enclosed marine Australian ecosystem. Mar Freshwater Res 50:597–611CrossRefGoogle Scholar
  52. Novaczek I (1984) Response of Ecklonia radiata (Laninariales) to light at 15 °C with reference to the field light budget at Goat Island Bay, New Zealand. Mar Biol 80:263–272CrossRefGoogle Scholar
  53. O’Brien AL, Volkenborn N, van Beusekom J, Morris L, Keough MJ (2009) Interactive effects of porewater nutrient enrichment, bioturbation and sediment characteristics on benthic assemblages in sandy sediments. J Exp Mar Biol Ecol 371:51–59CrossRefGoogle Scholar
  54. O’Brien AL, Morris L, Keough MJ (2010) Multiple sources of nutrients add to the complexities of predicting marine benthic community responses to enrichment. Mar Freshwater Res 61:1388–1398CrossRefGoogle Scholar
  55. Olff H, Alonso D, Berg MP, Eriksson BK, Loreau M, Piersma T, Rooney N (2009) Parallel ecological networks in ecosystems. Phil Trans R Soc B 364:1755–1779PubMedCentralPubMedCrossRefGoogle Scholar
  56. Paling EI (1991) The relationship between nitrogen cycling and productivity in macroalgal stands and seagrass meadows. Ph.D. thesis. University of Westem AustraliaGoogle Scholar
  57. Piola RF, Johnston EL (2008) Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities. Divers Distrib 14:329–342CrossRefGoogle Scholar
  58. Primo C, Hewitt CL, Campbell ML (2010) Reproductive phenology of the introduced kelp Undaria pinnatifida (Phaeophyceae, Laminariales) in Port Phillip Bay (Victoria, Australia). Biol Invas 12:3081–3092CrossRefGoogle Scholar
  59. Reed DC, Rassweiler A, Carr MH, Cavanaugh KC, Malone DP, Siegel DA (2011) Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2108–2116PubMedCrossRefGoogle Scholar
  60. Ross DJ, Longmore AR, Keough MJ (2013) Spatially variable effects of a marine pest on ecosystem function. Oecologia 172:525–538PubMedCrossRefGoogle Scholar
  61. 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
  62. 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 434–435:25–33CrossRefGoogle Scholar
  63. Shears NT, Ross PM (2010) Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs. Ecol Lett 13:1149–1159PubMedCrossRefGoogle Scholar
  64. Smale DA, Wernberg T, Vance T (2011) Community development on subtidal reefs in a biodiversity hotspot: the influences of wave energy and the stochastic recruitment of a dominant kelp. Mar Biol 158:1757–1766CrossRefGoogle Scholar
  65. Sousa WP (1984) The role of disturbance in natural communities. Annu Rev Ecol Syst 15:353–391CrossRefGoogle Scholar
  66. Steen H (2004) Interspecific competition between Enteromorpha (Ulvales: Chlorophyceae) and Fucus (Fucales: Phaeophyceae) germlings: effects of nutrient concentration, temperature, and settlement density. Mar Ecol Prog Ser 278:89–101CrossRefGoogle Scholar
  67. Steen H, Rueness J (2004) Comparison of survival and growth in germlings of six fucoid species (Fucales, Phaeophyceae) at two different temperature and nutrient regimes. Sarsia 89:175–183CrossRefGoogle Scholar
  68. Steen H, Scrosati R (2004) Intraspecific competition in Fucus serratus and F. evanescens (Phaeophyceae: Fucales) germlings: effects of settlement density, nutrient concentration, and temperature. Mar Biol 144:61–70CrossRefGoogle Scholar
  69. Steneck RS, Graham MH, Bourque BJ, Corbett B, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  70. Toohey BD, Kendrick GA (2007) Survival of juvenile Ecklonia radiata sporophytes after canopy loss. J Exp Mar Biol Ecol 349:170–182CrossRefGoogle Scholar
  71. Valdivia N, Stehbens JD, Hermelink B, Connell SD, Molis M, Wahl M (2008) Disturbance mediates the effects of nutrients on developing assemblages of epibiota. Aust Ecol 33:951–962CrossRefGoogle Scholar
  72. 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 295:63–90CrossRefGoogle Scholar
  73. Wahl M, Jormalainen V, Eriksson BK, Coyer JA, Molis M, Schubert H, Dethier M, Karez R, Kryse I, Lenz M, Pearson G, Rohde S, Wikstrom SA, Olsen JL (2011) Stress ecology in Fucus: abiotic, biotic, and genetic interactions. In: Lesser M (ed) Advances in Marine Biology, vol 59. Elsevier Academic Press, California, pp 37–105Google Scholar
  74. Wernberg T, Kendrick GA, Toohey BD (2005) Modification of physical environment by an Ecklonia radiata (Laminariales) canopy and its implications for associated foliose algae. Aquat Ecol 39:419–430CrossRefGoogle Scholar
  75. Worm B, Sommer U (2000) Rapid direct and indirect effects of a single nutrient pulse in a seaweed-epiphyte-grazer system. Mar Ecol Prog Ser 202:282–288CrossRefGoogle Scholar
  76. 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 Prog Ser 185:309–314CrossRefGoogle Scholar
  77. Worm B, Reusch TBH, Lotze HK (2000) In situ nutrient enrichment: methods for marine benthic ecology. Int Rev Hydrob 85:359–375CrossRefGoogle Scholar
  78. Worm B, Lotze HK, Hillebrand H, Sommer U (2002) Consumer versus resource control of species diversity and ecosystem functioning. Nature 417:848–851PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of ZoologyThe University of MelbourneParkvilleAustralia

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