Phenotypic plasticity promotes persistence following severe events: Physiological and morphological responses of seagrass to flooding

Journal of Ecology

Volumn 102, Issue 1, 2014, Pages 54-64

  Maxwell, Paul S ^a   Pitt, Kylie A ^a   Burfeind, Dana D ^a,b   Olds, Andrew D ^a   Babcock, Russell C ^c   Connolly, Rod M ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c CSIRO   (Australia)

Author keywords

Aquatic plant ecology; Habitat forming species; Moreton Bay; Photoacclimation; Resilience; Water quality gradient; Zostera muelleri

Indexed keywords

ACCLIMATION; ECOSYSTEM FUNCTION; ECOSYSTEM RESILIENCE; ECOSYSTEM STRUCTURE; FLOODING; MORPHOLOGY; PHENOTYPIC PLASTICITY; PHYSIOLOGICAL RESPONSE; SEAGRASS; WATER QUALITY;

AUSTRALIA; MORETON BAY; QUEENSLAND;

ZOSTERA MUELLERI;

EID: 84890312627     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12167     Document Type: Article

References (72)

1. Abal, E., Loneragan, N., Bowen, P., Perry, C., Udy, J. & Dennison, W. (1994) Physiological and morphological responses of the seagrass Zostera capricorni Aschers, to light intensity. Journal of Experimental Marine Biology and Ecology, 178, 113-129.
2. Alcoverro, T., Manzanera, M. & Romero, J. (2001) Annual metabolic carbon balance of the seagrass Posidonia oceanica: the importance of carbohydrate reserves. Marine Ecology Progress Series, 211, 105-116.
3. Alcoverro, T., Zimmerman, R.C., Kohrs, D.G. & Alberte, R.S. (1999) Resource allocation and sucrose mobilization in light-limited eelgrass Zostera marina. Marine Ecology Progress Series, 187, 121-131.
4. Allen, C.D. & Breshears, D.D. (1998) Drought-induced shift of a forest-woodland ecotone: rapid landscape response to climate variation. Proceedings of the National Academy of Sciences of the United States of America, 95, 14839-14842.
5. Anderson, M.J., Gorley, R.N. & Clarke, K.R. (2008) PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK.
6. Anderson, M.J. & Willis, T.J. (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology, 84, 511-525.
7. Anderson, M.J., Crist, T.O., Chase, J.M., Vellend, M., Inouye, B.D., Freestone, A.L. et al. (2011) Navigating the multiple meanings of β diversity: a roadmap for the practicing ecologist. Ecology Letters, 14, 19-28.
8. Arnone, J.A. III, Jasoni, R.L., Lucchesi, A.J., Larsen, J.D., Leger, E.A., Sherry, R.A., Luo, Y., Schimel, D.S. & Verburg, P.S.J. (2011) A climatically extreme year has large impacts on C4 species in tallgrass prairie ecosystems but only minor effects on species richness and other plant functional groups. Journal of Ecology, 99, 678-688.
9. Barrett, J.E., Virginia, R.A., Wall, D.H., Doran, P.T., Fountain, A.G., Welch, K.A. & Lyons, W.B. (2008) Persistent effects of a discrete warming event on a polar desert ecosystem. Global Change Biology, 14, 2249-2261.
10. Beer, S., Björk, M., Gademann, R. & Ralph, P.J. (2001) Measurements of photosynthetic rates in seagrasses. Global Seagrass Research Methods (eds F.T. Short & R. Coles), pp. 183-198. Elsevier, Amsterdam.
11. Beierkuhnlein, C., Thiel, D., Jentsch, A., Willner, E. & Kreyling, J. (2011) Ecotypes of European grass species respond differently to warming and extreme drought. Journal of Ecology, 99, 703-713.
12. Beisner, B.E., Haydon, D.T. & Cuddington, K. (2003) Alternative stable states in ecology. Frontiers in Ecology and the Environment, 1, 376-382.
13. Bennett, E.M., Peterson, G.D. & Gordon, L.J. (2009) Understanding relationships among multiple ecosystem services. Ecology Letters, 12, 1394-1404.
14. Boon, P.I., Moriarty, D. & Saffigna, P.G. (1986) Nitrate metabolism in sediments from seagrass (Zostera capricorni) beds of Moreton Bay, Australia. Marine Biology, 91, 269-275.
15. Bouillon, S., Connolly, R.M. & Lee, S.Y. (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. Journal of Sea Research, 59, 44-58.
16. Brun, F.G., Olivé, I., Malta, E.J., Vergara, J.J., Hernández, I. & Pérez-Lloréns, J.J. (2008) Increased vulnerability of Zostera noltii to stress caused by low light and elevated ammonium levels under phosphate deficiency. Marine Ecology Progress Series, 365, 67-75.
17. Bulthuis, D.A. (1983) Effects of in situ light reduction on density and growth of the seagrass Heterozostera tasmanica(Martens ex Aschers.) den Hartog in Western Port, Victoria, Australia. Journal of Experimental Marine Biology and Ecology, 67, 91-103.
18. Burke, M., Dennison, W. & Moore, K. (1996) Non-structural carbohydrate reserves of eelgrass Zostera marina. Marine Ecology Progress Series, 137, 195-201.
19. Cai, W. & Rensch, P. (2012) The 2011 southeast Queensland extreme summer rainfall: a confirmation of a negative Pacific Decadal Oscillation phase? Geophysical Research Letters, 39, L08702.
20. Campbell, S.J. & McKenzie, L.J. (2004) Flood related loss and recovery of intertidal seagrass meadows in southern Queensland, Australia. Estuarine, Coastal and Shelf Science, 60, 477-490.
21. Carpenter, S., Arrow, K., Barrett, S., Biggs, R., Brock, W., Crépin, A.-S. et al. (2012) General resilience to cope with extreme events. Sustainability, 4, 3248-3259.
22. Casanova, M.T. & Brock, M.A. (2000) How do depth, duration and frequency of flooding influence the establishment of wetland plant communities? Plant Ecology, 147, 237-250.
23. Clarke, K.R., Somerfield, P.J. & Gorley, R.N. (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. Journal of Experimental Marine Biology and Ecology, 366, 56-69.
24. Collier, C.J., Lavery, P.S., Ralph, P.J. & Masini, R.J. (2008) Physiological characteristics of the seagrass Posidonia sinuosa along a depth-related gradient of light availability. Marine Ecology Progress Series, 353, 65-79.
25. Collier, C.J., Lavery, P.S., Ralph, P.J. & Masini, R.J. (2009) Shade-induced response and recovery of the seagrass Posidonia sinuosa. Journal of Experimental Marine Biology and Ecology, 370, 89-103.
26. Costanza, R., d'Arge, R., De Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K., Naeem, S., O'Neill, R.V. & Paruelo, J. (1997) The value of the world's ecosystem services and natural capital. Nature, 387, 253-260.
27. Coumou, D. & Rahmstorf, S. (2012) A decade of weather extremes. Nature Climate Change, 2, 491-496.
28. CSIRO (2007) Climate Change in Australia - Technical Report 2007. CSIRO, Canberra.
29. Dennison, W.C. (1990) Chlorophyll content. Seagrass research methods (eds R.C. Phillips & C.P. McRoy), pp. 83-86 UNESCO, USA.
30. Dennison, W.C. & Abal, E.G. (1999) Moreton Bay Study: A Scientific Basis for the Healthy Waterways Campaign. South East Qld Regional Water Quality Management Strategy Team, Brisbane.
31. Dennison, W.C. & Alberte, R.S. (1985) Role of daily light period in the depth distribution of Zostera marina(eelgrass). Marine Ecology Progress Series, 25, 51-61.
32. Dennison, W.C. & Alberte, R.S. (1986) Photoadaptation and growth of Zostera marina L. (eelgrass) transplants along a depth gradient. Journal of Experimental Marine Biology and Ecology, 98, 265-282.
33. Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P. & Smith, A.M. (1956) Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350-356.
34. EHMP (2010) Ecosystem Health Monitoring Program 2008-09 Annual Technical Report. South East Queensland Healthy Waterways Partnership, Brisbane.
35. EHMP (2013) Ecosystem Healthy Monitoring Program. http://www.healthywaterways.org/ehmphome.aspx [accessed 22 March 2013].
36. Gell, F.R. & Roberts, C.M. (2003) Benefits beyond boundaries: the fishery effects of marine reserves. Trends in Ecology & Evolution, 18, 448-455.
37. Gordon, D.M., Grey, K.A., Chase, S.C. & Simpson, C.J. (1994) Changes to the structure and productivity of a Posidonia sinuosa meadow during and after imposed shading. Aquatic Botany, 47, 265-275.
38. Grice, A., Loneragan, N. & Dennison, W. (1996) Light intensity and the interactions between physiology, morphology and stable isotope ratios in five species of seagrass. Journal of Experimental Marine Biology and Ecology, 195, 91-110.
39. Hemminga, M.A. & Mateo, M.A. (1996) Stable carbon isotopes in seagrasses: variability in ratios and use in ecological studies. Marine Ecology Progress Series, 140, 285-298.
40. van den Honert, R.C. & McAneney, J. (2011) The 2011 Brisbane floods: causes, impacts and implications. Water, 3, 1149-1173.
41. Hughes, A.R., Stachowicz, J.J. & Williams, S.L. (2009) Morphological and physiological variation among seagrass (Zostera marina) genotypes. Oecologia, 159, 725-733.
42. Jentsch, A. & Beierkuhnlein, C. (2008) Research frontiers in climate change: effects of extreme meteorological events on ecosystems. Comptes Rendus Geoscience, 340, 621-628.
43. Kirkman, H. (1978) Decline of seagrass in northern areas of Moreton Bay, Queensland. Aquatic Botany, 5, 63-76.
44. Larkum, A.W.D., Orth, R.J. & Duarte, C.M. (2006) Seagrasses: Biology, Ecology and Conservation. Springer, Dordrecht.
45. Lee, K.S. & Dunton, K.H. (1997) Effects of in situ light reduction on the maintenance, growth and partitioning of carbon resources in Thalassia testudinum Banks ex Kijnig. Journal of Experimental Marine Biology and Ecology, 210, 53-73.
46. Lloret, F., Escudero, A., Iriondo, J.M., Martínez Vilalta, J. & Valladares, F. (2012) Extreme climatic events and vegetation: the role of stabilizing processes. Global Change Biology, 18, 797-805.
47. Longstaff, B.J. (2003) Investigations into the Light Requirements of Seagrasses in Northeast Australia. PhD thesis, University of Queensland, Brisbane.
48. Longstaff, B.J. & Dennison, W.C. (1999) Seagrass survival during pulsed turbidity events: the effects of light deprivation on the seagrasses Halodule pinifolia and Halophila ovalis. Aquatic Botany, 65, 105-121.
49. Longstaff, B., Loneragan, N., O'Donohue, M. & Dennison, W. (1999) Effects of light deprivation on the survival and recovery of the seagrass Halophila ovalis (R. Br.) Hook. Journal of Experimental Marine Biology and Ecology, 234, 1-27.
50. Lovell, E.R. (1989) Coral assemblages of Moreton Bay, Queensland, Australia, before and after a major flood. Memoirs of the Queensland Museum, 27, 535-550.
51. McCabe, D.J. & Gotelli, N.J. (2000) Effects of disturbance frequency, intensity, and area on assemblages of stream macroinvertebrates. Oecologia, 124, 270-279.
52. Miner, B.G., Sultan, S.E., Morgan, S.G., Padilla, D.K. & Relyea, R.A. (2005) Ecological consequences of phenotypic plasticity. Trends in Ecology & Evolution, 20, 685-692.
53. Olds, A., Connolly, R.M., Pitt, K.A. & Maxwell, P.S. (2012a) Primacy of seascape connectivity effects in structuring coral reef fish assemblages. Marine Ecology Progress Series, 462, 191-203.
54. Olds, A., Pitt, K.A., Maxwell, P.S. & Connolly, R.M. (2012b) Synergistic effects of reserves and connectivity on ecological resilience. Journal of Applied Ecology, 49, 1195-1203.
55. Orth, R.J., Carruthers, T.J.B., Dennison, W.C., Duarte, C.M., Fourqurean, J.W., Heck, K.L. Jr, Hughes, A.R., Kendrick, G.A., Kenworthy, W.J. & Olyarnik, S. (2006) A global crisis for seagrass ecosystems. BioScience, 56, 987-996.
56. 2 of seagrass in Hervey Bay, Queensland, Australia. Aquatic Botany, 52, 3-17.
57. Quarmby, C. & Allen, S.E. (1989) Organic constituents. Chemical Analysis of Ecological Materials (ed. S.E. Allen), pp. 172-176. Blackwell Scientific, Oxford.
58. Roelfsema, C., Phinn, S., Udy, N. & Maxwell, P. (2009) An integrated field and remote sensing approach for mapping seagrass cover, Moreton Bay, Australia. Journal of Spatial Science, 54, 45-62.
59. Ruiz, J.M. & Romero, J. (2003) Effects of disturbances caused by coastal constructions on spatial structure, growth dynamics and photosynthesis of the seagrass Posidonia oceanica. Marine Pollution Bulletin, 46, 1523-1533.
60. Short, F., Carruthers, T., Dennison, W. & Waycott, M. (2007) Global seagrass distribution and diversity: a bioregional model. Journal of Experimental Marine Biology and Ecology, 350, 3-20.
61. Smith, M.D. (2011) An ecological perspective on extreme climatic events: a synthetic definition and framework to guide future research. Journal of Ecology, 99, 656-663.
62. Suding, K.N. & Hobbs, R.J. (2009) Threshold models in restoration and conservation: a developing framework. Trends in Ecology & Evolution, 24, 271-279.
63. Sultan, S.E. (2000) Phenotypic plasticity for plant development, function and life history. Trends in Plant Science, 5, 537-542.
64. Sultan, S.E., Wilczek, A.M., Bell, D.L. & Hand, G. (1998) Physiological response to complex environments in annual Polygonum species of contrasting ecological breadth. Oecologia, 115, 564-578.
65. Thrush, S.F., Hewitt, J.E., Cummings, V.J., Ellis, J.I., Hatton, C., Lohrer, A., Norkko, A. (2004) Muddy water: elevating sediment input to coastal and estuarine habitats. Frontiers in Ecology and the Environment, 2, 299-306.
66. Tibbetts, I.R., Hall, N.J. & Dennison, W.C. (1998) Moreton Bay and Catchment. School of Marine Science, University of Queensland, Brisbane.
67. Udy, J.W. & Dennison, W.C. (1997) Growth and physiological responses of three seagrass species to elevated sediment nutrients in Moreton Bay, Australia. Journal of Experimental Marine Biology and Ecology, 217, 253-277.
68. Valladares, F., Gianoli, E. & Gómez, J.M. (2007) Ecological limits to plant phenotypic plasticity. New Phytologist, 176, 749-763.
69. Vermaat, J.E. & Verhagen, F.C.A. (1996) Seasonal variation in the intertidal seagrass Zostera noltii Hornem.: coupling demographic and physiological patterns. Aquatic Botany, 52, 259-281.
70. Vichkovitten, T., Holmer, M. & Frederiksen, M.S. (2007) Spatial and temporal changes in non-structural carbohydrate reserves in eelgrass (Zostera marina L.) in Danish coastal waters. Botanica Marina, 50, 75-87.
71. Waycott, M., Longstaff, B.J. & Mellors, J. (2005) Seagrass population dynamics and water quality in the Great Barrier Reef region: a review and future research directions. Marine Pollution Bulletin, 51, 343-350.
72. Waycott, M., Duarte, C.M., Carruthers, T.J.B., Orth, R.J., Dennison, W.C., Olyarnik, S., Calladine, A., Fourqurean, J.W., Heck, K.L. & Hughes, A.R. (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106, 12377-12381.