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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Intense storms and the delivery of materials that relieve nutrient limitations in mangroves of an arid zone estuary

Catherine E. Lovelock A D , Ilka C. Feller B , Maria Fernanda Adame A , Ruth Reef A , Helen M. Penrose A , Lili Wei A and Marilyn C. Ball C
+ Author Affiliations
- Author Affiliations

A The School of Biological Science, The University of Queensland, Brisbane, Qld 4072, Australia.

B Smithsonian Environmental Research Center, Smithsonian Institution, Edgewater, MD 21037, USA.

C Division of Plant Sciences, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia.

D Corresponding author. Email: c.lovelock@uq.edu.au

Functional Plant Biology 38(6) 514-522 https://doi.org/10.1071/FP11027
Submitted: 24 January 2011  Accepted: 21 April 2011   Published: 3 June 2011

Abstract

Tropical cyclones can be devastating to ecosystems, but they can also result in pulses of fresh water and sediments delivered in floodwaters to the coastal zone. In the arid zone the pulses provided by cyclones may be particularly important for the maintenance of productivity. We examined the impacts of Cyclone Pancho on growth and nutrient limitations to growth in mangroves on the arid coast of Western Australia. We found that growth of trees was enhanced after the cyclone, more than doubling their rates of stem extension. Fertilisation studies showed that before the cyclone tree growth was nutrient limited. After the cyclone fertilisation treatments had no significant effect on growth, indicating nutrients had been delivered during the storm. Additionally, before the cyclone the efficiency of resorption of phosphorus and nitrogen from senescent leaves was higher than after the cyclone, suggesting that nutrient availability was enhanced. Analysis of stable isotopes of leaf tissue indicated that the cyclone was associated with small changes in water use efficiency, consistent with decreased soil salinity associated with the cyclone. There was, however, significant reductions in δ15N indicating enhanced N supply potentially from a new source. We conclude that in the arid zone, floodwater associated with cyclones is important for the delivery of nutrient subsidies that stimulate mangrove growth and that predicted future reductions in the frequency of cyclones will have negative impacts on the productivity of these ecosystems.

Additional keywords: Avicennia marina, Cyclone Pancho, Exmouth Gulf, Giralia Bay, nitrogen, phosphate, resorption efficiency, Western Australia, δ15N.


References

Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608.
Nutrient resorption from senescing leaves of perennials: are there general patterns?Crossref | GoogleScholarGoogle Scholar |

Aerts R, Chapin FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 1–67.
The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVejurw%3D&md5=3f5c0d72d56c648a60b495b37eced45eCAS |

Baeta A, Pinto R, Valiela I, Richard P, Niquil N, Marques J (2009) δ15N and δ13C in the Mondego estuary food web, seasonal variation in producers and consumers. Marine Environmental Research 67, 109–116.
δ15N and δ13C in the Mondego estuary food web, seasonal variation in producers and consumers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1Oksbo%3D&md5=bb705dff9dd86f388753ff326483bf52CAS | 19111337PubMed |

Baldwin A, Egnotovich M, Ford M, Platt W (2001) Regeneration in fringe mangrove forests damaged by Hurricane Andrew. Plant Ecology 157, 151–164.
Regeneration in fringe mangrove forests damaged by Hurricane Andrew.Crossref | GoogleScholarGoogle Scholar |

Barnes CJ, Jacobson G, Smith GD (1992) The origin of high-nitrate ground waters in the Australian arid zone. Journal of Hydrology 137, 181–197.
The origin of high-nitrate ground waters in the Australian arid zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlsFOiu7o%3D&md5=a19a8c6b156b87e74e976aea3145b314CAS |

Böhlke JK, Ericksen GE, Revesz K (1997) Stable isotope evidence for an atmospheric origin of desert nitrate deposits in northern Chile and southern California, USA. Chemical Geology 136, 135–152.
Stable isotope evidence for an atmospheric origin of desert nitrate deposits in northern Chile and southern California, USA.Crossref | GoogleScholarGoogle Scholar |

Boose ER, Foster DR, Fluet M (1994) Hurricane impacts to tropical and temperate forest landscapes. Ecological Monographs 64, 369–400.
Hurricane impacts to tropical and temperate forest landscapes.Crossref | GoogleScholarGoogle Scholar |

Brunskill GJ, Orpin AR, Zagorskis I, Woolfe KJ, Ellison J (2001) Geochemistry and particle size of surface sediments of Exmouth Gulf, Northwest Shelf, Australia. Continental Shelf Research 21, 157–201.
Geochemistry and particle size of surface sediments of Exmouth Gulf, Northwest Shelf, Australia.Crossref | GoogleScholarGoogle Scholar |

Cahoon DR, Hensel P, Rybczyk J, McKee KL, Profitt CE, Perez BC (2003) Mass tree mortality leads to mangrove peat collapse at Islands, Honduras after Hurricane Mitch. Journal of Ecology 91, 1093–1105.
Mass tree mortality leads to mangrove peat collapse at Islands, Honduras after Hurricane Mitch.Crossref | GoogleScholarGoogle Scholar |

Castañeda-Moya E, Twilley RR, Rivera-Monroy VH, Zhang K, Davis SE, Ross M (2010) Sediment and nutrient deposition associated with Hurricane Wilma in mangroves of the Florida coastal everglades. Estuaries and Coasts 33, 45–58.
Sediment and nutrient deposition associated with Hurricane Wilma in mangroves of the Florida coastal everglades.Crossref | GoogleScholarGoogle Scholar |

Chapin FS III, Van Cleve K (1989) Approaches to studying nutrient uptake, use and loss in plants. In, ‘Plant physiological ecology. Field methods and instrumentation’. (Eds RW Pearcy, J Ehleringer, HA Mooney, PW Rundel) pp. 185–207. (Chapman and Hall: London)

Davis SE, Cabe JE, Childers DL, Coronado-Molina C, Day JW, Hittle CD, Madden CJ, Reyes E, Rudnick D, Sklar F (2004) Importance of storm events in controlling ecosystem structure and function in a Florida gulf coast estuary. Journal of Coastal Research 20, 1198–1208.
Importance of storm events in controlling ecosystem structure and function in a Florida gulf coast estuary.Crossref | GoogleScholarGoogle Scholar |

Day JW, Boesch DF, Clairain EG, Kemp GP, Laska SB, Mitsch WJ, Orth K, Mashriqui H, Reed DJ, Shabman L, Simenstad CA, Streever BJ, Twilley RR, Watson CC, Wells JT, Whigham DF (2007) Restoration of the Mississippi Delta, lessons from Hurricanes Katrina and Rita. Science 315, 1679–1684.
Restoration of the Mississippi Delta, lessons from Hurricanes Katrina and Rita.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjtlWnurc%3D&md5=21bd303bf7c054dfea764645620b79b9CAS | 17379799PubMed |

Downing JA, Osenberg CW, Sarnelle O (1999) Meta-analysis of marine nutrient-enrichment experiments, variation in the magnitude of nutrient limitation. Ecology 80, 1157–1167.
Meta-analysis of marine nutrient-enrichment experiments, variation in the magnitude of nutrient limitation.Crossref | GoogleScholarGoogle Scholar |

Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary production in freshwater, marine, and terrestrial ecosystems. Ecology Letters 10, 1135–1142.
Global analysis of nitrogen and phosphorus limitation of primary production in freshwater, marine, and terrestrial ecosystems.Crossref | GoogleScholarGoogle Scholar | 17922835PubMed |

Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.
Physiological mechanisms influencing plant nitrogen isotope composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFGrsr4%3D&md5=086cc848f88af22632bca6f19e22dfabCAS | 11239611PubMed |

Farquhar GD, Richards RA (1984) Isotopic composition of plant carbon correlates with water use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.
Isotopic composition of plant carbon correlates with water use efficiency of wheat genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSju7w%3D&md5=2bc86e501de53296dec1e1f4f445c720CAS |

Feller IC (1995) Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove, Rhizophora mangle. Ecological Monographs 65, 477–505.
Effects of nutrient enrichment on growth and herbivory of dwarf red mangrove, Rhizophora mangle.Crossref | GoogleScholarGoogle Scholar |

Feller IC, McKee KL, Whigham DF, O’Neill JP (2003) Nitrogen vs. phosphorus limitation across and ecotonal gradient in a mangrove forest. Biogeochemistry 62, 145–175.
Nitrogen vs. phosphorus limitation across and ecotonal gradient in a mangrove forest.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVGjtrs%3D&md5=3a6f13983c766cf10793adad37fb5ff1CAS |

Feller IC, Lovelock CE, Ball MC, Joye S, McKee KL, Berger U (2010) Biocomplexity of mangroves. Annual Review of Marine Science 2, 395–417.
Biocomplexity of mangroves.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FjvVCrtQ%3D%3D&md5=941244399c57d17fbb7129cdf649f76eCAS | 21141670PubMed |

Fry B (2006) ‘Stable isotope ecology.’ (Springer-Verlag: New York)

Handley LL, Raven JA (1992) The use of natural abundance of nitrogen isotopes in plant physiology and ecology. Plant, Cell & Environment 15, 965–985.
The use of natural abundance of nitrogen isotopes in plant physiology and ecology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvVOju74%3D&md5=8da2ec5eae4c734d5a19c4f5a13ac97fCAS |

Knutson TR, McBride JL, Chan J, Emanuel K, Holland G, Landsea C, Held I, Kossin JP, Srivastava AK, Sugi M (2010) Tropical cyclones and climate change. Nature Geoscience 3, 157–163.
Tropical cyclones and climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXisVahur4%3D&md5=a95ffd02b2f9167eecb4713b00c73043CAS |

Lin GH, Sternberg LDL (1992a) Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.). Australian Journal of Plant Physiology 19, 509–517.
Effect of growth form, salinity, nutrient and sulfide on photosynthesis, carbon isotope discrimination and growth of red mangrove (Rhizophora mangle L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXjs1Wjug%3D%3D&md5=985b66dbe8bd15e0d5a039fb8ce34d65CAS |

Lin GH, Sternberg LDL (1992b) Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L. Oecologia 90, 399–403.
Comparative study of water uptake and photosynthetic gas exchange between scrub and fringe red mangroves, Rhizophora mangle L.Crossref | GoogleScholarGoogle Scholar |

Lovelock CE, Feller IC, McKee KL, Engelbrecht BM, Ball MC (2004) The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama. Functional Ecology 18, 25–33.
The effect of nutrient enrichment on growth, photosynthesis and hydraulic conductance of dwarf mangroves in Panama.Crossref | GoogleScholarGoogle Scholar |

Lovelock CE, Ball MC, Feller IC, Engelbrecht BMJ, Ewe ML (2006) Plant function in nitrogen and phosphorus limited mangrove ecosystems. New Phytologist 172, 514–522.
Plant function in nitrogen and phosphorus limited mangrove ecosystems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1GntbrL&md5=81d40a3ac71160c9efad076fc22f09b3CAS | 17083681PubMed |

Lovelock CE, Grinham A, Adame MF, Penrose HM (2010) Elemental composition and productivity of cyanobacterial mats in an arid zone estuary in north Western Australia. Wetlands Ecology and Management 18, 37–47.
Elemental composition and productivity of cyanobacterial mats in an arid zone estuary in north Western Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlGrtw%3D%3D&md5=22a1eff7782775850390c868517615b8CAS |

Martin KC, Bruhn D, Lovelock CE, Feller IC, Evans J, Ball MC (2010) Nitrogen fertilization enhances water use efficiency in a saline environment. Plant, Cell & Environment 33, 344–357.
Nitrogen fertilization enhances water use efficiency in a saline environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFOgur0%3D&md5=71a5e3e1e610a737d1d88eb56c0bf681CAS | 19906150PubMed |

McKee KL (1993) Soil physicochemical patterns and mangrove species distribution – reciprocal effects. Journal of Ecology 81, 477–487.
Soil physicochemical patterns and mangrove species distribution – reciprocal effects.Crossref | GoogleScholarGoogle Scholar |

McKee KL, Feller IC, Popp M, Wanek W (2002) Mangrove isotopic (δ15N and δ13C) fractionation across a nitrogen versus phosphorus limitation gradient. Ecology 83, 1065–1075.

Morrisey DA, Swales A, Dittmann S, Morrison MA, Lovelock CE, Beard CM (2010) The ecology and management of temperate mangroves. Oceanography and Marine Biology: An Annual Review 48, 43–160.
The ecology and management of temperate mangroves.Crossref | GoogleScholarGoogle Scholar |

Nambiar EKS, Fife DN (1987) Growth and nutrient retranslocation in needles of radiata pine in relation to nitrogen supply. Annals of Botany 60, 147–156.

Paerl HW, Bales JD, Ausley LW, Buzzelli CP, Crowder LB, Eby LA, Fear JM, Go M, Peierls BL, Richardson TL, Ramus JS (2001) Ecosystem impacts of three sequential hurricanes (Dennis, Floyd, and Irene) on the United States’ largest lagoonal estuary, Pamlico Sound, NC. Proceedings of the National Academy of Sciences of the United States of America 98, 5655–5660.
Ecosystem impacts of three sequential hurricanes (Dennis, Floyd, and Irene) on the United States’ largest lagoonal estuary, Pamlico Sound, NC.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Wns7Y%3D&md5=0d2ae43a510105235df55fce179be8e0CAS | 11344306PubMed |

Paling EI, Kobryn HT, Humphreys G (2008) Assessing the extent of mangrove change caused by Cyclone Vance in the eastern Exmouth Gulf, northwestern Australia. Estuarine, Coastal and Shelf Science 75, 1–11.

Penn JW, Caputi N (1986) Spawning stock-recruitment relationships and environmental influences on the tiger prawn Penaeus esculentus fishery in Exmouth Gulf, Western Australia. Australian Journal of Marine and Freshwater Research 37, 491–505.
Spawning stock-recruitment relationships and environmental influences on the tiger prawn Penaeus esculentus fishery in Exmouth Gulf, Western Australia.Crossref | GoogleScholarGoogle Scholar |

Piou C, Feller IC, Berger U, Chi F (2006) Zonation patterns of Belizean offshore mangrove forests 41 years after a catastrophic hurricane. Biotropica 38, 365–374.
Zonation patterns of Belizean offshore mangrove forests 41 years after a catastrophic hurricane.Crossref | GoogleScholarGoogle Scholar |

Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape ecology and food web ecology, the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28, 289–316.
Toward an integration of landscape ecology and food web ecology, the dynamics of spatially subsidized food webs.Crossref | GoogleScholarGoogle Scholar |

Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiology 30, 1148–1160.
Nutrition of mangroves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKhtLfP&md5=b48a04ca436324c6598d3b224a6bcfecCAS | 20566581PubMed |

Ridd PV, Sandstrom MW, Wolanski E (1988) Outwelling from tropical tidal salt flats. Estuarine, Coastal and Shelf Science 26, 243–253.
Outwelling from tropical tidal salt flats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhsleitrk%3D&md5=06ebbd14798d221b1dd955edfb7e665aCAS |

Semeniuk V (1985) Development of mangrove habitats along ria coasts in north and north-western Australia. Vegetatio 60, 3–23.
Development of mangrove habitats along ria coasts in north and north-western Australia.Crossref | GoogleScholarGoogle Scholar |

Smith T, Robblee M, Wanless H, Doyle T (1994) Mangroves, hurricanes and lightning strikes. Bioscience 44, 256–262.
Mangroves, hurricanes and lightning strikes.Crossref | GoogleScholarGoogle Scholar |

Smith TJ, Anderson GH, Balentine K, Tiling G, Ward GA, Whelan KRT (2009) Cumulative impacts of hurricanes on Florida mangrove ecosystems: sediment deposition, storm surges and vegetation. Wetlands 29, 24–34.
Cumulative impacts of hurricanes on Florida mangrove ecosystems: sediment deposition, storm surges and vegetation.Crossref | GoogleScholarGoogle Scholar |

Valiela I (1995) ‘Marine ecological processes.’ 2nd edn. (Springer-Verlag: New York)

Wolanski E (2007) ‘Estuarine ecohydrology.’ (Elsevier: Amsterdam, The Netherlands)

Yasumura Y, Onoda Y, Hikosaka K, Hirose T (2005) Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecology 178, 29–37.
Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species.Crossref | GoogleScholarGoogle Scholar |