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

Nitrogen sharing and water source partitioning co-occur in estuarine wetlands

Lili Wei A B C D * , David A. Lockington B D E , Shen Yu A and Catherine E. Lovelock B C *
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China.

B National Centre for Groundwater Research and Training, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.

C School of Biological Sciences, The University of Queensland, Brisbane, St Lucia, Qld 4072, Australia.

D School of Civil Engineering, The University of Queensland, Brisbane, St Lucia, Qld 4072, Australia.

E Corresponding author. Email: d.lockington@uq.edu.au

Functional Plant Biology 42(4) 410-417 https://doi.org/10.1071/FP14141
Submitted: 17 May 2014  Accepted: 23 December 2014   Published: 12 February 2015

Abstract

Plant–plant interactions are particularly complex in multi-resource limited environments. The aim of this study was to assess species interactions in estuarine wetlands where both N and fresh water are limited. We combined stable isotope methods and dissimilarity analyses to compare interspecific interactions in N source use and water source use. Both Melaleuca quinquenervia (Cav.) S. T Blake and Avicennia marina (Forssk.) Vierh. had a lower leaf δ15N when they were growing together with the N-fixer Casuarina glauca Sieb. ex Spreng. compared with those trees growing in monospecific stands, but their water isotopes, δ18O and δD, were different from C. glauca. Our results indicate that the N-fixer C. glauca shared their N with co-existing neighbours, either indirectly or directly, but that water sources were partitioned among them. Further analyses showed that M. quinquenervia and C. glauca had lower dissimilarity in N source use but higher dissimilarity in water source use than the C. glaucaA. marina pair, implying that the co-existence between M. quinquenervia and C. glauca is relatively stable. Our results suggest that facilitative interaction and resource partitioning can co-occur in estuarine wetlands, and which could be important in maintaining diversity across resource gradients.

Additional keywords: actinorhizal plant, mangroves, paper-bark tea tree, resource partitioning, resource sharing, swamp oak.


References

Bertness MD, Callaway R (1994) Positive interactions in communities. Trends in Ecology & Evolution 9, 191–193.
Positive interactions in communities.CrossRef | 1:STN:280:DC%2BC3M7itFSntg%3D%3D&md5=93a2ff95fb84eae675f3b18cabcdec28CAS |

Boland DJ, Brooker MIH, Chippendale GM, Hall N, Hyland BPM, Johnston RD, Kleinig DA, McDonald MW, Turner JD (2006) ‘Forest trees of Australia.’ (5th edn) pp. 11. (CSIRO Publishing: Melbourne)

Brooker RW, Maestre FT, Callaway RM, Lortie CL, Cavieres LA, Kunstler G, Liancourt P, Tielbörger K, Travis JMJ, Anthelme F (2008) Facilitation in plant communities: the past, the present, and the future. Journal of Ecology 96, 18–34.

Callaway RM (1994) Facilitative and interfering effects of Arthrocnemum subterminale on winter annuals. Ecology 75, 681–686.
Facilitative and interfering effects of Arthrocnemum subterminale on winter annuals.CrossRef |

Callaway RM (1995) Positive interactions among plants. Botanical Review 61, 306–349.
Positive interactions among plants.CrossRef |

Canadell J, Jackson R, Ehleringer J, Mooney HA, Sala O, Schulze ED (1996) Maximum rooting depth of vegetation types at the global scale. Oecologia 108, 583–595.
Maximum rooting depth of vegetation types at the global scale.CrossRef |

Casper BB, Jackson RB (1997) Plant competition underground. Annual Review of Ecology and Systematics 28, 545–570.
Plant competition underground.CrossRef |

Clarke LD, Hannon NJ (1970) The mangrove swamp and salt marsh communities of the Sydney district: III. Plant growth in relation to salinity and waterlogging. Journal of Ecology 58, 351–369.
The mangrove swamp and salt marsh communities of the Sydney district: III. Plant growth in relation to salinity and waterlogging.CrossRef |

Coates KD, Lilles EB, Astrup R (2013) Competitive interactions across a soil fertility gradient in a multispecies forest. Journal of Ecology 101, 806–818.
Competitive interactions across a soil fertility gradient in a multispecies forest.CrossRef |

Coronado-Molina C, Alvarez-Guillen H, Day J, Reyes E, Perez B, Vera-Herrera F, Twilley R (2012) Litterfall dynamics in carbonate and deltaic mangrove ecosystems in the Gulf of Mexico. Wetlands Ecology and Management 20, 123–136.
Litterfall dynamics in carbonate and deltaic mangrove ecosystems in the Gulf of Mexico.CrossRef | 1:CAS:528:DC%2BC38Xkt1OrsLg%3D&md5=31b149aab8e270fe08cce9a216968620CAS |

Costanzo S, O’Donohue M, Dennison W, Loneragan N, Thomas M (2001) A new approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 42, 149–156.
A new approach for detecting and mapping sewage impacts.CrossRef | 1:CAS:528:DC%2BD3MXit1arsr4%3D&md5=71d93418d03a1e0698d01dd5857d1697CAS | 11381886PubMed |

Craig H (1961) Isotopic variations in meteoric waters. Science 133, 1702–1703.
Isotopic variations in meteoric waters.CrossRef | 1:CAS:528:DyaF3MXhtVeis7w%3D&md5=98e832ac054554aedb96d24b7bb20239CAS | 17814749PubMed |

Cramer VA, Thorburn PJ, Fraser GW (1999) Transpiration and groundwater uptake from farm forest plots of Casuarina glauca and Eucalyptus camaldulensis in saline areas of southeast Queensland, Australia. Agricultural Water Management 39, 187–204.
Transpiration and groundwater uptake from farm forest plots of Casuarina glauca and Eucalyptus camaldulensis in saline areas of southeast Queensland, Australia.CrossRef |

Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant–plant interactions. Oecologia 95, 565–574.
Hydraulic lift and water use by plants: implications for water balance, performance and plant–plant interactions.CrossRef |

Dawson TE, Ehleringer JR (1991) Streamside trees that do not use stream water. Nature 350, 335–337.
Streamside trees that do not use stream water.CrossRef |

Day J, Christian R, Boesch D, Yáñez-Arancibia A, Morris J, Twilley R, Naylor L, Schaffner L, Stevenson C (2008) Consequences of climate change on the ecogeomorphology of coastal wetlands. Estuaries and Coasts 31, 477–491.
Consequences of climate change on the ecogeomorphology of coastal wetlands.CrossRef |

Diouf D, Gherbi H, Prin Y, Franche C, Buhoux E, Bogusz D (1995) Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree. Molecular Plant-Microbe Interactions 8, 532–537.
Hairy root nodulation of Casuarina glauca: a system for the study of symbiotic gene expression in an actinorhizal tree.CrossRef | 1:CAS:528:DyaK2MXnt1ahtbs%3D&md5=590b4de08b6f7d1755ec3ed98e16a4eaCAS | 8589409PubMed |

Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant, Cell & Environment 15, 1073–1082.
Water uptake by plants: perspectives from stable isotope composition.CrossRef | 1:CAS:528:DyaK3sXhvVOktL8%3D&md5=5ab21cefc96fe2e90cdda23194af5aeeCAS |

Ellsworth PZ, Williams DG (2007) Hydrogen isotope fractionation during water uptake by woody xerophytes. Plant and Soil 291, 93–107.
Hydrogen isotope fractionation during water uptake by woody xerophytes.CrossRef | 1:CAS:528:DC%2BD2sXjsFygur4%3D&md5=8c898c691d3839ba5f22a5f911dcc8eeCAS |

Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Jacqueline TN, Eric WS, Jonathan BS, Jennifer ES (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10, 1135–1142.
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems.CrossRef | 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 | 1:CAS:528:DC%2BD3MXlsFGrsr4%3D&md5=049afcc7fd3c150fe6e01ff556896ca8CAS | 11239611PubMed |

February EC, Allsopp N, Shabane T, Hattas D (2011) Co-existence of a C4 grass and a leaf succulent shrub in an arid ecosystem. The relationship between rooting depth, water and nitrogen. Plant and Soil 349, 253–260.
Co-existence of a C4 grass and a leaf succulent shrub in an arid ecosystem. The relationship between rooting depth, water and nitrogen.CrossRef | 1:CAS:528:DC%2BC3MXhsFKntLfM&md5=cd2b71e817b173afa3b63e45f00c8d8aCAS |

Feller IC, Whigham DF, McKee KL, Lovelock CE (2003) Nitrogen limitation of growth and nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida. Oecologia 134, 405–414.
Nitrogen limitation of growth and nutrient dynamics in a disturbed mangrove forest, Indian River Lagoon, Florida.CrossRef | 12647149PubMed |

Flanagan LB, Ehleringer JR (1991) Stable isotope composition of stem and leaf water: applications to the study of plant water-use. Functional Ecology 5, 270–277.
Stable isotope composition of stem and leaf water: applications to the study of plant water-use.CrossRef |

Gómez-Guerrero A, Silva LCR, Barrera-Reyes M, Kishchuk B, Velázquez-Martínez A, Martínez-Trinidad T, Plascencia-Escalante FO, Horwath WR (2013) Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests. Global Change Biology 19, 1748–1758.
Growth decline and divergent tree ring isotopic composition (δ13C and δ18O) contradict predictions of CO2 stimulation in high altitudinal forests.CrossRef | 23504983PubMed |

Greaver TL, Sternberg LLS (2006) Linking marine resources to ecotonal shifts of water uptake by terrestrial dune vegetation. Ecology 87, 2389–2396.
Linking marine resources to ecotonal shifts of water uptake by terrestrial dune vegetation.CrossRef | 16995639PubMed |

He X, Critchley C, Ng H, Bledsoe C (2005) Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4 + or 15NO3 - supplied as ammonium nitrate. New Phytologist 167, 897–912.
Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4 + or 15NO3 - supplied as ammonium nitrate.CrossRef | 1:CAS:528:DC%2BD2MXhtVGitr%2FN&md5=2d3b5a138504736ed794899069c43ad9CAS | 16101925PubMed |

He XH, Critchley C, Nara K, Southworth D, Bledsoe CS (2009) 15N enrichment methods to quantify two-way nitrogen transfer between plants linked by mychorrhizal networks. Symbiotic Fungi 18, 285–291.
15N enrichment methods to quantify two-way nitrogen transfer between plants linked by mychorrhizal networks.CrossRef | 1:CAS:528:DC%2BC3cXitFCqs7s%3D&md5=84a147ebdee08ea910c57d856929cddfCAS |

Høgh-Jensen H, Schjoerring J (1994) Measurement of biological dinitrogen fixation in grassland: comparison of the enriched 15N dilution and the natural 15N abundance methods at different nitrogen application rates and defoliation frequencies. Plant and Soil 166, 153–163.
Measurement of biological dinitrogen fixation in grassland: comparison of the enriched 15N dilution and the natural 15N abundance methods at different nitrogen application rates and defoliation frequencies.CrossRef |

Iversen CM, Bridgham SD, Kellogg LE (2010) Scaling plant nitrogen use and uptake efficiencies in response to nutrient addition in peatlands. Ecology 91, 693–707.
Scaling plant nitrogen use and uptake efficiencies in response to nutrient addition in peatlands.CrossRef | 20426329PubMed |

Jacobsen-Lyon K, Jensen EO, Jørgensen JE, Marcker KA, Peacock WJ, Dennis ES (1995) Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. The Plant Cell 7, 213–223.
Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca.CrossRef | 1:CAS:528:DyaK2MXktVOkt74%3D&md5=a23824ed51370238e5116a2cb3d71f11CAS | 7756831PubMed |

Kuebbing SE, Nuñez MA (2014) Negative, neutral, and positive interactions among nonnative plants: patterns, processes, and management implications. Global Change Biology.
Negative, neutral, and positive interactions among nonnative plants: patterns, processes, and management implications.CrossRef | 25142018PubMed |

Le QV, Bogusz D, Gherbi H, Lappartient A, Duhoux E, Franche C (1996) Agrobacterium tumefaciens gene transfer to Casuarina glauca, a tropical nitrogen-fixing tree. Plant Science 118, 57–69.
Agrobacterium tumefaciens gene transfer to Casuarina glauca, a tropical nitrogen-fixing tree.CrossRef | 1:CAS:528:DyaK28XjsFOlsbc%3D&md5=e4b57da421d1a719001d337ef1f2fa0aCAS |

Lin G, Sternberg L, Ehleringer J, Hall A, Farquhar G (1993) Hydrogen isotopic fractionation by plant roots during water uptake in coastal wetland plants. In ‘Proceedings of the stable isotopes and plant carbon-water relations’. pp. 497–510. (Academic Press Inc.: New York)

Maestre FT, Valladares F, Reynolds JF (2005) Is the change of plant–plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments. Journal of Ecology 93, 748–757.
Is the change of plant–plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments.CrossRef |

Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. Journal of Ecology 97, 199–205.
Refining the stress-gradient hypothesis for competition and facilitation in plant communities.CrossRef |

Marcar N, Crawford D, Leppert P, Jovanovic T, Floyd R, Farrow R (1995) ‘Trees for saltland: a guide to selecting native species for Australia.’ (CSIRO Australia: Canberra)

National Research Council (1984) ‘Casuarinas: nitrogen fixing trees for adverse sites.’ (National Academy Press, Washington DC)

Nemiah Ladd SN, Sachs JP (2012) Inverse relationship between salinity and n-alkane δD values in the mangrove Avicennia marina. Organic Geochemistry 48, 25–36.
Inverse relationship between salinity and n-alkane δD values in the mangrove Avicennia marina.CrossRef | 1:CAS:528:DC%2BC38Xot1Cisrs%3D&md5=cd13c6dd14f708eeb04183a6bdd198ffCAS |

McJannet D (2008) Water table and transpiration dynamics in a seasonally inundated Melaleuca quinquenervia forest, north Queensland, Australia. Hydrological Processes 22, 3079–3090.
Water table and transpiration dynamics in a seasonally inundated Melaleuca quinquenervia forest, north Queensland, Australia.CrossRef |

Nock CA, Baker PJ, Wanek W, Leis A, Grabner M, Bunyavejchewin S, Hietz P (2011) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Global Change Biology 17, 1049–1063.
Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand.CrossRef |

Passarge J, Hol S, Escher M, Huisman J (2006) Competition for nutrient and light: stable co-existence, alternative stable states, or competitive exclusion? Ecological Monographs 76, 57–72.
Competition for nutrient and light: stable co-existence, alternative stable states, or competitive exclusion?CrossRef |

Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant and Soil 229, 235–243.
Root exudates: a pathway for short-term N transfer from clover and ryegrass.CrossRef | 1:CAS:528:DC%2BD3MXit1ejsr4%3D&md5=e44b20480124a65c0cb553f3c656d397CAS |

Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136, 261–269.
Source partitioning using stable isotopes: coping with too many sources.CrossRef | 12759813PubMed |

Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144, 520–527.
Combining sources in stable isotope mixing models: alternative methods.CrossRef | 15711995PubMed |

Pons TL, Perreijn K, Kessel CV, Werger MJA (2007) Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment. New Phytologist 173, 154–167.
Symbiotic nitrogen fixation in a tropical rainforest: 15N natural abundance measurements supported by experimental isotopic enrichment.CrossRef | 1:CAS:528:DC%2BD2sXht1ant7g%3D&md5=87eb53f1a7f5b30c02accd57804072dbCAS | 17176402PubMed |

Richards AE, Forrester DI, Bauhus J, Scherer-Lorenzen M (2010) The influence of mixed tree plantations on the nutrition of individual species: a review. Tree Physiology 30, 1192–1208.
The influence of mixed tree plantations on the nutrition of individual species: a review.CrossRef | 20472645PubMed |

Rivera-Monroy VH, Twilley RR, Davis SE, Childers DL, Simard M, Chambers R, Jaffe R, Boyer JN, Rudnick DT, Zhang K, Castañeda-Moya E, Ewe SML, Price RM, Coronado-Molina C, Ross M, Smith TJ, Michot B, Meselhe E, Nuttle W, Troxler TG, Noe GB (2011) The role of the Everglades Mangrove Ecotone Region (EMER) in regulating nutrient cycling and wetland productivity in South Florida. Critical Reviews in Environmental Science and Technology 41, 633–669.
The role of the Everglades Mangrove Ecotone Region (EMER) in regulating nutrient cycling and wetland productivity in South Florida.CrossRef | 1:CAS:528:DC%2BC3MXit1aqt7Y%3D&md5=d15781f7778e5ab1cd0b644d36362a1fCAS |

Roggy JC, Prévost MF, Gourbiere F, Casabianca H, Garbaye J, Domenach AM (1999) Leaf natural 15N abundance and total N concentration as potential indicators of plant N nutrition in legumes and pioneer species in a rain forest of French Guiana. Oecologia 120, 171–182.
Leaf natural 15N abundance and total N concentration as potential indicators of plant N nutrition in legumes and pioneer species in a rain forest of French Guiana.CrossRef |

Rossatto DR, Silva LCR, Villalobos-Vega R, Sternberg LSL, Franco AC (2012) Depth of water uptake in woody plants relates to groundwater level and vegetation structure along a topographic gradient in a neotropical savanna. Environmental and Experimental Botany 77, 259–266.
Depth of water uptake in woody plants relates to groundwater level and vegetation structure along a topographic gradient in a neotropical savanna.CrossRef |

Rossatto DR, Silvab LCR, Sternbergc LSL, Francod AC (2014) Do woody and herbaceous species compete for soil water across topographic gradients? Evidence for niche partitioning in a neotropical savanna. South African Journal of Botany 91, 14–18.
Do woody and herbaceous species compete for soil water across topographic gradients? Evidence for niche partitioning in a neotropical savanna.CrossRef |

Saha AK, Sternberg LSL, Miralles-Wilhelm F (2009) Linking water sources with foliar nutrient status in upland plant communities in the Everglades National Park, USA. Ecohydrology 2, 42–54.
Linking water sources with foliar nutrient status in upland plant communities in the Everglades National Park, USA.CrossRef | 1:CAS:528:DC%2BD1MXksFartLk%3D&md5=d23461c4685bd2f19972951b020da33eCAS |

Saha AK, Sternberg LSL, Ross MS, Miralles-Wilhelm F (2010) Water source utilization and foliar nutrient status differs between upland and flooded plant communities in wetland tree islands. Wetlands Ecology and Management 18, 343–355.
Water source utilization and foliar nutrient status differs between upland and flooded plant communities in wetland tree islands.CrossRef |

Silvertown J (2004) Plant co-existence and the niche. Trends in Ecology & Evolution 19, 605–611.
Plant co-existence and the niche.CrossRef |

Sternberg LSL, Swart PK (1987) Utilization of freshwater and ocean water by coastal plants of southern Florida. Ecology 68, 1898–1905.
Utilization of freshwater and ocean water by coastal plants of southern Florida.CrossRef |

Sternberg LSL, Ish-Shalom-Gordon N, Ross M, O’Brien J (1991) Water relations of coastal plant communities near the ocean/freshwater boundary. Oecologia 88, 305–310.
Water relations of coastal plant communities near the ocean/freshwater boundary.CrossRef |

Sun D, Dickinson GR (1995) Survival and growth responses of a number of Australian tree species planted on a saline site in tropical north Australia. Journal of Applied Ecology 32, 817–826.
Survival and growth responses of a number of Australian tree species planted on a saline site in tropical north Australia.CrossRef |

Tamooh F, Huxham M, Karachi M, Mencuccini M, Kairo J, Kirui B (2008) Below-ground root yield and distribution in natural and replanted mangrove forests at Gazi bay, Kenya. Forest Ecology and Management 256, 1290–1297.
Below-ground root yield and distribution in natural and replanted mangrove forests at Gazi bay, Kenya.CrossRef |

van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. Journal of Ecology 97, 1139–1150.
Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems.CrossRef |

Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115.
Nitrogen limitation on land and in the sea: how can it occur?CrossRef |

Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57, 1–45.
Towards an ecological understanding of biological nitrogen fixation.CrossRef |

Watt MS, Kriticos DJ, Manning LK (2009) The current and future potential distribution of Melaleuca quinquenervia. Weed Research 49, 381–390.
The current and future potential distribution of Melaleuca quinquenervia.CrossRef |

Wei L, Lockington DA, Poh SC, Gasparon M, Lovelock CE (2013) Water use patterns of estuarine vegetation in a tidal creek system. Oecologia 172, 485–494.
Water use patterns of estuarine vegetation in a tidal creek system.CrossRef | 23070143PubMed |

Wulff F, Eyre BD, Johnstone R (2011) Nitrogen versus phosphorus limitation in a subtropical coastal embayment (Moreton Bay, Australia): implications for management. Ecological Modelling 222, 120–130.
Nitrogen versus phosphorus limitation in a subtropical coastal embayment (Moreton Bay, Australia): implications for management.CrossRef | 1:CAS:528:DC%2BC3cXhtlynt7jP&md5=29e9e514c508908f4991b2f71bec020eCAS |



Rent Article (via Deepdyve) Export Citation Cited By (2)