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Environmental problems - Chemical approaches
RESEARCH ARTICLE

Proteins are a major component of dissolved organic nitrogen (DON) leached from terrestrially aged Eucalyptus camaldulensis leaves

Clayton W. Harris A E , Ewen Silvester A , Gavin N. Rees B , John Pengelly B and Ljiljana Puskar C D
+ Author Affiliations
- Author Affiliations

A Department of Ecology, Environment and Evolution, La Trobe University, Wodonga, Vic. 3690, Australia.

B Murray–Darling Freshwater Research Centre and CSIRO Land and Water, Wodonga, Vic. 3690, Australia.

C The Australian Synchrotron, Clayton, Vic. 3168, Australia.

D Present address: Methods for Material Development, Helmholtz-Zentrum für Materialien und Energie GmbH, Berlin 12489, Germany.

E Corresponding author. Email: clayton.harris@latrobe.edu.au

Environmental Chemistry 13(5) 877-887 https://doi.org/10.1071/EN16005
Submitted: 12 January 2016  Accepted: 18 May 2016   Published: 4 July 2016

Environmental context. Dissolved organic nitrogen often constitutes the largest portion of the dissolved nitrogen pool yet is a commonly overlooked nutrient source in aquatic systems. Terrestrially aged Eucalyptus camaldulensis, a common lowland leaf litter species, rapidly released proteinaceous dissolved organic nitrogen during the first 24 h of leaching. The results indicate that terrestrial leaf litter may play an important role in satisfying nutrient demand within aquatic systems through both direct deposition and floodplain interactions.

Abstract. Understanding sources and forms of dissolved nitrogen is of critical importance to the management of aquatic systems worldwide. Dissolved organic nitrogen (DON) often constitutes the largest portion of the dissolved nitrogen pool, yet is commonly overlooked as a nutrient source to aquatic food webs, likely owing to its bound nature within organic material and the non-specific methods by which it is measured. In this study, we determined the protein and peptide (dissolved combined amino acid (DCAA)) contribution to DON leached from Eucalyptus camaldulensis leaves over 24 h. The distribution of proteinaceous material in unleached and leached leaves was characterised using Fourier-transform infrared (FTIR) microspectroscopy to determine the likely source of DCAA within the leaf tissue. DCAAs were found to be a significant component (38.5 %) of the leached DON; however, >90 % of the leaf protein remained in the leaves after 24 h. FTIR microspectroscopy shows that proteinaceous material is strongly partitioned to fungal colonised palisade cells in the leaf mesophyll, with evidence for depletion of this material after leaching. Comparison of leaching kinetics in the presence and absence of a microbial inhibitor (sodium azide) suggests that microbial uptake or adsorption commences within the timescales of these leaching experiments. The work shows that DON in the form of peptides and proteins leached from leaf litter is a likely source of bioavailable nutrients to in-stream and floodplain systems.

Additional keywords: amino acids, FTIR spectroscopy, leaf leachate, red gum leaves.


References

[1]  P. S. Giller, B. Malmqvist, The Biology of Streams and Rivers 1998 (Oxford University Press: Oxford).

[2]  P. M. Vitousek, J. R. Gosz, C. C. Grier, J. M. Melillo, W. A. Reiners, R. L. Todd, Nitrate losses from disturbed ecosystems. Science 1979, 204, 469.
Nitrate losses from disturbed ecosystems.CrossRef | 1:CAS:528:DyaE1MXktVCmsrc%3D&md5=690504a4edfa0a30fba8fd669a791f26CAS | 17819936PubMed | open url image1

[3]  R. W. Howarth, Nutrient limitation of net primary production in marine ecosystems. Annu. Rev. Ecol. Syst. 1988, 19, 89.
Nutrient limitation of net primary production in marine ecosystems.CrossRef | open url image1

[4]  S. P. Seitzinger, Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol. Oceanogr. 1988, 33, 702.
Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance.CrossRef | 1:CAS:528:DyaL1cXlslGktbY%3D&md5=d9f54b1caf472d13e2bc09aeffede39fCAS | open url image1

[5]  J. L. Campbell, J. W. Hornbeck, W. H. McDowell, D. C. Buso, J. B. Shanley, G. E. Likens, Dissolved organic nitrogen budgets for upland, forested ecosystems in New England. Biogeochemistry 2000, 49, 123.
Dissolved organic nitrogen budgets for upland, forested ecosystems in New England.CrossRef | 1:CAS:528:DC%2BD3cXis1yjt7g%3D&md5=504e084e771513f01227a0a1fb961397CAS | open url image1

[6]  E. H. Stanley, J. T. Maxted, Changes in the dissolved nitrogen pool across land-cover gradients in Wisconsin streams. Ecol. Appl. 2008, 18, 1579.
Changes in the dissolved nitrogen pool across land-cover gradients in Wisconsin streams.CrossRef | 18839755PubMed | open url image1

[7]  R. A. Martin, J. A. Harrison, Effect of high-flow events on in-stream dissolved organic nitrogen concentration. Ecosystems 2011, 14, 1328.
Effect of high-flow events on in-stream dissolved organic nitrogen concentration.CrossRef | 1:CAS:528:DC%2BC3MXhsFaitL%2FJ&md5=378299db66a116a91f47602aef4469e2CAS | open url image1

[8]  S. S. Kaushal, W. M. Lewis, Patterns in the chemical fractionation of organic nitrogen in Rocky Mountain streams. Ecosystems 2003, 6, 483.
Patterns in the chemical fractionation of organic nitrogen in Rocky Mountain streams.CrossRef | 1:CAS:528:DC%2BD3sXotVemsL0%3D&md5=75892ad5b18ebe584b3a303ff4b76536CAS | open url image1

[9]  R. Stepanauskas, Differential dissolved organic nitrogen availability and bacterial aminopeptidase activity in limnic and marine waters. Microb. Ecol. 1999, 38, 264.
Differential dissolved organic nitrogen availability and bacterial aminopeptidase activity in limnic and marine waters.CrossRef | 1:CAS:528:DyaK1MXnslyqtL0%3D&md5=43d1cf99e5a32a7c1e210720dbffeda5CAS | 10541788PubMed | open url image1

[10]  T. A. Frankovich, R. D. Jones, A rapid, precise and sensitive method for the determination of total nitrogen in natural waters. Mar. Chem. 1998, 60, 227.
A rapid, precise and sensitive method for the determination of total nitrogen in natural waters.CrossRef | 1:CAS:528:DyaK1cXivVWgsLs%3D&md5=21b55f0fbd14f3fac5f9c59706a10988CAS | open url image1

[11]  S. Seitzinger, R. Sanders, Contribution of dissolved organic nitrogen from rivers to estuarine eutrophication. Mar. Ecol. Prog. Ser. 1997, 159, 1.
Contribution of dissolved organic nitrogen from rivers to estuarine eutrophication.CrossRef | 1:CAS:528:DyaK1cXjsVersw%3D%3D&md5=921adea3026b14c4fd1a26fad1cc0711CAS | open url image1

[12]  S. P. Seitzinger, R. V. Styles, E. W. Boyer, R. B. Alexander, G. Billen, R. W. Howarth, B. Mayer, N. Van Breemen, Nitrogen retention in rivers: model development and application to watersheds in the north-eastern US. Biogeochemistry 2002, 57, 199.
Nitrogen retention in rivers: model development and application to watersheds in the north-eastern US.CrossRef | open url image1

[13]  E. N. J. Brookshire, H. M. Valett, S. A. Thomas, J. R. Webster, Coupled cycling of dissolved organic nitrogen and carbon in a forest stream. Ecology 2005, 86, 2487.
Coupled cycling of dissolved organic nitrogen and carbon in a forest stream.CrossRef | open url image1

[14]  D. S. Baldwin, A. Mitchell, The effects of drying and reflooding on the sediment and soil nutrient dynamics of lowland river–floodplain systems: a synthesis. Regul. Rivers Res. Manage. 2000, 16, 457.
The effects of drying and reflooding on the sediment and soil nutrient dynamics of lowland river–floodplain systems: a synthesis.CrossRef | open url image1

[15]  A. Boulton, Eucalypt leaf decomposition in an intermittent stream in south-eastern Australia. Hydrobiologia 1991, 211, 123.
Eucalypt leaf decomposition in an intermittent stream in south-eastern Australia.CrossRef | open url image1

[16]  S. Briggs, M. Maher, Litter fall and leaf decomposition in a river red gum (Eucalyptus camaldulensis) swamp. Aust. J. Bot. 1983, 31, 307.
Litter fall and leaf decomposition in a river red gum (Eucalyptus camaldulensis) swamp.CrossRef | 1:CAS:528:DyaL3sXks12msLw%3D&md5=a1dc7d7427c40c65773e79409daea243CAS | open url image1

[17]  J. L. Meyer, J. B. Wallace, S. L. Eggert, Leaf litter as a source of dissolved organic carbon in streams. Ecosystems 1998, 1, 240.
Leaf litter as a source of dissolved organic carbon in streams.CrossRef | 1:CAS:528:DC%2BD3cXptFehsw%3D%3D&md5=52414583c0621f88e14f33bf7b3f2448CAS | open url image1

[18]  M. Witkamp, J. Van der Drift, Breakdown of forest litter in relation to environmental factors. Plant Soil 1961, 15, 295.
Breakdown of forest litter in relation to environmental factors.CrossRef | 1:CAS:528:DyaF3sXmvFGmtA%3D%3D&md5=09ad97152171212dfede7da2d69a5c12CAS | open url image1

[19]  M. O’Connell, D. S. Baldwin, A. I. Robertson, G. Rees, Release and bioavailability of dissolved organic matter from floodplain litter: influence of origin and oxygen levels. Freshw. Biol. 2000, 45, 333.
Release and bioavailability of dissolved organic matter from floodplain litter: influence of origin and oxygen levels.CrossRef | 1:CAS:528:DC%2BD3cXos1Omu7g%3D&md5=4ef74f7176873b78e30c9cb824bc4c98CAS | open url image1

[20]  T. Riutta, E. M. Slade, D. P. Bebber, M. E. Taylor, Y. Malhi, P. Riordan, D. W. Macdonald, M. D. Morecroft, Experimental evidence for the interacting effects of forest edge, moisture and soil macrofauna on leaf litter decomposition. Soil Biol. Biochem. 2012, 49, 124.
Experimental evidence for the interacting effects of forest edge, moisture and soil macrofauna on leaf litter decomposition.CrossRef | 1:CAS:528:DC%2BC38Xlt1Oku7s%3D&md5=ae6750972133b80fbcef0406d2b0fe93CAS | open url image1

[21]  J. P. Schimel, J. M. Gulledge, J. S. Clein-Curley, J. E. Lindstrom, J. F. Braddock, Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biol. Biochem. 1999, 31, 831.
Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga.CrossRef | 1:CAS:528:DyaK1MXjtFSrsL4%3D&md5=38b76a715c983e18bd17581e6ffa702fCAS | open url image1

[22]  D. S. Baldwin, Dissolved organic matter and phosphorus leached from fresh and ‘terrestrially’ aged river red gum leaves: implications for assessing river–floodplain interactions. Freshw. Biol. 1999, 41, 675.
Dissolved organic matter and phosphorus leached from fresh and ‘terrestrially’ aged river red gum leaves: implications for assessing river–floodplain interactions.CrossRef | 1:CAS:528:DyaK1MXlslKjtLg%3D&md5=2dc3a9bb0836a68eb892c4d22dcc0157CAS | open url image1

[23]  M. Hosomi, R. Sudo, Simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulfate digestion. Int. J. Environ. Stud. 1986, 27, 267.
Simultaneous determination of total nitrogen and total phosphorus in freshwater samples using persulfate digestion.CrossRef | 1:CAS:528:DyaL28XlvFKrtbc%3D&md5=b012e3b7e58606f891efe0862d6a1275CAS | open url image1

[24]  N. O. G. Jørgensen, R. E. Jensen, Determination of dissolved combined amino acids using microwave-assisted hydrolysis and HPLC precolumn derivatization for labeling of primary and secondary amines. Mar. Chem. 1997, 57, 287.
Determination of dissolved combined amino acids using microwave-assisted hydrolysis and HPLC precolumn derivatization for labeling of primary and secondary amines.CrossRef | open url image1

[25]  M. Fountoulakis, H.-W. Lahm, Hydrolysis and amino acid composition analysis of proteins. J. Chromatogr. A 1998, 826, 109.
Hydrolysis and amino acid composition analysis of proteins.CrossRef | 1:CAS:528:DyaK1MXjsFah&md5=876bf27ed9b64e0ae11a3a203b2abcc7CAS | 9917165PubMed | open url image1

[26]  A. Tsugita, T. Uchida, H.W. Mewes, T. Ataka, A rapid vapor-phase acid (hydrochloric acid and trifluoroacetic acid) hydrolysis of peptide and protein. J. Biochem. 1987, 102, 1593.
| 1:CAS:528:DyaL1cXjsVCksg%3D%3D&md5=2b3ccafa68579f0a4b001c761dde6ff8CAS | 2834350PubMed | open url image1

[27]  J. C. Anders, B. F. Parten, G. E. Petrie, R. L. Marlowe, J. E. McEntire, Using amino acid analysis to determine absorptivity constants. Biopharm Int. 2003, 2, 30. open url image1

[28]  M. Manneberg, H.-W. Lahm, M. Fountoulakis, Oxidation of cysteine and methionine residues during acid hydrolysis of proteins in the presence of sodium azide. Anal. Biochem. 1995, 224, 122.
Oxidation of cysteine and methionine residues during acid hydrolysis of proteins in the presence of sodium azide.CrossRef | 1:CAS:528:DyaK2MXjtFOrsrw%3D&md5=d81965da311dcd5f69f2cf44f00a66b1CAS | 7710058PubMed | open url image1

[29]  P. Heraud, S. Caine, G. Sanson, R. Gleadow, B. R. Wood, D. McNaughton, Focal plane array infrared imaging: a new way to analyse leaf tissue. New Phytol. 2007, 173, 216.
Focal plane array infrared imaging: a new way to analyse leaf tissue.CrossRef | 17176407PubMed | open url image1

[30]  F. Bärlocher, Leaf-eating invertebrates as competitors of aquatic hyphomycetes. Oecologia 1980, 47, 303.
Leaf-eating invertebrates as competitors of aquatic hyphomycetes.CrossRef | open url image1

[31]  J. L. Kerr, D. S. Baldwin, M. J. Tobin, L. Puskar, P. Kappen, G. N. Rees, E. Silvester, High-spatial-resolution infrared microspectroscopy reveals the mechanism of leaf lignin decomposition by aquatic fungi. PLoS One 2013, 8, e60857.
High-spatial-resolution infrared microspectroscopy reveals the mechanism of leaf lignin decomposition by aquatic fungi.CrossRef | 1:CAS:528:DC%2BC3sXmtlSgsLc%3D&md5=c1f2b4540da11ce8dae3f8c052f6e051CAS | 23577169PubMed | open url image1

[32]  A. Leck, Preparation of lactophenol cotton blue slide mounts. Community Eye Health 1999, 12, 24.
| 1:STN:280:DC%2BD2s3osVCgsg%3D%3D&md5=f4c72223a49c94d60308a201eaac70d2CAS | 17491984PubMed | open url image1

[33]  J. Kong, S. Yu, Fourier-transform infrared spectroscopic analysis of protein secondary structures. Acta Biochim. Biophys. Sin. 2007, 39, 549.
Fourier-transform infrared spectroscopic analysis of protein secondary structures.CrossRef | 1:CAS:528:DC%2BD2sXhtFSks7bP&md5=fcf7c5a7e8ae390d73beb6390c243bebCAS | 17687489PubMed | open url image1

[34]  R. M. Silverstein, G. C. Bassler, Spectrometric identification of organic compounds. J. Chem. Educ. 1962, 39, 546.
Spectrometric identification of organic compounds.CrossRef | 1:CAS:528:DyaF3sXls1ak&md5=98d43286e5383d08155181d48fbb7798CAS | open url image1

[35]  M. Anderson, R. N. Gorley, R. K. Clarke, Permanova+ for Primer: Guide to Software and Statistical Methods 2008 (Plymouth, UK).

[36]  W. H. Press, B. P. Flannery, S. A. Teukolsky, W. T. Vetterling, Numerical Recipes 1990 (Cambridge University Press: Cambridge, UK).

[37]  H. Susi, D. M. Byler, Protein structure by Fourier-transform infrared spectroscopy: second-derivative spectra. Biochem. Biophys. Res. Commun. 1983, 115, 391.
Protein structure by Fourier-transform infrared spectroscopy: second-derivative spectra.CrossRef | 1:CAS:528:DyaL3sXltFyisrc%3D&md5=b6f84d2b61448a54e24148d27fd7be58CAS | 6615537PubMed | open url image1

[38]  Y. Noishiki, H. Takami, Y. Nishiyama, M. Wada, S. Okada, S. Kuga, Alkali-induced conversion of β-chitin to α-chitin. Biomacromolecules 2003, 4, 896.
Alkali-induced conversion of β-chitin to α-chitin.CrossRef | 1:CAS:528:DC%2BD3sXjs12qsb0%3D&md5=56614d0e7bd0f24ecb935bbabe9f0f2eCAS | 12857070PubMed | open url image1

[39]  R. G. Wetzel, B. A. Manny, Decomposition of dissolved organic carbon and nitrogen compounds from leaves in an experimental hard-water stream. Limnol. Oceanogr. 1972, 17, 927.
Decomposition of dissolved organic carbon and nitrogen compounds from leaves in an experimental hard-water stream.CrossRef | 1:CAS:528:DyaE3sXhtFGju74%3D&md5=8cfddf08919866dce5d5ab71d7554c59CAS | open url image1

[40]  T. A. Wallace, G. G. Ganf, J. D. Brookes, A comparison of phosphorus and DOC leachates from different types of leaf litter in an urban environment. Freshw. Biol. 2008, 53, 1902.
A comparison of phosphorus and DOC leachates from different types of leaf litter in an urban environment.CrossRef | 1:CAS:528:DC%2BD1cXhtFKisLnF&md5=a0006b459460c74cb7d9dd9c9df90eceCAS | open url image1

[41]  C. Francis, F. Sheldon, River red gum (Eucalyptus camaldulensis Dehnh.) organic matter as a carbon source in the lower Darling River, Australia. Hydrobiologia 2002, 481, 113.
River red gum (Eucalyptus camaldulensis Dehnh.) organic matter as a carbon source in the lower Darling River, Australia.CrossRef | 1:CAS:528:DC%2BD38XovFShuro%3D&md5=ae8016bab9090dc99639ad2355830335CAS | open url image1

[42]  C. Corrigan, M. Oelbermann, Mass and nutrient loss of leaf litter collecting in littertraps: an in situ and ex situ study. For. Sci. 2013, 59, 484.
Mass and nutrient loss of leaf litter collecting in littertraps: an in situ and ex situ study.CrossRef | open url image1

[43]  G. L. Cowie, J. I. Hedges, Sources and reactivities of amino acids in a coastal marine environment. Limnol. Oceanogr. 1992, 37, 703.
Sources and reactivities of amino acids in a coastal marine environment.CrossRef | 1:CAS:528:DyaK38XmsFOltr4%3D&md5=21edce0049d066cb304909b22a7dd580CAS | open url image1

[44]  M. O. Gessner, E. Chauvet, M. Dobson, A perspective on leaf litter breakdown in streams. Oikos 1999, 85, 377.
A perspective on leaf litter breakdown in streams.CrossRef | open url image1

[45]  J. B. Fellman, K. Petrone, P. Grierson, Leaf litter age, chemical quality, and photodegradation control the fate of leachate dissolved organic matter in a dryland river. J. Arid Environ. 2013, 89, 30.
Leaf litter age, chemical quality, and photodegradation control the fate of leachate dissolved organic matter in a dryland river.CrossRef | open url image1

[46]  R. L. Nicholson, L. G. Butler, T. N. Asquith, Glycoproteins from Colletotrichum graminicola that bind phenols: implications for survival and virulence of phytopathogenic fungi. Phytopathology 1986, 76, 1315.
Glycoproteins from Colletotrichum graminicola that bind phenols: implications for survival and virulence of phytopathogenic fungi.CrossRef | 1:CAS:528:DyaL2sXhtFKnsLw%3D&md5=75d25a4a70ba89e0c2a9b4696ad539fbCAS | open url image1

[47]  J. F. Staab, C. A. Ferrer, P. Sundstrom, Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces of Candida albicans. J. Biol. Chem. 1996, 271, 6298.
Developmental expression of a tandemly repeated, proline-and glutamine-rich amino acid motif on hyphal surfaces of Candida albicans.CrossRef | 1:CAS:528:DyaK28XhslGgtbk%3D&md5=78e1f489449ca036782547383e5c8975CAS | 8626424PubMed | open url image1

[48]  L. W. Janson, M. E. Tischler, The Big Picture: Medical Biochemistry 2012 (McGraw-Hill Medical: Chicago, IL).

[49]  T. Berman, D. A. Bronk, Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquat. Microb. Ecol. 2003, 31, 279.
Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems.CrossRef | open url image1

[50]  A. Fioretto, C. Di Nardo, S. Papa, A. Fuggi, Lignin and cellulose degradation and nitrogen dynamics during decomposition of three leaf litter species in a Mediterranean ecosystem. Soil Biol. Biochem. 2005, 37, 1083.
Lignin and cellulose degradation and nitrogen dynamics during decomposition of three leaf litter species in a Mediterranean ecosystem.CrossRef | 1:CAS:528:DC%2BD2MXisFGrtbg%3D&md5=8f7ecb746eb08c0a9111e5dafdb8f341CAS | open url image1

[51]  S. M. Armstrong, F. Bärlocher, Adsorption and release of amino acids from epilithic biofilms in streams. Freshw. Biol. 1989, 22, 153.
Adsorption and release of amino acids from epilithic biofilms in streams.CrossRef | 1:CAS:528:DyaK3cXht1CltrY%3D&md5=533f5eedc78c371ec99dfe11fffe6cd6CAS | open url image1

[52]  S. Armstrong, F. Bärlocher, Adsorption of three amino acids to biofilms on glass beads. Arch. Hydrobiol. 1989, 115, 391.
| 1:CAS:528:DyaL1MXksFaksbo%3D&md5=6bbce0278fed5bab3f42c9c7cf4bb943CAS | open url image1

[53]  W. E. Hillis, Polyphenols in the leaves of eucalyptus l’herit: a chemotaxonomic survey – I: introduction and a study of the series globulares. Phytochemistry 1966, 5, 1075.
Polyphenols in the leaves of eucalyptus l’herit: a chemotaxonomic survey – I: introduction and a study of the series globulares.CrossRef | 1:CAS:528:DyaF2sXlt12gtQ%3D%3D&md5=d3e96c3576e214dfd6de9943cf460b79CAS | open url image1

[54]  C. Canhoto, M. Graça, Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus. Microb. Ecol. 1999, 37, 163.
Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus.CrossRef | 10227874PubMed | open url image1

[55]  C. Canhoto, M. A. Graça, Leaf litter processing in low-order streams. Limnetica 2006, 25, 1. open url image1

[56]  L. Chapuis-Lardy, D. Contour-Ansel, F. Bernhard-Reversat, High-performance liquid chromatography of water-soluble phenolics in leaf litter of three Eucalyptus hybrids (Congo). Plant Sci. 2002, 163, 217.
High-performance liquid chromatography of water-soluble phenolics in leaf litter of three Eucalyptus hybrids (Congo).CrossRef | 1:CAS:528:DC%2BD38XmtVWntLc%3D&md5=d0308bad8c796a61a6719cdec737854bCAS | open url image1

[57]  W. L. Hadwen, C. S. Fellows, D. P. Westhorpe, G. N. Rees, S. M. Mitrovic, B. Taylor, D. S. Baldwin, E. Silvester, R. Croome, Longitudinal trends in river functioning: patterns of nutrient and carbon processing in three Australian rivers. River Res. Appl. 2010, 26, 1129.
Longitudinal trends in river functioning: patterns of nutrient and carbon processing in three Australian rivers.CrossRef | open url image1

[58]  W. J. Junk, P. B. Bayley, R. E. Sparks, The flood pulse concept in river–floodplain systems. Can. Spec. Publ. Fish. Aquat. Sci. 1989, 106, 110. open url image1



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