Abstract
δ13C was used to identify seasonal variations in the importance of autochthonous and allochthonous sources of productivity for fish communities in intermittently connected estuarine areas of Australia’s dry tropics. A total of 224 fish from 38 species were collected from six intermittently connected estuarine pools, three in central Queensland (two dominated by C3 forest and one by C4 pasture) and three in north Queensland (one dominated by C3 and two by C4 vegetation). Samples were collected before and after the wet season. Fish collected in the two forested areas in central Queensland had the lowest δ13C, suggesting a greater incorporation of C3 terrestrial material. A seasonal variation in δ13C was also detected for these areas, with mean δ13C varying from −20 to −23‰ from the pre- to the post-wet season, indicating a greater incorporation of terrestrial carbon after the wet season. Negative seasonal shifts in fish δ13C were also present at the pasture site, suggesting a greater dependence on carbon of riparian vegetation (C3 Juncus sp.) in the post-wet season. In north Queensland, terrestrial carbon seemed to be incorporated by fish in the two C4 areas, as δ13C of most species shifted towards slightly heavier values in the post-wet season. A two-source, one-isotope mixing model also indicated a greater incorporation of carbon of terrestrial origin in the post-wet season. However, no seasonal differences in δ13C were detected for fish from the forested area of north Queensland. Overall, hydrologic connectivity seemed to be a key factor in regulating the ultimate sources of carbon in these areas. It is therefore important to preserve the surrounding habitats and to maintain the hydrologic regimes as close to natural conditions as possible, for the conservation of the ecological functioning of these areas.
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References
Bayley PB (1995) Understanding large river-floodplain ecosystems. Bioscience 45:153–158
Boon PI, Bunn SE (1994) Variations in the stable isotope composition of aquatic plants and their implications for food web analysis. Aquat Bot 48:99–108
Boston HL, Hill WR (1991) Photosynthesis-light relations of stream periphyton communities. Limnol Oceanogr 36:644–656
Bouillon S, Mohan PC, Sreenivas N, Dehairs F (2000) Sources of suspended organic matter and selective feeding by zooplankton in an estuarine mangrove ecosystem as traced by stable isotopes. Mar Ecol Prog Ser 208:79–92
Bouillon S, Connolly R, Lee SY (2008) Organic matter exchange and cycling in mangrove ecosystems: recent insights from stable isotope studies. J Sea Res 59:44–58
Bunn SE, Arthington AH (2002) Basic principles and ecological consequences of altered flow regimes for aquatic biodiversity. Environ Manage 30:492–507
Carpenter SR, Cole JJ, Pace ML, Van De Bogert M, Bade DL, Bastviken D, Gille CM, Hodgson JR, Kitchell JF, Kritzberg ES (2005) Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86:2737–2750
Childers DL, Boyer JN, Davis SE, Madden CJ, Rudnick DT, Sklar FH (2006) Relating precipitation and water management to nutrient concentrations in the oligotrophic “upside-down” estuaries of the Florida Everglades. Limnol Oceanogr 51:602–616
Clapcott JE, Bunn SE (2003) Can C4 plants contribute to aquatic food webs of subtropical streams? Freshw Biol 48:1105–1116
Cloern JE, Alpine AE, Cole BE, Wong RLJ, Arthur JF, Ball MD (1983) River discharge controls phytoplankton dynamics in the northern San Francisco Bay estuary. Est Coast Shelf Sci 16:415–429
Cole JJ, Carpenter SR, Kitchell JF, Pace ML (2002) Pathways of organic C utilization in small lakes: results from a whole-lake 13C addition and coupled model. Limnol Oceanogr 47:1664–1675
De’ath G, Fabricius KE (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 81:3178–3192
DeNiro MJ, Epstein S (1977) A mechanism of carbon isotope fractionation associated with lipid synthesis. Science 197:261–263
Doi H (2009) Spatial patterns of autochthonous and allochthonous resources in aquatic food webs. Popul Ecol 51:57–64
Douglas MM, Bunn SE, Davies PM (2005) River and wetland food webs in Australia’s wet-dry tropics: general principles and implications for management. Mar Freshw Res 56:329–342
Eyre B (1998) Transport, retention and transformation of material in Australian estuaries. Estuaries 21:540–551
Finlayson B, McMahon T (1988) Australia vs. the world: a comparative analysis of stream flow characteristics. In: Werner RF (ed) Fluvial geomorphology of Australia. Academic Press, Sydney
France RL (1996) Scope for use of stable carbon isotopes in discerning the incorporation of forest detritus into aquatic foodwebs. Hydrobiologia 325:219–222
France RL (1997) Stable carbon and nitrogen isotopic evidence for ecotonal coupling between boreal forests and fishes. Ecol Freshw Fish 6:78–83
Freeman MC, Bowen ZH, Bovee KD, Irwin ER (2001) Flow and habitat effects on juvenile fish abundance in natural and altered flow regimes. Ecol Appl 11:179–190
Fry B, Arnold C (1982) Rapid 13C/12C turnover during growth of brown shrimp (Penaeus aztecus). Oecologia 54:200–204
Gelin A, Crivelli A, Rosecchi E, Kerambrun P (2001) Can salinity changes affect reproductive success in the brown shrimp Crangon crangon? J Crustac Biol 21:905–911
Gorokhova E, Hansson S (1999) An experimental study on variations in stable carbon and nitrogen fractionation during growth of Mysis mixta and Neomysis integer. Can J Fish Aquat Sci 56:2203–2210
Grange N, Whitfield AK, de Villiers CJ, Allanson BR (2000) The response of two South African east coast estuaries to altered river flow regimes. Aquat Conserv: Mar Freshw Ecosyst 10:155–177
Guest MA, Connolly RM, Loneragan RL (2004) Within and among-site variability in δ13C and δ15N for three estuarine producers, Sporobolus virginicus, Zostera capricorni, and epiphytes of Z. capricorni. Aquat Bot 79:87–94
Hein T, Baranyi C, Herndl GJ, Wanek W, Schiemer F (2003) Allochthonous and autochthonous particulate organic matter in floodplains of the River Danube: the importance of hydrological connectivity. Freshw Biol 48:220–232
Herwig BR, Soluk DA, Dettmers JM, Wahl DH (2004) Trophic structure and energy flow in backwater lakes of two large floodplain rivers assessed using stable isotopes. Can J Fish Aquat Sci 61:12–22
Hesslein RH, Halard KA, Ramlal P (1993) Replacement of sulfur, carbon and nitrogen in tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S, δ13C, and δ15N. Can J Fish Aquat Sci 50:2071–2076
Huryn AD, Riley RH, Young RG, Arbuckle CJ, Peacock K, Lyon G (2001) Temporal shift in contribution of terrestrial organic matter to consumer production in a grassland river. Freshw Biol 46:213–226
Jaywardane PAAT, MacLusky DS, Tytler P (2002) Factors influencing migration of Penaeus indicus in the Negombo lagoon on the west coast of Sri Lanka. Fisheries Manag Ecol 9:351–363
Johnston R, Sheaves M (2006) Tropical fisheries ecology of urban waterways: part B—Curralea and Paradise Lakes. Report prepared for Townsville City Council, North Queensland Water and Twin Cities Fish Stocking Society, Townsville, 16 pp
Junk W, Bayley P, Sparks R (1989) The flood pulse concept in river-floodplain system. Spec Publ Can J Fish Aquat Sci 106:110–127
Loneragan NR, Bunn SE (1999) River flows and estuarine ecosystems: implications for coastal fisheries from a review and a case study of the Logan River, southeast Queensland. Aust Ecol 24:431–440
MacAvoy SE, Macki SA, Garman GC (2001) Isotopic turnover in aquatic predators: quantifying the exploitation of migratory prey. Can J Fish Aquat Sci 58:923–932
Mallin MA, Paerl HW, Rudek J, Bates PW (1993) Regulation of estuarine primary production by watershed rainfall and river flow. Mar Ecol Prog Ser 93:199–203
Marczak LB, Thompson RM, Richardson JS (2007) Meta analysis: trophic level, habitat, and productivity shape the food web effects of resource subsidies. Ecology 88:140–148
McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering Sea. Mar Biol 53:257–262
McCulloch M, Cappo M, Aumend J, Müller W (2005) Tracing the life history of individual barramundi using laser-ablation MC-ICP-MS Sr-isotopic and Sr/Ba ratios in otoliths. Mar Freshw Res 56:637–644
McCutchan JH, Lewis WM Jr, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378–390
McMahon TA, Finlayson B, Haines A, Srikanthan R (1992) Global runoff: continental comparisons of annual flows and peak discharges. Catena Verlag, Cremlingen-Destedt
Michener WK, Blood ER, Bildstein KL, Brinson MM, Gardner LR (1997) Climate change, hurricanes and tropical storms, and rising sea level in coastal wetlands. Ecol Appl 7:770–801
Pace ML, Cole JJ, Carpenter SR, Kitchell JF, Hodgson JR, Van De Bogert MC, Bade DL, Kritzberg ES, Bastviken D (2004) Whole-lake carbon-13 additions reveal terrestrial support of aquatic food webs. Nature 427:240–243
Peterson B, Howarth RW (1987) Sulfur, carbon and nitrogen isotopes used to trace organic matter flow in the salt-marsh estuaries of Sapelo Island, Georgia. Limnol Oceanogr 32:1195–1213
Phillips DL, Gregg JW (2001) Uncertainty in source partitioning using stable isotopes. Oecologia 127:171–179
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231
Polis GA, Anderson WB, Holt RD (1997) Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316
Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montanã CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189
Rounick JS, Winterbourn MJ, Lyon GL (1982) Differential utilization of allochthonous and autochthonous inputs by aquatic invertebrates in some New Zealand streams: a stable carbon isotope study. Oikos 39:191–198
Russell DJ, Garrett RN (1983) Use by juvenile barramundi, Lates calcarifer (Bloch), and other fishes of temporal supralittoral habitats in a tropical estuary in Northern Australia. Aust J Mar Freshw Res 34:805–811
Russell D, Garrett R (1985) Early life history of barramundi, Lates calcarifer (Bloch), in north-eastern Queensland. Aust J Mar Freshw Res 36:191–201
Russell DJ, McDougall AJ (2005) Movement and juvenile recruitment of mangrove jack, Lutjanus argentimaculatus (Forsskål), in Northern Australia. Mar Freshw Res 56:465–475
Scheirs J, Bruyn LD, Verhagen R (2001) A test of the C3–C4 hypothesis with two grass miners. Ecology 82:410–421
Sheaves M, Johnston R (2006) The physical nature of Fitzroy floodplain wetland pools. In: Sheaves M, Collins JM, Houston W, Dale P, Revill A, Johnston R, Abrantes K (eds) Contribution of floodplain wetland pools to the ecological functioning of the Fitzroy River estuary. Cooperative Research Centre for Coastal, Estuary and Waterway Management, Brisbane
Sheaves M, Johnston R (2008) Influence of marine and freshwater connectivity on the dynamics of subtropical estuarine wetland fish metapopulations. Mar Ecol Prog Ser 357:225–243
Sheaves M, Revill A, Abrantes K, Johnston R (2006) Trophic support of Fitzroy wetland pool ecosystems. In: Sheaves M, Collins J, Houston W, Dale P, Revill A, Johnston R, Abrantes K (eds) Contribution of floodplain wetland pools to the ecological functioning of the Fitzroy River estuary. Cooperative Research Centre for Coastal, Estuary and Waterway Management, Brisbane
Sheaves M, Brodie J, Brooke B, Dale P, Lovelock C, Waycott M, Gehrke P, Johnston R, Baker R (2007a) Chapter 19—vulnerability of coastal and estuarine habitats in the Great Barrier Reef to climate change. In: Johnson JE, Marshall PA (eds) Climate change and the Barrier Reef: a vulnerability assessment. Great Barrier Reef Marine Park Authority and Australian Greenhouse Office, Australia
Sheaves M, Johnston R, Abrantes K (2007b) Fish fauna of dry tropical and subtropical estuarine floodplain wetlands. Mar Freshw Res 58:931–943
Sklar FH, Browder JA (1998) Coastal environmental impacts brought about by alterations to freshwater flow in the Gulf of Mexico. Environ Manage 22:547–562
Sweeting CJ, Polunin NVC, Jennings S (2006) Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun Mass Spectrom 20:595–601
Thorp J, Delong M (1994) The riverine productivity model: an heuristic view of carbon sources and organic processing in large river ecosystems. Oikos 70:305–308
Thorp JH, Delong MD, Greenwood KS, Casper AF (1998) Isotopic analysis of three food web theories in constricted and floodplain regions of a large river. Oecologia 117:551–563
Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–38
Vörösmarty CJ, Green P, Salisbury J, Lammers RB (2000) Global water resources: vulnerability from climate change and population growth. Science 289:284–288
Wantzen KM, Machado FA, Voss M, Boriss H, Junk WJ (2002) Seasonal isotopic shifts in fish of the Pantanal wetland, Brazil. Aquat Sci 64:239–251
Ward JV, Tockner K, Schiemer F (1999) Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regul Rivers Res Mgmt 15:125–139
Wilson JR, Hacker JB (1987) Comparative digestibility and anatomy of some sympatric C3 and C4 arid zone grasses. Aust J Agr Res 38:287–295
Wilson JR, Hattersley PW (1989) Anatomical characteristics and digestibility of leaves of Panicum and other grass genera with C3 and different types of C4 photosynthetic pathway. Aust J Agr Res 40:125–136
Yokoyama H, Tamaki A, Harada K, Shimoda K, Koyama K, Ishihi Y (2005) Variability of diet-tissue isotopic fractionation in estuarine macrobenthos. Mar Ecol Prog Ser 296:115–128
Acknowledgments
We thank R. Johnston, A. Penny and R. Baker for field assistance, and A. Revill and R. Diocares for the analyses of stable isotope samples. We would also like to thank the three anonymous reviewers for their comments, which significantly improved the quality of this manuscript. This work was supported by the Cooperative Research Centre for Coastal Zone, Estuary and Waterway Management, CSIRO Marine Research Laboratories and the Townsville City Council, and was part of K.A’s PhD funded by the Foundation for Science and Technology, Portugal. All research procedures reported comply with the current Australian law and received the approval from the Animal Ethics Committee, James Cook University (Ethics Approval A852_03).
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Abrantes, K.G., Sheaves, M. Importance of freshwater flow in terrestrial–aquatic energetic connectivity in intermittently connected estuaries of tropical Australia. Mar Biol 157, 2071–2086 (2010). https://doi.org/10.1007/s00227-010-1475-8
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DOI: https://doi.org/10.1007/s00227-010-1475-8