Environmental biology of fishes, tập 90, số 1, 2011

Environ Biol Fish (2011) 90:117 DOI 10.1007/s10641-010-9706-x Allochthonous and autochthonous carbon sources for fish in floodplain lagoons of an Australian dryland river Elvio S F Medeiros & Angela H Arthington Received: 14 January 2010 / Accepted: August 2010 / Published online: 10 September 2010 # Springer Science+Business Media B.V 2010 Abstract Dryland rivers associated with arid and semi-arid land areas offer an opportunity to explore food web concepts and models of energy sources in systems that experience unpredictable flooding and long dry spells This study investigated the sources of energy supporting three species of fish feeding at different trophic levels within floodplain lagoons of the Macintyre River in the headwaters of the MurrayDarling river system, Australia Stable isotope analyses revealed that fish consumers derived, on average, 46.9% of their biomass from zooplankton, 38.1% from Coarse Particulate Organic Matter (CPOM) and 24.0% from algae Ambassis agassizii derived on average 57.6% of its biomass carbon from zooplankton and 20.427.8% from algae or CPOM Leiopotherapon unicolor derived most of its carbon from zooplankton and CPOM (38.339.5%), with relatively high contributions from algae compared to the other species (33.3%) An average of 48.4% of the biomass of Nematalosa erebi was derived from zooplankton, with CPOM contributing another 38.1% Zooplankton was the most important source of organic carbon supporting all three fish species in floodplain lagoons Phytoplankton, and possibly, particulate organic matter in the seston, are the most likely energy sources for the planktonic suspension feeders (zooplankton) and, consequently, the fish that feed on them These results indicate a stronger dependence of consumers on autochthonous sources and on locally produced organic matter from the riparian zone (i.e., the Riverine Productivity Model), than on other resources Keywords Fish Food web Stable isotopes Riverine Productivity Model E S F Medeiros : A H Arthington Australian Rivers Institute and eWater Cooperative Research Centre, Griffith University, Nathan QLD 4111, Australia Present Address: E S F Medeiros (*) Centro de Ciờncias Biolúgicas e Sociais Aplicadas, Universidade Estadual da ParaớbaUEPB, Campus V Av Monsenhor Walfredo Leal, no 487, Tambiỏ CEP 58020-540 Joóo PessoaPB, Brazil e-mail: elviomedeiros@uepb.edu.br Introduction Food webs in freshwaters can be supported from bottom detritus and/or primary production in the pelagic zone In many river systems, the detrital food chain is considered more important, based largely on the delivery of allochthonous materials from headwaters and/or the decomposition of aquatic macrophytes (the River Continuum Concept, RCC; Vannote et al 1980) This model argues that downstream communities are adapted to capitalize on upstream processing inefficiencies (leakage), therefore, emphasizing the influence of nutrients and organic matter from upstream processes on the structure and function of lowland reaches However, food webs in large floodplain rivers can be fueled by terrestrial inputs and organic matter delivered laterally from floodplains (the Flood Pulse Concept; Junk et al 1989) During floods, aquatic organisms migrate to the floodplain and exploit the newly available habitats and their resources, whereas, as floodwaters recede, nutrients and newly produced animal biomass are returned to the main river channel In both models, strong reliance on allochthonous inputs has been emphasized Other studies suggest that autochthonous primary production is an important, often major, contributor to metazoan production in rivers (Thorp and Delong 2002; Bunn et al 2006) For example, studies on the Orinoco River and its floodplain showed that phytoplankton and periphyton were the main carbon sources for invertebrates and fish (Lewis et al 2000; Lewis et al 2001) Similarly, Araujo-Lima et al (1986) showed that detritivorous fish in the Amazon River floodplain, despite feeding mostly on detritus, derived most of their carbon from phytoplankton production Nevertheless, these studies were developed in tropical and temperate river systems with predictable flooding patters and low flow variability (Puckridge et al 1998) Dryland rivers offer an opportunity to explore food web concepts in systems that experience far less predictable flooding patterns than mesic floodplain rivers In the arid regions of Australia, dryland rivers feature extensive floodplains and a network of anabranching tributaries that provide a vast terrestrial-water interface (Walker et al 1995; Bunn et al 2003), but for most of the time these systems exist as disconnected and highly turbid waterholes and floodplain lagoons (Bunn and Davies 1999) During seasonal or extended dry periods these isolated waterbodies act as refugia for obligate aquatic organisms such as fish (Morton et al 1995; Bunn and Davies 1999; Arthington et al 2005) When flooding is resumed, fish left in isolated waterholes are able to colonize new habitats and resources opened up on the floodplain, and when floods recede, fish return again to isolated waterholes It is of interest to know how fish are sustained in these remnant waterholes and what energy sources support individuals that may recolonize the river floodplain and channel network when flooding is resumed (Winemiller 1996; Burford et al 2008) Environ Biol Fish (2011) 90:117 Fish consumers in Australian dryland floodplain rivers use a range of trophic resources for nutrition, including algae, aquatic invertebrates and zooplankton (Balcombe et al 2005) In Cooper Creek, a large arid-zone floodplain river in western Queensland (Australia), aquatic consumers have been shown to derive most of their carbon from algae growing in a bathtub ring around the shallow littoral zone of channel waterholes and floodplain lagoons (Bunn and Davies 1999; Bunn et al 2003) This dependency on algae suggests the Riverine Productivity Model (RPM, Thorp and Delong 1994) as a more relevant model for these dryland rivers than the Flood Pulse Concept (FPC) The RPM highlights the importance of local in-stream production by phytoplankton, benthic algae and/or aquatic plants and suggests that the role of autochthonous sources has been underestimated in previous models and assessments of food webs in large river systems (Thorp and Delong 1994) An integrated model that synthesizes the above mentioned views and their corollaries into an heuristic approach for riverine ecosystems (the Riverine Ecosystem Synthesis, RES) is proposed by Thorp et al (2006) According to the RES, algal production is the primary source of organic energy fueling aquatic metazoan food webs in the floodplain of riverine systems during flooding Nevertheless, this model also recognizes the importance of allochthonous organic matter to some species and in seasons when interaction between riparian vegetation and the aquatic environment is at its maximum Like those of Cooper Creek, isolated waterbodies on the floodplains of the Macintyre River in the headwaters of the Murray-Darling river system are highly turbid (Houldsworth 1995; Medeiros 2005) The production of aquatic plants and algae in this system is likely to be limited by low light availability and by the absence of water flow and associated nutrient pulses during dry periods Given these constraints on primary production in turbid waterbodies, we hypothesize that fish consumers in the Macintyre River are dependent on allochthonous organic carbon during dry periods, that is, carbon derived from riparian vegetation To test this hypothesis, we used stable isotope techniques to investigate the importance of a range of energy sources to three fish species feeding at different trophic levels, the olive perchlet Ambassis agassizii Steindachner, 1867 (microcarnivore), spangled perch Leiopotherapon unicolor (Gỹnther, 1859) (omnivore) and bony bream Environ Biol Fish (2011) 90:117 Nematalosa erebi (Gỹnther, 1868) (algivore/detritivore) (Pusey et al 2004; Medeiros and Arthington 2008a; Medeiros and Arthington 2008b) In this paper we document the types and origin of energy sources and their relative importance in supporting the three species of fish in floodplain lagoons of the Macintyre River Specifically, we assess the importance of allochthonous versus autochthonous carbon sources in light of the current models proposed (RCC, FPC, RPM) to explain energy flow in large river systems Materials and methods Study area This study was conducted on the floodplain of the Macintyre River, a dryland river in the Border Rivers catchment, located along the southern Queensland and northern New South Wales border and comprising a major portion of the headwaters of the Barwon and Darling River systems (McCosker 1996) (Fig 1) In the study area, a number of streams diverge from the Macintyre River in the vicinity of the towns of Boggabilla and Goondiwindi (DWR 1995) where the river passes through a relatively well-defined floodplain containing numerous intermittent and semi-permanent billabongs on prior river channels (see McCosker 1996; Medeiros 2005 for further details) The study period (20022003) was relatively dry compared to previous years, with average discharges of the Macintyre River between 780 and 845 megaliters per day (MLãday1) (data from the Boggabilla gauging station416002) Major to moderate floods occurred early and late in 2001, however only minor to moderate floods were recorded for the study period, with mean discharges of 14487 MLãday1 on 31 March 2002 and 17412 MLãday1 on 26 February 2003 (Fig 2) Mean water levels rose up to m during the 2002 flood and 4.6 m during the 2003 flood Even though such floods may cause inundation of low lying areas adjacent to the main river channel, they were not sufficient to inundate all study sites Study design Seven study sites, including six floodplain lagoons and one site in the main channel of the Macintyre River (Fig 1) were sampled on three occasions in 20022003 The first sampling event took place in the dry season of 2002, that is, early in the summer of that year (2031 October) The second sampling event occurred near the end of the 20022003 summer, soon after the wet season (1020 March 2003), when some of the study sites experienced minor flooding The third sampling event occurred in the winter of 2003 (1525 July), during the dry season During the study period, two of the six lagoons were flooded (South Callandoon East and Rainbow lagoons, see Fig 1) and one dried up completely (Broomfield Lagoon) The remaining sites, Serpentine, Punbougal and Maynes lagoons, decreased in size and volume continuously throughout the study period but did not dry up completely (Medeiros 2005) Collection of primary sources and consumers Major primary sources of terrestrial and aquatic origin were collected from each study site on each sampling occasion Fallen leaves from major riparian trees (mostly Eucalyptus spp.) were collected by hand from the margins Benthic detritus was collected with dip and hand nets and wet-sieved in the field into coarse (>1 mm to cm) particulate organic matter (CPOM) Samples of algae (Rhizoclonium sp and Cladophora sp.) were taken from the shallow littoral margins both directly off the mud surface and from submerged wood or rocks, and washed in the field to remove any associated organic debris Because of the high levels of suspended sediment and the presence of unidentified particulate matter in the water, it was not possible to take clean samples of phytoplankton Zooplankton (calanoids and cladocerans) was sampled at dusk and dawn by towing a 250 m plankton net just below the surface of the water The three species of fish were sampled by hauling a seine net along the littoral zone of the study sites Where possible, three replicate samples of each of the potential food sources and consumers and five replicate fish samples were collected from different areas of habitat in each lagoon All animal and plant samples were immediately refrigerated, frozen within four hours of collection and stored frozen prior to processing for stable isotope analysis Environ Biol Fish (2011) 90:117 Border Rivers catchment QLD NT Brisbane SA NSW Sydney VIC N Broomfield Lg Goondiwindi South Callandoon Lg East Serpentine Lg Goondiwindi Weir River site Boggabilla Boggabilla Weir Rainbow Lg Morella Watercourse Macintyre River Punbougal Lg Maynes Lg km Flow Fig Location of the lagoons studied in the floodplain of the Macintyre River and the Border Rivers catchment within the MurrayDarling River system Sample preparation In the laboratory, primary carbon sources (tree leaves, particulate organic matter and algae) were rinsed in distilled water, and, in the case of algae, any remaining organic debris was removed All samples were oven-dried at 60C for 36 to 48 h and then ground to a powder-like consistency in a ring grinder For each of the zooplankton samples collected, half was treated in 10% HCl for approximately two hours to remove carbonates from exoskeletons in preparation for 13C analysis The remaining half of the sample was not treated in acid and was used for 15N analysis (after Bunn et al 1995) Samples of muscle tissue were taken from individuals of each fish species, from the region above the lateral line and adjacent to the dorsal fin (after the fish was scaled and skinned) Stable isotope signatures were analyzed from single individuals of the three study species All animal samples were oven-dried at 60C for 24 to 48 h and then ground by hand with a mortar and pestle Lipids were not removed from tissue samples Dried and ground samples were oxidized at high temperature and the resultant CO2 and N2 were analyzed for percentage C, N and stable isotope ratios using a continuous-flow isotope-ratio mass spectrometer (Europa Tracermass and Roboprep, Crewe, England) at the Stable Isotope Analysis laboratory at Griffith University Ratios of 13C/12C and 15 N/14 N Environ Biol Fish (2011) 90:117 90000 2001 2002 2003 80000 Discharge (ML/day) 70000 60000 30 Nov 01 50000 40000 30000 20000 26 Feb 03 31 Mar 02 10000 wet dry Jan/01 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan/02 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan/03 Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec late dry Month Fig Daily discharge (MLãday ) in the Macintyre River (recorded at the Boggabilla gauging station416002) between 2001 and 2003 Arrows indicate sampling occasions Dates of flooding events during the study period are also indicated were expressed as the relative per million () difference between the sample and the conventional standards (PeeDee Belemnite carbonate and N2 in air) as follows: X() = Rsample Rs tan dard Rs tan dard ì 1000 where Xẳ 13 C or 15 N and Rẳ13 C =12 C or 15 N=14 N: Measurement precision of the mass spectrometer was approximately 0.1 for 13C/12C and 0.3 for 15 N/14 N Data analysis Data were first analyzed using the stable isotope values of sources and consumers for each sampling occasion and site The significance of differences among sites and sampling occasions were tested using simple ANOVA (Zar 1999) followed by post-hoc multiple comparisons using Tukeys HSD test (significance level of 0.05) Pearson correlations between 13C and 15N signatures of the three species of fish were used to add weight to mixing model results The contribution of the more abundant primary sources to the biomass of fish was calculated using the two- and three-source linear mixing models of Phillips and Gregg (2001) The two-source mixing model was based on 13C signatures of zooplankton and either organic matter (CPOM) or algae, depending upon which was collected Where all three major sources were available, the three-source linear mixing model was based on 13C and 15N signatures of zooplankton, algae and organic matter (CPOM) (Phillips 2001; Phillips and Gregg 2001) For three-source mixing models, when the isotopic signatures for the mixture fall outside the region constrained by the source isotopic signatures, negative source proportions and variances may result, therefore yielding an unfeasible solution In such cases, the contribution of the more abundant primary sources to the biomass of fish was calculated using the twosource linear mixing model of carbon signatures of the two sources closest to the consumer This adjustment is mentioned where appropriate Field studies generally find a carbon enrichment of to and to for nitrogen, for each increase in trophic level (Peterson and Fry 1987) To account for fractionation, to 2.5 per trophic level from the nitrogen isotopic signature of the fish was added to 15N values of food sources, and for 13C an adjustment of 0.10.3 per trophic level was made (DeNiro and Epstein 1981; France 1996; Vander Zanden and Rasmussen 2001; Bunn et al 2003) For the mixing models only, algal 13C and 15N values for Rainbow Lagoon in October 2002 were estimated from algae values from South Callandoon Lagoon on the same sampling occasion, as both sites had similar algal composition and it was not possible to separate algae from benthic detritus collected from Rainbow Lagoon on that occasion Results Primary sources Algae were significantly more 13C enriched than all other primary sources (ANOVA, df=2,153; F=65.3; p[...]... salinity on the chemotaxis of glass eels, Anguilla anguilla, to organic earthy and green odorants Environ Biol Fish 47:213–218 Sorensen PW, Bianchini ML (1986) Environmental correlates of the freshwater migration of elvers of the American eel in a Rhode Island Brook Trans Am Fish Soc 115:258–268 Sorenson PW (1986) Origins of the freshwater attractants of migrating elvers of the American eel, Anguilla... values of consumers and sources of carbon (Hein et al 2003) This lack of connectivity of floodplain lagoons with the Macintyre River may have had an affect on nutrient inputs and levels over time, leading to the overall absence of strong temporal patterns of isotope values for both sources and consumers In general, fish had relatively similar δ13C isotopic signatures, indicating similar sources of organic... organic matter, were an important source of organic carbon for fish consumers, it would be expected that the variability in isotopic signatures of 11 these sources would track the variability in signatures of fish in space and time That is, the isotopic signatures of each of the three species of fish should be positively correlated with the isotopic signatures of their food source across sampling occasions... the major source of energy for zooplankton Huryn et al (2001) found significant temporal changes in isotopic signatures in several size classes of seston and argued that such changes were the result of changes in the ratio of terrestrial to aquatic (phytoplankton) sources of organic carbon related to seasonal changes in water flow This could explain the variations in isotopic signatures of zooplankton... combination of zooplankton (and, presumably, ultimately phytoplankton) and organic matter of riparian origin as their main energy sources (cf Pusey et al 2004) In that case, the integration of RPM into the broader RES model would better represent the sources of carbon for fish in isolated floodplain lagoons of the Macintyre catchment Predictions from the RES would also suggest Environ Biol Fish (2011) 90:1–17... neighborhood window size of 5% of the sample size; sparse data points were interpolated within this window using a Gaussian weighting function Thus, the interpolation smoothed the response surface across environmental predictors We sought the most parsimonious model that maximized the amount of variance explained in CPUE or %P with the fewest number of predictors The number of predictors allowed in... upstream migration of glass eels in New Zealand: implications of climate change Environ Biol Fish 81:195–205 Baker SM, Mann R (1992) Effects of hypoxia and anoxia on larval settlement, juvenile growth, and juvenile survival of the oyster Crassostrea virginica Biol Bull 182:265–269 Bonhommeau S, Chassot E, Planque B, Rivot E, Knap AH, Pape OL (2008) Impact of climate on eel populations of the northern... and activity of juvenile Japanese eels in relation to temperature and fish size J Fish Biol 63:152–165 Edeline E, Dufour S, Elie P (2005) Role of glass eel salinity preference in the control of habitat selection and growth Environ Biol Fish (2011) 90:19–27 plasticity in Anguilla anguilla Mar Ecol Prog Ser 304:191–199 Facey DE, Van Den Avyle MJ (1987) Species profiles: life histories and environmental. .. fish consumers, explaining only 6% of the variation in δ13C for N erebi and less than 1% of A agassizii and L unicolor (Fig 3) Contribution of autochthonous versus allochthonous sources of carbon to consumer biomass Estimates derived from mixing models for study sites where zooplankton was present suggest an important contribution of zooplankton carbon to the biomass of fish consumers (Table 4) Averaged... Sola C, Tongiorgi P (1990) Relation of water odour, salinity, and temperature to ascent of glasseels, Anguilla anguilla (L.): a laboratory study J Fish Biol 36:327–340 Wang CH, Tzeng WN (2000) The timing of metamorphosis and growth rates of American and European eel leptocephali: A mechanism of larval segregative migration Fish Res 46:191–205 Environ Biol Fish (2011) 90:29–41 DOI 10.1007/s10641-010-9714-x