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With the collaboration of: Research

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Water for a Healthy Country

Trophodynamics

of the Coorong

Spatial variability in food web structure along a

hypersaline coastal lagoon

B.M. Deegan, S. Lamontagne, K.T. Aldridge

& J.D. Brookes

March 2010

Trophodynamics of the Coorong i

Water for a Healthy Country

Trophodynamics

of the Coorong

Spatial variability in food web structure along a

hypersaline coastal lagoon

B.M. Deegan1,*, S. Lamontagne2, K.T. Aldridge1

& J.D. Brookes1

1School of Earth and Environmental Sciences, The University of Adelaide, Adelaide SA 5005, Australia 2CSIRO Land and Water and Water for a Healthy Country Research Flagship, PMB 2, Glen Osmond SA 5064, Australia

*Corresponding author: [email protected]

March 2010

Trophodynamics of the Coorong ii

Water for a Healthy Country Flagship Report series ISSN: 1835-095X

ISBN: 978 0 643 09771 1

The Water for a Healthy Country National Research Flagship is a research partnership between CSIRO, state and Australian governments, private and public industry and other research providers. The Flagship aims to achieve a tenfold increase in the economic, social and environmental benefits from water by 2025.

The Australian Government, through the Collaboration Fund, provides $97M over seven years to the National Research Flagships to further enhance collaboration between CSIRO, Australian universities and other publicly funded research agencies, enabling the skills of the wider research community to be applied to the major national challenges targeted by the Flagships initiative.

© Commonwealth of Australia 2010 All rights reserved. This work is copyright. Apart from any use as permitted under the Copyright Act 1968, no part may be reproduced by any process without prior written permission from the Commonwealth.

Citation: Deegan, B. M., Lamontagne, S., Aldridge, K.T. and Brookes, J.D. (2010). Trophodynamics of the Coorong. Spatial variability in food web structure along a hypersaline coastal lagoon. CSIRO: Water for a Healthy Country National Research Flagship.

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Trophodynamics of the Coorong iii

Foreword

The environmental assets of the Coorong, Lower Lakes and Murray Mouth (CLLAMM) region in South Australia are currently under threat as a result of ongoing changes in the hydrological regime of the River Murray, at the end of the Murray-Darling Basin. While a number of initiatives are underway to halt or reverse this environmental decline, rehabilitation efforts are hampered by the lack of knowledge about the links between flows and ecological responses in the system.

The CLLAMM program is a collaborative research effort that aims to produce a decision-support framework for environmental flow management for the CLLAMM region. This involves research to understand the links between the key ecosystem drivers for the region (such as water level and salinity) and key ecological processes (generation of bird habitat, fish recruitment, etc). A second step involves the development of tools to predict how ecological communities will respond to manipulations of the “management levers” for environmental flows in the region. These levers include flow releases from upstream reservoirs, the Lower Lakes barrages, and the Upper South-East Drainage scheme, and dredging of the Murray Mouth. The framework aims to evaluate the environmental trade-offs for different scenarios of manipulation of management levers, as well as different future climate scenarios for the Murray-Darling Basin.

One of the most challenging tasks in the development of the framework is predicting the response of ecological communities to future changes in environmental conditions in the CLLAMM region. The CLLAMMecology Research Cluster is a partnership between CSIRO, the University of Adelaide, Flinders University and SARDI Aquatic Sciences that is supported through CSIRO’s Flagship Collaboration Fund. CLLAMMecology brings together a range in skills in theoretical and applied ecology with the aim to produce a new generation of ecological response models for the CLLAMM region.

This report is part of a series summarising the output from the CLLAMMecology Research Cluster. Previous reports and additional information about the program can be found at http://www.csiro.au/partnerships/CLLAMMecologyCluster.html

Trophodynamics of the Coorong iv

Table of Contents

Table of Contents.................................. ...................................................................................iv Acknowledgements ................................... ..............................................................................vi Executive Summary.................................. ..............................................................................vii Introduction to the CLLAMMecology food web studies. .......................................................ix 1. The influence of a salinity gradient on the baselin e isotopic signature of a semi-arid coastal lagoon food web ............................ ..............................................................................1

1.1. Introduction.................................................................................................................................. 1 1.2. Methods....................................................................................................................................... 2

1.2.1. Selection of Study sites........................................................................................................... 2 1.2.2. Sampling of targeted primary consumers ............................................................................... 3 1.2.3. Sample preparation and analysis: .......................................................................................... 4 1.2.4. Water sample analysis............................................................................................................ 4 1.2.5. Determination of δ34S-SO4

2– ................................................................................................... 4 1.3. Results......................................................................................................................................... 5

1.3.1. Salinity trends.......................................................................................................................... 5 1.3.2. δ

34S-SO42– ............................................................................................................................... 5

1.3.3. Primary consumers isotope signatures along the salinity gradient......................................... 5 1.3.4. Primary consumers isotope signatures along a depth gradient.............................................. 8

1.4. Discussion ................................................................................................................................... 9 1.4.1. Review of the hydrodynamic and biogeochemical properties of the Coorong lagoons.......... 9 1.4.2. Possible mechanisms driving the shifts in baseline isotopic signature ................................ 10

1.5. Conclusion................................................................................................................................. 11 2. Food web structure leading to large fish along the Coorong salinity gradient ...........12

2.1. Introduction................................................................................................................................ 12 2.2. Methods..................................................................................................................................... 13

2.2.1. Selection of study sites ......................................................................................................... 13 2.2.2. Sampling protocol and collection of organisms .................................................................... 13 2.2.3. Sample preparation and analysis.......................................................................................... 14 2.2.4. Analysis and modelling of trophic position............................................................................ 14 2.2.5. Modelling feasible source mixtures to explain fish diet......................................................... 15

2.3. Results....................................................................................................................................... 15 2.3.1. Food web structure and trophic guilds.................................................................................. 15 2.3.2. Estimation of trophic position ................................................................................................ 22 2.3.3. Modelling estimation of fish diet............................................................................................ 24

2.4. Discussion ................................................................................................................................. 26 2.4.1. Fish diet and trophic position in the Coorong based on SIA................................................. 26 2.4.2. Smallmouth hardyhead distribution ...................................................................................... 27 2.4.3. Predatory invertebrates......................................................................................................... 28 2.4.4. Ontogenic diet shifts in yelloweye mullet and mulloway....................................................... 28

2.5. Conclusion................................................................................................................................. 28 3. Fish diet and preferred foraging areas in the Cooro ng inferred from stable isotope analysis ........................................... ........................................................................................30

3.1. Introduction................................................................................................................................ 30 3.2. Methods..................................................................................................................................... 30

3.2.1. Selection of Study sites......................................................................................................... 30 3.2.2. Sampling protocol and collection of organisms .................................................................... 31 3.2.3. Sample preparation and analysis.......................................................................................... 31 3.2.4. Modelling feasible source mixtures to explain fish diet......................................................... 31

3.3. Results....................................................................................................................................... 31 3.3.1. Gut contents.......................................................................................................................... 31 3.3.2. Modelled feasible source mixtures to explain fish diet ......................................................... 31

3.4. Discussion ................................................................................................................................. 43 3.5. Conclusion................................................................................................................................. 44

General Conclusion ................................. ...............................................................................45

Trophodynamics of the Coorong v

References ......................................... .....................................................................................47

Trophodynamics of the Coorong vi

Acknowledgements

This research was supported by the CSIRO Flagship Collaboration Fund and represents a collaboration between CSIRO, the University of Adelaide, Flinders University and SARDI Aquatic Sciences.

We also acknowledge the contribution of several other funding agencies to the CLLAMM program and the CLLAMMecology Research Cluster, including Land & Water Australia, the Fisheries Research and Development Corporation, SA Water, the Murray Darling Basin Commission’s (now the Murrray-Darling Basin Authority) Living Murray program and the SA Murray-Darling Basin Natural Resources Management Board. Other research partners include Geoscience Australia, the WA Centre for Water Research, and the Flinders Research Centre for Coastal and Catchment Environments. The objectives of this program have been endorsed by the SA Department of Environment and Heritage, SA Department of Water, Land and Biodiversity Conservation, SA Murray-Darling Basin NRM Board and Murray-Darling Basin Commission.

We thank Julie Francis, Alex Payne and Trevor Aldridge for assistance with sample preparation as part of the stable isotope analysis, and the CLLAMM Ecology steering committee for their insightful development of the research program and support.

Trophodynamics of the Coorong vii

Executive Summary

Food webs attempt to describe how energy is transferred across an ecosystem, in other words, to describe “who eats what”. Because of its significance as a feeding ground for fish and waterbirds, it is important to understand what food webs are present in the Coorong and how they could change following management intervention. As a component of CLLAMMecology, the food webs leading to large fish (yelloweye mullet [Aldrichetta forsteri], black bream [Acanthopagrus butcheri], greenback flounder [Rhombosolea tapirina] and mulloway [Argyrosomus hololepidotus]) along the Coorong salinity gradient were evaluated using fish stomach content analysis and stable isotope analysis (SIA) for carbon (δ13C), nitrogen (δ15N) and (to a more limited extent) sulfur (δ34S), in combination with fish and prey distribution surveys. In SIA analysis, predators acquire their isotopic signature from the prey they eat. When prey have different isotopic signatures, it is then possible to infer what predators have been eating. In addition, the nitrogen stable isotope signature in predators is slightly enriched relative to their prey. This property can be used to measure how many “links” (the food chain) are present in a food web.

Three investigations were undertaken to study food webs within the Coorong, an estuarine and coastal lagoon system at the end of the Murray-Darling Basin. One of the characteristics of the Coorong is a strong salinity gradient, but extreme hypersalinity (several times saltier than seawater) were present in part of the system at the time of the study (November 2007) following a prolonged period without freshwater inflows. The first investigation examined the influence of the Coorong salinity gradient on the baseline isotopic signature of key components of the food webs, a necessary step before undertaking SIA analysis. The second investigation examined how food web structure varied along the Coorong salinity gradient. As SIA analysis integrates the diet of fish over time, in the third investigation, this property was used to infer the preferred feeding areas for key fish species in the Coorong.

Baseline isotopic signatures

Along the Coorong salinity gradient (ranging from 34 to 122 g L–1 at the time of the study), primary consumers (herbivores) did not have a constant stable isotope signature for N and S. The average isotopic signature of first order consumers increased from 5.8 to 9.4‰ for δ15N and from 10.8 to 18.0‰ for δ34S. The average δ13C of primary consumers decreased from –16.0 to –18.8‰ along the same gradient but this decline was not statistically significant (P = 0.056). In contrast to salinity, water depth did not appear to influence the baseline isotopic signature of first order consumers at one intensively studied site (Pelican Point). The biogeochemical processes responsible for shifting the baseline isotopic signature for N and S along the salinity gradient are unclear. The implications of this study are that prey stable isotope signatures must be characterised across the Coorong salinity gradient before undertaking SIA.

Spatial changes in food web structure along the Coo rong salinity gradient

Changes in the food web structure along the Coorong salinity gradient were extensive. Four trophic guilds (that is, groups of organisms performing a similar ecological function) were identified based on δ15N. These included “herbivores” (various invertebrate taxa) “predatory invertebrates” (Nephtys, Phyllodoce and Macrobrachium), “benthic feeders” (smaller fish species or smaller size-classes of larger fish species feeding on invertebrates), and “piscivorous fish” (larger black bream and all size-classes of mulloway that were feeding, in part, on other fish). There was a loss of trophic guilds over a relatively short distance (Murray Mouth to Pelican Point) as salinity increased. As species and guild diversity decreased along the salinity gradient, food chains became shorter. In the vicinity of the Murray Mouth, the food chain length leading to the top predator was ~4.6 (with Level 1 – plants, Level 2 – herbivores, Level 3 – first order predators, etc), whereas the food chain length was only ~3.3 at moderately to highly hypersaline locations in the North and South lagoons, where piscivorous fish were absent. Black bream, mulloway and greenback flounder decreased in trophic position with increased salinity, possibly reflecting a decreased availability of larger prey or an increased reliance on omnivory (that is, feeding across several trophic levels). These findings suggest that habitat

Trophodynamics of the Coorong viii

quality for predatory fish decreases with increasing salinity in the Coorong because prey diversity decreases. The SIA analysis also demonstrated that polychaetes and crabs are key components of the Coorong food web leading to large fish.

Stable isotopes identify both dietary sources and s ource location

In a preliminary study, Lamontagne et al. (2007) had found that fish caught at Pelican Point had limited overlap in isotopic signature with prey at this site, suggesting that they mostly foraged elsewhere before being caught. SIA analysis and a mixing model were used to infer where predatory fish fed in the Coorong. The mixing model suggested that smallmouth hardyhead (Atherinosoma microstoma) sampled at both Goolwa and Long Point, together with juvenile yelloweye mullet sampled at Goolwa, foraged at alternate but nearby locations to where they were caught. Likewise, black bream sampled at Mundoo appeared to be utilising food resources from Goolwa Channel. The isotopic signatures of large greenback flounder sampled at Goolwa reflected a prey source signature from Pelican Pt. Mulloway sampled at Mundoo, Goolwa and Pelican Pt. appeared to be using food resources from both Goolwa and Pelican Pt. No fish sampled appeared to be using resources from Mundoo, even though mulloway were sampled there. The results indicate that mulloway found within the Coorong were feeding throughout the region between Goolwa Channel and Pelican Pt., but not significantly at Mundoo Channel.

Conclusions

• SIA analysis can provide useful information about the structure of the Coorong food-web, providing that the variation in the baseline isotopic signature along the salinity gradient is accounted for. Food webs with different lengths and structures were identified along the Coorong salinity gradient using SIA. Omnivory was important in fish diet;

• Larger fish species, such as mulloway, were probably foraging widely across the areas of the Coorong that did not exceed their physiological tolerance to salinity. However, this foraging habitat was limited, typically ranging from the Murray Mouth to upper North Lagoon (Pelican Point). In addition, lower prey diversity and shorter food chains suggest that the more saline areas within this range were less favourable;

• When the habitat is reduced by hypersalinity, the concentration of the fish populations over a smaller area of the Coorong may generate an increased predation pressure on the food resources available. This implies that the biomass of large fish species that the Coorong can sustain when hypersalinity is widespread is probably even smaller than the reduction in their range would suggest;

• Due to the absence of large aquatic plants (Ruppia spp. and others) at the time of the study, the “estuarine” Coorong food web may not have been present. It is hypothesised that this estuarine food web would have had a greater diversity of prey for large fish and a longer food chain.

Recommendations

Future interventions aiming to lower salinity in the Coorong should be used to test some of the hypotheses about the structure of its food web. These hypotheses include that:

• Fish populations will benefit from lower salinity in the Coorong both from the expansion of their range and by having access to a larger diversity of prey within their range;

• Freshwater inflows from the Lower Lakes would directly subsidise the Coorong food web through the input of organic matter (including dissolved organic matter, phytoplankton, zooplankton, etc);

• The reestablishment of Ruppia and other large aquatic plants would foster a more diverse food web, a longer food chain and a greater fish biomass in the Coorong by providing habitat (as shelter and food resources) for their prey.

Trophodynamics of the Coorong ix

Introduction to the CLLAMMecology food web studies

The Coorong relies on freshwater flow from the River Murray to maintain salinity below the tolerance threshold for the organisms that inhabit the region. The salinity gradient provides a range of aquatic habitats that support different communities. At the time of the study, the Coorong could be broadly divided into an estuarine/marine, slightly hypersaline (1-2x seawater), moderately hypersaline (2-4x seawater) and highly hypersaline (>4x seawater) regions. The estuarine/marine system, near the Murray Mouth, was characterised by the presence of several commercial fish species (yelloweye mullet [Aldrichetta forsteri], black bream [Acanthopagrus butcheri], greenback flounder [Rhombosolea tapirina] and mulloway [Argyrosomus hololepidotus]) and abundant populations of polychaetes (marine worms) and other benthic invertebrates (molluscs, crabs, etc) on the tidal mudflats. The slightly hypersaline condition in part of the North Lagoon supports a subset of the estuarine fauna but is ecologically simpler and less diverse. This system grades into the moderately hypersaline one that, until recently, dominated the South Lagoon. This moderately hypersaline system was dominated by the highly productive aquatic angiosperm Ruppia tuberosa, the chironomid Tanytarsus barbitarsus and a single fish species, the smallmouth hardyhead (Atherinosoma microstoma). These communities supported a large number of migratory waders, piscivorous birds (terns, pelicans) and waterfowl (ducks).

In years preceding the study, as a result of diversions from the River Murray and a drought, there was little to no freshwater inflow to the Coorong. This resulted in the development of a new, previously unrecorded, highly hypersaline system in the South Lagoon. This highly hypersaline system had a much simplified macroinvertebrate community (mainly brine shrimp [Parartemia zietziana] and a few dipteran larvae; Rolston and Dittmann 2009) and no fish (with the occasional exception of a limited density of hardyhead in winter, when salinity is slightly lower; Noell et al. 2009). The loss of diversity with increasing salinity along the Coorong is common across all taxonomic classes: birds, fish, plants and benthic fauna. While this ecologically simplified highly hypersaline system has relatively high primary production rates (Haese et al. 2009; Nayar and Loo 2009) and can support large numbers of a few specialist bird species, such as banded stilts (Cladorhynchus leucocephalus; a species usually associated with inland salt lakes; Wainwright and Christie 2008; Paton and Rogers 2009), it cannot support any large predatory fish.

To plan the rehabilitation of the Coorong, it is necessary to understand how the food web leading to large fish changes as salinity increases. In this study, the Coorong food web was examined using fish gut content analysis and stable isotope analysis (SIA), in combination with fish and prey distribution surveys. Changes in biogeochemical cycling along an environmental gradient, such as the salinity gradient in the Coorong, can impact on the isotopic signatures of primary producers. In Chapter 1, the potential for a shift in the baseline isotopic signature of the Coorong food web along the salinity gradient is evaluated. In Chapter 2, food web structure and food chain length along the salinity gradient are examined. Finally, Chapter 3 evaluates where predatory fish tended to forage in the Coorong.

Trophodynamics of the Coorong 1

1. The influence of a salinity gradient on the base line isotopic signature of a semi-arid coastal lagoon fo od

web

1.1. Introduction

The stable isotope ratios of C, N and S are a useful tool for determining the structure of aquatic food webs because predators acquire their isotopic signature for these elements from their prey (Boon and Bunn 1994; Fry and Sherr 1984; Peterson 1999; Wada et al. 1991). However, within an ecosystem the isotopic signatures at a given trophic level are not always constant across habitats (Vander Zanden and Rasmussen 1999). These differences occur when the physical and biogeochemical processes associated with different habitats change the isotopic signature of the organic matter at the base of the food web (Vander Zanden and Rasmussen 1999; Tewfik et al. 2007). For example, it is common for the food web of the littoral, pelagic and profundal habitats of temperate lakes to have slightly different C isotope signatures at a given trophic level because primary producers in each habitat use a source of inorganic C with slightly different isotopic signatures (Vander Zanden and Rasmussen 1999). Not taking into account the variability in baseline isotopic signature can lead to significant errors in the interpretation of the trophic structure of food webs and the diet of organism that utilise more than one habitat within the ecosystem.

Because of its fundamental role in biogeochemical cycles, ecosystems with large salinity gradients may also host gradients in baseline isotopic signatures. The relative proportion of bicarbonate available to primary producers during photosynthesis tends to increase at higher salinities and pH (Stumm and Morgan 1996), and results in enriched δ13C values (Hecky and Hesslein 1995). The principal source of sulfur to estuaries and coastal lagoons will be derived from marine sulfate, which has an isotopic signature of ~ 21‰. At elevated salinities the rate of sulfate reduction in estuarine sediments can increase and the end products tend to be depleted in δ34S (Peterson and Howarth 1987), which is then reflected in the signatures of both primary producers and their consumers (Peterson and Fry 1987). The consequence of this for stable isotope food web studies is that there may be different baseline signatures that propagate through the food web.

In the Coorong, Lamontagne et al. (2007) found little overlap in δ13C and δ34S signatures between fish and various prey at one site. Lamontagne et al. (2007) hypothesised that fish fed over a larger area and that their prey had different isotopic signatures at other locations. The purpose of this study was to evaluate if the baseline isotopic signatures for C, N and S vary across the Coorong salinity gradient. Primary consumers (filter-feeders, grazers, etc) were chosen over primary producers (algae, macrophytes, etc) to define the baseline isotopic signature because they are easier to collect and their isotopic signatures tend to be less variable over time (Cabana and Rasmussen 1996). In a secondary objective, the potential for water depth in the Coorong to be another environmental gradient impacting on the baseline isotopic signatures was evaluated using a detailed sampling of primary consumers along a depth gradient at one location.


1.2. Methods

1.2.1. Selection of Study sites

The Coorong is a 100 km long estuarine and coastal lagoon system that receives inflows from Lake Alexandrina and the River Murray via the Barrages, exchanges estuarine and ocean water through the Murray Mouth and can receive inflows from Salt Creek at the southern end of the South Lagoon (Geddes 2005) (see Fig. 1.1). It is divided into the North and South lagoons by a constricted area which limits water exchange (Parnka Point). The North Lagoon has an area of approximately 73 km2, while the South Lagoon has an area of approximately 80 km2 (Geddes and Butler 1984). The Coorong is relatively shallow (~1.1 m on average) and characterised by significant water level variations on seasonal and shorter time scales (Webster 2005). At the time of the study, an extreme salinity gradient had developed across the Coorong following several years without or with very low River Murray inflow (Webster 2005, 2007).

Figure 1.1 Locations of study sites along the Cooro ng and Murray Mouth salinity gradient.

Seven locations were selected along the salinity gradient in November, 2007 (Figure 1.1); Goolwa Channel and Mundoo Channel were located close to the Murray Mouth and had salinities of 35 and 34 g L–1 (total dissolved solids), respectively. Pelican Point, Mark Point, Long Point and Noonameena were all located in the North Lagoon, and had salinities of 45, 74, 88 and 93 g L–1 respectively, while Jack Point was located in the South Lagoon and had a salinity of 122 g L–1.


1.2.2. Sampling of targeted primary consumers

The isotopic signatures of primary consumers and primary producers from different habitats within a system can vary substantially (France 1997). This difference can be so great that the signatures of any one primary consumer may not be shared by other primary consumers within the same system (Vander Zanden and Rasmussen 1999). For this reason a number of primary consumers with known life history strategies (Table 1.1) and relatively common in the Coorong, were identified for collection and subsequent analysis.

Table 1.1 Macroinvertebrates and their feeding mod es used to determine the ‘Baseline Isotopic Signatures’ of first order consumers for the food w ebs found within the Coorong.

Species

Habitat Feeding mode

Australonereis ehlersi Polychaete – Benthic infauna Algal grazer

Parartemia zietziana Brine shrimp - Pelagic Filter feeder

Ficopomatus enigmaticus Polychaete - Epibenthic Filter feeder

Notospisula spp. Bivalve – Benthic infauna Filter feeder

Sampling took place between the 5th and 15th of November, 2007. November was chosen as the ideal time to sample as in the late Austral spring the water levels are high, salinities lower than in summer months yet productivity is high due to increased temperatures, and invertebrates generally more abundant. To reduce the potential effect of depth on isotopic signatures, all organisms were collected between a water depth of 40 to 80 cm. Triplicate samples were collected using a net (250 µm mesh) for pelagic organisms and an Ekman Birge grab for the benthic infauna. Several samples were collected and pooled for each replicate at each site, until each replicate had a fresh weight of ~2 g. Ficopomatus enigmaticus forms calcareous tube mounds which were sampled by removing portions of mounds (several portions of mounds were collected for each replicate).

To evaluate if depth may also influence isotopic signatures in the Coorong, a more detailed sampling protocol was utilised at one site (Pelican Point). Three replicate transects perpendicular to the shoreline and 300 meters apart were established. Across each transect the targeted primary consumers (Amphipoda, Capitella, Ficopomatus and Simplisetia) were sampled at different depth intervals (0-40 cm, 40-80 cm, 80-120 cm, 120-200 cm and >200 cm). These targeted primary consumers were selected for sampling at Pelican Point due to their relatively even level of distribution across the depth gradient at this location in comparison to other primary consumers. Primary consumers were collected using the same techniques as at the other sites.

Invertebrates were sorted within 12 hours of collection. Ficopomatus were gently removed from their calcareous tubes with tweezers. All invertebrates were allowed to sit in water from their collection sites overnight to clear their gut. Each replicate contained from 1 to 200 individuals for a given taxon, depending on the size and availability of the organism. None of the targeted organisms were collected at all sites due to the extreme salinity gradient along this ecosystem. When in low abundance, several samples were pooled for each replicate at a given site to have enough material for analysis. All samples were frozen whole and transported back to the laboratory for subsequent analysis.

At each site, and a few additional ones along the salinity gradient, a 1.25 L water sample was also collected for laboratory determination of pH, EC, alkalinity, major ions and δ34S-SO4

2–.


Water samples were kept at 4°C until they were deli vered to the CSIRO laboratories at the Waite Campus (Adelaide) for analysis.

1.2.3. Sample preparation and analysis:

All invertebrate samples were washed in distilled water and debris material removed. Those invertebrates with an exoskeleton (e.g. Parartemia) were acidified (Bunn et al. 1995). All samples were oven-dried at 60oC for 36-48 h and ground to a fine homogenised powder-like consistency using a mortar and pestle. Dried, ground samples were oxidized at high temperatures and the resultant CO2 and N2 were analysed with a Finnegan Delta-EA 13C, 15N stable isotope ratio mass spectrometers at the University of Waterloo Environmental Isotope Laboratory. Ratios of 13C/12C and 15N/14N were expressed as parts per thousands (‰) difference between the sample and conventional standards (Vienna Pee Dee belemnite for C, atmospheric N2 for N and CDT for S) (Gorokhova et al. 2005) where:

δX (‰) = (Rsample / Rstandard – 1) x 1000 (1.1)

and X = 13C, 15N or 34S and R = 13C/12C,15N/14N or 34S/32S.

Repeated analyses of homogeneous material yielded SD of 0.1‰, 0.2‰ and 0.2‰ for δ13C, δ15N and δ34S, respectively.

1.2.4. Water sample analysis

For each water sample, a 100-mL subsample was filtered using a 0.45 µm syringe filter (Pall Supor membrane). Major cations (Ca2+, Mg2+, K+, Na+) were measured by ICP emission spectrometry (APHA 1999, Method 3120), major anions (Cl– and SO4

2–) by ion chromatography (APHA 1999, Method 4110) and alkalinity by titration to a fixed endpoint of pH 4.5 (APHA 1999). TDS was estimated as the sum of all major cations and anions.

1.2.5. Determination of δ34S-SO42–

For each water sample, a 40 ml sub-samples was filtered through a 0.45 µm syringe filter into a 50 mL centrifuge tube. Three drops of concentrated HCl were added using a Pasteur pipette to each tube and indicator paper used to verify that pH had dropped below 3. The tubes were capped and shaken vigorously to purge any dissolved inorganic carbon and to assist in the degassing of H2S. Approximately 10 mL of saturated SrCl2 was then added to precipitate dissolved SO4 as SrSO4. Some dissolved organic S will co-precipitate with the SrSO4 at this stage, but the amount will be small relative to SO4

2--S in these saline to hypersaline waters (Ford 2007). Samples were then centrifuged at 3500 rpm for 10 minutes. The supernatant was aspirated using a pipette attached to a liquid trap at a reduced pressure supplied by a vacuum pump. Hydrogen peroxide (30% v/v) was then added to the remaining pellet and the solution gently heated with a hot air gun to release any organic S. Final purification was achieved by a further two steps of re-suspension in de-ionised water, centrifugation and aspiration. The resultant precipitate was dried in an oven at 105ºC for 3 hours and then ground to a fine powder in situ in the falcon tube with a round bottom glass rod. Precipitate samples were sent for δ34S-SO4

2– analysis at Environmental Isotopes Pty Ltd (North Ryde, Australia).

1.2.6 Analysis

The baseline isotopic signature at each site was estimated by averaging the signature for all taxa of targeted first order consumers present. Whether or not a significant change in baseline


isotopic signature was present relative to salinity was evaluated with least-square linear regressions using Sigmaplot 10.0.

1.3. Results

1.3.1. Salinity trends

A very strong salinity gradient was present in the Coorong at the time of the study, with TDS ranging from ~35 g L–1 near the Murray Mouth to ~122 g L–1 at Jack Point in the South Lagoon. The main ions were Na+ and Cl– and pH was alkaline (7.9 – 8.4). The steepest gradient in salinity was at the southern end of the North Lagoon, between Pelican and Parnka points.

1.3.2. δ34S-SO4

2–

The stable isotope signature of sulfate was similar to marine sulfate (~21‰) across the Coorong (Fig. 1.2), with no evidence of enrichment or depletion in δ34S across the salinity gradient. This suggests that processes such as mineral precipitation (i.e, gypsum, etc) and sulfate reduction do not significantly change the isotopic signature of the sulfate pool in the water column in the Coorong.

1.3.3. Primary consumers isotope signatures along t he salinity gradient

There were important trends in the average stable isotope signature of first order consumers along the Coorong salinity gradient (Figure 1.3). First order consumer δ15N increased with rising salinity (P = 0.0004) from 5.8 to 9.4‰, while first order consumers δ34S values also increased with salinity (P = 0.025) from 10.8 to 18.0‰. In contrast to N and S, the baseline isotopic signature for δ13C decreased with increasing salinity from –16.0 to –18.8‰ but was not statistically significant (P = 0.056). The trend in δ15N and δ34S enrichment with increasing salinity was also found when looking at individual taxa (Fig. 1.4). In general, Parartemia, Notospisula, Australonereis and Ficopomatus were more enriched in δ15N and δ34S at higher salinities. The differences in isotopic values between taxa at a given salinity were small (1 – 3 ‰). It was not possible to evaluate systematic differences between taxa because they had different distributions relative to salinity, i.e. no taxon was found across the whole salinity gradient and only Parartemia was found at higher salinities. The trends on a per taxa basis suggest that using an average value for all primary consumers present is a suitable method to evaluate the baseline isotopic signature in the Coorong.

Figure 1.2. Sulfur stable isotope signature of sulfate along the Coorong salinity gradient in November 2007.


Figure 1.3. Average baseline stable isotope signatu res for first order consumers along the Coorong salinity gradient. A) δδδδ13C; B) δδδδ15N; C) δδδδ34S.


Figure 1.4. Average baseline stable isotope signatu res for individual taxa along the Coorong salinity gradient. A) δδδδ13C; B) δδδδ15N; C) δδδδ34S. Error bars represent ±1 standard deviation (smaller than symbol when not visible).


1.3.4. Primary consumers isotope signatures along a depth gradient

Primary consumers were collected at different depth intervals at Pelican Point to evaluate if depth may also impact on the baseline isotopic signature of primary consumers in the Coorong. Note that this analysis targeted all primary consumers that were collected at Pelican Point, not only the subset used for comparison between all sites (Table 1.1). Based on the taxa that were common at most depth (Amphipoda and Ficopomatus), the stable isotope composition of primary consumers was not related to water depth at Pelican Point (Figure 1.5). However, there were consistent differences in isotopic signaturesbetween taxa. For example, Amphipoda consistently had a lower δ15N (~6.5‰) than the other primary consumers (~8‰). For δ13C, Amphipoda and Ficopomatus were relatively depleted (–20 to –18‰) when compared to Capitella and Simplisetia (–15 to –12‰). Finally, Amphipoda were more δ34S enriched (15 to 18‰) than the other taxa (13 to 14‰). This suggests that there are different sources of organic matter used by primary consumers at Pelican Point and that some of these sources have different isotopic signatures.

Figure 1.5. Average baseline stable isotope signatu res for first order consumers along a water depth gradient at Pelican P oint. A) δδδδ13C; B) δδδδ15N; C) δδδδ34S. Error bars represent ±1 standard deviation.


1.4. Discussion

The stable isotope signature of primary consumers varies in a systematic fashion across the Coorong salinity gradient. This implies that care should be taken when using stable isotopes to infer the diet and trophic position of higher order consumers in the Coorong and other coastal lagoons with strong salinity gradients. This is consistent with the findings of Lamontagne et al. (2007) in the Coorong, where the stable isotope signature of large predatory fish was outside the range found in primary consumers at one location. Revill et al. (2009) also found a tendency for bulk sediment organic matter δ15N to become enriched along the Coorong salinity gradient. On the other hand, while water depth has been found to be a significant environmental gradient for baseline isotopic signatures in some environments (Tewfik et al. 2007; Vander Zanden and Rasmussen 1999), this was not the case in the Coorong. This can be probably attributed to the shallow average depth of the Coorong (~1.1 m) and corresponding absence of density stratification.

This study was trying to establish if the baseline isotopic signatures for C, N and S changed along the Coorong salinity gradient, not necessarily “why”. However, in the following, potential mechanisms to generate this shift in baseline isotopic signature along the salinity gradient will be hypothesised based on some of the biogeochemical properties of the Coorong. This is done with the aim to guide future research efforts in this area.

1.4.1. Review of the hydrodynamic and biogeochemica l properties of the Coorong lagoons

Water exchange and the development of the salinity gradient in the Coorong are controlled by a complex combination of climate and hydrodynamic processes (Webster 2005, 2007). At the time of the study, seawater input through the Murray Mouth and rainfall were the principal sources of water to the Coorong and evaporation and export from the Murray Mouth the principal losses. Other minor sources of water to the Coorong during this period included episodic input from the Upper South East Drainage Scheme and regional groundwater discharge to the South Lagoon (Haese et al. 2009). While the presence of a salinity gradient is a characteristic feature of the Coorong (Phillips and Muller 2006), an extreme salinity gradient was present at the time of the study because of the lack of River Murray inflow (Webster 2005, 2007).

Ford (2007) recently reviewed the water quality database for the Coorong Lagoons for the 1997 to 2003 period and Haese et al. (2009) measured primary production and nutrient recycling along the Coorong salinity gradient in August 2007 (winter conditions) and February 2008 (summer conditions). Both studies indicated that N and P concentrations in the water column tended to increase along the salinity gradient. However, most of this N and P was in the particulate and dissolved organic pools, with low concentrations in bioavailable forms (NH4

+, NO3

– and PO43–). Ford (2007) hypothesised that the high phytoplankton biomass observed in

the South Lagoon either indicates a very efficient recycling of the organic nutrient pool or that phytoplankton productivity is low relative to its biomass. Due to the shallow depth of the Coorong, Ford (2007) hypothesised that benthic primary production would be important, as later confirmed by Haese et al. (2009) and Nayar and Loo (2009). Using algal pigments and lipid biomarkers, Revill et al. (2009) noted that while phytoplankton biomass is high, most of the organic carbon stored in shallow Coorong sediments is derived from benthic algae. The recycling of nutrients (including silica) by organic matter decomposition appears seasonal and would be higher in summer because of the higher water temperatures (Haese et al. 2009). However, much of the N, P and Si recycled during benthic respiration appears to be used in benthic primary production, resulting in relatively low releases to the water column.

Ford (2007) noted that the elevated salinity and alkalinity in the Coorong should be favourable to the formation of a range of minerals (carbonates, gypsum, etc). Mineral formation could also partially control the availability of some inorganic nutrient species in the water column, such as PO4

3– during the formation of apatite (Ford 2007). Based on sequential titrations, Hease et al.


(2009) proposed that the weak organic acids that are a part of the DOC pool could contribute up to a third of the alkalinity in the Coorong (as determined by fixed end-point titration). This suggests that carbonate alkalinity is best measured by from DIC measurements in the Coorong. However, most of the dissociation constants estimated for the carbonate system in seawater are for salinities less than ~50 g L–1 as TDS. Thus, the relative contribution of dissolved CO2, HCO3

– and CO32– to the total DIC pool in the Coorong is unclear at present, but the contribution

of HCO3– and CO3

2– is large.

Ford (2007) proposed that salinity would be a strong control on the recycling of nutrients in sediments either by limiting some processes (such as nitrification) or favouring others (such as SO4

2– reduction) as it increases. Haese et al. (2009) also noted the presence of significant groundwater discharge features to the South Lagoon and hypothesised that these may represent a significant source of NH4

+. Overall, despite low nutrient inputs from the River Murray between 2000 and 2008, primary production rates remained high in the Coorong, indicating that nutrient recycling is a key source of nutrients in this system. This tendency to use the recycled nutrient pool could be an important factor to shift the baseline isotopic signature in the Coorong.

1.4.2. Possible mechanisms driving the shifts in ba seline isotopic signature

Carbon

First order consumers collected from estuaries around the world have shown an increase in tissue δ13C with increased salinity levels along a freshwater to marine salinity gradient (Incze et al. 1982; Richard et al. 1997; Riera and Richard 1996; Doi et al. 2006). An earlier study had also shown that mixing and hydrologic residence times influence carbon isotope distributions in estuaries (Sackett and Moore 1966). In Coorong modern sediments (last ~50 years), Krull et al. (2009) found a tendency for δ13C to increase from the North to the South lagoon. However, there was no statistically significant shift in δ13Cbaseline across the Coorong salinity gradient in this study, but this baseline was relatively elevated (–19 to –8‰, as opposed to –25‰ or less expected in freshwater).

The relatively δ13C-enriched values of primary consumers in the Coorong are consistent with a marine or hypersaline environment, where bicarbonate (HCO3

–) can be an important source of carbon for photosynthesis (see also Section 1.4.1 above). The details of the inorganic carbon cycle and its implications for δ13C signatures are beyond the scope of this report. However, the key process would be that HCO3

– tends to be enriched by ~9‰ enriched relative to dissolved CO2 (Clark and Fritz 1997). Thus, it is likely that the limited variability in δ13Cbaseline in the Coorong at the time of the study was due to HCO3

– being the main form of inorganic carbon available for photosynthesis across the region instead of dissolved CO2. As observed in other estuaries, a more significant range in δ13Cbaseline may be present when freshwater inflows to the Coorong occur. Under freshwater conditions, dissolved CO2 would more likely be the main form of inorganic C used for photosynthesis.

The range in δ13C found between different primary consumers in the Coorong is relatively large (see also Section 2 for the δ13C signatures of additional primary consumer taxa), suggesting that they used different sources of organic matter. In particular, it should be expected that organic matter produced by phytoplankton and by benthic algae will have different isotopic signatures (Hecky and Hesslein 1995), as demonstrated for the Coorong by Revill et al. (2009). This property could be used in future studies to help understand the relative contribution of the organic carbon produced by phytoplankton or by benthic algae to energy flow in the Coorong food web.

Nitrogen

The increase in baseline δ15N along the Coorong salinity gradient is probably related to the tendency for the N pool to become isotopically enriched during remineralisation and recycling processes (Peterson and Fry 1987). This is consistent with nutrient mass-balance budgets for the Coorong, which suggest that recycling is a relatively more important source of nutrients


relative to external inputs in the South Lagoon (Grigg et al. 2009). Organic matter decomposition in coastal marine systems will release substantial amounts of ammonium, which provides an important source of nitrogen for phytoplankton production (Middelburg and Nieuwenhuize 1998). However, salinity not only regulates ammonium fluxes but also other mineralisation processes, such as nitrification and denitrification rates (Seitzinger et al. 1991). Hypersaline waters such as those that occur in the Coorong will favour a high ammonium:nitrate ratio in the water column by reducing nitrification rates (Ford 2007). Many of the biogeochemical processes involved in nitrogen cycling occur in the sediments and are also affected by the higher sulfide concentrations under elevated salinities. Both nitrification and denitrification are inhibited, while dissimilatory nitrate reduction to ammonia and nitrogen fixation are stimulated by sulfides (Ford 2007). In general, recycling processes are accompanied by considerable N isotopic fractionation, resulting in a 15N-enriched pool of inorganic N available for uptake by primary producers (Cifuentes et al. 1988). Regional groundwater discharge may also be a significant source of N to the South Lagoon (Haese et al. 2009), but the isotopic signature of this groundwater N is not known at present.

Sulfur

The principal source of sulfur to the Coorong is marine sulfate, which has an isotopic signature of ~21‰. However, the δ34S values of Coorong first order consumers was always less than marine sulfate, indicating a significant contribution from a depleted S source. This depleted S source is most likely derived from sedimentary sulfides, which tend to be isotopically depleted. This is consistent with the high rates of benthic primary production in the Coorong, where access to this depleted S source would be greater. However, why primary consumers δ34S values increase along the salinity gradient is less clear. A change in the proportion of phytoplankton to benthic algal primary production, in the rates of sulfate reduction, in the δ34S fractionation during sulfate reduction, or in organic S recycling along the salinity gradient could all be involved (Habicht and Canfield 1996; Deegan and Garrit 1997; Detmers et al. 2001; Ford 2007). Further studies should have a closer look at the source of S used by benthic algae in the Coorong.

1.5. Conclusion

This study has determined that salinity but not water depth is a significant environmental gradient for the baseline isotopic signature of the Coorong food webs. This implies that some care must be taken when using SIA to infer fish diet in this system, because the same prey may have a different isotopic signature at different locations. On the other hand, this potential variability in prey isotopic signatures could also be used to investigate where fish tend to forage in the Coorong (Chapter 3). Future studies should investigate in more details the biogeochemical processes associated with the salinity gradient that give rise to a shift in baseline isotopic signature in the Coorong.


2. Food web structure leading to large fish along t he Coorong salinity gradient

2.1. Introduction

Food webs describe the trophic relationships between organisms at the whole community level. An organism’s position within a particular food web is defined by its function, for example, whether it is a decomposer, a herbivore or a predator (Eggers and Jones 2000), and may also be influenced by the biodiversity within that community (Borrvall et al. 2000). The trophic position of an organism within a food web represents the number of feeding links (or food chain) separating that organism from the base of production (Thompson et al. 2007). Until recently, ecology has viewed food webs as a collection of linear chains, with herbivores feeding on plants and predators feeding on herbivores, with clear distinctions between trophic levels (Thompson et al. 2007; Vandermeer 2006; Williams and Martinez 2004). When considered using this traditional scenario, organisms’ trophic positions tend to fall at defining discrete trophic levels such as herbivores or predators. However, the trophic level concept is limited by the strict use of discrete trophic levels and inability to capture the complex interactions and omnivory that are prevalent in many ecosystems (Burns 1989; Polis 1991; Polis and Strong 1996; Vander Zanden and Rasmussen 1999). The occurrence of omnivory in relation to a food web structure and dynamics is of fundamental importance, as it can be either stabilizing or destabilizing, depending on the background conditions (Vandermeer 2006). Omnivory occurs when taxa feed at more than one trophic level (Pimm and Lawton 1978), resulting in non-discrete trophic positions, or trophic guilds. Omnivory may diffuse top-down influences in food webs (that is, the control of prey populations by predators) (Bascompte et al. 2005; Strong 1992) and may lessen the risk of extinction of specific prey or predator by offering more flexibility in the diet of predators (Strong 1992).

The Coorong and Lower Lakes region hosts at least 49 native fish species (Phillips and Muller 2006) of which approximately 26 species occupy the Murray Mouth and Coorong area under recent conditions (Noell et al. 2009). These species have diverse life history strategies and also occur as discrete communities along the Coorong and Murray Mouth region salinity gradient (Phillips and Muller 2006; Noell et al. 2009). However, the structure of the food web leading to predatory fish has received limited attention in the Coorong (Lamontagne et al. 2007). The aim of this study was to investigate how the structure of the food web leading to predatory fish changes along the Coorong salinity gradient. It was hypothesised that as the salinity level increased, there would be a concomitant decrease in the diversity of organisms and the food web would become shorter. Furthermore, it was hypothesised that as prey diversity decreased, omnivory would become more pronounced.

The food web leading to large fish species (yelloweye mullet [Aldrichetta forsteri], black bream [Acanthopagrus butcheri], greenback flounder [Rhombosolea tapirina] and mulloway [Argyrosomus hololepidotus]) along the Coorong salinity gradient as evaluated using fish stomach contents analysis and stable isotope analysis (SIA) for carbon (δ13C) and nitrogen (δ15N). In SIA analysis, predators acquire their isotopic signature from the prey they eat (Connolly et al. 2005). When prey have different isotopic signatures, it is possible to infer what the predators have been eating. In addition, the nitrogen stable isotope signature in predators is slightly enriched relative to their prey. This property can be used to measure how many trophic levels are present in a food web (Vander Zanden and Rasmussen 1999). A key advantage of using SIA is that it tends to integrate the diet of fish over longer periods of time than stomach content analysis.


2.2. Methods

2.2.1. Selection of study sites

Six locations were selected along the Coorong salinity gradient (Figure 1.1); Goolwa Channel and Mundoo Channel were located close to the Murray Mouth and at the time of sampling had salinities of 35 and 34 g L–1 (as TDS) respectively. Pelican Point, Long Point and Noonameena were all located in the North lagoon, and had salinities of 45, 88 and 93 g L–1 respectively, while Jack Point was located in the South lagoon and had a salinity of 122 g L–1 (Fig. 2.1).

Figure 2.1. Salinity in the Coorong over three peri ods with different antecedent inflows from the Lower Lakes barrages. The profile in 2007 represent conditions following little to no freshwater inflows in the preceding two year s.

2.2.2. Sampling protocol and collection of organism s

Primary consumers were sampled using the same protocol and techniques as detailed in Chapter 1. In addition, epibenthic invertebrates (Macrobrachium, etc) were also collected either using a sweep net or by sieving surficial sediments through a bucket fitted with a 250 µm mesh. Some large organisms (Mytilis, crabs) were also collected by hand when available. Fish species were sampled using a combination of fyke, gill and seine nets across all study sites. Fish were identified and separated into species and then different size classes for each species (S = small, M = medium and L = large bodied specimens; See Table 2.2 for the definition of the size classes for each species). This was done because size will influence trophic position within a food web. Five replicate samples of each fish species and size class were collected from all sites where possible. All samples were frozen whole and transported back to the laboratory for subsequent analysis. All sampling took place between 5 – 15 March 2007.


2.2.3. Sample preparation and analysis

Dorsal muscle tissue was removed from each fish sample (1-2 g fresh weight) and all samples (both fish and invertebrate) were prepared and subsequently analysed as detailed in Chapter 1, with the exception and exclusion of S.

2.2.4. Analysis and modelling of trophic position

To standardise for within system variation of δ15N at the base of the food web (δ15Nbaseline), δ15N values of first order consumers with known life history strategies (Table 2.1) were averaged and used for each site. The δ15N values for higher order consumer populations at each site were then converted to a continuous measure of trophic position (Vander Zanden and Rasmussen 1999) using:

TPconsumer = ((δ15Nconsumer - δ15Nbaseline) / 3.3) + 2 (2.2)

where +3.3‰ was used to correct for the fractionation increase in the 15N isotope per trophic guild (McCutchan et al. 2003). The fractionation rate per trophic guild can vary considerably depending on the organism’s position within a particular food web (McCutchan et al. 2003). Vanderklift and Ponsard (2003) found that there were no significant differences between animals feeding on plant food, animal food, or manufactured mixtures, but detritivores yielded significantly lower estimates of N enrichment per trophic guild. Since first order consumers were chosen to define the base of the food webs at each site and the subsequent food web structures were developed from that base, a single value may be used to correct for the fractionation increase per trophic guild due to each organisms position (i.e., all predators, above the first order consumers).

Table 2.1. Macroinvertebrates with known feeding modes that we re used to determine the δ15Nbaseline (trophic position 2) for the food webs found at ea ch study site within the Coorong.

Macroinvertebrates

Species Habitat Feeding mode

Mytilis spp. Sessile Filter feeder

Australonereis ehlersi Benthic infauna Algal grazer

Parartemia zietziana Pelagic Filter feeder

Ficopomatus enigmaticus Sessile Filter feeder

Melita spp. Epibenthic Surface deposit-feeder

Tellina spp. Benthic infauna Filter feeder

Notospisula spp. Benthic infauna Filter feeder

Amphipoda spp. Epibenthic Surface deposit-feeder

Sipunculida spp. Benthic infauna Surface deposit-feeder

Simplisetia aequisetis Benthic infauna Surface deposit-feeder

Oligochaeta indet Benthic infauna Surface deposit-feeder

Capitella spp. Benthic infauna Non-selective motile deposit feeders

Salinator fragilis Epibenthic Algal or algal-detrital feeders

Chironomid spp. Benthic infauna Algal or algal-detrital feeders


Primary producers are trophic guild 1, first order consumers are trophic guild 2, and so on. The population-specific trophic position was estimated for each individual species not included as a δ15Nbaseline species using Eq. 2.2. Population-specific trophic position estimates the mean trophic position of all individuals sampled from a population at a particular site.

2.2.5. Modelling feasible source mixtures to explai n fish diet

The range of potential food sources contributing towards a consumer’s diet was determined from stomach content analysis (see Part 3 of this report). In determining the relative contributions of different food sources to an animal’s diet, a number of different mixing model procedures can be used. In general, the proportional contribution of n + 1 different sources can be uniquely determined by the use of n different isotope system tracers (e.g. δ13C, δ15N) with linear mixing models based on mass balance equations. However, often the number of potential sources exceeds n + 1, which prevents finding a unique solution. When no definitive solution exists, there is a method that is informative in determining bounds for the contributions of each source – the IsoSource Model (Phillips and Gregg 2003).

All feasible source mixture models are presented for a number of individual species who’s trophic position dropped down a trophic guild between Mundoo channel and Long Point. Mean δ13C and δ15N values were calculated for both the consumers and their food sources at each site and used in the IsoSource model to calculate feasible combinations of food source material that could explain the consumer signatures. This method examined all possible combinations of each food source’s potential contribution (0 to 100%) in small increments (here 1%) (Phillips and Gregg 2003). Combinations that added to within 0.01‰ of the consumer signature were considered feasible solutions (Connolly et al. 2005; Melville and Connolly 2003). As recommended by Phillips and Gregg (2003), results are reported as the distribution of feasible solutions for each food source. The median contribution and the 1 and 99 percentile range is given, rather than the full range, which is sensitive to small numbers of observations in the tails of the distribution (Phillips and Gregg 2003).

Interpretation of these potential contributions deserves some discussion here. According to Benstead et al. (2006), low maxima are least ambiguous and therefore most useful; they indicate that the organic matter source can be rejected as important. Relatively high minima indicate that the source may be important. Large ranges between minima and maxima are clearly not informative, unless the minima are relatively high, and small ranges represent relatively well constrained estimates of the source contribution (Benstead et al. 2006).

To account for fractionation, we used a correction based on the most recently reported average fractionation increase of +1.0‰ for carbon isotopes and +3.3‰ for nitrogen isotopes per trophic level (McCutchan et al. 2003).

2.3. Results

2.3.1. Food web structure and trophic guilds

A large range in isotopic signature for δ13C and δ15N was found in Coorong organisms. The range in δ15N at each site indicated that several trophic levels were present but the more saline sites appeared to have fewer (Figs. 2.3 – 2.8). Many organisms tended to occur in groups with similar isotopic signatures, suggesting that “trophic guilds” were present (that is, organisms with similar diets). The less saline sites tended to have up to four trophic guilds, but the more saline ones had only one or two.


The less saline sites (Mundoo, Goolwa and Pelican Point) had a larger number of taxa present. The taxa assumed to be at trophic level 2 (the “herbivore” trophic guild; Table 2.1) had the lowest δ15N and tended to have more variability in δ13C (range up to 10‰) than in δ15N (range 2–3‰). The low δ15N of taxa assumed to be a trophic level 2 supports the assumption that they are herbivores. The large range in herbivore δ13C also suggests that they fed on different sources of organic matter (which would have different isotopic signatures). Common herbivore taxa at the less saline sites included Ficopomatus, Salinator, Notospisula, Capitella and amphipods. However, a few taxa not assumed to be at trophic level 2 (such as crabs) may also have been herbivores based on their δ15N values at some of the sites. The second “grouping” of organisms occurred close to but not quite up to trophic level 3 and included the larger invertebrate predators, such as Nephtys and Phyllodoce and Macrobrachium suggesting that a “predatory invertebrate” trophic guild is present. When not falling in the herbivore guild, juvenile and adult crabs (Paragrapsis) were also part of the predatory invertebrate guild. However, the relatively low δ15N enrichment of the predatory invertebrates indicates that they are probably not feeding exclusively on the taxa assumed to be at trophic level 2.

Figure 2.3. Trophic levels present at Mundoo Channe l in the Murray Estuary based on δ15N signatures for a range of predators and prey. Error bars represent the standard deviation in population specific isotope signatures. The average δ15N of taxa highlighted in the grey box (excluding juvenile crab) defines trophic level 2, with subsequent trophic levels assumed to be at +3.3‰ increments.


Figure 2.4. Trophic levels present at Goolwa Channe l in the Murray Estuary based on δ15N signatures for a range of predators and prey. Error bars represent the standard deviation in population specific isotope signatures. Trophic le vel 2 was defined as the average δ15N value of taxa highlighted in the grey box (excluding juvenil e and adult crabs).


Figure 2.5. Trophic levels present at Pelican Point in the North Lagoon of the Coorong based on δ15N signatures for a range of predators and prey. Err or bars represent the standard deviation in population specific isotope signatures. Trophic lev el 2 was defined as the average δ15N value of taxa highlighted in the grey box (excluding juvenil e crab).

The two other trophic guilds present were at or above trophic level 3 and consisted of various fish size-class taxa. At Mundoo and Goolwa (Figs. 2.3 – 2.4), the first group was found between trophic level 3 and 4 and was made-up of small bodied fish species (congolli, sandy sprat, hardyhead, Tamar goby), smaller size classes of larger fish species (bream S), and all mullet and flounder size-classes. This guild can be referred to as the “benthic feeders” because their δ15N falls within the range expected if they were to feed on a mixture of prey from the herbivores and predatory invertebrate guilds, which are generally associated with the substrate. The last trophic guild was at or above trophic level four and included mulloway and bream L (Figs 2.3 – 2.4). Based on their δ15N, these taxa could either be feeding on fish from the benthic feeders guild or on a mixture from the benthic feeders and predatory invertebrate guilds. For simplicity, this last guild can be called “piscivorous fish” as some feeding on fish is likely. A similar pattern in guild distribution was also observed at Pelican Point (a slightly more saline site than Goolwa and Mundoo), but the difference in δ15N between benthic feeders and piscivorous fish was not as pronounced.

In general, there was a larger in range in δ13C within taxa in the fish-dominated guilds. This pattern could be the result of several processes. Firstly, the isotopic signature of fish was usually measured on individual specimens, while for the invertebrates several specimens had to be pooled for each sample in order to collect enough tissue for analysis. This pooling of specimens would tend to lower isotopic variability between invertebrate samples. Alternatively, individual fish could have been feeding preferentially on different prey (with slightly different


isotopic signatures) or have been feeding preferentially in different parts of the Coorong prior to being sampled. The shift in the baseline isotopic signature along the Coorong salinity gradient would tend to impart more variability in fish isotopic signature even if they were to feed on the same prey across different sites. While there was generally a good overlap in piscivorous fish δ13C relative to their potential prey at a given site, in some instances there was little or no overlap (see bream S and mulloway S at Goolwa; Fig. 2.4). This is consistent with fish not exclusively feeding at the site where they were caught. A more quantitative assessment of diet using SIA for selected fish taxa is presented in section 2.3.3 and an analysis of fish foraging range also using SIA is presented in Chapter 3.

Food web structure changed markedly as salinity increased from Pelican Point to the other sites. The number of taxa collected diminished from 22 at Pelican Point (salinity = 45 g L–1), to nine at Long Point (88 g L–1; Fig. 2.6), four at Noonameena (93 g L–1; Fig. 2.7) and two at Jack Point (122 g L–1; Fig. 2.8). This loss of taxon diversity did not occur evenly across all trophic guilds. The piscivorous fish and predatory invertebrate guilds (with the exception of crabs at Long Point) were absent at all the sites with salinity above 45 g L–1. Benthic feeders were markedly reduced in diversity but were still present at Long Point (three taxa) and Noonamena (one taxon) but not at Jack Point. The number of herbivore taxa also diminished but was more resilient than the other guilds, partially owing to the appearance of two new taxa (chironomids and Parartemia) at Noonamena and Jack Point. Overall, at the more saline sites, the loss of trophic guilds resulted in the food web being reduced to approximately three trophic levels at Noonamena and two trophic levels at Jack Point.

Based on the δ13C signatures, at Long Point the diet of congolli M, flounder S and hardyhead could include crab, Capitella and Simplisetia but is unlikely to have a large Australonereis, juvenile crab or Ficopomatus component (Fig 2.6). Capitella and chironomids appear to be major components of smallmouth hardyhead diet at Noonameena (Fig. 2.7). There are no fish or predatory invertebrates at Jack Point, but chironomids and Parartemia could still be preyed upon by other types of predators, such as wading birds.


Figure 2.6. Trophic levels present at Long Point in the North Lagoon of the Coorong based on δ15N signatures for a range of predators and prey. Error bars represent the standard deviation in population specific isotope signatures. Trophic lev el 2 was defined as the average δ15N value of taxa highlighted in the grey box (excluding juvenil e crab).


Figure 2.7. Trophic levels present at Noonameena in the North Lagoon of the Coorong based on δ15N signatures for a range of predators and prey. Err or bars represent the standard deviation in population specific isotope signatures. Trophic lev el 2 was defined as the average δ15N value of taxa highlighted in the grey box.


Figure 2.8. Trophic levels present at Jack Point in the South Lagoon of the Coorong based on δ15N signatures. Trophic level 2 was defined as the aver age δ15N of the two taxa present.

2.3.2. Estimation of trophic position

Based on the δ15Nbaseline found at each site and Eq. 2.1, the trophic position of many taxa was not constant between sites (Table 2.2). The trophic position of the predatory invertebrates (Phyllodoce, Nephtys and Macrobrachium) ranged between 2.54 to 2.89, with no obvious trends between Mundoo, Goolwa and Pelican Point. However, many of the larger fish taxa tended to be at a lower trophic level with increasing salinity. For example, flounder S decreased in trophic position from 3.28 to 2.87 between Goolwa and Long Point, mulloway L decreased from 4.13 to 3.89 between Mundoo and Pelican Point, and mullet L decreased from 3.48 to 3.03 between Goolwa and Pelican Point. Smaller-bodied fish had no apparent pattern in trophic position relative to salinity. For example, hardyhead trophic position ranged from 3.29 at Mundoo to 3.40 at Goolwa to 3.28 at Noonameena. Juvenile (1.96 to 2.27) and adult crab (2.36 to 2.87) also had variable trophic positions between Mundoo and Pelican Point but there was no evident trend relative to salinity. Overall, the food chains were shorter at Long Point, Noonameena and Jack Point because of the absence of the piscivorous fish guild at these sites. Within their salinity tolerance range, piscivorous fish may also have occupied a slightly lower trophic position at higher salinities.


Table 2.2. Summary of the trophic positions of all organisms sampled across all sites (*** denotes organism not collected at that location). Fish spec ies were separated into distinct size classes.

Mundoo Goolwa Pelican Pt. Long Pt. Noonameena Jack Pt.

Salinity (g L–1) 34 35 45 88 93 122

Species Trophic position

Ficopomatus 2.00 2.00 2.00 2.00 *** ***

Salinator 2.00 2.00 2.00 *** *** ***

Notospisula 2.00 *** 2.00 *** *** ***

Capitella 2.00 *** 2.00 2.00 2.00 ***

Sipunculoid 2.00 *** *** *** *** ***

Mytilis 2.00 *** *** *** *** ***

Amphipoda 2.00 2.00 2.00 *** *** ***

Melita 2.00 *** *** *** *** ***

Australonereis *** 2.00 *** 2.00 *** ***

Simplisetia *** 2.00 2.00 2.00 *** ***

Tellina *** *** 2.00 *** *** ***

Oligochaetes *** *** 2.00 *** *** ***

Chironomids *** *** *** *** 2.00 2.00

Parartemia *** *** *** *** 2.00 2.00

Juvenile crab 2.26 1.96 2.27 1.96 *** ***

Adult crab 2.87 2.36 2.74 2.36 *** ***

Phyllodoce 2.88 *** 2.89 *** *** ***

Nephtys 2.63 2.69 2.81 *** *** ***

Macrobrachium 2.81 2.81 2.54 *** *** ***

Mullet S (50-80mm) 3.75 3.62 3.55 *** *** ***

Mullet M (120-240mm) 3.17 3.37 *** *** *** ***

Mullet L (250-400mm) 3.47 3.48 3.03 *** *** ***

Flounder S (50-100mm) 3.23 3.28 3.05 2.87 *** ***

Flounder L (160-360mm) 3.47 3.65 3.17 *** *** ***

Congolli S (40-80mm) 3.27 3.34 3.30 *** *** ***

Congolli M (100-170mm) *** *** *** 3.34 *** ***

Congolli L (180-220mm) 3.31 3.20 *** *** *** ***

Hardyhead (40-80mm) 3.29 3.40 3.38 3.21 3.28 ***

Tamar goby (40-80mm) 3.24 3.10 3.30 *** *** ***

Sandy sprat (20-50mm) *** 3.33 *** *** *** ***

Galaxias (40-80mm) *** 3.49 *** *** *** ***

Bream S (80-180mm) 3.51 2.91 *** *** *** ***

Bream L (220-400mm) *** 4.33 3.83 *** *** ***

Mulloway S (120-190mm) 4.11 4.62 *** *** *** ***

Mulloway M (250-380mm) 4.13 *** *** *** *** ***

Mulloway L (400-600mm) 4.13 4.11 3.89 *** *** ***


2.3.3. Modelling estimation of fish diet

A more quantitative assessment of fish diet was attempted for bream L, flounder S and mulloway L using the IsoSource model at sites with different salinities. These taxa were chosen because they were relatively widely distributed and had a good matching stomach content analysis to identify the range of potential prey that they were consuming at the time of the study (see Chapter 3). Modelling the feasible contributions of each food source towards fish diets (Table 2.3) identified sandy sprat (18 – 50%) and mullet (0 – 42%) as potential principal food sources of mulloway L at Goolwa. Mulloway L sampled at Pelican Point had a greater percentage of their diet comprised of crabs (0 – 40%), Nephtys (0 – 48%) and gobies (0 – 44%). Likewise, bream L sampled at Goolwa fed predominantly on sandy sprat (32 – 64%) and juvenile fish (0 – 64%), while those sampled at Pelican Point fed on Ficopomatus (42 – 52%) and gobies (44 – 48%). For flounder S sampled at Goolwa, Nephtys (12 – 44%) formed a major part of their diet, which has a higher trophic position than Simplisetia (Table 2.2), recognising that Simplisetia (53 – 75%) was the principle component in flounder S diets at Long Point (Table 2.3).

This analysis suggests that the piscivorous fish guild in the Coorong fed has an omnivorous diet, feeding at two or possibly three trophic levels (herbivores, predatory invertebrates and benthic feeders). Likewise, flounder S (from the “benthic feeders” guild) also has an omnivorous diet that comprises both herbivores and predatory invertebrates. In addition, the IsoSource modelling suggested that the three fish taxa investigated fed more extensively at lower trophic levels at the more saline site (had a more omnivorous diet).

A potential confounding factor in this analysis is that the larger-bodied fish may forage extensively across the Coorong, including in areas where their favourite prey have slightly different isotopic signatures. In Chapter 3, SIA analysis is used to explore this topic in more detail by evaluating the preferred foraging areas for some of the larger-bodied fish species.


Table 2.3. Distribution of feasible contributions t o fish diet from food sources collected from sites with different salinities based on δ13C and δ15N values.

Ranges: 1 and 99 percentiles. Median in brackets. T P = trophic position. (*** denotes organism not col lected at that location).

Species

Site & TP

Food Sources

Crab

Ficopomatus Juvenile fish

Sandy sprat

Congolli Hardyhead Goby Nephtys Macrobrachium Juvenile Crabs

Goolwa TP = 4.33

0 – 4% (0%)

0 – 2% (0%)

0 – 64% (24%)

32 – 64% (52%)

***

0 – 32% (18%)

0 – 16% (2%)

0 – 6% (0%)

0 – 8% (0%)

***

Bream L

Pelican Pt TP = 3.83

0 – 0% (0%)

42 – 52% (48%)

***

***

0 – 4% (0%)

0 – 4% (0%)

44 – 48% (46%)

0 – 4% (0%)

0 – 10% (2%)

0 – 6% (0%)

Australonereis Nephtys Amphipod Simplisetia Capitella Juvenile Crabs

Goolwa TP = 3.28

11 – 34% (23%)

12 – 44% (29%)

0 - 48% (23%)

0 – 54% (25%)

***

***

Flounder S

Long Pt. TP = 2.87

0 – 24% (12%)

***

***

53 – 75% (63%)

0 – 24% (11%)

0 – 31% (14%)

Crab Mullet Juvenile Crab

Sandy sprat

Nephtys Hardyhead Goby Congolli Macrobrachium

Goolwa TP = 4.11

0 –22% (4%)

0 –42% (10%)

0 – 22% (8%)

18 – 50% (38%)

0 – 4% (2%)

0 – 26% (6%)

0 – 34% (6%)

0 – 32% (6%)

0 – 40% (10%)

Mulloway L

Pelican Pt TP = 3.89

0 – 40% (8%)

8 – 30% (20%)

0 – 32% (12%)

***

0 – 48% (10%)

0 – 32% (8%)

0 – 44% (10%)

0 – 32% (8%)

0 – 40% (14%)


2.4. Discussion

2.4.1. Fish diet and trophic position in the Cooron g based on SIA

In the Coorong, invertebrate and fish diversity decreased along the salinity gradient, which resulted in shorter food chains according to 15N-based measurements of the trophic position of consumers. The distribution of fish and invertebrates noted here (that is, in November 2007) is consistent with larger surveys undertaken during this period (Noell et al., 2009; Rolston and Dittmann 2009). In gillnet and seine surveys between October 2006 and September 2008, Noell et al. (2009) determined that larger-bodied fish distribution was strongly limited by salinity, with the upper salinity limit ranging from ~60 g L–1 for black bream, ~62 g L–1 for mulloway and ~74 g L–1 for yelloweye mullet and greenback flounder. Thus, a key factor in the reduction of the food chain length at higher salinity in the Coorong is that the piscivorous fish guild disappears once salinity exceeds twice seawater.

However, within the salinity tolerance range of the larger fish, there was also a tendency for them to occupy a lower trophic position at higher salinities. This decrease in trophic position may have been caused by the decreased diversity and biomass of potential prey (fish and invertebrates) as salinity increased (Noell et al. 2009; Rolston and Dittman 2009). For example, during surveys between December 2006 and March 2007, Rolston and Dittman (2009) collected between 8 to 12 benthic macroinvertebrate taxa in the Murray Mouth region, 3 to 7 in the upper North Lagoon, and two or less in the lower North Lagoon. This decrease in the choice of prey may have forced predators to feed on smaller prey within a given guild or to rely on prey sources at lower trophic levels. This suggests that some fish became increasingly omnivorous as they foraged in more saline areas of the Coorong, a common strategy used by fish to persist in less desirable habitats (Borrvall et al. 2000).

However, the estimated trophic position for piscivorous fish is also dependent on the estimated δ15Nbaseline at a given site. As demonstrated in Chapter 1, the δ15Nbaseline was not constant from site to site and tended to increase at higher salinities. At sites within the salinity tolerance range of the piscivorous fish, the δ15Nbaseline was 5.54‰ at Goolwa, 6.17‰ at Mundoo and 6.85‰ at Pelican Point. Thus, if unaccounted for, the difference in δ15Nbaseline between Goolwa and Pelican Point could induce a bias of up to ~0.4 in the estimation of trophic level. However, this assumes that predators and potential prey obtained all their food from the site where they were caught. In the case of the more mobile species (like large fish), the trophic position could also be over or underestimated if they actually fed most of the time at a site but were caught elsewhere. This can be evaluated if there is a general shift in δ15N across sites for organisms with more (large fish) or less mobility (predatory invertebrates).

The variation in δ15N in predatory invertebrates and in small fish is positively correlated to site δ15Nbaseline (Fig. 2.9). This indicates that predatory invertebrates and small fish foraged mostly at the sites where they were caught. In addition, this shows that the larger fish taxa could acquire a site-specific δ15N should they limit their foraging to a specific site. However, while sample sizes were small (n = 3), there was no correlation between large fish average δ15N and δ15Nbaseline (Fig. 2.9), indicating that larger fish foraged across sites. The larger variability in both δ13C and δ15N signatures between samples is also consistent with a tendency for larger fish species to have a larger foraging range (see also Chapter 3).


2.4.2. Smallmouth hardyhead distribution

At the time of the study, the highest density of prey fish (mostly smallmouth hardyhead) was found in areas of the North Lagoon apparently too saline for predatory fish. Between October 2006 and September 2008, smallmouth hardyhead density was generally less than 50 individuals per 500 m–2 in the Murray Mouth region but densities ranged between 80 to 1040 individuals per 500 m–2 in the North Lagoon (Noell et al. 2009). Thus, salinity may also influence fish diet by creating refugia for some prey organisms.

Figure 2.9. Relationships between δδδδ15Nbaseline and the δδδδ15N signature of different groups of organisms at higher trophic levels. Solid lines indicate that the relationship is significant at P < 0.05. “Predatory invertebrates” – Phyllodoce, Nephtys and Macrobrachium; “Crabs” – juvenile crab and crab; “Small fish” – hardyhead, flounder S; congolli S + M, Tamar goby, mullet S. Only taxa found at three or more sites were included.


2.4.3. Predatory invertebrates

Predatory invertebrates (Nephtys, Phyllodoce and Macrobrachium) had an intermediate trophic position (2.5 – 2.9) between first consumers and benthic feeders (hardyhead, sandy sprat, etc). However, despite being predators (Fauchald and Jumars 1979; King et al. 2004; Wilson 2000), they were never a full trophic level above their putative “prey” (those taxa listed as trophic level 2 in Table 2.2). This discrepancy could indicate that these predatory invertebrates have an omnivorous diet (that is, are partially herbivores). On the other hand, all potential predatory invertebrate prey items may not have been properly characterised by our sampling procedure, which focussed on the relatively larger benthic macroinvertebrates used by fish. Future food web studies in the Coorong could address this problem by attempting to determine the baseline isotopic signature in primary producers (a more difficult task than determining the baseline isotopic signature in primary consumers).

2.4.4. Ontogenic diet shifts in yelloweye mullet an d mulloway

As predatory fish become larger, they feed on larger prey and they tend to increase in trophic position. However, the reverse pattern was apparent for yelloweye mullet and mulloway in the Coorong. Mulloway L at Goolwa had a relatively low trophic position (4.11) relative to mulloway S (4.62) or black bream L (4.33). This pattern may have been caused by a large proportion of adult crabs (such as Paragrapsis sp.) in mulloway L diet. While the largest invertebrates in the Coorong, adult crabs occupy a relatively low trophic level (2.36 at Goolwa) when compared to smaller predatory invertebrates (Table 2.2). Crabs are a common stomach content item in mulloway in the Coorong (Lamontagne et al., 2007; Geddes and Francis 2008; Chapter 3). Mulloway L may prey more effectively and consume more adult crabs than other mulloway size classes, which will tend to lower their 15N signature relative to a diet relying on prey fish only. Ontogenic shifts are common in the diet of mulloway, with a tendency to prey on larger organisms during growth (Hall 1986; Taylor et al. 2006).

The trophic position of mullet S varied between 3.55 and 3.75 in the Murray Mouth region while mullet L varied between 3.03 to 3.48 (Table 2.2). Lamontagne et al. (2007) observed a similar pattern in yelloweye mullet collected in the Pelican Point area in 2005, with larger mullet having consistently lower δ15N than juveniles. From the stomach content analyses, it is not clear why different size-classes of mullet have different trophic positions in the Coorong. All size classes of mullet fed on Capitella and amphipods at the time of the study (Table 3.2). However, mullet L also preyed on more varied food items, including crabs. Previous studies have identified that yelloweye mullet diet is diverse and includes organic matter detritus and macroalgae (Thomson 1957; Webb 1973; Higham et al. 2005). The lower trophic position of mullet L in the Coorong may indicate that they have a larger proportion of organic detritus and macroalgae in their diet relative to mullet S.

2.5. Conclusion

The food web leading to predatory fish varies significantly along the Coorong salinity gradient. At the time of the study, following several years without freshwater inflows from the River Murray, large fish were restricted to the Murray Mouth region because salinities were too high in most of the North and all of the South Lagoon. Historically, large fish species have occupied the North and the South lagoons of the Coorong when salinity was lower (Geddes 1987; Phillips and Muller 2006). However, the loss of habitat for fish under recent conditions may be more significant than what that their salinity tolerance range would suggest. The loss of prey diversity, in particular large prey, in the more saline component of the predatory fish habitat could result in less efficient foraging. In addition, having fewer prey species available may put more pressure on the prey populations remaining in marginal habitats, which could eventually result in a further degradation of habitat quality for predators (Mittelbach et al. 1995). These findings are consistent with the tendency for fish species with a strong estuarine component in


their life cycle (such as black bream and greenback flounder) to currently have a relatively low abundance in the Coorong when compared to species which use the Coorong in a more opportunistic fashion (Noell et al. 2009). Thus, lowering salinity in the Coorong may benefit its large fish species by improving both the quantity and the quality of available habitat.

The SIA analysis also indicated the key role played by polychaetes and crabs in the Coorong food web. The smaller herbivorous polychaetes (along with amphipods) were a key food resource for the smaller fish, while predatory polychaetes and crabs were an important component of the diet of the larger fish taxa. Thus, maintaining suitable habitats for polychaetes in the Coorong would also indirectly benefit its fish populations by providing key food resources.


3. Fish diet and preferred foraging areas in the Co orong inferred from stable isotope analysis

3.1. Introduction

When compared with terrestrial ecosystems, the food webs in aquatic environments are challenging to investigate. In terrestrial environments there are a range of techniques available to examine food webs, including direct observation of predation or ingestion, and faecal or pellet examination. The nature of aquatic environments limits our ability to accurately determine predator-prey relationships (Hobson and Welch 1995). The study of diet based on stomach content analysis has been a standard practice in fish ecology (Hyslop 1980). Stomach content analysis, however, only allows the stomach contents of a predator to be quantified in terms of specific taxa ingested, but not necessarily assimilated (Grey et al. 2002). It only provides information about feeding immediately prior to capture, and provides limited information regarding the source of those food items (e.g. pelagic, littoral, benthic, etc,). Moreover, ingested items can often be masticated or digested beyond recognition, and the softer body components of the diet may be significantly underestimated (Burns et al. 1998). Stable isotope analysis can be utilised to augment conventional dietary analysis techniques such as stomach content analysis, providing additional information on diet over time periods of weeks to months.

Stable isotopes are a powerful and effective tool for tracing the movement of energy and nutrients from primary producers to consumers (Connolly et al. 2005). The stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) differ among primary producers (Bouillon et al. 2002; Fry 1984) and these ratios, the isotopic signatures, are taken on by the consumers and reflected in their tissues at whatever trophic level they occur (Boon and Bunn 1994; Fry and Sherr 1984; Peterson 1999; Wada et al. 1991). Both the nitrogen and carbon in consumer tissues are derived exclusively from their diet, and therefore trophic estimates using stable isotopes are based on food that has been assimilated rather than just ingested (Gearing 1991).

In aquatic ecosystems, variation in the isotopic signatures of primary producers is a widespread phenomenon. These variations occur as a result of habitat specific differences in biogeochemical cycling (Vander Zanden and Rasmussen 1999) together with habitat specific primary producers. Changes in both biogeochemical cycling and primary producers along an environmental gradient will impact the isotopic signatures of the food webs along that gradient, resulting in food webs with different baseline isotopic signatures (Tewfik et al. 2007). Therefore, the different baseline signatures from locations along that environmental gradient may be used to identify the location of the food resources utilised by a consumer.

Stable isotopes, stomach content analysis and the IsoSource model were used to determine fish diet and fish foraging areas in the Coorong. This evaluation of preferred fish foraging is made possible because of the tendency for fish prey to have slightly different isotopic signatures in different regions of the Coorong (Chapter 1).

3.2. Methods

3.2.1. Selection of Study sites

Five locations were selected along the present Coorong salinity gradient (Figure 1.1); Goolwa Channel and Mundoo Channel were located close to the Murray Mouth and had salinities of 35 and 34 g L–1 respectively. Pelican Point, Long Point and Noonameena were all located in the North lagoon, and had salinities of 45, 88 and 93 g L–1 respectively. All fish species were sampled between Goolwa Channel and Pelican Point, apart from Hardyhead, which were also sampled at both Long Point and Noonameena.


3.2.2. Sampling protocol and collection of organism s

All invertebrates and fish were sampled using the same protocol and techniques as detailed in Chapter 2. To reduce the effect of habitat type, only habitats to a water depth of 1 m were sampled. The invertebrates sampled included the polychaetes; Ficopomatus spp., Capitella spp., Nephtys spp., Simplisetiaspp., Oligochaete spp., Phyllodoce spp., Sipunculoid spp. and Australonereis spp. A range of other invertebrates were obtained from both the pelagic and benthic zones, including amphipods, chironomids, brine shrimp (Parartemia spp.), crabs (Paragrapsis spp.) and shrimp (Macrobrachium spp.). The fish sampled included; Black bream (Acanthopagrus butcheri), yelloweye mullet (Aldrichetta forsteri), greenback flounder (Rhombosolea tapirina), mulloway (Argyrosomus japonicus), smallmouth hardyhead (Atherinosoma microstoma), sandy sprat (Hyperlophus vittatus) and congolli (Pseudaphritis urvillii).

3.2.3. Sample preparation and analysis

All samples (both fish and invertebrate) were prepared and subsequently analysed as detailed in Chapter 2.

3.2.4. Modelling feasible source mixtures to explai n fish diet

Modelling to explain fish diet followed Chapter 2. Food sources from the same location as where the fish species were sampled, together with food sources from the remaining locations, were analysed for feasible mixture solutions. If all combinations from a particular site were outside a tolerance of 0.01%, the number of observations (= feasible mixtures) was equal to 0 and no statistics were generated (Phillips and Gregg 2003). In such an event, the food sources from that site were deemed not to have formed a significant part of the dietary intake of the consumer. If food sources from more than one site generated feasible solutions, then it was deemed that the consumer relied on resources across a combination of sites in close proximity. Note, not all modelled outputs are presented; if feasible solutions were identified using food sources from the same locations as where the fish species were collected and no other feasible solutions were generated using food sources from subsequent sites, then only those feasible solutions are presented.

3.3. Results

3.3.1. Gut contents

The gut contents of the individual species varied (Table 3.1); Mulloway were found at the time of sampling to mainly consume other smaller fish species and crabs, but also Macrobrachium and polychaetes with less frequency; the diet of black bream mainly consisted of smaller fish species, crabs and polychaete worms; while both flounder and hardyhead consumed small crustaceans and polychaete worms, as indicated by the percent occurrence and mean number of food items per fish (Table 3.1). Mullet (Table 3.2) were found to mainly contain a combination of amphipods and polychaete worms, except for the larger mullet, which also contained crabs and Macrobrachium spp.

3.3.2. Modelled feasible source mixtures to explain fish diet

Smallmouth harydhead

The principal dietary component of hardyhead across all sites sampled were Capitella, with contributions of between 65 – 84% at Mundoo, 56 – 73% at Goolwa, 88 – 95% at Pelican Point,


92 – 99% at Long Point and 63-76% at Noonameena (Table 3.3). The remainder of hardyhead diets consisted of small crustaceans and polychaete worms, depending on the species present at individual sites (Table 3.3). 30 – 90% of the hardyheads contained Amphipoda in their gut (Table 3.3), however, this contribution was not reflected in the isotopic signatures of their tissue, with Amphipoda being a minor dietary contribution compared with Capitella (Table 3.3). No feasible source mixture solutions were identified for hardyhead at Goolwa and Long Point without including food sources from other locations (Table 3.3). When modelled using food sources from adjacent sites (Mundoo for hardyhead sampled at Goolwa and Pelican Point for those sampled at Long Point) feasible solutions were identified, which were consistent with results from the remaining study sites. This would suggest that hardyhead sampled at both Goolwa and Long Point had spent significant time feeding on the resources present at Mundoo and Pelican Point respectively, and had only recently moved to the locations where they were caught.

Black bream

The gut contents of black bream identified gobies (12 – 33% of individuals), crabs (25 – 66% of individuals) and polychaete worms (8% of individuals) as food sources (Table 3.1). Modelling of feasible source mixtures identified two preferred food sources, dependent on location and fish size (Table 3.4). At Pelican Point, Ficopomatus (42 – 52%) and gobies (44 – 48%) formed the principal dietary intake, while sandy sprat (32 – 64%) and juvenile fish (0 – 64%) were the primary sources at Goolwa. No feasible source mixture solutions were identified for black bream from Mundoo using food sources from both Mundoo and Pelican Point (Table 3.4). However, modelling did identify Ficopomatus (46 – 55%) and sandy sprat (42 – 48%) from Goolwa as potential primary sources, suggesting that these bream had spent significant time feeding at Goolwa.

Greenback flounder

Flounder were divided into two separate size classes (Table 3.5). Irrespective of size class however, specimens from all sites sampled contained Amphipoda in their gut (5 – 53% of individuals sampled at each site), together with a range of polychaete worms (Table 3.1). Modelling of feasible source mixtures identified Capitella (23 – 61%), Phyllodoce (0 – 40%) and Nephtys (0 – 67%) as being the principal dietary intake of large flounder (160 – 360mm) at Mundoo. However, the primary sources supporting large flounder at both Goolwa and Pelican Point were Capitella (0 – 60% and 0 – 50% respectively), Simplisetia (0 – 74% and 0 – 50% respectively) and Oligochaete (0 – 66% and 22 – 80% respectively), modelled on sources from Pelican Point (Table 3.5). No feasible source mixture solutions were identified for large flounder sampled from Goolwa using food sources from either Goolwa or Mundoo (Table 3.5), suggesting that flounder sampled at Goolwa had spent significant time feeding at Pelican Point.

The smaller size class of flounder (50 – 100mm) appeared to be less transient in their movement, as feasible source mixtures were identified using food sources from the locations where the fish were sampled (Table 3.5). Again the principal dietary components varied with site and the potential sources present. Small flounder sampled from Mundoo primarily consumed Capitella (76 – 92%), while the principal dietary intake of those sampled at Goolwa were Nephtys (14 – 45%) and Simplisetia (0 – 51%). Oligochaetes (52 – 84%) were a major component of the diets of flounder sampled from Pelican Point.

Mulloway

Mulloway specimens sampled from Mundoo, Goolwa and Pelican Point fed principally on a diet of smaller bodied fish species, crabs and Macrobrachium (Tables 3.1 & 3.6). The only feasible source mixture solutions identified for mulloway sampled from Mundoo, Goolwa and Pelican Point used food sources from both Goolwa and Pelican Point, suggesting that mulloway fed primarily at these locations (Table 3.6).

Yelloweye mullet

Large mullet (>250mm) sampled from Mundoo, Goolwa and Pelican Point fed principally on a diet of amphipods, polychaete worms, crabs and Macrobrachium at both Goolwa and Mundoo Channels (Tables 3.7). However, no feasible solutions were generated with food sources from


Pelican Point even for fish sampled at Pelican Point (Table 3.7). Likewise, for medium mullet (120 – 240mm) sampled at both Mundoo and Goolwa Channels, feasible solutions were identified for food sources from both locations, but not Pelican Point (Table 3.8). When identified as a potential food source at a given site, Capitella played a more substantial role in the diet of medium mullet (86 – 90% and 80 – 88%) compared to the role it played in the diets of larger mullet (0 – 32%, 0 – 54% and 2 – 68%). Smaller mullet (<80mm) also relied on Capitella as a major component in their diet, followed by amphipods and other polychaete worms (Table 3.9). No feasible source mixture solutions were identified for small mullet at Goolwa using food sources from Goolwa (Table 3.9). When modelled using food sources from Mundoo, feasible solutions were identified, which were consistent with results from the remaining study sites. This would suggest that small mullet sampled at Goolwa had spent significant time feeding at Mundoo.


Table 3.1. Gut contents of mulloway, black bream, f lounder and smallmouth hardyhead (% occurrence /mea n number of food items per fish; n = 4-24).

Fish Crustacea Polychaetes Molluscs

Species Location

Mul

let

Har

dyhe

ad

Gob

y

Am

ipho

d

Cra

bs

Mac

robr

achi

um

Cap

itella

Nep

hyts

phyl

lodo

ce

Sim

plis

etia

Aus

tral

oner

eis

Art

hrith

ica

Not

ospi

sula

Mulloway Mundoo 5/1 12/2 70/2 15/2 Mulloway Goolwa 6/2 6/1 41/2 12/2 6/2

Mulloway Pelican 30/2 10/2 20/2 50/3 Black Bream Mundoo 33/2 66/2 Black Bream Goolwa 59/2 8/13 8/1 8/1 16/2 Black Bream Pelican 12/3 25/6

Flounder Mundoo 50/180 25/2 25/1 Flounder Goolwa 33/10 25/2 33/1 Flounder Pelican 5/60 15/2 Flounder <100mm Mundoo 40/52 40/2 Flounder <100mm Goolwa 53/37 15/2 15/1 Hardyhead Mundoo 90/3 35/7 Hardyhead Goolwa 30/2 Hardyhead Pelican 75/4 20/2


Table 3.2. Gut contents of yelloweye mullet (% occu rrence/mean number of food items per fish; n = 4-18 ).

Fish Crustacea Polychaetes Molluscs

Species Location

Mul

let

Har

dyhe

ad

Gob

y

Am

ipho

d

Cra

bs

Mac

robr

achi

um

Cap

itella

Nep

hyts

phyl

lodo

ce

Sim

plis

etia

Aus

tral

oner

eis

Sip

uncu

loid

Art

hrith

ica

Not

ospi

sula

Mullet >250mm Mundoo 28/46 19/6 19/3 28/49 19/2 Mullet >250mm Goolwa 20/20 20/9 5/3 33/76 10/2 Mullet 120-240mm Mundoo 55/23 30/2 10/2 Mullet 120-240mm Pelican 50/29 35/57 40/2 5/2 35/9 5/1 Mullet <80mm Mundoo 45/2 40/7 Mullet <80mm Goolwa 10/2 50/8 Mullet <80mm Pelican 10/2 90/13


Table 3.3. Smallmouth hardyhead: Distribution of fe asible contributions to hardyhead diet from food so urces collected from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in bra ckets. (*** denotes organism not collected at that location).

Species

Location of consumer & food

source (FS)

Food Sources & Feasible Source Mixtures

Amphipoda

Capitella

Phyllodoce

Nephyts Simplisetia

Australonereis Chironomid

Parartemia

Mundoo FS - Mundoo

5 – 8% (6%)

65 – 84% (75%)

0 – 16% (6)

0 – 27% (12%)

***

***

***

***

Goolwa FS - Goolwa

NO OBSERVATIONS (potential food sources – Amphipoda, Australonereis, Simplisetia and Nephtys)

Goolwa FS - Mundoo

24 – 27% (26%)

56 – 73% (65%)

1 – 10% (3%)

0 – 16% (5%)

***

***

***

***

Pelican Pt. FS – Pelican Pt.

0 – 1% (0%)

88 – 95% (92%)

0 – 7% (2%)

0 – 11% (4%)

0 – 5% (1%)

***

***

***

Long Pt. FS – Long Pt.

NO OBSERVATIONS (potential food sources – Capitella, Australonereis and Simplisetia)

Long Pt. FS – Pelican Pt.

0 – 1% (0%)

92 – 99% (95%)

0 – 5% (1%)

0 – 6% (1%)

0 – 6% (1%)

***

***

***

Long Pt. FS - Noonameena

NO OBSERVATIONS (potential food sources – Capitella, Chironomid and Parartemia)

Hardyhead

Noonameena FS- Noonameena

***

63 – 76% (70%)

***

***

***

***

0 – 10% (5%)

24 – 27% (25%)


Table 3.4. Black bream: Distribution of feasible co ntributions to black bream diet from food sources c ollected from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in brackets. * Denotes that the tissue samples were from small bl ack bream when compared to the other specimens. (*** denotes organism not collected at t hat location).

Species

Location of consumer &

food source (FS)


Crab

Ficopomatus

Juvenile Crab

Congolli

Hardyhead

Goby Nephtys

Macrobrachium

Sandy sprat

Juvenile fish

Mundoo * FS - Mundoo

NO OBSERVATIONS (potential food sources – Crab, Ficopomatus, Juvenile crab, Congolli, Hardyhead, Goby, Nephtys and Macrobrachium)

Mundoo * FS – Pelican Pt.

NO OBSERVATIONS (potential food sources – Crab, Ficopomatus, Juvenile crab, Congolli, Hardyhead, Goby, Nephtys and Macrobrachium)

Mundoo * FS - Goolwa

0 – 2%

(2%)

46 – 55% (50%)

***

***

0 – 2% (0%)

0 – 4% (0%)

0 – 4% (0%)

0 – 6% (0%)

42 – 48% (44%)

0 – 8% (2%)

Goolwa FS - Goolwa

0 – 4%

(0%)

0 – 2% (0%)

***

***

0 – 32% (18%)

0 – 16% (2%)

0 – 6% (0%)

0 – 8% (0%)

32 – 64% (52%)

0 – 64% (24%)

Black Bream


0 – 0%

(0%)

42 – 52% (48%)

0 – 6% (2%)

0 – 4% (0%)

0 – 4% (0%)

44 – 48%

(46%)

0 – 4% (0%)

0 – 10% (2%)

***

***


Table 3.5. Greenback flounder: Distribution of feas ible contributions to flounder diet from food sourc es collected from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in bra ckets. (*** denotes organism not collected at that location).

Species


food source (FS)


Amphipoda

Capitella

Phyllodoce

Nephtys Simplisetia

Australonereis Oligochaete

Juvenile crab

Mundoo FS - Mundoo

0 – 3% (0%)

23 – 61% (43%)

0 – 40% (14%)

0 – 67% (40%)

***

***

***

0 – 4% (0%)

Goolwa FS - Goolwa

NO OBSERVATIONS (potential food sources – Amphipoda, Australonereis, Simplisetia, Juvenile crabs and Nephtys)

Goolwa FS - Mundoo

NO OBSERVATIONS (potential food sources – Amphipoda, Capitellas, Phyllodoce, Juvenile crab and Nephtys)

Goolwa. FS – Pelican Pt.

0 – 22% (6%)

0 – 60% (24%)

0 – 20% (4%)

0 – 24% (6%)

0 – 74% (16%)

***

0 – 66% (30%)

0 – 22% (4%)


0 – 18% (4%)

0 – 50% (16%)

0 – 12% (2%)

0 – 14% (2%)

0 – 50% (10%)

***

22 – 80% (54%)

0 – 14% (2%)

Mundoo FS – Mundoo

0 – 11% (6%)

76 – 92% (84%)

0 – 8% (2%)

0 – 13% (4%)

***

***

***

0 – 2% (0%)

Goolwa FS - Goolwa

0 – 45% (17%)

***

***

15 – 45% (30%)

0 – 51% (27%)

0 – 31% (12%)

***

0 – 32% (12%)

Flounder 160–360mm

Flounder 50–100mm


12 – 22% (14%)

0 – 24% (4%)

0 – 6% (0%)

0 – 6% (0%)

0 – 24% (14%)

52 – 84% (70%)

0 – 6% (2%)


Table 3.6. Mulloway: Distribution of feasible contr ibutions to mulloway diet from food sources collect ed from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in brackets. ( *** denotes organism not collected at that location ).

Species


food source (FS)


Crab

Mullet

Juvenile Crab

Congolli

Hardyhead

Goby Nephtys

Macrobrachium

Sandy sprat

Mundoo FS - Mundoo

NO OBSERVATIONS (potential food sources – Crab, Mullet, Juvenile crab, Congolli, Hardyhead, Goby, Nephtys and Macrobrachium)

Mundoo FS - Goolwa

0 – 10% (2%)

0 – 56% (26%)

0 – 10% (2%)

0 – 36% (8%)

0 – 30% (6%)

0 – 26% (4%)

***

0 – 20% (4%)

24 – 54% (40%)

Mundoo FS – Pelican Pt.

0 – 34% (6%)

10 – 28% (20%)

0 – 38% (18%)

0 – 26% (6%)

0 – 26% (6%)

0 – 38% (8%)

0 – 42% (8%)

0 – 50% (16%)

***

Goolwa FS - Goolwa

0 – 22% (4%)

0 – 42% (10%)

0 – 22% (8%)

0 – 32% (6%)

0 – 26% (6%)

0 – 34% (6%)

***

0 – 40% (10%)

18 – 50% (38%)

Goolwa FS - Mundoo


Goolwa FS – Pelican Pt.

14 – 46% (38%)

0 – 4% (0%)

4 – 42% (28%)

0 – 18% (2%)

0 – 14% (2%)

0 – 12% (2%)

0 – 48% (10%)

0 – 48% (10%)

***


0 – 40% (8%)

8 – 30% (20%)

0 – 32% (12%)

0 – 32% (8%)

0 -32% (8%)

0 – 44% (10%)

0 – 48% (10%)

0 – 40% (14%)

***

Pelican Pt. FS – Mundoo


Mulloway

Pelican Pt. FS – Goolwa

0 – 10% (2%)

14 – 74% (46%)

1 – 10% (2%)

0 – 36% (6%)

0 – 32% (6%)

0 – 24% (4%)

***

0 – 18% (4%)

8 – 40% (22%)


Table 3.7. Yelloweye mullet: Distribution of feasib le contributions to yelloweye mullet (>250mm) diet from food sources collected from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in b rackets. (*** denotes organism not collected at tha t location).

Species

Location of consumer & food source

(FS)


Amphipoda Capitella Phyllodoce

Nephtys Simplisetia Australonereis Oligochaete Juvenile crab

Macrobrachium

Mundoo FS - Mundoo

0 – 34% (12%)

0 – 32% (8%)

0 – 44% (16%)

0 – 44% (12%)

***

***

0 – 32% (8%)

0 – 48% (14%)

0 – 46% (20%)

Mundoo FS – Goolwa.

0 – 22% (6%)

***

***

0 – 30% (16%)

0 – 26% (14%)

0 – 36% (10%)

***

0 – 34% (12%)

32 – 62% (50%)


NO OBSERVATIONS (potential food sources – Amphipoda, Australonereis, Simplisetia, Capitella, Phyllodoce, Macrobrachium, Oligochaete, Juvenile crabs and

Nephtys) Goolwa

FS – Goolwa. 0 – 22%

(6%)

***

*** 0 – 26%

(8%) 0 – 16%

(4%) 0 – 36% (16%)

***

0 – 34% (12%)

32 – 62% (50%)

Goolwa FS - Mundoo

0 – 24% (6%)

0 – 54% (24%)

0 – 26% (8%)

0 – 36% (10%)

***

***

0 – 56% (26%)

0 – 36% (10%)

0 – 24% (6%)



Nephtys) Pelican Pt.

FS – Pelican Pt. NO OBSERVATIONS

(potential food sources – Amphipoda, Australonereis, Simplisetia, Capitella, Phyllodoce, Macrobrachium, Oligochaete, Juvenile crabs and Nephtys)

Pelican Pt. FS – Goolwa.

0 – 48% (22%)

***

***

0 – 42% (14%)

0 – 34% (12%)

0 – 36% (12%)

***

0 – 36% (12%)

24 – 56% (42%)

Mullet >250mm

Pelican Pt. FS - Mundoo.

0 – 20% (4%)

2 – 68% (38%)

0 – 22% (4%)

0 – 32% (8%)

***

***

0 – 64% (30%)

0 – 26% (6%)

0 – 14% (2%)


Table 3.8. Yelloweye mullet: Distribution of feasib le contributions to yelloweye mullet (120 - 240mm) diet from food sources collected from sites based o n δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in b rackets. (*** denotes organism not collected at tha t location).

Species


(FS)




Macrobrachium

Mundoo FS - Mundoo

10 – 12% (10%)

86 - 90% (88%)

0 – 0% (0%)

0 – 0% (0%)

***

***

0 – 0% (0%)

0 – 4% (2%)

0 – 0% (0%)

Mundoo FS – Goolwa.

0 – 44% (14%)

***

***

0 – 52% (24%)

0 – 44% (18%)

0 – 34% (10%)

***

0 – 34% (12%)

0 – 38% (16%)



Nephtys) Goolwa

FS – Goolwa. 0 – 42% (12%)

***

***

0 – 54% (26%)

0 – 42% (16%)

0 – 34% (12%)

***

0 – 34% (10%)

0 – 40% (18%)

Goolwa FS - Mundoo

4 – 14% (10%)

80 - 88% (84%)

0 – 2% (0%)

0 – 4% (0%)

***

***

0 – 56% (26%)

0 – 12% (2%)

0 – 2% (0%)

Mullet 120 -

240mm



Nephtys)


Table 3.9. Yelloweye mullet: Distribution of feasib le contributions to yelloweye mullet (<80mm) diet f rom food sources collected from sites based on δ13C and δ15N values. Ranges: 1 and 99 percentiles. Median in b rackets. (*** denotes organism not collected at tha t location).

Species


(FS)




Macrobrachium

Mundoo FS - Mundoo

0 – 34% (12%)

24 – 62% (48%)

0 – 44% (16%)

0 – 44% (12%)

***

***

0 – 32% (8%)

0 – 48% (14%)

0 – 16% (10%)

Goolwa FS – Goolwa.

NO OBSERVATIONS (potential food sources – Amphipoda, Australonereis, Simplisetia, Juvenile crabs and Nephtys)

Goolwa FS - Mundoo

42 – 52% (47%)

28 - 82% (62%)

0 – 13% (3%)

0 – 9% (2%)

***

***

0 – 4% (2%)

0 – 6% (2%)

0 – 2% (0%)

Mullet <80mm


12 – 28% (18%)

32 – 64% (48%)

0 – 28% (10%)

0 – 9% (3%)

0 – 16% (8%)

1 – 13% (6%)

0 – 22% (8%)

0 – 2% (0%)

0 – 4% (2%)


3.4. Discussion

Geddes and Francis (2008) undertook a trophic ecology pilot study at Pelican Point, in which they recorded that the diet of small-bodied fish (hardyheads and small mullet), was composed mainly of amphipods, Capitella and other polychaetes, based on stomach content analysis. These observations are generally consistent with the result of this study, however, Amphipoda were not represented strongly in the feasible model outputs. Mulloway was the top predator, with mullet, crabs and congolli as important prey (Geddes and Francis 2008). They also noted that mulloway preyed heavily on crabs at certain times, especially when they were abundant after moulting. SIA analysis complements these types of study by quantifying over longer periods of time to what extent different types of prey are assimilated.

When an organism shifts its diet to a food source with a unique/different isotopic signature to its previous food source, two mechanisms (growth and tissue turnover) exist that contribute towards the change in its isotopic signature (Jardine et al. 2003). An alteration in the isotopic signature will occur during rapid growth periods due to the ‘dilution’ of the previous isotopic signature by adding tissue of differing isotopic composition. The second mechanism is a result of metabolic turnover, which involves the replacement of old tissue with new tissue of a different isotopic signature, and can occur with no net growth in the animal (Jardine et al. 2003).

Without making any direct statements regarding the movement of fish species within the Coorong through space and time, and taking into account that the baseline isotopic signatures of the food webs change along the Coorong salinity gradient (Deegan et al. Part 1 of this Report), feasible model outputs have been generated for a number of fish species using food resources from different locations to where those fish species were sampled. The isotopic signatures of those fish would have reflected the food resources that they had consumed provided that there had been a sufficient period to allow the turnover of their tissue to reflect that resource (Bosley et al. 2002; Perga and Gerdeaux 2005; Post 2002). Where fish are moving regularly between sites, as is likely the case for large Mulloway, the isotopic signature is likely to reflect incorporation of food from a combination of sites.

Turnover rates of tissue generally vary during an organisms life, being proportional to growth rate (Bosley et al. 2002). For example, muscle turnover rates can vary from ~2 d for red drum larvae (Herzka and Holt 2000) to >1 yr for adult broad whitefish (Bosley et al. 2002).Turnover rates of tissue will also be quicker in the spring and summer growth periods (Perga and Gerdeaux 2005), and as the sampling of the Coorong was carried out in late spring, the consumer signatures will reflect those of relatively recent resources.

Previous investigations have shown that the time required for tissues of juvenile fishes to reflect a diet shift is short relative to the time required by adult fishes. Presumably this observation is a reflection of the rapid relative growth rate of the juveniles (Bosley 1998). Hardyhead sampled at both Goolwa and Long Point, together with juvenile mullet (<80mm) sampled at Goolwa, all provided feasible model outputs with resources from alternate locations to where they were sampled, but in relatively close proximity. Hardyhead from other sites, juvenile mullet and juvenile flounder provided feasible model outputs with resources from the location where they were sampled. This would suggest that those juvenile fishes have relatively fast turnover rates, possibly weeks (Bosley et al. 2002) and also had restricted their movements to remain within the specified location prior to sampling.

The more mature/larger fish specimens sampled would have had slower tissue turnover rates (Bosley et al. 2002; Perga and Gerdeaux 2005), and feasible model outputs were generated with resources from alternate locations to where the specimens were sampled. Feasible model outputs were generated for black bream sampled at Mundoo using food resources from Goolwa, suggesting that those black bream had spent a significant period of time feeding in Goolwa Channel. The isotopic signatures of large flounder sampled at Goolwa reflected the source signatures from Pelican Point. Mulloway, being the largest predatory species found within the Coorong, can reasonably be assumed to move between locations with relative ease. Model outputs were generated for mulloway sampled at Mundoo, Goolwa and Pelican Point


using food resources form both Goolwa and Pelican Point. No model outputs were generated using resources from Mundoo even for those mulloway sampled at Mundoo. This would suggest that mulloway found within the Coorong were feeding throughout the region between Goolwa Channel and Pelican Point, but not at Mundoo Channel, at least not substantially.

Of course when the isotopic signatures of high order consumers cannot be explained by the isotopic signature of organisms at lower trophic levels then it must be questioned whether all possible food sources were sampled or whether fish movement has contributed to the discrepancy. In this case we concluded that fish had been feeding at different sites to where they were captured. Given the constraints under which we ran the ISOSOURCE model we considered combinations that added to within 0.01‰ of the consumer signature were feasible solutions. If potential food sources were omitted from the sampling then it is very likely that no feasible model outputs would have been generated at all. That is not to say that all potential food sources were collected in every case, but in this case we consider that the large fish had probably been feeding in several locations for a sufficient period of time to enable them to reflect the signatures from those locations.

Stable isotopes are especially powerful when used along environmental gradients with differing baseline signatures for determining the locations of the food resources consumed. Across ecosystems with environmental gradients this could become a very useful tool in determining those parts of that ecosystem which are important feeding grounds, supporting extensive communities, as opposed to other parts of that ecosystem which are less productive.

3.5. Conclusion

Using stable isotope analysis of fish tissue it is apparent that the food resources supporting the large fish communities were not restricted to where the fish were captured. Smallmouth hardyhead at both Goolwa and Long Point and juvenile mullet (<80mm) sampled at Goolwa all provided feasible model outputs with resources from alternate locations to where they were sampled, but in relatively close proximity. Hardyhead from other sites, juvenile mullet and juvenile flounder provided feasible model outputs with resources from the location where they were sampled suggesting they had restricted their movements to remain within the specified location prior to sampling.

When managing ecosystems, such as the Coorong for maintenance of fish populations it is important to consider their dietary needs. It is apparent from this study that the large bodied fish may move considerable distance and utilise a number of sites for feeding. Conservation therefore needs to recognise the importance of expansive available habitat for large bodied fish in addition to site specific habitat maintenance for the smaller bodied organisms.


General Conclusion

The combination of fish and invertebrate surveys, SIA analysis, and fish stomach content analysis has provided useful insights into the food webs supporting large benthic-feeding and piscovorous fish in the Coorong. This study demonstrated that the baseline signature of the aquatic food web varied along the salinity gradient, and this feature was exploited to determine where fish were feeding. The Coorong food web became shorter and larger fish appear to increase omnivory with increasing salinity (Fig. 4.1), suggesting that the habitat quality was lower at higher salinities. This is in addition to large fish only being able to use a small fraction of the Coorong at the time of the study due to the prevalence of hypersalinity.

This study focussed on the food web leading to fish only, but it is recognised that aquatic birds are a very important part of the food web in this ecosystem (Phillips and Muller 2006). In some instances, some bird species probably benefit from the absence of large fish in parts of the Coorong. For example, piscivorous birds can feed on the large density of smallmouth hardyheads which can be found in areas of the Coorong that are too saline for piscivorous fish (Noell et al. 2009; Roger and Paton 2009b). This suggests that there may be trade-offs between the size of piscivorous fish and piscivorous bird populations in the Coorong.

While River Murray inflows are likely to benefit fish populations in the Coorong by expanding the area with suitable salinity levels, it is less clear if riverine flows would also benefit the food webs leading to fish by providing an organic matter subsidy in the form of detritus, phytoplankton, zooplankton and prey fish exported from the upstream Lower Lakes (Aldridge et al. 2009; Gillanders and Kingsford 2002). Likewise, it is also unclear how the current food webs in the Coorong have been impacted by the nearly complete loss of the Ruppia beds that formerly covered large parts of the system (Rogers and Paton 2009a,b). In addition to providing a source of organic matter, beds of large aquatic plants can provide a habitat for a range of invertebrate and small fish species. What kind of food web would be associated with Ruppia in the Coorong could not be evaluated because Ruppia and other large aquatic plants had been largely extirpated from the system at the time of the study (Rogers and Paton 2009a,b).

The overall conclusion from the study is that both the extent and the quality of habitat for larger fish species were impacted by elevated salinity in the Coorong.

Recommendations

Future interventions aiming to lower salinity in the Coorong should be used to test some of the hypotheses about the structure of its food webs. These hypotheses include that:

• Fish populations will benefit from lower salinity in the Coorong both from the expansion of their range and by having access to a larger diversity of prey within their range;

• Freshwater inflows from the River Murray would directly subsidise the Coorong food web through the input of organic matter (including dissolved organic matter, phytoplankton, zooplankton, etc);

• The reestablishment of Ruppia and other large aquatic plants would foster a more diverse food web, a longer food chain and a greater fish biomass in the Coorong by providing habitat (as shelter and food resources) for their prey.


Figure 4.1. Guild-specific food webs in the Coorong at different salinity levels. The trophic position for the invertebrate and fish guilds was e stimated from the 15N enrichment values of representative species within the guild. The “inve rtebrates” guild includes all invertebrate taxa that were assumed to be primary consumers (grazers, filter feeder, etc). The “predatory invertebrates” guild includes larger omnivorous or predatory invertebrate species such as Nephtys and Macrobranchium. The “benthic feeders” guild includes smaller fis h species, such as smallmouth hardyhead and Tamar goby, or smaller siz e-classes of larger fish species. The piscivorous fish guild represents mainly black brea m and mulloway. Also included is the hypothesised trophic position and trophic relation (dashed lines) for “waders” (various species of shorebirds) and “piscivorous birds” (including tern s, Australian Pelican, etc). The trophic position of grazing birds (many ducks, swans and ge ese) is not included here as their principal food source (aquatic plants) was not represented.

Tro

phic

Leve

l

2

5

4

3

Marine/Slightly hypersaline(<2x seawater)

Moderately hypersaline

Invertebrates

(2-4x seawater) (>4x seawater)

Extremely hypersaline

InvertebratesInvertebrates

PredatoryInvertebrates

Benthic feeders

(Waders)

(Waders)(Waders)

Piscivorous fish

(Piscivorousbirds)

(PiscivorousBirds)

Benthic feeders

Tro

phic

Leve

l

2

5

4

3

Marine/Slightly hypersaline(<2x seawater)

Moderately hypersaline

Invertebrates

(2-4x seawater) (>4x seawater)

Extremely hypersaline

InvertebratesInvertebrates

PredatoryInvertebrates

Benthic feeders

(Waders)

(Waders)(Waders)

Piscivorous fish

(Piscivorousbirds)

(PiscivorousBirds)

Benthic feeders


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