Recovery of nitrogen stable isotope signatures in the food web of an intermittently open estuary following removal of wastewater loads

Accepted Manuscript Recovery of nitrogen stable isotope signatures in the food web of an intermittently open estuary following removal of wastewater loads Phoebe E. Smith, Joanne M. Oakes, Bradley D. Eyre PII:

S0272-7714(16)30432-2

DOI:

10.1016/j.ecss.2016.10.003

Reference:

YECSS 5262

To appear in:

Estuarine, Coastal and Shelf Science

Received Date: 4 April 2016 Revised Date:

18 August 2016

Accepted Date: 4 October 2016

Please cite this article as: Smith, P.E., Oakes, J.M., Eyre, B.D., Recovery of nitrogen stable isotope signatures in the food web of an intermittently open estuary following removal of wastewater loads, Estuarine, Coastal and Shelf Science (2016), doi: 10.1016/j.ecss.2016.10.003. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Graphical Abstract

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Recovery of nitrogen stable isotope signatures in the food web of an intermittently open estuary

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1,*

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Phoebe E. Smith , Joanne M. Oakes , Bradley D. Eyre

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following removal of wastewater loads

Centre for Coastal Biogeochemistry, School of Environment, Science and Engineering, Southern Cross University, PO Box 157, Lismore, New South Wales, Australia

Email addresses:

[email protected]

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[email protected]

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[email protected]

*Corresponding author:

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Phone: +61 (0) 2 6620 3092

Email address: [email protected] Postal Address: PO Box 157, Lismore, NSW, Australia 2480

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Abstract Nitrogen (N) stable isotope values (δ15N) were used to assess the removal of wastewater N from the food web within Tallow Creek, a small intermittently closed/open lake/lagoon (ICOLL) on the east

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coast of Australia, following the cessation of wastewater inputs in 2005. Current (2013) δ15N values of sediment organic carbon, plants, and animals within Tallow Creek were compared to values obtained before wastewater inputs ceased, and to values within a nearby near-pristine ICOLL

(Jerusalem Creek). Most biota had significantly depleted δ15N values compared to conspecifics

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collected before wastewater inputs ceased (mean reduction of 6.0‰; 38% of impacted enrichment), indicating substantial loss of wastewater N since inputs ceased. However, δ15N values remained

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enriched compared to the near-pristine ICOLL for some components (mean enrichment of 3.3‰ or 38%), suggesting that some wastewater N remains. The δ15N recovery rate (decrease in δ15N as a percentage of the impacted enrichment) for Tallow Creek biota was slow compared to that of biota in more open systems. This slow recovery rate and the persistence of some wastewater N, even after 8 years without new inputs, reflects differences in hydrology and nitrogen cycling between permanently

to anthropogenic N inputs.

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open and intermittently open estuarine systems and highlights the likely lower resilience of ICOLLs

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Key words: nitrogen isotopes; food webs; waste water; recovery, ICOLL; Australia

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1.0 Introduction Anthropogenic activities have profoundly altered the cycling of nitrogen (N) in the biosphere (Rockström et al. 2009), contributing large amounts of bioavailable N that impact ecosystems

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worldwide (Vitousek et al. 1997; Canfield et al. 2010). A major source of anthropogenic N to coastal systems is wastewater effluent (McClelland et al. 1997; Eyre and McKee 2002; Ferguson et al., 2004a; Schlacher et al. 2005). Although wastewater N can support ecosystem productivity by

providing a source of nutrients for primary producers that support higher consumers, nutrient over-

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enrichment is a major threat to aquatic ecosystems (Cloern 2001). Because plant growth in coastal systems is often limited by the availability of N (Costanzo et al. 2001), nutrient over-enrichment

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due to wastewater inputs may lead to eutrophication (excess production of organic matter). Decomposition of this excess organic matter leads to deoxygenation and recycling of nitrogen, which combined with the loss of key ecosystem processes such denitrification, may further stimulate excess production of organic matter (Anderson et al. 2002; Ferguson et al., 2004b; Eyre and Ferguson, 2009). It is therefore crucial to monitor the impacts of changes in wastewater

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discharge on aquatic ecosystems. However, management of wastewater-affected systems often focuses simply on improving the quality, and/or reducing the quantity of wastewater inputs (Wulff et al., 2011). Relatively few studies have assessed the recovery of ecosystems following reduction or removal of wastewater inputs (e.g. Rogers 2003; Pitt et al. 2009).

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The rate of ecosystem recovery following reduction of wastewater input is likely to be influenced by a number of factors, including system flushing, wastewater N load, N burial and

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storage, and the period of time over which wastewater inputs have occurred (Eyre 2000; Cloern 2001; Hadwen and Arthington 2006; Eyre et al., 2016a). Open systems such as permanently open estuaries and the open coast are flushed frequently, allowing constant dilution and distribution of wastewater effluent (e.g. Eyre and Twigg 1997; Oakes and Eyre 2015). In contrast, intermittently closed/opened lakes/lagoons (ICOLLs) are likely to retain wastewater N for longer periods, due to their isolation from the ocean, which leads to extended water residence times and infrequent flushing (Everett et al. 2007). ICOLLs are generally regarded as rare on a global scale (Haines 2008), but they are a 3

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prevalent feature along the coastline of New South Wales (NSW), Australia (Haines 2008; Maher et al. 2011). ICOLLs account for ~92% of all NSW estuarine waters (Williams et al. 1998) and 60% of all coastal waterways in southeastern Australia (Hadwen and Arthington 2006). Although

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long-term changes in the contribution of wastewater N to aquatic systems have been relatively well studied in open systems (e.g., Schlacher et al. 2001, 2005; Waldron et al. 2001; Pitt et al. 2009), there is little information regarding the effects of wastewater N on ICOLLs (Davis and Koop 2006; Everett et al. 2007; Hadwen and Arthington 2006; 2007) and how they recover

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following the removal of wastewater inputs.

One of the most common approaches used to detect wastewater in aquatic ecosystems is

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the analysis of nitrogen stable isotope ratios (Cabana and Rasmussen 1996; Pitt et al. 2009). Due to preferential removal of the light nitrogen isotope (14N) during wastewater treatment (Heaton 1986), wastewater N commonly has a distinct, 15N-enriched, δ15N value that can be traced through food webs. Numerous studies have used stable isotopes to trace wastewater in aquatic systems (e.g., Costanzo et al. 2001; Wayland and Hobson 2001; Connolly et al. 2013; Oakes and Eyre 2015), but

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few have investigated ecosystem recovery following wastewater reduction (Rogers 2003; Pitt et al. 2009). The few studies that have reported δ15N values following wastewater removal have assessed only relatively short-term changes and, although these studies looked at multiple biota at different trophic levels, the entire food web was not considered.

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Only one study has looked at the contribution of wastewater to an entire food web within an ICOLL (Tallow Creek, northern New South Wales, Australia; Hadwen and Arthington 2007).

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This study showed that wastewater N discharged into the ICOLL was assimilated and distributed throughout the entire food web. Furthermore, the δ15N signatures of biota at each trophic level were considerably more enriched in 15N than values reported for open systems receiving wastewater (e.g., rivers, deBruyn and Rasmussen 2002; permanently open estuaries, Costanzo et al. 2003, Schlacher et al. 2005; bays, Hansson et al. 1997, Waldron et al. 2001; exposed rocky shores, Oakes and Eyre 2015). The wastewater treatment plant (WWTP) that discharged into Tallow Creek was decommissioned in November 2005, resulting in cessation of wastewater inputs. Given that stable 4

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isotope data exists for the impacted ICOLL pre-WWTP removal (Hadwen and Arthington 2007), this provided the opportunity to assess, for the first time, the recovery of δ15N signatures at all trophic levels of the food web within an ICOLL following cessation of wastewater inputs.

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The aim of this study was to determine the level of removal of wastewater N by assessing the recovery of δ15N values of food web components within the Tallow Creek ICOLL ~ 8yrs after

cessation of wastewater inputs. The specific objectives were to (a) compare δ15N values of biota in Tallow Creek at the time of the study with conspecifics in Tallow Creek 8 years prior, during

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wastewater input, (b) compare δ15N values of biota in Tallow Creek at the time of the study and a nearby near-pristine ICOLL to determine if wastewater-derived nutrients are still present in the

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Tallow Creek food web ~8 yr after wastewater inputs ceased, (c) determine the rate of change (recovery) of δ15N values of biota at all trophic levels of the food web in Tallow Creek by comparing current δ15N values with those reported by Hadwen and Arthington (2006; 2007), and (d) compare the rate of recovery of δ15N values in Tallow Creek ICOLL and more open wastewater-impacted systems. It was hypothesised that the recovery rate of δ15N signatures in the

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ICOLL would be slower than in more open systems due to limited flushing. It was further hypothesised that δ15N signatures of biota and sediments would still have a wastewater signal,

2007).

2.0 Methods

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2.1 Study sites

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although this would be reduced compared to values reported by Hadwen and Arthington (2006;

Sites for the current study were located at the Tallow Creek and Jerusalem Creek ICOLLs, in northern NSW, Australia (28° 40’ 22.97” S, 153° 37’ 01.01” E and 29° 14’ 08.77” S, 153° 22’ 30.13” E, respectively; Figure 1). The two ICOLLs are in different hydrological catchments, but have a similar climate (Table 1).

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N

Tallow Creek

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1000 km

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1 km

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Jerusalem Creek

1 km

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Figure 1. The Tallow Creek and Jerusalem Creek ICOLLs. Inset map shows the location of the ICOLLs on the east coast of New South Wales, Australia. Data providers for inset images of Tallow

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Creek and Jerusalem Creek: Google, SIO, NOAA, U.S. Navy, NGA, GEBCO, DigitalGlobe, CNES/Astrium, TerraMetrics.

Tallow Creek is a small ICOLL (Table 1), which intermittently flows into the Pacific

Ocean, but is poorly flushed, with the mouth usually obstructed by a sandbar formed by northward littoral drift due to dominant south-easterly swells. For 32 years, until 2005, Tallow Creek received direct input of ~730 ML yr-1 secondary treated wastewater from the South Byron WWTP (M. Bingham, personal communication), equivalent to ~8-10 t N yr-1. This resulted in elevated

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concentrations of nutrients and algae in the ICOLL (McAlister et al. 2000). Even ~5 years after wastewater inputs ceased, total N concentrations exceeded maximum guideline (ANZECC 2000) values by >300%. Tallow Creek opened naturally approximately 15 times from 2007 to 2013 (J.

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Flockton, personal communication) and has sometimes been artificially opened. Tallow Creek was last opened artificially in November 2004, and was naturally opened one month prior to the current study (J. Flockton, personal communication).

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Table 1. Characteristics of the impacted system (Tallow Creek) and a near-pristine system (Jerusalem Creek) considered in the current study.

a

BOM (2014a)

b

BOM (2014b)

Jerusalem Creek (near-pristine) 29° 14’ 08.77” S 153° 22’ 30.13” E 4.8 0.3 178.9 48.3 1472.3 24.3 15.3

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Latitude Longitude Length (km) Area (km2) Volume (ML) Catchment area (km2) Mean annual rainfall (mm)a Mean annual maximum temperature (°C)b Mean annual minimum temperature (°C)b

Tallow Creek (impacted) 28° 40’ 22.97” S 153° 37’ 01.01” E ~3.2 0.1 46.6 5.3 1473.5 23.4 16.9

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Characteristic

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Jerusalem Creek has a relatively small catchment, although larger than that of Tallow Creek (Table 1). In contrast to Tallow Creek, Jerusalem Creek is as near as possible an

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undisturbed, pristine, natural waterway (McAlister et al. 2000). Its catchment is almost entirely within the Bundjalung National Park, with no identified sources of significant pollution (McAlister et al. 2000) and the creek complies with all water quality guidelines (McAlister et al. 2000; ANZECC 2000). Jerusalem Creek therefore served as a ‘control’ site, providing background isotope signatures for biota.

2.2 Sampling Strategy Samples of biota and sediment were collected from the mouth, and from the uppermost end of each

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ICOLL (~1 km and ~ 3 km upstream of the mouths of Tallow Creek and Jerusalem Creek, respectively), and from the WWTP outlet in Tallow Creek (as per Hadwen and Arthington 2007). Sampling in Tallow Creek occurred from 12th - 30th June 2013, during which time the entrance

during which time the entrance was open to the ocean.

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status changed from open to closed. Sampling in Jerusalem Creek occurred from 2nd - 4th July 2013,

At each location within the ICOLLs (i.e., mouth, WWTP, and upstream) the major primary producers were sampled as described by Hadwen and Arthington (2007). Where present, this

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included mangrove leaves (Avicennia marina), benthic fine particulate organic matter (FPOM), and benthic coarse particulate matter (CPOM), epilithon, filamentous algae, and suspended particulate

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organic matter (SPOM). FPOM and CPOM were collected by passing benthic sediments from the shoreline through a series of sieves (1 cm, 500 µm, and 250 µm). Material retained on the 250 µm sieve was retained as FPOM, and material on the 500 µm sieve as CPOM. Epilithon was removed from the sediment surface using forceps and a scalpel. Filamentous algae was collected from hard surfaces (e.g., mangrove pneumatophores, rocks and vegetative debris) using a scalpel and/or

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toothbrush. SPOM was collected from surface water using a plankton tow net (65 µm mesh size) hauled along a ~20 m transect at each location.

Fish (Sillago ciliata, Mugil cephalus, Ambassis marianus and Rhabdosargus sarba), prawns (Metapenaeus bennettae), and mud crabs (Scylla serrata) were collected using a 20 m

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seine net (6 mm mesh) trawled over mainly sandy substrates, preferably near littoral vegetation, submerged structures, rocks, and debris. Bloodworms (Glycera spp.) and yabbies (Trypaea

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australiensis) living within the sediment were collected using a yabby pump. Upon capture, animals were placed in a small volume of water in individual zip-lock bags, and then placed in ice slurry for immediate euthanasia. All samples were transported to the laboratory on ice and stored frozen until processed.

2.3 Sample processing The muscle tissue of fish and crustaceans was excised for analysis. All remaining samples, except sediments, were rinsed with distilled water to remove dirt and debris. All samples were dried in an 8

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oven (60°C, ≥ 48 h, to constant weight) then homogenised using a mortar and pestle. Subsamples of powdered material were weighed into tin capsules for analysis of δ15N.

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2.4 Sample analysis Samples were analysed for δ15N using an elemental analyser-isotope ratio mass spectrometer (Thermo Finnigan Flash Elemental Analyser 112 interfaced with a Thermo Delta V Plus IRMS via a Thermo Conflo III) (Eyre et al 2016b). Samples of acetanilide of known isotope composition were analysed

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periodically within the sample run to verify isotope signatures. Reproducibility for δ15N was ± 0.2‰. Isotope ratios are expressed in delta notation, with units of per mil (‰), according to the following

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equation:

δ15N = [(Rsample/Rstandard) – 1] × 1000

where Rsample is the ratio of heavy (15N) to light (14N) isotope for the sample and Rstandard is the ratio of

2.5 Data analysis

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heavy to light isotope in atmospheric N2.

An inability to capture or locate samples of each food web component across all locations prevented

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statistical comparison of locations within each ICOLL. However, the principal aim of this study was to determine if there were differences among three systems: Jerusalem Creek (control), Tallow Creek

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during wastewater input (Tallow Creek ‘During’), and Tallow Creek after wastewater input ceased (Tallow Creek ‘After’). For each food web component, data from all locations within each ICOLL (mouth, upstream and WWTP) were therefore combined and a one-way analysis of variance (ANOVA) was used to assess differences in δ15N among the three systems (control, Tallow Creek ‘After’, and Tallow Creek ‘During’). Data for Tallow Creek ‘During’ were those of Hadwen and Arthington (2006, 2007). The numbers of samples of each type collected from Tallow Creek ‘After’ and Jerusalem Creek are shown in Table A.1. Data were checked to ensure that the assumptions of an ANOVA were met. In some instances, Levene’s test indicated that variances were not homogeneous, 9

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and data were therefore transformed (log(x+1)) before analysis. Where ANOVAs revealed that there were significant differences among data sets (ɑ < 0.05), post-hoc Tukey tests showed which systems were different to one another.

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To increase the power of the analysis by effectively increasing replication, food web components were further pooled into functional groups, and one-way ANOVAs and post-hoc Tukey tests were used, as described above, to determine if δ13C and δ15N values within these functional

groups varied significantly among the three systems. Each functional group was comprised of food

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web components that were assumed to be at the same trophic level and obtain C and N via similar pathways. Functional groups were defined as: (1) Sediment (CPOM and FPOM), (2) Algae

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(filamentous algae and epilithon), (3) Fringing vegetation (mangroves, grasses, succulents), (4) Detritivorous fish (M. cephalus, Hadwen et al. (2007)), (5) Carnivorous fish (S. ciliata, Hadwen et al. (2007); A. marianus, Hurst et al. (2006); and R. sarba, Curley et al. (2013)), and (6) Crustaceans (M.

bennettae, S. serrata, and Trypaea australiensis). An additional one-way ANOVA was used to compare combined data for all food web components (‘Overall’) across the three systems. To ensure

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an even contribution of each food web component across all systems, the number of replicates of each sample type included in the analysis for each system was standardised by randomly selecting samples

3.0 Results

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to exclude from the analysis, for systems where more replicates were collected.

3.1 Comparison of isotope ratios in Tallow Creek ‘During’ and ‘After’ wastewater input

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At all trophic levels, δ15N values for food web components in Tallow Creek ‘After’ were 15Ndepleted compared to values in Tallow Creek ‘During’ (Figure 2). This depletion was substantial with an overall mean difference in δ15N of 5.0‰ for primary sources and 7.3‰ for consumers. The exception was seston, which had more enriched δ15N signatures in Tallow Creek 'After' than in Tallow Creek 'During' (Figure 2). In particular, epilithon, succulents, S. ciliata, S. serrata, Glycera spp. and M. bennettae all showed large decreases in δ15N ranging from 9.8‰ to 12.4‰ (Figure 2). The difference in δ15N between Tallow Creek ‘After’ and Tallow Creek ‘During’ was not significant for FPOM, CPOM, seston, Juncus sp., Cyperus spp, M. cephalus, and A. marianus. All 10

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other components were significantly 15N-depleted in Tallow Creek 'After' compared to Tallow Creek 'During' (Table 2). At the level of functional group, δ15N values in Tallow Creek ‘After’ were significantly 15N-depleted compared to Tallow Creek ‘During’ for all groups except

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sediment, detritivorous fish, and seston (Table 2). Comparison of all food web components combined confirmed that the overall food web in Tallow Creek was 15N-depleted in Tallow Creek

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‘After’ compared to Tallow Creek ‘During’ (Table 2).

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Figure 2. Comparison of mean (± SE) δ15N values of food web components collected within Tallow Creek 'During' and 'After' wastewater input, and within Jerusalem Creek, a nearby near-pristine ICOLL. Data for Tallow Creek ‘During’ wastewater input is taken from Hadwen and Arthington 2006, 2007).

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Table 2. Summary of results of ANOVA and Tukey tests comparing δ15N signatures of food web components across all sampling sites within Tallow Creek ‘During’ and ‘After’ impact (wastewater

ANOVA p-value

Sediment FPOM CPOM

2,16 2,6 2,6

0.040 0.076 0.470

Seston

2,12

0.826

Algae Epilithon Filamentous

2,15 2,2 2,11

<0.001* 0.008* 0.008*

Fringing vegetation Avicennia marina Succulents Juncus sp. Cyperus spp.

2,35 1,13 2,11 2,2 2,3

Detritivorous fish Mugil cephalus

0.244 0.354 0.668

0.033* 0.065 0.460

0.305 0.286 0.846

0.952

0.817

0.002* 0.008* 0.029*

<0.001* 0.010*

0.540 0.719

<0.001* 0.001* 0.003* 0.278 0.023*

<0.001* 0.001* 0.003* 0.278 0.078

<0.001* 0.018* 0.020*

0.019* 0.994 0.193

2,18

0.178

0.178

-

-

2,31 1,3 1,18 2,20

<0.001 0.605 0.023* <0.001*

<0.001 0.605 0.023* <0.001*

<0.001 <0.001*

0.019 <0.001*

Crustaceans Metapenaeus bennettae Scylla serrata Trypaea australiensis

2,19

<0.001* -

<0.001* -

<0.001* -

<0.001* -

Infauna (Glycera spp.)

1,12

<0.001*

<0.001*

-

-

Overall

2,60

<0.001*

0.001*

<0.001*

0.255

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0.973

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Carnivorous fish Ambassis marianus Rhabdosargus sarba Sillago ciliata

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Consumers

p-values of Tukey comparisons During During vs After vs vs After Jerusalem Jerusalem

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df

Sources

Food web component

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input), and within the near-pristine Jerusalem Creek ICOLL.

- = ≤ 1 replicate within at least one system * significant at alpha = 0.05

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3.2 Comparison of isotope signatures in Tallow Creek ‘After’ and Jerusalem Creek The Tallow Creek 'After' food web appeared more 15N-enriched than the 'Jerusalem' Creek food web

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at all trophic levels and in all food web components, with enrichment of ~2.8 ‰ for primary sources (mean) and ~4.3‰ for consumers (Figure 2). In particular, FPOM, epilithon, Cyperus spp., and M.

cephalus showed substantial enrichment in δ15N ranging from 4.1‰ to 6.6‰ (Figure 2). However, few of these differences were statistically significant.

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Overall, the food web in Tallow Creek ‘After’ was not significantly 15N-enriched

compared to that in the Jerusalem Creek control. However, one-way ANOVAs indicated that S.

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ciliata, and the functional groups ‘Crustaceans’ and ‘Fringing vegetation’, and ‘Carnivorous fish’ were significantly 15N-enriched in Tallow Creek 'After' relative to the Jerusalem Creek control system (Table 2). All other food web components did not differ significantly between the two systems and/or were unable to be analysed statistically (Table 2).

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4.0 Discussion

4.1 Changes in δ15N signatures in Tallow Creek

After 8 years without treated wastewater input, there appears to have been considerable removal of wastewater N from the Tallow Creek ICOLL. Whereas Hadwen and Arthington (2007)

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reported significantly enriched δ15N values for almost all food web components collected in Tallow Creek ‘During’ compared to a control ICOLL (Belongil Creek), reflecting wastewater N input to the

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ICOLL, few food web components remained significantly enriched in Tallow Creek ‘After’. Overall, there was a mean reduction of 6.0 ‰ (38%) in δ15N of Tallow Creek food web components from ‘During’ to ‘After’, with δ15N signatures of all food web components, except seston, substantially depleted compared to values recorded while wastewater was still being discharged to Tallow Creek. For most food web components, δ15N values in Tallow Creek ‘After’ were statistically similar to those in the near-pristine Jerusalem Creek ICOLL, suggesting that the majority of wastewater N may have been removed from the Tallow Creek system. However, there is evidence that some wastewater N remained, with carnivorous fish including S. ciliata, fringing vegetation, and 13

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crustaceans in Tallow Creek ‘After’ significantly 15N-enriched compared to conspecifics in the nearpristine Jerusalem Creek ICOLL, and sediment δ15N values in Tallow Creek ‘After’ intermediate to those in Tallow Creek ‘During’ and Jerusalem Creek,. Although not statistically significant in all

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N-enriched, on average, compared to the Jerusalem Creek food web.

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cases, the Tallow Creek ‘After’ food web components considered in this study remained 3.3 ‰ (38%)

The conclusion that some wastewater N remains in the Tallow Creek ICOLL is based on two assumptions: (1) δ15N values in the Jerusalem Creek ICOLL represent non-impacted values for

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Tallow Creek, and (2) elevated 15N values within Tallow Creek are due to remaining wastewater N.

These assumptions may not be valid if, for example, local geology and environmental conditions alter

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non-impacted δ15N values within Jerusalem Creek and Tallow Creek, or if there are continuing inputs of 15N-enriched N inputs from the urban area adjacent to Tallow Creek. However, the comparison of δ15N values in Tallow Creek and a number of other systems supports the retention of wastewater N within Tallow Creek ‘After’. Values of δ15N for all fish and prawn species captured in Tallow Creek ‘After’ were 15N-enriched compared to values in nearby systems (within 300 km) with little or no

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wastewater N (e.g., Noosa estuary, Schlacher et al. (2005); Mooloolah estuary, Schlacher et al. (2001), Schlacher and Caruthers (2002); and Belongil Creek, where wetlands remove nutrients from effluent, Hadwen and Arthington (2007) (Figure 4)). The persistence of relatively enriched δ15N values in some food web components in Tallow

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Creek ‘After’, suggests that there was recycling of wastewater N within the Tallow Creek food web over the 8 years following cessation of wastewater discharge. This is consistent with the hypothesis

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that ICOLLs take longer to recover from N input. Furthermore, δ15N values for S. ciliata and M.

cephalus in Tallow Creek ‘After’ were similar to values for conspecifics in the nearby wastewaterimpacted Maroochy estuary (Figure 4), which is an open estuary. This further supports the assertion that enriched δ15N values within Tallow Creek ‘After’ are due to retention of wastewater N. Although δ15N enrichment within a system due to wastewater input depends on a combination of the wastewater load, its δ15N value, within-system processing, and flushing, the similarity of δ15N values in Tallow Creek 8 years after wastewater inputs ceased, and δ15N values for an open system currently receiving wastewater highlights the potential for the poor flushing of ICOLLs to contribute to greater 14

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wastewater N retention than occurs in more open systems.

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Figure 4. A comparison of mean (± SE) δ15N signatures for Tallow Creek ‘During’ and ‘After’ to an estuary receiving wastewater (Maroochy River, Queensland, Australia), and estuaries receiving

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little or no wastewater input (Mooloolah estuary and Noosa estuary, in Queensland, Australia, and Belongil Creek and Jerusalem Creek, in New South Wales, Australia). Data for the Noosa, Mooloolah and Maroochy estuaries are taken from Schlacher et al. (2005). Data for the Belongil ICOLL are taken from Hadwen and Arthington (2007).

The intermediate δ15N value for sediment suggests that it is a potential long-term storage compartment for N, most likely through burial of particulate organic matter incorporating N derived from wastewater (Savage et al. 2004). This is consistent with the inference of Pitt et al. (2009), that

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wastewater N was likely to be retained within sediments up to two years after reduction of wastewater inputs to the Brisbane River estuary, even though that estuary is permanently open. Retention of wastewater N would be particularly pronounced in vegetated sediments (Eyre et al., 2016a), where

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plants are likely to have contributed to increased sediment deposition during wastewater input, and would have subsequently protected sediments from scouring, resuspension, and loss during flushing

of the ICOLL once inputs ceased (Yang et al. 2008). This may explain the presence of wastewater N

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particularly within fringing vegetation, which would utilise the sediment as a source of N.

4.2 Nitrogen uptake and removal (recovery) rates in open systems and ICOLLs

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Flushing time and dilution capacity are important controls on wastewater N uptake and, ultimately, the recovery of impacted systems following wastewater reduction or removal. The δ15N values reported for Tallow Creek ‘During’ were relatively enriched compared to other impacted systems, owing primarily to its small volume (46.6ML; Roper et al. 2011), which limited dilution, and extended water residence time. The creek is only episodically flushed ~ 2 times per year, with no

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significant flow at other times. Based on the inputs of ~8.5 t N yr-1 to Tallow Creek ‘During’ and a total volume of new water of 139.8 ML yr-1 (46.6 ML × 3, allowing for total replacement of water twice per year via flushing), wastewater N was discharged to Tallow Creek at the rate of ~6.1 g N L. In comparison, although the Brisbane River estuary (~130 km north of Tallow Creek) is

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completely flushed only ~1 time per year (Hossain et al. 2004), its considerable volume (~130 000 ML; Hossain et al. 2004) means that wastewater N was discharged at a rate of only 0.2 g N L-1

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before a WWTP upgrade (Pitt et al. 2009), and 0.04 g N L-1 after the upgrade. This difference in wastewater N dilution contributed to δ15N values for biota in the Brisbane River, pre-upgrade, that were less 15N-enriched than those seen in Tallow Creek ‘During’ (Pitt et al. 2009, Hadwen and Arthington 2007). Similarly, δ15N values in Tallow Creek ‘During’ were, on average, ~4.3 ‰ more enriched in 15N compared to those in the Maroochy Estuary in 2000-2001 (Figure 4). At that time, the Maroochy Estuary received about 5× more wastewater N than Tallow Creek ‘During’ but had a much shorter water residence time (flow of 1.8 m3 s-1, flushing rate of 74 days; Schlacher et al.

16

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2001). The mobility of animals may also contribute to differences in uptake of wastewater N and removal of wastewater N within open systems and ICOLLs. In open estuaries, mobile animals are able to move and feed outside the impacted area, diluting the wastewater δ15N signature in their

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tissues, and potentially removing wastewater N from the system. In contrast, animals are confined to ICOLLS, and the food sources therein, when the estuary is closed. This amplifies the wastewater

δ15N signal within these biota and enhances recycling within the system. This may be complicated, however, by the periodic opening of ICOLLs to the open ocean. At this time, flushing introduces

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new N to the system, which may be assimilated by biota, diluting any pre-existing wastewater δ15N

signal. Furthermore, individuals of mobile species that enter the ICOLL when the mouth is open will

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lack the expected enriched wastewater δ15N signal (e.g., Hadwen and Arthington 2007), with the time taken for their tissue to incorporate wastewater N depending on turnover time. The apparent presence of wastewater N within Tallow Creek 8 years after wastewater discharge ceased suggests that the system had a relatively low rate of recovery from wastewater input. The average annual recovery rate for δ15N values of algae and crustaceans in Tallow Creek was

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estimated to be 5.6% yr-1 and 4.8% yr-1, respectively (Table 3), where the rate represents the change in δ15N as a percentage of the difference between impacted (‘During’) and less-impacted (‘After’) δ15N, divided by the number of years since wastewater input ceased. Loss rates within a system are unlikely to ever be linear, as this calculation assumes, particularly in the case of ICOLLs, where periodic

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flushing would occasionally enhance loss rates. However, this simple calculation of recovery rates allows for a general comparison across systems. On this basis, average annual rates of wastewater N

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loss for Tallow Creek were considerably slower than those reported for algae and crustaceans in a local permanently open estuary (Brisbane River estuary, ~130 km north of Tallow Creek) following a WWTP upgrade (16.6 % yr-1 and 15.7% yr-1, respectively; Pitt et al. 2009) (Table 3). Recovery of δ15N to background signatures would take approximately three times longer in Tallow Creek than in the better-flushed Brisbane River estuary. The rate of wastewater N removal from Tallow Creek biota was also far slower than observed in an open bay (Moa Point, New Zealand) following closure of a WWTP outfall (Rogers 2003). Rogers (2003) reported that δ15N values returned to control levels within 1-3 months post-closure for the macroalga Ulva lactuca, and after 9 months for limpets and 17

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mussels. In contrast, δ15N values of Tallow Creek biota suggested that up to 38% of the initial wastewater N remained 8 years after wastewater inputs ceased. This represents far greater retention of wastewater N than would be expected over this period for an open estuary. It should, however, be

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noted that wastewater N loss rates in the current study may be underestimated. Due to the natural opening of the Tallow Creek ICOLL ~ 1 month before sampling commenced, it is possible that some of the collected biota were recent recruits, for which δ15N values would not have had time to

equilibrate to the new environment. True rates of wastewater N retention may therefore be higher for

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the ICOLL than is estimated here, further emphasising the potential for ICOLLs to retain wastewater N over extended periods.

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The slow recovery rate of δ15N values in Tallow Creek, as a percentage of the initial 15N enrichment, is consistent with the hypothesis that irregular flushing of ICOLLs limits dilution and removal of wastewater N, and recovery of δ15N signatures of biota. Within ICOLLs, periods with no or limited flushing would allow ample time for organic matter containing wastewater-derived N to be incorporated into the sediments, contributing to longer-term storage of wastewater N within the

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system. This is consistent with the intermediate δ15N values observed for sediment N in Tallow Creek ‘After’, which suggest that the sediment has retained some wastewater N.

Table 3. Mean (±SE) recovery rates for δ15N of algae and crustaceans sampled in Tallow Creek,

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NSW, and the Brisbane River Estuary, Queensland.

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Tallow Creek

Brisbane River Estuary

Algae δ N (‰)

Crustaceans δ15N (‰)

Total N discharge (t/year)

Algae δ N (‰)

Crustaceans δ15N (‰)

Total N discharge (t/year)

During

10.46 ± 0

24.6 ± 0

~8.5

19.3 ± 1.4

19

303 ± 71

After

5.74 ± 2.1

12.8 ± 0.4

0

13.0 ± 0.6

13

55

5.6

4.8

16.6

15.7

15

Decrease per year (%)

15

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4.3 Inter-specific differences in recovery Overall, δ15N values in the Tallow Creek ‘After’ food web were statistically indistinguishable from those in the Jerusalem Creek control. However, δ15N values for some biota

15

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(fringing vegetation, crustaceans, and carnivorous fish, including S. ciliata) remained enriched in N. These apparent differences in the rate of recovery of various food web components from

changes in the availability of wastewater N may relate to the growth rate and turnover times of the compartments sampled, the N source of biota, and/or their mobility (Rogers 2003; Dubois et al.

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2007; Deudero et al. 2009; Pitt et al. 2009).

Generally, primary producers and lower order consumers have rapid rates of growth and

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turnover and therefore respond rapidly to changes in wastewater N availability (Cabana and Rasmussen 1996). In contrast, biota with a slower turnover rate (e.g., higher order consumers), or which acquire their N from a source with a slow turnover rate (e.g., plants obtaining N from sediment; Alongi 1996, Pitt et al. 2009) can provide useful information on trophic transfers (McClelland et al. 1997), but provide lower temporal resolution, as they take longer to acquire new

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isotopic signatures (Gartner et al. 2002). Food web components with a faster turnover rate will reflect more recent levels of wastewater N within the Tallow Creek system. However, given that δ15N values within Tallow Creek appear to have changed very slowly over the 8 years since wastewater input ceased, there is little scope to detect differences in δ15N among taxa due to

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variations in N turnover. During the days, weeks, and months that tissue turnover is likely to have taken for the sampled biota (e.g., Hesslein et al. 1993; Tieszen et al. 1983), there would probably

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have been little change in δ15N of available sources, resulting in little difference in δ15N values among the sampled biota due to turnover rates at any point in time. The N source of sampled biota and/or their mobility are more likely explanations for the

observed differences in δ15N recovery rate. As aforementioned, longer-term storage of wastewater N is probably attributable to burial within sediments (Savage et al. 2004). This appears to be reflected in the persistent enrichment of fringing vegetation (Table 2). It is also possible that wastewater N was retained within plant tissues with a slow turnover rate, but is seems unlikely that this would have contributed substantially to the relatively new leaf material that was analysed. 19

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Fauna that assimilate N derived from sediment organic matter and/or fringing vegetation are therefore more likely to have a wastewater N signal, i.e., their δ15N values should be more enriched. For example, many of the prey items consumed by S. ciliata in the nearby Belongil Creek ICOLL

15

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studied by Hadwen et al. (2007) utilised fringing (riparian) vegetation as a source of nutrition. The N-enriched δ15N value of S. ciliata in Tallow Creek ‘After’ may therefore reflect the trophic

transfer of 15N-enriched fringing vegetarian via these prey items. The interpretation of δ15N values of mobile consumers is complicated, however, by the possibility that some of the individuals

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collected may be relatively recent recruits to the ICOLL that entered when it naturally opened

approximately one month before sampling occurred (as seen observed in the study by Hadwen and

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Arthington 2007). This would have reduced the apparent contribution of wastewater N to these individuals, even if they derived much of their N within the ICOLL from wastewater-derived sources, as their tissues would have had little time to equilibrate with their new diets. The enriched δ15N value of some mobile fish, despite the opening of the ICOLL, suggests that these individuals were long-term residents, or that the turnover time of tissues within the

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sampled fish, combined with the quantity of remaining wastewater N, was sufficient to elicit a change in δ15N value over a relatively short time period. Most fish sampled were estimated to be < 1 year old, based on total lengths of <10 cm for all R. sarba, and all but one S. ciliata, and <15 cm for all but one M. cephalus (Chubb et al. 1981; Ochwada-Doyle et al. 2014; Radebe et al. 2002).

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The fast growth rate and the formation of new tissues in these relatively young fish would allow rapid changes in δ15N (Hesslein et al 1993). Analysis of tissue types with different turnover rates

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could help to distinguish between new recruits and existing individuals. For an individual that has recently entered the ICOLL, an enriched ‘wastewater’ δ15N value may be detected in tissues with fast turnover (e.g., hepatopancreas of a crab; Oakes et al. 2010), but not in tissues with a slower turnover (e.g., muscle; Oakes et al. 2010).

4.5 Conclusions Although δ15N values of Tallow Creek biota demonstrated that the system has begun to recover from the impacts of wastewater input, the rate of recovery was far slower than has been 20

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observed in more open systems, owing to the limited flushing of the ICOLL. There is currently little available literature on recovery of ICOLLs following anthropogenic impact, but this study shows that the unique hydrology of these systems makes them potentially more susceptible to

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impacts such as nutrient enrichment, as they have reduced capacity for removing these inputs

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relative to more open estuaries.

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Acknowledgements

This work was supported Australian Research Council grants DE120101290, DP160100248, LP110200975 and LP150100451. Collections of marine fish, invertebrates and vegetation were made

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under Scientific Collection Permit # P13/0029-1.0 issued by the New South Wales Department of Primary Industries (Fisheries). Euthanasia of marine fish was approved by the Southern Cross

University Animal Care and Ethics Committee (research project authority number 13/25). We

acknowledge assistance in the field from E.S. Williams, the Cape Byron Marine Park and NSW

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Arakwal National Parks and Wildlife Services. We also thank M. Carvalho for isotope analysis and the Byron Shire Council for information regarding the decommissioned South Byron WWTP. Three

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anonymous reviewers are thanked for their comments which improved the manuscript.

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References Alongi, D. 1996. The dynamics of benthic nutrient pools and fluxes in tropical mangrove forests. Journal of Marine Research 54, 123-148.

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Anderson, D.M., Glibert, P.M., Burkholder, J.M. 2002. Harmful algal blooms and eutrophication: Nutrient sources, composition and consequences. Estuaries 25, 704-726.

(ANZECC) Australia and New Zealand Environment Conservation Council (2000). PIMC-

NRMMC (2009) National Water Quality Management Strategy Guideline Documents.

strategy. Accessed on 23rd August 2013.

SC

Canberra. http://www.mincos.gov.au/publications/national_water_quality_management_

M AN U

(BOM) Bureau of Meteorology. 2014a. Climate Statistics for Australian Locations – Monthly Statistics “Cape Byron, NSW”. http://www.bom.gov.au/climate/averages/tables/ cw_058216.html. Accessed on 8/05/2014.

(BOM) Bureau of Meteorology. 2014b. Climate Statistics for Australian Locations – Monthly Statistics “Cape Byron, NSW”. http://www.bom.gov.au/climate/averages/tables/

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cw_058212.shtml. Accessed on 8/05/2014

Cabana, G., Rasmussen, J.B. 1996. Comparison of aquatic food chains using nitrogen isotopes. Proceedings of the National Academy of Science, USA 93, 10844–10847. Canfield, D.E., Glazer, A.N., Falkowski, P.G. 2010. The evolution and future of earth’s nitrogen

EP

cycle. Science 330, 192–196. Chubb, C.F., Potter, I.C., Grant, C.J., Lenanton, R.C.J., Wallace, J. 1981. Age, structure, growth rates

AC C

and movements of sea mullet, Mugil cephalus L., and Yellow-eye Mullet, Aldrichetta forsteri

(Valenciennes), in the Swan-Avon river system, Western Australia. Australian Journal of Marine and Freshwater Research 32:605-628.

Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210, 223–253. Connolly, R.M., Gorman, D., Hindell, J.S., Kildea, T.N., Schlacher, T.A. 2013. High congruence of isotope sewage signals in multiple marine taxa. Marine Pollution Bulletin 71, 152-158. Costanzo, S.D., O’Donohue, M.J., Dennison, W.C., Loneragan, N.R., Thomas, M. 2001. A new 23

ACCEPTED MANUSCRIPT

approach for detecting and mapping sewage impacts. Marine Pollution Bulletin 42, 149156. Costanzo, S.D., O’Donohue, M.J., Dennison, W.C. 2003. Assessing the seasonal influence of

RI PT

sewage and agricultural nutrient inputs in a subtropical river estuary. Estuaries 26, 857865.

Curley, B.G., Jordan, A.R., Figueira W.F., Valenzuela, V.C. 2013. A review of the biology and ecology of key fishes targeted by coastal fisheries in south-east Australia: identifying

SC

critical knowledge gaps required to improve spatial management. Reviews in Fish Biology and Fisheries 23, 435-458.

M AN U

Davis, J.R., Koop, K 2006. Eutrophication in Australian rivers, reservoirs and estuaries - a southern hemisphere perspective on the science and its implications. Hydrobiologia 559, 23-76. deBruyn, A.M.H., Rasmussen, J.B. 2002. Quantifying assimilation of sewage-derived organic matter by riverine benthos. Ecological Applications 12, 511-520.

Deudero, S., Cabanellas, M., Blanco, A., Tejada, S. 2009. Stable isotopic fractionation in the digestive

TE D

gland, muscle and gills tissues of the marine mussel Mytilus galloprovincialis. Journal of Experimental Marine Biology and Ecology 368, 181–188. Dubois, S., Blin, J.L., Bouchaud, B., Lefebvre, S. 2007. Isotope trophic-step fractionation of suspension-feeding species: implications for food partitioning in coastal ecosystems. Journal

EP

of Experimental Marine Biology and Ecology 351, 121–128. Everett. J.D., Baird. M.E., Suthers, I.M. 2007. Nutrient and plankton dynamics in an intermittently

AC C

closed/open lagoon, Smiths Lake, south-eastern Australia: An ecological model. Estuarine

Coastal and Shelf Science 72, 690-707.

Eyre, B.D 2000. Regional evaluation of nutrient transformation and phytoplankton growth in nine river-dominated sub-tropical east Australian estuaries. Marine Ecology Progress Series 205, 61-83. Eyre, B.D., Ferguson, A.J.P. 2009. Denitrification efficiency for defining critical loads of carbon in shallow coastal ecosystems. Hydrobiologia 629, 137-146. Eyre, B.D., Maher, D.T., Sanders, C. 2016a. The contribution of denitrification and burial to the 24

ACCEPTED MANUSCRIPT

nitrogen budgets of three geomorphically distinct Australian estuaries: importance of seagrass habitats. Limnology and Oceanography 61, 1144-1156. Eyre, B.D., McKee, L. 2002. Carbon, nitrogen and phosphorus budgets for a shallow sub-

RI PT

tropical coastal embayment (Moreton Bay, Australia). Limnology and Oceanography 47, 1043-1055.

Eyre, B.D., Oakes, J.M., Middelburg, J.J. 2016b. Fate of microphytobenthos nitrogen in

subtropical subtidal sediments: a 15N pulse-chase study. Limnology and Oceanography.

SC

doi: 10.1002/lno.10356

Eyre, B., Twigg, C. 1997. Nutrient behaviour during post-flood recovery of the Richmond River

M AN U

Estuary northern NSW, Australia. Estuarine, Coastal and Shelf Science 44, 311-26. Ferguson, A.J.P., Eyre, B.D., Gay, J. 2004a. Nutrient cycling in the sub-tropical Brunswick estuary, northern NSW, Australia. Estuaries 27, 1-18.

Ferguson, A.J.P., Eyre, B.D., Gay, J. 2004b. Benthic nutrient fluxes in euphotic sediments along shallow sub-tropical estuaries, northern NSW, Australia. Aquatic Microbial Ecology 37,

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219-235.

Gartner, A., Lavery, P., Smith, A.J. 2002. Use of δ15N signatures of different functional forms of macroalgae and filter-feeders to reveal temporal and spatial patterns in sewage dispersal. Marine Ecology Progress Series 235, 63–73.

EP

Hadwen, W.L., Arthington, A.H. 2006. Ecology, threats and management options for small estuaries and ICOLLs. Sustainable Tourism Cooperative Research Centre, CRCST Press:

AC C

Gold Coast.pp.86.

Hadwen, W.L., Arthington, A.H. 2007. Food webs of two intermittently open estuaries receiving 15

N-enriched sewage effluent. Estuarine, Coastal and Shelf Science 71, 347-358.

Hadwen, W. L., Russell, G. L., Arthington, A. H. 2007. Gut content- and stable isotope-derived diets of four commercially and recreationally important fish species in two intermittently open estuaries. Marine and Freshwater Research 58, 363-375. Haines, P. E. 2008. ICOLL Management: Strategies for a sustainable future. BMT WBM Pty Ltd, Broadmeadow, NSW. 25

ACCEPTED MANUSCRIPT

Hansson, S., Hobbie, J.E., Elmgren, R., Larsson, U., Fry, B., Johansson, S. 1997. The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78, 2249– 2257.

review. Chemical Geology 59, 87-102.

RI PT

Heaton, T.H.E. 1986. Isotopic studies of nitrogen pollution in the hydrosphere and atmosphere: a

Hesslein R.H., Hallard K.A., Ramlal P. 1993. Replacement of sulphur, carbon, and nitrogen tissue of growing broad whitefish (Coregonus nasus) in response to a change in diet traced by δ34S,

SC

δ13C, and δ15N. Canadian Journal of Fisheries and Aquatic Sciences 50, 2071–2076.

Hossain, S., Eyre, B.D., McKee, L.J. 2004. Impacts of dredging on dry season suspended sediment

Shelf Science 61, 539-545.

M AN U

concentration in the Brisbane River estuary, Queensland, Australia. Estuarine, Coastal and

Hurst, T.P., Kay, B.H., Brown, M.D., Ryan, P.A. 2006. Laboratory evaluation of the effect of alternative prey and vegetation on predation of Culex annulirostris immatures by Australian native fish species. Journal of the American Mosquiot Control Association 22, 412-417.

TE D

Maher, W., Mikac, K.M., Foster, S., Spooner, D., Williams, D. 2011. Form and functioning of micro size intermittent closed open lake lagoons (ICOLLs) in NSW, Australia. Nova Science Publishers, Inc. pp. 119-151

McAlister T., Richardson D., Agnew L., Rowlands L., Longmore A. 2000. Tallow and Belongil

EP

Creek Ecological Studies - Final Report. WBM Oceanics Australia, Spring Hill, Brisbane, Queensland, 206 pp.

AC C

McClelland, J.W., Valiela, I., Michener, R.H. 1997. Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnology and Oceanography 42, 930–937.

Oakes, J. M., Connolly, R. M., Revill, A. T. 2010. Isotope enrichment in mangrove forests separates microphytobenthos and detritus as carbon sources for animals. Limnology and Oceanography 55, 393-402. Oakes, J. M., Eyre, B. D. 2015. Wastewater nitrogen and trace metal uptake by biota on a highenergy rocky shore detected using stable isotopes. Marine Pollution Bulletin 100, 40626

ACCEPTED MANUSCRIPT

413. Ochwada-Doyle, F. A., Stocks, J., Barnes, L., Gray, C.A., 2014. Reproduction, growth and mortality of the exploited sillaginid, Sillago ciliata Cuvier, 1829. Journal of Applied

RI PT

Ichthyology 1-11. Pitt, K.A., Connolly, R.M., Maxwell, P. 2009. Redistribution of sewage-nitrogen in estuarine food webs following sewage treatment upgrades. Marine Pollution Bulletin 58, 573-580.

Radebe, P. V., Mann, B. Q., Beckley, L. E. , Govender, A. (2002) Age and growth of Rhadosargus

SC

sarba (Pisces: Sparidae), from KwaZulu-Natal, South Africa. Fisheries Research 58-193-201. Rockström, J., Steffen, W.,Noone, K., Persson, A., Chapin, F.S., Lambin, E.F., Lenton, T.M.,

M AN U

Scheffer, M., Folke, C., Joachim Schellnhuber, H., Nykvist, B., de Wit, C.A., Hughes, T., van der Leeuw, S., Rodhe, H., Sörlin, S., Snyder, P.K., Costanza, R., Svedin, U., Falkenmark, M., Karlberg, L., Corell, R.W., Fabry, V.J., Hansen, J., Walker, B., Liverman, D., Richardson, K., Crutzen, P., Foley, J.A. 2009. A safe operating space for humanity. Nature 461, 472-475.

TE D

Rogers, K.M. 2003. Stable carbon and nitrogen isotope signatures indicate recovery of marine biota from sewage pollution at Moa Point, New Zealand. Marine Pollution Bulletin 46, 821-827 Roper, T, Creese, B, Scanes, P, Stephens, K, Williams, R, Dela Cruz, J, Coade, G, Coates, B, Fraser, M 2011. State of the Catchments Report – Estuaries and Coastal lakes, technical

EP

Report Series. Assessing the condition of estuaries and coastal lake ecosystems in NSW. State of NSW and Office Environment and Heritage.

AC C

Savage, C., Leavitt, P.R., Elmgren, R. 2004. Distribution and retention of effluent nitrogen in surface sediments of a coastal bay. Limnology and Oceanography 49, 1503–1511.

Schlacher T.A., Caruthers T. 2002. Mooloolah River. In: Abal EG, Moore KB, Gibbes BR, Dennison WC (eds) State of the southeast Queensland waterways report 2001. Moreton

Bay Waterways and Catchments Partnership, Brisbane, pp 18–25 Schlacher T.A., Carruthers T., Dennison WC, Pocock J., Katouli, M. 2001. Maroochy Mooloolah loads and impacts study. WBM Oceanics, Brisbane Schlacher, T.A., Liddell, B., Gaston, T.F., Schlacher-Hoenlinger, M. 2005. Fish track wastewater 27

ACCEPTED MANUSCRIPT

pollution to estuaries. Oecologia 144, 570-584. Tieszen, L. L., Boutton, T. W., Tesdahl, K. G., Slade, N. A. 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57,

RI PT

32-37. Vitousek, P.M., Aber, J.D., Howarth, R.W., Likens, G.E., Matson, P.A., Schindler, D.W.,

Schlesinger, W.H., Tilman, D.G. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Journal of Applied Ecology 7, 737–750.

SC

Waldron, S., Tatner, P., Jack, I., Arnott, C. 2001. The impact of sewage discharge in a marine

embayment: a stable isotope reconnaissance. Estuarine, Coastal and Shelf Science 52, 111–

M AN U

115.

Wayland, M., Hobson, K 2001. Stable carbon, nitrogen, and sulfur isotope ratios in riparian food webs on rivers receiving sewage and pulp-mill effluents. Canadian Journal of Zoology 79, 5-15.

Williams, R.J., Watford, M.A., Taylor, M.A., Button, M.L. 1998. New South Wales coastal aquatic

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estate. Wetlands Australia Journal 18, 25-47.

Wulff, F., Eyre, B.D. and Johnstone, R. 2011. Nitrogen versus phosphorus limitation in a sub-tropical coastal embayment (Moreton Bay, Australia): Implications for Management. Ecological Modelling 222, 120-130.

EP

Yang, S. L., Li, H., Ysebaert, T., Bouma, T. J., Zhang, W. X., Wang, Y. Y., Li, P., Li, M., Ding, P. X. 2008. Spatial and temporal variations in sediment grain size in tidal wetlands, Yangtze

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Delta: On the role of physical and biotic controls. Estuarine, Coastal and Shelf Science 77, 657-671.

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APPENDIX Table A.1 Sample sizes for the food web components collected from Tallow Creek ‘After’ and Jerusalem Creek.

Sources 4

Coarse particulate organic matter (CPOM)

4

Epilithon

2

Filamentous algae

5

Seston

10

2

2

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Fine particulate organic matter (FPOM)

Jerusalem Creek

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Tallow Creek ‘After’

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Sample type

Mangroves

1

4

2

13

0

9

2

2

2

2

1

7

10

8

1

Rhadosargus sarba

5

0

Ambassis marianus

2

0

Scylla serrata

1

0

Glycera sp.

10

0

Metapenaeus bennettae

5

0

Trypaea australiensis

0

6

Succulents

Cyperus sp.

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Juncus sp.

Consumers Sillago ciliata

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Mugil cephalus

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Highlights δ15N values in an ICOLL food web reduced over 8 years without wastewater N input

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Some δ15N values remained enriched versus a pristine ICOLL, 8 years post-impact

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Slow recovery of δ15N, compared to open systems, reflects low flushing of ICOLLs

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•