Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

Oluwuyi Babaranti; Stephen Horn; Tim Jowett; Russell Frew

doi:10.1080/24749508.2018.1485079

Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

Babaranti, Oluwuyi; Horn, Stephen; Jowett, Tim; Frew, Russell 2019-01-02 00:00:00 GEOLOGY, ECOLOGY, AND LANDSCAPES 2019, VOL. 3, NO. 1, 53–64 INWASCON https://doi.org/10.1080/24749508.2018.1485079 Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage eﬄuent in coastal waters along Otago Peninsula, New Zealand a b c a Oluwuyi Babaranti , Stephen Horn , Tim Jowett and Russell Frew a b Department of Chemistry, University of Otago, Dunedin, New Zealand; Department of Conservation, Wellington, New Zealand; Department of Mathematics & Statistics, University of Otago, Dunedin, New Zealand ABSTRACT ARTICLE HISTORY Received 30 January 2018 Sewage, waste organic matter from domestic and municipal wastewater, causes increased Accepted 3 June 2018 secondary productivity, eutrophication and trace metal contamination, reduced oxygen levels, and biodiversity which can lead to ecological disturbances in the natural aquatic KEYWORDS ecosystem. The impact of sewage-derived organic matter (SDOM) on the nearshore marine Sewage eﬄuent; ecosystem of the Otago Coast was assessed before, and 15 years after upgrade of the wastewater; isotopic Dunedin sewage treatment plant. Carbon and nitrogen isotopic ratios in the tissues of enrichment factor; organic sentinel organisms were used as bioindicators to elucidate the primary sources of nutrition matter; linear mixed eﬀect modelling; bioindicators the coastal environment. Mytilus galloprovincialis, a marine bivalve, exhibited a strong inﬂu- ence of SDOM from two sites in 2001. In 2015, M. galloprovincialis had a trophic enrichment 15 13 factor of 3‰ (δ N) and 1‰ (δ C) when compared to the marine particulate organic matter (POM), suggestive of a dietary change away from the SDOM. Suspended POM collected from riverine and estuarine sources revealed other possible nitrogen sources from human-driven activities such as pastoral farming, application of organic manure and inorganic fertilisers, nitriﬁcation of ammonium from semi-urban septic tanks, and animal organic waste residues. 1. Introduction Wastewater Plant and Tahanu Wastewater Treatment Plant (TWWTP) serving over 120,000 people in Sewage, a major organic component of domestic and Dunedin, New Zealand, discharge adequately treated municipal wastewater, can cause increased second- wastewater eﬄuent from Waldronville and Lawyers ary productivity (Hillebrand & Sommer, 2000), Head, respectively (see Figure 1), into the Paciﬁc eutrophication (Jarvie, Neal, & Withers, 2006), Ocean from two ocean outfalls pipes that were extended heavy metal contamination (Chary, Kamala, & Raj, from 550 to 1100 m in 2009. Between 2010 and 2013, 2008; Cheevaporn & Menasveta, 2003; Morillo, the wastewater treatment plant facilities were improved Usero, & Gracia, 2004), reduced oxygen levels, and to handle both primary and secondary wastewater treat- biodiversity which can lead to ecological distur- ment processes. The advancement in the wastewater bances (Browne et al., 2011; Diaz, Rhoads, Blake, management involved the construction of a new Kropp, & Keay, 2008) in the natural aquatic ecosys- pump station to the increased ﬂow rate of the waste- tems (Deegan & Buchsbaum, 2005; Hargrave, water treatment plants. This was done to improve the Holmer, & Newcombe, 2008). Thus, it is imperative quality of eﬄuent and shoreline water quality, reduce we ensure that the quality of treated wastewater organic matter content, and ensure public health pro- eﬄuent from municipal treatment plants meets the tection which was a major concern at that time stipulated safe levels approved by the statutory and (Bouman & Archer, 2014). regulatory authorities before discharged into the Before the extension of the ocean outfalls pipes, receiving waterbodies (Ellis, 2004; Teklehaimanot, discharged wastewater eﬄuent contaminated parts of Coetzee, & Momba, 2014). the Otago coastal marine area which has more than Inadequately treated eﬄuent discharged into the 80 protected wildlife areas which accommodated marine area poses environmental and health hazards marine mammals and birds along its landward edge to the resident biota in the adjacent nearshore waters. (Council, 2001; Gormley et al., 2012; Rayment, Between 1908 and 1950s, raw sewage was discharged Dawson, & Slooten, 2010). The various bacteriologi- directly into the Paciﬁc Ocean at Lawyers Head cal studies (measurement of Escherichia coli con- (Council, 2001) by the Dunedin Water Pollution ducted on shellﬁsh, sediments, and seawater) had Control Plant (now called Tahuna Wastewater ascribed the contamination of the portions of Otago Treatment Plant). Presently, the Green Island coastline to the wastewater eﬄuent discharge from CONTACT Oluwuyi Babaranti olua_babs@yahoo.com Department of Chemistry, University of Otago, Dunedin, New Zealand © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 54 O. BABARANTI ET AL. various beaches along the Otago Peninsula to trace the pattern and distribution of sewage eﬄuent dis- charged from Lawyers Head. He observed that the nitrogen isotopic ratios of the digestive tissues of the end member mussels vary considerably. He reported that major sewage contamination occurred at Lawyers Head and Tomahawk while there was minor contamination at St. Kilda and Smaills. He found out that more than 60% of the mussels and seaweeds sampled at Lawyers Head and Tomahawk Beach had their isotopic ratios wedged by discharged sewage eﬄuent. Isotopic study carried out by North, Frew, and Hale (2006) on the possibility of landﬁll leachates as source of contamination from solid waste Figure 1. Schematic representation study sites along Otago disposal site which involved the collection and ana- Peninsula with adjoining tidal channels, creeks, and waste- lyses of surface water samples from Kaikorai wetland water outfalls. areas made up of stream and estuary waters from Green Island Landﬁll over an 8-month period revealed that landﬁll leachates could also be possible the TWWTP (Lewis, Loutit, & Austin, 2010; source of contamination to the Kaikorai downstream Nicholson, Lewis, & Loutit, 1989; RCL, 2000). One (North et al., 2006; North, Frew, & Peake, 2004) of such studies reported that over 50% of shellﬁsh which eventually has a run-oﬀ into the Otago coast- collected from the sites close to the sewage outfalls at line at Waldronville. Consequently, there is the pro- Lawyers Head had elevated level of faecal coliforms spect of using stable isotopic ratios in the tissues of and enteric viruses of >230 and <4600/100 g ﬂesh, organisms to assess the impact SDOM and other well above the European Union Class A standard for terrigenous materials on the nearshore marine eco- shellﬁsh ﬂesh. Five downstream sites closest to the system because stable isotopic signatures in the tis- sewage outfall were found to be heavily contaminated sues of organisms had been found to be connected by faecal coliforms and enteric viruses while two with an organism diet over time and space (Bump upstream sites were considered uncontaminated et al., 2007; Rogers, 2003). Stable isotopic analyses on (Greening, Lewis, & Dollimore, 2007). However, the tissues of marine ﬂora and fauna have been these studies were only spot tests (Doré, extensively exploited to assess the impact of SDOM Henshilwood, & Lees, 2000; Ebner, McAllister, & on the food web structure of nearshore marine eco- Suter, 2009) and appropriate for assessing water qual- systems as well as to investigate the recovery of mar- ity standards (Abbasi & Abbasi, 2011; Dede, Telci, & ine ﬂora and fauna at sites disrupted by sewage Aral, 2013). They failed to account for other possible eﬄuent discharges (Barr, Dudley, Rogers, & sources of contamination and provide no estimate of Cornelisen, 2013; Michener & Kaufman, 2008; the amount of sewage-derived organic matter Savage, 2005). SDOM had been known to signiﬁ- (SDOM) in the nearshore marine ﬂora and fauna. cantly alter the stable carbon and nitrogen isotopic Horn (2001) conducted an isotopic monitoring 13 15 signatures (expressed as the δ C and δ N) of marine study on seawater samples, and the tissues of ﬂora (i.e., macro-algae) and fauna (e.g., ﬁlter-feeders) Mytilus galloprovincialis and Ulva lactuca across Figure 2. Comparison of carbon and nitrogen-stable isotopic ratios in the digestive tissues of Mytilus galloprovincialis and particulate materials collected in 2001 along the Otago coastline, New Zealand. GEOLOGY, ECOLOGY, AND LANDSCAPES 55 (Bedard-Haughn, Van Groenigen, & Van Kessel, rates and isotopic enrichment in organisms are tis- 2003; Dudley & Shima, 2010) permitting them to sue speciﬁcand inﬂuenced by lipid content of the exhibit distinct isotopic signatures in their tissues as tissue (Lorrain et al., 2002;Thompson,Phillips, areﬂection of the integration, assimilation, and utili- Stewart, & Waldron, 2000). Thus, a preliminary sation of the SDOM in their immediate environment stable isotopic study to investigate the variance in over time. The carbon and nitrogen isotopic signa- isotopic ratios of carbon and nitrogen in the diﬀer- tures are the comparisons of ratios of the heavy-to- ent tissues of M. galloprovincialis was carried out to light isotope of the element. They are mathematically determine the appropriate tissues to be used for this expressed (see Equation 1) in δ notation in terms of study. The results obtained were compared with parts per thousand (‰)or “per mil” and calculated as other isotopic studies using power analysis for deter- follows: mining sample size. This was done to control the number of samples to be collected to avoid unne- n sample cessary sacriﬁce of biological samples to be used and δ X¼ 1 (1) (Coplen, 2011) standard ensure the reliability of our results. The abductor tissue was noted to have the highest isotopic carbon where n is the atomic mass of the heavy element, X and nitrogen turnover whereas the digestive tissue can either be C or N whereas R is the isotopic ratios has the lowest isotopic tissue turnover. This obser- 13 15 of X (l3C/12C or 15N/14N). The δ C and δ N are vation was in accordance with other workers measured relative to international reference standards (Deudero,Box,Tejada, &Tintoré, 2009;Gaston& of Vienna PeeDee Belemnite and Atmospheric Suthers, 2004). The abductor and digestive tissues of Nitrogen, respectively. Consumer organisms have thebluemusselwerechosenasthe appropriate been known to exhibit isotopic signatures which can indicators forassessing theimpactofSDOMon either be similar or vary from their diets with an the nearshore marine fauna in the nearshore marine average fractionation trophic enrichment of 0.4–1‰ waters. To the best of our knowledge, no stable 13 15 for δ C 1987 and 3–4‰ for δ N (Kline & Thomas, isotopic studies to assess the impact of the modiﬁca- 1999; Post, 2002). tions in the sewage treatment and disposal on the In assessing the impact of SDOM in a nearshore nearshore marine waters and resident biota along marine ecosystem, the disparities in the carbon and the Otago Peninsula had been carried out. Hence, nitrogen isotopic ratios in the tissues of end members our study is attempted to exploit the isotopic ratios can become useful monitoring tools for providing of sentinel organisms at these sites so as to ﬁnd out more information on the source and magnitude of the current status of organic materials in the tissues sewage contribution to the diet of resident biota of M. galloprovincialis and Ulva latuca of the near- (Peterson, 1999). Hence for the purpose of this shore marine waters. This present study will address study, stable isotopic ratios in the tissues of M. gallo- the following research questions: provincialis (marine bivalve) and U. lactuca (sea let- tuce) were speciﬁcally chosen as indicators to be used. 13 15 (1) Are the variabilities in the δ C and δ Nin Mussels are sedentary and long-lived (Alfaro, Jeﬀs, & the tissues of M. galloprovincialis and U. lac- Hooker, 2001; Nordsieck, 2006; SITO, 2006) charac- tuca reliable indicators of assessing sewage teristic features which make them suitable sentinel contamination in the nearshore marine waters organisms as time-averaged integrators of sewage along the Otago Peninsula? exposure for the sea lettuces which are short lived (2) Has the improvement in the sewage treatment by nature (Cabana & Rasmussen, 1996; Dudley & processes and disposal at the TWWTP brought Shima, 2010; Post, 2002). signiﬁcant changes in the carbon and nitrogen Furthermore, ﬁlter feeders such as bivalves (i.e., isotopic signatures of M. galloprovincialis and mussels) can directly ingest (via the gills) and assim- U. lactuca collected from the nearshore marine ilate sewage particulate organic matter (POM) (con- ecosystem along the Otago Peninsula? taining carbon and nitrogen) along with their diet (3) Are there other possible terrestrial-based organic (phytoplankton and detritus) from the water column materials contributing carbon and nitrogenous into the tissues and reassigned such higher up the materials to the nearshore waters which may food chain (biomagniﬁcation) (Ouédraogo, Chételat, sway the carbon and nitrogen isotopic ratios of &Amyot, 2015;Pan &Wen-Xiong, 2004). In choos- M. galloprovincialis and U. lactuca? ing the most appropriate tissues for the stable iso- (4) How much of terrestrial-based organic δ C topic study, consideration was given to the previous carbon and δ N nitrogenous materials are studies conducted by other workers on carbon and integrated into the tissues (i.e., digestive) of nitrogen isotopic turnover and enrichment in the M. galloprovincialis collected from the near- diﬀerent tissues of organisms. Most of the studies shore marine waters along the Otago showed that carbon and nitrogen isotopic turnover Peninsula? 56 O. BABARANTI ET AL. To answer these questions, the linear mixed eﬀects uniform sizes to avoid sampling bias which might model analysis, an extension of regression analysis, ensue from in-site and site–site isotopic variability. was used to compare the stable carbon and nitrogen The study sites cover about 48 km within the Otago 13 15 isotopic ratios (δ C and δ N) in the tissues of M. Marine Area. Water samples were collected from the galloprovincialis and U. lactuca collected in 2001 three tidal channels having a free connection to the (before upgrade of the sewage treatment plant) and nearshore marine waters (Figure 1). At each of the 2015/16 (after upgrade of the sewage treatment plant) sampling sites, the date and time of sampling, pre- in the end members so as to determine if there had vailing weather conditions, swell, wind direction, as 13 15 been changes in the isotopic signatures δ C and δ N well as possible visible sources of contamination, in the tissues of M. galloprovincialis and U. lactuca were noted and recorded. The location of each of collected from the study sites classiﬁed into control the sampling sites was noted and recorded with the sites (uncontaminated sites) and previously sewage- aid of a handheld GPS tracking device and illu- contaminated sites comprising eight beaches and strated in Table 1. three tidal channels. The groupings of these sites were based on proximity to the sewage outfall, the 2.2. Sample preparation and analysis written reports of the 2000 ORC Resource Consent 97530 97530 (RCL, 2000) and 2007 FRST Programme M. galloprovincialis and U. latuca were individually C03X0301 (Greening et al., 2007). The nature of placed into clean ziplock plastic bags labelled with possible sources of carbon and nitrogen into the date and sample site location. They were immedi- nearshore marine waters was identiﬁed and discerned ately placed in a plastic cooler for onward trans- from the distinctive isotopic ratios of the POM col- port to the laboratory where they were rinsed in lected from the tidal channels feeding the coastal distilled water and frozen prior to analysis. M. marine waters. A mass balance linear mixing model galloprovincialis was dissected into diﬀerent tissues equation was used in estimating the source contribu- (the abductor and digestive tissues of interest in tions of carbon and nitrogen materials in the tissue of this study). The dissected tissues and samples of U. marine biota collected from the study sites along latuca were dried at 70°C for 24 h. Once dry Otago Peninsula. The two main sources considered samples were homogenised with the aid of an were marine POM and sewage eﬄuent POM. This MM400 bench-top Retsch ball mill, duplicate ali- was done to quantify the contribution of sewage quots of 0.8 mg of homogenised tissues of the material in the marine biota. The ﬁndings from this biological samples were weighed into separate study will show the potential of deploying multistable 5 × 3.5 mm tin cups and further dried under isotopic techniques and ﬁtting mixing model to be vacuum overnight. Water samples collected from used as a tool to elucidate the ﬂow and fate of various the eight beaches and three tidal channels were sources of organic materials in the nearshore marine ﬁltered through 25 mm GF/F grade to collect sus- waters. This will enhance better understanding of the pended POM. Sewage eﬄuent and seal faecal mat- impact of anthropogenic organic carbon and nitro- ter were collected from source and processed for genous materials on the nearshore marine waters and isotopic analysis. The samples with internal and its consequences on the functioning of the coastal certiﬁed pre-calibrated standards and blanks were marine ecosystem. Insights into the inﬂuence of placed in an autosampler carousel and combusted human-induced stressors on the dynamics of organic using the Carlo Erba NA1500. The elemental ana- materials in the nearshore marine ecosystem will lysis–isotope ratio mass spectrometry operates in a ensure proper management, conservation, and pre- continuous ﬂow mode for the determination of the servation of the coastal marine aquaculture resources carbon and nitrogen isotope ratios (δ Cand through comprehensive ecosystem-based manage- δ N). Nitrogen and carbon isotopes were assayed ment with a focus on proper land-use management. by combustion of the samples in the chromium Table 1. Sampling site with assigned code, name, and 2. Material and methods coordinates. Site Latitude Longitude 2.1. Sampling sites Allans 45.857 170.679 BlackHead 40.168 176.827 M. galloprovincialis and U. lactuca were collected Brighton 45.948 170.335 from the eight beaches along the Otago coastline at St. Clair 45.910 170.501 St. Kilda 45.908 170.517 low tide before the upgrade of the treatment plants Sandﬂy Bay 40.925 173.055 from 4/05/01 to 10/08/01 (weekly) and after the Smaills 46.019 169.089 Tomahawk 45.907 170.540 upgrade from 9/12/15 to 13/4/2016 (weekly). Tomahawk Creek 46.019 169.089 Sampleswerecollected fromtherocks in theinter- Atakore Creek 46.109 170.177 tidal zone. The marine bivalves were of average Taeiri Mouth 46.051 170.190 GEOLOGY, ECOLOGY, AND LANDSCAPES 57 oxide combustion column of the elemental analyser sample (IANZ, 2004) and random inclusion of two to produce N and CO , using helium carrier gas. in-house standards (green mussel and copepod) to 2 2 These gases were resolved in a packed molecular mimic the nature of the sample materials being sieve GC column and sent sequentially to the inlet analysed. of Europa Scientiﬁccontinuous ﬂow mode “20/20 Hydra” (Europa Scientiﬁc, UK) isotope ratio mass spectrometer (CF-IRMS) interfaced to the Sercon 2.3. Statistical analysis System Controller which runs on Sercon Callisto The carbon and nitrogen isotopic signature values Software. During the programmed run tests, the obtained in the tissues of M. galloprovincialis and samples were combusted at 1050°C, and U. lactuca were subjected to statistical evaluation NO reduced to N at 650°C within the elemental 2 2 via linear mixed-eﬀect models. The average values analyser using its normal reaction scheme. Raw of carbon and nitrogen isotopic ratios with stan- isotopic ratios obtained were normalised by three- dard errors are represented in Table 2.Using the point calibration to the international scales using R Statistical Software via the linear mixed-eﬀects 4 two International Atomic Energy Agency reference (lme4) (Bates, 2010), separate built-in linear materials (USGS-40 and USGS-41) and internal mixed-eﬀect models (see Equation 2) were ﬁtted laboratory standard (ethylenediaminetetra-acetic for the carbon and nitrogen isotopic signature acid [EDTA-OAS], δ C= − 38.92‰ ± 0.04; values in the tissues of M. galloprovincialis and δ N= −0.70‰ ± 0.17) of known carbon and U. lactuca in order to perform a likelihood of nitrogen isotopic signatures, assayed with the ratio testing of interactions among the random unknown samples. Owing to the large number of and ﬁxed eﬀects. The random eﬀects were the samples, a linearity correction method was applied various sites while primary factors of interest to ensure that the isotopic values obtained were not such as contamination, tissue type, and year were aﬀected by instrumental drift. Accuracy and preci- the ﬁxed eﬀects. The built-in ﬁtted model used for sion of the obtained isotopic results were assessed the linear mixed-eﬀect modelling analysis (LMM) by employing the root mean square RMS diﬀer- is expressed as follows: ences between sequential duplicates of every 10th Table 2. Mean isotopic carbon and nitrogen signatures (with their respective standard errors) in the tissues of Mytilus galloprovincialis and Ulva latuca collected from the uncontaminated and previously contaminated sites along Otago coastline, New Zealand in 2001 and 2015. 2001 2015 15 13 15 13 Site δ N (‰)±SE δ C (‰)± SE δ N (‰)±SE δ C (‰)±SE AIR VPDB AIR VPDB Uncontaminated sites (Mytilus galloprovincialis) Abductor Allans 8.78 ± 0.25 −18.00 ± 0.29 9.02 ± 0.13 −18.08 ± 0.40 BlackHead 7.73 ± 0.03 −20.42 ± 0.19 8.65 ± 0.29 −18.89 ± 0.30 Brighton 11.21 ± 0.56 −17.91 ± 0.23 9.26 ± 0.27 −18.48 ± 0.15 Sandﬂy Bay 10.19 ± 0.10 −20.82 ± 0.91 9.79 ± 0.09 −19.20 ± 0.04 Digestive Allans 7.20 ± 0.17 −20.49 ± 0.10 8.91 ± 0.18 −20.08 ± 0.09 BlackHead 7.65 ± 0.31 −20.36 ± 0.17 7.86 ± 0.19 −19.98 ± 0.04 Brighton 10.54 ± 0.98 −20.77 ± 0.21 8.02 ± 0.34 −19.16 ± 0.07 Sandﬂy Bay 7.06 ± 0.25 −20.62 ± 0.11 8.24 ± 0.13 −21.23 ± 0.02 Previously contaminated sites (Mytilus galloprovincialis) Abductor St. Clair 10.04 ± 0.18 −18.08 ± 0.17 9.72 ± 0.09 −17.86 ± 0.04 St. Kilda 8.64 ± 0.11 −17.33 ± 0.41 9.76 ± 0.17 −17.80 ± 0.20 Smaills 9.34 ± 0.13 −18.29 ± 0.32 8.95 ± 0.15 −19.53 ± 0.26 Tomahawk 7.33 ± 0.08 −18. 49 ± 0.50 9.68 ± 0.28 −18.72 ± 0.03 Digestive St. Clair 7.08 ± 0.27 −20.81 ± 0.30 8.45 ± 0.07 −19.14 ± 0.14 St. Kilda 6.34 ± 0.22 −17.19 ± 0.24 8.68 ± 025 −19.33 ± 0.03 Smaills 7.20 ± 0.24 −20.65 ± 0.47 8.07 ± 0.15 −20.35 ± 0.07 Tomahawk 4.83 ± 0.31 −22.81 ± 0.44 8.84 ± 0.22 −20.08 ± 0.09 Uncontaminated site (Ulva latuca) Allans 9.12 ± 0.38 −10.41 ± 0.36 9.02 ± 0.11 −18.08 ± 0.01 BlackHead 8.05 ± 0.05 −16.63 ± 0.10 8.39 ± 0.00 −20.08 ± 0.06 Brighton 7.54 ± 0.05 −16.42 ± 0.19 8.55 ± 0.22 −19.67 ± 0.03 Sandﬂy Bay 9.18 ± 0.10 −14.63 ± 0.34 9.37 ± 0.02 −16.75 ± 0.08 Previously contaminated sites (Ulva latuca) St. Clair 6.88 ± 0.06 −14.47 ± 0.72 8.81 ± 0.29 −20.39 ± 0.03 St. Kilda 5.34 ± 0.67 −16.29 ± 0.30 9.10 ± 0.08 −21.63 ± 0.04 Smaills 10.46 ± 0.15 −12.38 ± 0.15 9.10 ± 0.16 −21.63 ± 0.01 Tomahawk −3.07 ± 0.45 −15.74 ± 0.25 8.52 ± 0.01 −19.51 ± 0.03 58 O. BABARANTI ET AL. Table 3. Noticeable diﬀerences (disparity values) between the y ¼ β þ β x þ β x þ β x þ β x x þ β x x i 1i 2i 3i 1i 2i 1i 3i 0 1 2 3 4 5 mean carbon and nitrogen isotopic ratios in Mytilus gallopro- þ β x x þ α þ ε 2i 3i jiðÞ i vincialis and Ulva latuca collected in 2001 (before the (2) upgrade of TWWTP) and 2015 (after the upgrade of TWWTP) from the nearshore marine waters along Otago where Peninsula. y is the outcome for the ith experimental unit i Mytilus galloprovincialis Ulva latuca (sample) from site j, Abductor Digestive Seaweed β is the coeﬃcient for the intercept, 15 13 15 13 15 13 δ N δ C δ N δ C δ N δ C β is the coeﬃcient for the contamination eﬀect, Site (‰)(‰)(‰)(‰)(‰)(‰) β is the coeﬃcient for the year eﬀect, Uncontaminated β is the coeﬃcient for the tissue eﬀect, Allans +0.24 −0.08 +1.71 +0.41 −0.10 −7.67 BlackHead +0.92 +1.53 +0.21 +0.38 +0.34 −3.45 β is the coeﬃcient for the interaction between Brighton −1.95 −0.57 −2.52 +1.61 +1.01 −3.25 contamination and year eﬀects, Sandﬂy Bay −0.40 +1.62 +1.18 −0.61 +0.19 −2.12 Previously contaminated β is the coeﬃcient for the interaction between St. Clair −0.32 +0.22 +1.37 −1.06 +1.93 −5.92 contamination and tissue eﬀects, St. Kilda +1.12 −0.47 +2.34 −2.00 +3.76 −5.34 Smaills −0.39 −1.24 +0.87 −2.06 −1.36 −9.25 β is the coeﬃcient for the interaction between Tomahawk +2.35 −0.23 +4.01 −1.59 +11.59 −3.77 year and tissue eﬀects, α is the random eﬀect for the ith was obtained, jiðÞ where α Normalð0;σ ), jiðÞ Clair where it was 0.22‰ larger than noted in 2001. ε is the residual error term for the ith unit, where In the digestive tissues, the recorded disparity values α Normalð0;σ ), and jiðÞ 15 in the means δ N values in 2015 ranged between x , x , and x are indicator variables for the 1i 2i 3i 1.37‰ and 4.01‰ larger across all the previously contamination, year, and tissue eﬀects, respectively, contaminated sites. The recorded disparity values for the ith experimental unit where a value of 0 for the means of δ C varied between 1.06‰ and indicates the absence of a factor, and 1 indicates the 2.06‰ lesser across all the previously contaminated presence. sites (Table 3). In the tissues of U. latuca, the recorded disparity values for δ N means varied between 1.93‰ and 11.59‰ larger across three sites 3. Results and 1.36‰ lesser at Smaills than observed in 2001. 3.1. Variations in the carbon and nitrogen Contrasts between the end member’s nitrogen and isotopic ratios in M. galloprovincialis and U. carbon isotopic ratios recorded in the abductor and latuca digestive tissues of the mussels sampled in 2015 revealed that the weighted mean δ N values diﬀered The mean carbon and nitrogen isotopic ratios in M. from 0.11‰ to 1.55‰ larger in the abductor tissues galloprovincialis and U. latuca sampled in 2001 and than in the digestive tissues whereas the mean δ C 2015 are illustrated in Table 2. The disparity values of values varied from 0.68‰ to 2.03‰ larger at the the mean carbon and nitrogen isotopic ratios in M. uncontaminated sites. At the previously contami- galloprovincialis and U. latuca collected in 2001 and nated sites, weighted mean δ N values ﬂuctuated 2015 along Otago Peninsula are represented in between 0.84‰ and 1.27‰ larger in the abductor Table 3. At the uncontaminated sites, the mean tissue than digestive tissue while the weighted mean δ N values recorded in the abductor tissues of M. δ C values varied between 0.82‰ and 1.82‰ larger. galloprovincialis diﬀered between 0.21‰ and 1.71‰ larger at BlackHead and Allans correspondingly whereas disparity values ranged between 2.52‰ and 3.2. POM in samples 0.40‰ lower at Brighton and Sandﬂy Bay accordingly than previously noted in 2001. The noticeable diﬀer- The mean δ N values for POM from ﬁltered water ences for the means of δ C ﬂuctuated from 0.38‰ to samples ranged from 5.70 ± 0.20‰ to 10.06 ± 0.05‰ 1.61‰ larger at BlackHead and the Brighton accord- recorded at Akatore and Tomahawk Creek, respec- 15 13 ingly. The mean δ N values recorded in the abductor tively. The mean δ C values for the POM ranged tissues of M. galloprovincialis had disparity values from −27.18 ± 0.01‰ to −21.57 ± 0.61‰ documen- ﬂuctuated between 1.12‰ and 2.35‰ larger at St. ted at Tomahawk Creek and Akatore correspondingly Kilda and Tomahawk correspondingly whereas dis- (Table 3). The isotopic signatures of POM from these parity values varied between 0.32‰ and 0.39‰ lower varying aquatic systems indicated the probable at St. Clair and Smaills accordingly than previously sources and type of anthropogenic materials been noted in 2001. The disparity values for the means of transported into them for onward transport to the δ C ﬂuctuated from 0.23‰ to 1.24‰ lower across coastal marine waters. The reported higher mean the three previously contaminated sites except at St. carbon isotopic (δ C) and lower nitrogen isotopic GEOLOGY, ECOLOGY, AND LANDSCAPES 59 (δ N) values of Akatore Creek and Taieri Mouth Clair Beach also indicated inﬂuence by sewage eﬄu- indicated marine-based organic matter while that of ent. In 2015, M. galloprovincialis collected and ana- Tomahawk Creek seemed terrestrial due to the higher lysed showed no sign of sewage eﬄuent 15 13 δ N and lower δ C isotopic ratios. contamination. The contrast between the carbon and nitrogen isotopic ratios in the digestive tissues of the mussels from all sites evidently seemed clus- 3.3. Sewage, marine, and terrigenous particulate tered close to one another (Figure 3) in 2015 a direct matter in M. galloprovincialis contrast to 2001 observations (Figure 2). This may be attributed to these mussels feeding on a single major The nitrogen and carbon isotopic signatures analyses food source. It was observed that the mussels tend to on digestive tissues of M. galloprovincialis collected in obtain nutrition from the marine POM as most of the 2001 before the upgrade of the sewage treatment mussels sampled at the previously contaminated and plant revealed that 90% of M. galloprovincialis col- uncontaminated sites assumed trophic shift (enrich- lected from Tomahawk were heavily isotopically 15 13 ment factor) of roughly 3‰ for δ N and 1‰ for the depleted in δ N and δ C with 60% of nitrogen and δ C cf. to the marine POM. The marine bivalve 40% of carbon in the digestive tissue derived from might also be deriving sustenance from other terres- sewage particulate matter while between 30% and trial organic materials incursions to the nearshore 60% of mussels from St. Kilda, Smaills, and St. Clair waters. The contrasts of carbon and nitrogen ratios showed signs of mild sewage contamination. This is in the tissues of U. latuca in the 2015 sampling were indicative that eﬄuent seemed to provide a source of unpredictable as opposed to the trend observed in sustenance for the ingested phytoplankton biomass or 2001. Of particular note are the results from at direct ingestion of sewage POM by M. galloprovincia- Tomahawk and St. Clair when 2001 nutrient enrich- lis appraised at the previously contaminated sites so ment was predominantly SDOM (Figure 4) whereas much to sway the marine bivalve isotopic ratios all sites exhibit the marine source predominantly in greatly. U. latuca collected in 2001 from Tomahawk 15 2015 (Figure 5). In 2015, no detectable sewage eﬄu- has negative mean δ N, an indication of sewage ent inﬂuence was observed, rather the isotopic values eﬄuent alteration, and 40% of U. latuca sampled St. Figure 3. Comparison of carbon and nitrogen-stable isotopic ratios in the digestive tissues of Mytilus galloprovincialis and particulate materials collected in 2015 along the Otago coastline, New Zealand. Figure 4. Comparison of carbon and nitrogen-stable isotopic ratios in the tissues of Ulva lactuca and particulate materials collected in 2001 along the Otago coastline, New Zealand. 60 O. BABARANTI ET AL. Figure 5. Comparison of carbon and nitrogen-stable isotopic ratios in the tissues of Ulva lactuca and particulate materials collected in 2015 along the Otago coastline, New Zealand. plotted towards the seal faecal matter were at Allans assumption, the obtained δ N – percentage contri- and Sandﬂy Bay and terrigenous-based sources at all bution of the marine to terrestrial contribution in the other sites sampled (Figures 4 and 5). The outline of digestive tissues of the mussels collected from each of the isotopic ratios of analysis on tissues of U. latuca the previously contaminated sites – was as follows: St. seemed to assume orientation towards enrichment Clair (37%:63%), St. Kilda (49%:51%), Smaills from characterised ﬁltered water samples (POM) a (87%:13%), and Tomahawk (52%:48%). The δ C – pointer to possible nutrient enrichment from terres- percentage contribution was principally from marine trial sources. particulate matter for most of the sites. Smaills and Tomahawk had 4% and 1% of δ C terrestrial parti- culate matter contribution accordingly. No inﬂuence 3.4. Linear isotopic mixing model of terrestrial particulate matter was detected at St. Kilda and St. Clair could not be estimated. We tried Estimating the relative contributions of carbon and to estimate the contribution of the sewage eﬄuent in nitrogen organic materials from terrestrial sources in the digestive tissue of M. galloprovincialis we the digestive tissues of M. galloprovincialis sampled in 13 15 obtained negative values for both δ C and δ N. 2015 so as to quantify the magnitude of suspended POM (i.e., terrigenous materials) in the biological samples, a simple modiﬁed two-end member linear 3.5. Analysis of variance between carbon and isotopic mixing model (Waldron, Tatner, Jack, & nitrogen isotopic signatures in M. Arnott, 2001) as expressed in Equations 3 and 4 galloprovincialis and U. lactuca below was used: The mean carbon and nitrogen isotopic ratio values 15 15 15 δ N ¼ δ N X þ Y δ N (3) in the tissues of M. galloprovincialis and U. lactuca mussel POM control for 2001 and 2015 were subjected to statistical analy- 13 13 13 sis using the LMM to determine if there were signiﬁ- δ C ¼ δ C XþY δ C (4) mussel POM control cant interactions between the carbon and nitrogen X is the contribution from marine/phytoplankton isotopic ratios reported in 2001 and 2015 within source and Y =(1 − X) which is the terrigenous and across the study sites. The LMM determined materials (multiplied by 100). the ratio testing values for the crisscross in the varia- Using the observed mean isotopic ratios of the bility of carbon and nitrogen isotopic ratios recorded POM from ﬁltered water samples collected from in M. galloprovincialis and U. lactuca across the end Tomahawk Creek (δ N = 10.06‰ and member sites (uncontaminated and previously con- δ C= − 27.18‰) as the terrestrial source and taminated). The outcomes of the interactions are mean isotopic ratios of mussels collected from represented in Table 4. Highly signiﬁcant diﬀerences BlackHead (uncontaminated site) (i.e., (p = < 0.0001, n = 169 [abductor]; p = 0.0022, n = 169 15 13 δ N = 7.86‰ and δ C= − 19.98‰) as the control [digestive]) were recorded between 2001 and 2015 15 13 end member while δ N and δ C were for nitrogen isotopic ratios in the digestive tissues of M. mussel mussel the carbon and nitrogen isotopic ratios of mussels galloprovincialis and tissues of U. lactuca sampled from the previously sewage contaminated (p = < 0.0001, n = 30) collected at the previously sites. We assumed a two-source nutrient-enrichment contaminated sites. There were no signiﬁcant diﬀer- isotopic mixing model for the mussels coming from ences in the 2015 nitrogen isotopic ratios in the marine and terrigenous sources. Based on this digestive and abductor tissues of M. galloprovincialis GEOLOGY, ECOLOGY, AND LANDSCAPES 61 Table 4. Mean with standard error values of nitrogen and carbon isotopic signatures values from the particulate organic matter in ﬁltered water, sewage eﬄuent, and seal faeces samples collected from the coastal marine waters along Otago coastline in 2001(bracket) and 2015. 15 13 Site δ N (‰)±SE δ C (‰)± SE AIR PVB Atakore creek 5.70 ± 0.20 (5.80 ± 1.70) −21.57 ± 0.61(−17.30 ± 2.10) Teaeiri Mouth 5.80 ± 0.16 (5.40 ± 2.60) −24.03 ± 0.73 (24.30 ± 1.50) Tomahawk Creek 10.06 ± 0.06 (8.70 ± 0.50) −27.18 ± 0.01 (−27.00 ± 0.30) Eﬄuent POM 3.10 ± 0.50 −25.80 ± 0.10 Seal faeces POM 14.20 ± 0.60 −21.90 ± 0.30 (p = 0.3831, n = 8 [abductor]; p = 0.8587, n =8 δ N than the other sites suggestive of uptake of [digestive]). No signiﬁcant diﬀerences were observed the sewage eﬄuent. Sewage eﬄuent and other in the 2015 carbon isotopic ratios in the digestive and anthropogenic inputs had been known to modify abductor tissues of M. galloprovincialis (p = 0.2476, the carbon and nitrogen isotopic ratios of macro- n = 6 [abductor]; p = 0.8357, n = 6 [digestive]). No algae (Fry, 2002; Fry, Gace, & McClelland, 2003; signiﬁcant diﬀerences were observed in δ N Gartner, Lavery, & Smit, 2002; Rogers, 2003; (p = 0.8469, n = 6) and δ C(p = 0.0022, n =6)in Savage, 2005; Savage & Elmgren, 2004) and respon- the tissues of U. lactuca sampled at the uncontami- siblefor excessivegrowthofmicroalgaeinnear- nated and previously contaminated sites in 2015 shore marine waters (Baker, MacAvoy, & Kim, (Table 5). 2007; Connolly, Gorman, Hindell, Kildea, & Schlacher, 2013; Morand & Merceron, 2005; Yang, Wu,Hao,&He, 2008). 4. Discussion In 2015, the tissues of U. latuca sampled at Tomahawk and St. Kilda were found to be N ele- At thetimeofthe ﬁrst sampling event (Horn, vated by 11.59‰ and 3.76‰, respectively, than 2001), two of the study sites (Smaills and recorded in 2001 indicating a remarkable recovery Tomahawk Beaches) were known to be contami- from sewage inﬂuence. There was good agreement nated with sewage-derived matter and exhibited between the 2001 and 2015 mean δ N values in the high faecal coliform counts (Greening et al., 2007; tissues of U. latuca between the recorded values at the Lewis et al., 2010). In 2001, the carbon and nitro- uncontaminated sites (i.e., reference sites) which var- genisotopicratiosinthe tissuesof M. galloprovin- ied between 8‰ and 9‰ (p = 0.112, n = 30) sugges- cialis and U. latuca indicated that two sites (i.e., tive of absence of sewage organic matter as nutrient Tomahawk and Smaills) were heavily impacted by source. However, the recorded δ C mean values the discharged sewage eﬄuent demonstrated in the 13 15 between 2001 and 2015 in the tissues of U. latuca lower δ C and δ Nvalues. Thetissues of U. were a departure from the observed trend in δ Nat latuca sampled at Tomahawk (closest site to the the reference sites varying from −20‰ to −10‰ outfall) and St. Kilda were found to have lower Table 5. Linear mixed-eﬀects model (LMM) analysis result of the stable carbon and nitrogen isotopic signatures in the tissues of Mytilus galloprovincialis and Ulva latuca collected in 2001 and 2015 from the various study sites along Otago coastline. Site contrast Year Variable Tissue df (n − 1) t Ratio p-Value* Previously contaminated 2001–2015 δ N Abductor 169 −3.61 0.0022 Uncontaminated 2001–2015 δ N Abductor 169 1.71 0.3202 Previously contaminated 2001–2015 δ N Digestive 169 −9.26 <0.0001 Uncontaminated 2001–2015 δ N Digestive 169 −3.75 0.0014 Previously contaminated 2001–2015 δ N Seaweed 30 −8.09 <0.0001 Uncontaminated 2001–2015 δ N Seaweed 30 1.65 0.1102 Previously contaminated 2001–2015 δ C Abductor 177 0.52 0.9546 Uncontaminated 2001–2015 δ C Abductor 177 0.79 0.8595 Previously contaminated 2001–2015 δ C Digestive 177 −6.84 <0.0001 Uncontaminated 2001–2015 δ C Digestive 177 −4.98 <0.0001 Previously contaminated 2001–2015 δ C Seaweed 30 15.69 <0.0001 Uncontaminated 2001–2015 δ C Seaweed 30 34.19 <0.0001 Uncontaminated–previously contaminated 2001 δ N Abductor 6 1.35 0.0170 Uncontaminated–previously contaminated 2001 δ N Digestive 6 2.50 0.0401 Uncontaminated–previously contaminated 2001 δ C Abductor 6 −0.89 0.4067 Uncontaminated–previously contaminated 2001 δ C Digestive 6 1.70 0.1404 Uncontaminated–previously contaminated 2001 δ N Seaweed 6 3.59 0.0115 Uncontaminated–previously contaminated 2001 δ C Seaweed 6 0.43 0.6838 Uncontaminated–previously contaminated 2015 δ N Abductor 8 −0.92 0.3831 Uncontaminated–previously contaminated 2015 δ N Digestive 8 0.18 0.8587 Uncontaminated–previously contaminated 2015 δ C Abductor 6 −1.28 0.2476 Uncontaminated–previously contaminated 2015 δ C Digestive 6 0.22 0.8357 Uncontaminated–previously contaminated 2015 δ N Seaweed 6 0.20 0.8469 Uncontaminated–previously contaminated 2015 δ C Seaweed 6 0.68 0.5235 (*The level of signiﬁcance was set at 5%. Values of p < 0.05 were considered signiﬁcant, p < 0.01 and p < 0.001.) 62 O. BABARANTI ET AL. (p < 0.0001, n = 30). This abnormality in the variance 5. Conclusion of δ C might be attributed to the discrepancies in Carbon and nitrogen isotopic ratios in the tissues C discrimination during photosynthesis and of M. galloprovincialis and U. lactuca were found respiration by the seaweeds rather than nutrient to be suitable bioindicators for investigating the enhancement. impact of SDOM and possible terrigenous materi- The modiﬁcations in the treatment and disposal als on the nearshore marine waters. M. gallopro- of sewage eﬄuent have had a profound positive vincialis and U. lactuca were inﬂuenced by sewage eﬀect on the environmental conditions at the pre- at the two previously contaminated beaches in viously contaminated sites. The extension of the 2001. Repeat survey in 2015 showed positive outfall pipes had assisted in limiting the inﬂuence changes in the isotope ratios values of the near- of periodic ﬂood currents associated with the tidal shore marine resident sentinel organisms in com- and wave actions that usually cascade sewage parison with the values reported 2001, suggesting eﬄuent towards the previously contaminated that the modiﬁcations of the sewage treatment sites. The digestive tissues of M. galloprovincialis processes and extension of the outfalls have been provided a good pointer to the declined inﬂuence eﬀective in directing sewage-derived C and N of the sewage-derived exhibiting a trophic enrich- away from the previously contaminated sites. 13 13 ment (δ C~1‰ and δ N~3‰)towards the Contrast of the isotopic ratios of these sentinel marine POM. Discriminating between the 2010 organisms from previously and reference sites and 2015 carbon and nitrogen isotopic ratios in was indistinguishable in 2015 contrary from the the tissues of M. galloprovincialis from reference 2001 survey. Mixing models reveal mussels at the and previously contaminated sites revealed highly two previously contaminated beaches now get signiﬁcant diﬀerences in both abductor and diges- most of their nutrition from marine POM with a tive tissues. The contrast of the 2015carbon and minor subsidy from terrestrial sources. nitrogen isotopic ratios in the tissues (i.e., abduc- tor and digestive) of M. galloprovincialis from the reference and previously contaminated sites 6. Implications and directions for future revealed no signiﬁcant diﬀerences. study The two-source isotopic mixing model revealed The sentinel organisms provided an opportunity for the contribution of terrigenous organic materials in further temporal and spatial scale isotopic studies the marine bivalve to vary from 1% to 5% for δ C juxtaposed with conceptual isotopic mixing models and 13% to 51% for δ N. The carbon and nitrogen and application of chemical tracers to trace the isotopic values of the suspended POM from ﬁltered sources, ﬂow, cycling, and providence of nutrients water samples of the riverine and estuarine systems and organic materials in the nearshore marine with open connection to the ocean reﬂected the waters. Surveying the environmental conditions, diversiﬁed nature of the pool of organic materials biological activity and hydrodynamics of the near- incursions to the nearshore coastal waters. These shore waters will provide additional insight on the sources range from natural to human-induced activ- underlying mechanisms responsible for the cross- ities, e.g., atmospheric deposition, organic waste boundary (i.e., land-ocean coupling) transfer of materials from the farm (manure) and grazing mar- nutrients and organic materials to the nearshore ine animals (sea lions and birds), fertilisers, and pos- waters and their eventual sequestration to the near- sibly groundwater leachates arising from the shore marine food web. nitriﬁcation of ammonium from animal organic waste residues underground. Land-based nitrogen sources from tidal channels seemed to sway the near- Disclosure statement shore marine waters while carbon sources were pre- No potential conﬂict of interest was reported by the authors. dominantly marine origin. The macro-algae communities (such as Macrocystis sp.) that are washed onshore and into the tidal channels contri- Funding bute a substantial amount of carbon and nutrients to This work was supported by the University of Otago the nearshore waters and freshwater systems along [Doctoral scholarship]. the coastline (Duggins, 1988; Hepburn, Holborow, Wing, Frew, & Hurd, 2007; Michelou, Caporaso, Knight, & Palumbi, 2013). Other likely sources are Statement of Ethics sewage-derived matter inﬂuxes from pastoral ani- The number of shellﬁsh collected per day from each of the mals, farm organic manure, detrital matter (i.e., study sites during the course of this study was in accordance decomposition of plant materials, seagrasses in estu- with the New Zealand Fisheries Amended Act (Amateur aries), rural runoﬀs, and watershed catchment area. Fishing) Regulations of 1986: revoked, on 1 February 2014, GEOLOGY, ECOLOGY, AND LANDSCAPES 63 by regulation 161(1) (a) of the Fisheries (Amateur Fishing) sewage signals in multiple marine taxa. Marine Regulations 2013 (SR 2013/482) stipulated in Section 19 Pollution Bulletin, 71(1–2), 152–158. Sub-clause 1 and 2. Furthermore, numbers of biological Coplen, T. B. (2011). Guidelines and recommended terms samples collected and analysed did not in any way aﬀect for expression of stable-isotope-ratio and gas-ratio mea- the species composition, diversity, and coastal ecosystem surement results. Rapid Communications in Mass functioning of the nearshore marine waters. Spectrometry, 25(17), 2538–2560. Council, O. R. (2001). Regional Plan: Coast. Accessed Online January, 12, 2008. Dede, O.T., Telci, I. T.,&Aral, M.M.(2013). The use ORCID of water quality index models for the evaluation of surface water quality: A case study for Kirmir Basin, Oluwuyi Babaranti http://orcid.org/0000-0002-9047- Ankara, Turkey. Water Quality, Exposure and Health, 5(1), 41–56. Tim Jowett http://orcid.org/0000-0001-7146-5188 Deegan, L. A., & Buchsbaum, R. (2005). The eﬀect of Russell Frew http://orcid.org/0000-0002-3492-9454 habitat loss and degradation on ﬁsheries. The decline of ﬁsheries resources in New England: Evaluating the impact of overﬁshing, contamination, and habitat degradation References (pp. 67–96). MA: MIT Sea Grant College Program. Deudero, S., Box, A., Tejada, S., & Tintoré, J. (2009). Stable Abbasi, T., & Abbasi, S. (2011). Water quality indices based isotopes and metal contamination in caged marine mus- on bioassessment: The biotic indices. Journal of Water sel. Mytilus Galloprovincialis. Marine Pollution Bulletin, and Health, 9(2), 330–348. 58(7), 1025–1031. Alfaro, A. C., Jeﬀs, A. G., & Hooker, S. H. (2001). Diaz, R. J., Rhoads, D. C., Blake, J. A., Kropp, R. K., & Reproductive behavior of the green-lipped mussel, Keay, K. E. (2008). Long-term trends of benthic habitats Perna canaliculus, in Northern New Zealand. Bulletin related to reduction in wastewater discharge to Boston of Marine Science, 69(3), 1095–1108. Harbor. Estuaries and Coasts, 31(6), 1184–1197. Baker, D. M., MacAvoy, S. E., & Kim, K. (2007). Doré, W. J., Henshilwood, K., & Lees, D. N. (2000). Relationship between water quality, δ N, and aspergil- Evaluation of F-speciﬁc RNA bacteriophage as a candi- losis of Caribbean sea fan corals. Marine Ecology date human enteric virus indicator for bivalve molluscan Progress Series, 343, 123–130. shellﬁsh. Applied and Environmental Microbiology, 66 Barr, N. G., Dudley, B. D., Rogers, K. M., & Cornelisen, C. (4), 1280–1285. D. (2013). Broad-scale patterns of tissue-δ Nand tissue- Dudley, B. D., & Shima, J. S. (2010). Algal and invertebrate N indices in frondose Ulva spp.; Developing a national bioindicators detect sewage eﬄuent along the coast of baseline indicator of nitrogen-loading for coastal New Titahi Bay, Wellington, New Zealand. New Zealand Zealand. Marine Pollution Bulletin, 67(1), 203–216. Journal of Marine and Freshwater Research, 44(1), 39–51. Bates, D. M. (2010). lme4: Mixed-eﬀects modeling with R. Duggins, D. (1988). The eﬀects of kelp forests on nearshore Retrieved from http://lme4.r-forge.r-project.org/book. environments: Biomass, detritus, and altered ﬂow. The Bedard-Haughn, A., Van Groenigen, J., & Van Kessel, C. Community Ecology of Sea Otters, 65(9), 192–201. (2003). Tracing 15N through landscapes: Potential uses Ebner, B. C., McAllister, R. R., & Suter, P. (2009). Eﬀects of and precautions. Journal of Hydrology, 272(1–4), 175–190. sample size on numerical estimates of diet prey con- Bouman, R., & Archer, H. (2014). Tahuna WWTP, sumption in a ﬁsh population. New Zealand Journal of Dunedin, New Zealand: An innovative upgrade. Marine and Freshwater Research, 43(2), 579–590. Proceedings of the Water Environment Federation, 2014 Ellis, T. G. (2004). Chemistry of wastewater. Encyclopedia (16), 4096–4116. of Life Support System (EOLSS), 2, 1–10. Browne, M. A., Crump, P., Niven, S. J., Teuten, E., Tonkin, Fry, B. (2002). Conservative mixing of stable isotopes A., Galloway, T., et al. (2011). Accumulation of micro- across estuarine salinity gradients: A conceptual frame- plastic on shorelines worldwide: Sources and sinks. work for monitoring watershed inﬂuences on down- Environmental Science & Technology, 45(21), 9175–9179. stream ﬁsheries production. Estuaries, 25(2), 264–271. Bump, J. K., Fox-Dobbs, K., Bada, J. L., Koch, P. L., Fry, B., Gace, A., & McClelland, J. W. (2003). Chemical Peterson, R. O., & Vucetich, J. A. (2007). Stable isotopes, indicators of anthropogenic nitrogen-loading in four ecological integration and environmental change: Paciﬁc estuaries. Paciﬁc Science, 57(1), 77–101. Wolves record atmospheric carbon isotope trend better Gartner, A., Lavery, P., & Smit, A. (2002). Use of δ N than tree rings. Proceedings of the Royal Society of signatures of diﬀerent functional forms of macroalgae London B: Biological Sciences, 274(1624), 2471–2480. and ﬁlter-feeders to reveal temporal and spatial pat- Cabana, G., & Rasmussen, J. B. (1996). Comparison of terns in sewage dispersal. Marine Ecology Progress aquatic food chains using nitrogen isotopes. Series, 235,63–73. Proceedings of the National Academy of Sciences, 93 Gaston, T. F., & Suthers, I. M. (2004). Spatial variation in (20), 10844–10847. 13 15 δ C and δ N of liver, muscle and bone in a rocky reef Chary, N. S., Kamala, C., & Raj, D. S. S. (2008). Assessing planktivorous ﬁsh: The relative contribution of sewage. risk of heavy metals from consuming food grown on Journal of Experimental Marine Biology and Ecology, 304 sewage irrigated soils and food chain transfer. (1), 17–33. Ecotoxicology and Environmental Safety, 69(3), 513–524. Gormley,A.M.,Slooten,E.,Dawson,S.,Barker,R.J., Cheevaporn, V., & Menasveta, P. (2003). Water pollution Rayment,W.,DuFresne,S.,&Bräger,S.(2012). First and habitat degradation in the Gulf of Thailand. Marine evidence that marine protected areas can work for Pollution Bulletin, 47(1), 43–51. marine mammals. Journal of Applied Ecology, 49(2), Connolly, R. M., Gorman, D., Hindell, J. S., Kildea, T. N., & 474–480. Schlacher, T. A. (2013). High congruence of isotope 64 O. BABARANTI ET AL. Greening, G. E., Lewis, G. D., & Dollimore, J. (2007). FRST North, J. C., Frew, R. D., & Hale, R. V. (2006). Can stable programme C03X0301 safeguarding environmental isotopes be used to monitor landﬁll leachate impact on health and market access for NZ foods objective 2: surface waters? Journal of Geochemical Exploration, 88 Virus prevalence in shellﬁsh. 1,1–45. (1–3), 49–53. Hargrave, B., Holmer, M., & Newcombe, C. (2008). North, J. C., Frew, R. D., & Peake, B. M. (2004). The use of Towards a classiﬁcation of organic enrichment in mar- carbon and nitrogen isotope ratios to identify landﬁll lea- ine sediments based on biogeochemical indicators. chate contamination: Green Island Landﬁll, Dunedin, New Marine Pollution Bulletin, 56(5), 810–824. Zealand. Environment International, 30(5), 631–637. Hepburn, C. D., Holborow, J. D., Wing, S. R., Frew, R. D., Ouédraogo, O., Chételat, J., & Amyot, M. (2015). & Hurd, C. L. (2007). Exposure to waves enhances the Bioaccumulation and trophic transfer of mercury and growth rate and nitrogen status of the giant kelp selenium in African sub-tropical ﬂuvial reservoirs food Macrocystis pyrifera. Marine Ecology Progress Series, webs (Burkina Faso). PloS One, 10(4), e0123048. 339,99–108. Pan, J.-F., & Wen-Xiong, W. (2004). Diﬀerential uptake of Hillebrand, H., & Sommer, U. (2000). Diversity of benthic dissolved and particulate organic carbon by the marine microalgae in response to colonization time and eutro- mussel. Perna Viridis. Limnology and Oceanography, 49 phication. Aquatic Botany, 67(3), 221–236. (6), 1980–1991. Horn, S. (2001). Tracking marine sewage outfall along the Peterson, B. J. (1999). Stable isotopes as tracers of organic Otago Peninsula using stable isotope analysis of blue matter input and transfer in benthic food webs: A mussels Mytilus galloprovincialis, and sea lettuce Ulva review. Acta Oecologica, 20(4), 479–487. lactuca, as biotracer species, pp33 (BSc (Hons) Post, D. M. (2002). Using stable isotopes to estimate Dissertation). Otago, Dunedin, New Zealand. trophic position: Models, methods, and assumptions. IANZ. (2004). Uncertainty of measurement, precision and Ecology, 83(3), 703–718. limits of detection chemical and microbiological testing Rayment, W., Dawson, S., & Slooten, E. (2010). Seasonal laboratories. International Accrediation New Zealand: changes in distribution of Hector’s dolphin at Banks Auckland. Peninsula, New Zealand: Implications for protected Jarvie, H. P., Neal, C., & Withers, P. J. (2006). Sewage- area design. Aquatic Conservation: Marine and eﬄuent phosphorus: A greater risk to river eutrophica- Freshwater Ecosystems, 20(1), 106–116. tion than agricultural phosphorus? Science of the Total RCL. (2000). Otago regional council resource consent 97530 Environment, 360(1–3), 246–253. condition 8: Rocky Shore Ecological Monitoring-January/ Kline, J., & Thomas, C. (1999). Temporal and spatial varia- February 2000. Dunedin, New Zealand: Ryder 13 12 15 14 bility of C/ C and N/ N in pelagic biota of Prince Consulting Ltd. William Sound, Alaska. Canadian Journal of Fisheries Rogers, K. M. (2003). Stable carbon and nitrogen isotope and Aquatic Sciences, 56(S1), 94–117. signatures indicate recovery of marine biota from sewage Lewis, G. D., Loutit, M. W., & Austin, F. J. (2010). Human pollution at Moa Point, New Zealand. Marine Pollution enteroviruses in marine sediments near a sewage outfall Bulletin, 46(7), 821–827. on the Otago Coast. New Zealand Journal of Marine and Savage, C. (2005). Tracing the inﬂuence of sewage nitrogen in Freshwater Research, 19(2), 187–192. a coastal ecosystem using stable nitrogen isotopes. AMBIO: Lorrain, A., Paulet, Y.-M., Chauvaud, L., Savoye, N., A Journal of the Human Environment, 34(2), 145–150. Donval, A., & Saout, C. (2002). Diﬀerential δ C and Savage, C., & Elmgren, R. (2004). Macroalgal (Fucus vesi- 15 15 δ N signatures among scallop tissues: Implications for culosus) δ N values trace decrease in sewage inﬂuence. ecology and physiology. Journal of Experimental Marine Ecological Applications, 14(2), 517–526. Biology and Ecology, 275(1), 47–61. SITO. (2006). Seafood industry training organisation- learn- Michelou, V. K., Caporaso, J. G., Knight, R., & Palumbi, ing resource for unit standard 16340 v3 “Biology of new S. R. (2013). The ecology of microbial communities zealand green mussels” 1, 1–23. associated with Macrocystis pyrifera. PLoS One, 8(6), Teklehaimanot, G. Z., Coetzee, M. A., & Momba, M. N. e67480. (2014). Faecal pollution loads in the wastewater eﬄuents Michener, R. H., & Kaufman, L. (2008). Stable isotope and receiving water bodies: A potential threat to the ratios as tracers in marine food webs: An update. health of Sedibeng and Soshanguve communities, Stable Isotopes in Ecology and Environmental Science, South Africa. Environmental Science and Pollution Second Edition, 2, 238–282. Research, 21(16), 9589–9603. Morand, P., & Merceron, M. (2005). Macroalgal population Thompson, D., Phillips, R., Stewart, F., & Waldron, S. and sustainability. Journal of Coastal Research, 215, (2000). Low δ C signatures in pelagic seabirds: Lipid 1009–1020. ingestion as a potential source of C-depleted carbon in Morillo, J., Usero, J., & Gracia, I. (2004). Heavy metal the Procellariiformes. Marine Ecology Progress Series, distribution in marine sediments from the Southwest 208, 265–271. coast of Spain. Chemosphere, 55(3), 431–442. Waldron, S., Tatner, P., Jack, I., & Arnott, C. (2001). The Nicholson, C. M., Lewis, G. D., & Loutit, M. W. (1989). impact of sewage discharge in a marine embayment: A Survey of human pathogenic bacteria and viruses in stable isotope reconnaissance. Estuarine, Coastal and cockle beds at Otakou, Otago Harbour, New Zealand. Shelf Science, 52(1), 111–115. New Zealand Journal of Marine and Freshwater Yang, X. E., Wu, X., Hao, H.-L., & He, Z.-L. (2008). Research, 23(4), 529–532. Mechanisms and assessment of water eutrophication. Nordsieck, R. (2006, December 12). The living world of Journal of Zhejiang University Science B: Biomedicine molluscs. The Common Mussel (Mytilus edulis). and Biotechnology, 9(3), 197–209. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Geology Ecology and Landscapes Taylor & Francis http://www.deepdyve.com/lp/taylor-francis/isotopic-signatures-in-mytilus-galloprovincialis-and-ulva-latuca-as-jLJM9G5GSX

Loading next page...

References (69)

T. Coplen (2011)
Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results.
Rapid communications in mass spectrometry : RCM, 25 17
A. Alfaro, A. Jeffs, S. Hooker (2001)
Reproductive behavior of the green-lipped mussel, Perna canaliculus, in Northern New Zealand
Bulletin of Marine Science, 69
O. Ouédraogo, J. Chételat, Marc Amyot (2015)
Bioaccumulation and Trophic Transfer of Mercury and Selenium in African Sub-Tropical Fluvial Reservoirs Food Webs (Burkina Faso)
PLoS ONE, 10
B. Peterson (1999)
Stable isotopes as tracers of organic matter input and transfer in benthic food webs: A review
Acta Oecologica-international Journal of Ecology, 20
N. Chary, C. Kamala, D. Raj (2008)
Assessing risk of heavy metals from consuming food grown on sewage irrigated soils and food chain transfer.
Ecotoxicology and environmental safety, 69 3
C. Savage (2005)
Tracing the Influence of Sewage Nitrogen in a Coastal Ecosystem Using Stable Nitrogen Isotopes
, 34
(2008)
Stable isotope ratios as tracers in marine food webs: An update. Stable Isotopes in Ecology and Environmental Science
G. Lewis, M. Loutit, F. Austin (1985)
Human enteroviruses in marine sediments near a sewage outfall on the Otago Coast
New Zealand Journal of Marine and Freshwater Research, 19
S. Waldron, P. Tatner, I. Jack, C. Arnott (2001)
The impact of sewage discharge in a marine embayment : A stable isotope reconnaissance
Estuarine Coastal and Shelf Science, 52
Ozlem Tunc Dede, Ilker Telci, M. Aral (2013)
The Use of Water Quality Index Models for the Evaluation of Surface Water Quality: A Case Study for Kirmir Basin, Ankara, Turkey
Water Quality, Exposure and Health, 5
A. Bedard-Haughn, J. Groenigen, C. Kessel (2003)
Tracing 15N through landscapes: potential uses and precautions
Journal of Hydrology, 272
G. Teklehaimanot, M. Coetzee, M. Momba (2014)
Faecal pollution loads in the wastewater effluents and receiving water bodies: a potential threat to the health of Sedibeng and Soshanguve communities, South Africa
Environmental Science and Pollution Research, 21
B. Hargrave, M. Holmer, C. Newcombe (2008)
Towards a classification of organic enrichment in marine sediments based on biogeochemical indicators.
Marine pollution bulletin, 56 5
B. Fry (2002)
Conservative mixing of stable isotopes across estuarine salinity gradients: A conceptual framework for monitoring watershed influences on downstream fisheries production
Estuaries, 25
B. Dudley, J. Shima (2010)
Algal and invertebrate bioindicators detect sewage effluent along the coast of Titahi Bay, Wellington, New Zealand
New Zealand Journal of Marine and Freshwater Research, 44
J. North, Russell Frew, B. Peake (2004)
The use of carbon and nitrogen isotope ratios to identify landfill leachate contamination: Green Island Landfill, Dunedin, New Zealand.
Environment international, 30 5
R. Buchsbaum, J. Pederson, W. Robinson (2005)
The decline of fisheries resources in New England : evaluating the impact of overfishing, contamination, and habitat degradation
A. Gartner, P. Lavery, A. Smit (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
V. Cheevaporn, P. Menasveta (2003)
Water pollution and habitat degradation in the Gulf of Thailand.
Marine pollution bulletin, 47 1-6
(2001)
Regional Plan: Coast
R. Michener, L. Kaufman (2008)
Stable Isotope Ratios as Tracers in Marine Food Webs: An Update
(2010)
lme4: Mixed-effects modeling with R
Vanessa Michelou, J. Caporaso, R. Knight, S. Palumbi (2013)
The Ecology of Microbial Communities Associated with Macrocystis pyrifera
PLoS ONE, 8
B. Ebner, R. McALLISTER, P. Suter (2009)
Effects of sample size on numerical estimates of diel prey consumption in a fish population
New Zealand Journal of Marine and Freshwater Research, 43
Tasneem Abbasi, S. Abbasi (2011)
Water quality indices based on bioassessment: the biotic indices.
Journal of water and health, 9 2
W. Rayment, S. Dawson, E. Slooten (2009)
Seasonal changes in distribution of Hector's dolphin at Banks Peninsula, New Zealand: implications for protected area design
Aquatic Conservation-marine and Freshwater Ecosystems, 20
N. Barr, B. Dudley, K. Rogers, Christopher Cornelisen (2013)
Broad-scale patterns of tissue-δ15N and tissue-N indices in frondose Ulva spp.; developing a national baseline indicator of nitrogen-loading for coastal New Zealand.
Marine pollution bulletin, 67 1-2
J. Morillo, J. Usero, I. Gracia (2004)
Heavy metal distribution in marine sediments from the southwest coast of Spain.
Chemosphere, 55 3
C. Savage, R. Elmgren (2004)
MACROALGAL (FUCUS VESICULOSUS) δ15N VALUES TRACE DECREASE IN SEWAGE INFLUENCE
Ecological Applications, 14
T. Gaston, I. Suthers (2004)
Spatial variation in δ13C and δ15N of liver, muscle and bone in a rocky reef planktivorous fish: the relative contribution of sewage
Journal of Experimental Marine Biology and Ecology, 304
H. Hillebrand, U. Sommer (2000)
Diversity of benthic microalgae in response to colonization time and eutrophication
Aquatic Botany, 67
(2004)
Heavy metal distribution in marine sediments from the Southwest coast
B. Fry, Arian Gace, J. McClelland (2003)
Chemical Indicators of Anthropogenic Nitrogen-Loading in Four Pacific Estuaries
Pacific Science, 57
D. Thompson, R. Phillips, F. Stewart, S. Waldron (2000)
Low δ13C signatures in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in the Procellariiformes
Marine Ecology Progress Series, 208
D. Post (2002)
USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS
Ecology, 83
The living world of molluscs. The Common Mussel
Jinfen Pan, Wang Wen-xiong (2004)
Differential uptake of dissolved and particulate organic carbon by the marine mussel Perna viridis
Limnology and Oceanography, 49
(2009)
Stable isotopes and metal contamination in caged marine mussel
W. Doré, K. Henshilwood, D. Lees (2000)
Evaluation of F-Specific RNA Bacteriophage as a Candidate Human Enteric Virus Indicator for Bivalve Molluscan Shellfish
Applied and Environmental Microbiology, 66
Jr. Kline (1999)
Temporal and spatial variability of 13C/12C and 15N/14N in pelagic biota of Prince William Sound, Alaska
Canadian Journal of Fisheries and Aquatic Sciences, 56
M. Browne, Phillip Crump, S. Niven, Emma Teuten, A. Tonkin, T. Galloway, Richard Thompson (2011)
Accumulation of microplastic on shorelines woldwide: sources and sinks.
Environmental science & technology, 45 21
J. Bump, K. Fox-Dobbs, J. Bada, P. Koch, R. Peterson, J. Vucetich (2007)
Stable isotopes, ecological integration and environmental change: wolves record atmospheric carbon isotope trend better than tree rings
Proceedings of the Royal Society B: Biological Sciences, 274
(2007)
FRST programme C03X0301 safeguarding environmental health and market access for NZ foods objective 2: Virus prevalence in shellfish
(2004)
Uncertainty of measurement, precision and limits of detection chemical and microbiological testing laboratories
G. Cabana, J. Rasmussen (1996)
Comparison of aquatic food chains using nitrogen isotopes.
Proceedings of the National Academy of Sciences of the United States of America, 93 20
(2000)
Otago regional council resource consent 97530 condition 8: Rocky Shore Ecological Monitoring-January/ February 2000
Regional Plan: Coast. Accessed Online
H. Jarvie, C. Neal, P. Withers (2006)
Sewage-effluent phosphorus: a greater risk to river eutrophication than agricultural phosphorus?
The Science of the total environment, 360 1-3
C. Nicholson, G. Lewis, M. Loutit (1989)
Survey of human pathogenic bacteria and viruses in cockle beds at Otakou, Otago Harbour, New Zealand
New Zealand Journal of Marine and Freshwater Research, 23
(2003)
Stable carbon and nitrogen isotope signatures indicate recovery of marine biota from sewage pollution at Moa Point
(2006)
Seafood industry training organisation-learning resource for unit standard 16340 v3
D. Duggins (1988)
The Effects of Kelp Forests on Nearshore Environments: Biomass, Detritus, and Altered Flow
P. Morand, M. Merceron (2005)
Macroalgal Population and Sustainability
(2013)
High congruence of isotope
K. Rogers (2003)
Stable carbon and nitrogen isotope signatures indicate recovery of marine biota from sewage pollution at Moa Point, New Zealand.
Marine pollution bulletin, 46 7
J. North, Russell Frew, R. Hale (2006)
Can stable isotopes be used to monitor landfill leachate impact on surface waters
Journal of Geochemical Exploration, 88
R. Connolly, D. Gorman, J. Hindell, T. Kildea, T. Schlacher (2013)
High congruence of isotope sewage signals in multiple marine taxa.
Marine pollution bulletin, 71 1-2
Otago regional council resource consent 97530 condition 8: Rocky Shore Ecological Monitoring
R. Bouman, H. Archer (2014)
Tahuna WWTP, Dunedin, New Zealand: An Innovative Upgrade
, 2014
A. Lorrain, Y. Paulet, L. Chauvaud, N. Savoye, A. Donval, C. Saout (2002)
Differential δ13C and δ15N signatures among scallop tissues: implications for ecology and physiology
Journal of Experimental Marine Biology and Ecology, 275
(2004)
Chemistry of wastewater
(1999)
Temporal and spatial variability of 13 C/ 12 C and 15 N/ 14 N in pelagic biota of Prince William Sound
R. Díaz, D. Rhoads, J. Blake, R. Kropp, K. Keay (2008)
Long-term Trends of Benthic Habitats Related to Reduction in Wastewater Discharge to Boston Harbor
Estuaries and Coasts, 31
A. Gormley, E. Slooten, S. Dawson, R. Barker, W. Rayment, S. Fresne, S. Bräger (2012)
First evidence that marine protected areas can work for marine mammals
Journal of Applied Ecology, 49
(2005)
The effect of habitat loss and degradation on fisheries. The decline of fisheries resources in New England: Evaluating the impact of overfishing, contamination, and habitat degradation (pp. 67–96)
S. Deudero, A. Box, Silvia Tejada, Joaquín Tintoré (2009)
Stable isotopes and metal contamination in caged marine mussel Mytilus galloprovincialis.
Marine pollution bulletin, 58 7
Xiao-E. Yang, Xiangyun Wu, Hu-lin Hao, Zhenjun He (2008)
Mechanisms and assessment of water eutrophication
Journal of Zhejiang University SCIENCE B, 9
D. Baker, S. Macavoy, K. Kim (2007)
Relationship between water quality, δ15N, and aspergillosis of Caribbean sea fan corals
Marine Ecology Progress Series, 343
C. Hepburn, J. Holborow, S. Wing, Russell Frew, C. Hurd (2007)
Exposure to waves enhances the growth rate and nitrogen status of the giant kelp Macrocystis pyrifera
Marine Ecology Progress Series, 339

Publisher: Taylor & Francis
Copyright: © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
ISSN: 2474-9508
DOI: 10.1080/24749508.2018.1485079
Publisher site: See Article on Publisher Site

Abstract

GEOLOGY, ECOLOGY, AND LANDSCAPES 2019, VOL. 3, NO. 1, 53–64 INWASCON https://doi.org/10.1080/24749508.2018.1485079 Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage eﬄuent in coastal waters along Otago Peninsula, New Zealand a b c a Oluwuyi Babaranti , Stephen Horn , Tim Jowett and Russell Frew a b Department of Chemistry, University of Otago, Dunedin, New Zealand; Department of Conservation, Wellington, New Zealand; Department of Mathematics & Statistics, University of Otago, Dunedin, New Zealand ABSTRACT ARTICLE HISTORY Received 30 January 2018 Sewage, waste organic matter from domestic and municipal wastewater, causes increased Accepted 3 June 2018 secondary productivity, eutrophication and trace metal contamination, reduced oxygen levels, and biodiversity which can lead to ecological disturbances in the natural aquatic KEYWORDS ecosystem. The impact of sewage-derived organic matter (SDOM) on the nearshore marine Sewage eﬄuent; ecosystem of the Otago Coast was assessed before, and 15 years after upgrade of the wastewater; isotopic Dunedin sewage treatment plant. Carbon and nitrogen isotopic ratios in the tissues of enrichment factor; organic sentinel organisms were used as bioindicators to elucidate the primary sources of nutrition matter; linear mixed eﬀect modelling; bioindicators the coastal environment. Mytilus galloprovincialis, a marine bivalve, exhibited a strong inﬂu- ence of SDOM from two sites in 2001. In 2015, M. galloprovincialis had a trophic enrichment 15 13 factor of 3‰ (δ N) and 1‰ (δ C) when compared to the marine particulate organic matter (POM), suggestive of a dietary change away from the SDOM. Suspended POM collected from riverine and estuarine sources revealed other possible nitrogen sources from human-driven activities such as pastoral farming, application of organic manure and inorganic fertilisers, nitriﬁcation of ammonium from semi-urban septic tanks, and animal organic waste residues. 1. Introduction Wastewater Plant and Tahanu Wastewater Treatment Plant (TWWTP) serving over 120,000 people in Sewage, a major organic component of domestic and Dunedin, New Zealand, discharge adequately treated municipal wastewater, can cause increased second- wastewater eﬄuent from Waldronville and Lawyers ary productivity (Hillebrand & Sommer, 2000), Head, respectively (see Figure 1), into the Paciﬁc eutrophication (Jarvie, Neal, & Withers, 2006), Ocean from two ocean outfalls pipes that were extended heavy metal contamination (Chary, Kamala, & Raj, from 550 to 1100 m in 2009. Between 2010 and 2013, 2008; Cheevaporn & Menasveta, 2003; Morillo, the wastewater treatment plant facilities were improved Usero, & Gracia, 2004), reduced oxygen levels, and to handle both primary and secondary wastewater treat- biodiversity which can lead to ecological distur- ment processes. The advancement in the wastewater bances (Browne et al., 2011; Diaz, Rhoads, Blake, management involved the construction of a new Kropp, & Keay, 2008) in the natural aquatic ecosys- pump station to the increased ﬂow rate of the waste- tems (Deegan & Buchsbaum, 2005; Hargrave, water treatment plants. This was done to improve the Holmer, & Newcombe, 2008). Thus, it is imperative quality of eﬄuent and shoreline water quality, reduce we ensure that the quality of treated wastewater organic matter content, and ensure public health pro- eﬄuent from municipal treatment plants meets the tection which was a major concern at that time stipulated safe levels approved by the statutory and (Bouman & Archer, 2014). regulatory authorities before discharged into the Before the extension of the ocean outfalls pipes, receiving waterbodies (Ellis, 2004; Teklehaimanot, discharged wastewater eﬄuent contaminated parts of Coetzee, & Momba, 2014). the Otago coastal marine area which has more than Inadequately treated eﬄuent discharged into the 80 protected wildlife areas which accommodated marine area poses environmental and health hazards marine mammals and birds along its landward edge to the resident biota in the adjacent nearshore waters. (Council, 2001; Gormley et al., 2012; Rayment, Between 1908 and 1950s, raw sewage was discharged Dawson, & Slooten, 2010). The various bacteriologi- directly into the Paciﬁc Ocean at Lawyers Head cal studies (measurement of Escherichia coli con- (Council, 2001) by the Dunedin Water Pollution ducted on shellﬁsh, sediments, and seawater) had Control Plant (now called Tahuna Wastewater ascribed the contamination of the portions of Otago Treatment Plant). Presently, the Green Island coastline to the wastewater eﬄuent discharge from CONTACT Oluwuyi Babaranti olua_babs@yahoo.com Department of Chemistry, University of Otago, Dunedin, New Zealand © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 54 O. BABARANTI ET AL. various beaches along the Otago Peninsula to trace the pattern and distribution of sewage eﬄuent dis- charged from Lawyers Head. He observed that the nitrogen isotopic ratios of the digestive tissues of the end member mussels vary considerably. He reported that major sewage contamination occurred at Lawyers Head and Tomahawk while there was minor contamination at St. Kilda and Smaills. He found out that more than 60% of the mussels and seaweeds sampled at Lawyers Head and Tomahawk Beach had their isotopic ratios wedged by discharged sewage eﬄuent. Isotopic study carried out by North, Frew, and Hale (2006) on the possibility of landﬁll leachates as source of contamination from solid waste Figure 1. Schematic representation study sites along Otago disposal site which involved the collection and ana- Peninsula with adjoining tidal channels, creeks, and waste- lyses of surface water samples from Kaikorai wetland water outfalls. areas made up of stream and estuary waters from Green Island Landﬁll over an 8-month period revealed that landﬁll leachates could also be possible the TWWTP (Lewis, Loutit, & Austin, 2010; source of contamination to the Kaikorai downstream Nicholson, Lewis, & Loutit, 1989; RCL, 2000). One (North et al., 2006; North, Frew, & Peake, 2004) of such studies reported that over 50% of shellﬁsh which eventually has a run-oﬀ into the Otago coast- collected from the sites close to the sewage outfalls at line at Waldronville. Consequently, there is the pro- Lawyers Head had elevated level of faecal coliforms spect of using stable isotopic ratios in the tissues of and enteric viruses of >230 and <4600/100 g ﬂesh, organisms to assess the impact SDOM and other well above the European Union Class A standard for terrigenous materials on the nearshore marine eco- shellﬁsh ﬂesh. Five downstream sites closest to the system because stable isotopic signatures in the tis- sewage outfall were found to be heavily contaminated sues of organisms had been found to be connected by faecal coliforms and enteric viruses while two with an organism diet over time and space (Bump upstream sites were considered uncontaminated et al., 2007; Rogers, 2003). Stable isotopic analyses on (Greening, Lewis, & Dollimore, 2007). However, the tissues of marine ﬂora and fauna have been these studies were only spot tests (Doré, extensively exploited to assess the impact of SDOM Henshilwood, & Lees, 2000; Ebner, McAllister, & on the food web structure of nearshore marine eco- Suter, 2009) and appropriate for assessing water qual- systems as well as to investigate the recovery of mar- ity standards (Abbasi & Abbasi, 2011; Dede, Telci, & ine ﬂora and fauna at sites disrupted by sewage Aral, 2013). They failed to account for other possible eﬄuent discharges (Barr, Dudley, Rogers, & sources of contamination and provide no estimate of Cornelisen, 2013; Michener & Kaufman, 2008; the amount of sewage-derived organic matter Savage, 2005). SDOM had been known to signiﬁ- (SDOM) in the nearshore marine ﬂora and fauna. cantly alter the stable carbon and nitrogen isotopic Horn (2001) conducted an isotopic monitoring 13 15 signatures (expressed as the δ C and δ N) of marine study on seawater samples, and the tissues of ﬂora (i.e., macro-algae) and fauna (e.g., ﬁlter-feeders) Mytilus galloprovincialis and Ulva lactuca across Figure 2. Comparison of carbon and nitrogen-stable isotopic ratios in the digestive tissues of Mytilus galloprovincialis and particulate materials collected in 2001 along the Otago coastline, New Zealand. GEOLOGY, ECOLOGY, AND LANDSCAPES 55 (Bedard-Haughn, Van Groenigen, & Van Kessel, rates and isotopic enrichment in organisms are tis- 2003; Dudley & Shima, 2010) permitting them to sue speciﬁcand inﬂuenced by lipid content of the exhibit distinct isotopic signatures in their tissues as tissue (Lorrain et al., 2002;Thompson,Phillips, areﬂection of the integration, assimilation, and utili- Stewart, & Waldron, 2000). Thus, a preliminary sation of the SDOM in their immediate environment stable isotopic study to investigate the variance in over time. The carbon and nitrogen isotopic signa- isotopic ratios of carbon and nitrogen in the diﬀer- tures are the comparisons of ratios of the heavy-to- ent tissues of M. galloprovincialis was carried out to light isotope of the element. They are mathematically determine the appropriate tissues to be used for this expressed (see Equation 1) in δ notation in terms of study. The results obtained were compared with parts per thousand (‰)or “per mil” and calculated as other isotopic studies using power analysis for deter- follows: mining sample size. This was done to control the number of samples to be collected to avoid unne- n sample cessary sacriﬁce of biological samples to be used and δ X¼ 1 (1) (Coplen, 2011) standard ensure the reliability of our results. The abductor tissue was noted to have the highest isotopic carbon where n is the atomic mass of the heavy element, X and nitrogen turnover whereas the digestive tissue can either be C or N whereas R is the isotopic ratios has the lowest isotopic tissue turnover. This obser- 13 15 of X (l3C/12C or 15N/14N). The δ C and δ N are vation was in accordance with other workers measured relative to international reference standards (Deudero,Box,Tejada, &Tintoré, 2009;Gaston& of Vienna PeeDee Belemnite and Atmospheric Suthers, 2004). The abductor and digestive tissues of Nitrogen, respectively. Consumer organisms have thebluemusselwerechosenasthe appropriate been known to exhibit isotopic signatures which can indicators forassessing theimpactofSDOMon either be similar or vary from their diets with an the nearshore marine fauna in the nearshore marine average fractionation trophic enrichment of 0.4–1‰ waters. To the best of our knowledge, no stable 13 15 for δ C 1987 and 3–4‰ for δ N (Kline & Thomas, isotopic studies to assess the impact of the modiﬁca- 1999; Post, 2002). tions in the sewage treatment and disposal on the In assessing the impact of SDOM in a nearshore nearshore marine waters and resident biota along marine ecosystem, the disparities in the carbon and the Otago Peninsula had been carried out. Hence, nitrogen isotopic ratios in the tissues of end members our study is attempted to exploit the isotopic ratios can become useful monitoring tools for providing of sentinel organisms at these sites so as to ﬁnd out more information on the source and magnitude of the current status of organic materials in the tissues sewage contribution to the diet of resident biota of M. galloprovincialis and Ulva latuca of the near- (Peterson, 1999). Hence for the purpose of this shore marine waters. This present study will address study, stable isotopic ratios in the tissues of M. gallo- the following research questions: provincialis (marine bivalve) and U. lactuca (sea let- tuce) were speciﬁcally chosen as indicators to be used. 13 15 (1) Are the variabilities in the δ C and δ Nin Mussels are sedentary and long-lived (Alfaro, Jeﬀs, & the tissues of M. galloprovincialis and U. lac- Hooker, 2001; Nordsieck, 2006; SITO, 2006) charac- tuca reliable indicators of assessing sewage teristic features which make them suitable sentinel contamination in the nearshore marine waters organisms as time-averaged integrators of sewage along the Otago Peninsula? exposure for the sea lettuces which are short lived (2) Has the improvement in the sewage treatment by nature (Cabana & Rasmussen, 1996; Dudley & processes and disposal at the TWWTP brought Shima, 2010; Post, 2002). signiﬁcant changes in the carbon and nitrogen Furthermore, ﬁlter feeders such as bivalves (i.e., isotopic signatures of M. galloprovincialis and mussels) can directly ingest (via the gills) and assim- U. lactuca collected from the nearshore marine ilate sewage particulate organic matter (POM) (con- ecosystem along the Otago Peninsula? taining carbon and nitrogen) along with their diet (3) Are there other possible terrestrial-based organic (phytoplankton and detritus) from the water column materials contributing carbon and nitrogenous into the tissues and reassigned such higher up the materials to the nearshore waters which may food chain (biomagniﬁcation) (Ouédraogo, Chételat, sway the carbon and nitrogen isotopic ratios of &Amyot, 2015;Pan &Wen-Xiong, 2004). In choos- M. galloprovincialis and U. lactuca? ing the most appropriate tissues for the stable iso- (4) How much of terrestrial-based organic δ C topic study, consideration was given to the previous carbon and δ N nitrogenous materials are studies conducted by other workers on carbon and integrated into the tissues (i.e., digestive) of nitrogen isotopic turnover and enrichment in the M. galloprovincialis collected from the near- diﬀerent tissues of organisms. Most of the studies shore marine waters along the Otago showed that carbon and nitrogen isotopic turnover Peninsula? 56 O. BABARANTI ET AL. To answer these questions, the linear mixed eﬀects uniform sizes to avoid sampling bias which might model analysis, an extension of regression analysis, ensue from in-site and site–site isotopic variability. was used to compare the stable carbon and nitrogen The study sites cover about 48 km within the Otago 13 15 isotopic ratios (δ C and δ N) in the tissues of M. Marine Area. Water samples were collected from the galloprovincialis and U. lactuca collected in 2001 three tidal channels having a free connection to the (before upgrade of the sewage treatment plant) and nearshore marine waters (Figure 1). At each of the 2015/16 (after upgrade of the sewage treatment plant) sampling sites, the date and time of sampling, pre- in the end members so as to determine if there had vailing weather conditions, swell, wind direction, as 13 15 been changes in the isotopic signatures δ C and δ N well as possible visible sources of contamination, in the tissues of M. galloprovincialis and U. lactuca were noted and recorded. The location of each of collected from the study sites classiﬁed into control the sampling sites was noted and recorded with the sites (uncontaminated sites) and previously sewage- aid of a handheld GPS tracking device and illu- contaminated sites comprising eight beaches and strated in Table 1. three tidal channels. The groupings of these sites were based on proximity to the sewage outfall, the 2.2. Sample preparation and analysis written reports of the 2000 ORC Resource Consent 97530 97530 (RCL, 2000) and 2007 FRST Programme M. galloprovincialis and U. latuca were individually C03X0301 (Greening et al., 2007). The nature of placed into clean ziplock plastic bags labelled with possible sources of carbon and nitrogen into the date and sample site location. They were immedi- nearshore marine waters was identiﬁed and discerned ately placed in a plastic cooler for onward trans- from the distinctive isotopic ratios of the POM col- port to the laboratory where they were rinsed in lected from the tidal channels feeding the coastal distilled water and frozen prior to analysis. M. marine waters. A mass balance linear mixing model galloprovincialis was dissected into diﬀerent tissues equation was used in estimating the source contribu- (the abductor and digestive tissues of interest in tions of carbon and nitrogen materials in the tissue of this study). The dissected tissues and samples of U. marine biota collected from the study sites along latuca were dried at 70°C for 24 h. Once dry Otago Peninsula. The two main sources considered samples were homogenised with the aid of an were marine POM and sewage eﬄuent POM. This MM400 bench-top Retsch ball mill, duplicate ali- was done to quantify the contribution of sewage quots of 0.8 mg of homogenised tissues of the material in the marine biota. The ﬁndings from this biological samples were weighed into separate study will show the potential of deploying multistable 5 × 3.5 mm tin cups and further dried under isotopic techniques and ﬁtting mixing model to be vacuum overnight. Water samples collected from used as a tool to elucidate the ﬂow and fate of various the eight beaches and three tidal channels were sources of organic materials in the nearshore marine ﬁltered through 25 mm GF/F grade to collect sus- waters. This will enhance better understanding of the pended POM. Sewage eﬄuent and seal faecal mat- impact of anthropogenic organic carbon and nitro- ter were collected from source and processed for genous materials on the nearshore marine waters and isotopic analysis. The samples with internal and its consequences on the functioning of the coastal certiﬁed pre-calibrated standards and blanks were marine ecosystem. Insights into the inﬂuence of placed in an autosampler carousel and combusted human-induced stressors on the dynamics of organic using the Carlo Erba NA1500. The elemental ana- materials in the nearshore marine ecosystem will lysis–isotope ratio mass spectrometry operates in a ensure proper management, conservation, and pre- continuous ﬂow mode for the determination of the servation of the coastal marine aquaculture resources carbon and nitrogen isotope ratios (δ Cand through comprehensive ecosystem-based manage- δ N). Nitrogen and carbon isotopes were assayed ment with a focus on proper land-use management. by combustion of the samples in the chromium Table 1. Sampling site with assigned code, name, and 2. Material and methods coordinates. Site Latitude Longitude 2.1. Sampling sites Allans 45.857 170.679 BlackHead 40.168 176.827 M. galloprovincialis and U. lactuca were collected Brighton 45.948 170.335 from the eight beaches along the Otago coastline at St. Clair 45.910 170.501 St. Kilda 45.908 170.517 low tide before the upgrade of the treatment plants Sandﬂy Bay 40.925 173.055 from 4/05/01 to 10/08/01 (weekly) and after the Smaills 46.019 169.089 Tomahawk 45.907 170.540 upgrade from 9/12/15 to 13/4/2016 (weekly). Tomahawk Creek 46.019 169.089 Sampleswerecollected fromtherocks in theinter- Atakore Creek 46.109 170.177 tidal zone. The marine bivalves were of average Taeiri Mouth 46.051 170.190 GEOLOGY, ECOLOGY, AND LANDSCAPES 57 oxide combustion column of the elemental analyser sample (IANZ, 2004) and random inclusion of two to produce N and CO , using helium carrier gas. in-house standards (green mussel and copepod) to 2 2 These gases were resolved in a packed molecular mimic the nature of the sample materials being sieve GC column and sent sequentially to the inlet analysed. of Europa Scientiﬁccontinuous ﬂow mode “20/20 Hydra” (Europa Scientiﬁc, UK) isotope ratio mass spectrometer (CF-IRMS) interfaced to the Sercon 2.3. Statistical analysis System Controller which runs on Sercon Callisto The carbon and nitrogen isotopic signature values Software. During the programmed run tests, the obtained in the tissues of M. galloprovincialis and samples were combusted at 1050°C, and U. lactuca were subjected to statistical evaluation NO reduced to N at 650°C within the elemental 2 2 via linear mixed-eﬀect models. The average values analyser using its normal reaction scheme. Raw of carbon and nitrogen isotopic ratios with stan- isotopic ratios obtained were normalised by three- dard errors are represented in Table 2.Using the point calibration to the international scales using R Statistical Software via the linear mixed-eﬀects 4 two International Atomic Energy Agency reference (lme4) (Bates, 2010), separate built-in linear materials (USGS-40 and USGS-41) and internal mixed-eﬀect models (see Equation 2) were ﬁtted laboratory standard (ethylenediaminetetra-acetic for the carbon and nitrogen isotopic signature acid [EDTA-OAS], δ C= − 38.92‰ ± 0.04; values in the tissues of M. galloprovincialis and δ N= −0.70‰ ± 0.17) of known carbon and U. lactuca in order to perform a likelihood of nitrogen isotopic signatures, assayed with the ratio testing of interactions among the random unknown samples. Owing to the large number of and ﬁxed eﬀects. The random eﬀects were the samples, a linearity correction method was applied various sites while primary factors of interest to ensure that the isotopic values obtained were not such as contamination, tissue type, and year were aﬀected by instrumental drift. Accuracy and preci- the ﬁxed eﬀects. The built-in ﬁtted model used for sion of the obtained isotopic results were assessed the linear mixed-eﬀect modelling analysis (LMM) by employing the root mean square RMS diﬀer- is expressed as follows: ences between sequential duplicates of every 10th Table 2. Mean isotopic carbon and nitrogen signatures (with their respective standard errors) in the tissues of Mytilus galloprovincialis and Ulva latuca collected from the uncontaminated and previously contaminated sites along Otago coastline, New Zealand in 2001 and 2015. 2001 2015 15 13 15 13 Site δ N (‰)±SE δ C (‰)± SE δ N (‰)±SE δ C (‰)±SE AIR VPDB AIR VPDB Uncontaminated sites (Mytilus galloprovincialis) Abductor Allans 8.78 ± 0.25 −18.00 ± 0.29 9.02 ± 0.13 −18.08 ± 0.40 BlackHead 7.73 ± 0.03 −20.42 ± 0.19 8.65 ± 0.29 −18.89 ± 0.30 Brighton 11.21 ± 0.56 −17.91 ± 0.23 9.26 ± 0.27 −18.48 ± 0.15 Sandﬂy Bay 10.19 ± 0.10 −20.82 ± 0.91 9.79 ± 0.09 −19.20 ± 0.04 Digestive Allans 7.20 ± 0.17 −20.49 ± 0.10 8.91 ± 0.18 −20.08 ± 0.09 BlackHead 7.65 ± 0.31 −20.36 ± 0.17 7.86 ± 0.19 −19.98 ± 0.04 Brighton 10.54 ± 0.98 −20.77 ± 0.21 8.02 ± 0.34 −19.16 ± 0.07 Sandﬂy Bay 7.06 ± 0.25 −20.62 ± 0.11 8.24 ± 0.13 −21.23 ± 0.02 Previously contaminated sites (Mytilus galloprovincialis) Abductor St. Clair 10.04 ± 0.18 −18.08 ± 0.17 9.72 ± 0.09 −17.86 ± 0.04 St. Kilda 8.64 ± 0.11 −17.33 ± 0.41 9.76 ± 0.17 −17.80 ± 0.20 Smaills 9.34 ± 0.13 −18.29 ± 0.32 8.95 ± 0.15 −19.53 ± 0.26 Tomahawk 7.33 ± 0.08 −18. 49 ± 0.50 9.68 ± 0.28 −18.72 ± 0.03 Digestive St. Clair 7.08 ± 0.27 −20.81 ± 0.30 8.45 ± 0.07 −19.14 ± 0.14 St. Kilda 6.34 ± 0.22 −17.19 ± 0.24 8.68 ± 025 −19.33 ± 0.03 Smaills 7.20 ± 0.24 −20.65 ± 0.47 8.07 ± 0.15 −20.35 ± 0.07 Tomahawk 4.83 ± 0.31 −22.81 ± 0.44 8.84 ± 0.22 −20.08 ± 0.09 Uncontaminated site (Ulva latuca) Allans 9.12 ± 0.38 −10.41 ± 0.36 9.02 ± 0.11 −18.08 ± 0.01 BlackHead 8.05 ± 0.05 −16.63 ± 0.10 8.39 ± 0.00 −20.08 ± 0.06 Brighton 7.54 ± 0.05 −16.42 ± 0.19 8.55 ± 0.22 −19.67 ± 0.03 Sandﬂy Bay 9.18 ± 0.10 −14.63 ± 0.34 9.37 ± 0.02 −16.75 ± 0.08 Previously contaminated sites (Ulva latuca) St. Clair 6.88 ± 0.06 −14.47 ± 0.72 8.81 ± 0.29 −20.39 ± 0.03 St. Kilda 5.34 ± 0.67 −16.29 ± 0.30 9.10 ± 0.08 −21.63 ± 0.04 Smaills 10.46 ± 0.15 −12.38 ± 0.15 9.10 ± 0.16 −21.63 ± 0.01 Tomahawk −3.07 ± 0.45 −15.74 ± 0.25 8.52 ± 0.01 −19.51 ± 0.03 58 O. BABARANTI ET AL. Table 3. Noticeable diﬀerences (disparity values) between the y ¼ β þ β x þ β x þ β x þ β x x þ β x x i 1i 2i 3i 1i 2i 1i 3i 0 1 2 3 4 5 mean carbon and nitrogen isotopic ratios in Mytilus gallopro- þ β x x þ α þ ε 2i 3i jiðÞ i vincialis and Ulva latuca collected in 2001 (before the (2) upgrade of TWWTP) and 2015 (after the upgrade of TWWTP) from the nearshore marine waters along Otago where Peninsula. y is the outcome for the ith experimental unit i Mytilus galloprovincialis Ulva latuca (sample) from site j, Abductor Digestive Seaweed β is the coeﬃcient for the intercept, 15 13 15 13 15 13 δ N δ C δ N δ C δ N δ C β is the coeﬃcient for the contamination eﬀect, Site (‰)(‰)(‰)(‰)(‰)(‰) β is the coeﬃcient for the year eﬀect, Uncontaminated β is the coeﬃcient for the tissue eﬀect, Allans +0.24 −0.08 +1.71 +0.41 −0.10 −7.67 BlackHead +0.92 +1.53 +0.21 +0.38 +0.34 −3.45 β is the coeﬃcient for the interaction between Brighton −1.95 −0.57 −2.52 +1.61 +1.01 −3.25 contamination and year eﬀects, Sandﬂy Bay −0.40 +1.62 +1.18 −0.61 +0.19 −2.12 Previously contaminated β is the coeﬃcient for the interaction between St. Clair −0.32 +0.22 +1.37 −1.06 +1.93 −5.92 contamination and tissue eﬀects, St. Kilda +1.12 −0.47 +2.34 −2.00 +3.76 −5.34 Smaills −0.39 −1.24 +0.87 −2.06 −1.36 −9.25 β is the coeﬃcient for the interaction between Tomahawk +2.35 −0.23 +4.01 −1.59 +11.59 −3.77 year and tissue eﬀects, α is the random eﬀect for the ith was obtained, jiðÞ where α Normalð0;σ ), jiðÞ Clair where it was 0.22‰ larger than noted in 2001. ε is the residual error term for the ith unit, where In the digestive tissues, the recorded disparity values α Normalð0;σ ), and jiðÞ 15 in the means δ N values in 2015 ranged between x , x , and x are indicator variables for the 1i 2i 3i 1.37‰ and 4.01‰ larger across all the previously contamination, year, and tissue eﬀects, respectively, contaminated sites. The recorded disparity values for the ith experimental unit where a value of 0 for the means of δ C varied between 1.06‰ and indicates the absence of a factor, and 1 indicates the 2.06‰ lesser across all the previously contaminated presence. sites (Table 3). In the tissues of U. latuca, the recorded disparity values for δ N means varied between 1.93‰ and 11.59‰ larger across three sites 3. Results and 1.36‰ lesser at Smaills than observed in 2001. 3.1. Variations in the carbon and nitrogen Contrasts between the end member’s nitrogen and isotopic ratios in M. galloprovincialis and U. carbon isotopic ratios recorded in the abductor and latuca digestive tissues of the mussels sampled in 2015 revealed that the weighted mean δ N values diﬀered The mean carbon and nitrogen isotopic ratios in M. from 0.11‰ to 1.55‰ larger in the abductor tissues galloprovincialis and U. latuca sampled in 2001 and than in the digestive tissues whereas the mean δ C 2015 are illustrated in Table 2. The disparity values of values varied from 0.68‰ to 2.03‰ larger at the the mean carbon and nitrogen isotopic ratios in M. uncontaminated sites. At the previously contami- galloprovincialis and U. latuca collected in 2001 and nated sites, weighted mean δ N values ﬂuctuated 2015 along Otago Peninsula are represented in between 0.84‰ and 1.27‰ larger in the abductor Table 3. At the uncontaminated sites, the mean tissue than digestive tissue while the weighted mean δ N values recorded in the abductor tissues of M. δ C values varied between 0.82‰ and 1.82‰ larger. galloprovincialis diﬀered between 0.21‰ and 1.71‰ larger at BlackHead and Allans correspondingly whereas disparity values ranged between 2.52‰ and 3.2. POM in samples 0.40‰ lower at Brighton and Sandﬂy Bay accordingly than previously noted in 2001. The noticeable diﬀer- The mean δ N values for POM from ﬁltered water ences for the means of δ C ﬂuctuated from 0.38‰ to samples ranged from 5.70 ± 0.20‰ to 10.06 ± 0.05‰ 1.61‰ larger at BlackHead and the Brighton accord- recorded at Akatore and Tomahawk Creek, respec- 15 13 ingly. The mean δ N values recorded in the abductor tively. The mean δ C values for the POM ranged tissues of M. galloprovincialis had disparity values from −27.18 ± 0.01‰ to −21.57 ± 0.61‰ documen- ﬂuctuated between 1.12‰ and 2.35‰ larger at St. ted at Tomahawk Creek and Akatore correspondingly Kilda and Tomahawk correspondingly whereas dis- (Table 3). The isotopic signatures of POM from these parity values varied between 0.32‰ and 0.39‰ lower varying aquatic systems indicated the probable at St. Clair and Smaills accordingly than previously sources and type of anthropogenic materials been noted in 2001. The disparity values for the means of transported into them for onward transport to the δ C ﬂuctuated from 0.23‰ to 1.24‰ lower across coastal marine waters. The reported higher mean the three previously contaminated sites except at St. carbon isotopic (δ C) and lower nitrogen isotopic GEOLOGY, ECOLOGY, AND LANDSCAPES 59 (δ N) values of Akatore Creek and Taieri Mouth Clair Beach also indicated inﬂuence by sewage eﬄu- indicated marine-based organic matter while that of ent. In 2015, M. galloprovincialis collected and ana- Tomahawk Creek seemed terrestrial due to the higher lysed showed no sign of sewage eﬄuent 15 13 δ N and lower δ C isotopic ratios. contamination. The contrast between the carbon and nitrogen isotopic ratios in the digestive tissues of the mussels from all sites evidently seemed clus- 3.3. Sewage, marine, and terrigenous particulate tered close to one another (Figure 3) in 2015 a direct matter in M. galloprovincialis contrast to 2001 observations (Figure 2). This may be attributed to these mussels feeding on a single major The nitrogen and carbon isotopic signatures analyses food source. It was observed that the mussels tend to on digestive tissues of M. galloprovincialis collected in obtain nutrition from the marine POM as most of the 2001 before the upgrade of the sewage treatment mussels sampled at the previously contaminated and plant revealed that 90% of M. galloprovincialis col- uncontaminated sites assumed trophic shift (enrich- lected from Tomahawk were heavily isotopically 15 13 ment factor) of roughly 3‰ for δ N and 1‰ for the depleted in δ N and δ C with 60% of nitrogen and δ C cf. to the marine POM. The marine bivalve 40% of carbon in the digestive tissue derived from might also be deriving sustenance from other terres- sewage particulate matter while between 30% and trial organic materials incursions to the nearshore 60% of mussels from St. Kilda, Smaills, and St. Clair waters. The contrasts of carbon and nitrogen ratios showed signs of mild sewage contamination. This is in the tissues of U. latuca in the 2015 sampling were indicative that eﬄuent seemed to provide a source of unpredictable as opposed to the trend observed in sustenance for the ingested phytoplankton biomass or 2001. Of particular note are the results from at direct ingestion of sewage POM by M. galloprovincia- Tomahawk and St. Clair when 2001 nutrient enrich- lis appraised at the previously contaminated sites so ment was predominantly SDOM (Figure 4) whereas much to sway the marine bivalve isotopic ratios all sites exhibit the marine source predominantly in greatly. U. latuca collected in 2001 from Tomahawk 15 2015 (Figure 5). In 2015, no detectable sewage eﬄu- has negative mean δ N, an indication of sewage ent inﬂuence was observed, rather the isotopic values eﬄuent alteration, and 40% of U. latuca sampled St. Figure 3. Comparison of carbon and nitrogen-stable isotopic ratios in the digestive tissues of Mytilus galloprovincialis and particulate materials collected in 2015 along the Otago coastline, New Zealand. Figure 4. Comparison of carbon and nitrogen-stable isotopic ratios in the tissues of Ulva lactuca and particulate materials collected in 2001 along the Otago coastline, New Zealand. 60 O. BABARANTI ET AL. Figure 5. Comparison of carbon and nitrogen-stable isotopic ratios in the tissues of Ulva lactuca and particulate materials collected in 2015 along the Otago coastline, New Zealand. plotted towards the seal faecal matter were at Allans assumption, the obtained δ N – percentage contri- and Sandﬂy Bay and terrigenous-based sources at all bution of the marine to terrestrial contribution in the other sites sampled (Figures 4 and 5). The outline of digestive tissues of the mussels collected from each of the isotopic ratios of analysis on tissues of U. latuca the previously contaminated sites – was as follows: St. seemed to assume orientation towards enrichment Clair (37%:63%), St. Kilda (49%:51%), Smaills from characterised ﬁltered water samples (POM) a (87%:13%), and Tomahawk (52%:48%). The δ C – pointer to possible nutrient enrichment from terres- percentage contribution was principally from marine trial sources. particulate matter for most of the sites. Smaills and Tomahawk had 4% and 1% of δ C terrestrial parti- culate matter contribution accordingly. No inﬂuence 3.4. Linear isotopic mixing model of terrestrial particulate matter was detected at St. Kilda and St. Clair could not be estimated. We tried Estimating the relative contributions of carbon and to estimate the contribution of the sewage eﬄuent in nitrogen organic materials from terrestrial sources in the digestive tissue of M. galloprovincialis we the digestive tissues of M. galloprovincialis sampled in 13 15 obtained negative values for both δ C and δ N. 2015 so as to quantify the magnitude of suspended POM (i.e., terrigenous materials) in the biological samples, a simple modiﬁed two-end member linear 3.5. Analysis of variance between carbon and isotopic mixing model (Waldron, Tatner, Jack, & nitrogen isotopic signatures in M. Arnott, 2001) as expressed in Equations 3 and 4 galloprovincialis and U. lactuca below was used: The mean carbon and nitrogen isotopic ratio values 15 15 15 δ N ¼ δ N X þ Y δ N (3) in the tissues of M. galloprovincialis and U. lactuca mussel POM control for 2001 and 2015 were subjected to statistical analy- 13 13 13 sis using the LMM to determine if there were signiﬁ- δ C ¼ δ C XþY δ C (4) mussel POM control cant interactions between the carbon and nitrogen X is the contribution from marine/phytoplankton isotopic ratios reported in 2001 and 2015 within source and Y =(1 − X) which is the terrigenous and across the study sites. The LMM determined materials (multiplied by 100). the ratio testing values for the crisscross in the varia- Using the observed mean isotopic ratios of the bility of carbon and nitrogen isotopic ratios recorded POM from ﬁltered water samples collected from in M. galloprovincialis and U. lactuca across the end Tomahawk Creek (δ N = 10.06‰ and member sites (uncontaminated and previously con- δ C= − 27.18‰) as the terrestrial source and taminated). The outcomes of the interactions are mean isotopic ratios of mussels collected from represented in Table 4. Highly signiﬁcant diﬀerences BlackHead (uncontaminated site) (i.e., (p = < 0.0001, n = 169 [abductor]; p = 0.0022, n = 169 15 13 δ N = 7.86‰ and δ C= − 19.98‰) as the control [digestive]) were recorded between 2001 and 2015 15 13 end member while δ N and δ C were for nitrogen isotopic ratios in the digestive tissues of M. mussel mussel the carbon and nitrogen isotopic ratios of mussels galloprovincialis and tissues of U. lactuca sampled from the previously sewage contaminated (p = < 0.0001, n = 30) collected at the previously sites. We assumed a two-source nutrient-enrichment contaminated sites. There were no signiﬁcant diﬀer- isotopic mixing model for the mussels coming from ences in the 2015 nitrogen isotopic ratios in the marine and terrigenous sources. Based on this digestive and abductor tissues of M. galloprovincialis GEOLOGY, ECOLOGY, AND LANDSCAPES 61 Table 4. Mean with standard error values of nitrogen and carbon isotopic signatures values from the particulate organic matter in ﬁltered water, sewage eﬄuent, and seal faeces samples collected from the coastal marine waters along Otago coastline in 2001(bracket) and 2015. 15 13 Site δ N (‰)±SE δ C (‰)± SE AIR PVB Atakore creek 5.70 ± 0.20 (5.80 ± 1.70) −21.57 ± 0.61(−17.30 ± 2.10) Teaeiri Mouth 5.80 ± 0.16 (5.40 ± 2.60) −24.03 ± 0.73 (24.30 ± 1.50) Tomahawk Creek 10.06 ± 0.06 (8.70 ± 0.50) −27.18 ± 0.01 (−27.00 ± 0.30) Eﬄuent POM 3.10 ± 0.50 −25.80 ± 0.10 Seal faeces POM 14.20 ± 0.60 −21.90 ± 0.30 (p = 0.3831, n = 8 [abductor]; p = 0.8587, n =8 δ N than the other sites suggestive of uptake of [digestive]). No signiﬁcant diﬀerences were observed the sewage eﬄuent. Sewage eﬄuent and other in the 2015 carbon isotopic ratios in the digestive and anthropogenic inputs had been known to modify abductor tissues of M. galloprovincialis (p = 0.2476, the carbon and nitrogen isotopic ratios of macro- n = 6 [abductor]; p = 0.8357, n = 6 [digestive]). No algae (Fry, 2002; Fry, Gace, & McClelland, 2003; signiﬁcant diﬀerences were observed in δ N Gartner, Lavery, & Smit, 2002; Rogers, 2003; (p = 0.8469, n = 6) and δ C(p = 0.0022, n =6)in Savage, 2005; Savage & Elmgren, 2004) and respon- the tissues of U. lactuca sampled at the uncontami- siblefor excessivegrowthofmicroalgaeinnear- nated and previously contaminated sites in 2015 shore marine waters (Baker, MacAvoy, & Kim, (Table 5). 2007; Connolly, Gorman, Hindell, Kildea, & Schlacher, 2013; Morand & Merceron, 2005; Yang, Wu,Hao,&He, 2008). 4. Discussion In 2015, the tissues of U. latuca sampled at Tomahawk and St. Kilda were found to be N ele- At thetimeofthe ﬁrst sampling event (Horn, vated by 11.59‰ and 3.76‰, respectively, than 2001), two of the study sites (Smaills and recorded in 2001 indicating a remarkable recovery Tomahawk Beaches) were known to be contami- from sewage inﬂuence. There was good agreement nated with sewage-derived matter and exhibited between the 2001 and 2015 mean δ N values in the high faecal coliform counts (Greening et al., 2007; tissues of U. latuca between the recorded values at the Lewis et al., 2010). In 2001, the carbon and nitro- uncontaminated sites (i.e., reference sites) which var- genisotopicratiosinthe tissuesof M. galloprovin- ied between 8‰ and 9‰ (p = 0.112, n = 30) sugges- cialis and U. latuca indicated that two sites (i.e., tive of absence of sewage organic matter as nutrient Tomahawk and Smaills) were heavily impacted by source. However, the recorded δ C mean values the discharged sewage eﬄuent demonstrated in the 13 15 between 2001 and 2015 in the tissues of U. latuca lower δ C and δ Nvalues. Thetissues of U. were a departure from the observed trend in δ Nat latuca sampled at Tomahawk (closest site to the the reference sites varying from −20‰ to −10‰ outfall) and St. Kilda were found to have lower Table 5. Linear mixed-eﬀects model (LMM) analysis result of the stable carbon and nitrogen isotopic signatures in the tissues of Mytilus galloprovincialis and Ulva latuca collected in 2001 and 2015 from the various study sites along Otago coastline. Site contrast Year Variable Tissue df (n − 1) t Ratio p-Value* Previously contaminated 2001–2015 δ N Abductor 169 −3.61 0.0022 Uncontaminated 2001–2015 δ N Abductor 169 1.71 0.3202 Previously contaminated 2001–2015 δ N Digestive 169 −9.26 <0.0001 Uncontaminated 2001–2015 δ N Digestive 169 −3.75 0.0014 Previously contaminated 2001–2015 δ N Seaweed 30 −8.09 <0.0001 Uncontaminated 2001–2015 δ N Seaweed 30 1.65 0.1102 Previously contaminated 2001–2015 δ C Abductor 177 0.52 0.9546 Uncontaminated 2001–2015 δ C Abductor 177 0.79 0.8595 Previously contaminated 2001–2015 δ C Digestive 177 −6.84 <0.0001 Uncontaminated 2001–2015 δ C Digestive 177 −4.98 <0.0001 Previously contaminated 2001–2015 δ C Seaweed 30 15.69 <0.0001 Uncontaminated 2001–2015 δ C Seaweed 30 34.19 <0.0001 Uncontaminated–previously contaminated 2001 δ N Abductor 6 1.35 0.0170 Uncontaminated–previously contaminated 2001 δ N Digestive 6 2.50 0.0401 Uncontaminated–previously contaminated 2001 δ C Abductor 6 −0.89 0.4067 Uncontaminated–previously contaminated 2001 δ C Digestive 6 1.70 0.1404 Uncontaminated–previously contaminated 2001 δ N Seaweed 6 3.59 0.0115 Uncontaminated–previously contaminated 2001 δ C Seaweed 6 0.43 0.6838 Uncontaminated–previously contaminated 2015 δ N Abductor 8 −0.92 0.3831 Uncontaminated–previously contaminated 2015 δ N Digestive 8 0.18 0.8587 Uncontaminated–previously contaminated 2015 δ C Abductor 6 −1.28 0.2476 Uncontaminated–previously contaminated 2015 δ C Digestive 6 0.22 0.8357 Uncontaminated–previously contaminated 2015 δ N Seaweed 6 0.20 0.8469 Uncontaminated–previously contaminated 2015 δ C Seaweed 6 0.68 0.5235 (*The level of signiﬁcance was set at 5%. Values of p < 0.05 were considered signiﬁcant, p < 0.01 and p < 0.001.) 62 O. BABARANTI ET AL. (p < 0.0001, n = 30). This abnormality in the variance 5. Conclusion of δ C might be attributed to the discrepancies in Carbon and nitrogen isotopic ratios in the tissues C discrimination during photosynthesis and of M. galloprovincialis and U. lactuca were found respiration by the seaweeds rather than nutrient to be suitable bioindicators for investigating the enhancement. impact of SDOM and possible terrigenous materi- The modiﬁcations in the treatment and disposal als on the nearshore marine waters. M. gallopro- of sewage eﬄuent have had a profound positive vincialis and U. lactuca were inﬂuenced by sewage eﬀect on the environmental conditions at the pre- at the two previously contaminated beaches in viously contaminated sites. The extension of the 2001. Repeat survey in 2015 showed positive outfall pipes had assisted in limiting the inﬂuence changes in the isotope ratios values of the near- of periodic ﬂood currents associated with the tidal shore marine resident sentinel organisms in com- and wave actions that usually cascade sewage parison with the values reported 2001, suggesting eﬄuent towards the previously contaminated that the modiﬁcations of the sewage treatment sites. The digestive tissues of M. galloprovincialis processes and extension of the outfalls have been provided a good pointer to the declined inﬂuence eﬀective in directing sewage-derived C and N of the sewage-derived exhibiting a trophic enrich- away from the previously contaminated sites. 13 13 ment (δ C~1‰ and δ N~3‰)towards the Contrast of the isotopic ratios of these sentinel marine POM. Discriminating between the 2010 organisms from previously and reference sites and 2015 carbon and nitrogen isotopic ratios in was indistinguishable in 2015 contrary from the the tissues of M. galloprovincialis from reference 2001 survey. Mixing models reveal mussels at the and previously contaminated sites revealed highly two previously contaminated beaches now get signiﬁcant diﬀerences in both abductor and diges- most of their nutrition from marine POM with a tive tissues. The contrast of the 2015carbon and minor subsidy from terrestrial sources. nitrogen isotopic ratios in the tissues (i.e., abduc- tor and digestive) of M. galloprovincialis from the reference and previously contaminated sites 6. Implications and directions for future revealed no signiﬁcant diﬀerences. study The two-source isotopic mixing model revealed The sentinel organisms provided an opportunity for the contribution of terrigenous organic materials in further temporal and spatial scale isotopic studies the marine bivalve to vary from 1% to 5% for δ C juxtaposed with conceptual isotopic mixing models and 13% to 51% for δ N. The carbon and nitrogen and application of chemical tracers to trace the isotopic values of the suspended POM from ﬁltered sources, ﬂow, cycling, and providence of nutrients water samples of the riverine and estuarine systems and organic materials in the nearshore marine with open connection to the ocean reﬂected the waters. Surveying the environmental conditions, diversiﬁed nature of the pool of organic materials biological activity and hydrodynamics of the near- incursions to the nearshore coastal waters. These shore waters will provide additional insight on the sources range from natural to human-induced activ- underlying mechanisms responsible for the cross- ities, e.g., atmospheric deposition, organic waste boundary (i.e., land-ocean coupling) transfer of materials from the farm (manure) and grazing mar- nutrients and organic materials to the nearshore ine animals (sea lions and birds), fertilisers, and pos- waters and their eventual sequestration to the near- sibly groundwater leachates arising from the shore marine food web. nitriﬁcation of ammonium from animal organic waste residues underground. Land-based nitrogen sources from tidal channels seemed to sway the near- Disclosure statement shore marine waters while carbon sources were pre- No potential conﬂict of interest was reported by the authors. dominantly marine origin. The macro-algae communities (such as Macrocystis sp.) that are washed onshore and into the tidal channels contri- Funding bute a substantial amount of carbon and nutrients to This work was supported by the University of Otago the nearshore waters and freshwater systems along [Doctoral scholarship]. the coastline (Duggins, 1988; Hepburn, Holborow, Wing, Frew, & Hurd, 2007; Michelou, Caporaso, Knight, & Palumbi, 2013). Other likely sources are Statement of Ethics sewage-derived matter inﬂuxes from pastoral ani- The number of shellﬁsh collected per day from each of the mals, farm organic manure, detrital matter (i.e., study sites during the course of this study was in accordance decomposition of plant materials, seagrasses in estu- with the New Zealand Fisheries Amended Act (Amateur aries), rural runoﬀs, and watershed catchment area. Fishing) Regulations of 1986: revoked, on 1 February 2014, GEOLOGY, ECOLOGY, AND LANDSCAPES 63 by regulation 161(1) (a) of the Fisheries (Amateur Fishing) sewage signals in multiple marine taxa. Marine Regulations 2013 (SR 2013/482) stipulated in Section 19 Pollution Bulletin, 71(1–2), 152–158. Sub-clause 1 and 2. Furthermore, numbers of biological Coplen, T. B. (2011). Guidelines and recommended terms samples collected and analysed did not in any way aﬀect for expression of stable-isotope-ratio and gas-ratio mea- the species composition, diversity, and coastal ecosystem surement results. Rapid Communications in Mass functioning of the nearshore marine waters. Spectrometry, 25(17), 2538–2560. Council, O. R. (2001). Regional Plan: Coast. Accessed Online January, 12, 2008. Dede, O.T., Telci, I. T.,&Aral, M.M.(2013). The use ORCID of water quality index models for the evaluation of surface water quality: A case study for Kirmir Basin, Oluwuyi Babaranti http://orcid.org/0000-0002-9047- Ankara, Turkey. Water Quality, Exposure and Health, 5(1), 41–56. Tim Jowett http://orcid.org/0000-0001-7146-5188 Deegan, L. A., & Buchsbaum, R. (2005). The eﬀect of Russell Frew http://orcid.org/0000-0002-3492-9454 habitat loss and degradation on ﬁsheries. The decline of ﬁsheries resources in New England: Evaluating the impact of overﬁshing, contamination, and habitat degradation References (pp. 67–96). MA: MIT Sea Grant College Program. Deudero, S., Box, A., Tejada, S., & Tintoré, J. (2009). Stable Abbasi, T., & Abbasi, S. (2011). Water quality indices based isotopes and metal contamination in caged marine mus- on bioassessment: The biotic indices. Journal of Water sel. Mytilus Galloprovincialis. Marine Pollution Bulletin, and Health, 9(2), 330–348. 58(7), 1025–1031. Alfaro, A. C., Jeﬀs, A. G., & Hooker, S. H. (2001). Diaz, R. J., Rhoads, D. C., Blake, J. A., Kropp, R. K., & Reproductive behavior of the green-lipped mussel, Keay, K. E. (2008). Long-term trends of benthic habitats Perna canaliculus, in Northern New Zealand. Bulletin related to reduction in wastewater discharge to Boston of Marine Science, 69(3), 1095–1108. Harbor. Estuaries and Coasts, 31(6), 1184–1197. Baker, D. M., MacAvoy, S. E., & Kim, K. (2007). Doré, W. J., Henshilwood, K., & Lees, D. N. (2000). Relationship between water quality, δ N, and aspergil- Evaluation of F-speciﬁc RNA bacteriophage as a candi- losis of Caribbean sea fan corals. Marine Ecology date human enteric virus indicator for bivalve molluscan Progress Series, 343, 123–130. shellﬁsh. Applied and Environmental Microbiology, 66 Barr, N. G., Dudley, B. D., Rogers, K. M., & Cornelisen, C. (4), 1280–1285. D. (2013). Broad-scale patterns of tissue-δ Nand tissue- Dudley, B. D., & Shima, J. S. (2010). Algal and invertebrate N indices in frondose Ulva spp.; Developing a national bioindicators detect sewage eﬄuent along the coast of baseline indicator of nitrogen-loading for coastal New Titahi Bay, Wellington, New Zealand. New Zealand Zealand. Marine Pollution Bulletin, 67(1), 203–216. Journal of Marine and Freshwater Research, 44(1), 39–51. Bates, D. M. (2010). lme4: Mixed-eﬀects modeling with R. Duggins, D. (1988). The eﬀects of kelp forests on nearshore Retrieved from http://lme4.r-forge.r-project.org/book. environments: Biomass, detritus, and altered ﬂow. The Bedard-Haughn, A., Van Groenigen, J., & Van Kessel, C. Community Ecology of Sea Otters, 65(9), 192–201. (2003). Tracing 15N through landscapes: Potential uses Ebner, B. C., McAllister, R. R., & Suter, P. (2009). Eﬀects of and precautions. Journal of Hydrology, 272(1–4), 175–190. sample size on numerical estimates of diet prey con- Bouman, R., & Archer, H. (2014). Tahuna WWTP, sumption in a ﬁsh population. New Zealand Journal of Dunedin, New Zealand: An innovative upgrade. Marine and Freshwater Research, 43(2), 579–590. Proceedings of the Water Environment Federation, 2014 Ellis, T. G. (2004). Chemistry of wastewater. Encyclopedia (16), 4096–4116. of Life Support System (EOLSS), 2, 1–10. Browne, M. A., Crump, P., Niven, S. J., Teuten, E., Tonkin, Fry, B. (2002). Conservative mixing of stable isotopes A., Galloway, T., et al. (2011). Accumulation of micro- across estuarine salinity gradients: A conceptual frame- plastic on shorelines worldwide: Sources and sinks. work for monitoring watershed inﬂuences on down- Environmental Science & Technology, 45(21), 9175–9179. stream ﬁsheries production. Estuaries, 25(2), 264–271. Bump, J. K., Fox-Dobbs, K., Bada, J. L., Koch, P. L., Fry, B., Gace, A., & McClelland, J. W. (2003). Chemical Peterson, R. O., & Vucetich, J. A. (2007). Stable isotopes, indicators of anthropogenic nitrogen-loading in four ecological integration and environmental change: Paciﬁc estuaries. Paciﬁc Science, 57(1), 77–101. Wolves record atmospheric carbon isotope trend better Gartner, A., Lavery, P., & Smit, A. (2002). Use of δ N than tree rings. Proceedings of the Royal Society of signatures of diﬀerent functional forms of macroalgae London B: Biological Sciences, 274(1624), 2471–2480. and ﬁlter-feeders to reveal temporal and spatial pat- Cabana, G., & Rasmussen, J. B. (1996). Comparison of terns in sewage dispersal. Marine Ecology Progress aquatic food chains using nitrogen isotopes. Series, 235,63–73. Proceedings of the National Academy of Sciences, 93 Gaston, T. F., & Suthers, I. M. (2004). Spatial variation in (20), 10844–10847. 13 15 δ C and δ N of liver, muscle and bone in a rocky reef Chary, N. S., Kamala, C., & Raj, D. S. S. (2008). Assessing planktivorous ﬁsh: The relative contribution of sewage. risk of heavy metals from consuming food grown on Journal of Experimental Marine Biology and Ecology, 304 sewage irrigated soils and food chain transfer. (1), 17–33. Ecotoxicology and Environmental Safety, 69(3), 513–524. Gormley,A.M.,Slooten,E.,Dawson,S.,Barker,R.J., Cheevaporn, V., & Menasveta, P. (2003). Water pollution Rayment,W.,DuFresne,S.,&Bräger,S.(2012). First and habitat degradation in the Gulf of Thailand. Marine evidence that marine protected areas can work for Pollution Bulletin, 47(1), 43–51. marine mammals. Journal of Applied Ecology, 49(2), Connolly, R. M., Gorman, D., Hindell, J. S., Kildea, T. N., & 474–480. Schlacher, T. A. (2013). High congruence of isotope 64 O. BABARANTI ET AL. Greening, G. E., Lewis, G. D., & Dollimore, J. (2007). FRST North, J. C., Frew, R. D., & Hale, R. V. (2006). Can stable programme C03X0301 safeguarding environmental isotopes be used to monitor landﬁll leachate impact on health and market access for NZ foods objective 2: surface waters? Journal of Geochemical Exploration, 88 Virus prevalence in shellﬁsh. 1,1–45. (1–3), 49–53. Hargrave, B., Holmer, M., & Newcombe, C. (2008). North, J. C., Frew, R. D., & Peake, B. M. (2004). The use of Towards a classiﬁcation of organic enrichment in mar- carbon and nitrogen isotope ratios to identify landﬁll lea- ine sediments based on biogeochemical indicators. chate contamination: Green Island Landﬁll, Dunedin, New Marine Pollution Bulletin, 56(5), 810–824. Zealand. Environment International, 30(5), 631–637. Hepburn, C. D., Holborow, J. D., Wing, S. R., Frew, R. D., Ouédraogo, O., Chételat, J., & Amyot, M. (2015). & Hurd, C. L. (2007). Exposure to waves enhances the Bioaccumulation and trophic transfer of mercury and growth rate and nitrogen status of the giant kelp selenium in African sub-tropical ﬂuvial reservoirs food Macrocystis pyrifera. Marine Ecology Progress Series, webs (Burkina Faso). PloS One, 10(4), e0123048. 339,99–108. Pan, J.-F., & Wen-Xiong, W. (2004). Diﬀerential uptake of Hillebrand, H., & Sommer, U. (2000). Diversity of benthic dissolved and particulate organic carbon by the marine microalgae in response to colonization time and eutro- mussel. Perna Viridis. Limnology and Oceanography, 49 phication. Aquatic Botany, 67(3), 221–236. (6), 1980–1991. Horn, S. (2001). Tracking marine sewage outfall along the Peterson, B. J. (1999). Stable isotopes as tracers of organic Otago Peninsula using stable isotope analysis of blue matter input and transfer in benthic food webs: A mussels Mytilus galloprovincialis, and sea lettuce Ulva review. Acta Oecologica, 20(4), 479–487. lactuca, as biotracer species, pp33 (BSc (Hons) Post, D. M. (2002). Using stable isotopes to estimate Dissertation). Otago, Dunedin, New Zealand. trophic position: Models, methods, and assumptions. IANZ. (2004). Uncertainty of measurement, precision and Ecology, 83(3), 703–718. limits of detection chemical and microbiological testing Rayment, W., Dawson, S., & Slooten, E. (2010). Seasonal laboratories. International Accrediation New Zealand: changes in distribution of Hector’s dolphin at Banks Auckland. Peninsula, New Zealand: Implications for protected Jarvie, H. P., Neal, C., & Withers, P. J. (2006). Sewage- area design. Aquatic Conservation: Marine and eﬄuent phosphorus: A greater risk to river eutrophica- Freshwater Ecosystems, 20(1), 106–116. tion than agricultural phosphorus? Science of the Total RCL. (2000). Otago regional council resource consent 97530 Environment, 360(1–3), 246–253. condition 8: Rocky Shore Ecological Monitoring-January/ Kline, J., & Thomas, C. (1999). Temporal and spatial varia- February 2000. Dunedin, New Zealand: Ryder 13 12 15 14 bility of C/ C and N/ N in pelagic biota of Prince Consulting Ltd. William Sound, Alaska. Canadian Journal of Fisheries Rogers, K. M. (2003). Stable carbon and nitrogen isotope and Aquatic Sciences, 56(S1), 94–117. signatures indicate recovery of marine biota from sewage Lewis, G. D., Loutit, M. W., & Austin, F. J. (2010). Human pollution at Moa Point, New Zealand. Marine Pollution enteroviruses in marine sediments near a sewage outfall Bulletin, 46(7), 821–827. on the Otago Coast. New Zealand Journal of Marine and Savage, C. (2005). Tracing the inﬂuence of sewage nitrogen in Freshwater Research, 19(2), 187–192. a coastal ecosystem using stable nitrogen isotopes. AMBIO: Lorrain, A., Paulet, Y.-M., Chauvaud, L., Savoye, N., A Journal of the Human Environment, 34(2), 145–150. Donval, A., & Saout, C. (2002). Diﬀerential δ C and Savage, C., & Elmgren, R. (2004). Macroalgal (Fucus vesi- 15 15 δ N signatures among scallop tissues: Implications for culosus) δ N values trace decrease in sewage inﬂuence. ecology and physiology. Journal of Experimental Marine Ecological Applications, 14(2), 517–526. Biology and Ecology, 275(1), 47–61. SITO. (2006). Seafood industry training organisation- learn- Michelou, V. K., Caporaso, J. G., Knight, R., & Palumbi, ing resource for unit standard 16340 v3 “Biology of new S. R. (2013). The ecology of microbial communities zealand green mussels” 1, 1–23. associated with Macrocystis pyrifera. PLoS One, 8(6), Teklehaimanot, G. Z., Coetzee, M. A., & Momba, M. N. e67480. (2014). Faecal pollution loads in the wastewater eﬄuents Michener, R. H., & Kaufman, L. (2008). Stable isotope and receiving water bodies: A potential threat to the ratios as tracers in marine food webs: An update. health of Sedibeng and Soshanguve communities, Stable Isotopes in Ecology and Environmental Science, South Africa. Environmental Science and Pollution Second Edition, 2, 238–282. Research, 21(16), 9589–9603. Morand, P., & Merceron, M. (2005). Macroalgal population Thompson, D., Phillips, R., Stewart, F., & Waldron, S. and sustainability. Journal of Coastal Research, 215, (2000). Low δ C signatures in pelagic seabirds: Lipid 1009–1020. ingestion as a potential source of C-depleted carbon in Morillo, J., Usero, J., & Gracia, I. (2004). Heavy metal the Procellariiformes. Marine Ecology Progress Series, distribution in marine sediments from the Southwest 208, 265–271. coast of Spain. Chemosphere, 55(3), 431–442. Waldron, S., Tatner, P., Jack, I., & Arnott, C. (2001). The Nicholson, C. M., Lewis, G. D., & Loutit, M. W. (1989). impact of sewage discharge in a marine embayment: A Survey of human pathogenic bacteria and viruses in stable isotope reconnaissance. Estuarine, Coastal and cockle beds at Otakou, Otago Harbour, New Zealand. Shelf Science, 52(1), 111–115. New Zealand Journal of Marine and Freshwater Yang, X. E., Wu, X., Hao, H.-L., & He, Z.-L. (2008). Research, 23(4), 529–532. Mechanisms and assessment of water eutrophication. Nordsieck, R. (2006, December 12). The living world of Journal of Zhejiang University Science B: Biomedicine molluscs. The Common Mussel (Mytilus edulis). and Biotechnology, 9(3), 197–209.

Journal

Geology Ecology and Landscapes – Taylor & Francis

Published: Jan 2, 2019

Keywords: Sewage effluent; wastewater; isotopic enrichment factor; organic matter; linear mixed effect modelling; bioindicators

Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

Isotopic signatures in Mytilus galloprovincialis and Ulva latuca as bioindicators for assessing discharged sewage effluent in coastal waters along Otago Peninsula, New Zealand

References (69)

Abstract

Journal

Recommended Articles

There are no references for this article.

Our policy towards the use of cookies