Marine Pollution Bulletin 77 (2013) 140–146

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The use of the brown macroalgae, Sargassum flavicans, as a potential bioindicator of industrial nutrient enrichment Ralph Alquezar a,⇑, Lionel Glendenning b, Simon Costanzo c a

Central Queensland University, Centre for Environmental Management, Bryan Jordan Drive, PO Box 1319, Gladstone, Qld 4680, Australia James Cook University, Australian Centre for Tropical Freshwater Research, James Cook Drive, Townsville, Qld 4811, Australia c University of Maryland, Center for Environmental Science, PO Box 775, 2020 Horns Point Rd, Cambridge, MD 21613, USA b

a r t i c l e Keywords: Sargassum flavicans Stable isotopes Nutrient enrichment Bioindicator species Brown algae

i n f o

a b s t r a c t Nutrient bioindicators are increasingly being recognised as a diagnostic tool for nutrient enrichment of estuarine and marine ecosystems. Few studies, however, have focused on field translocation of bioindicator organisms to detect nutrient discharge from industrial waste. The brown macroalgae, Sargassum flavicans, was investigated as a potential bioindicator of nutrient-enriched industrial effluent originating from a nickel refinery in tropical north-eastern Australia. S. flavicans was translocated to a number of nutrient enriched creek and oceanic sites over two seasons and assessed for changes in stable isotope ratios of 15N and 13C within the plant tissue in comparison to reference sites. Nutrient uptake in macroalgae, translocated to the nutrient enriched sites adjacent to the refinery, increased 3–4-fold in d15N, compared to reference sites. Using d15N of translocated S. flavicans proved to be a successful method for monitoring time-integrated uptake of nitrogen, given the current lack of passive sampler technology for nutrient monitoring. Ó 2013 Elsevier Ltd. All rights reserved.

1. Introduction Estuarine and marine concentrations of Dissolved Inorganic Nitrogen (DIN), particularly in the form of ammonia, nitrate and nitrite, have steadily increased due to anthropogenic activity (Ahad et al., 2006; Eddy, 2005; Harris, 1999; Liu et al., 2007). DIN can originate from a number of sources, including urban and agricultural activities, aquaculture facilities, and Waste Water Treatment Plants (WWTP) (Costanzo et al., 2003; Lapointe et al., 2010; Lin and Fong, 2008; Stephens and Farris, 2004; Volkman et al., 2007), affecting natural nitrogen cycling, phytoplankton communities and lower trophic level stability (Balata et al., 2008; Bishop et al., 2006; Burkholder et al., 2007; Camargo and Alonso, 2006; Dolbeth et al., 2007; Fabricius, 2005). Moreover, increased DIN inputs into adjacent estuarine systems from industrial inputs, such as pulp mills, mining and refining processes, are consistent point sources of DIN, which require regulatory monitoring and assessment for the maintenance of the neighbouring estuarine and marine environments (Bothwell, 1992; Camargo and Alonso, 2006; Church et al., 2006; Friese et al., 1998; Scrimgeour and Chambers, 2000; Seitzinger et al., 2002; Woelfl et al., 2000).

⇑ Corresponding author. Present address: Vision Environment Queensland, PO Box 1267, Gladstone, Qld 4680, Australia. Tel.: +61 7 4972 7530; fax: +61 7 4972 1313. E-mail address: [email protected] (R. Alquezar). 0025-326X/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.marpolbul.2013.10.013

Given the dynamic and varying nature of the hydrology and underlying water characteristics in tropical estuarine and marine environments, which are mainly influenced by local geology, ecohydrology, micro-climates, and more broadly, seasonal changes, traditional, in situ, water quality sampling only represents a snapshot in time. ChemcatchersÒ and passive samplers can quantify certain chemicals, such as metals and pesticides within the water column over time (Don and Vroblesky, 2007; Greenwood et al., 2007; O’Brien et al., 2012; Vermeirssen et al., 2009; Warnken et al., 2007), however, there is a deficiency in passive sampler technologies that can be used to determine nutrient levels in the water column over specific time periods. The use of indicator species benefits over traditional grab samples in that the extended period of deployment allow nutrient concentrations within the water column to be accumulated in the indicator organisms, providing a calculable time-averaged measurement of bioavailable nutrients in waters over a period of several days. A number of natural floral and faunal bioindicators such as macroalgae, mangroves, mussels, earth worms, seagrass, and corals, have been used in the past to detect nutrient enrichment from sewage treatment facilities, shrimp farms, and agricultural runoff (Costanzo et al., 2003,2004; Lin and Fong, 2008; Risk et al., 2009; Schmidt and Ostle, 1999). On the other hand, very few studies have used manipulative translocation techniques to detect anthropogenic inputs, such as industrial nutrient inputs, into an estuarine or marine environment (Costanzo et al., 2005; Fertig et al., 2009;

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Udy and Dennison, 1997). The advantages of using translocation techniques include the fact that the translocated species has not been previously exposed to local or regional contaminants; all sites contain algae from the same remote source site, reducing spatial variability; and a ‘before and after’ exposure estimate can therefore be accurately obtained. For the study described below, the use of the brown macroalgae, Sargassum flavicans, was examined as a potential bioindicator of industrial nutrient enrichment using stable isotope analysis, by translocating the algae into areas of known higher concentrations of DIN. A number of algae species have successfully been used as bioindicators of estuarine and marine nutrient enrichment (eutrophication) (Pihl et al., 1999; Smith, 1996), by using stable isotope (d15N/d13C) signatures (Costanzo et al., 2005; Rogers, 2003). Stable isotope signatures have also successfully been applied as tracers of nutrient enrichment on flora and fauna, particularly with respect to algae and algal grazers such as limpets and mussels (Fry and Allen, 2003; Gray, 2002; Rogers, 2003). Higher order plants, such as mangroves, have been used as longer term biomonitors of nutrient enrichment (Costanzo et al., 2004). Changes in carbon and nitrogen ratios in organisms can identify prominent nutrient sources (Peterson and Fry, 1987; Risk et al., 2009). S. flavicans was selected due to its favourable attributes as a bioindicator species, given that the species is readily available in subtropical and tropical estuarine and marine systems, is available all year round, and shares similar traits with other Sargassum species such as being a nutrient opportunist and sensitive to nutrient uptake (Matsuo et al., 2009; Roberts et al., 2008; Rossi et al., 2009; Yuka et al., 2001). The geographic range of S. flavicans is extensive, as it can be found in Southwest Asia, Africa, Southeast Asia, Australia and New Zealand and the Pacific Islands (Phillips, 1995). This study was conducted in Halifax Bay, situated to the north of the city of Townsville (19° 15.480 S, 146° 49.090 E) and south of the town of Ingham (18° 39.070 S, 146° 9.310 E) in far north Queensland, Australia (Fig. 1). The bay forms part of the Great Barrier Reef World Heritage Area and the Wet Tropics World Heritage Area. There are a number of ephemeral tropical creeks and rivers that flow into Halifax Bay, which receive inputs from a variety of coastal catchments from both mixed land use and industry. The majority of the land adjacent to Halifax Bay consists of dry sclerophyll forest and patches of rainforest in the upper catchments, with very little urban development, and only a number of small beach communities. Apart from a refinery, there are negligible to very low amounts of other industrial nutrient discharges within the bay (Longstaff et al., 2001). The Burdekin River, which is located approximately 120 km south of Halifax Bay, can intermittently discharge large amounts of sediments, nutrients and toxicants during significant wet seasons, causing elevated nutrient rich and turbid water on a regional scale (Bainbridge et al., 2012). Industry refining processes use a number of technologies to extract metals from ore. For example, nickel and cobalt can be selectively extracted by using concentrated ammonia, in the form of concentrated ammonium carbonate liquor, to separate the metals as ammine complexes from the ore (Forbes et al., 2000; Jana and Akerkar, 1989; Pandey and Kumar, 1991; Price and Reid, 1993). Given the large quantities and high concentrations of ammonia as part of the refining process, particularly for cobalt and nickel extraction, ammonia may become an artificial footprint of nickel refineries if sufficient quantities of ammonia inadvertently find its way into the adjacent receiving environment of such facilities. The current study was implemented in 2010, close to a nickel/cobalt refinery, to determine novel techniques on the use of indicator species to monitor nutrient inputs using a time integrated approach. The objectives of this study were to determine the usefulness of the brown algae, S. flavicans, as a potential bioindicator of estuarine and marine nutrient loads by use of stable isotope analysis. The

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specific aims of the study were to (a) determine changes in nutrient uptake in S. flavicans along known nutrient enriched gradients, compared to reference sites, (b) compare differences among creek sites and oceanic sites, and (c) determine differences between wet and dry season uptake in a tropical marine coastal environment. 2. Methods 2.1. Sampling design In order to determine the usefulness of S. flavicans as a potential bioindicator of nutrient enrichment, a series of creek and oceanic sites were established in the receiving environment adjacent to industrial infrastructure and in reference locations. The study was conducted in Halifax Bay, northern Queensland, Australia (19°030 S, 146°290 E). A total of ten sites were established, five creek sites and five oceanic sites (Fig. 1). Experiments were undertaken during the 2010 wet season (February/March) and revisited during the dry season of June 2010 to determine seasonal changes. Creek sites included three sites adjacent to an industrial refinery (AC, BC, HC), and two reference sites, (SW and RC). In order to compare creek nutrient concentrations with nutrient concentrations within Halifax Bay, five oceanic sites were established. Two sites adjacent to the refinery (C2 and B2) as well as three reference sites (K2, G2 and I2) (Fig. 1). 2.2. Sample collection The brown marine macroalgae, S. flavicans, was collected from a relatively low nutrient, oligotrophic location ( 0.05). Mean temperatures differed among sampling times (P < 0.05), as expected (28.3 ± 0.4 °C in the wet season and 21.7 ± 0.3 °C during the dry season). There were no significant differences in pH values among sampling times (P < 0.05), with ranges from 7.1 to 8.2 for all sites and sampling events, conductivity did not differ among sampling times with mean concentrations of (45.5 ± 1.3 mS/cm) (P > 0.05), and dissolved oxygen was highest in the wet season (91.9 ± 3.0%) compared to the dry season (75.7 ± 3.6%) (P < 0.05). There were no significant differences in % carbon, % nitrogen content (Fig. 2), d13C signatures, or carbon/nitrogen (C:N) ratios among creek sites, controls (cutting and transport controls) or oceanic sites, irrespective of sampling time (P > 0.05) (Table 1). However, significant differences in d15N signatures, among creek sites compared to oceanic sites were observed (P < 0.05), with over a threefold increase among creek sites (Fig. 3a and b). Moreover, seasonal differences in % carbon and % nitrogen content were signifi-

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42

(a) Creeks 40

% Carbon

(b) Oceanic

Dry season 2010 Wet season 2010

40

38

38

36

36

34

34

32

32

30

30

28

28

3.0

3.0

(b) Oceanic

% Nitrogen

(a) Creeks 2.5

2.5

2.0

2.0

1.5

1.5

1.0

1.0

0.5

0.5

REF CC TC AC BC HC SW RC

REF CC TC

C2

B2

I2

G2

K2

Fig. 2. Mean (±se) % carbon and % nitrogen values for the marine macroalgae, Sargassum flavicans, at (a) creek sites and (b) Halifax Bay oceanic sites among seasons. White circles denote wet season samples and black circles denote dry season samples.

(Fig. 3a). There were no site differences in d15N signatures during the dry season (P > 0.05) (1.6–3.5‰) (Fig. 3). Similar spatial and season trends in macroalgal % carbon and % nitrogen content (Fig. 2b), d13C signatures and C/N ratios were observed for oceanic sites, compared to creek sites, with significant differences in % carbon among sites but not necessarily adjacent industry sites (P < 0.05), and no significant differences in nitrogen (Fig. 2b), or C/N isotope ratios among sites (P > 0.05), irrespective of season (Site x season; P > 0.05). Similar to creek sites, d15N signatures of macroalgal tissues deployed among oceanic sites were significantly higher, up to twofold, at sites C2 and B2 (5.7–6.1‰; adjacent industrial sites) compared to all control and reference sites (4.2–4.5‰), particularly during the wet season sampling event of 2010 (P < 0.05) (Fig. 3b). Water column nutrient concentrations (Dissolved Inorganic Nitrogen) were concomitantly elevated at the same creek sites, AC and BC, during the wet season, and to a lesser extent, during the dry season (Fig. 3c), as was observed for nitrogen enrichment in macroalgae samples (Fig. 3a and b).

cantly higher during the dry season compared to the wet season (P < 0.05) (Fig. 2a), with wet season d13C signatures, d15N signatures and C:N ratios all higher (Table 1). Given that distinct differences in d15N signatures were evident among creek sites compared to oceanic sites, creek sites were analysed separately from oceanic sites to further discriminate differences in potential enrichment among adjacent industrial sites (Fig. 3). For creek sites only, although some differences were observed for % nitrogen (P < 0.05), increased % nitrogen was not necessarily observed at adjacent industrial sites alone (Fig. 2). There were no significant (P > 0.05) differences in % carbon or d13C signatures among sites (Table 1). Moreover, d13C signatures were significantly higher during the wet season compared to the dry season (P < 0.05), irrespective of site (Site x Season interaction; P > 0.05) (Table 1). Conversely, d15N signatures of macroalgal tissues deployed at creek sites adjacent to Halifax Bay revealed a significant enrichment of nitrogen at BC (12.6‰) and AC (9.2‰) compared to reference sites (4.2–4.4‰) during the wet season (P < 0.05)

Table 1 Mean (±se) % carbon and % nitrogen in the marine algae, Sargassum flavicans, during the wet and dry seasons of 2010 at creek, oceanic, control and reference sites within Halifax Bay and near Gladstone. (–) denotes no results available due to vandalism. Sites

REF – Reference TC – Control CC – Control AC – Creek BC – Creek HC – Creek SW – Creek RC – Creek B2 – Oceanic C2 – Oceanic I2 – Oceanic G2 – Oceanic K2 – Oceanic

Wet season 2010

Dry season 2010

%C

%N

C:N

%C

%N

C:N

32.7 ± 0.4 34.5 ± 0.4 33.4 ± 0.7 33.9 ± 1.4 31.5 ± 1.0 – 34.0 ± 0.5 32.4 ± 0.6 31.3 ± 0.4 31.9 ± 0.4 33.1 ± 0.5 32.0 ± 0.9 30.9 ± 1.0

1.4 ± 0.1 1.6 ± 0.1 1.7 ± 0.1 1.4 ± 0.1 1.7 ± 0.1 – 1.5 ± 0.1 1.3 ± 0.1 1.4 ± 0.1 1.6 ± 0.1 1.5 ± 0.1 1.4 ± 0.1 1.4 ± 0.1

22.7 ± 1.3 21.4 ± 1.8 20.3 ± 1.6 23.4 ± 1.2 18.3 ± 1.1 – 23.4 ± 0.5 25.8 ± 1.3 22.3 ± 0.7 20.2 ± 0.5 21.8 ± 0.5 23.1 ± 0.8 22.6 ± 1.7

36.3 ± 0.3 36.3 ± 0.3 34.5 ± 0.6 34.6 ± 0.7 34.3 ± 0.7 34.6 ± 0.8 32.7 ± 0.5 32.6 ± 0.3 33.8 ± 1.1 35.5 ± 0.5 35.3 ± 0.5 35.1 ± 0.5 35.2 ± 0.6

2.1 ± 0.1 1.7 ± 0.1 1.8 ± 0.1 1.7 ± 0.1 1.6 ± 0.1 1.5 ± 0.1 1.4 ± 0.1 1.4 ± 0.1 1.5 ± 0.3 2.0 ± 0.1 1.8 ± 0.1 1.8 ± 0.1 1.8 ± 0.1

17.3 ± 0.9 20.2 ± 1.2 21.2 ± 1.9 20.0 ± 0.9 21.4 ± 0.7 22.7 ± 1.5 22.5 ± 0.9 22.9 ± 0.5 24.7 ± 5.4 17.9 ± 0.4 19.6 ± 1.1 19.8 ± 1.4 20.1 ± 0.4

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μ

δ

δ

144

Fig. 3. Mean (±se) nitrogen stable isotope values (d15N) for the marine macroalgae, Sargassum flavicans, (a) creek sites and (b) Halifax Bay oceanic sites, and (c) nutrient samples along the same creek sites between seasons. White circles/bars denote wet season samples and black circles/bars denote dry season samples.*Denotes significant (P < 0.01) difference from background or reference sites.

4. Discussion Sargassum beds host important ecological function to other food webs by providing surfaces for other epiphytic algae to adhere to, and provide food, shelter and protection to a number of small vertebrates and invertebrate organisms (Roberts et al., 2008; Rossi et al., 2009; Yuka et al., 2001). Marine algae and phytoplankton, in general, have the ability to turn over nutrients in the overlaying water column at a rapid rate, thus, giving a relatively quick assessment of nutrient enrichment, and making them suitable as biological indicators (Costanzo et al., 2004, 2005). Nitrogen values (d15N) in waters greater than 2‰ are said to be elevated. This can happen due to biological or chemical processed such as denitrification by bacteria, volatilisation from water evaporation, nitrification from excess sewage/nutrient runoff, or organ-

ic decomposition by bacteria (Augley et al., 2007; Costanzo et al., 2004, 2005; Peterson and Fry, 1987). Moreover, industrial discharge or seepage can contribute to ammonia enrichment from refining practices into receiving environments (Jana and Akerkar, 1989; Pandey and Kumar, 1991; Price and Reid, 1993). Given that there were no significant differences in % carbon content among locations (Table 1; Fig. 2), our results suggest that carbon material absorbed by the macroalgae S. flavicans, at all sites, were from similar regional sources (Lepoint et al., 2004; Post, 2002). Carbon signatures are indicative of the source environment or the origin of a sample (Peterson and Fry, 1987). BC and AC, adjacent creeks to the refinery, showed elevated levels of d15N of up to 3 times higher than reference/control sites during the 2010 wet season, following the five day deployment (Fig. 3). A similar trend was observed for the oceanic sites within Halifax Bay, with sites C2 and B2, adjacent to BC and AC, being the closest oceanic sites to the refinery, also showing a discernibly elevated nutrient signature in the macroalgal tissue, of up to 2 times reference and control levels (Fig. 2b), suggesting that runoff from the adjacent creeks and associated catchment area significantly contribute to nutrient enrichment along the southern section of Halifax Bay. However, oceanic values were significantly lower than creek values, irrespective of the season (Fig. 3). Decreasing values in oceanic sites may be indicative of greater mixing within the water column, causing a dilution effect from the nitrogen enriched creeks, as tropical oceanic waters are oligotrophic systems, hence, are generally lower in nitrogen ( 0.05) differences in elevated nutrient signatures (d13C or d15N) for sites adjacent to the refinery, compared to reference or control sites, during the 2010 dry season. This suggests that the significant rainfall events, typical of northern Australian wet seasons, could potentially contribute to the transport of excess nutrients into adjacent receiving environments (Fertig et al., 2009; Lapointe et al., 2010). Previous monitoring studies have identified sources of nitrogen enrichment in the tailings Dam of nickel refineries to be up to 43‰, suggesting strong fractionation of nitrogen from nickel processing (Longstaff et al., 2001). Nutrient concentrations in the water column of creek sites, and to a lesser extent, oceanic sites, were significantly higher during the wet season compared to the dry season (Fig. 3), particularly for sites adjacent to the refinery, which clearly indicate the observed increased levels of d15N values in S. flavicans was from dissolved inorganic nitrogen enrichment (Fig. 3c). Other studies have also shown increased rates of nutrient uptake in a number of organisms in relation to changes in seasonal water chemistry and physiological function (Fertig et al., 2009). In a similar study using a different species of Sargassum, d15N values from sites adjacent to a fish aquaculture facility were enriched up to 7.4 ± 1.3‰, compared to our study of up to 12‰ and 6.5‰ in adjacent refinery creek sites and oceanic sites, respectively (Matsuo et al., 2009). Matsuo et al. (2009) reported over 200 lg/LDIN in the water column adjacent to a fish aquaculture facility. In our study, concentrations of over 30 lg/L-DIN were reported during the dry season and over 400 lg/L-DIN during the wet season (Fig. 3c), which coincided with an increase in nutrient uptake in the brown algae of 350% in creek sites and 150% in oceanic sites following the five day deployment. To conclude, given the lack of manipulative studies to discern suitability of bioindicator species, and lack of nutrient passive sampler technology, this novel study demonstrates the usefulness of the common brown macroalgae species, S. flavicans, as a potential bioindicator of nutrient enrichment, to determine bioavailable uptake from industrial refinery loading into estuarine and marine environments. In particular, d15N values were the most sensitive endpoints to determine biological uptake in the brown algae.

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Acknowledgements The authors acknowledge CQUniversity Australia for funding contributions. Additional support came from QNPL. We would like to thank the field team, including, Amie Anastasi, Adam Balkin, Brett Buckle, Dylan Charlesworth, and a special thanks to Rene Diocares for isotope analyses. This study was conducted under the GBRMPA permit number G09/02-017, and Fisheries permit number 138966.

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The use of the brown macroalgae, Sargassum flavicans, as a potential bioindicator of industrial nutrient enrichment.

Nutrient bioindicators are increasingly being recognised as a diagnostic tool for nutrient enrichment of estuarine and marine ecosystems. Few studies,...
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