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Neogastropoda. Food security. 1. Introduction. The combination of changing ecological landscapes and disturbance regimes associated with ocean warming ...

Journal of Experimental Marine Biology and Ecology 493 (2017) 7–13

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Ocean acidification and warming impacts the nutritional properties of the predatory whelk, Dicathais orbita Rick D. Tate a,⁎, Kirsten Benkendorff b, Roslizawati Ab Lah b,c, Brendan P. Kelaher a a b c

National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia Marine Ecology Research Centre, School of Environment, Science and Engineering, Southern Cross University, 2480 Lismore, NSW, Australia School of Fisheries Science and Aquaculture, University Malaysia Terengganu, 21030 Kuala Terengganu, Terengganu, Malaysia

a r t i c l e

i n f o

Article history: Received 19 November 2016 Received in revised form 1 March 2017 Accepted 13 March 2017 Available online xxxx Keywords: Ocean acidification Ocean warming Climate change Proximate composition Nutrition Muricidae Neogastropoda Food security

a b s t r a c t Ocean warming and acidification have the potential to impact the quality of seafood with flow on effects for future food security and ecosystem stability. Here, we used a 35-day experiment to evaluate how ocean warming and acidification may impact the nutritional qualities and physiological health of Dicathais orbita, a predatory muricid whelk common on the east coast of Australia, and discuss the broader ecological implications. Using an orthogonal experimental design with four treatments (current conditions [~23 °C and ~380 ppm of pCO2], ocean warming treatment [~ 25 and ~ 380 ppm of pCO2], ocean acidification treatment [CO2 ~ 23 °C and ~750 ppm of pCO2], and ocean warming and acidification treatment [CO2, ~25 °C and ~750 ppm of pCO2]), we showed that changes in moisture and protein content were driven by significant interactions between ocean warming and acidification. Elevated ocean temperature significantly decreased protein in the whelk flesh and resulted in concurrent increases in moisture. Lipid, glycogen, potassium, sulfur, and phosphorus content also decreased under elevated temperature conditions, whereas sodium, boron and copper increased. Furthermore, elevated pCO2 significantly decreased lipid, protein and lead content. Whelks from control conditions had levels of lead in excess of that considered safe for human consumption, although lead uptake appears to be lowered under future ocean conditions and will be site specific. In conclusion, while D. orbita has received research attention as a potential food product with nutritious value, ocean climate change may compromise its nutritional qualities and reduce sustainable harvests in the future. Furthermore, ocean climate change may have deleterious impacts on the longevity and reproductive potential of this important rocky shore predator. © 2017 Elsevier B.V. All rights reserved.

1. Introduction The combination of changing ecological landscapes and disturbance regimes associated with ocean warming and acidification, as well as other stressors (e.g. pollution, fishing pressure, species invasions) creates an uncertain future for nearshore marine environments and the important fisheries that they support (Cooley et al., 2012). Ocean climate change is likely to influence fisheries productivity and value, with potentially negative consequences for food security (Cooley et al., 2012; Lloret et al., 2015; Tirado et al., 2010) and ecosystem integrity (Ferrari et al., 2011; Kroeker et al., 2013; Manriquez et al., 2016). While the potential impacts of ocean climate change on fisheries production have been well studied, almost no work has been done investigating the influence of ocean warming and acidification on seafood quality (but see Anacleto et al., 2014 and Valles-Regino et al., 2015). The future production of high protein seafood is important to support ever growing ⁎ Corresponding author at: National Marine Science Centre, Southern Cross University, P.O. Box 4321, Coffs Harbour, NSW 2450, Australia. E-mail address: [email protected] (R.D. Tate).

http://dx.doi.org/10.1016/j.jembe.2017.03.006 0022-0981/© 2017 Elsevier B.V. All rights reserved.

human populations with reduced agricultural capacity (Cooley et al., 2012; Doney et al., 2009). Proximate variables provide an overview of an animal's energetic resources (Berthelin et al., 2000; Pérez-Camacho et al., 2003) and nutritional value for human consumption, breaking down edible flesh into its primary constituents; moisture, ash, protein, and lipid (Begum et al., 2012; Silva and Chamul, 2000; Soufia et al., 2014). Changes in the composition of these proximate variables may alter the reproductive potential (Marshall et al., 1999) and nutritive value of commercially important fisheries species (Spitz et al., 2010). Thus, an assessment of proximate composition under future ocean conditions provides an opportunity to analyse the potential impacts on seafood quality and population sustainability. A previous study demonstrated that future ocean conditions can lead to a significant decrease in total lipids and omega 3 and 6 polyunsaturated fatty acids in the edible flesh of predatory marine whelks (Valles-Regino et al., 2015). In two species of bivalves, Anacleto et al. (2014) found that elevated temperature significantly decreased the relative proportion of some fatty acids, but not protein. Seafood quality and safety can also depend on accumulation of trace elements, including essential minerals and heavy metals in the flesh


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(Ab Lah et al., 2016), and environmental factors such a temperature and pH can influence the uptake of certain metal ions (Baines et al., 2006; López et al., 2010). Molluscs have been identified as one of the most sensitive phyla to ocean climate change (Byrne et al., 2013; Kroeker et al., 2013; Parker et al., 2013). Meanwhile, fisheries are diversifying and expanding the breadth of targeted species (Kasperski and Holland, 2013; McClenachan et al., 2014; Witkin et al., 2015). While invertebrate fisheries research focus over the past few decades has generally favoured typical bivalve molluscs, like oysters (Guo et al., 2016), some researchers are exploring underexploited gastropod species that provide potential new sources of protein (Ab Lah et al., 2016; Appukuttan and Philip, 1994; Noble et al., 2013; Woodcock and Benkendorff, 2008; Zarai et al., 2011). For example, gastropods in the family Muricidae represent an emerging fisheries resource and comprise approximately 39% of the global gastropod harvest (FAO, 2015). However, the majority of Muricidae production is based on Rapana venosa in China (Castell, 2012), so muricid whelks are still considered to be under-represented in fisheries and aquaculture on a global scale (FAO, 2014). Dicathais orbita (Muricidae) is a marine predatory whelk species (Neogastropoda) common in the temperate waters off the central and southern coasts of Australia and New Zealand (Woodcock and Benkendorff, 2008). This species has functional food potential, with high quality polyunsaturated fatty acids (Valles-Regino et al., 2015) and anticancer compounds (Benkendorff, 2013; Benkendorff et al., 2015) and have been investigated for their aquaculture potential (Noble et al., 2013; Woodcock and Benkendorff, 2008). Here, we evaluated the influence of ocean warming and acidification on the nutritional properties and physiological health of D. orbita. We measured proximate response variables (lipid, moisture, ash and protein content), a stress indicator (glycogen content), trace elements, change in shell length and animal weight as well as feeding rate to establish the biochemical responses of D. orbita to future ocean change. It was hypothesised that D. orbita nutritional quality and physiological health would deteriorate under induced warming and acidification stress.

Beach, New Zealand). Water pH was manipulated by bubbling CO2enriched air via a gas mixer (PEGAS 4000MF) through the CO2enriched header tanks, while the water in the current treatment header tanks was bubbled with ambient air. Each of the 12 header tanks supplied temperature and pH controlled water at 3 L·min−1 to a tray (860 × 650 × 96 mm) that housed twelve D. orbita. Animals were weighed (pan top balance to 0.01 g precision) and their maximum shell length was measured using callipers (1 mm precision) at the start and end of the experiment (analysed as percentage change). Whelks were acclimated in experimental conditions for one week before feeding trials commenced. Whelks were fed Sydney rock oysters (Saccostrea glomerata), which are a common prey item on local intertidal reefs. The whelks were initially fed a consistent number of oysters ranging 30–50 mm, with new oysters of similar size added daily to ensure whelk feeding rates were not influenced by food scarcity. Feeding rate was calculated as the mean number of oysters eaten per day per tray. Water pH, alkalinity, temperature and salinity readings were measured daily and used to calculate the partial pressure of CO2 (pCO2) using the CO2SYS program (Pierrot et al., 2006) with constants from Mehrbach et al. (1973) as adjusted by Dickson and Millero (1987). For the remainder of this publication, low pH conditions will be referred to as having elevated pCO2. 2.2. Sample preparation and proximate analyses of foot meat Whelks were dissected for proximate analysis according to Ab Lah et al. (2016). This was done to establish the percentage of whelk foot meat attributable to moisture (weight loss after drying at 40 °C), protein (Biuret protein assay), lipid (1:1 chloroform: methanol extract) and ash (incinerated in a muffle furnace). One sample of foot meat (~0.35 g) was taken from three whelks per tray at random to create three physically homogenized replicates for each proximate response variable. All samples were frozen (−80 °C) for later use and were defrosted immediately prior to analysis.

2. Materials and method

2.3. Physiological health indicators from gills

2.1. Experimental set up

Gills were removed for glycogen analysis. These were dissected from three randomly selected whelks per tray, as above. Samples of gill tissue were frozen in liquid nitrogen to slow enzymatic activity and tissue degradation, and subsequently hand ground in 10 mL of 0.06 M perchloric acid (PCA) within a falcon tube using a Teflon masher for 3 min. Adjusting the method described in Krisman (1962), the homogenized samples were centrifuged at 4200 rpm for 2.5 min and 1 mL of the resultant supernatant was transferred into smaller vials for glycogen analysis. Glycogen was analysed following Krisman (1962) as described by Roberts et al. (2009). Glycogen concentration in the gill samples was then estimated from the linear regression equation of a standard curve using oyster glycogen Type II (Sigma-Aldrich) and adjusted for dilution to obtain the final amount of glycogen as a percent of fresh weight.

To test the hypotheses that both ocean warming and acidification will reduce the physiological health and nutritional value of Dicathais orbita, 144 adult whelks were divided into control and experimentally induced warming and acidification treatments for 35 days at the National Marine Science Centre (NMSC) in Coffs Harbour, Australia (30° 16′3.70″S, 153° 8′15.31″E). The experiment utilised D. orbita (51–79 mm shell length) from rock platforms around the Coffs Harbour region and had a two-factor design with four treatments, each with three replicate trays (n = 3, current conditions representing our control, mean ± SD = 22.9 ± 0.5 °C and 378.6 ± 35.6 ppm; elevated temperature, 25.2 ± 0.6 °C and 382.2 ± 35.5 ppm; elevated CO2, 22.9 ± 0.5 °C and 749.9 ± 80.6 ppm and increased temperature and elevated CO2, 25.3 ± 0.6 °C and 763.0 ± 104.6 ppm), adapted from Provost et al. (2016). Current sea surface temperatures were based on average sea surface temperature (± SD) for the Coffs Harbour region during the time of the experiment (21.3 ± 1 °C, Navy Metoc (2015)). Current pH during the experimental period was expected to be ~8.1 (Poore et al., 2013). Future temperature and pH were based on the IPCC (2013) predictions for future oceanic conditions under climate change scenario RCP8.5; approximately +3 °C in water temperature and −0.3 pH units. The temperature and pH of seawater was controlled in twelve, 1100 L circular, fibreglass, outdoor header tanks (1.35 m diameter × 0.9 m high). Sea water was pumped from the adjacent ocean into the NMSC flow-through aquarium system and filtered at 50 μm prior to entering header tanks at 3 L·min− 1. Water temperature in the header tanks was controlled using heater chiller units (Aquahort Ltd., Omana

2.4. Trace element analysis of foot meat For trace element analysis, 1 g samples of whelk foot tissue were submitted to the Environmental Analysis Laboratory (EAL), Southern Cross University (NATA Accreditation Number 14960). Fresh samples of D. orbita foot tissues were dissolved in a mixture of HNO3 (25%) and HCl (75%) (1:3, v/v) and subjected to hot-block (Hot-Block; Environmental Express, South Carolina, U.S.A) according to an acid digestion procedure (APHA, 2012). Elemental concentrations were analysed by inductively-coupled plasma mass spectrometry (ICPMS) using a NexION 300 D series ICP spectrometer with an ESI SC-FAST Auto Sampler (Perkin Elmer, Waltham, Massachusetts, U.S.A.).

R.D. Tate et al. / Journal of Experimental Marine Biology and Ecology 493 (2017) 7–13

2.5. Statistical analyses Hypotheses were tested using multivariate and univariate permutational analyses of variance (PERMANOVA, Anderson (2001)). Similarity matrices were created using Euclidean distance, and 9999 permutations were run for each analysis. Two-factor PERMANOVAs were used to test hypotheses about the influence of ocean warming and acidification on proximate variables and glycogen. Pairwise tests were used to establish patterns among means for response variables with a significant interaction between temperature and pCO2. A third factor, ‘tray’ was nested in the interaction of temperature and pCO2 for shell growth and animal weight analyses. The Monte Carlo method was applied to estimate pvalues for pair-wise tests with b 100 permutations. Trace element data were normalised to the same scale and shell length data was transformed using a log (x + 1) function prior to analysis. Both animal weight and shell length were analysed on the percentage change. The outputs of PERMANOVA analyses can be found in Supplementary Tables S1–S6. Supplementary Table S7 provides mean (± SD) values for water chemistry data. 3. Results 3.1. Survival, growth and consumption No Dicathais orbita died during the experiment, and these animals grew an average of 0.03 ± 1.21% in shell length and lost an average of 2.25 ± 4.43% in wet weight, although there was no significant variation between treatments and the control, nor was a tray effect detected (see Supplementary Table S1). Neither ocean acidification nor ocean warming had a significant impact on the consumption rate of oysters, although, on average D. orbita ate more often under elevated temperature and elevated pCO2 (Fig. 1, Supplementary Table S2). 3.2. Proximate analyses of foot meat Protein content was significantly affected by an interaction between ocean warming and acidification (Fig. 2A). Elevated temperatures significantly reduced average protein content under current pCO2 exposure (pair-wise, p b 0.05, mean change 54%), and elevated pCO2 exposure at 22 °C resulted in a similar reduction in average protein content (pair-wise, p b 0.05, mean change 45%). Moisture content was significantly altered by an interaction between ocean warming and acidification (Fig. 2B). Average moisture content significantly increased in response to elevated temperatures under both current pCO2 exposure


(pair-wise, p b 0.01, mean change 14%) and elevated pCO2 exposure (pair-wise, p b 0.001, mean change 13%). D. orbita foot meat contained significantly greater average moisture content resulting from elevated pCO2 at 22 °C (pair-wise, p b 0.05, mean change 6%), but not at 25 °C (pair-wise, p N 0.05). Both elevated temperature (mean change 20%) and pCO2 (mean change 17%) significantly reduced the average lipid content and no interaction was detected by PERMANOVA (Fig. 2C). Ash content was not significantly affected by either warming or acidification, nor was there an interaction between these factors (Table 1). PERMANOVA outputs can be found in Supplementary Table S3. 3.3. Physiological health indicators from gills Elevated temperature significantly reduced average glycogen content (mean change 35%, Fig. 2D). Elevated pCO2 had no impact on glycogen content (Supplementary Table S3). 3.4. Trace element analyses of foot meat 3.4.1. Macronutrients Neither calcium nor magnesium content was significantly influenced by elevated temperature or pCO2 (Table 1). A significant mean reduction of 8% in potassium content resulted at elevated temperatures (Table 1). Average sodium content significantly increased in response to elevated temperatures (mean change 102%, Table 1). Elevated temperature significantly reduced average sulfur content (mean change 7%, Table 1). Phosphorus content was significantly reduced by elevated temperatures (mean change 11%, Table 1). See Supplementary Table S4 for PERMANOVA results. 3.4.2. Micronutrients There was a significant increase in average boron content at elevated temperatures equating to a mean increase of 51% (Table 1). Manganese content was affected by a significant interaction between temperature and pCO2, although pair-wise tests were not powerful enough to establish significant difference among treatments (Table 1). Nevertheless, there is a trend towards an increase in average manganese content at 25 °C under current pCO2 conditions, whereas under future pCO2 conditions average manganese content is elevated at 22 °C, but not 25 °C (Table 1). There was no significant change to selenium, zinc or acid soluble silicon content (Table 1). Supplementary Table S5 provides PERMANOVA analyses of micronutrients. 3.4.3. Heavy metals There was a significant increase in average copper content by 211% of the ambient controls as a result of elevated temperatures (Table 1). Average lead content under current conditions was 7 ± 3 mg/kg, which experienced a significant mean decrease of 66% as a result of elevated pCO2 (Table 1). Silver, arsenic, cadmium and mercury content showed no significant differences (Table 1). Total arsenic content averaged 226 ± 32 mg/kg overall. See Supplementary Table S6 for further information regarding PERMANOVA results. 4. Discussion

Fig. 1. Mean number of oysters eaten per day per treatment and control by D. orbita (±SD).

Predatory rocky shore invertebrates, such as Muricidae molluscs can be important predators, as well as providing a source of food for human consumption. Many communities around the world rely heavily on marine sources of protein (Cooley et al., 2012) and the pressures on associated fisheries will intensify as human population growth continues (Lloret et al., 2015). As well as increased harvesting pressure, valuable fisheries species are also subject to chemical contaminants (Lloret et al., 2015) and ocean acidification and warming (Tirado et al., 2010). It is, therefore, important that we understand how ocean climate change will impact the energetic reserves and nutritional quality of seafood and attempt to identify potentially robust species. In this regard,


R.D. Tate et al. / Journal of Experimental Marine Biology and Ecology 493 (2017) 7–13

Fig. 2. Mean percentage (±SD) that each proximate variable contributed to D. orbita foot meat, where blue and non-lined bars represent the current temperature and low pCO2 controls, respectively, and red and lined bars represent the experimentally elevated temperature and high pCO2 treatments, respectively. Statistical results as detected by PERMANOVA (n = 3, pair-wise tests where interactions were detected) are described in Section 3.2.

our novel study clearly shows that ocean warming and acidification will likely reduce the nutritional quality and physiological health of D. orbita. In particular, the protein content of the foot meat of D. orbita declined by approximately 45% as a result of an interaction between ocean warming and acidification. Concurrently, moisture content significantly increased in response to these two factors. As a model for other molluscan species sought after for human consumption, the reduced protein content per kilogram would drastically reduce the quality of the meat, while driving up the need for either greater harvests or faster/larger aquaculture production, potentially impacting sustainable supply. The additional reduction in growth rates of many molluscs may compound this reduction in nutritional quality with reduced

meat yield (Doney et al., 2009). Furthermore, as the accumulation of protein stores in the body tissue of molluscs provides energy for growth and gametogenesis (Moussa et al., 2014; Racotta et al., 1998; Rodriguez-Astudillo et al., 2005), the substantial reduction in tissue protein under future ocean conditions could lead to reduced fecundity. If these changes are more general across other seafood taxa, the reduction in seafood quality in response to ocean warming and acidification will influence the capacity of wild fisheries to support future human populations. Lipids are functionally important for reproduction, particularly the production of eggs in molluscs (Napolitano et al., 1992), but are also beneficial for human health. Consistent with a previous study on

Table 1 The percentage of the proximate composition of D. orbita foot meat attributable to inorganic matter (mean percentage ash ± SD) and broken into its constituent trace elements (mean mg/kg ± SD). Statistically significant differences among experimental factors in PERMANOVA analyses are noted. Trace element Inorganic content Macronutrients (mg/kg)

Micronutrients (mg/kg)

Heavy metals (mg/kg)

Ash (% of foot meat) Potassium Sodium Sulfur Phosphorus Calcium Magnesium Boron Manganese Selenium Zinc Silicon (acid soluble) Copper Lead Silver Arsenic Cadmium Mercury

22 °C (low pCO2)

25 °C (low pCO2)

22 °C (high pCO2)

25 °C (high pCO2)



Temp × pCO2

2.4 ± 0.2 9975.7 ± 371.0 11,347.3 ± 1630.6 17,715.7 ± 980.7 4888.0 ± 171.9 3381.7 ± 1926.2 6414.7 ± 1191.3 6.7 ± 0.6 7.2 ± 0.4 2.5 ± 0.4 105.2 ± 63.9 48.3 ± 16.3 12.7 ± 1.7 7.3 ± 3.0 6.6 ± 3.0 219.0 ± 50.1 0.3 ± 0.2 0.1 ± b0.1

2.3 ± 0.1 9253.0 ± 542.5 30,102.0 ± 7806.6 16,742.7 ± 915.7 4129.0 ± 301.8 2687.7 ± 322.8 6716.3 ± 388.3 10.3 ± 1.0 9.9 ± 2.7 3.1 ± 2.7 81.0 ± 5.0 195.0 ± 128.4 89.4 ± 42.5 2.5 ± 2.7 4.1 ± 0.6 259.7 ± 50.1 0.3 ± 0.2 0.2 ± 0.1

2.3 ± 0.1 10,194.0 ± 257.2 17,017.3 ± 1591.9 17,594.7 ± 564.6 4661.3 ± 236.5 4749.0 ± 4414.1 5440.0 ± 1076.6 6.5 ± 0.3 9.9 ± 2.8 3.1 ± 1.0 75.4 ± 2.5 140.7 ± 111.5 37.1 ± 5.9 1.5 ± 0.6 4.3 ± 2.2 240.0 ± 69.6 0.3 ± 0.1 0.2 ± b0.1

2.3 ± 0.1 9220.3 ± 696.0 27,095.0 ± 6313.7 16,207.7 ± 1037.6 4358.3 ± 257.9 2629.7 ± 655.5 5979.3 ± 317.9 9.6 ± 1.3 6.2 ± 0.7 1.6 ± 0.2 78.2 ± 2.7 207.3 ± 92.6 65.1 ± 9.0 1.8 ± 0.8 2.5 ± 1.0 185.0 ± 19.7 0.1 ± b0.1 0.2 ± 0.1

ns b0.05 b0.01 b0.05 b0.01 ns ns b0.01 ns ns ns ns b0.001 ns ns ns ns ns

ns ns ns ns ns ns ns ns ns ns ns ns ns b0.05 ns ns ns ns

ns ns ns ns ns ns ns ns b0.05 ns ns ns ns ns ns ns ns ns

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D. orbita (Valles-Regino et al., 2015), in current conditions the foot meat contained substantial concentrations of lipids (~6% lipid). The lipid content significantly decreased in response to elevated temperature and pCO2, but was nevertheless still high relative to other muricid whelks, which have been shown to contain between 1 and 2% lipid content (Ramesh and Ayyakkannu, 1992; Soufia et al., 2014; Vasconcelos et al., 2009). The foot meat lipid profile of D. orbita is dominated by polyunsaturated fatty acids (PUFAs), particularly Omega-3 PUFAs (Valles-Regino et al., 2015). These PUFAs are considered beneficial for humans as they provide essential fatty acids, carry fat-soluble vitamins, reduce the risk of heart disease, have anti-inflammatory properties and aid in suppressing abnormal heart beats and promoting efficient blood circulation, among other benefits (Simopoulos, 1991; Simopoulos, 2008; Swanson et al., 2012). Similar to many of the response variables we measured, there was a reduction in the proportion of Omega-3 PUFAs in D. orbita flesh after exposure to elevated water temperature (Valles-Regino et al., 2015). Overall, the loss of lipid content reported here, combined with the alterations in the fatty acid profile (VallesRegino et al., 2015), in response to ocean warming reduces the nutritional value of D. orbita for human consumption, and may impact their fecundity, egg production and overall fitness. The proportional increase in moisture in whelk flesh was likely linked to the loss of lipid, and protein content under elevated temperatures, as well as the increased sodium content. Elevated sodium levels have implications for osmoregulation and homeostasis (Voisin and Bourque, 2002), and may increase blood pressure (He and MacGregor, 2002). In contrast, the decrease in potassium content may impact the intracellular ion balance and further impede acid-base regulatory ability (Zarai et al., 2011) of D. orbita, thus contributing to stress. High water temperature reduced glycogen content in the gills of D. orbita. This is likely to be related to the higher metabolic rates of molluscs under elevated temperature requiring more energy for respiration (Miller et al., 2015). As the storage form of glucose, glycogen levels indicate the energy available in a particular structure (Lau and Leung, 2004). Relatively higher glycogen levels are likely to be found in structures allocated to costly metabolic functions such as respiration and reproduction (Lau and Leung, 2004; Santini and Chelazzi, 1995). Glycogen can be a useful biomarker for its sensitivity to a range of stressors (Lagadic et al., 1994; Lucas and Beninger, 1985), and a number of studies have found a significant decline in molluscan tissue glycogen content as a result of different stressors (Ansaldo et al., 2006; Duquesne et al., 2004; Hummel et al., 1996; Leung and Furness, 2001). For example, Li et al. (2007) found a significant drop in mantle glycogen in response to heat stress in oysters (Crassostrea gigas). Furthermore, in oysters that had recently spawned, there was a three-fold reduction in glycogen and no recovery after 10 days in oysters subjected to heat stress (Li et al., 2007). If the glycogen reserves in other vital organs respond to elevated temperatures in a similar manner to the glycogen in D. orbita gills, reproductive success, fitness and survival may be compromised under future climate change scenarios. Under current conditions the copper content of D. orbita foot meat was well below the allowable limits for safe consumption by humans. However, elevated temperature resulted in a large increase in copper content to 89.4 ± 42.5 mg/kg, beyond the 70 mg/kg maximum considered safe in molluscs (NSW Health Department, 2001). In contrast, the average lead content (7.3 ± 3.0 mg/kg) was above the limits for safe human consumption (2 mg/kg lead in molluscs, see Abbott et al. (2003) and ComLaw (2015)) in whelks held under current conditions, likely the result of anthropogenic land uses in and around the study area. The total arsenic in whelk flesh was also high (219.0 ± 50.1 mg/kg), although the dangerous inorganic component is only considered to be approximately 1% of the total arsenic in marine invertebrates, including molluscs (Fabris et al., 2006; Sloth et al., 2005). Nevertheless, this metric still indicates that the levels of arsenic in D. orbita under current conditions are above the safe limits for human consumption (1 mg/kg inorganic arsenic, Abbott et al. (2003) and


ComLaw (2015)). However, people would have to regularly consume large amounts of D. orbita to experience toxicity, and heavy metal bioaccumulation is site-specific depending on local industry (Kılıç and Belivermiş, 2013; Scherz and Kirchhoff, 2006). While arsenic levels stayed high in all treatments, there was a significant drop in lead content of D. orbita foot meat as a result of ocean acidification. These complex results suggest the influence of bioaccumulated metal in marine gastropods will be challenging to predict in future ocean climates. Although survival and growth showed no significant changes, this experiment only covered a 35 day period, which may not be long enough for any physiological deterioration to physically manifest. It is possible that prolonged exposure to future ocean conditions impacts the performance of D. orbita. Elevated temperature (Miller et al., 2015) and elevated pCO2 (Cummings et al., 2011; Pörtner et al., 2004), have been shown to increase metabolic rates, and concurrently energy demand, to cope with the stress (Brown et al., 2004; Li et al., 2007; Miller et al., 2015). Initially, rapid glycogenesis may explain the observed drop in lipid and glycogen content in D. orbita tissue in order to meet this demand under elevated temperature stress. However, the chronic exposure to both elevated temperatures and pCO2 may also result in tissue catabolism, perhaps explaining the reduction in protein content as a result of these stressors interacting with one another. Pörtner et al. (1998) examined the impact of elevated pCO2 on the marine invertebrate, Sipunclulus nudus, in part concluding that metabolic depression related to hypercapnia increased the catabolism of proteins and amino acids. Furthermore, chronic elevated pCO2 exposure may reduce protein synthesis. Overall, ocean acidification and warming resulted in a clear deterioration in nutritional quality and in particular protein content, which may impact the value of whelk fisheries in the future. There are also clear physiological deteriorations in D. orbita tissue that may reflect the impact of chronic, multiple stressors on reserves for growth, survival and reproduction, suggesting that ocean climate change may have greater ecological consequences. While we have only examined these effects in one species, if these patterns are mirrored by other harvested marine molluscs, it may have significant consequences for value of molluscs in future food production. Certainly, this study highlights the need for further research into the nutritional consequences of ocean climate change on seafood quality across broader taxonomic groups, as this may have significant consequences for effective fisheries profitability and production in coming decades. Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.jembe.2017.03.006.

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