Environ Sci Pollut Res (2015) 22:495–507 DOI 10.1007/s11356-014-3333-6


Environmental mercury concentrations in cultured low-trophic-level fish using food waste-based diets Zhang Cheng & Wing Yin Mo & Yu Bon Man & Cheung Lung Lam & Wai Ming Choi & Xiang Ping Nie & Yi Hui Liu & Ming Hung Wong

Received: 25 September 2013 / Accepted: 13 July 2014 / Published online: 5 August 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract In this study, different types of food wastes were used as the major source of protein to replace the fish meal in fish feeds to produce quality fish (polyculture of different freshwater fish). During October 2011–April 2012, the concentrations of Hg in water, suspended particulate matter, and sediment of the three experimental fish ponds located in Sha Tau Kok Organic Farm were monitored, and the results were similar to or lower than those detected in commercial fish Responsible editor: Philippe Garrigues Electronic supplementary material The online version of this article (doi:10.1007/s11356-014-3333-6) contains supplementary material, which is available to authorized users. Z. Cheng : M. H. Wong Key Laboratory for Heavy Metal Pollution Control and Reutilization, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen 518055, People’s Republic of China Z. Cheng College of Resources and Environment, Sichuan Agricultural University, Chengdu, People’s Republic of China Y. B. Man : M. H. Wong Consortium on Health, Environment, Education and Research (CHEER), and Department of Science and Environmental Studies, Hong Kong Institute of Education, Tai Po Hong Kong, People’s Republic of China Z. Cheng : W. Y. Mo : Y. B. Man : C. L. Lam : W. M. Choi : M. H. Wong (*) Croucher Institute for Environmental Sciences, Hong Kong Baptist University, Hong Kong, People’s Republic of China e-mail: [email protected] X. P. Nie Institute of the Hydrobiology, Jinan University, Guangzhou 510632, People’s Republic of China Y. H. Liu Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, People’s Republic of China

ponds around the Pearl River Delta (PRD) region (by comparing data of previous and present studies). Health risk assessments indicated that human consumption of grass carp (Ctenopharyngodon idellus), a herbivore which fed food waste feed pellets would be safer than other fish species: m u d c a r p ( C i r rh i n a m o l i t o re l l a ) , b i g h e a d c a r p (Hypophthalmichthys nobilis), and largemouth bass (Lepomis macrochirus). Due to the lower species diversity and substantially shorter food chains of the polyculture system consisting of only three fish species, the extent of Hg biomagnification was significantly lower than other polyculture ponds around PRD. Furthermore, the use of food waste instead of fish meal (mainly consisted of contaminated trash fish) further reduced the mercury accumulation in the cultured fish. Keywords Food waste . China . Bioaccumulation . Total mercury . Methylmercury

Introduction Food waste is food that is discarded or lost uneaten, and it is a global phenomenon that impacts the environment and society. About one third of all edible food produced for human consumption is wasted globally, which is about 1.3 billion tonnes/ year (Gustavsson et al. 2011). In medium- and high-income countries and areas, food is to a great extent wasted, e.g., per capita food wasted by consumers in Europe and North America is 10–15 times higher than in North Africa and Southeast Asia (Gustavsson et al. 2011). Food waste rotting in landfills produces substantial quantities of methane—a potent greenhouse gas with 25 times the global warming potential of CO2. The food processing and transportation also consume large quantities of freshwater and fossil fuels. Along with CO2 emissions, these impact on climate change (Hall


et al. 2009). Therefore, how to effectively and safely recycle food waste has become a focus of research. Most of the studies dealt with food waste composting (Komilis and Ham 2006; Lee et al. 2004), but attempts have been made to use food waste as feeds in recent years. It has been noted that recycled food waste could partially replace fish meal in fish feeds (Bake et al. 2009) and serve as animal feeds (Sugiura et al. 2009). At present, only limited information is available on the utilization prospects of recycled food waste as an alternative or additional protein source in fish feeds. Furthermore, there is a lack of information on pollutant contents, especially mercury (Hg) of food waste feeds and safety of the aqua-products (farmed fish) feeding by these food waste feeds. There are two main sources (sediment and fish feeds) of Hg to farmed fish from fish ponds. Our previous studies demonstrated rather high concentrations of different persistent organic pollutants (POPs) and Hg in fish reared in fish ponds around the Pearl River Delta (PRD) (Nie et al. 2006; Zhou and Wong 2000) and those purchased in local markets in Hong Kong (Cheung et al. 2007, 2008). Hg concentrations in fish tissues correlated to Hg levels in their ambient environment notably sediment (Zhou and Wong 2000). Sediments could accumulate higher concentrations of Hg from different sources of Hg pollution through atmospheric deposition, urban storm water, and agricultural and industrial runoff entering into fish ponds (Ruddle and Zhung 1988). Sulfate-reducing bacteria can convert the inorganic Hg in sediments into methylmercury (MeHg), releasing through the chemical flux into the water, adsorbed by particulate matter, and then accumulated in fish (Raposo et al. 2008). Fish meal is the major component of fish feeds used in aquaculture, but most of the fish meal may contain high levels of various pollutants such as DDT and Hg (Dickman and Leung 1998; Zhou and Wong 2000). The poor-quality fish feeds seemed to be the major source for Hg accumulated in fish (Cheng et al. 2011; Lacerda et al. 2011). It is commonly observed that Hg can be biomagnified through the food chains and ultimately exert human health risks (US EPA 2000a, b), and therefore food safety and quality have become issues of recent public concern. In most previous studies, MeHg concentrations were used for estimating the human health risks via consumption of fish (Cheung et al. 2008; Shao et al. 2011). Nevertheless, using raw MeHg concentrations to conduct risk assessments usually overestimate the actual health risk because these contaminants were extracted in undigested form from the fish flesh but not in the bioavailable form. Evaluating the health risks by using bioavailable pollutant concentrations is commonly regarded as a more accurate method, because only the bioavailable portion of the contaminants will ultimately reach our bloodstream and exert adverse effects on our body (Brown et al. 1999). Therefore, assessing bioaccessible fractions of

Environ Sci Pollut Res (2015) 22:495–507

pollutants (e.g., MeHg) would be a more suitable alternative in portraying the reality by using in vitro digestion models for conducting risk assessments (Moreda-Pineiro et al. 2011). It is hypothesized that food waste can replace part of the fish meal used in fish feeds to produce quality fish, with a lower level of Hg. The major objectives of the present study were to (1) investigate the variations of total mercury (THg) and MeHg in the experimental ponds in Sha Tau Kok, with food wastes used as fish feeds; (2) analyze bioaccumulations and biomagnifications of these pollutants in the food chains; (3) use in vitro digestion method for analyzing the bioaccessibility of MeHg contained in fish muscle; and (4) assess potential health risks based on digestible MeHg concentrations in fish muscle. The basic data were shared among different members, and Table 1 and 3 were derived from Mo et al. (2014).

Materials and methods Experimental design Field experiments (rearing commercial fish using food waste as feeds) were conducted in Sha Tau Kok Organic Farm in Sha Tau Kok, Hong Kong, China. There were three ponds (20× 10 m) used in this experiment filled up with spring water (depth, 4 m). Every 3 months, 30 % water of the ponds was refreshed with underground water (pH 6.84; dissolve oxygen, 3.99 mg/l; temperature, 21.8 °C) for maintaining the water quality. Bighead carp (BH; Hypophthalmichthys nobilis; 10– 12 cm), grass carp (GC; Ctenopharyngodon idellus) (13– 16 cm), and mud carp (MD; Cirrhina molitorella; 4–6 cm) (all imported from mainland China) were placed in the ponds (1,000 fish fries per pond), at a ratio of 1:3:1 (Chen et al. 2002). GC mainly consumes macrophytes, and also commercial feed pellets and the feed pellets containing food waste. BH is a filter feeder (plankton), and MD is a detritus feeder. They are commonly used to maintain the pond water quality in polyculture ponds (Wong et al. 2004). The food wastes used in present study included food processing (i.e., transformation of raw ingredients into food) waste and partially postconsumption waste collected from local hotels and restaurants. They were classified into four major categories: vegetables and fruits, cereals, meat products, and bones. Fruit waste contained mainly peels with some flesh of various fruits, about 25 % of pineapple, 25 % watermelon, 15 % cantaloupe, and 35 % others (e.g., strawberry, banana, apple, etc.). Meat waste included 60 to 70 % of beef, pork, and chicken and 30 to 40 % of fish such as salmon (Oncorhynchus keta) and grouper (Epinephelussp). Vegetable contained various types of leafy vegetables, such as lettuce and spinach. Cereals usually included rice bran, soy bean meal, rice grain, and spaghetti. All the food wastes collected every day were transferred to a local food waste feed pellets factory (Kowloon

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Biotechnology Limited located in Pak Lai, Hong Kong) for further processing. They were diced into small pieces, with excessive water squeezed out by machines. After drying at 80 °C for 6 h, they were ground into powder to form different food waste products. Different ratios of food waste products were mixed with other raw materials, such as fish meals, and corn starch for pelleting fish feed (Fig. 1). Food waste feed pellets A and B (FW A and FW B) were used in ponds A and B (Fig. 1; Table 1), while commercial feed Jinfeng®, 613 formulated feed, a common fish feed used in aquaculture in PRD and Hong Kong, was used in pond C as a control. All fish were fed twice per day at a fixed feeding rate of 4 % body weight/day for 6 months (October 2011–April 2012). Details about the composite analysis (i.e., lipid, protein, fiber, and carbohydrates) method of experimental feeds are described in the Electronic supplementary material. Sampling During October 2011–April 2012, water, sediment, and plankton samples were collected bimonthly from the experimental ponds. In April 2012, fish samples (GC (n>10), BH (n>10), and MD (n>5) were collected from each pond to compare the Hg bioaccumulation and biomagnification in aquatic food chains of freshwater fish ponds of different cultured models. According to Hg concentration of freshwater fish collected from PRD reported by previous studies (Cheung et al. 2008; Zhou and Wong 2000), four abandoned fish ponds in Hong Kong and three farmed ponds located in the Guangdong province were selected for sampling (Fig. 2; Table 2). Fish samples including BH (n=3), GC (n=8), largemouth bass (Lepomis macrochirus; n= 6), and tilapia (Sarotherodon mossambicus; n=8) were collected from these fishponds, using a nylon net. Fish lengths and weights were recorded (Table 3). The surface sediment samples (0–10 cm, three replicates from each site) were collected using a stainless steel shovel. Commercial fish feeds were also purchased from each sampling site. Sediment and fish samples (muscle, gill, and liver) Fig. 1 Food waste fish feed formulation. Note: Each type of food waste fish feed pellets contains 75 % of food waste (fruit and vegetables, meat products, cereals, bone meal, and others)

were wrapped in aluminum foil, frozen in zip-lock bags at −20 °C, and transported to the laboratory until analyses. Water and zooplankton were sampled at approximately 0.5–1.0 m depth from fish ponds of each sampling site. Water samples were collected from each site in precleaned amber glasses bottles (6 h at 440 °C), acidified immediately with 4 M HCl to pH 10

Abandoned pond Abandoned pond Abandoned pond

Tilapia No No

Hong Kong

added into 30 ml of synthetic gastric juice (2.0 g/l pepsin in 0.15 M NaCl, acidified with HCl to pH 1.8) and shaken at 100 rpm for 2 h at 37 °C. The mixture was then centrifuged (20 min, 37 °C, 3,000 rpm) and the supernatant filtered through a 0.45-mm glass fiber filter. Artificial intestinal juice (30 ml, 2.0 g/l pancreatin, 2.0 g/l amylase, and 5 g/l bile salts, in 0.15 M NaCl, pH 6.8) was added. Then, the mixture was resuspended and shaken at 30 rpm for 6 h at 37 °C. Finally, the tubes were centrifuged at 3,000 rpm at 37 °C for 20 min to separate supernatant and solids and the supernatant was filtered through a 0.45-mm glass fiber filter. The bioaccessibility (%BA) of MeHg was calculated by adding the percentages in stomach and intestinal phase (Oomen et al. 2002).

%BA ¼

BA extracted Hgðstomach phase þ intestinal phaseÞ  100 % Hg concentration in muscle tissue


Bioaccumulation factor Bioaccumulation factor (BAF) and biota-sediment accumulation factor (BSAF) can be obtained from Eq. (1) (Streets et al. 2006; Szefer et al. 1999): BAF ¼ C t =C w


BSAF ¼ C t =C s


where Ct is Hg concentration in the tissues (ng/g dry weight), Cw is Hg concentration in water, Cs is Hg concentration in sediment. Stable isotope analysis The biota samples were analyzed for stable isotopes at the Institute of Soil Science (Nanjing, China), Chinese

Table 3 Growth performance and nutrient utilization in freshwater fish (fed with food waste fish feed pellets and commercial fish feed pellets) from Sha Tau Kok (mean±SD) Grass carp

Bighead carp


Control (n=11)

Length (cm)





















Weight (g)

FW A (n=10)

103±6.52 e


Weight gain (%)

76.4±11.2 f


FW B (n=9)





Control (n=19)

Mud carp







Specific growth rate (%)g






Protein efficiency ratio (%)






FW B (n=25)




Control (n=6)




FW A (n=6)




FW B (n=6)

17.4±5.91 232±104


Feed conversion ratio


FW A (n=21)


Control commercial fish feed pellets, FW A food waste A, FW B food waste B a,b,c,d Means with the same letter in feeding groups are not significantly different according to Duncan’s multiple range test at (p

Environmental mercury concentrations in cultured low-trophic-level fish using food waste-based diets.

In this study, different types of food wastes were used as the major source of protein to replace the fish meal in fish feeds to produce quality fish ...
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