Aug 19, 2016 - The mean value of MeHg concentrations in shark fins of 9 different studies ..... licha), birdbeak dogfish (Deania calcea), leafscale gulper shark.
Methylmercury concentrations in shark fins from the Hong Kong and Chinese shark fin market and related health risks for human consumption by NADJA SOEST August 2016
Submitted as part assessment for the degree of Master of Science (M.Sc.) in
Marine Resource Development & Protection Supervisor: Dr. Mark Hartl School of Life Sciences Heriot-Watt University, Edinburgh
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Abstract More than half of sharks species traded in the shark fin market are threatened with extinction due to overexploitation, while the high demand for shark fin is the main driver for shark mortality. The major shark fin consumer countries are Hong Kong and China, where shark fin soup has a long tradition and is considered as health promoting food. Methylmercury (MeHg) is a very potent toxin that can damage among others the central nervous system, and fertility. The major MeHg source to humans is via seafood consumption while highest concentrations are found in top predators like sharks, tuna and swordfish. The aim of this study was to examine whether health risks of shark fin consumption are severe enough to constitute another argument for consumers to cease or limit shark fin consumption. The mean value of MeHg concentrations in shark fins of 9 different studies has been calculated and used to estimate MeHg exposure for different consumption patterns. 26% of the samples exceeded MeHg safety limits for fish set by the Japanese Health Authority (0.3 mg/kg wet weight). For frequent shark fin soup consumption between once per month and 3 times per week, the US EPA safety limit of 0.1 µg/kg body weight per day were reached by 22-329% (men), 26-988% (women) and 83-3234% (young children). Frequent consumption of shark fins can pose serious health risk, while also less frequent consumption should be seen in the context of additional daily MeHg intake for the populations of Hong Kong and China were average seafood intake is 196g/day and 91g/day respectively. The consumption of shark fins is in particular not recommended for children or breast-feeding women because of the severe neurodevelopmental damages that MeHg can cause in early-life stages. Conservative consumption of sharks and their fins would not only make a significant difference for consumer health, but also for the status of decreasing and endangered shark populations and the marine ecosystem.
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Acknowledgements I would like to thank my boyfriend Thomas, my brother Luca and my friend Katrin for all their patience, support and helpful inputs, and for always making sure that I, totally absorbed from my work, do not forget one of the most important things in life: to live it. Special thanks also to my uncle Eric, who dedicated his limited time to proofread my work, to Dr. Mark Hartl who made it possible for me to continue my MSc programme from Switzerland and for his expert inputs, to Dr. Silvia Frey (OceanCare), who gave me very helpful tips and feedback, and - most importantly - saved my motivation in the last phase of my work. I would also like to thank Stanley Shea (Bloom Asscociation, Hong Kong) for sharing very detailed information about shark fin soup consumption in Hong Kong and for his helpfulness and friendly way of communication. Many thanks also Ran Elfassy (Shark Rescue) and to Yandy (Shark Foundation Hong Kong) for providing helpful tips for my research on shark fin consumption in Hong Kong and China, and to Yann Gilbert who shared the raw data of her study with me.
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I certify that this dissertation is my own work based on my personal investigation and that I have cited all material and sources used in its elaboration.
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Contents 1
Introduction .......................................................................................................................... 6
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Global conservation status of shark species ......................................................................... 9
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Characteristics of shark fin soup, cultural background, market dimensions and trends.... 18
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Global distribution of mercury and bioaccumulation of methylmercury in marine organisms and in the human body...................................................................................... 23
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Biological and ecological factors that influence MeHg concentration in shark tissue ....... 30
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Effects of mercury on human health .................................................................................. 38
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Methods .............................................................................................................................. 47
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Results ................................................................................................................................. 53
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Discussion ............................................................................................................................ 56
References................................................................................................................................... 66 Appendix - List of shark species discussed .................................................................................. 83
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1
Introduction
Shark populations have dramatically declined over recent decades and many shark species are categorized as nearly threatened, vulnerable or endangered on the IUCN Red List (IUCN, 2016). The main driver of declining shark populations is the high demand for shark fins that leads to overexploitation of shark populations. Shark fins are consumed in many Asian countries in the form of shark fin soup, especially in Hong Kong and China where shark fin soup has been a traditional meal since the Song dynasty (960-1279) and where it is still associated with traditional values, health, strength and social status today. A fast growing Chinese economy since the mid 90’s led to an increasing demand for shark fins and other luxury seafood products with the consequence of overfishing of shark populations. In addition, official numbers of the global shark capture production do not include unreported and illegal catches and recent studies estimated that the latter ones make up at least 78% of the global capture production (Clarke et al., 2006b). Apart from the ecological impact, shark fin consumption also has severe impacts on human health, as sharks are top predators and many contaminants, such as heavy metals and organochlorines, biomagnify along the food chain and lead to high concentrations of contaminants in predators on top of the food pyramid. Methylmercury (MeHg) is an organic form of mercury and is of special importance (in general but also in comparison to other forms of mercury) when looking at mercury exposure from seafood consumption. It is very potent neurotoxin, primarily occurs in aquatic systems, and is, due to its lipophilic nature, very easily absorbed in animal and humans bodies. MeHg accumulates in different parts of the body, easily passes the blood-brain barrier and causes severe damages principally in the nervous system, but it also causes impairments of other body functions, for example in the reproductive and cardiovascular system. The main source of MeHg to humans is via seafood consumption. The most famous example of effects of MeHg exposure to humans was the Minamata incident in Japan in 1956, where large volumes of mercury were discharged from a chemical plant into nearby waterways. Consumption of mercury contaminated fish and shellfish led to mercury poisoning of large parts of the 6
population in the area. The poisoning caused different neurological disorders, for example disturbed coordination, impairment of vision speech and motor functions and neurodevelopmental damage in neonatal and children including limb deformations. While there are several studies available that analyse total mercury (THg) and MeHg levels in muscle tissue of different shark species, only a few studies are available that analyse mercury levels in shark fins. In this study, mercury levels in shark fins from 9 different studies have been evaluated, and MeHg levels have been calculated where only THg levels were given. The mean MeHg concentration of all studies was calculated and compared to international safety limits of maximum allowable MeHg levels in shark tissue. The same mean MeHg concentration was used to estimate exposure for different scenarios of consumption frequency and dish sizes and compared to international safety limits for daily intake for men, women and children, based on body weight. Even though mercury levels in shark fins are much lower than in shark meat, 26% of all shark fin samples of these 9 studies exceeded MeHg limits for fish by the Japanese Health Authority (0.3 mg/kg wet weight) and 22% of the samples exceeded the safety limits for THg in shark products of 1 mg/kg wet weight, adopted by the European Union, Australia, New Zealand and Canada. 24% of the samples exceeded the Japanese safety limits for THg in fish (0.4 mg/g) and 26% exceeded the US safety limit of 0.3 mg/g for fish and shellfish. Mean MeHg concentrations of all studies were 0.83 mg/kg dry weight and 0.37 mg/kg wet weight. Exposure estimates based on this mean concentration were below the recommended safety limit by US EPA of 0.1 µg/kg body weight per day, if shark fin soup is eaten 3 times per year or less. Young children may already reach more than 60% of the safety limit if they consume large 150g shark fin portions 3 times a year, not including mercury intake by additional seafood. If consumed once per month, MeHg intake exceeds the safety limits for young children by far, while adult men and women might reach 67-77% of their safety limits, just by shark fin consumption. If shark fin soup is consumed once per week or more often, all three groups reach or exceed safety limits by several factors, even for dishes with small (50g) portions of shark fin. 7
In conclusion, the consumption of large portions of shark fins or the frequent consumption of small portions can have severe health risks. In addition, for the consumption of small portions at a lower frequency it should be kept in mind that small dosages also add to the daily mercury intake, which is already high in populations with high seafood consumption, as is the case for Hong Kong and China. In particular, children, pregnant and breast-feeding women should avoid the consumption of shark fins and other products of high predator fish because of the particular sensitivity of the nervous system in early life stages to mercury exposure. While many studies have examined MeHg levels in shark muscle tissue and a few examined MeHg levels in shark fins, no metastudy was found that combined the results of MeHg in shark fins of different studies to estimate exposure based on different consumption scenarios. The aim of this study therefore was to fill this gap and to examine whether, apart from the ecological aspects, there are also health concerns that would influence consumer behaviour to limit or cease shark fin consumption.
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Global conservation status of shark species
All shark species which were found to occur in the global fin trade by different studies (Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016) are threatened with higher risk of extinction (IUCN, 2016), i.e. they are in the categories ‘near threatened, vulnerable or endangered (Figure 1). The reasons are overexploitation and bad fisheries management in combination with a typically low productivity of most shark species (Clarke et al., 2013; Dulvy et al., 2008; Davidson et al., 2015). The high value of fins is considered to be the main driver of shark mortality (Clarke et al., 2006b; Clarke et al., 2007). Sharks and ray landings increased by 227% between 1950 and 2003, and then declined by 15% between 2003 and 2011. Also, catch sizes decreased significantly (Clarke et al., 2013) which underlines the finding that decreasing populations are not the result of improved fisheries management. An average 81% to 89% decline from the baseline of global elasmobranch populations has been estimated for 2009 (Costello et al., 2012; Dulvy et al., 2008).
Figure 1: IUCN Red List categories; EW: Extinct in the wild; CR: Critically Endangered; EN: Endangered; VU: Vulnerable; NT: Near Threatened (IUCN 2016).
Why are so many shark species listed as threatened with extinction?
The main reason for declining shark landings is overexploitation, either as bycatch or as target species. Different studies found that sharks presented 27% of total bycatch in the Western Pacific (Bailey et al., 1996), 18% in subtropical fisheries (Francis et al. 2001) and 25% of total bycatch in the US Atlantic longline swordfish and tuna fisheries 9
Table 1: Global IUCN Red List Status (IUCN, 2016) of shark species found to occur in the global fin trade by different studies (Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016). Species (scientific name)
Species (common name)
IUCN Status
Alopias pelagicus
Pelagic thresher shark
Vulnerable
Alopias superciliosus
Bigeye Thresher Shark
Vulnerable
Alopias vulpinus
Common thresher
Vulnerable
Carcharhinus brachyurus
Copper shark
Near Threatened
Carcharhinus brevipinna
Spinner shark
Near Threatened
Carcharhinus falciformis
Silky shark
Near Threatened
Carcharhinus leucas
Bull shark
Near Threatened
Carcharhinus limbatus
Blacktip shark
Near Threatened
Carcharhinus longimanus
Oceanic whitetip shark
Vulnerable
Carcharhinus melanopterus
Blacktip reef shark
Near Threatened
Carcharhinus obscurus
Dusky shark
Vulnerable
Carcharhinus plumbeus
Sandbar shark
Vulnerable
Carcharodon carcharias
Great white
Vulnerable
Cetorhinus maximus
Basking shark
Vulnerable
Galeocerdo cuvier
Tiger shark
Near Threatened
Galeorhinus galeus
Tope shark
Vulnerable
Isurus oxyrinchus
Shortfin mako shark
Vulnerable
Negaprion brevirostris
Lemon shark
Near Threatened
Prionace glauca
Blue shark
Near Threatened
Rhincodon typus
Whale shark
Endangered
Rhynchobatus djiddensis
Giant guitarfish
Vulnerable
Scoliodon laticaudus
Spadenose shark
Near Threatened
Sphyrna lewini
Scalloped hammerhead
Endangered
Sphyrna mokarran
Great hammerhead
Endangered
Sphyrna zygaena
Smooth hammerhead
Vulnerable
Squalus acanthias
Spiny dogfish
Vulnerable
(Abercrombie et al., 2005), while (Bonfil, 1997) found similar numbers in target shark fisheries compared to shark numbers of bycatch in tuna fisheries. In the Northern Australian trawl prawn fishery, total bycatch (sharks, rays, turtles, sea snakes and others) is often as high as 75-95% (Brewer et al., 2006; Brewer et al., 1998) with sharks and rays making up about 50% (by quantity) of the bycatch with equal shares (about 25% sharks and 25% rays) (Brewer et al., 2006). In the case that sharks are released after capture and if the appropriate discard practices are followed, they seem to have high chances of survival. A study using satellite tags found that 97.5% of pelagic sharks
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survived capture in longline gear after release (Gilman et al., 2008) and 94% of shortfin mako sharks (Isurus oxyrinchus) were found to survive beyond two months after capture in longline gear after release (NMFS, 2005). Shark mortality can be reduced by turtle excluder devices and bycatch reduction devices (Brewer et al., 2006) in the trawl net fishery or by chemical, electrical, magnetic or electropositive rare earth metal repellents in longline fisheries (Gilman et al., 2008). However, the present use of these devices is limited, and with an increasing value of shark fins and shark meat, shark bycatch is more often retained (Dulvy et al., 2008). In recent years, many shark species have become target species, due to the increasing demand for their fins and meat, and other products like liver oil, cartilage and skin (Dulvy et al., 2008). Shark meat has become more popular as other target fish landings are declining while demand for fish is increasing. For example, Spain, Hong Kong’s most important import partner in recent years, has started to target blue sharks (prionace glauca) for their meat and fins. The meat is sold on the domestic or European market - Spain and Italy are the top shark meat consumer countries in Europe - or it is sold in other international landing ports around the world. The more valuable fins are frozen and shipped mainly to Hong Kong. The bulk of the fin trade is represented by fins of blue shark, oceanic whitetip shark (Carcharhinus longimanus), silky shark (Carcharhinus falciformis), thresher sharks (Alopias spp.) and hammerhead sharks (Sphyrna spp.) (Clarke et al., 2004). Global shark populations would be in a better condition if shark fisheries were wellmanaged, however, despite their high value fins, most fisheries continue to regard sharks as bycatch and not as target species (Clarke et al., 2013). Another reason, why shark fisheries are poorly managed or not managed at all is the lack of data. Catches remain often unreported or underreported, and species are misidentified or unidentified (Clarke et al. 2013). For example only 15% of FAO recorded shark are reported by species (Lack et al. 2006). The near extinction of the angel shark (Squatina squatina) in Europe went almost undiscovered, as they were reported under the same product name as anglerfish (Lophius spp.) and the declining catches of the angel shark were masked by increasing catches of anglerfish (Dulvy and Forrest, 2010). Estimates of real catches, including unreported catches, exceed reported catches by far. Exports 11
of Atlantic blue shark fins are much higher than reported landings (ICCAT, 2005; Campana et al., 2006; Pilling et al., 2008). Furthermore, a study comparing shark fins auctioned on the Hong Kong fin market to trade statistics found that shark biomass represented in the global fin trade is more than 4 times higher than FAO estimates (Clarke et al. 2006b). This lack of data also makes it difficult to assess the impact of overexploitation and to define each species’ conservation status. As a consequence their conservation status might be upgraded to higher categories as soon as more data are available (Dulvy et al. 2008).
Why do different shark species have different conservation statuses?
Sharks are especially vulnerable to over-exploitation as they are so-called K-selected species. This means that their biology and their role in the ecosystem makes them long-lived, slow-growing and late-maturing, with low reproduction rates and - in an environment with limited human impact - with naturally low mortality rates (Field et al. 2009). These characteristics make them highly vulnerable to over-exploitation (Cortés 2002; Fowler & Cavanagh 2005).
Different shark species have different
conservation statuses because of their different demographic resilience and because of different intensities of exploitation for each species (Dulvy et al., 2008). For example, the blue shark and the shortfin mako shark are both heavily exploited for their fins and meat, however the blue shark has a higher productivity, while the shortfin mako shark is less productive, which is one of the reasons why the short fin mako is classified as vulnerable and the blue shark as near threatened. Apart from their global status shark species might have different regional conservation statuses. For example, the shortfin mako is globally classified as vulnerable but classified as critically endangered in the Mediterranean Sea and as near-threatened in the Northeast Pacific, where they are not targeted and where the US swordfish fishery is comparatively well-managed (Taylor and Bedford, 2001). Declining shark populations also have consequences for marine ecosystems, especially if they are a keystone species. Species have a “keystone role” if their abundance
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strongly influences the abundance and diversity of other species in the same ecosystem. For example, sea otter populations in British Columbia and Alaska have a keystone role and influence sea urchin and kelp forest populations. (Watson and Estes, 2011; Estes et al., 1998). Sea otters were extinct in British Columbia waters by about 1850 (Watson and Estes, 2011) as they had been previously overexploited for their fur (Kenyon, 1969). In 1969, 89 sea otters were reintroduced to Checleset Bay, British Columbia and sea otter population of British Columbia increased to 3180 animals in 2001 (Watson and Estes, 2011). Sea otters feed on sea urchins which graze on kelp forest, and the reintroduction of sea otters led to a recovery of the kelp forest in most areas of British Columbian waters. The opposite effect has been reported for declining sea otter populations in Alaskan regions due to increased predation by killer whales, resulting in high sea urchin abundances and a declining kelp forest, (Estes et al., 1998). These effects, when removal of top predators leads to a chain reaction in the food web, strongly influencing abundance of other species, and in this way also ecosystem structure, primary production and nutrient cycling are called “trophic cascades” (Paine, 1980; Terborgh and Estes, 2013). Many other studies have shown that the removal of predators can reduce species richness which can lead to reduced productivity, stability and nutrient cycling (Duffy, 2006; Schmitz et al., 2000; Stachowicz et al., 2007; Worm et al., 2006) and that depleting shark populations can lead to trophic cascades (Stevens et al., 2000; Kitchell et al., 2002; Myers et al., 2007). Simulations of the French Frigate shoals in Hawaii, the Venezuelan shelf and the Alaska Gyre predicted changes in prey species abundances after the removal of sharks (Stevens et al., 2000), while over-fishing of top predator sharks might have led to increasing abundance of cownose rays (Rhinoptera bonasus) in the North Atlantic (Myers et al., 2007). Other studies state that the influence of sharks on diversity and ecosystem structure is still unexplored (Camhi et al., 1998) and that the effects of removing large marine predators from marine ecosystems are not clearly understood for most ecosystems (Bruno and O’Connor, 2005).
A number of different international treaties and initiatives aim to protect threatened sharks species and to prevent further over-exploitation. Annex II ‘List of endangered or 13
threatened species’ of the Barcelona Convention for the Protection of the Mediterranean Sea Against Pollution lists the basking shark (Cetorhinus maximus) and the great white shark (Carcharodon carcharias). Appendix II ‘List of species whose exploitation is regulated’ lists shortfin mako, porbeagle (Lamna nasus), blue shark and angel shark (Squatina squatina). Parties of the Barcelona convention are obliged to provide maximum protection and to support the recovery of listed species in Appendix II and are required ‘to adopt measures to ensure the protection and conservation’ of species listed in Annex II and III (Barcelona, 1995). The relevant protocol (Protocol Concerning Specially Protected Areas and Biological Diversity in the Mediterranean) was signed by 18 Mediterranean member states and entered into force in 2015 (Barcelona, 2013; Barcelona, 2016). The same shark species as in the Barcelona convention are listed in Appendix I and II of the Bern Convention on the Conservation of European Wildlife and Natural Habitats (CETS, 2002a; CETS 2002b), however, the regulations only concern the Mediterranean populations of shortfin mako, porbeagle, blue and angel shark. Appendix I ensures maximum protection and prohibits any taking or killing of the listed species while Appendix II limits the exploitation of listed species. Whale shark (Rhincodon typus), basking shark, great white shark, hammerhead sharks, oceanic white tip shark and manta rays (Manta spp.) are listed in Appendix II of CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora), that lists species for which trade is only permitted with an export permit and a certificate of origin from the state of the member country who has listed the species (CITES, 2016). Great white shark and basking shark are listed under CMS Appendix I (Convention on the Conservation of Migratory Species of Wild Animals), which requires member states to prohibit any taking of these species with very few exceptions. CMS Appendix II lists species with an ‘unfavourable conservation status’ and encourages member states to take actions that benefit the species listed. These include whale, great white and basking shark, shortfin mako, longfin mako, thresher sharks (Alopias spp.), silky shark, scalloped hammerhead (Sphyrna lewini), great hammerhead (Sphyrna mokarran), porbeagle shark and Northern hemisphere populations of the spiny dogfish (CMS, 2014). The convention has 123 parties including the majority of 14
European, South American, African and Middle East countries, Australia and New Zealand. The United States and Canada are not members. The last amendments of the convention (CMS, 2014) entered into force in February 2015. Apart from these international conventions, there are also different regional initiatives and action plans with the aim to improve protection of threatened, vulnerable or endangered shark species. The provisions of these conventions are however not legally binding nor highly enforced (Oceana, 2009). The EU has adopted the prohibition of catches of some shark species into EU law, including basking shark, great white shark, porbeagle and angel shark in EU waters, and of spiny dogfish, tope shark (Galeorhinus galeus), smooth lantern shark (Etmopterus pusillus), great lanternshark (Etmopterus princeps), kitefin shark (Dalatias licha), birdbeak dogfish (Deania calcea), leafscale gulper shark (Centrophorus squamosus), Portuguese dogfish (Centroscymnus coelolepis) and guitarfishes (Rhinobatidae) in specific areas of EU waters (EC, 2015b, Article 44). No such prohibitions or catch limits in form of quotas or total allowable catch (TAC) have been adopted by the European Commission for the other shark species listed in Appendix II of the Barcelona and Bern Convention (shortfin mako and blue shark), and for the shark species listed in Appendix II of the CMS (shortfin mako, longfin mako, thresher sharks, silky shark, scalloped hammerhead, great hammerhead shark). Moreover, even for species where prohibitions of catches or TACs have been adapted into European law, enforcement is absent or inefficient due to very limited monitoring, control and surveillance for chondrichthyans captures and landings (Fowler et al., 2004). Different NGOs claim a lack of enforcement and abundance of loopholes in the legal provisions that aim to protect sharks (Oceana, 2009; Oceana, 2009b; Seashepherd, 2016). The size of seas and oceans makes it difficult to control fishery activities, many governments cannot afford controls and often there is a lack of political will and corruption. For example, the government of Costa Rica received several million dollars for infrastructure investments from Taiwan, ignoring in return the large-scale illegal shark fin trade run by a number of private docks in Costa Rica (Seashepherd, 2016). 15
The EU profits by the lacking policies of other countries as well. The EU has the second largest chondrichthyan capture production in the world (FAO, 2014). EU vessels can fish under bilateral agreements in the waters of developing countries where species are unprotected or less protected and where they can report shark catches as bycatch even if they make up to 80% of their total catch (Oceana, 2009). It has to be kept in mind as well, that policies can only work if enforcement and controls are in place. For example the great white shark, which is the most protected shark species in the world, is still illegally caught, despite its protection status (Shivji et al., 2005; Gilbert et al., 2015). Apart from that, the regulations of conventions are only valid for the parties that signed the convention and are not relevant for non-members. This means that any capture of protected species on the High Seas, where no state has any sovereignty rights and where no state has the right to create any regulations for another state, unless it is in a form of a convention, and in that case it only has to be respected by the parties who signed the convention. However, despite these difficulties, a number of species recovered with the help of strict management regulations. For example, white shark populations in California recovered after their taking was prohibited in 1994 (Burgess et al. 2014) and spiny dogfish populations increased after catch quotas had been introduced in the United States (COSEWIC, 2011). Seven West African countries (Dulvy et al., 2014) and four South American countries (Gomez, 2008) implemented regional action plans for shark and ray fisheries management, which did not introduce any catch quotas or legal bindings, but improved landing records, public awareness and improved cooperation with international conservation efforts. Finning bans have been recently introduced by several countries. Their aim is to prevent the cruel and wasteful finning of sharks and the disposal of the live shark carcass at sea. The enforcement works by defining a maximum fin to carcass (i.e. normally the gutted body of the shark excluding fins and head) ratio that is permitted to be landed. This measure aims to reduce the cruel act of finning of live sharks, however it does not reduce shark mortality (Clarke et al., 2013).
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The International Commission for the Conservation of Atlantic Tunas and tuna-like Species (ICCAT) introduced a prohibition to retain bycatch of oceanic whitetip and silky sharks. This measure has bigger potential to reduce shark mortality compared to finning bans, however, in a study about the Atlantic long-line fishery, 69% of silky sharks did not survive despite release. Clarke et al. (2013) criticizes such prohibitions as they take away the focus from on-board-handling practices, that would improve postrelease survival rates, and from the fact that sharks are an economically valuable target species that should be sustainably managed. In addition, sharks are less likely to be recorded if their catch is prohibited. Future recommendations of different studies are therefore an improved management of shark fisheries with introduction of catch quotas and improvement of bycatch handling techniques.
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Characteristics of shark fin soup, cultural background, market dimensions and trends
Shark fin soup has a long tradition in China and is a symbol for health and good fortune. Different media and an the San-Francisco-based NGO WildAid have reported strong declines of about 70% in the demand for shark fin in the last years, claiming public awareness campaigns to be the main reason (Tsui, 2013; Duggan, 2014; Wild Aid, 2014). However there is scientific evidence that these numbers are overestimated and market declines are much smaller. The high demand for shark fin is still the main driver of the global shark capture production. Shark fin consumption has a long history dating back to the Song dynasty (960-1279) where it became popular as a delicacy (Freeman, 1977). During the Ming Dynasty (1368-1644), it became part of imperial banquets (Rose, 1996). Until the 1990s, shark fin was mainly consumed in the southern Chinese provinces of Hong Kong, Beijing and Shanghai (Clarke, 2007; Li, 2007). Shark fin soup is a luxury food product and the rapid growth of the Chinese economy since the 1990s led to an increasing number of seafood and luxury seafood consumers (Fabinyi, 2012). Shark fins have kept their popularity in China and other Asian countries until today, where they mainly stand for tradition, health and status. In a survey undertaken in Hong Kong, people indicated the main reasons for eating shark fin soup to be tradition (52%), taste (51%), texture (40%), health (27%) and status (19%) (Bloom, 2015). In terms of their health symbolism, it is important to understand the origins of their health aspects in Traditional Chinese Medicine (TCM). They form part of the bu foods which are considered as ‘strengthening or tonic-like’ (Anderson 1988; Simoons 1991; Newman 2004). Apart from that, there is a connection between bu foods and wild foods as these are considered ‘unpolluted’, ‘precious’ and ‘special’ (TRAFFIC, 2010) and therefore ‘more bu’ compared to non-wild foods. Bu foods are also considered to promote sexual potency and virility (Anderson 1988) and are for this reason more popular among men than women (Zhang et al. 2008; TRAFFIC, 2010). For the same
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reason wild caught reef fish sells in China for much higher prices than cultured fish (Vincent 2002). Apart from their health symbolism, consumption of shark fins reflects social status. Shark fin soup is an expensive dish, often found in Chinese upper-class restaurants. It is mainly consumed on special occasions like wedding and birthday banquets, family reunions, New Year, corporate events, festivals and friend gatherings (Bloom/SSRC, 2015). In some social circles, not serving shark fin is considered as equal to admitting to be poor (Watts, 2001). According to an internet blog by Wild Aid conservation photojournalist Alex Hofford, shark fin soup has become much more affordable in recent years and is also available in buffets and all-you-can-eat menus of simpler restaurants, with prices in the range of 10 to 40 USD instead of the usual prices of 100 US$ or more (Hofford, 2009). Regarding shark fin soup some information sources have to be carefully re-evaluated, as it seems to be a sensitive and emotional topic for the main consumer countries, who want to defend their tradition, believes and their global image as well as for environmentalists who fear the cruel treatment of sharks and a near extinction of a number of species. However, this blog seems reliable as it provided photographs of the restaurant menus that were discussed.
The price range can be explained by the amount and quality of fins added to the soup. (Hausfather, 2004). For most traders, the size of the fin is more important than the species in terms of pricing (Eilperrin, 2011). Other sources list some shark species with large fins, for example thresher sharks (Alopias spp.), whale shark and basking shark only in the ‘third choice’ category (Vannuccini, 1999). The reason might however be a lesser suitability of the fin texture, as this is another important criterion. The selection of species that occur in the fin market is rather small, with only 14 species representing 40% of the Hong Kong fin market, of which blue shark alone makes up 17% (Clarke et al., 2004). According to records from the Hong Kong fin market, the most important fin market in the world with a global share of about 52% (1996-2000), preferred fin types are the first dorsal (Figure 2), pectoral and lower caudal lope fins (Clarke et al., 2006b) due to
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their higher amount of fin needles which are important for the texture of the soup (Vannuccini, 1999).
Figure 2: Body parts of a shark (Source: Wikipedia, drawing by Chris Huh).
Before being sold on the market, shark fins are usually processed. They are soaked in water and heated in order to soften the denticles and skin, which can then be easier removed. After that, the fins normally undergo a bleaching process, either through smoking with sulfur for a couple of hours or by a short treatment with hydrogen peroxide which will give them a more demanded whitish colour. The fins are then either sold as ‘wet fins’ or sundried and sold as ‘dry fins’ (Vannuccini, 1999). For the making of the shark fin soup, either wet fins are used or dry fins which are soaked into water before the preparation of the soup. The fins are the most important ingredient of the soup, but rather in terms of symbolism than flavour. As the fins themselves do not add any flavour to the soup (Pamela, 2015), many other ingredients are added, for example chicken, pork, ham, crab meat or eggs and spices (Singapore Food Recipes, 2012; Pamela, 2015). In the further process, all the ingredients are cooked in chicken stock for about six to eight hours (Pamela 2015). Information about how much shark fin is used per portion of shark fin soup is scarce. In an online recipe for the preparation of shark fin soup at home, 300g of shark fins were used, however without an indication of the number of servings (Singapore Food
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Recipes, 2012). Much larger portions of 150g of shark fin per serving can be found in restaurants as well (Man et al., 2015). Shark fins are consumed in several Asian countries, with China being the world’s leading consumer market, followed by Hong Kong, Japan, Malaysia, Singapore, Taiwan (FAO 2015) and South Korea (Kim et al., 2016). Reliable numbers of sharks globally traded in the fin trade are difficult to find, as large numbers of catches are illegal or remain unreported. The use of customs data has also become more difficult. First of all, information from Chinese customs records is unreliable (FAO, 2015), and second, a worldwide change in custom commodity codes in 2012 resulted in shark fins being recorded as shark meat in the trade statistics (Erikson and Clarke, 2015). As a result, even the reported and legal part of shark fin capture production does not appear anymore as a separate unit in import and export statistics, not only for China, but also for Hong Kong. One study has estimated the real dimension of the fin market by genetic identification of shark fins found on the Hong Kong market. Recordings of species and numbers of different fin positions, information from local traders, Hong Kong trade statistics and FAO records of shark capture production data were combined and statistically evaluated. The annual number of sharks caught for the global fin trade was estimated to be 26-73 million, with a median of 38 million, corresponding to 1.7 million tons of shark biomass. These numbers were more than four times higher than the FAO estimate of 0.39 million tons (Clarke et al., 2006b). WildAid had launched a campaign for public awareness on shark finning, and claimed that shark fin consumption had fallen by 70% in 2012 (Wild Aid, 2014) supported by media reports (e.g. Tsui, 2013; Duggan, 2014). A study from 2015 discussed that demand of shark fins did decrease but not to such a large extent and mainly because of other reasons than conservation concerns (Eriksson and Clarke, 2015). A decline of 50% can be seen in the official trade statistics, however, this was mainly influenced by the aforementioned change in customs commodity codes in 2012. Recalculation of trade volumes using this information resulted in a decline of imports by 22% in 2012 from the 2008-2010 average.
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Actual declines in fin trade volumes were also influenced by a campaign of the Chinese government that banned certain luxury seafood products including shark fin soup at official government banquets as part of an anti-corruption campaign. Shark fin demand was also negatively influenced by increasing media reports about incidents where artificial shark fin has been sold as real shark fin. Import numbers of shark fins along with chondrichthyan capture production (sharks, skates, rays and chimaeras) (FAO, 2014b) are also believed to be decreasing due to overfishing (Dulvy et al. 2008; Field et al. 2009; Clarke et al. 2013; Davidson et al., 2015). A media report about a survey by the Hong Kong Shark Foundation confirmed the assumptions that the decrease of shark fin consumption might not be as significant as reported, by stating that shark fin soup is still served in 98% of Hong Kong restaurants, and that the foundation had expected the number to be much lower due to several conservation campaigns and decreasing consumption trends reported in recent years (Karacs 2016).
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4
Global distribution of mercury and bioaccumulation of methylmercury in marine organisms and in the human body
Mercury is emitted from natural as well as from anthropogenic sources, such as fossil fuel consumption and gold mining. Mercury concentrations in the atmosphere and in the environment increased dramatically with industrialization. Mercury exists in different forms and the most toxic form, also the most relevant form in seafood consumption, is MeHg as it is a severe neurotoxin, lipophilic and therefore highly absorbable by animals and humans. It tends to accumulate and biomagnify along the food chain and makes up 72-100% of total mercury in fish (Storelli et al., 2001). Mercury naturally occurs in geologic deposits and in the atmosphere. In geologic formations, it occurs in particularly high concentrations in the areas of mercuriferous belts, which are associated with tectonic plates. Mercury stored in geologic formations can be released into the atmosphere by volcanoes, geothermal vents, erosion, volatilization or by forest fires (Jitaru and Adams, 2004) (Figure 3). Apart from natural processes, mercury is released by a number of anthropogenic processes, mainly fossil fuel combustion (for power generation), mining of mercury and other elements, especially gold mining, waste incineration and by industrial processes, for example fertilizer production (Stein et al., 1996). Combustion processes release mercury into the atmosphere, and its high volatility results in long residence times in the atmosphere and transport over long distances (Jitaru and Adams, 2004). Mercury is used for electrical products (e.g. batteries and lamps), thermometers, in the chlor-alkali-production, and for the production of fungicides, herbicides and fertilizers. In industrial processes it is most often released into the environment by leakages, waste-water discharges or improper disposal of products. Anthropogenic release of mercury into the atmosphere has been happening for centuries, but only the industrial revolution led to serious increases of mercury in the atmosphere. Anthropogenic mercury emissions are estimated to make up 75% (Barkay et al., 2003) of the total mercury emissions. The largest sources are fossil fuel plants for power generation and gold production (Figure 4).
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Figure 3: Mercury cycle (Source: Open Computing Facility, University of California, Berkeley).
Fossil fuel combustion made up 45% of total global emissions in 2008, with 880 tons out of 1930 tons of total mercury emissions and is considered to be the major source of anthropogenic mercury emissions (Liu et al., 2012; AMAP/UNEP, 2008). More recent figures show that artisanal and small scale gold mining (ASGM) is the largest source of anthropogenic mercury emissions, with 700 tons discharged yearly into the atmosphere and additional 800 tons of mercury released into water bodies and land (AMAP/UNEP, 2013). Mercury occurs in three major forms: Elemental mercury (Hg0) in both liquid and gaseous states, inorganic mercury (mainly occurring as salts of Hg2+ and Hg+) (Risher, 2003) and as organic mercury, for example methyl mercury (MeHg or CH3Hg+) or phenylmercury (C6H5Hg+) (Morita et al., 1998). All of these forms are toxic, but they lead to different types of exposure and vary in their toxicity and adverse health effects. Hg0 is predominant in the atmosphere (about 95% of total mercury) in its gaseous form (Pirrone and Mahaffey, 2005) and exposure to Hg0 occurs via inhalation. It is chemically
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Figure 4: Annual global anthropogenic emissions in tons (Liu et al., 2012) with data from (AMAP/UNEP, 2008). Fossil fuel combustion refers to power plants including residential heating. Metal production includes mercury mining and production but not gold mining and production.
very stable and can stay in the atmosphere from 2 months up to 6 years and thus can be transported and distributed globally (Pirrone and Mahaffey, 2005). Looking at mercury exposure from seafood consumption, only the inorganic and organic forms of mercury are relevant, because these occur in aqueous systems and can be absorbed by marine animals via ingestion, and in smaller parts via the gills and skin. MeHg is especially relevant, as it is, in contrast to inorganic forms, very efficiently absorbed and accumulated in the body and along the food chain due to its lipophilic (fat-soluble) character. As a result, it is the predominant form of mercury found in fish making up about 72-100% of total mercury in fish (Storelli et al., 2001). In addition, it is able to cause severe damages to the nervous system. MeHg is formed within the chemical cycle of mercury. Hg0 from the atmosphere reaches land and water surfaces by wet or dry deposition. In water, mercury only occurs as inorganic mercury (mainly Hg2+) or organic mercury (mainly MeHg). Hg2+ is formed by oxidation of Hg0 at the water surface due to the high chloride concentration in water which promotes the oxidation reaction. Hg2+ can be reduced to Hg0 again and 25
released back into the atmosphere or it may be absorbed by organic particles or organic matter (Ullrich et al., 2001) and precipitate with the particles to the seabed. Once in the sediments, it may bind to sulfide groups to form mercury sulfide (HgS) and be stored in the sediments in this non-bioavailable form. Alternatively Hg2+ can bind to organic alkyl groups and in this way form organic mercury, with MeHg being the most common form. This process is called mercury methylation (Stein et al., 1996). MeHg can be formed by abiotic and biotic processes, but it is primarily produced by anaerobic sulfate-reducing bacteria in the sediments (Mason and Benoit, 2003). The resulting organic mercury compound is highly lipophilic, which facilitates its transport into the cells of organisms, and is one of the reasons why MeHg is so toxic. Without methylation, mercury would be stored in the sediments, not being bioavailable to any marine organism. The sulfate reducing bacteria however turn it into a highly bioavailable form and in this way turn the sediments from a mercury sink into a mercury source (Gochfeld, 2003). MeHg is taken up from the water column by marine organisms at lower trophic levels and bioaccumulates in their tissues, and as it is difficult to eliminate by the body, the uptake rate is usually higher than the excretion. When these organisms are eaten by marine organisms of higher trophic levels, mercury is transferred from the prey to the predator. As organisms of higher trophic levels need to consume more biomass in order to survive, their intake of mercury is higher. In this way, the concentration of mercury in the body tissue increases along the food chain, a process called biomagnification. Francesconi and Lenanton (1992) found mean MeHg levels of 0.002 µg/g in macroalgae, 0.01 µg/g in seagrass, 0.05 µg/g in echinoderms, 0.09 µg/g in polychaetes, 0.14 µg/g in molluscs, 0.25 µg/g in crustaceans, 0.46 µg/g in smaller fish species and 2.3 µg/g in large predatory fish. These findings confirm that organisms of higher trophic levels usually have higher mercury concentrations in their tissue. Apart from the trophic position of an animal, also its ages plays an important role, as exposure time and accumulated MeHg increase with age. MeHg uptake by marine organisms of higher trophic levels does not only work via ingestion but also via the skin and gills (Olson et al., 1973; Phillips and Buhler, 1978; Kudo and Mortimer, 1979; Klinck et al., 2005). However the water column only contains small amounts of MeHg, and 26
the uptake via ingestion is about a seven fold higher compared to direct uptake from the water column (Monteiro et al., 1996). Of ingested mercury 95% is absorbed (Clarkson, 2002) by the digestive system and distributed to other parts of the body through the circulatory system. Its lipophilic character facilitates its transport through cell membranes and the blood brain barrier. For Hg2+ it is more difficult to cross the blood brain barrier and it mainly accumulates in the liver and kidney, where it is broken down and excreted from the body. Possible health implications of Hg2+ exposure are damage to the gastrointestinal tract or to the kidneys including kidney failure (Hać et al., 2000). Several studies examined the distribution of THg in different body tissues of sharks. In demersal shark species from Australia, the highest THg concentrations were found in the muscle tissue (1.49 g/kg wet weight), followed by the liver (0.93 g/kg) and kidney (0.63 g/kg), and the lowest concentrations in the skin with 0.21 g/kg (Pethybridge et al., 2010) (Table 2). In a study of Hg concentrations in dusky (Carcharhinus obscurus), sandbar (Carcharhinus plumbeus) and great white sharks from southeastern Australia, Gilbert et al. (2015) found the highest concentrations of THg in liver and in muscle tissue, and only small amounts in fins (Table 2). Table 2: Total mercury (THg) in g/kg in tissue types of different shark species. Species Dusky shark Sandbar shark Great white shark Spiny dogfish Shortnose Spurdog Shortspine Spurdog Silky shark Bonnethead shark Porbeagle shark
Scientific name Carcharhinus obscurus Carcharhinus plumbeus Carcharodon carcharias Squalus acanthias Squalus megalops Squalus mitsukurii Carcharhinus falciformis Sphyrna tiburo Lamna nasus
dry weight/ wet weight
Muscle
Liver
dw dw dw ww ww ww dw dw ww
8.5 6.71 9.71 0.64–1.45 0.75–0.79 2.83–3.23 2.61 3.1 0.84
11.59 37.87 0.86 0.61–0.83 0.38–0.70 2.83–3.23 2.1 1.82 0.06
Kidney
Skin
Fin
Upper caudal fin
0.07 0.02 0.09 0.28 1.35–1.63 0.66 2.15
Reference (Gilbert et al., 2015b)
0.12–0.18 0.03–0.1 0.14
(Pethybridge et al., 2010)
0.02 0.04
0.98 0.68
(O’Bryhim, 2015) (Nicolaus et al., 2016)
The fact that Hg concentrations were greater in liver tissue than in muscle tissue for dusky and sandbar sharks, but not in white sharks, can be explained by the correlation between body distribution of metals and metalloids and age or growth, as it has been found by Endo et al. (2008) for tiger sharks (Galeocerdo cuvier). Concentrations in liver tissue increased rapidly after reaching and during maturity in sharks in both studies (Endo et al., 2008; Gilbert et al., 2015) and can be explained by age-related changes in diets in combination with slower growth rates (Endo et al., 2008). In juvenile sharks, 27
faster growth rates caused dilution effects in the ratio of body weight to mercury concentration. Liver concentrations in great white sharks were lower in relation to muscle tissue concentrations because all of the white sharks in the study were juveniles (Gilbert et al., 2015). O’Bryhim (2015) found highest THg concentrations in the muscle tissue of bonnethead sharks (Sphyrna tiburo) and silky sharks from the Atlantic Coast of Florida, followed by the kidney and liver, with lowest concentrations in the fins. The highest THg levels among the different fin types were found in the upper caudal fins (Figure 2) which the authors explained by a higher concentration of muscle tissue in this type of fin. While muscle tissue contains mainly MeHg (Storelli et al., 2001), shark liver has been found to contain primarily inorganic mercury (Branco et al., 2007; Nam et al., 2011). This is because MeHg is believed to be demethylated by binding to selenium and to be converted into inorganic mercury, which facilitates the excretion of MeHg (Nam et al., 2011). However, for this detoxification process, a selenium-mercury molar ratio of at least 1:1 is necessary. Below this ratio, MeHg continues to accumulate in the liver and in other organs (Das et al., 2000; Storelli and Marcotrigiano, 2002; Endo et al., 2002; Endo et al., 2006) and because of this high THg levels in liver tissue might indicate that the organism did not have high enough selenium levels in order to break-down and excrete mercury. The global distribution of anthropogenic mercury emissions (Figure 5) shows areas which are expected to have higher mercury concentrations in the environment and in food sources. Asia causes more than half of the global mercury emissions and China’s rapid economic growth made it the leader in mercury emissions (Jiang et al., 2006; Zhang and Wong, 2007) with one third of global mercury emissions in 1999 (Streets et al., 2005). Many developing countries have such a large share in mercury emissions because they lack control measures and mitigation technologies, e.g. flue gas cleaning and emission controls (Cheng and Hu, 2011). Another reason is that the manufacture of many consumer products for the rest of the world, especially Western countries, has been outsourced to China, which has to supply the energy (mainly fossil fuels) for these 28
processes. Apart from fossil fuel combustion, gold mining is an important source of mercury emissions (Li and Tse, 2015). Even the levels of mercury in the atmosphere in China are much higher than the global average and deposition from the atmosphere to soil and water surfaces is three times greater compared to the global average (Cheng and Hu, 2011), resulting not only in higher contamination of seafood but also a higher contamination of rice (Li and Tse, 2015). There are many other mercury hotspots worldwide; for example, in the Czech Republic (chlor-alkali chemical factories with two plants located close to the liver Labe that drains into the North Sea), in Russia (chlor-alkali facilities with direct release into the atmosphere and into the Volga river that flows into the Caspian Sea) or Albania (a chlor-alkali plant that was in operation from 1967 to 1992). In Tanzania, artisanal and small-scale gold mining (ASGM) causes direct mercury discharges into the atmosphere and into the Lupa River, which borders a large game reserve in Uganda. ASGM in Indonesia is also operated by many private households, with direct discharges into the atmosphere and nearby waterways. A chlor-alkali plant in Mexico discharges into the Coatzacoalcos River that flows into the Gulf of Mexico (Evers et al., 2013).
Figure 5: Global distribution of anthropogenic mercury emissions in 2010 reproduced by (Deborah, 2013) using data from (AMAP/UNEP, 2013).
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5
Biological and ecological factors that influence MeHg concentration in shark tissue
Mercury levels vary a lot, even between species in the same studies. There are multiple factors that influence accumulation of mercury in sharks, such as body length, age, feeding habits, trophic position, reproduction mode and geographical factors. There are currently no available studies in the available literature which examined correlations between MeHg levels in shark fins and these factors. Therefore, correlations are discussed based on the findings of studies examining MeHg in muscle tissue.
Body Length Most studies that examined the correlation between mercury levels in shark tissue and body length found a positive correlation. For blacknose, blacktip, and sharpnose sharks from Southwest Florida, intraspecific variation in Hg concentrations could be related to total length (Rumbold et al., 2014). In a study with 17 shark species from the South African East Coast, total intraspecific length was found to be the dominant factor for THg levels in muscle tissue (McKinney et al., 2015). Maz-Courrau et al. (2011) examined 68 samples of blue, short fin mako, silky and smooth hammerhead (Sphyrna zygaena) shark at the Pacific and Gulf Coast of Baja California, Mexico and found a positive relationship between size and mercury concentrations for all species except blue shark. This exception can be explained by other factors like feeding habits, metabolism (Maz-Courrau et al., 2011), and is explained later in this chapter. In 16 demersal shark species from Southeast Australia Pethybridge et al. (2010) found higher mercury concentrations in the muscle tissue of larger and supposedly older individuals. Several other studies found similar patterns (Walker, 1976, 1988; Taguchi et al., 1979; Hueter et al.,1995).
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Body length, however cannot be regarded as an independent, isolated factor. Body length, age, trophic level and also feeding habits that vary with age are dependent factors, i.e. they influence each other. The typical correlation between mercury concentrations and size (body length or weight) in fish, is caused by the fact that mercury bioaccumulates with age (Boudou and Ribeyre, 1997; Driscoll et al. 2013). Therefore it is difficult to define which of these factors has the most influence on mercury accumulation for a specific species. McKinney et al. (2015) found that the correlation between mercury levels and body length was significant for most of the sharks in the study. Missing correlations for the smooth hammerhead sharks could be explained by the fact that all smooth hammerhead sharks in the study were juveniles. In most available studies, influences of different factors were found. For example, McKinney et al. (2015) could relate interspecific and intraspecific variations of mercury levels to body length, as the dominant factor (age was not assessed) and to tropic position and feeding habits.
Age and growth rate The correlation between age and mercury levels is not only influenced by a longer exposure time and the fact that mercury accumulates with time, but also by the fact that sharks have different diets in different life phases. For example neonate and juvenile sharks were found to have a higher percentage of crustaceans in their diet compared to adult sharks (Medved et al., 1985; Bornatowski et al., 2014). Older (larger) sharks usually prefer prey of a higher trophic level, or their habitats are different than those of younger (smaller) sharks (Cortés, 1999). This also means that where increasing mercury levels are found to correlate with body length or age, the underlying reasons for higher mercury levels could also be changes in foraging habitats or trophic position (Rumbold et al., 2014). Some studies also connected mercury levels to age-related growth rates. In a study of five demersal sharks from Brazil, young sharks had lower mercury levels compared to adult sharks and the authors speculated that, apart from shorter exposure times, the
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greater growth rates of juvenile sharks might be an additional factor for the low mercury levels (de Pinho et al., 2002). In life stages with faster growth rate, mercury might be rather diluted than accumulated. A study from Mexico about mercury in top predator fish did not find any mercury-length correlation in some species and attributed this to their moderate to rapid growth rates compared to the slower growth rates of other species in the same study (García-Hernández et al., 2007). In tiger sharks in a study from Japan, an exponential increase of mercury levels was observed at about 270 cm body length. The authors concluded that this phenomenon was the result of continuous mercury intake at a slowing growth rate at the start of maturity (Endo et al., 2008).
Trophic position Trophic level and related diet and ecology, are some one of the most important factors for different interspecific metal concentrations (Vas & Gordon, 1993; Turoczy et al., 2000; Pethybridge et al., 2010). For 17 shark species of South Africa, trophic position and body length explained most of the interspecific variations in Hg levels (McKinney et al., 2015). Pethybridge et al. (2010) found low mercury levels in species from lower trophic levels. However, as with all factors that influence mercury levels in shark body tissue, other factors can still have a stronger influence. For example, Pethybridge et al. (2010) also found low Hg levels in the sevengill shark (Notorynchus cepedianus) which had low Hg levels despite its high trophic position.
Feeding habits Feeding habits were found to be a significant factor apart from body length for 17 South African shark species (McKinney et al., 2015). High THg levels were found in ragged-tooth, Java, and white sharks which preferentially feed on teleost fish and other chondrichthyans. The lowest THg levels were found in smooth hammerhead, spinner (Carcharhinus brevipinna) and tiger sharks which preferably feed on cephalopods or teleosts and/or reptiles (Cortés, 1999). Species which feed on 32
cephalopods and crustaceans mainly accumulate cadmium (cephalopods) and arsenic (crustaceans) instead of mercury compared to piscivorous species (Bustamante et al., 1998; Storelli and Marcotrigiano, 1999; Storelli and Marcotrigiano, 2000). For especially high THg levels found in scalloped hammerhead shark, the authors explained that apart from other factors like body length and trophic position and prey items, their habit of foraging at greater depth would be an additional important factor. Pethybridge et al. (2010) found higher mercury concentrations in deep-demersal species of 16 demersal sharks from Australia and attributed this finding to the fact that they forage in deep-sea environments which are a sink for contaminants (Tatsukawa and Tanabe, 1984). Moreover, deepsea sharks are longer-lived, and have higher trophic positions than shark species living in shallower waters. Maz-Courrau et al. (2011) found highest THg levels in silky shark, an epipelagic predator that is typically found in coastal areas, compared to lower levels in blue shark, which has pelagic feeding habits. Mercury contamination tends to be higher in coastal areas with a higher abundance of anthropogenic mercury sources, which causes coastal prey species to be particularly exposed.
Geographic Location Despite sharks being highly migratory species, several studies found correlations between the areas where sharks were caught and their mercury levels. Maz-Courrau et al. (2011) found average mercury concentrations in samples of smooth hammerhead sharks of the Pacific coast of Mexico to be about ten times higher than those from a Mediterranean study (Storelli et al., 2003). THg concentrations in South African sharks were higher than in their conspecifics from the North-east Atlantic coast (US), North Pacific (US, Japan, Mexico) and South Pacific (Australia, Chile, Papua New Guinea) (McKinney et al., 2015). However, THg levels were lower compared to the same species from the Mediterranean Sea. Mediterranean fish of higher trophic levels have particularly high Hg body burdens, which are believed to be the result of lower growth rates and greater Hg bioavailability due to higher mercury emissions in the area (Cossa et al., 2012). However, the same authors found similar levels of MeHg 33
when comparing the Mediterranean Sea, with the Tasmanian margin and the Celtic Sea (Cossa et al., 2008), two regions where lower mercury levels in sharks have been reported compared to the Mediterranean Sea (Pethybridge et al., 2010). It has to be considered that, apart from local mercury emissions, other factors, such as a different food web structure, growth rates could be the reason for high Hg levels in shark tissue (Gilbert et al., 2015). García-Hernández et al. (2007) found similar levels in smooth hammerhead sharks of the Gulf of California (Mexico) compared to smooth hammerheads of the Mediterranean Sea. The peninsula of Baja California Sur, to the west side of the Gulf, is considered to be an unpolluted pristine region with little mercury emissions by several authors that undertook studies of mercury levels in sharks in this area (Maz-Courrau et al., 2011; Escobar-Sánchez et al., 2011; Barrera-García et al., 2012). One of these authors underlines that higher mercury concentrations in this region could be caused by natural Hg sources including hydrothermal vents associated with the presence of the San Andres Fault (Barrera-García et al., 2012). High mercury levels in South African sharks, compared to conspecifics from other regions can be explained by the proximity of their feeding habitats to South African regions with high mercury emissions or discharges (McKinney et al., 2015). For example, a mercury processing plant in the region of KwaZulu-Natal has been reported to discharge mercury into adjacent waters in 1990 (Papu-Zamxaka et al., 2010). Moreover, South Africa’s energy supply is exclusively covered by coal power plants.
Sex and maternal transfer Shark species have different ways of reproduction. Some are viviparous, i.e. they give live birth. Viviparous placental species, for example mothers of hammerhead sharks (Sphyrna spp.) or blue sharks have a placental connection to their embryos for the entire gestation period (Balon, 1975; Dulvy and Reynolds, 1997). In Blacktip sharks (Carcharhinus limbatus) (viviparous), the placental connection to their embryos is only established after the first 8 weeks of gestation. In the first weeks of gestation, embryos
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are nourished by a yolk sac (Castro 1996). Oviparous shark species lay fertilized eggs while in the case of ovoviviparous sharks, embryos stay inside the mother’s body without a placental connection, being nourished by a yolk sac for the entire gestation period. Members of the family of requiem sharks (Carcharhinidae), such as silky shark, oceanic whitetip, blacktip reef shark (Carcharhinus melanopterus), copper shark (Carcharhinus brachyurus), dusky and sandbar shark belong to the viviparous sharks. Shortfin mako sharks and great white sharks (both belonging to the family of mackerel sharks (Lamnidae)), and thresher sharks (Alopiidae) are ovoviviparous, with embryos feeding on other ova produced by the mother after the yolk sac is absorbed (Dulvy and Reynolds, 1997). Lower mercury levels observed in female sharks can be the result of maternal transfer of mercury from the mother to the embryos or developing ova (Walker, 1976). In a study of five shark species from the Florida east coast, THg levels in embryos of blacktip sharks, bonnethead sharks (Sphyrna tiburo) and Atlantic sharpnose sharks (Rhizoprionodon terraenovae), were between 20 and 53% of the THg levels of adults sharks of the same species (Adams and McMichael 1999). For juvenile sharks, high mercury levels can also be the result of higher tendency to forage in coastal areas compared to adults sharks (Rumbold et al., 2014). Pethybridge et al. (2010) found different mercury levels between male and female sharks, which were partly related to the fact that females of most species were larger than the males. However, a normalisation of THg levels with size showed that males had higher mercury levels than females, which could be the result of maternal transfer. The phenomenon of maternal transfer could also be observed for other Carcharhinus species (Lyle, 1984; de Pinho et al., 2002) and for white sharks (Lowe et al., 2012; Mull et al., 2012). Some studies did not find any significant correlation between THg levels in sharks and maternal transfer for tiger sharks (Endo et al. 2008), common thresher (Alopias vulpinus) and shortfin mako sharks (Suk et al. 2009), blue sharks (Escobar-Sánchez et al, 2011), and 17 different shark species of the South African coast (McKinney et al
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2015, ). An explanation could be that the majority of sharks in these studies were juveniles. There are other factors, apart from body length, that can influence correlations between mercury levels and sex, for example different growth rates in males and females (Walker, 1976; Marcovecchio et al., 1991; de Pinho et al., 2002; Geraghty et al., 2013). Male sandbar and dusky sharks from Australia had higher growth rates compared to juvenile females and slower growth rates after reaching maturity.
Metabolism Different mercury levels in different shark species might also be the caused by their metabolism. Suk et al. (2009) studied mercury levels in five shark specie of the Florida east coast and found particularly high levels in shortfin mako shark, with an average THg concentration of 2.90 μg/g in the muscle tissue of the largest individuals (nearly 3 times the EU safety limit of 1 μg/g). The shortfin mako is one of the few pelagic fish species with an excess of mercury relative to selenium in its muscle tissue (Kaneko and Ralston 2007). Selenium binds to MeHg and in this way weakens its toxicity of MeHg (Raymond and Ralston 2004). Maz-Courrau et al. (2011) did not find a significant THg-body length correlation for blue sharks and explained this by more efficient mercury elimination mechanisms of this species, because of a higher synthesis of metallothioneine (Núñez Nogeira et al., 1998). Increasing Hg concentrations in sharks with decreasing Se:Hg molar ratios were also found by a number of other authors (Burger et al., 2012; Bergés-Tiznado et al., 2015).
Temporal trends Because mercury is persistent in the environment and the positive trends in the use of fossil fuels and gold-mining, mercury levels in the environment and organisms can be expected to rise as well. McKinney et al. (2015) found 50% higher mercury levels in 36
shortfin mako sharks sampled between 2005 and 2010 (161-220cm body length) compared to the shortfin mako sharks of similar sizes (110-260 cm) from the same geographical area in 1980 (Watling et al. 1981).
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6
Effects of mercury on human health
Fish consumption is the main source of mercury exposure to humans (Mergler et al. 2007; Escobar-Sánchez et al., 2014; McKinney et al., 2015). Consumption of top predators such as whale, shark, swordfish and tuna bear the highest exposure risks for humans, as mercury levels in seafood biomagnify along the food chain. About 70 to 100% of mercury in fish (more than 90% in muscle tissue) is MeHg, its most toxic form (Storelli et al., 2002a; Storelli et al., 2002b; Burger and Gochfeld, 2004). Mercury is ranked as the third most toxic substance after lead and arsenic in the list of most toxic elements by the US Agency for Toxic Substances and Disease Registry (US ATSDR, 1999). Exposure to MeHg can have various negative effects on the human body, including the nervous system as the most sensitive target (Aschner, 2002), endocrine system and reproductive system, among others. Exposure of embryos and children during development are of special concern due to the damages that MeHg can cause to the developing brain and the nervous system. The populations of China and Hong Kong are particularly affected as seafood represents the main protein source in their diet.
Neuro- and neurodevelopmental toxicity of mercury The presence of mercury in the nervous system leads to various effects, including abnormal tissue formation and cell damage in the brain, causing impairments of motor function, visual function, memory function, attention and speech processing (Tsubaki, 1975; Takeuchi, 1977; Chang et al., 1977; Reuhl et al., 1981), neurocognitive deficits and neuromotor disabilities (Bose-O’Reilly et al., 2010). MeHg blocks Ca2+ ion channels in the axon membranes of neurons, which are essential for the interneuronal information transfer (Shafer and Atchison, 1989; Rossi et al., 1993). It also damages the sheaths of myelinated axons and in this way impairs impulse conduction of signals in the nervous system. Mercury has also been found to damage the blood brain barrier and facilitate access of other toxic metals to the brain and to impair the synthesis of
38
actin and tubulin, important components of the neuronal cell structure and essential for a number of detoxification processes (Kazantzis, 2002). Mercury targets granule cells in the cerebellum of both, adults and neonates. The fact, that damages in neonates and children lead to much more severe symptoms can be explained by the role of mercury in the phase of neurological development. The structure of the mitotic spindle, which eukaryotic cells use to separate their chromosomes during cell division, is formed by microtubules. The assembly of such microtubules requires free sulfhydryl groups on monomeric tubulin. Mercury binds those sulfhydryl groups and in this way inhibits the assembly of immature microtubules, which results in destabilized microtubules causing impaired mitoses (cell division process) and perturbation of other critical processes in the development of the brain (Graff et al., 1997). More mature microtubules are in contrary to immature microtubules resistant to destabilization through MeHg (Philbert et al., 2000). Neurological biomarkers of elevated mercury exposure are well documented in major historic incidents of mercury poisoning. Excessive releases of MeHg via the wastewater of the Chisso Cooperation’s chemical factory in the Minamata Bay, Japan, between 1932 and 1968, led to elevated bioaccumulation in fish and shell fish and finally to mercury poisoning of the local population in the Kumamoto prefecture (Harada, 1995). Several hundred people died and about 9000 people showed severe neurological symptoms (Tsubaki and Takahashi, 1986). The factory primarily produced acetaldehyde, using mercury sulfate as a catalyst. The first human victims were discovered in 1956 and 2273 official patients of the so-called Minamata-disease were registered by 2011 (Harada, 1995). Both adults and children showed symptoms of mercury poisoning, but most severely affected were children who had been indirectly exposed to mercury as foetuses via the placental connection to their mother and/or as babies via mercury transferred over their mother’s milk. The mothers developed weaker symptoms of mercury poisoning as most of the mercury in their body transferred to their foetuses.
Symptoms are characterized by different
neurodevelopmental and neurocognitive impairments, such as cerebral palsy (a neurological disorder appearing in early childhood with permanent impairment of muscle coordination and balance), deformation of limbs, impairment of growth, 39
disturbed coordination, hyperactivity, squints, muscular spasms and uncontrollable writhing, vision and speech impairment, paresthesias (sensation of tingling, tickling, pricking, or burning on the skin), neuralgias (pain in the nerves), dermographism (red weals appearing on the skin), malfunctions of smell, taste and hearing, seizures and in some cases coma and death (Harada, 1978). The fact that mercury from the incident was transferred from mothers to their embryos was discovered by Masazumi Harada in 1968, when he had the idea to measure mercury concentrations in umbilical cords, which in the Japanese tradition are preserved, enabling him to collect them from residents in the area. In this way, he was able to find a correlation between the mercury concentrations in umbilical cords and the Minamata incident (Nishigaki and Harada, 1975). In 1965 a similar outbreak was detected in the Niigata Prefecture, caused by the excessive release of MeHg into the Agano river basin by the Showa Electrical chemical factory (Takizawa et al., 1970). In Iraq, a mercury poising occurred throughout the country between 1971 and 1972 due to consumption of flour, wheat and barley that had been treated with MeHg containing fungicides (Bakir et al., 1973). 6530 people showed symptoms of mercury poisoning and 459 deaths were reported. Reported symptoms were loss of sensation in hands, feet and around the mouth, loss of coordination, impairment of vision, speech and hearing, and blindness. Fatalities were caused by failure of the central nervous system and in rare cases of the cardiovascular system (Bakir et al., 1973). Similar incidents occurred in Pakistan and Guatemala (Bakir et al., 1973). Cohort studies conducted in the Seychelles, Faroe Islands and New Zealand have examined the effects of MeHg exposure of children whose mothers ate fish and whale meat during pregnancy. The ‘high exposure group’ of mothers in the New Zealand study consumed fish, including shark, 3 times a week and had mercury hair levels above 6 µg/g. The children of this group showed lower scores in their mental and motoric development at the age of four, compared to less exposed groups (Kjellström et al., 1986; Kjellström et al., 1989). Meat and intestines of pilot whales are traditionally consumed by the population of the Faroe Islands. Mothers of the test group ate episodically pilot whale meat, which 40
usually has high mercury levels, and frequently ate fish. Their children underwent different tests at the age of 7 and 14, where deficits in attention, memory and language faculty were observed, and under-developed motoric and visuospatial abilities. These symptoms were correlated to prenatal MeHg exposure (Debes et al., 2006; Grandjean et al., 1997). The study from the Seychelles did not find any evident correlation between prenatal MeHg exposure and mercury related health effects. Mothers in the test group frequently consumed fish, however not including shark or whale meat contrary to the other two studies. Cernichiari et al. (1994) found higher mean mercury levels in maternal hair of test groups in the Seychelles (5.8 µg/g) compared to test groups from the Faroer Islands (4.5 µg/g) (Grandjean et al., 1992). However, Hg concentration in hair is also influenced by hair colour, hair type and permanent hair treatment (Grandjean et al., 1992). In comparison, populations with minimum fish consumption have average mercury hair levels between 0.1 and 1.0 µg/g (Stern et al., 2001 (US); Pesch and Wilhelm, 2002 (Germany); Björnberg et al., 2003 (Sweden)). Exposure to mercury from seafood consumption is not the only way to cause symptoms of mercury poisoning. There are many reported cases of children who were exposed to mercury by interior latex paint (Agocs et al., 1990) and of children exposed to phenylmercury, another organic form of mercury, used as a fungicide in nappy rinse (Langford and Ferner, 1999). Symptoms observed in these cases were rashes, limb pain, swollen nodes, peripheral neuropathy (damage to or disease affecting nerves, which may impair sensation, movement, gland or organ function), hypertension, and kidney dysfunction (Agocs et al., 1990; Langford and Ferner, 1999).
Immunotoxicity of mercury Mercury exposure leads to impairment of the immune system most likely by preventing the production and function of polymorphonuclear leucocytes (PMNs), a type of white blood cells (leucocytes). Leucocytes are an essential part of the immune system, destroying bacteria, viruses, toxic substances and other exogenous threats to the body (Wada et al., 2009). Mercury exposure by ingestion often causes increased 41
levels of bacteria, yeasts and molds, which protect the body by absorbing excess mercury. Fungi, such as Candida Albicans, which occurs naturally in the human gut flora, can be destroyed by antibiotics, and this may lead to an enormous release of heavy metals in adults with a high body burden (Rice et al., 2014). A high mercury body burden has been correlated to a number of different immune or autoimmune diseases, for example allergies, psoriasis, asthma, arthritis, autism, attention deficit hyperactivity disorder, epilepsy, multiple sclerosis, thyroiditis, schizophrenia and scleroderma (Warren, 1989; Schofield, 2005; Johnson and Atchison, 2009; Singh, 2009; Gardner et al., 2010; Hybenova et al., 2010; Landrigan, 2010). In a study from the Amazonas region, increased Malaria infections were correlated to elevated occupational mercury exposure of gold miners (Silbergeld et al., 2005).
Cardiovascular toxicity of mercury In the 14-year follow-up of the already mentioned cohort study from the Faroe Islands, an alteration of heart function was observed in the test group of 14 year-old children whose mothers consumed pilot whale meat and fish during pregnancy (Grandjean et al., 2004). The children showed a decreased heart rate variability, which might be caused by MeHg damage to brainstem nuclei. The brainstem is the posterior part of the brain, which provides important nerve connections for the motor and sensory functions. Among others, it is essential for control of cardiac and respiratory functions. Sørensen et al. (1999) reported similar observations, with a 47% decrease in heart rate variability in a study of 7-year old Faroese children with prenatal mercury exposure. In a study from Korea, an increase in children’s cholesterol levels, which is a risk factor for coronary or cardiovascular diseases, has been associated to MeHg exposure (Kim et al., 2005), and in a study from the Seychelles, elevated blood pressure levels in teenage boys were correlated with prenatal mercury exposure (Thurston et al., 2007). MeHg exposure from latex paint evoked hypertension in children (Agocs et al., 1990) and in a study from the Brazilian Amazon hypertension in adults has been associated 42
with mercury exposure (Fillion et al., 2006). In a study from Finland, men with high fish consumption were found to have exceptionally high mortality associated with coronary heart disease (Salonen et al., 1995).
Effects on the endocrine system The endocrine system consists of glands that produce hormones that regulate almost every biological process, for example metabolism, growth, development, sexual maturation reproduction, sleep, mood, immune functions and memory. The glands producing these hormones include the pituitary gland, thyroid gland, parathyroid glands, adrenal glands, pancreas, ovaries, and testicles. Endocrine disruption can be caused by natural or man-made chemicals, which either target the hormone itself, the glands where the hormones are produced or the hormone receptors, with dramatic effects on the regulation of body functions. Insulin, estrogen, testosterone and adrenaline belong to the hormones most affected by mercury exposure (Rice et al., 2014). Autopsy studies have found that the thyroid and the pituitary have an affinity to accumulate mercury, even more than the kidneys (Tan et al., 2009). Mercury occupies iodine-binding receptors, which leads to the inhibition or alteration of hormone production in the thyroid (McGregor and Mason, 1991; Wada et al., 2009). A decreased activity of the thyroid (hypothyreosis) or an increased activity of the thyroid (hyperthyreosis) can lead to disruptions of the cardiovascular system, the nervous system, the psyche, the gastro-intestinal system, metabolism, skin, muscle and skeleton system and sexual functions. A hyperthyreosis can for example lead to acceleration of heartbeat (tachycardia), nervousness and weight loss. A hypothyreosis can lead to a deceleration of the heartbeat (bradycardia), increase in weight, depression or loss of libido. Mercury has also been found to accumulate in the pituitary glands of humans (Kanabrocki et al., 1976; Nylander, 1986; Erfurth et al., 1990) and animals. While in tested animals, mercury had adverse effects on the pituary (Thorlacius-Ussing et al., 1985; Danscher et al., 1990) and other glands (thyroid, adrenal, gonads) (Ghosh and 43
Bhattacharya, 1992; Thaxton et al., 1975; Vachhrajani and Chowdhury, 1990), no such effects could be found for the human pituary. In mercury exposed workers (McGregor and Mason, 1991; Erfurth et al., 1990), dentists (Erfurth et al., 1990) and chlor-alkali workers (Barregard et al., 1994), no changes were found in the levels of different pituitary-related hormones, even though tested individuals had elevated mercury levels in their blood and urine and in the pituitary glands (Nylander, 1986; Erfurth et al., 1990).
Effects on the reproductive system Several studies could correlate MeHg exposures to impairments of the reproductive system. After the outbreak of the Minamata disease, an increasing number of male stillborns was observed and concluded that male embryos might be more sensitive to mercury exposure (Sakamoto et al., 2001). The mercury mass poising in Iraq led to a strong decline in pregnancies (Bakir et al., 1973). Two studies from Hong Kong with couples who underwent in-vitro fertilization, seafood consumption could be correlated to blood mercury concentration and infertility (Leung et al., 2001; Choy et al., 2002). In 35% of infertile men and 23% of infertile women had abnormally high blood mercury concentrations (Choy et al., 2002). Mercury can bind to membranes of the acrosome, the anterior part of a spermatozoon, and impair its function (Ernst et al., 1991). The acrosome contains enzymes which break down the outer membrane of the ovum, allowing the sperm cell to join with the ovum. Other possible toxic effects of mercury on sperm are disruptions of sperm membrane permeability and DNA synthesis (Vogel et al., 1985; Ernst et al., 1991; Liu et al., 1995). Apart from sperm, mercury can target cells in the testis (Ernst et al., 1991), and in the seminal vesicles (Li et al., 1995), which are essential for the energy supply of the spermatozoa, and in the epididymis (Working et al., 1985), which is essential for the maturation process and storage of the spermatozoa. Observed infertility in women with mercury exposure might be explained by similar disruptions in the female gametes. For example, it has been reported that mercury damages ova chromosomes of rodents (Jagiello and Lin, 1973). 44
In another study from Hong Kong, infertility of males could be linked to mercury levels in their hair and to the intensity of fish consumption. High hair mercury levels could also be correlated to age, explained by the fact that the intake rate of mercury was higher than the rate of degradation and excretion, leading to an accumulation of mercury over time. The study also discussed that organochlorine contaminants in seafood (e.g. PCBs, PAHs and DDT) add to the effects of mercury on the reproductive system (Dickman et al., 1998). Organochlorines have been correlated to impairments in the endocrine system and to reduced sperm counts in humans (Richardson, 1993). Owing to the problem of mercury accumulation with age and high seafood consumption in Hong Kong, Dickman et al., (1998) claimed that the MeHg safety limit of 0.5 g/kg fish established by the WHO (WHO, 1990) should be reduced for regions like Hong Kong where seafood is the major protein source, to the safety limit used in Japan (0.3 g/kg) (MOE, 2002), in order to match annual intake rates to annual excretion rates. Even for lower mercury dosages, a correlation was observed between mercury exposure and effects on the reproductive system. Dental assistants who were exposed to mercury vapour when assisting with amalgam fillings, were found to have abnormal numbers of miscarriages and stillbirths (Sikorski et al., 1987).
Carcinogenicity MeHg compounds were classified as possible carcinogens to humans by the International Agency for Research on Cancer (IARC, 1993). In a study from Slovenia, different types of cancer (oral, pharyngeal and lung cancers) among mercury miners have been associated to occupational mercury exposure (Zadnik and Pompe-Kirn, 2007). In mercury miners from Spain, increased cancer mortality was observed, including liver, colon, bladder, kidney, lung and central nervous system cancers, and a trend in cancer mortality was positively correlated to duration of exposure (García Gómez et al., 2007). For mercury miners and mercury millers from Italy, Ukraine, Spain and Slovenia, correlations were found between mercury exposure and liver and lung 45
cancer, however not for kidney cancer. A correlation between the occurrence of cancer and duration of exposure could not be found. The authors also mentioned that increased cases of lung cancer could be explained by co-exposure to radon and crystalline silica (Boffetta et al., 1998). In victims of the Minamata outbreak increased cases of leukemia were observed and correlated to mercury exposure (Yorifuji et al., 2007).
46
7
Methods
MeHg levels in shark fins of 9 different studies were collected and results were used to estimate exposure of the Hong Kong and Chinese population, depending on their consumption patterns and compared to the recommended safety limits.
Methylmercury concentrations in fins Of the shark species represented in the different studies, the only ones considered were those that typically occur in the shark fin trade (Table 3). The authors of these studies presented their results either as MeHg concentrations or as total mercury (THg) concentrations, and either based on dry-weight or based on wet weight. Therefore, mercury concentrations were converted into values based on dry weight and wet weight, where necessary, as international mercury limit values per kg fish are represented on a wet weight basis, while dry weight values are more convenient to compare daily exposure related to consumption of shark fins which are normally bought from the market in dried or processed form. A ratio of 1:2.27 for wet weight to dry weight of fin tissue of was used for the conversion (Gilbert et al., 2015). Where only total mercury (THg) information was available, data have been normalised to MeHg values, in order to make values comparable. Different studies report quite wide ranges of MeHg to THg ratios. (Kim et al., 2016) found average MeHg to THg ratios of 77% for all species in the study and of about 80% for larger shark species of higher trophic levels. Nalluri et al. (2014) found ratios in the range of 55-89%, however, not specifying the respective shark species for each percentage. The wide range of MeHg to THg ratios may be explained by differences in age, size, origin, diet and trophic level which influence bioaccumulation of MeHg (de Pinho et al., 2002) and different studies confirmed a positive correlation between MeHg to THg ratio and trophic level (Holsbeek et al., 1997; Watras et al., 1998; Francesconi and Lenanton, 1992). As all the shark species considered in this study belong to sharks of high trophic
47
Table 3: Shark species of the reviewed selection of studies which are known to typically occur in the global fin trade according to the listed references. Species
Scientific name
Reference
Pelagic thresher shark Bigeye Thresher Shark Common thresher Copper shark Spinner shark Silky shark Bull shark Blacktip shark Oceanic whitetip Blacktip reef shark Dusky shark Sandbar shark
Alopias pelagicus Alopias superciliosus Alopias vulpinus Carcharhinus brachyurus Carcharhinus brevipinna Carcharhinus falciformis Carcharhinus leucas Carcharhinus limbatus Carcharhinus longimanus Carcharhinus melanopterus Carcharhinus obscurus Carcharhinus plumbeus
Great white Shortfin mako shark Blue shark Scalloped hammerhead Great hammerhead Smooth hammerhead Spiny dogfish
Carcharodon carcharias Isurus oxyrinchus Prionace glauca Sphyrna lewini Sphyrna mokarran Sphyrna zygaena Squalus acanthias
Vannuccini, 1999; Clarke et al., 2006a; Kim et al., 2016 Vannuccini, 1999; Clarke et al., 2006a Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014 Nalluri et al., 2014 Nalluri et al., 2014 Clarke et al., 2006a Clarke et al., 2006a; Nalluri et al., 2014 Vannuccini, 1999 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016 Vannuccini, 1999; Kim et al., 2016 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014 Vannuccini, 1999; Shivji et al., 2005; Nalluri et al., 2014 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014 Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016 Kim et al., 2016
levels (Cortés, 1999; Li et al., 2014), their MeHg levels were estimated with 80% of THg concentrations, according to MeHg-THg ratios reported in (Kim et al., 2016) for sharks of this trophic group (blue shark, pelagic thresher (Alopias pelagicus), blacktip reef shark, shortfin mako, and smooth hammerhead). One exception were data collected from the 13 scalloped hammerhead sharks (Mazaba Lara, 2015), which consisted mainly of neonates and juveniles younger than a year. For these, MeHg concentration has been estimated with 63% of the THg concentration, which is the average value of ratios found by (Kim et al., 2016) for species of lower trophic levels. Correlations between MeHg concentrations and influencing factors (e.g. body length, trophic position, species-specific factors like trophic position or feeding habit, geographic location) have not been statistically evaluated as available data from literature originate from different study designs and the number of samples as compared to the complexity of variables has been considered insufficient.
Consumption patterns and exposure Due to a lack of reliable data regarding per capita shark fin consumption, a rough estimate was made using data of the Hong Kong and Chinese reported fin trade and estimates for unreported and illegal catching (Clarke et al., 2006b). The obtained 48
average yearly consumption was then compared to a survey on shark fin consumption in Hong Kong (Bloom/SSRC, 2015).
Figure 6: Mass balance of shark fin trade for China and Hong Kong based on average data for 20012011 in fin volumes (tons) and in percent of global imports to Hong Kong (FAO, 2015).
Overall shark fin consumption for Mainland China and Hong Kong was estimated by a mass balance of import, export and capture production data (Figure 6). Own capture production of the two countries were neglected as Hong Kong does not have any own or at maximum very little capture production of sharks (Clarke, 2004; FAO, 2015). Chinas own capture production was only available as total chondrichthyan (sharks, rays, skates and chimaeras) capture production which was about 1464 tons between 2001 and 2011. Clarke et al. (2006b) estimates the share of sharks used in the fin trade to be 45% of total chondrichthyan capture production, which results in about 658 tons per year for China’s own capture production. In order to calculate the corresponding weight of shark fins, the ratio of shark fin to total body weight has been estimated with of 10.7 %, as an average of values listed for relevant shark species in (Hindmarsh, 49
2007). Using this ratio, 658 tons of sharks correspond to 33 tons of shark fins that are yearly produced in China’s own capture production. This small volume of shark fins corresponded to 0.3 % of global import to Hong Kong and was therefore neglected. Consumption in tons of shark fins for Hong Kong and China was calculated by taking average global shark fin imports to Hong Kong and China, subtracting Chinese exports to other countries than Hong Kong and Hong Kong exports to other countries than China. The sum of Hong Kong exports to other countries than China, non-Hong-Kong imports to China and non-Hong-Kong exports from China were about 6% of the global imports to Hong Kong and for this reason these three addends have been neglected as well. As a result, shark fin consumption in Hong Kong and mainland China was considered to more or less equal to the volume of global shark fin imports to Hong Kong. In order to correct the reported trade values in terms of more realistic values which include the dimensions of unreported and illegal catches, a correction factor of 4.4 (Clarke et al., 2006b), was applied to the import (=consumption) volume. This correction factor has been statistically estimated using genetic identification of shark fins of the Hong Kong fin market combined with Hong Kong trade statistics and FAO records. In the next step, the present import data for 2015 were estimated. Latest import trends for shark fins are not available as China stopped registering shark fins as a separate custom code in 2005 and Hong Kong followed suit in 2012 (FAO, 2015; Clarke et al., 2006b). According to different media reports, shark fin consumption in Hong Kong and China decreased due to various reasons in the last years and in some media reports decreases of 70% have been mentioned (Tsui, 2013; Duggan, 2014; Wild Aid, 2014). However Eriksson & Clarke (2015) explained why this value is far too optimistic. 2012 imports were 22% lower than the 2008-2011 average (Eriksson & Clarke, 2015). Due to a lack of reliable information on recent import numbers, a further decline of imports between 2012 and 2015 has been estimated with 25% to 2012 imports. This estimate was made under the assumption, that imports kept decreasing, but not with a continuing linear trend (which would have been a steep linear decrease of 22% per 50
year) but a rather asymptotic trend, as there have not been any events in the last years that would justify drastic yearly import declines. Applying a correction factor of 4.4 (Clarke et al., 2006b) and assumed consumption declines (22% between 2011 and 2012; 25% between 2012 and 2015) to the mass balance of average import and export data of 2001-2011 (i.e. imports to Hong Kong ≙ consumption in Kong Kong and China), 55334 tons of shark fins were estimated to
have been imported to Hong Kong, which correspond to the volume of shark fins consumed in Hong Kong and China for 2015. Divided by the 2015 population of Hong Kong (7,287,983) and the Chinese urban population (56.6% of 1,376,048,943) (United Nations Population Division, 2016), the per capita consumption would be 70 g per person per year, which would correspond to approximately 1-2 shark fin soups of 50g fins each on average per person per year. As large parts of the population, especially of the rural population and people with lower income, do not consume shark fins at all, the Chinese share has been estimated using only the urban population. This estimate roughly agrees with data of a telephone interview survey conducted in Hong Kong where 1030 people between 18 and 75 years where asked how often they consumed shark fin soup per year in 2009. 44.1 % of people had consumed shark fin soup one or more times a year, while 43.6 % had consumed shark fin soup less than once a year and 12.3% indicated that they never had eaten shark fin soup (unpublished data of Bloom/SSRC, 2015). It is uncertain in how far the Hong Kong consumption patterns can be applied to consumption patterns in China. However estimates for consumption in Hong Kong and China using trade statistics with correction factors from Clarke et al. (2006b) do not differ significantly from the Hong Kong interview data, and these were the only two available reference points. In order to account for these uncertainties, consumption MeHg exposure has been calculated for different possible consumption scenarios. Possible MeHg exposures were calculated for five different shark fin soup consumption frequencies between once per year and three times a week, in order to calculate possible MeHg exposures for adult men (62kg), adult women (54kg) and children between one and six years (16.5kg). Average body weights were obtained from Lee et al. (1994) and Yang et al. (2005). Two indicators of typical amounts of shark fin used in 51
the fin soups were found. Man et al. (2015) reported a restaurant in Hong Kong that serves dishes with large amounts of shark fin (150g). An internet recipe indicated 300g of shark fin to be used, however no number of servings was given (Singapore Food Recipes, 2012). Assuming 6 servings, the amount per person would result in 50g. These two different amounts of fins were used to calculate daily MeHg exposure, using the mean MeHg concentration in mg/kg dry weight calculated from the selection of studies.
52
8
Results
Mean values of MeHg and THg concentrations were calculated based on dry weight and wet weight. Results were compared with international safety limits for THg concentrations in fish as well as safety limits for daily MeHg exposure. Mean MeHg concentration in dry weight was used to estimate exposure for different consumption frequencies for adults and children.
Comparison of MeHg and THg concentrations with international safety limits for concentrations in fish Of the 9 studies on mercury levels in shark fins, 26% of the samples exceeded the safety limits of MeHg concentration in fish set by the Japanese Health Authority (0.3 mg/kg wet weight). 22% of the samples exceeded the safety limits for THg concentration in shark products of 1 mg/kg wet weight, adopted by the European Union (EC, 2002), Australia and New Zealand (FSANZ, 2004) and Canada (Health Canada, 2008), 24% exceeded the Japanese safety limits for THg concentration in fish (0.4 mg/g) (MOE, 2002; UNEP, 2008) and 26% exceeded the US safety limits for THg concentration in fish and shellfish (0.3mg/g) (US EPA, 2001b). MeHg concentrations varied between 0.006 mg/kg wet weight (0.01 mg/kg dry weight) for juvenile scalloped hammerhead sharks (103±35cm) of the Pacific Ocean (Mexico) and 5.96 mg/kg wet weight (13.53 mg/kg dry weight) for a larger sample of the same species (183 cm, 7cm below first maturity body length) of the Gulf of Mexico (Table 4).
53
Table 4: MeHg and THg concentrations in shark fins in g/kg wet weight (ww) and dry weight (dw); References for BL/ML: (1) Cervigón et al., (1992), (2) Compagno (1998b), (3) Compagno (1998), (4) Ebert (2003), (5) Compagno et al. (1995), (6) Compagno et al. (1989), (7) Compagno (2001), (8) Compagno and Niem (1998), (10) Randall et al. (1997), (11) Frimodt (1995), (12) Sommer (1996), (13) Natanson (2001), (14) Castro (1996). Species common name
Scientific name
TL
n
BL
CL
ML (range or mean)
CF
MeHg ww
THg ww
MeHg dw
Blue shark Shortfin mako shark Smooth hammerhead shark Pelagic thresher shark Oceanic whitetip shark Blacktip reef shark Spiny dogfish Smooth hammerhead shark Silky shark Bigeye Thresher Shark Copper shark Silky shark Sandbar shark Common thresher shark Smooth hammerhead shark Bull shark Spinner shark Dusky shark Great white shark Blue shark Shortfin mako shark Oceanic whitetip shark Great hammerhead shark Copper shark Scalloped hammerhead shark Scalloped hammerhead shark Scalloped hammerhead shark Dusky shark Sandbar shark Great white shark Smooth hammerhead Blue shark Shortfin mako shark Pelagic thresher shark Blacktip shark Unknown Species Unknown Species Unknown Species Unknown Species Unknown Species
Prionace glauca Isurus oxyrinchus Sphyrna zygaena Alopias pelagicus Carcharhinus longimanus Carcharhinus melanopterus Squalus acanthias Sphyrna zygaena Carcharhinus falciformis Alopias superciliosus Carcharhinus brachyurus Carcharhinus falciformis Carcharhinus plumbeus Alopias vulpinus Sphyrna zygaena Carcharhinus leucas Carcharhinus brevipinna Carcharhinus obscurus Carcharodon carcharias Prionace glauca Isurus oxyrinchus Carcharhinus longimanus Sphyrna mokarran Carcharhinus brachyurus Sphyrna lewini Sphyrna lewini** Sphyrna lewini Carcharhinus obscurus Carcharhinus plumbeus
4.1 4.3 4.2 4.5 4.2 3.9 3.9 4.2 4.2 4.2 4.2 4.2 4.1 4.2 4.2 4.3 4.2 4.2 4.5 4.1 4.3 4.2 4.3 4.2 4.1 4.1 4.1 4.2 4.1 4.5 4.2 4.1 4.3 4.5 4.2
15 7 3 13 3 26 17 15 18 8 1 3 5 6 3 3 4 6 4 6 3 2 2 2 4 13 1 12 12 10 15 33 24 5 8 12 12 14 12 12
110 ± 20 120 ± 10 110 ± 20 100 ± 30 90 ± 30 90 ± 20 80 ± 10 103 ± 35 87-220 266 ±32 131.1 102 ± 7 n.s. n.s.
