Methylmercury concentrations in shark fins

1

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, Dr. Silvia Frey (Oceancare)

School of Life Sciences

Heriot-Watt University, Edinburgh

2

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.

3

Acknowledgements

I would like to thank Thomas, Luca and 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 Eric, who dedicated his limited time to proofread my work, to

my supervisor Dr. Mark Hartl for his feedback and to my external supervisor 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.

4

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.

5

Contents

1 Introduction .......................................................................................................................... 6

2 Global conservation status of shark species ......................................................................... 9

3 Characteristics of shark fin soup, cultural background, market dimensions and trends.... 18

4 Global distribution of mercury and bioaccumulation of methylmercury in marine

organisms and in the human body ...................................................................................... 23

5 Biological and ecological factors that influence MeHg concentration in shark tissue ....... 30

6 Effects of mercury on human health .................................................................................. 38

7 Methods .............................................................................................................................. 47

8 Results ................................................................................................................................. 53

9 Discussion ............................................................................................................................ 56

References................................................................................................................................... 66

Appendix - List of shark species discussed .................................................................................. 83

6

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

7

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.

8

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.

2 Global conservation status of shark species

All shark species which were found to occur in the global fin trade by

(Vannuccini, 1999; Clarke et al.

threatened with higher risk of extinction (IUCN

‘near threatened, vulnerable or

exploitation 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).

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 o

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

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 bycat

9

Global conservation status of shark species

which were found to occur in the global fin trade by

Clarke et al., 2006a; Nalluri et al., 2014; Kim et

threatened with higher risk of extinction (IUCN, 2016), i.e. they are in the categories

‘near threatened, vulnerable or endangered (Figure 1). The reasons

n and bad fisheries management in combination with a typically low



; Clarke et al., 2007). Sharks and ray landings

between 1950 and 2003, and then declined by 15% between 2003 and 2011. Also


ng populations are not the result of improved fisheries management.


been estimated for 2009 (Costello et al., 2012; Dulvy et al., 2008).

: 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



(Francis et al. 2001) and 25% of total bycatch in the US Atlantic longline swordfish

which were found to occur in the global fin trade by different studies

Kim et al., 2016) are

2016), i.e. they are in the categories

The reasons are over-

n and bad fisheries management in combination with a typically low



increased by 227%

between 1950 and 2003, and then declined by 15% between 2003 and 2011. Also,


f improved fisheries management. An


: IUCN Red List categories; EW: Extinct in the wild; CR: Critically Endangered; EN:

landings is overexploitation, either as bycatch



ch in the US Atlantic longline swordfish

10

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).

and tuna fisheries (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

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

11

that 97.5% of pelagic sharks 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 well-

managed, 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

12

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 North-

east 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

13

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

14

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

15

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).

16

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).

17

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 post-

release 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.

18

3 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

19

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

their higher amount of fin needles which are important fo

(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

smoking with sulfur for a couple of hours or by a short treatment with hydrogen

peroxide which will give them

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 preparatio

ingredient of the soup, but rather in terms of symbolism

themselves do not add any flavour to the soup (Pamela, 2015), many other ingredients

are added, for example chicken, pork, ham

Food Recipes, 2012; Pamela, 2015). In the further process, all

cooked in chicken stock for about six to eight hours (Pamela 2015).

Information about how much shark fin is used per portion of sha

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

20

their higher amount of fin needles which are important for the texture of the soup

: Body parts of a shark (Source: Wikipedia, drawing by Chris Huh).


rder to soften the denticles and skin, which can then be easier

moved. After that, the fins normally undergo a bleaching process, either through


peroxide which will give them a more demanded whitish colour. The fins are then



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


are added, for example chicken, pork, ham, crab meat or eggs and spices (Singapore

es, 2012; Pamela, 2015). In the further process, all the ingredients

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



r the texture of the soup


rder to soften the denticles and skin, which can then be easier

normally undergo a bleaching process, either through


a more demanded whitish colour. The fins are then



n of the soup. The fins are the most important

flavour. As the fins


, crab meat or eggs and spices (Singapore

the ingredients are

rk fin soup is scarce. In



21

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.

22

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).

23

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).

24

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

25

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

26

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

27

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.

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,

Species Scientific namedry weight/

wet weightMuscle Liver Kidney Skin Fin

Upper

caudal finReference

Dusky shark Carcharhinus obscurus dw 8.5 11.59 0.07 (Gilbert et al., 2015b)

Sandbar shark Carcharhinus plumbeus dw 6.71 37.87 0.02

Great white shark Carcharodon carcharias dw 9.71 0.86 0.09

Spiny dogfish Squalus acanthias ww 0.64–1.45 0.61–0.83 0.12–0.18 (Pethybridge et al., 2010)

Shortnose Spurdog Squalus megalops ww 0.75–0.79 0.38–0.70 0.28 0.03–0.1

Shortspine Spurdog Squalus mitsukurii ww 2.83–3.23 2.83–3.23 1.35–1.63 0.14

Silky shark Carcharhinus falciformis dw 2.61 2.1 0.66 0.02 0.98 (O’Bryhim, 2015)

Bonnethead shark Sphyrna tiburo dw 3.1 1.82 2.15 0.04 0.68

Porbeagle shark Lamna nasus ww 0.84 0.06 (Nicolaus et al., 2016)

28

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

29

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).

30

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).

31

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

32

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

33

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

34

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

35

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

36

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

37

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).

38

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

39

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,

40

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

41

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

42

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

43

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

44

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).

45

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

46

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).

47

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

48

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.

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

Species Scientific name Reference

Pelagic thresher shark Alopias pelagicus Vannuccini, 1999; Clarke et al., 2006a; Kim et al., 2016

Bigeye Thresher Shark Alopias superciliosus Vannuccini, 1999; Clarke et al., 2006a

Common thresher Alopias vulpinus Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014

Copper shark Carcharhinus brachyurus Nalluri et al., 2014

Spinner shark Carcharhinus brevipinna Nalluri et al., 2014

Silky shark Carcharhinus falciformis Clarke et al., 2006a

Bull shark Carcharhinus leucas Clarke et al., 2006a; Nalluri et al., 2014

Blacktip shark Carcharhinus limbatus Vannuccini, 1999

Oceanic whitetip Carcharhinus longimanus Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016

Blacktip reef shark Carcharhinus melanopterus Vannuccini, 1999; Kim et al., 2016

Dusky shark Carcharhinus obscurus Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014

Sandbar shark Carcharhinus plumbeus Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014

Great white Carcharodon carcharias Vannuccini, 1999; Shivji et al., 2005; Nalluri et al., 2014

Shortfin mako shark Isurus oxyrinchus Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016

Blue shark Prionace glauca Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016

Scalloped hammerhead Sphyrna lewini Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014

Great hammerhead Sphyrna mokarran Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014

Smooth hammerhead Sphyrna zygaena Vannuccini, 1999; Clarke et al., 2006a; Nalluri et al., 2014; Kim et al., 2016

Spiny dogfish Squalus acanthias Kim et al., 2016

average yearly consumption was

in Hong Kong (Bloom/SSRC

Figure 6: Mass balance of shark fin tr

2011 in fin volumes (tons) and in percent of global imports

Overall shark fin consumption for Mainland China and Hong Kong was estimated by a

mass balance of import, export and capture production data (

production of the two co

or at maximum very little capture production of sharks (Clarke

Chinas own capture production was only available as total

rays, skates and chimaeras

2001 and 2011. Clarke et al.

to be 45% of total chondrichthyan

per year for China’s own

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

ge yearly consumption was then compared to a survey on shark fin consumption

Bloom/SSRC, 2015).

: Mass balance of shark fin trade for China and Hong Kong based on average data for 2001

tons) and in percent of global imports to Hong Kong (FAO


mass balance of import, export and capture production data (Figure 6

production of the two countries were neglected as Hong Kong does

very little capture production of sharks (Clarke, 2004;

own capture production was only available as total chondrichthyan

himaeras) capture production which was about 1464 tons between

Clarke et al. (2006b) estimates the share of sharks used in the fin trade

45% of total chondrichthyan capture production, which results

per year for China’s own capture production. In order to calculate the corresponding



pared to a survey on shark fin consumption

for China and Hong Kong based on average data for 2001-

(FAO, 2015).


Figure 6). Own capture

untries were neglected as Hong Kong does not have any own

, 2004; FAO, 2015).

chondrichthyan (sharks,

was about 1464 tons between

the share of sharks used in the fin trade

, which results in about 658 tons

In order to calculate the corresponding



50

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

51

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

52

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.

53

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).

54

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 CLML (range or

mean)CF

MeHg

ww

THg

ww

MeHg

dwSD Min-Max Origin

Time

periodReference

Reference

for BL/ML

Blue shark Prionace glauca 4.1 15 110 ± 20 335 170-221 n.a 1.95 2.40 4.43 1.1 0.68–4.5 Offshore Pacific Ocean 2010 Kim et al., 2016 1

Shortfin mako shark Isurus oxyrinchus 4.3 7 120 ± 10 270 275-285 n.a 2.55 3.15 5.79 0.57 2.10-3.8 Offshore Pacific/Indian Ocean 2010 Kim et al., 2016 2

Smooth hammerhead shark Sphyrna zygaena 4.2 3 110 ± 20 335 265-? n.a 1.40 1.65 3.18 0.96 0.33–2.0 Offsh. Pacific Ocean/Korean Coast 2010 Kim et al., 2016 3

Pelagic thresher shark Alopias pelagicus 4.5 13 100 ± 30 276 260-292 n.a 1.35 1.55 3.06 0.6 0.20–2.7 Offshore Pacific Ocean 2010 Kim et al., 2016 4

Oceanic whitetip shark Carcharhinus longimanus 4.2 3 90 ± 30 270 180-200 n.a 0.39 0.53 0.89 0.52 0.09-1.2 Offshore Pacific Ocean 2010 Kim et al., 2016 5

Blacktip reef shark Carcharhinus melanopterus 3.9 26 90 ± 20 n.a 91-120 n.a 0.91 1.10 2.07 0.67 0.12–2.6 Offshore Pacific Ocean 2010 Kim et al., 2016 6

Spiny dogfish Squalus acanthias 3.9 17 80 ± 10 100 69-100 n.a 0.89 1.08 2.02 0.34 0.39-1.6 Offshore Pacific Ocean 2010 Kim et al., 2017 7

Smooth hammerhead shark Sphyrna zygaena 4.2 15 103 ± 35 335 265-? 0.8 0.01 0.01 0.01 0.004-0.007 Pacific Ocean (Mexican Coast) Escobar Sánchez et al., 2010 3

Silky shark Carcharhinus falciformis 4.2 18 87-220 250 202-260 0.8 0.09 0.11 0.21 n.s. 0.02-3.20*** Atlantic Ocean (Florida Coast) 2012-2013 O’Bryhim, 2015 8

Bigeye Thresher Shark Alopias superciliosus 4.2 8 266 ±32 350 154-341 0.8 0.41 0.51 0.93 0.15 0.16-0.67 Indian Ocean (Bay of Bengal) 2007 Penjai et al., 2008 1

Copper shark Carcharhinus brachyurus 4.2 1 131.1 n.a 230 0.8 0.20 0.25 0.45 0.1 0.09-0.34 Indian Ocean (Bay of Bengal) 2007 Penjai et al., 2008 10

Silky shark Carcharhinus falciformis 4.2 3 102 ± 7 250 202-260 0.8 0.10 0.13 0.23 0.28 0.06-0.13 Indian Ocean (Bay of Bengal) 2007 Penjai et al., 2008 8

Sandbar shark Carcharhinus plumbeus 4.1 5 n.s. 200 126-183 0.8 0.02 0.02 0.04 0.36 0.03-0.12 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 11

Common thresher shark Alopias vulpinus 4.2 6 n.s. 450 226-400 0.8 0.04 0.05 0.09 0.19 0.02-0.54 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 9

Smooth hammerhead shark Sphyrna zygaena 4.2 3 <120 335 265-? 0.8 0.04 0.06 0.10 0.12 0.10-0.32 Durban, South Africa n.s. Nalluri et al., 2014 3

Bull shark Carcharhinus leucas 4.3 3 n.s. 260 180-230 0.8 0.05 0.06 0.11 0.12 0.17-0.39 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 5

Spinner shark Carcharhinus brevipinna 4.2 4 n.s. 250 170-266 0.8 0.05 0.06 0.11 0.16 0.25-0.39 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 12

Dusky shark Carcharhinus obscurus 4.2 6 n.s. 250 220-300 0.8 0.07 0.09 0.16 0.15 0.09-0.52 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 6

Great white shark Carcharodon carcharias 4.5 4 n.s. 450-500 n.s. 0.8 0.08 0.10 0.18 0.33 0.19-0.90 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 13

Blue shark Prionace glauca 4.1 6 n.s. 335 170-221 0.8 0.11 0.14 0.25 0.63 0.04-1.73 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 1

Shortfin mako shark Isurus oxyrinchus 4.3 3 n.s. 270 275-285 0.8 0.12 0.15 0.27 0.22 0.38-0.82 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 2

Oceanic whitetip shark Carcharhinus longimanus 4.2 2 n.s. 270 180-200 0.8 0.13 0.16 0.30 n.s. 0.15-1.20 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 5

Great hammerhead shark Sphyrna mokarran 4.3 2 n.s. 370 250-300 0.8 0.15 0.19 0.34 n.s. 0.68-0.84 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 3

Copper shark Carcharhinus brachyurus 4.2 2 n.s. n.a 230 0.8 0.19 0.24 0.43 n.s. 0.50-1.46 U.S., Sri Lanka, Fiji, South Africa n.s. Nalluri et al., 2014 10

Scalloped hammerhead shark Sphyrna lewini 4.1 4 n.s. 360 200-273 0.8 0.38 0.48 0.87 1.45 0.49-3.90 Durban, South Africa n.s. Nalluri et al., 2014 3

Scalloped hammerhead shark Sphyrna lewini** 4.1 13 72 (51-81) 360 200-273 0.63 0.07 0.11 0.15 0.03 0.03-0.24 Gulf of Mexico, Mexico 2013 Mazaba Lara, 2015 3

Scalloped hammerhead shark Sphyrna lewini 4.1 1 183 360 200-273 0.8 5.96 7.45 13.53 0 n.a. Gulf of Mexico, Mexico 2013 Mazaba Lara, 2015 3

Dusky shark Carcharhinus obscurus 4.2 12 243±104 250 220-300 0.8 0.02 0.03 0.06 n.s. n.s. Pacific Ocean, Australia 2013 Gilbert et al., 2015* 6

Sandbar shark Carcharhinus plumbeus 4.1 12 172±79 200 126-183 0.8 0.01 0.01 0.02 n.s. n.s. Pacific Ocean, Australia 2013 Gilbert et al., 2015* 11

Great white shark Carcharodon carcharias 4.5 10 206±53 450-500 n.s. 0.8 0.03 0.04 0.07 n.s. n.s. Pacific Ocean, Australia 2013 Gilbert et al., 2015* 13

Smooth hammerhead Sphyrna zygaena 4.2 15 103 (93-131) 335 265-? 0.8 0.01 0.01 0.02 0.00 0.01 Gulf of California, Mexico 2006-2007 Escobar Sánchez, 2011 3

Blue shark Prionace glauca 4.1 33 180 (113-287) 335 170-221 0.8 0.01 0.01 0.02 0.01 0.01-0.07 Gulf of California, Mexico 2006-2008 Escobar Sánchez, 2011 1

Shortfin mako shark Isurus oxyrinchus 4.3 24 126 (71-158) 270 275-285 0.8 0.07 0.09 0.16 0.07 0.02-0.19 Gulf of California, Mexico 2006-2009 Escobar Sánchez, 2011 2

Pelagic thresher shark Alopias pelagicus 4.5 5 263 (222-290) 276 260-292 0.8 0.01 0.01 0.02 0.01 0.01-0.02 Gulf of California, Mexico 2006-2010 Escobar Sánchez, 2011 4

Blacktip shark Carcharhinus limbatus 4.2 8 198 (118-233) 150 120-194 0.8 0.10 0.12 0.22 0.90 0.01-0.27 Gulf of California, Mexico 2006-2011 Escobar Sánchez, 2011 14

Unknown Species 12 n.s. n.s. n.s. n.a. 0.02 0.26 0.05 0.03 N.D.-0.072 Hong Kong market n.s. Man et al., 2014

Unknown Species 12 n.s. n.s. n.s. n.a. 0.10 0.29 0.22 0.87 N.D.-0.259 Shanghai market n.s. Man et al., 2014

Unknown Species 14 n.s. n.s. n.s. n.a. 0.08 0.13 0.17 0.58 N.D.-0.209 Beijing market n.s. Man et al., 2014

Unknown Species 12 n.s. n.s. n.s. n.a. 0.19 0.23 0.42 0.14 0.0277-0.395 Haikou market n.s. Man et al., 2014

Unknown Species 12 n.s. n.s. n.s. n.a. 0.18 0.35 0.41 0.21 0.0406-0.789 Wenzhou market n.s. Man et al., 2014

n: Number of samples BL: Body length in cm *: unpublishe raw data of (Gilbert et al., 2015)

TL: Trophic Level CF: Conversion Factor for THg to MeHg concentration **62% neonates and 38% juveniles

CL: Common length in cm SD/min-Max: refering to values in fat letters ***: refers to original value in THg dry weight (0.26mg/kg)

ML: Body length at first maturity in cm n.s.: not specified n.a.: not applicable

55

Comparison of estimated MeHg exposure with US EPA safety limit for daily MeHg

exposure

Mean MeHg concentrations of all studies were 0.83 mg/kg dry weight and 0.37 mg/kg

wet weight. Based on the mean value of 0.83 mg/kg dry weight, MeHg intake was

found to be below the recommended safety limit of 0.1 µg/kg body weight per day (US

EPA, 2001b) (Table 5) if shark fin soup is consumed 3 times per year or less frequently.

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 additional consumption of

other seafood. If consumed once per month, MeHg intake exceeds the safety limits for

young children by far, while adult man and women might reach 67-77% of their safety

limits, just by shark fin consumption. For a once-per-week consumption of shark fin

soup, all groups reach or exceed safety limits by several factors, even for small 50g

portions.

Table 5: Daily intake of MeHg in % of US EPA safety limit of 1ug/kg body weight per day, for a

MeHg concentration of 0.83 k/kg dry weight.

Group Number of portions consumed

1 per year 3 per year 1 per month 1 per week 3 per week

Adult man (62 kg)* 50 2 6 22 96 287

150 6 17 67 287 861

Adult woman (54 kg) 50 2 6 26 110 329

150 6 19 77 329 988

Child (1-6 years, 16.5kg)** 50 7 21 83 357 1071

150 21 64 252 1078 3234

*(Lee et al. 1994), (Yang et al. 2005)

**(Yang et al. 2005)

Amount of shark fin

[g] in a fin soup dish

56

9 Discussion

MeHg concentrations

Average MeHg concentrations found in shark fins were in general about an order of

magnitude lower compared to shark muscle tissue (Storelli et al., 2002a; Storelli et al.,

2003; Pethybridge et al., 2010; Maz-Courrau et al., 2011; Rumbold et al., 2014;

McKinney et al., 2015). One important factor might be that the majority of samples

were of sharks below maturity lengths (at least 52% juveniles, at least 19% adults and

29% undefined). Despite the young age of sharks and comparatively low

concentrations in shark fins in general, still about a quarter of the fins had MeHg

concentrations above international safety limits.

Kim et al. (2016) found the highest mean concentrations of all studies, even if all

recorded species except the blacktip reef shark had juvenile body lengths (Castro,

1996) (Table 4).

The reason might be higher mercury contaminations in the geographic area where the

sharks were caught or their feeding habits. Smooth hammerhead sharks of a similar

size from the Gulf of California (Escobar Sánchez, 2011) had nearly 200 times lower

MeHg concentrations and similar differences can be found between the two studies

for blue shark, pelagic thresher and shortfin mako that had higher average body

lengths (Escobar Sánchez, 2011). In conclusion, trophic level, size and species specific

feeding habits cannot be significant factors in this case, unless their feeding habits are

different in different geographic locations, as it has been reported for dusky sharks in

Australia and South Africa (Gilbert, 2015; Cortés, 1999; Dudley et al., 2005). The

concentration of mercury in the water column could be an important factor, as the

region around Korea has higher mercury emissions compared to the Mexican west

coast (Figure 5), however smooth hammerhead sharks (Kim et al., 2016) came from

different locations (offshore Pacific Ocean and Korean coast).

Also compared to the other studies, trophic levels of sharks in Kim’s study were similar

or even lower and body lengths were comparatively small, which indicates a an

influence of local factors in the geographic area, where the sharks were caught, These

57

factors can be high mercury levels in the local marine environment or special feeding

habits and food web structure related to this area.

MeHg concentrations for smooth hammerhead, blue shark, shortfin mako shark

(Nalluri et al., 2014) were much lower than Kim’s results however but higher than

MeHg levels of the same species by (Escobar Sánchez, 2011). Yet, factors like body

length, age and geographic source, could be the reason. Furthermore, smooth

hammerheads (Nalluri et al., 2014) from Durban, South Africa, a region in which

different studies found elevated MeHg levels in shark muscle tissue (Watling et al.,

1981; McKinney et al., 2015; Bosch et al., 2016). High mercury levels in this region

might be correlated to an extensive usage of coal power plants in South Africa and a

mercury processing plant which discharged mercury into nearby waterways in 1990

(Papu-Zamxaka et al., 2010). Regarding body size of the smooth hammerheads, it is

only known that they were smaller than 120cm, i.e. about the same size or even

smaller than those sampled by (Escobar Sánchez, 2011). For the other species studied,

Nalluri et al. (2014) did not specify body length or geographic location.

Three studies (Escobar Sánchez et. al, 2011, Escobar Sánchez, 2011, Gilbert et al.,

2015) found comparatively low mean MeHg levels in shark fins in general and also

compared to the same species in other studies (Nalluri et al., 2014, Kim et al., 2016).

Age could be one reason, as many of the sharks in these studies were smaller than the

typical body length at first maturity. However, average body length of samples in most

of the other studies was below maturity length as well. Geographic location could be

an important factor, as already mentioned for the comparison between MeHg levels of

smooth hammerhead sharks from South Africa (Nalluri et al., 2014) and the Mexican

Pacific Ocean (Escobar Sánchez, 2011). However, (Gilbert et al., 2015) found that

mercury levels in muscle tissue of white shark (9.71 mg/kg dry weight; 206 mean body

length) and dusky shark (8.5mg/kg dry weight; 243 cm mean body length) were

comparable with a study from South Africa (great white shark: 10.26 mg/kg dry weight,

217 cm mean body length; dusky shark: 5.82 mg/kg dry weight, 164 mean body length)

(McKinney et al., 2015). This would mean that mercury contamination in Australian

waters is similar to the South African region, which has comparatively high mercury

emissions. It has to be kept in mind though, that feeding habits are also an important

factor. Dusky sharks from Australia (Cortés, 1999) have been reported to have a higher

58

percentage of cephalopods in their diet than conspecifics from South African waters

(Dudley et al., 2005). Species which feed preferentially on 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).

A finding that stands out in Gilbert’s study are the comparatively high mercury levels in

the muscle tissue of the dusky shark and great white shark in combination with

comparatively low mercury levels in their fins. All white sharks in the study were

juveniles, judging from their body length (Natanson, 2001). However it is not evident

why they would have low mercury levels in their fins but still high mercury levels in

their muscle tissue compared to conspecifics of other studies (McKinney et al., 2015).

Reasons for comparatively low MeHg levels reported by Man et al. (2014) could be

that this is the only study in which dried fins from Chinese markets were analysed. Fins

found on the market have often been de-skinned and have usually been bleached

(Vannuccini, 1999). These processes might have had an influence on their mercury

concentration. Apart from that, MeHg concentrations might have incorrect values, as a

majority of MeHg concentrations were 9% and 59% of the THg concentrations which is

much lower than MeHg-THg ratios found by Nalluri et al. (2014), 67 ± 22%, and Kim et

al. (2016), who reported an average of 77%. Other reasons might be species, origin,

trophic level and body length of the sampled sharks, which have not been presented in

the study.

Comparing MeHg levels of different species, the highest concentration was found in

one scalloped hammerhead from the Mexican Gulf (Mazaba Lara, 2015), exceeding the

safety limit of 1 mg/kg wet weight (EC, 2002, FSANZ, 2004, Health Canada, 2008) by

nearly 14 times. These might have been caused by a combination of body length,

trophic level, feeding habits and geographic location, also keeping in mind that this is

only one sample. This shark was 183 cm long, still below the typical size of first

maturity (200cm) (Compagno, 1998), but was nevertheless more than twice as large as

its conspecifics from the same study (72 cm mean body length) (Table 4). As the other

individuals in this study had comparatively low MeHg concentrations (Table 4), the

exceptionally high MeHg concentrations in this one individual of 183 cm size are

unlikely to be a result of the analytical methods used in this study. The Mexican Gulf is

59

close to areas with medium to high mercury emissions (Figure 5) which might result in

higher concentrations of mercury in the marine environment. In addition, scalloped

hammerhead sharks usually feed at greater depths (McKinney et al., 2015), i.e. their

diet contains prey items with higher exposure to mercury stored in the sediments.

Scalloped hammerhead sharks (Nalluri et al., 2014) also had comparatively high MeHg

levels, and except for the geographic location and body length, which have already

been discussed, feeding habits might be an additional factor. Other species with

comparatively high MeHg levels are blacktip reef shark and spiny dogfish (Squalus

acanthias) (Kim et al., 2016) considering their lower trophic level compared to other

species in the same study. In addition to the reasons for high average mercury

concentrations in the study itself that have already been discussed, samples of these

two species were mainly adults in terms of the blacktip shark and all adults in terms of

the spiny dogfish. Also for other studies where only adults were sampled,

comparatively high mercury levels were present, 0.41 mg/kg wet weight for the bigeye

thresher shark (Alopias superciliosus) (Penjai et al., 2008) and 0.1 mg/kg wet weight for

the blacktip shark (Escobar Sánchez, 2011) which was a high value compared to other

shark species in this study.

High MeHg levels in blacktip sharks compared to other shark species (Escobar Sánchez,

2011) might be, apart from age, related to feeding habits and reproduction mode.

Blacktip sharks are known to inhabit shallow near shore waters (McKinnney et al.,

2015), while juvenile blacktip sharks are able to enter estuaries (Rumbold et al., 2014).

Blacktip sharks, being viviparous, placental sharks, also receive larger loads of mercury

through maternal transfer. Their embryos are nourished by yolk for the first eight

weeks of the gestation, however they have a placental connection with their

mother for the remaining 9 months of gestation (Castro, 1996). In a study of mercury

levels in shark embryos, four embryos in a blacktip female had the highest mercury

levels in their tissue (0.69 ± 0.08 mg/kg) while the mother had mercury levels of 2.3

mg/kg (Adams and McMichael, 1999).

Comparatively low mercury concentrations were found in the fins of sandbar sharks

(Nalluri et al., 2014, Gilbert et al., 2015). In the latter study, 11 of 12 sampled sandbar

sharks were adults and in combination with the high trophic level, it might be

60

surprising that lower mercury levels were found (in fin tissue and in muscle tissue)

compared to dusky shark and great white shark. This might be explained by the fact

that sandbar sharks have a larger percentage of crustaceans (Cortés, 1999) and

cephalopods (Cortés, 1999; McAuley et al., 2006) in their diet, compared to dusky and

great white sharks, which have a larger percentage of large carnivorous teleost fish,

marine mammals and other elasmobranches in their diet (Walker, 1976; Cortés, 1999;

de Pinho et al., 2002). As already mentioned, cephalopods mainly accumulate

cadmium and crustaceans mainly accumulate arsenic. The hypothesis of lower mercury

levels as a result of feeding habits was also confirmed by highest levels of arsenic and

cadmium found in sandbar sharks in this study (Gilbert et al., 2015).

As an overall conclusion, mean MeHg concentrations found in the reviewed studies fit

into the common opinion that different MeHg levels result in a combination of

different factors, like tropic level, body length or age, reproduction mode, feeding

habits and Hg levels in the environment of different geographic regions.

Different MeHg levels for the same shark species of different studies might be

explained by body length or age where these were different, by geographic factors like

mercury levels in the water column, distinct feeding habits of a species in a certain

geographic region or different food web structures in different regions. However, as

interactions between the different factors that influence MeHg levels are very

complex, differences and similarities can easily misinterpreted, especially as the

number of studies and samples were rather small compared to the number of factors.

The studies reviewed here only cover a part of the species found in the shark fin trade.

Other species caught for their fins are, for example, great hammerhead, common

thresher shark, bull shark (Carcharhinus leucas), tiger shark, giant guitarfish, basking

shark, whale shark, lemon shark and tope shark (Vannuccini, 1999; Clarke et al., 2006a;

Nalluri et al., 2014).

Sharks sampled came from a number of different regions, however no studies of MeHg

in shark fins have been found for most of the geographic regions with high mercury

emissions, e.g. China, the South American West Coast, West Africa, India, Indonesia

(Figure 5) or for regions where noticeably high mercury levels in shark muscle tissue

have been reported, for example the Mediterranean (Storelli et al., 2001; Storelli et al.,

61

2003) and South Africa (McKinney et al., 2015). Apparently shark fins are used in sun-

dried form, in dried and bleached form with skin removed (Pamela, 2015) and also as

wet fins (Shea, 2016). One of the studies examined dried and processed fins from

Chinese markets (Man et al., 2014), and one study analysed sun-dried fins (Nalluri et

al., 2014), all other studies analysed unprocessed wet fins. It is uncertain, in how far

drying and bleaching processes might have an impact on the mercury concentration in

the fins.

Health risks of shark fin consumption

Even if shark fins contain lower MeHg concentrations compared to shark muscle tissue,

and other high-predator fish species like tuna and swordfish, frequent consumption of

shark fin soup can pose serious health risks, especially for children and if the soup

contains larger portions of fin tissue. MeHg levels found in the presented studies are

relevant for Chinese and Hong Kong consumers, as all shark species evaluated in this

study are present in the Hong Kong and Chinese fin markets (Vannuccini, 1999; Clarke

et al., 2006a; Nalluri et al., 2014). It is also very likely that sharks found on the Hong

Kong and Chinese fin markets originate from locations discussed in this study, due to

the global character of the fin trade. Sharks are caught all over the world and then

shipped to Hong Kong, the world’s biggest fin market, and further exported to China

(81% of Hong Kong exports in 2001-2011 (FAO, 2015)). As an example, Spain has the

third largest shark capture production in the world, is the most important shark fin

importer to Hong Kong (27% of Hong Kong imports in 2001-2011) and exported 80% of

its shark fin exports to Hong Kong in 2001-2011 (FAO, 2015). The Spanish fleet works

mainly in the Atlantic Ocean, but also in the Pacific and Indian Ocean with its main

landing ports distributed all over the world: Spain, Portugal, Cap Verde, Brazil,

Namibia, South Africa, Mauritius, Seychelles, Indonesia, French Polynesia and Peru

(Chabrol, 2015). Other crucial importers for Hong Kong were, in order of importance,

Taiwan, Indonesia, Singapore, United Arab Emirates, Mexico, Japan, Brazil, Australia,

United States, Yemen, Costa Rica and India.

62

It is uncertain, if size and age of sharks examined in this study are representative for

the global fin trade. Most of the sharks were juveniles. It is unknown whether the

actual average age of sharks caught is higher or even lower compared to the

individuals of the studies reviewed here, which means that average MeHg levels found

here could be under- or overestimated. However it is evident that most of the shark

species discussed here and most of the shark species used in the fin trade (Vannuccini,

1999; Clarke et al., 2006a; Nalluri et al., 2014) belong to the group of sharks with top

trophic levels above 4.1 (in a range between 3.1 (zebra shark (Stegostoma fasciatum))

and 4.5 (great white shark) (Cortés, 1999), which results in generally higher MeHg

levels compared to shark species of lower trophic levels.

Estimates of consumption patterns for different groups showed that frequent

consumption of shark fin can pose serious health risks. For children, even a

consumption of three times a year can be critical, if additional seafood or other

mercury sources are consumed. Consumption of shark fin soup once per month can

become critical also for adult men and women if they consume larger portions (150g)

of shark fin. Consuming shark fin soup once per week and more exceeds the US EPA

safety limit of 1 µg/kg body weight per day for all groups (except adult men eating 50g

portions: 96% of the US EPA safety limit).

Early life exposure to MeHg is of particular concern, because of its potential neuro-

developmental effects. Even the exposure of a single-meal can be critical during

pregnancy (Ginsberg and Toal, 2000), especially in the phase where the embryo is

developing (Burger et al., 2001). As MeHg has a half-life of 70 to 80 days in the human

body, fish consumption can already be critical before or at the beginning of pregnancy

(Björnberg et al., 2005). For this reason, the US Food and Drug Administration

(FDA) and the Environmental Protection Agency (EPA) recommend to sensitive

populations like pregnant women, young children and women of childbearing age to

avoid the consumption of shark, swordfish and king mackerel and to keep the

consumption of tuna and other species within limits (US EPA, 2001a; FDA, 2004).

The only available study in the literature which tested MeHg concentrations in shark

fin soup, examined 50 shark fin soup samples from restaurants all over the United

63

States (Nalluri et al., 2014). The authors found a mean MeHg concentration of 4.6

ng/ml, resulting in a dose of 1.1 μg for a 250ml bowl, which is 15% of the US EPA safety

limit (0.1 µg/kg body weight per day) for a US American with an average weight of 74

kg. It is unclear, which shark species were used for the soup and whether the soups

were freshly made or canned. The amount of shark fin used per soup was not given

either. If the average MeHg concentration of 0.23 µg/g found in dried shark fins from a

separate survey of the same study is used to calculate the necessary amount of shark

fin that would be needed for a soup which contains 1.1 µg of MeHg, the resulting

amount would be 5 g of fins. This value differs significantly from amounts reported for

a restaurant by a study from Hong Kong (150g) (Man et al., 2014) and amounts used in

home recipes (50g) (Singapore Food Recipes, 2012).

In order to evaluate health risks of shark fin consumption based on findings and

estimations of this study, additional aspects should be considered. First of all, the limit

value of 0.1 µg/kg body weight per day established by US EPA is a reference value that

has been calculated for the average US American seafood consumption patterns.

Seafood consumption in the United States is with 17.5 g fish/day (US EPA, 2001b) and

not comparable to seafood consumption of 196 g/day in Hong Kong (WWF, 2011) or

with 91 g/day in China (FAO, 2014).

Regarding EU total mercury (THg) safety limits of 1mg/kg for shark, swordfish, tuna

and other species (EC, 2002), it should be mentioned that limits for fish species with

usually lower mercury concentrations are stricter, with a limit of 0.5 mg/kg. From the

consumer health perspective this does not make any sense. Apart from that, these

limits are based on seafood consumption of European member states (60g/day for 28

EU member states in 2010 (FAO, 2007).

Evaluating the risks of shark fin consumption for the population in Hong Kong and

China, it has also be taken into account that China has by far the highest mercury

emissions in the world (McKinney, 2015) and besides seafood, other food sources,

such as rice, might have higher mercury concentrations compared to other regions.

Shark fin soup is most often served as a starter, usually consumed at wedding and

birthday banquets, family reunions, New Year and corporate events as a component of

64

an extensive menu, where other seafood dishes follow (Bloom/SSRC, 2015; Shea,

2016). This means that the exposure values shown in this study have to be seen as a

small piece of the entire mercury exposure picture. For example, consumption of a 200

g of albacore tuna, containing 1.06 µg MeHg per gram wet weight (Storelli et al., 2001)

would result in an additional dose of 212 μg of MeHg, compared to a shark fin soup

with 50g fins (42 μg). According to an internet blog, shark fin soup might have become

much more affordable in recent years, being sold in all you-can-eat shark fin buffets for

30-42 USD in restaurants of medium to high budget hotels and promotion menus

including shark fin soup for 8 USD in a cheaper restaurant (Hofford, 2009). It is not

clear whether the shark fins used are real or artificial and how much shark fin hotels

can afford to add to the dishes for such low prices. However it might mean that shark

fin consumption has become much better accessible to the population, which would

result in a more frequent and more widespread consumption over the whole

population.

It might easily be forgotten that MeHg does not only accumulate in seafood but also in

humans. With a consumption of only 10 g of fish per day humans can

accumulate significant mercury levels over a lifetime (WHO, 1991). Dickman and Leung

(1998) stated that even with a small mean mercury level of 0.12 mg/kg in fish, a Hong

Kong male adult would have accumulated 4mg/kg mercury in his hair by the age of 30,

and 7.5 mg/kg by the age of 60, which is more than the hair mercury levels of

fishermen from Minamata Bay, Japan in 1982 (Fjuiki, 1985). This study is from 1998

where mercury levels in fish and per capita seafood consumption in Hong Kong (164

g/day) were lower than today (196 g/day) (Dickman and Leung, 1998; WWF, 2011).

Adult males of this study from Hong Kong with only 5 mg/kg hair mercury levels

showed signs of subfertility. Studies from Iraq and Japan over a period of 1 - 10 years

found adults with hair mercury levels of 50 m/kg body weight that showed symptoms

of mercury poisoning (Bakir et al., 1973; Fjuiki, 1985).

Due to very unreliable records of Chinese shark fin consumption data, production data

and customs data (FAO, 2015) and a lack of respective information in the literature,

the real dimension of the shark fin trade and shark fin consumption remains unknown

and can only be estimated. Additionally individual fin consumption might vary a lot, for

65

example with more frequent consumption in the urban and high income population

and less frequent consumption in the rural or low income population.

Conclusions

Estimations of the actual dimensions of shark fin trade result in the assumption that

large quantities are still consumed despite signs of decreasing demand. MeHg

exposure by shark fin consumption is small compared to consumption meat of shark

and of other top marine predators, however frequent consumption of shark fin can still

pose serious health risks and is in particular not recommended for children and

pregnant and breast-feeding women because of the severe neurodevelopmental

damages that MeHg can cause in early-life stages. 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.

Conservative consumption of sharks and their fins would not only make a significant

difference for the health of their consumers, but also for the status of decreasing and

endangered shark populations and the marine ecosystem.

66

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Appendix - List of shark species discussed

List of shark species discussed in the reviewed studies about MeHg concentrations in shark fins.

Illustrations: Ann Hecht (http://www.biodiversityexplorer.org).

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Documents

Methylmercury concentrations in shark fins