Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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with a muscular foot, and they are manually re-

moved with a blunt knife or similar implement.

Owing to the slow growth rates and high value,

most countries regulate harvesting. Size and catch

limits and closed seasons apply in Australia, New

Zealand, South Africa and the USA, although with

variable management success.

0046 Aquaculture World aquaculture production in 1999

was estimated at 1885 tonnes, valued at US$30.6

million. China dominated with 1799 tonnes (H.

discus hannai and H. diversicolor) and Chile with

48 tonnes (H. discus hannai). Variable production

since 1990 has originated from South Africa, the

USA, Australia, and New Zealand. The principal

culture methods include suspended net culture, race-

way culture, or tidal pond culture. (See Shellfish:

Aquaculture of Commercially Important Molluscs

and Crustaceans.)

0047 Product types Most Australian abalone production

is canned, with 2340 tonnes (US$60 million)

exported to Hong Kong (40%), Japan (27%), and

Taiwan (20%) in 1999–2000. Other product types

for fished and cultivated abalone include; parboiled

and frozen on shell, frozen on shell, chilled, frozen, or

salted meat, and vacuum packing. Live abalone are

common as a value-added market product or mail

order.

0048 Issues The long growout period of most abalone, up

to 5 years, may affect aquaculture viability, although

their final value is significant and may offset cash

flow issues. Abalone are affected by potentially sig-

nificant diseases, notably the protozoan, Perkinsus

olseni, Rickettsia-like infections, and the bacterial

pathogen Vibrio.

0049Other Gastropod species The following gastropod

molluscs are of minor commercial importance in

terms of volume, but may be regionally or tradition-

ally important.

0050Periwinkles Periwinkles of the family Littorinidae

are small, intertidal algal grazers, associated with

rocky shores. They are a traditional source of food

throughout their almost-worldwide distribution, par-

ticularly in Europe, where commercial production is

greatest.

0051Production of wild-harvested Littorinids was 4828

tonnes in 1999. The principal species is Littorina

littorea, with 3144 tonnes, mainly derived from Ire-

land (3018 tonnes) and Spain (126 tonnes). Other

Littorinids, without species designation, contributed

1714 tonnes, 78% from the UK, with the remainder

from the USA and Canada. European production

is by hand harvesting from intertidal areas and

represents a source of income for both local

and transient workers. Periwinkles are bagged and

sold as a live product, or processed as brined or

pickled meat only. There is interest in cultivation,

principally in France and Scotland. French aquacul-

ture production of Littorina spp. in 1999 was 800

tonnes, worth US$2.08 million.

0052Conchs The family Strombidae includes algal or

detrital feeders, mainly associated with inshore

sandy or muddy areas throughout tropical and sub-

tropical seas. Conchs are an important marine

resource in the Caribbean, where the Queen conch

(Strombus gigas) is particularly well known. Conch

fishery production was 15 487 tonnes in 1999. The

largest producer was Mexico (8591 tonnes), followed

by Jamaica (1366 tonnes) and the Dominican Repub-

lic (1257 tonnes). Aquaculture of Strombus spp. is

developing with 9 tonnes, valued at US$61 000, pro-

duced by Netherlands Antilles and Turks and Caicos

Islands in 1999.

0053Whelks Whelks are predatory or scavenging mol-

luscs, of boreal, temperate, and tropical seas. The

term ‘whelk’ is associated with several families, with

Buccinidae and Melongenidae being commercially

important. The common whelk, Buccinum undatum,

and Busycon spp. are the principal species with

17 988 and 6181 tonnes, respectively, in 1999. The

B. undatum fishery is dominated by France (7885

tonnes), the UK (4925 tonnes), and Ireland (4561

tonnes). The USA and Canada produce all Busycon

spp., with 4624 and 1557 tonnes, respectively.

0054Nutritional features of commercially important

molluscs Table 5 provides information on the

tbl0004 Table 4 Principal commercial abalone, including main

production sources and methods

Species Commonname Main production

sourcesandmethod

Haliotis gigantea Giant Japan (F)

Haliotis tuberculata Tuberculate

or Ormer

Channel Islands,

France (F/A)

Haliotis midae Perlemoen South Africa (F/A)

Haliotis rubra Black lip Australia,

Solomon Islands (F/A)

Haliotis laevigata Green lip Australia (F/A)

Haliotis roei Roe’s Australia (F)

Haliotis conicopora Brown lip Australia (F)

Haliotis iris Paua New Zealand (F)

Haliotis rufescens Red Pacific North

America (F/A)

A, aquaculture; F, fisheries.

SHELLFISH/Commercially Important Molluscs 5227

nutritional composition of edible molluscs. It should

be noted that, particularly for molluscs consumed

whole, there is considerable variation in content, as

gonadal tissue is highly seasonal.

See also: Marine Foods: Edible Animals Found in the Sea;

Shellfish: Aquaculture of Commercially Important

Molluscs and Crustaceans

Further Reading

FAO (2001a) FAO Yearbook, Fishery Statistics: Aquacul-

ture Production 1999. Fisheries Series No. 58, vol. 88/2.

Rome: FAO.

FAO (2001b) FAO Yearbook, Fishery Statistics: Capture

Production 1999. Fisheries Series No. 57, vol. 88/1.

Rome: FAO.

Gosling E (ed.) (1992) The Mussel Mytilus. Developments

in Aquaculture and Fisheries, vol. 25. Amsterdam

Elsevier.

Guo X, Ford SE and Zhang F (1999) Molluscan aquaculture

in China. Journal of Shellfish Research 18(1): 19–31.

Hallegraeff GM (1993) A review of harmful algal blooms

and their apparent global increase. Phycologia 32(2):

79–99.

Kraeuter JN and Castagna M (eds) (2001) Biology of the

Hard Clam. Developments in Aquaculture and Fisher-

ies, vol. 31. Amsterdam: Elsevier.

Nettleton J (1985) Seafood Nutrition: Facts, Issues and

Marketing of Nutrition in Fish and Shellfish. New

York: Osprey Seafood Handbooks.

OIE (Office International des Epizooties) (2001) Inter-

national Aquatic Animal Health Code, 4th edn. Paris:

OIE.

Sheperd SA, Tegner MJ and Guzman del Proo SA (1992)

Abalone of the World. Oxford: Blackwell.

Shumway SE (ed.) (1991) Scallops: Biology, Ecology and

Aquaculture. Developments in Aquaculture and Fisher-

ies Science, vol. 21. Amsterdam: Elsevier.

Vlieg P (1988) Proximate Composition of New Zealand

Marine Finfish and Shellfish. Palmerston North, New

Zealand: Biotechnology Division, Department of Scien-

tific and Industrial Research.

Contamination and Spoilage of

Molluscs and Crustaceans

D R Livingstone, Plymouth Marine Laboratory,

Plymouth, Devon, UK

S Gallacher, Fisheries Research Services, Aberdeen,

Introduction

0001Seafood is of worldwide economic and nutritional

importance, providing about 16% of the total animal

protein consumed globally. Of this, approximately

25% is shellfish, corresponding to an annual 17 mil-

lion tons taken from sea, coastal, and estuarine

waters, with a total value on landing of about £10

billion. Included in the shellfish are crustaceans

(e.g., crab, lobster, shrimp), and bivalve (e.g., mussel,

oyster, clam, scallop), gastropod (e.g., whelk,

tbl0005 Table 5 Proximate nutritional composition (per 100 g fresh weight) of principal commercial molluscs (sources: Nettleton (1985),

Ulieg (1988))

Species Protein (g) Total fat (g) Carbohydrate (g) Energy (kJ) Cholesterol (mg) Fattyacids

(saturated/

monounsaturated/

polyunsaturated/o-3)

Moisture (%)

Abalone 20.8 1.0 0.9 415 111

0.1/0.09/0.12/ 0.04

75.7

Haliotis iris

Scallop 15.4 1.3 2.7 349 102

0.1/0.06/0.24/0.18

78.7

Pecten novaezelandiae

Oyster 11–13 2.7 (0.8–3.2) 5.8 360 47 0.49/0.36/0.90/0.71 79.7

Crassostrea gigas

Mussel 12.0 2.2 (1.2–2.1) 4.5 372 63 0.41/0.50/0.75/0.43 80.9

Mytilus edulis

Periwinkle 18.2 3.0 (1.2–4.5) 2.3 114 0.45/0.83/0.90/0.44

Littorina littorea

Hard-shell clam 9.2 1.0 (0.2–2.0) 60 11.7 40

0.16/0.16/0.33/0.24

Mercenaria mercenaria

Data from Haliotis japonica.

Data from Pecten fumatus.

Data from Placopecten magellanicus.

Data from Perna canaliculus.

Estimated from cooked product assuming 95% retention.

5228 SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans

periwinkle), and cephalopod (octopus, squid, cuttle-

fish) molluscs. The nutritional value of shellfish and

other seafood resides in their high-quality protein,

essential amino acids, vitamins, and minerals. They

are also the only natural dietary source of n-3 poly-

unsaturated fatty acids (or PUFAs), necessary for

normal development of human neural, cerebral, and

visual functions. The health benefits of this food

source are reflected in the lower risk of coronary

heart disease, hypertension, and cancer indicated in

human populations eating seafood. However, spoil-

age of shellfish can occur through two major and

distinct processes, namely the uptake of chemical

pollutants, such as metals and organic compounds,

and the accumulation of biological agents, principally

bacteria, viruses, and specific toxins produced by

phytoplankton (Table 1). In both cases, there are

usually no visible signs of contamination. Chemical

pollutants may take from days to years to show

adverse effects towards human consumers, whereas

the impact of biological agents is generally more im-

mediate and obvious, with illness occurring within

hours to weeks. (See Fatty Acids: Properties.)

0002 The section on chemical contaminants covers the

variety and levels of chemicals found in tissues from

near pristine through to highly polluted environ-

ments; the processes of uptake, metabolism, accumu-

lation, elimination, and persistence, including food

chain aspects; the toxic threat to consumers; and

monitoring and regulatory considerations. The

section on biological agents is divided into two. The

first covers the types and characteristics of shellfish

toxins and the second deals with microbial infectious

agents, particularly viruses and bacteria. Some infor-

mation is given on monitoring procedures and the

methods applied to biological contaminants of shell-

fish. In addition, the effectiveness of depuration and

processing on these agents is discussed.

0003 The terms ‘contaminant’ and ‘pollutant’ are often

used interchangeably and arbitrarily in both the

scientific and lay literature in referring to chemicals

which are generally regarded as not normal to the

environment and potentially harmful. The term ‘pol-

lutant’ will be used in this article to describe chem-

icals that are potentially toxic to the consumer that

may be synthetic, or natural but present at levels

significantly above what is considered to be in the

normal biological range. ‘Contamination’ in this

article is taken to describe the presence of pollu-

tants, algal toxins, bacteria, or viruses in the mol-

luscs or crustaceans leading to the condition of

spoilage, i.e., rendering them unsuitable for human

consumption. The term ‘xenobiotic’ also appears

widely in the scientific literature in relation to the

metabolism of pollutants, drugs, and other organic

chemicals by organisms, and refers to a chemical

that is foreign to an animal, i.e., not part of its

normal metabolism.

Pollutants

Types of Pollutants, Routes of Entry, and Tissue

Levels

0004The amount, variety and number of industrial, agri-

cultural, and other chemicals produced by humans

are continually increasing. In the early 1990s, the

Organization for Economic Cooperation and Devel-

opment (OECD) estimated that approximately 1000–

1500 new substances entered daily use each year,

adding to the already existing 60 000 substances.

Of these chemicals, it was estimated that about

11 000 were being manufactured in sufficient quan-

tities to merit environmental attention and assess-

ment. Additionally, more pollutants are produced

by the process used to treat industrial and domestic

waste such as chlorination. The major classes of

chemical pollutant are given in Table 1, most of

which are synthetic, but also include natural chem-

icals whose presence in the environment has been

increased by human activities, e.g., metals and

polycyclic aromatic hydrocarbons (PAHs). A part of

tbl0001 Table 1 Sources of contamination of molluscs and crustanceans

Nature of contamination Type of contamination Major sources

Pollutant Metals Industrial

Organic compounds Industrial, agricultural, combustion, domestic

Organometallic compounds Industrial, agricultural, boating

Shellfish toxins Paralytic, diarrhetic, amnesic, and neurotoxic shellfish

poisons

Phytoplankton

Bacteria Campylobacter spp., Escherichia coli Fecal sources

Salmonella spp.

Vibrio spp. Natural sources

Shigella spp., Staphylococcus aureus Food handling

Viruses Norwalk-like viruses, hepatitis A Fecal sources

SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans 5229

this potentially toxic material enters the aquatic

environment where it comprises a diverse range of

chemicals of both long-standing and more recent

concern. The former includes PAHs, organochlor-

ine pesticides and industrial compounds, and metals

(sometimes called heavy metals) such as arsenic

(As), cadmium (Cd), copper (Cu), iron (Fe), lead

(Pb), mercury (Hg), silver (Ag), and zinc (Zn).

Pollutants of more recent concern include polychlor-

inated dibenzo-p-dioxins (PCDDs) and polychlorin-

ated dibenzofurans (PCDFs), organophosphorous

insecticides, organotin antifouling agents such as

tributyltin (TBT), and estrogenic compounds such

as alkylphenol ethoxylate surfactants. Whereas some

of the metals, such as Cd and Hg, have as yet no

discernible biological function, most are essential to

animals and pose a toxic threat only at concentrations

considerably in excess of the normal levels. (See

Arsenic: Requirements and Toxicology; Cadmium:

Toxicology; Copper: Properties and Determination;

Iron: Properties and Determination; Mercury: Toxi-

cology; Zinc: Properties and Determination.)

0005 Pollutants enter and are dispersed in aquatic eco-

systems by various routes, including direct dis-

charge,direct use, land run-off, atmospheric

deposition, in situ production, abiotic and biotic

movement, and food chain transfer. Pollutants are

generally readily taken up into the tissues of molluscs,

crustaceans, and other resident animals. The uptake

into the individual organism can occur via several

routes, including from bottom sediments, suspended

particulate material, the water column and food

sources. The major routes of input depend on the

particular dietary and ecological lifestyle of the

species, e.g., via algae, particulates, and water

column for filter-feeding bivalves; detritus and

mixed diet for scavenging crabs; and the food chain

for carnivorous cephalopods. All species of molluscs

and crustaceans will therefore likely take up pollu-

tants from the environment into their tissues, and

any pollutant present in the environment is likely to

be present in the tissues of resident organisms. Excep-

tions to the latter are those pollutants that are not

bioavailable to the animal, e.g., those that for physi-

cochemical reasons are tightly bound and ‘locked up,’

such as PAHs in sediment particles and metals in

biological granules.

0006 The extent to which pollutants taken up by shellfish

remain in their tissues depends on a number of factors,

including continuing input from the environment,

duration of exposure, biotransformation and depur-

ation, which are discussed in a later section. Pollutants

have been measured in the tissues of many different

commercial and noncommercial crustacean and mol-

luscan species, and many different types of pollutants

have been detected. The crustaceans include crabs,

crayfish, lobsters, prawns, shrimps, copepods, amphi-

pods, and barnacles. The molluscs include clams,

cockles, mussels, oysters, scallops, snails, whelks,

winkles, squids, chitons, and limpets. Examples of

the range of pollutants detected in shellfish tissues

are given in Table 2. Also, taken up into the tissues

of shellfish are radionuclides associated with the nu-

clear fuel cycle, such as uranium and the transura-

nium elements plutonium (Pu) and americium (Am),

i.e.,

239,240

Pu,

238

Pu, and

241

Am.

0007The major factor determining the levels of pollu-

tants in the tissues of shellfish is the levels in the

immediate environment and their food sources. Thus,

the more polluted the environment, the greater the

chemical contamination of the tissues. This is parti-

cularly evident in pollution incidents, such as oil

spills, and in comparisons of urban or industrial

tbl0002Table 2 Examples of pollutants detected in crustaceans and/or

molluscs in the field

Ty p e C h e m i c a l s

Metals Cadmium, chromium, cobalt, copper,

iron, lead, mercury, manganese,

nickel, silver, zinc

Organic compounds

Aliphatic hydrocarbons Acyclic isoprenoids, n-alkanes (C

), UCM

PAHs and related

compounds

Many two-through to six-ring PAHs,

including naphthalene,

phenanthrene, anthracene,

fluorene, fluoranthene, pyrene,

benzo[a]anthracene, chrysene,

benzo[b]fluoranthene,

benzo[k]fluoranthene,

benzo[a]pyrene, benzo[e]pyrene,

dibenz[ah]anthracene,

benzo[ghi]perylene indeno[1,2,3-

cd]pyrene, dibenzothiophenes,

methylated PAHs

PCBs Many of the possible 209 congeners,

including tri-, tetra, penta-, hexa-,

hepta-, octa-, nona-, and

decachlorobiphenyls

PCDDs, PCDFs 2,3,7,8-Tetrachlorodibenzodioxin,

others

Other organochlorine

compounds

Chlordanes, chlorinated cyclodienes

(e.g., aldrin, dieldrin), DDTs, DDDs,

DDEs, hexachlorobenzene,

hexachlorocyclohexanes (e.g.,

lindane), polychlorinated phenols

(e.g., pentachlorophenol)

Organometallic Compounds Tributyltin, triphenyltin,

methylmercury

UCM, unresolved complex mixture of alkanes; PAH, polycyclic aromatic

hydrocarbon; PCB, polychlorobiphenyl; PCDD, polychlorinated dibenzo-p-

dioxin; PCDF, polychlorinated dibenzofuran; DDT, 1,1-bis(4-chlorophenyl)-

2,2,2-trichloroethane; DDD, 1,1-dichloro-2,2-bis(p-chlorophenyl)ethane;

DDE, 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene.

5230 SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans

locations with remote pristine environments. The pol-

lutants are generally not distributed evenly through

the different tissue types, but are often highest in

tissues concerned with the processing of food, such

as the hepatopancreas and digestive gland, and in the

case of organic pollutants are highest in tissues high in

fat, such as digestive tissues (hepatopancreas/digest-

ive gland) and ripe reproductive tissues, e.g., mantle

of mussels. Some pollutants, such as organopho-

sphorous pesticides, are short-lived and readily

broken down in the environment, and therefore

their concentrations are often low in the tissues of

animals. Examples of levels of pollutants found in

different tissues of crustaceans and molluscs from

different types of environment are given in Tables 3

and 4 respectively.

0008 Because of the marked accumulation of pollutants

by shellfish, the analysis of their tissues has for many

years been used in pollution monitoring as a measure

of environmental contamination. Mussel and oyster

species in particular have been extensively used in

so-called ‘mussel watch’ monitoring programs be-

cause of their bioaccumulating properties, sessile

nature, wide geographical distribution, and resistance

to general stress. Such programs have been carried

out on the coasts and inland waters of North and

South America, Europe, Asia, and Australia, includ-

ing the North and South Atlantic, Pacific, Indian,

and Mediterranean regions. Common species of

marine and fresh-water mussel used include the blue

mussel (Mytilus edulis), Mediterranean mussel (Myti-

lus galloprovincialis), American mussel (Mytilus cali-

fornianus), horse mussel (Modiolus modiolus), swan

mussel (Anodonta cyngea), and green-lipped mussel

(Perna viridis). Commonly used oyster species include

Crassostrea virginica and Crassostrea gigas.

Processes of Uptake, Depuration,

Biotransformation, Bioaccumulation, and

Persistence

0009Organic pollutants The accumulation of organic

pollutants in shellfish (i.e., bioaccumulation) depends

principally upon the processes of uptake and depur-

ation, with probably lesser roles for active excretion,

‘storage’ and biotransformation. The uptake and dep-

uration of pollutants by shellfish depend on a number

of physicochemical and biological variables, but

mainly on the environmental concentration of the

chemical and its fat-solubility. Other environmental

and biological factors that may affect uptake and

depuration to varying degrees include temperature,

tidal cycle, dissolved organic material, algae, nutri-

tional state, feeding habits, and reproductive con-

dition and/or seasonality.

0010Uptake and depuration are thought to be largely

passive processes, involving movement and equilib-

rium of the chemical between aqueous (external en-

vironment) and biotic (animal) compartments. Rates

of uptake are usually greater from the water column

than from sediments and abiotic particles. Distribu-

tion of the pollutant within the animal depends on

route of intake and tissue fat levels, e.g., gills are an

initial site of bioaccumulation where uptake is from

the water, whereas digestive tissues are important for

pollutant input from food sources. If the external

exposure concentration of the pollutant is constant,

then the uptake usually involves an initial linear rate,

followed by the eventual reaching of a maximal tissue

equilibrium concentration. Uptake of the pollutant

into the shellfish will thus continue for as long as

pollutant is present in the environment and/or food

source, and until the tissue equilibrium concentration

is reached. Multiphasic patterns of uptake have also

tbl0003 Table 3 Examples of pollutant levels in different tissues of crustaceans from different environments

Animal Chemical Location Tissue Level (mgg

1

wet wt)

Barnacle (Balanus amphrite) Copper Hong Kong Total tissue 12–694

Zinc – clean to polluted 545–1871

Cadmium 1.1–1.5

Crab (Carcinus maenas) Copper Scotland Total tissue 6

Zinc 19

Cadmium 0.2

Total PAHs (2–5-ring) Norwegian fjord Total tissue 0.03–0.05

Crab (Uca pugnax) Total PAHs Oil spill Total tissue 18.3–56

Crab (Carcinus maenas) Total PCBs Norwegian fjord Total tissues 0.03–0.10

Crab (Carcinus mediterraneus) Total PCBs NE Mediterranean Sea Total tissues 0.3–3.6

Blue crab (Callinectes sapidus) Total PCBs S. Carolina, USA – industrial gradient Muscle 0.20–7.73

Dry weight converted to wet weight levels using a conversion factor of  0.2.

PAH, polycyclic aromatic hydrocarbon; PCB, polychlorobiphenyl.

Source of date: Livingstone DR (1991) Organic xenobiotic metabolism in marine invertebrates. In: Gilles R (ed.) Advances in Comparative and

Environmental Physiology, vol. 7, pp. 1–185. Berlin: Springer-Verlag; and Langston WJ and Bebianno MJ (eds) (1998) Metal Metabolism in Aquatic

Environments. Ecotoxicology Series, vol. 7. London: Chapman and Hall.

SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans 5231

been seen, which have been interpreted in terms of

equilibration of the pollutant into multiple compart-

ments (tissue, cellular, subcellular, or molecular)

within the animal. The initial rate of uptake and

final tissue equilibrium concentration of the pollutant

increase with increasing concentration of the chem-

ical in the environment.

0011 The tendency of organic pollutants to bioaccumu-

late increases with increasing fat-solubility of the

chemical and with increasing levels of fats (lipids) in

the shellfish tissue. For many organic pollutants taken

up by molluscs and crustaceans, a linear relationship

exists between the equilibrium bioconcentration

factor (BCF; ratio of pollutant concentration in the

animal to that in the environment) and fat-solubility,

i.e., chemical hydrophobicity, the latter being meas-

ured in terms of either octanol/water coefficient (K

)

or water-solubility. Positive linearity of BCF with K

in shellfish is seen over a log K

range of about 2–6

which encompasses most of the organic pollutants

of environmental importance, i.e., aliphatic hydrocar-

bons, many polycyclic aromatic hydrocarbons (PAHs)

and polychlorobiphenyls (PCBs), dioxins, and other

organochlorine compounds. Thus, pollutants of high

hydrophobicity, such as PCBs and 1,1-bis(4-chloro-

phenyl)-2,2,2-trichloroethanes (DDTs), show high

BCF values of up to 100 000. Deviations from

these relationships also occur, particularly for very

hydrophobic compounds (K

> 6), such as the five-

ringed PAH benzo[a]pyrene and high hexachloropo-

lybiphenyls, which show BCFs less than expected. In

other cases, higher BCFs than predicted from K

have been seen, e.g., > 100-fold higher bioaccumula-

tion of the antifouling paint TBT by mussel (Mytilus

edulis). These enhanced BCF are probably due to

strong interactions between pollutant and the bio-

logical system, particularly proteins. The time re-

quired for the uptake of the pollutant to reach the

tissue equilibrium concentration is relatively quick

for water-soluble compounds, e.g., hours for toluene

(log K

< 3), but may take weeks or even months for

very fat-soluble compounds, e.g., hexachlorobiphe-

nyl (log K

> 7).

0012Partial or complete decrease in pollutant levels in

the environment, either by cessation of input, or

transfer of the shellfish to clean water, will result in

depuration, i.e., loss of pollutant from the tissues

back into the water. This depuration will continue

tbl0004 Table 4 Examples of pollutant levels in molluscs from different environments

Animal Chemical Location Level (mgg

1

wet wt)

Mussel (Mytilus edulis) Silver Mediterranean, France, Italy 0.02–0.38

Cadmium 0.08–1.18

Cobalt 0.10–1.48

Chromium 0.10–5.76

Copper 0.48–30.8

Iron 29.8–444

Manganese 0.66–14.0

Nickel 0.18–2.82

Lead 0.54–23.4

Zinc 19.4–129

Mercury England 0.02–0.21

Green-lipped mussel (Perna viridis) Cadmium Hong Kong 0.02–0.29

Copper 1.7–55.6

Mercury 0.02–0.03

Mussel (Mytilus edulis) Total PAHs Norwegian fjord – clean to industrial 0.45–3.09

(2–5-ring)

Total PAHs Norwegian fjord – industrial gradient 0.74–29.9

(2–5-ring)

Mussel (Perna viridis) Total PCBs Hong Kong coast – industrial gradient 0.01–0.38

Mussel (Mytilus galloprovincialis) Total PCBs Mediterranean coast 0.02–1.63

Mussel (Mytilus edulis) Total PCDDs Norwegian waters 0.03–0.30

Hexachlorohexane UK waters 2.4–15.2

Mussel (Mytilus californianus) Total DDT, DDE, DDD S. California, USA – clean to industrial 0.02–1.05

Mussel (Mytilus edulis) Tributyltin European waters 0.04–2.04

USA, Pacific waters 0.02–2.2

Values are for whole-body tissues, dry weight converted to wet weight levels using a conversion factor of 0.2.

PAH, polycyclic aromatic hydrocarbon; PCB, polychlorobiphenyl. DDT, 1,1-bis(4-chlorophenyl)-2,2,2-trichloroethane; DDE, 1,1-dichloro-2,2-bis

(p-chlorophenyl)ethylene; DDD, 1,1-dichloro-2,2-bis(p-chlorophenyl)ethane. Source of data: Livingstone DR (1991) Organic xenobiotic metabolism in

marine invertebrates. In: Gilles R (ed.) Advances in Comparative and Environmental Physiology, vol. 7, pp. 1–185. Berlin: Springer-Verlag; Gosling E (ed.)

(1992) The Mussel Mytilus: Ecology, Physiology, Genetics and Culture. Amsterdam: Elsevier; and Lasserre P and Marzollo A (eds) (2000) The Venice Lagoon

Ecosystem. Inputs and Interactions Between Land and Sea. Man and the Biophere Series, vol. 25. Paris: Parthenon Publishing.

5232 SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans

as long as the environmental pollutant level remains

very low by dilution into a large body of water,

replacement with fresh clean water, or removal of

the pollutant. Depuration is normally exponential,

with the pattern of loss being resolved into an initial

faster phase followed by a longer-term slower phase.

The rate of loss during the phases can be described

in terms of the depuration half-life (t

1/2

), i.e., the

time required for the tissue concentration of contam-

inant to be reduced by 50%. Single-phase depur-

ation has also been seen in some instances.

Depuration can also be markedly affected by the

length of time of the exposure period. Short-term

exposure results in rapid and complete, or almost

complete, elimination of the pollutant during subse-

quent depuration, whereas longer-term exposure is

followed by slower and often incomplete elimin-

ation. This is particularly evident for the depuration

of petroleum hydrocarbons by bivalve molluscs

where the t

1/2

of depuration is seen to increase with

increasing time period of previous exposure

(Table 5). Therefore it may be very difficult, if not

impossible, to remove all organic pollutants by dep-

uration in clean water from shellfish that have had a

long history of exposure to pollution in the field. For

pollutants of similar fat-solubilities, the chemical

structure of the chemical may also affect uptake

and depuration, e.g., PAHs were bioaccumulated

less from sediments than were PCBs of similar log

by mussel (M. edulis), but PCBs were depurated

more slowly than equivalent PAHs. (See Polycyclic

Aromatic Hydrocarbons.)

0013The bioaccumulation of organic pollutants in shell-

fish can also be affected by active excretion processes,

‘storage,’ and biotransformation. Although know-

ledge of these processes is relatively limited, their

quantitative impact is indicated not to be great, at

least in the long term, because the bioaccumulation of

most types of organic pollutant occurs according to

a simple water/octanol partitioning model, where

water is the environment and octanol represents the

animal, i.e., BCF is directly related to K

. Active

excretion has been indicated in some studies; e.g.,

naphthalene lost from gills and kidney of mussel

(M. edulis), but not others; e.g., the anus and kidney

played little or no role in the clearance of naphthalene

from crab (Hemigrapsus nudus). Active energy-

driven pumps that function to pump xenobiotics out

of cells, variously known as P-glycoproteins, multi-

drug resistance (MDR) transporters or multixeno-

biotc (MXR) transporters, have recently been

identified in a wide range of aquatic organisms, in-

cluding molluscs and crustaceans. However, rela-

tively little is yet known about their ability to pump

out organic pollutants, although hydrocarbons, pen-

tachlorophenol, DDTs, and PCBs have been indicated

as potential substrates for some shellfish species, but

not others.

0014Fecal material and urine can also make a contribu-

tion to elimination, e.g., in the loss of sulfadimethox-

ine from lobster (Homarus americanus). The term

‘storage’ is probably a misnomer, but organic pollu-

tants are known to accumulate in specific subcellular

organelles, namely lysosomes that are present in high

tbl0005 Table 5 Increase in duration of exposure period results in increased length of time for subsequent depuration of a range of

hydrocarbons by various bivalve shellfish

Shellfish Pollutant Exposure period Depurationhalf-life

Mussel (Mytilus edulis) Naphthalene 4 h 2 h

Heptadecane 24 h <24 h

n-alkanes 2 days 0.5 days

Naphthalenes 2.8 days 0.9 days

Alkanes 41 days 3.1 days

4–6-ring PAHs 40 days 12–30 days

Benzo[a]pyrene Field 16 days

Alkanes/PAHs Field 70 days

Clam (Rangia cuneata) n-alkanes 8 h > 3 h

2–3-ring PAHs 8 h 3 h

Anthracene 15 h 5 days

Benzo[a]pyrene 1 day 8 days

Oyster (Crassostrea virginica) n-alkanes 8 h 4.5 h

2–3-ring PAHs 8 h 6 h

Horse mussel (Modiolus modiolus) Phenanthrene 2 days 1.5 days

Clam (Macoma balthica) Alkanes/PAHs 170 days > 60 days

Clam Alkanes/PAHs Field > 120 days

PAHs, polycyclic aromatic hydrocarbons.

Data source: Livingstone DR (1991) Organic xenobiotic metabolism in marine invertebrates. In: Gilles R (ed.) Advances in Comparative and Environmental

Physiology, vol. 7, pp. 1–185. Berlin: Springer-Verlag.

SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans 5233

numbers in tissues such as the hepatopancreas and

digestive gland. They can also become chemically

bound to macromolecules, including in particular

proteins and DNA, to form macromolecular adducts.

Such adducts are likely eventually removed and the

macromolecules repaired or replaced, but neverthe-

less will contribute to the persistence of a pollutant in

an animal. Examples of pollutants indicated, or dem-

onstrated, to give rise to adducts in shellfish include

chlorinated paraffins, vinyl chloride, PAHs, nitro-

aromatics, fenitrothion (organophosphate pesticide),

picric acid, and phthalate ester plasticizers. In

common with all other animals, shellfish also possess

a suite of biotransformation enzymes, present in sev-

eral tissues but highest in the hepatopancreas or di-

gestive gland, the major function of which is to

convert fat-soluble organic xenobiotics such as pollu-

tants to water-soluble excretable products (metabol-

ites). Modeling of biotransformation in shellfish

shows that: (1) biotransformation is significantly

slower than uptake, such that bioaccumulation of

the original pollutant inevitably occurs; and (2) gen-

erally crustaceans have slightly higher biotransforma-

tion rates than molluscs for both hydrocarbons and

other types of organic pollutants. Paradoxically, bio-

transformation, which is meant to speed up elimin-

ation, can contribute to persistence if the rate of loss

of metabolite to clean water is slower than the rate of

depuration of the original unchanged pollutant. This

has been seen for mussel (M. edulis) for 1-naphthol

and for several crustaceans for phenoxyacetic and

phenylacetic acid herbicides, hydrocarbons, and

sulfadimethoxine.

0015 Because pollutant uptake from the environment is

largely a passive process determined by physicochem-

ical principles, the rates of uptake are therefore some-

what similar for different animal groups, including

shellfish and vertebrates such as fish. In contrast,

rates of biotransformation of pollutants and excre-

tion of the water-soluble metabolites are intrinsic to

the particular animal or group of animals, and

depend on the level of biotransformation enzymes in

the organism and the effectiveness of its excretory

mechanisms. These are generally significantly greater

in vertebrates such as finfish than in invertebrates

such as shellfish. Rates of biotransformation ap-

proach more rates of uptake in finfish than shellfish,

and can therefore reduce the long-term bioaccumula-

tion of readily metabolizable pollutants in the former

compared to the latter. In food chains, the differences

between uptake and biotransformation therefore

result in different patterns of bioaccumulation in

different animal groups, with readily metabolized

pollutants, such as PAHs, reaching highest tissue

concentrations near the bottom of food chains in

shellfish, and poorly metabolized or recalcitrant pol-

lutants, such as many PCBs, accumulating to highest

tissue concentrations in vertebrates at the top of food

chains.

0016Metals and radionuclides The uptake and depur-

ation of metals have some, but not all, similarities

with the situation for organic pollutants. Bioaccumu-

lation depends on chemical speciation of the metal,

routes and mechanisms of uptake, intracellular com-

partmentation, cellular control of metal levels, excre-

tion, and depuration. All of these processes may be

strongly affected by the species’ particular biology,

including morphology, physiology, feeding mode,

and environmental adaptations. Overall, there is

probably more variability in bioaccumulation trends

with respect to species and individual pollutant for

metals compared to organic compounds, particularly

for crustaceans. For example, below a certain thresh-

old metal tissue level, a range of bioaccumulating

properties for essential metals such as Zn and Cu

may be seen in crustaceans, ranging from regulation

(i.e., no accumulation where rate of uptake equals

rate of excretion) to accumulation, e.g., at an expos-

ure concentration of 100 p.p.b., Cu was bioaccumu-

lated from sea water by the barnacle Elminius

modestus but not by the decapod Palaemon elegans.

0017Direct uptake of metals and radionuclides from the

water column is a quantitatively important process

because most metals occur in highly water-soluble

forms, e.g., Am, Cd, Hg, Pb, Pu, and vanadium.

Rates of uptake are generally proportional to the

metal concentration in the water column. Uptake is

thought to occur mainly by passive transport pro-

cesses, involving both diffusion of polar metal ions/

complexes and partitioning of hydrophobic metal

organic complexes into lipid membranes. The influ-

ence of dissolved organic matter, particulates, and

food on uptake is complex. Depending on the nature

of these substances and the metal, either increased or

decreased bioaccumulation can occur, e.g., in one

study, food contributed significantly to the uptake of

Am, Pu, and Pb, but not Cd, by mussel (M. edulis).

The gills are an important site for soluble metal

uptake, whereas digestive gland is a major site for

particulate-bound metal uptake. The latter occurs

via an active transport process, endocytosis, which

results in the fusion of the endocytotic vesicles, con-

taining the metal, with the lysosomes. The kidney is

another major site of metal accumulation, and metals

can also be incorporated into the shells of, for

example, bivalves. Major sites of localization of

radionuclides in bivalves include byssal threads and

the periostracum covering the shell. The metals are

retained within the tissues by binding to various

5234 SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans

specific and nonspecific sites. The former includes

specialized proteins called metallothioneins, special-

ized sulfur- or phosphate-containing insoluble inor-

ganic granules, and lysosomal residual bodies, all of

which have high affinities for metals. The inorganic

granules in particular can result in very high levels of

metals in certain shellfish, e.g., metal/phosphate gran-

ules in scallops, winkles, and crabs.

0018 Exposure of the shellfish to clean water will result

in depuration and loss of part or all of the previously

accumulated metal. Like the situation for organic

pollutants, the depuration is biphasic with a fast ini-

tial loss followed a slower subsequent loss, describ-

able in terms of t

1/2

values. Overall t

1/2

values can

vary from days to several months. The observations

on depuration profiles for both metals and organic

pollutants indicate at least a two-compartment model

(often called the ‘fast’ and slow’ compartments) of

pollutant uptake and release. The slow compartment

likely includes fat stores, lysosomes, and macromol-

ecular adducts for organic pollutants, and metal-

lothioneins, lysosomes, and granules for metals. The

phenomenon of induction, i.e., increased synthesis of

metallothionein, in response to metal exposure could

also contribute to the slow compartment. Active

excretion of metals in molluscs can occur through

elimination of residual bodies by the process of exo-

cytosis. Such processes appear to be more important

for some metals than others, resulting in very differ-

ent t

1/2

for certain metals and species, e.g., in mussels

(Mytilus spp.), the t

1/2

for Cu was 9 days compared to

7 months for Cd. Metal that is nonbioavailable in

metal/phosphate granules can also be eliminated

when prey are eaten by predators, e.g., the metal/

phosphate granules contained in barnacles eaten by

whelks are lost from the latter in its feces. The conse-

quence of such nonbioavailability is that generally

metals, like readily metabolizable organic pollutants

such as PAHs, are present in highest tissue concen-

trations at the bottom of food chains, i.e., in shellfish,

and do not bioaccumulate to higher concentrations in

top predators, such as fish and other vertebrates. The

exception is Hg that is bioaccumulated along food

chains, but principally in the form of fat-soluble

methylmercury.

Toxic Threat and Regulatory Standards

0019 The vast range and diversity of pollutants that are

produced by human activities permeate to varying

degrees every part of the earth’s ecosystem, from

urban and industrial centers through to remote areas

such as deep oceans and the Arctic and Antarctic

circles. For example, polychlorinated aromatic com-

pounds such as PCBs, PCDDs, and PCDFs appear

ubiquitous, having been found in air, soot particles,

sediments, water column, and all types of animal

tissue from shellfish to fish and other vertebrate wild-

life, to human fat, milk, and blood serum. Therefore,

unlike the biological agents described later, and

excepting localized pollution incidents such as the

Minamata disease tragedy, the main potential health

threat to humans of pollutants in shellfish is probably

their contribution to the general body-burden of such

chemicals. The latter can receive a wide range of

inputs of pollutants from various sources, including

other foodstuffs, cooking procedures, smoking, and

atmospheric pollution. Depending on the fat content

and which part is eaten, shellfish may make a particu-

lar contribution in the case of very fat-soluble organic

pollutants, such as PAHs, PCBs, dioxins, and other

chlorinated hydrocarbons. Because there are so many

pollutants that may be present in shellfish, the poten-

tial deleterious effects that they may cause in the

short, medium, and long term are many and diverse

and encompass most known mechanisms of chem-

ical-mediated toxicity. Examples of some of these

are given in Table 6. The extent to which such illness

and effects will be manifested or not will depend on

the dosage of pollutant to which the consumer is

exposed, of which the shellfish may contribute only

a part. Some routes of exposure may be much more

important for some pollutants than others, e.g., at-

mospheric pollution can be a major route for Pb.

0020Localized poisoning incidents involving shellfish

have happened in the past, but largely due to major

ignorance at the time. In the infamous Minamata

disease incident in the 1950s, industrial waste that

included mercuric chloride was discharged into Min-

amata Bay in Japan. The water-soluble Hg was meth-

ylated by bacteria to fat-soluble methylmercury that

was then bioaccumulated and passed along the food

chain. The combination of the high toxicity of Hg,

and the seafood forming a major part of the diet,

resulted in illness appearing within a year and even-

tually over 70 deaths and 700 cases of poisoning in

the local population.

0021Chemical analysis of processed commercial sea-

food in the 1970s through to the 1990s revealed

highest levels of PAHs in molluscs, lower levels in

crustaceans, and lowest in fish, consistent with their

general capacity for biotransformation. In one study,

the carcinogenic PAH benzo[a]pyrene was detectable

in commercial molluscan seafood from nine coun-

tries. Levels of benzo[a]pyrene were 0–36 ng g

1

wet weight in molluscs compared to 0–8ngg

1

wet

weight in crustaceans, and were higher in smoked

seafood and in animals collected or kept near obvious

environmental sources of PAHs, e.g., lobsters held in

a commercial tidal pound constructed of creosoted

timber had levels of benzo[a]pyrene of 2300 and

SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans 5235

281 ng g

1

wet weight in the hepatopancreas and

edible tail meat respectively.

0022 Various national and international bodies issue

regulations and/or advise on matters relating to the

health quality, production, and marketing of fishery

products, including shellfish, e.g., the European

Union (EU) issues directives which pertain both to

member countries and to exports received within the

EU. In the UK, environmental quality standards

(EQS) exist for some pollutants, whereas guidelines

only are identified for others. Examples of these for

shellfish from UK waters are given in Table 7. In the

USA, the Food and Drug Administration (FDA) issues

action levels and guidelines for shellfish; guidelines

are also issued by the US Environmental Protection

Agency (EPA). Depending on the country, contraven-

tion of statutory EQS, action levels, or guidelines can

form the basis for closure of a shellfish fishery and/or

removal of products from outlets. Guidelines may

also be used in conjunction with risk assessment to

provide health advice on minimizing chronic effects

of pollutants such as PCBs, dioxins, and Hg through

limiting shellfish consumption. This advice may be

targeted at particularly vulnerable groups such as

pregnant and nursing women, children and women

of child-bearing age. On the other hand, in the case of

certain metals, higher levels may be permitted in some

shellfish species if environmental or tissue levels are

considered to be high naturally, e.g., Cu and Zn.

Chemical analytical techniques exist for many thou-

sands of pollutants, but routine measurement is gen-

erally limited to a select few which are of particular

concern (Table 7). The bodies responsible for the

measurement, and the conditions of measurement

(e.g., sampling frequency), vary with the national or

international organization. The depuration proced-

ures required for treatment of shellfish prior to

marketing (i.e., to remove bacteria and other

biological agents) will also remove most or many of

the pollutants.

Shellfish Toxins

0023Shellfish, particularly marine bivalve molluscs, can be

contaminated with naturally occurring poisons, also

known as toxins, phycotoxins, or marine biotoxins.

It is common to refer to the toxins under generic

headings (Tables 1 and 8), with each grouping

tbl0007Table 7 Outlineofstandards/guidelinesformaximum

acceptablepollutantlevelsinshellfishfromUKwaters

PollutantEnglandandWales

(mgkg

1

wetwt)

Scotlandand

NorthernIreland

(mgkg

1

wetwt)

PCBsMolluscs0.02–0.1Mussel0.3–1.0

Crustaceans0.01–0.05

DDTFishliver0.5Mussel0.03–0.1

DieldrinFishliver0.2–0.3Mussel0.015–0.05

HexachlorobenzeneFishliver0.1Mussel0.03–0.1

MercuryMolluscs0.12–0.2Mussel0.2–0.6

Crustaceans 0.1–0.3

Cadmium Mussel 0.4–1.0 Mussel 1.0–3.0

Copper Some molluscs 5.0 Mussel 3.0–6.0

Crustaceans 20–30

Lead Some molluscs 4.0 Mussel 3.0–10

Crustaceans 1.0

Zinc Some molluscs 100 Mussel 50–100

Crustaceans 100

For full details see the specified reports.

Data from CEFAS Science Series Aquatic Monitoring Report no. 47,

Annex2.(www.cefas.co.uk/homepage.htm)

Data from Fisheries Research Services, Aberdeen: Henderson A and

Davies IM (2001) Review of the regulation and monitoring of aquaculture in

Scotland, with emphasis on environment and consumer protection. FRS

Marine Laboratory Report 01/01.

Dry wt converted to wet wt using a conversion factor of  0.2.

PCBs, polychlorobiphenyls; DDT, 1,1, bis(4-chlorophenyl)-2,2,

2-trichloroethane.

tbl0006 Table 6 Examples of possible deleterious effects and mechanisms of toxicity of pollutants found in shellfish to human consumers

Pollutant Toxic effect Biochemicaleffects

PCBs, PCDDs, PCDFs Cancer, developmental effects, immune

dysfunction, liver damage, reproductive effects,

thymic atrophy, weight loss

Induction of CYP1A, UDPGT

Certain PAHs, e.g., benzo[a]pyrene Cancer Induction of CYP1A, DNA adduct formation

Aromatic amines Bladder cancer

Organophosphorous pesticides Neuromuscular and neurotoxic effects Inhibition of acetyl cholinesterase

Cadmium Kidney damage, bone damage Induction of metallothionein

Lead Neurotoxic effects, bone and kidney damage Interference of heme and porphyrin

synthesis

Mercury and methyl mercury Neurotoxic effects, memory loss, loss of muscle

coordination, cerebral palsy

Binds to protein sulfhydryl groups

Data are for humans and/or mammalian studies.

PCB, polychlorobiphenyl; PCDD, polychlorinated dibenzo-p-dioxin; PCDF, polychlorinated dibenzofuran; CYP1A1, cytochrome P4501A1; UDPGT,

UDP-glucuronyl transferase; PAH, polycyclic aromatic hydrocarbon.

5236 SHELLFISH/Contamination and Spoilage of Molluscs and Crustaceans