Journal of Applied Microbiology Symposium Supplement 1999,85, 2348-2428
The effects of pollution on fish health
B. Austin
Department of Biological Sciences, Heriot-Watt University, Riccarton, Edinburgh, UK
1. Summary, 234s
2. Introduction, 234s
3. T h e presence of pollutants in the aquatic
environment, 235s
4.The presence of pollutants in the tissues of aquatic
animals, 235s
4.1 In-vitro studies, 235s
4.2 Investigations using animals obtained from t h e
aquatic environment, 235s
5. Effects of pollutants on aquatic animals, 236s
6. Effects of pollutants on disease processes in
aquatic animals, 237s
1. SUMMARY
Potentially harmful substances-e.g. pesticides, heavy metals
and hydrocarbons-are often released into the aquatic environ-
ment. When large quantities of pollutants are released there
may be an immediate impact as measured by large-scale
sudden mortalities of aquatic organisms, e.g. fish kills result-
ing from contamination of waterways with agricultural pes-
ticides. Lower levels of discharge may result in an
accumulation of the pollutants in aquatic organisms. T h e end
results, which may occur long after the pollutants have passed
through the environment, include immunosuppression,
reduced metabolism, and damage to gills and epithelia. How-
ever, the link between adverse water quality and fish diseases
is not proven. Alleged pollution-related diseases include epi-
dermal papilloma, fin/tail rot, gill disease, hyperplasia, liver
damage, neoplasia and ulceration. Many surveys have indi-
cated a greater proportion of diseased fish in polluted com-
pared to non-polluted marine sites. Yet, the value of such
surveys may be questioned. Specific examples of fish diseases
thought to reflect the effects of pollution include surface
lesions attributed to Serratia plymuthica, finand tail rot caused
by A m n o n a s hydrophila and PseudomonasJluorescens, gill dis-
ease resulting from the activity of Flavobacterjum SPP., vib-
CiIrWondence to: P r o l k o r B. Austin. Depurtmcnt ifBl&gt~~/s
f ~ ~ w ~ - W Unwrsif.y,
Uft Rirrurton, Edinburgh E1114 I/K.
6.1 The influence of contaminated fish food, 237s
6.2 The effect of heavy metals, 238s
6.3 Hydrocarbons, 238s
6.4 Nitrogenous compounds, 238s
6.5 Pesticides, 238s
6.6 Sewage, 238s
6.7 Stress, 239s
6.8 Unspecified causes, 239s
7. Conclusions, 239s
8. References, 239s
riosis as caused by Vibrio anguillarum, and enteric redmouth
(causal agent, Yersinia ruckeri). Research indicated that some
of the diseases caused by Aeromonas, Flavobacterium and
Pseudomonas resulted from generally adverse water quality,
i.e. higher than usual quantities of organic material, oxygen
depletion, changes in p H values and enhanced microbial
populations. Some infections with Serratia and Yersina may
well have reflected contamination of waterways with domestic
sewage, e.g. leaking septic tanks. At least one outbreak of
vibriosis was linked to high concentrations of copper, which
may have debilitated the fish making them more susceptible
to disease.
2. INTRODUCTION
There is considerable confusion over the precise role of pol-
lution on fish health (Bucke 1991, 1997). Nevertheless, there
is good evidence that long-term exposure to certain pollutants
has adversely affected the health of some fish species,
especially in the North Sea and Great Lakes. A summary of
the available information concerning pollution and fish health
suggests that:
1. Pollutants may enter the aquatic environment as a result
of natural occurrences, such as the collapse of algal blooms
~ ~ ~and/or~ as a result
~ ~ human
of ~ endeavours,
, leading to adverse
water quality.
0 1999 The Society for Applied Microbiology, 85, 2345-242s

Some pollutants, e.g. pesticides, have been found in the
tissues of aquatic animals.
High levels of certain pollutants, e.g. from oil spillages,
may be directly responsible for deaths of large numbers
of aquatic animals.
T h e presence of some pollutants may 'stress' aquatic ani-
mals possibly leading to greater susceptibility to attack by
pathogens.
T h e presence of organic material, e.g. faecal debris, in
water may lead to an increase in microbial populations,
some components of which may cause fish diseases.
It should be emphasized that mortalities among popu-
lations of aquatic animals do not necessarily imply the pres-
ence of a disease in the fish population. Thus, large-scale fish
kills resulting from spillage of pesticides or hydrocarbons into
waterways do not constitute a disease as defined by Campbell
et al. (1979). Furthermore, disease may develop long after the
pollutant has been removed from the aquatic environment.
In this circumstance, it would be difficult to prove that the
original pollution led to disease.
3. THE PRESENCE OF POLLUTANTS IN THE
AQUATIC ENVIRONMENT
It is well established that at various times pollutants enter the
aquatic environment. Examples of pollutants include:
1. Hydrocarbons: e.g. creosote (Sved et al. 1997), resulting
from accidental discharge from tankers or deliberate spill-
age during wartime (Evans et al. 1993; Turrell 1994; New-
ton and McKenzie 1995)
2. Pesticides: e.g. organochlorines (Dethlefsen et al. 1996),
dioxin (Guiney etal. 1996) and l,l,l-trichloro-2,2-bis-(l)-
chlorophenyl) ethane ( D D T ) (Fitzsimons 1995).
3. (Heavy) metals: e.g. tin, tributyltin and triphenyltin, have
been incorporated in anti-fouling paints used extensively
to prevent bioattachment and thence fouling of the under-
surfaces of ships (Horiguchi et al. 1995); arsenic, copper,
zinc (Gassman et al. 1994; Han et al. 1997); cadmium, lead
and mercury which are discharged in industrial effluents
(Gassman etal. 1994; Bernier etal. 1995).
4. Pulp mill effluents (Lehtinen etal. 1984; Sandstrom 1994;
Couillard and Hodson 1996).
5. Plastics (Goldberg 1995).
6. Organic sewage, including faecal debris, which may con-
tain large populations of bacteria (Dudley e t a / . 1980).
7. Inorganic nitrogen, as nitrate, nitrite and ammonia, which
may be derived from fish farming (i.e. aquaculture) activi-
ties (Ziemann e t a / . 1992) and agricultural run-off.
8. Toxins, such as from the collapse of dinoflagellate blooms
. " et al. 19961.
lNorra
There may be a continual or intermittent/irregular dis-
charge of pollutants into authorized or unauthorized dump
sites in the aquatic environment. However, adverse water
Q 1999 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement 85, 2348-242s
POLLUTION AND FISH HEALTH 235s
quality may occur widely, and not be related directly to
human activity. An example of the lattcr would be terrestrial
runoff into the sea, particularly during storms. This runoff
may enhance the organic loading of the receiving waters,
reduce the salinity, and cause localized temperature changes.
However, the extent and longevity of pollutants in the aquatic
environment needs to be established, and this will certainly
involve effective monitoring programmes (Ibe and Kul-
lenbcrg 1995).
4. THE PRESENCE OF POLLUTANTS IN THE
TISSUES OF AQUATIC ANIMALS
Many laboratory-based investigations and studies of animals
obtained from the aquatic environment have highlighted the
presence of pollutants in the tissues of a wide range of aquatic
animals.
4.1. In-vitro studies
A wide range of pollutants, including creosote fractions (Sved
et d. 1997), thiocyanate (Lanno and Dixon 1996), dide-
cyldimethylammonium chloride (Wood et af. 1996) and DDI'
(Fitzsimons 1995), have been found to be taken up into
aquatic organisms via waterborne exposure. However, it is
questionable what if any relevance such laboratory data have
to occurrences in the aquatic environment.
4.2. Investigations using animals obtained from the
aquatic environment
There is a good correlation between the presence of pollutants
in animals and the levels in the surrounding aquatic environ-
ment. For example, heavy metals, including copper and zinc,
have been detected in the tissues of rabbitfish (Siganus ora-
min) obtained from the polluted waters around Hong Kong
(Chan 1995), in a range of invertebrates and vertebrates
obtained from Taiwan (Han etal. 1997), and cod (Gadus
morhua) caught from off the coast of Newfoundland, Canada
(Hellou e t a / . 1992). Cadmium, lead and mercury have been
identified in small amounts in fish from the Great Lakes
(Bernier eta/. 1995). Interestingly, the levels for cadmium,
lead and mercury in cod were below the maximum permitted
limit for foods (Hellou eta/. 1992), casting some doubt on the
significance of the concentrations to the health of the animal.
Similarly, mercury, in concentrations considered to be insuf-
ficient to cause human health problems, has bccn found in
apparently healthy fish and shellfish collected from the vicin-
ity of discharges from a chlor-alkali plant in India (Joseph
and Srivastava 1993).
Crustaceans, fish and molluscs, obtained from the vicinity
of a sewage outfall, have been determined to be contaminated
with pesticides, namely chlordane, dieldrin, hexachloro-
2368 B. AUSTIN
benzene and DDT (hliskiewicz and Gibbs 1991).Similarly,
DDT and polychlorinated-biphenyls (PCB), organochlorine
residues and 2,3,7,8-tetrachlorobenzo-p-dioxin have been
found in fish caught from the Vaike Vain Strait in western
Estonia (Voigt 1991), from the North Sea (Dethlefsen e t a l .
1996),and the Great Lakes (Guiney et al. 1996),respectively.
Yet, there was not any indication that the compounds were
actually causing any harm to the animals.
5. EFFECTS OF POLLUTANTS ON AQUATIC
ANIMALS
T h e exposure of aquatic animals to high concentrations of
pollutants may lead rapidly to death (Fig. 1). Here, there is
a clear association between pollution and mortalities. Yet,
exposure to lower quantities of pollutants may lead to chronic
darnage, the implications of which need not be manifested
for a comparatively long period (e.g. hlayer e t a / . 1993).Here,
the animals may be weakened/immunosuppressed (Vos et ul.
1989;Sovenyi and Szakolczai 1993), leading to colonization
and ultimately death by opportunist bacteria and fungi (Aus-
tin and Austin 1993). Winter Stress Syndrome, which is
characterized by greatly reduced levels of lipid in fish, seems
likely to result from stresses, including the presence of pol-
lutants in the aquatic environment (Lemly 1997).
Sub-lethal concentrations of pesticides, namely atrazine
and lindane (Cossarini-Dunier 1987), heavy metals (O’Neill
1981) including cadmium (Sovenyi and Szakolczai 1993),
components of sewage (Secombes et ul. 1991,1992)and mem-
bers of the aquatic microflora (Robohm e t a / . 1979; Evans
e t a [ . 1997) have been documented to affect the immune
system of fish, either by stimulating or suppressing the pro-
duction of antibodies. Exposure to sewage sludge has been
implicated with effects on growth and protein synthesis in
common dab (Limanrla Iamanda) (Houlihan etal. 1991). In
addition, liver damage in fish has been associated with con-
tamination by components of sewage sludge (Moore et al.
1996), cadmium (Sovenyi and Szakolczai 1993) and thio-
Fig. 1 Exposure to high and low concentrations of toxicants may
lead rapidly to death or interact with other stressors, e.g. pathogens,
resulting in the development of disease.
0 1999 The Society for Applied Microbiology, Journal of Applied Microblology Symposium Supplement 85, 234s-2428
cyanate (Lanno and Dixon 1996). Similarly, renal problems
have resulted from contamination with cadmium (Sovenyi
and Szakolczai 1993), whereas exposure to thiocyanate has
led to the development of anaemia and an interference with
thyroid function (Lanno and Dixon 1996). Hydrocarbons
have been associated with breakages in the double-stranded
DNA, and enzyme induction in common dab (Everaarts et al.
1994).hloreover, stress factors (plasma cortisol, glucose and
lactate) have been elevated and swimming performance
decreased following chronic exposure of rainbow trout
(Onrorhynchus m,ykiss) to didecyldimethylammonium chlor-
ide (Wood etul. 1996).
External damage, notably to the gills, opercula, finage and
skin, has been reported following exposure to a wide range of
compounds, including creosote (Sved eta/. 1997), cadmium
(Sovenyi and Szakolczai 1993),ammonia, copper and phenol
(Kirk and Lewis 1993) and pulp mill effluents containing
chlorine (Lindesjoo and Thulin 1994;Lindesjoo et al. 1991;
Sandstrom 1991).T h e effects of ammonia, copper and phenol
on the ultrastructure of rainbow trout gills has been inves-
tigated by scanning electron microscopy (Kirk and Lewis
1993),and it was deduced that ammonia caused the devel-
opment of circular depressions and pitting of the gill
epithelium. Exposure to copper led to fusion of the gill lamel-
lae, and swelling to the tips of the filaments and epithelium,
whereas phenol destroyed the epithelial layers as far as the
cartilage (Kirk and Lewis 1993).
hlill effluents have been a common factor in many studies
of abnormalities/disease in fish (Lindesjoo and Thulin 1994;
Lindesjoo e r a / . 1991;Sandstrom 1991).For example during
1982-87 in the Baltic Sea, Sandstrom (1994)reported the
presence of abnormalities, including gonad malfunction, poor
embryo quality and mortalities, in coastal fish which were
apparently exposed to mill effluent. Coincidentally after 1984,
the toxicity of the effluent was reduced in turn by substituting
chlorine dioxide for chlorine and thence in 1992 by eli-
minating the use of chlorine altogether. This action reduced
the amount of organochlorines in the effluent, and with these
changes, there was a concomitant reduction in abnormalities
in the fisb populations.
Dinoflagellate toxins have been responsible for major fish
kills. In one example, exposure to the dinoflagellates resulted
in the erosion of the epithelium leading to the development
of ulceration (Noga etal. 1996). Even if the fish recovered
from the effects of the dinoflagellates, bacteria and/or fungi
colonized the ulcers. So, the dinoflagellate toxins initiated the
development of ulcers which became colonized by micro-
organisms. This scenario was considered to explain the epi-
demics of skin ulcers occurring in fish along the Atlantic
seaboard of the USA (Noga etal. 1996).
Pesticides, including DDT, have been associated with
reduced hatching, blue sac disease and swim-up syndrome
mortalities in lake trout eggs (Salzielinus nama.yrush) (Fitz-

simons 1995). Yet, these laboratory studies indicated that the
concentrations of pesticides necessary to affect eggs were
much higher than the levels found in feral fish eggs.
6. EFFECTS OF POLLUTANTS ON DISEASE
PROCESSES IN AQUATIC ANIMALS
T h e development of disease will reflect interactions between
the host, the disease causing situation and stressors (Fig. 2;
Austin and Austin 1993). Much of the work attempting to
correlate fish disease with aquatic pollution has stemmed
from the results of surveys, many of which have been carried
out in the North Sea (e.g. Dethlefsen and Watermann 1980;
Dethlefsen e t a / . 1987; hlcVicar e t a / . 1988; Vethaak and ap
Rheinallt 1992). Thus, fish are caught with nets, and the
relative incidence of disease determined. One conclusion from
these surveys is that larger numbers of diseased fish occur
generally in the polluted compared to clean/unpolluted
locations. Yet, the distinction between polluted and clean
sites is imprecise. Therefore, there would be some uncertainty
as to what comprises a truly polluted or clean site. hloreover,
it is uncertain from surveys how long fish might have been
in a polluted environment prior to capture. Thus, the effects
of fish migration on the incidence of disease needs to be
considered (Bucke ern/. 1992; Vethaak et al. 1992; Jacquez
e t a / . 1991). Nevertheless, it is accepted that disease reflects
complex interactions between the host and external factors,
which may involve pollution (Vethaak and Jo1 1996).
Fish diseases, which have been reported to be associated
with pollution of the aquatic environment, include epidermal
-
papilloma (Dethlefsen and Watermann 1980; Premdas and
Metcalfe 1991), fin and tail rot (Vethaak 1992; Vethaak e t a / .
1996), gill disease/hyperplasia (Kirk and Lewis 1993), liver
disease (Malins e t a l . 1980, 1987; Peters e t a l . 1987; Vethaak
etal. 1996), neoplasia (Malins e t a / . 1980; Bucke and Feist
1993; Depledge 1996; Vethaak and Jo1 1996), parasitic disease
(Pascoe and Cram 1977; Overstreet and Howse 1977; Das
Ei-rrR I recovered from diseased animals. However, it was considered
e.g. pollutant
CAUSING SITUATION
e.g. pathogen
Fig. 2 Interactions between the host, stressors and a disease
causing situation, e.g. a pathogen, are necessary for the development
of clinical disease.
0 1999 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement85, 2343-2428
POLLUTION AND FISH HEALTH 2378
and Shrivastava 1984; Khan 1987; Miiller 1987; Khan and
Thulin 1991), skin disease/ulceration (Vethaak 1992; Vethaak
and Jo1 1996) and viral diseases, e.g. lymphocystis (Vethaak
and Jo1 1996; Vethaak etal. 1996). T h e trigger for these
diseases has been blamed at various times on contaminated
diets (Landsberg 1995), heavy metals (e.g. Rmrdsaether eta/.
1977), hydrocarbons (e.g. Khan 1987), nitrogenous
compounds, i.e. ammonia (Kirk and Lewis 1993) and nitrites
(Hanson and Grizzle 1985), pesticides (e.g. Voigt 1994), sew-
age (e.g. Austin and Stobie 1992) and unspecified pollutants
(e.g. Vethaak and Jol 1996). Of these, fin/tail rot, gill dis-
ease/hyperplasia and ulceration may be linked to bacterial
involvement. Perhaps, the pollutants weaken the fish, leading
to colonization by micro-organisms and thence the devel-
opment of clinical disease. T h e action of viruses and, possibly,
the presence of carcinogens, may well lead to neoplasias.
Certainly, numerous ‘hot spots’ have been described where
the occurrence of tumours in fish and shellfish have been
correlated with increased concentrations of anthropogenic
compounds (see Depledge 1996). However, proof of cor-
relation between the occurrence of specific pollutants and
disease has seldom been documented. Surveys, which have
pointed to a correlation between pollution and disease, have
generally not considered the nature or concentration of the
pollutant(s). It would be relevant to determine: (1) whether
or not there could be a synergistic interaction between two
or more pollutants; and/or (2) the minimum exposure time
necessary to instigate a disease cycle.
6.1. The influence of contaminated fish food
Although definite proof was lacking, Landsberg (1995) con-
sidered that toxins in food, i.e. macroalgae (Caulerpu s ~ .or )
benthic dinoflagellates (Gumbzerrlzsrus to.rrcus), may have been
responsible for heavy mortalities in tropical reef fish in Flor-
ida, USA during 1993-1994. Pathological examination
revealed the presence of head lesions, ulcerations, fin and tail
rot, and the presence of a mucus layer on the body surface
(this may well have indicated exposure to an irritant; Austin
and Austin 1993). Bacteria, amoebae and turbellarians were
that these organisms were likely to have been secondary
invaders of the already damaged fish rather than the primary
cause of the mortalities (Landsberg 1995). It should be
emphasised that many serious microbial pathogens may well
need an already weakened host in order to initiate disease
(Austin and Austin 1993). Yet, whether or not such weak-
ening results from pollution is rarely considered.
T h e spread of some serious pathogens has been attributed
to contaminated fish food used in aquaculture. For example,
the causal agents of botulism (Huss etul. 197-1), myco-
bacteriosis (Dulin 1979), streptococcicosis (hlinami 1979),
and a new disease of chinook salmon (0.tshunytsc.hu) caused
2388 8 . AUSTIN
by Rhodococcus sp. (Claveau 1991) have possibly been trans-
mitted in diets containing contaminated fish products.
6.2. The effect of heavy metals
Research has suggested a role for heavy metals in exacerbating
microbial fish diseases. In particular, the debilitating effects
of copper, in terms of concentration and time of exposure,
have been well documented with regard to increasing sus-
ceptibility to vihriosis (e.g. Vibrio anguillarum; b d s a e t h e r
et al. 1977) and infections by Edmardsiellu tardu (Mushiake
et al. 1981). It was observed that exposure to copper resulted
in coagulation of the mucus layer of the gills, which inhibited
oxygen transport and caused respiratory stress (Westfall
1945) or reduced the number of lymphocytes and gra-
nulocytes in the blood, leading to reduced phagocytosis
(Mushiake etal. 1985).
T h e harmful effects of titanium dioxide on fish have been
repeatedly emphasized (e.g. Dethlefsen and Watermann
1980; Lehtinen 1980; Dethlefsen e t a / . 1987). For example,
as a result of a large scale survey of 5912 fish caught in Dutch
coastal waters during 198fk-1988, a higher incidence of disease
(epidermal hyperplasia/papilloma, lymphocystis, liver nod-
ules and infections with Glugeu spp.) was noted in the com-
mon dab collected from dump sites which received acids of
titanium dioxide compared to control areas (Vethaak and van
der Meer 1991). This reinforced a previous study which
reported a link between the incidence of epidermal papilloma
in common dabs in relation to dumping of titanium dioxide
wastes (Dethlefsen and Watermann 1980).
6.3. Hydrocarbons
Exposure to hydrocarbons has led to impairment of the
mucus, the development of defective immune systems, an
increased incidence of parasitism, the induction of hyper-
plasia and liver hypertrophy, and mortalities (Lehtinen 1980;
Fletcher e t a l . 1982; Haensly etal. 1982; Khan 1987, 1991).
Experimental evidence has demonstrated that fish may
develop epidermal lesions, fin erosion or die following
exposure to suspended sediments containing a high molecular
weight creosote fraction (Sved etal. 1997). In comparison, a
low molecular weight creosote fraction led to the appearance
of head lesions, i.e. around the mouth, nares and opercula
(Sved et al. 1997). It would have been useful to determine
whether or not there was any microbial involvment in the
development of these lesions.
6.4. Nitrogenous compounds
Some data have suggested the deleterious effect of nitrogen-
ous compounds on fish health. Thus, the presence of nitrites
at 6 m g I - ’ of water increased the susceptibility of channel
0 1999 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement 85.2348-2428
catfish (Ictalurus punctatus) to infection by Aeromonas hyd-
rophila (Hanson and Grizzle 1985).
6.5. Pesticides
T h e presence of pesticides, e.g. DDT and PCB, in the aquatic
environment has been associated with many diseases, includ-
ing ‘cauliflower disease’, lymphocystis and ulceration (Voigt
1991) and liver neoplasia (Moore rt a / . 1996). Malformations
in common dab, flounder (Plutichthys jlrsus), plaice (Pleu-
ronrctes plutessu) und whiting (hlrrlangus sp.) embryos from
the southern North Sea during 1984-1995 were considered
to be linked to pollution with organochlorines (Dethlefsen
rtul. 1996). T h u s as a result of long-term surveys, these
authors considered that the malformations resulted possibly
from low water temperatures that predisposed the embryos
to the effects of organochlorines.
Liver disease, including neoplasia, has been described in
winter flounder (Pleuronectes americanus) from Boston, USA,
particularly in the region of a sewage outfall (Moore etal.
1996). Of relevance, these workers noted that during 1987-
1993, there was a reduction in the incidence of neoplasia
concomitant with a decline in output of chemicals, notably
DDT and other chlorinated hydrocarbons, into the receiving
waters.
6.6. Sewage
An association has been made between fish diseases/parasitic
infestation and unknown components of sewage dumping
(Siddall etal. 1994). For example, in a survey of 16 sites in
the Dutch Wadden Sea, a higher incidence of skin ulcers and
fin rot was noted in fish caught near fresh water drainage
sluices than elsewhere (Vethaak 1992). Pollution by domestic
sewage, i.e. leakage from a septic tank, was attributed to a
new skin disease, which was characterized by the presence of
extensive skin lesions and muscle necrosis, in rainbow trout
(otherwise infected with enteric redmouth disease for which
there might also be a link with sewage sludge; Dudley e t a l .
1980) in Scotland during 1992 (Austin and Stobie 1992).
From diseased fish, two new pathogens, i.e. Serratia ply-
muthica and Pseudomonas pseudoalcaligenes, were recovered.
Interestingly, the skin lesions-but not enteric redmouth dis-
ease-declined substantially after the leaking septic tank was
repaired.
Eutrophic waters associated with faecal pollution and high
levels of organic material, have been attributed as the cause
of diseases by enteric bacteria, including Citrobacter freundii
(Austin and Austin 1993), E. tarda (hleyer and Bullock 1973),
Providencia rettgeri (Bejerano et al. 1979) and Serratia mar-
cescens (Baya etal. 1992). In addition, poultry faeces, which
was used to fertilize fish ponds, was blamed for mass mortality

in silver carp (Hypophthalmichthysmolitrix) in Israel (Bejer-
ano et al. 1979).
6.7. Stress
Unspecified stressors have been attributed to oxygen
deficiency and a statistically significant increase in the inci-
dence of epidermal papilloma, lymphocystis and skin ulcers
particularly in female common dab from waters around
Denmark during the summers of 1988-1993 (Mellergaard
and Nielsen 1995). Also, stress, attributed to unnamed
environmental factors, has been associated with septicaemia
in fish from Nigeria (Oladosu e t a l . 1994).
6.8. Unspecified causes
Many articles have considered the effect of non-specific pol-
lution/pollutants on the incidence of disease. For example
Vethaak et al. (1996) discussed the disease development in
flounder contained in mesocosms with contaminated dredged
spoil. Compared to clean systems, fish in the polluted
environment displayed a higher incidence of lymphocystis
and liver damage leading to (liver) neoplasia. Yet, there was
no appreciable difference in the development of epidermal
disease. These results indicated the health problems associ-
ated with long-term exposure to pollutants at levels com-
parable to those in the aquatic environment. In a parallel
study, the polluted waters of the Lower Lake of Bhopal were
blamed on the incidence of tumours (fibromas) in catfish
(Heteropneustesfossilis) (Qureshi and Prasad 1995).
7. CONCLUSION
It has been clearly established that pollutants enter the aquatic
environment (e.g. Sved et al. 1997), and may be found in the
tissues of aquatic vertebrate and invertebrate animals (e.g.
Han e t a l . 1997). Illoreover, some pollutants are instrumental
in damaging aquatic organisms (e.g. Lanno and Dixon 1996).
However, there is only limited evidence that pollutants are
actually responsible for the development of disease. Indeed,
there is negative evidence that has demonstrated that the
incidence of disease diminishes when pollution ceases (see
Sandstrom 1994). Certainly, many surveys have reported a
higher incidence of diseased animals from polluted compared
to control sites (e.g. Vethaak and ap Rheinallt 1992). Yet,
a weakness in most surveys concerns the absence of good
qualitative and quantitative data about the pollutants. There
remains serious doubts about the relative level of pollutants
in so-called polluted and clean sites. Moreover, it is specu-
lative what influence water movement and fish migration
patterns have on the results of the surveys. Nevertheless,
there is accumulating evidence that some pollutants immuno-
suppress/weaken fish (Sovenyi and Szakolczai 1993). In this
(Q 1ggg The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement 85, 2348-2423
POLLUTION AND FISH HEALTH 2398
case, such animals may well be more likely to succumb to
disease. Curiously, some forms of damage, e.g. to the gills
and skin (Sved e t a l . 1997), attributable to pollutants are
reminiscent of the signs associated with some infectious
diseases, namely gill disease and ulceration (Austin and Aus-
tin 1993), respectively. In this connection, it is relevant to
mention the increasing recognition of atypical isolates of rler.
salmoniczda as a cause of skin lesions/ulcerations in native
marine fish (e.g Wiklund and Bylund 1993; Nakatsugawa
1994; Pedersen e t a l . 1994; Wiklund etal. 1994; Wiklund
1995; Wiklund and Dalsgaard 1995; Larsen and Pedersen
1996; Austin et al. 1998). It remains to be proven whether or
not this taxon, which hitherto has been associated with the
disease furunculosis of freshwater salmonids (Austin and
Austin 1993), interacts mostly with marine fish that may have
been already weakened by pollutants.
8. REFERENCES
Austin, B. and Austin, D.A. (1993) Bucieriul Fish Puthugens, Diseuse
uf Fumed and IVild Fish, 2nd edn. Chichester: Ellis Horwood.
Austin, B. and Stobie, hl. (1992) Recovery of Serruiiu plymuthrru
and presumptive Psrudumonas pseuduultulrgrnes from skin lesions
in rainbow trout, Oncurh,ynehus mykiss (Walbaum), otherwise
infected with enteric red mouth.Juurnul of’Fish Diseuses 15, 541-
543.
Austin, B., Austin, D.A., Dalsgaard, I. et ul.( 1998) Characterization
of atypical Aerumonus sulmunrcidu by different methods. Systemuri~.
und Applied Microbiulogy 21, 50-64.
Baya, A.M., Toranzo, A.E., Lupiani, B. and Santos, Y. and €Ietrick,
F.hl. (1992) Serrurru murcescens: a potential pathogen for fish.
Journal of’Frsh Diseuses 15, 15-26.
Bejerano, Y., Sarig, S., IIorne, M.T. and Roberts, R.J. (1979) hlass
mortalities in silver carp Hypophthalmichthys mulrtrtx (Valen-
ciennes) associated with bacterial infection following handling.
-?ournu1 oJ’Fish Diseuses 2 , 4 9 4 6 .
Bernier, J., Brousseau, P., Krzystyniak, K., Tryphonas, €1. and
Fournier, hl. (1995) Immunotoxicity of heavy metals in relation
to Great Lakes. Envrrunmentul IIeultk Perspectives 103 (Suppl.),
23-34.
Bucke, D. (1991) Current approaches to the study of pollution-
related diseases of fish. Bulletin uf’the Euruprun .4ssuciariun ufFrsh
Putholngists 11, 46-53.
Bucke, D. (1997) Facts and myths regarding pollution and fish
health. Bulletin ofthe European Associution qf Ftsh Puthologists 17,
19 1-1 96.
Bucke, D. and Feist, S.W. (1993) Histopathological changes in the
livers of dab Limunda limunda L. Juurnul ($Fish Diseuses 16,281-
296.
Bucke, D., Vethaak, A.D. and Lang, T. (1992) Quantitative assess-
ment of melanomacrophage centres (hlMCs) in dab f,imundli
limundu as indicators of pollution effects on the non-specific
immune system. Marine Progress Serres 91, 193-196.
Campbell, E.J.M., Scadding, J.G. and Roberts, R.S. (1979) ‘The
concept of disease, British i2lrdiculJournul2, 757--762.
Chan, K.M. (1995) Concentrations of copper, zinc, cadmium and
240s B. AUSTIN
lead in rabbitfish (Siganus oramin) collected in Victoria Harbour,
fiong Kong. itlarine Pollution Bulletin 31, 277-280.
Claveau, R. (1991) Nephrite granulomateuse ii Rhodococcus spp. dans
un elevage de saumons de I'Atlantique (Siilmo salar). Midicine et
Vitirinaire Quibec 21, I6@16l.
Cossarini-Dunier, hl. (1987)Effect of the pesticides atrazine and
lindane and of manganese ions on cellular immunity of carp,
(,')ymniis cirrprn. Ji~iimiilo/Fi.rh Biology 31 (Suppl.), 67-73.
Couillard, C.hl. and Hodson, P.V. (1 996) Pigmented macrophage
aggregates: a toxic response in fish exposed to bleached-kraft mill
emuent? Environmental Toxicology and Chemistry 15, 1844-1854.
Das, M.C. and Shrivastava, '4.K. (1984)Fish mortality in Naini Tal
Lake (India)due to pollution and parasitism. Hydrobir~logyJ~jurnal
20,6@64.
Depledge, h1.H. (1996) Genetic ecotoxicity: an overview.Journal./'
Experimental Marinr Biology and Ecology 200, 57-66.
Dethlefsen, V. and Watermann, B. (1980)Epidermal papilloma of
North Sea dab, Limantlu limunilii: histology, epidemiology and
relation to dumping from Ti02industry. ICES Special Meeting
on Diseases of Commercially Importun1 Marine Fish and Shellfirh 8,
1-30.
Dethlefsen, V., Watermann, B. and Hoppenheit, M. (1987)Diseases
of North Sea dab (Limanda limanda L.) in relation to biological
and chemical parameters. Archiz*e,firFishereimissenschaji 37, 101-
237.
Dethlefsen, V., Von Westernhagen, If. and Cameron, P. (1996)
hlalformations in North Sea pelagic fish during the period 1984-
95. ICESJourniil oJMurine Science 53, 1024-1035.
Dudley, D.J., Guentzel, M.N., Ibarra, M.J., Moore, B.E. and Sagik,
B.P. (1980)Enumeration of potentially pathogenic bacteria from
sewage sludges. '4pplied imd Enrironmentul Microbiology 39, 1 18-
126.
Dulin, h1.P. (1979)A review of tuberculosis (mycobacteriosis) in
fish. I/eteriniiry hfedicine/Smull ..lnimal Clinician h1a.y 1979,735-
737.
Evans, M.I., Symens, P. and Pilcher, C.W.T. (1993)Short-term
damage to coastal bird populations in Saudi Arabia and Kuwait
following the 1991 Gulf War marine pollution. Marine Pollution
Bulletin 27, 157--lhl.
Evans, M R . , Larsen, S.-J., Riekerk, G.H.M. and Burnett, K.G.
(1 997) Patterns of immune response to environmental bacteria in
natural populations of the red drum, Sciaenops ocrllatus (Lin-
208,
naeus). Journal of' Experimental Alarine Biology and Ecolog~~
87-105.
Everaarts, J.M., Sleiderink, H.M., Den Besten, P.J., €lalbrook, R.S.
and Shugart, L.R. (1994) Molecular responses as indicators of
marine pollution: DNA damage and enzyme induction in Lim-
anda limanda and Asterias rubens. Environmental Health Per-
spectives 102, 37-43.
Fitzsimons, J.D. (1995) A critical review of the effects of con-
taminants on early life stage (ELS) mortality of lake trout in the
Great Lakes. Journal of Great Lakes Research 21 (Suppl.), 267-
276.
Fletcher, G.L., King, M.J., Kicenuik, J.W. and Addison, R.F.
(1982)I.iver hypertrophy in winter flounder following exposure
to experimentally oiled sediments. Compararioe BjochemjSryy and
Physiology C 73, 457-462.
Gassman, N.J., Nye, L.B. and Schmale, h1.C. (1994)Distribution
(B 1999 The Society for Applied Microbiology.
of abnormal biota and sediment contaminants in Biscayne Bay,
Florida. Bulletin of Marine Science 54, 929-913.
Goldberg, E.D. (1995) Emerging problems in the coastal zone for
the twenty-first century. Marine Pollution Bulletin 31, 152-158.
Guiney, P.D., Cook, P.M., Casselman, J.M., Fitzsimons, J.D.,
Simonin, H.A., Zabel, E.W. and Peterson, R.E. (1996)Assess-
ment of 2,3,7,8-tetrachlorodibenzo-p-dioxininduced sac fry mor-
tality in lake trout (Sulvelinus namaycush) from different regions
of the Great Lakes. Canadian 3~1urnalof Fisheries and Aquatic
Sciences 53, 2080-2092.
Haensly, W E . , Neff, J.hl., Sharp, J.R., Morris, A.C., Bedgood,
h1.F. and Reom. P.D. (1982)Histopathology of Pleuronertes pla-
tessa L from Aber Wrac'h and Aber Benoit, Brittany, France:
long-term effects of the Amoco Cadiz crude oil spill. Journal of
Fish Diseases 5, 365-391.
Han, B.C., Jeng, W.L., Jeng, ILI.S., Kao, L.T., hleng, PJ. and
Huang, Y.L. (1997)Rock-shells (Thai.r clurigera) as an indicator
of As, Cu, and Zn contamination on the Putai Coast of the
Black-Foot disease area in Taiwan. Archives of' Environmental
Contamination and Toxicolgy 32,456461.
Hanson, L.A. and Grizzle, J.M. (1985) Nitrite-induced pre-
disposition of channel catfish to bacterial diseases. Progressive Fish
Culturist 47, 98-101.
Hellou, J., Warren, W.G., Payne, J.F., Belkhode, S. and Lobel, P.
(1992)Heavy metals and other metals in three tissues ofcod Gadus
morhua from the northwest Atlantic. Marine Pollution Bulletin 24,
4521158.
Horiguchi, T., Shiraishi, €I., Shimizu, M., Yamazaki. S. and Morita,
M. (1995) Imposex in Japanese gastropods (Neogastropoda and
Mesogastropoda): effects of tributyltin and triphenyltin from anti-
fouling paints. Marine Pollution Bulletin 31, 402405.
Houlihan, D.F., Costello, M.J., Secombes, C.J., Stagg, R. and
Brechin, J. (1991)Effects of sewage sludge exposure on growth,
feeding and protein synthesis of dab (Limanda limanda (L.)).
hlarine Environmental Research 37, 331-353.
Huss, € H I . , Pedersen, A. and Cann, D.C. (1974)The incidence of
Clostridium hntuliniim in Danish trout farms. 1. Distribution in
fish and their environment. J o i ~ m a lof Food Technology 9, 445-
450.
Ihe, A.C. and Kullenherg, G. (1995)Quality assurance-quality con-
trol (QA-QC) regime in marine pollution monitoring pro-
grammes: The GIPhlE perspective. Marine Pollution Bulletin 31,
209-213.
Jacquez, G.hl., Ziskowski, J. and Rolfe, F.J. (1994) Criteria for
the evaluation of alternative environmental monitoring variables:
'Theory and an application using winter flounder (Pleuronectes
amerrcanus) and Dover sole (Microstomus Pacrficus). Environ-
mental Monitoring and Assessment 30, 275-290.
Joseph, K.O.and Srivastava, J.P. (1993)Mercury in finfishes and
shellfishes inhabiting Ennore estuary. Fish TechnoloKy 30, 15-
118.
Khan, R.A. (1987)Crude oil and parasites of fish. Parasitology Today
3,99-100.
Khan, R.A. (1991)Influence of concurent exposure to crude oil and
infection with Trypanosoma murmanensis (Protozoa: hlas-
tigophora) on mortality in winter flounder, Pseudopleuronectes
americanus. Canadian 3 0 ~ r n a of
l Zoology 69, 876880.
Journal of Applied Microbiology Symposium Supplement 85, 234s-2428

Khan, R.A. and Thulin, J. (1991) Influence of pollution on parasites
of aquatic animals. Advances rn Parasitology 30, 201-238.
Kirk, R.S. and Lewis, J.W. (1993) An evaluation of pollutant
induced changes in the gills of rainbow trout using scanning
electron microscopy. Environmeantal Technology 14, 577-585.
Landsberg, J.H. (1995) Tropical reef-fish disease outbreaks and
mass mortalities in Florida, USA: what is the role of dietary
biological toxins? Diseases of Aquatic Organisms 22, 83-100.
Lanno, R.P. and Dixon, D.G. (1996) Chronic toxicity of waterborne
thiocyanate to rainbow trout (Oncorhynchus m,ykiss). Cunadian
Jwrnal of Fisheries and Aquatic Sciences 53,2137-2146.
Larsen, J.L. and Pedersen, K. (1996) Atypical Aeromonas salmonicida
isolated from diseased turbot (Scophthalmus maximus). Acta Vet-
erinaria Scandinavia 37, 139-146.
Lehtinen, K.-J. (1980) Effects on fish exposed to efluent from a
titanium dioxide industry and tested with rotary-flow technique.
Ambio 9, 31-33.
Lehtinen, K.-J., Notini, M. and Lander, L. (1984) Tissue damage
and parasite frequency in flounders, Platichvs Jlesus chronically
exposed to bleached kraft pulp mill efluents. Annales de Zuologia
Frnnici 21, 23-28.
Lemly, A.D. (1997) Role of season in aquatic hazard assessment.
Environmental Monitoring and Assessment 45, 89-98.
Lindesjoo, E. and Thulin, J. (1994) Histopathology of skin and gills
of fish in pulp mill effluents. Diseases of Aquatic Organisms 18,
81-93.
Lindesjoo, E., Thulin, J., Bengtsson, B.-E. and Tjarnlund, U. (1994)
Abnormalities of a gill cover bone, the operculum, in perch Perca
Juvratilis from a pulp mill effluent area. Aquatic Toxicology 28,
189-207.
Malins, D.C., McCain, B.B., Landahl, J.T. et al. (1980) Neoplastic
and other diseases in fish in relation to toxic chemicals: an over-
view. Aquatic Toxicology 11, 43-67.
Malins, D.C., McCain, B.B., Myers, M.S. et d(1987) Field and
laboratory studies of the aetiology of liver neoplasms in marine
fish from Puget Sound. Envimnmentul Health Perspestives 71, 5-
16.
Mayer, F.L., Woodward, D.L. and Adams, W.J. (1993) Chronic
toxicity of pydraul 50E to lake trout. Bulletin of Environmentul
Contamination and Toxicology 5 1, 289-295.
McVicar, A.H., Bruno, D.W. and Fraser, C.O. (1988) Fish diseases
in the North Sea in relation to sewage sludge dumping. Murine
Pollution Bulletin 19, 169-173.
hlellergaard, S. and Nielsen, E. (1995) Impact of oxygen deficiency
on the disease status of common dab L i m a n h limandu. Diseuses
ofAquatic Organisms 22, 101-1 14.
hleyer, F.P. and Bullock, G.L. (1973) Edwardsiella turdu, a new
pathogen of channel catfish (Ictalurus punctatus). Applied Micro-
biology 25, 155-156.
hlinami, T. (1979) Streptococcus sp., pathogenic to cultured yellow-
tail, isolated from fishes for diets. Fish Pathology 14, 15-19.
hliskiewicz, A.G. and Gibbs, P.J. (1994) Organochlorine pesticides
and hexachlorobenzene in tissues of fish and invertebrates caught
near a sewage outfall. Envrronmental Pollution 84,269-277.
hloller, €1. (1987) Pollution and parasitism in the aquatic environ-
ment. Journal oJ’Purasitology 17, 353-361.
Moore, M.J., Shea, D., Hillman, R.E. and Stegeman, J.J. (1996)
Trends in hepatic tumours and hydropic vacuolation, fin erosion,
Q 1ggg The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement 85, 234s-2428
POLLUTION AND FISH HEALTH 241s
organic chemicals and stable isotope ratios in winter flounder
from Massachusetts, USA. Marine Pollution Bulletin 32,458470.
Mushiake, K., Muroga, K. and Nakai, T. (1984) Increased sus-
ceptibility of Japanese eel Anguilla luponrcu to Edwardsrellu turdu
and Pseudomonas anjiuilliseptrca following exposure to copper.
Bulletin of the Jupanese Society of’ Scrrnttjic Fisheries 50, 1797-
1801.
Mushiake, K., Nakai, T. and hluroga, K. (1985) Lowered phago-
cytosis in the blood of eels exposed to copper. Fish Pathology 20,
49-53.
Nakatsugawa, T. (1994) Atypical Aeromonas salmonrcida isolated
from cultured shotted halibut. Fish Pathology 29, 193-198.
Newton, L.C. and hlcKenzie, J.D. (1995) Echinoderms and oil
pollution: a potential stress assay using bacterial symbionts. Afar-
ine Pollution Bulletin 31, 453456.
Noga, E.J., Khoo, L., Stevens, J.B., Fan, Z. and Burkhoider, J.hl.
(1996) Novel dinoflagellate causes epidemic disease in estuarine
fish. Marine Pollution Bulletrn 32, 219-224.
O’Neill, J.G. (1981) The humoral immune response of Salmo truitcr
L. and Cyprinus carpio L. exposed to heavy rnetals.Joumalr~fF~sh
B i o l ~ g y19, 297-306.
Oladosu, G.A., Ayinla, O.A. and Ajiboye, M.O. (199.1) Isolation
and pathogenicity of a Bacillus sp. associated with a septicaemic
condition in some tropical freshwater fish species. Journal y/’
Applred Ichth,yoloKy 10, 69-72.
Overstreet, R.M. and Howse, H.D. (1977) Some parasites and dis-
eases of estuarine fish in polluted habitats of Mississippi. Annub
of the N e w York Academy nfScience 298, 427462.
Pascoe, D. and Cram, P. (1977) The effect of parasitism on the
toxicity of cadmium to the three-spined stickleback, Gusterosteus
aculeutus L. 31~urnalof Fish Biology 10, 467472.
Pedersen, K., Kofod, H., Dalsgaard, I. and Larsen, J.L. (1994)
Isolation of oxidase-negative Aeromonas sulmonrrida from diseased
turbot Scophthalmus maximus. Diseuses i!j’Ayuutri Organisms 18,
149-154.
Peters, N., Kiihler, ’4. and Kranz, H. (1987) Liver pathology in
fishes from the lower Elbe as a consequence of pollution. Diseases
ofAquutir Orgunisms 2, 87-97.
Premdas, P.D. and Metcalfe, C.D. (199-1) Regression, proliferation
and development of lip papillomas in wild white suckers, Cuto-
stomus conrmersoni, held in the laboratory. Environmental Biology
CfFishes 40, 263-269.
Qureshi, T.A. and Prasad, Y. (1995) An incidence of fibroma in a
catfish, HeteropneustesJ~ssflf.~(Bloch) caught from the Lower Lake,
Bhopal. Bionature 15, 107-1 1 1 .
Robohm, R.A., Brown, C. and hlurchelano, R.A. (1979) Com-
parison of antibodies in marine fish from clean and polluted
waters of the New York Bight: relative levels against 36 bacteria.
Applied and Environmental Microbiology 38, 248-2 57.
bdsaether, M.C., Okfsen, J., Raa, J., hlyhre, K. and Steen, J.B.
(1977) Copper as an initiating factor of vibriosis (Vthrio ung-
~ 17--
uillarum) in eel (Angudlu unjiuilla). Journril of’Ftsh B i o l o g ~10,
21.
Sandstrom, 0. (1994) Incomplete recover! in a coastal fish com-
munity exposed to efluent from a modernized Swedish kraft mill.
Canudian3i,urnul of Fisheries cind Ayuutic Scimcrs 51, 2195-2202.
Secombes, C.J., Fletcher, T.C., O’Flynn, J.A., Costello, hl.J.,
Stagg, R. and IIoulihan, D.F. (1991) Immunocompetence as a
2428 B. AUSTIN
measure of the biological effects of sewage sludge pollution in
fish. Comparative Biochemistry and PhvsioloRv lOOC, 133-136.
Secombes, C.J., Fletcher, T.C., White, A., Costello, hl.J., Stagg,
R. and floulihan, D.F. (1992) Effects of sewage sludge on immune
response in the dab, Limanda limanda (L.). Aquatic Toxicology 23,
217-230.
Siddall, R., Pike, A.W. and McVicar, A H . (1994) Parasites of
flatfish in relation to sewage dumping. Journal of Fish Biology 45,
193-209.
Sovenyi, J. and Szakolczai, J. (1993) Studies on the toxic and
immunosuppressive effects of cadmium on the common carp.
Acta Veterinaria Hungaricu 41, 41 5-426.
Sved, D.W., Roberts, M.H. Jr and Van Veld, P.A. (1997) Toxicity
of sediments contaminated with fractions of creosote. IVater
Research 31, 294-300.
Turrell, W.R. (1994) hlodelling the Braer oil spill: a retrospective
view. Marine Pollution Bulletin 28, 21 1-218.
Vethaak, A.D. (1992) Diseases of flounder (Platichth,ys Jesus L.)
in the Dutch Wadden Sea, and their relation to stress factors.
Netherlands 3ournal of’Sea Research 29, 257-272.
Vethaak, A.D. and ap Rheinallt, T. (1992) Fish disease as a monitor
for marine pollution: the case of the North Sea. Reviews in Fish
B i o l q y and Fisheries 2, 1-32.
Vethaak, A.D. and Jol, J.G. (1996) Diseases of flounder Platichth,ys
Jesus in Dutch coastal and estuarine waters, with particular ref-
erence to environmental stress factors. 1. Epizootiology of gross
lesions. Diseases ofAyuatic Organisms 26, 81-97.
Vethaak, A.D. and van der hfeer, J. (1991) Fish disease monitoring
in the Dutch part of the North Sea in relation to the dumping of
waste from titanium dioxide production. Chemical Ecology 5,149-
170.
Vethaak, A.D., Bucke, D., Lang, T., Wester, P., Johl, J. and Carr,
hf. (1992) Fish disease monitoring along a pollution transect: a
case study using dab Limanda limanda in the German Bight,
North Sea. hlurine Ecology Progress Series 91, 173-192.
0 1999 The Society for Applied Microbiology, Journal of Applied Microbiology Symposium Supplement 85,234s-2428
Vethaak, A.D., Jol, J.G., Meijboom, A. et al. (1996) Skin and liver
diseases induced in flounder (Platichthys Jesus) after long-term
exposure to contaminated sediments in large-scale mesocosms.
Environmental Health Perspectives 104, 12 18-1 229.
Voigt, €I.-R. (1994) Fish surveys in the Vaike Vain Strait between
the islands of Saaremaa and Muhu, western Estonia. Proceedings
of the Estonian Academy of Science and Ecology 4, 128-135.
Vos, J.G., Van Loveren, €I.,Wester, P.W. and Vethaak, A.D. (1989)
Toxic effects of environmental chemicals on the immune system.
Trends in Pharmacological Science 10, 289-293.
Westfall, B.A. (1945) Coagulation film anoxia in fishes. Ecology 26,
283-287.
Wiklund, T. (1995) Virulence of ‘atypical’ Aeromonas salmonicida
isolated from ulcerated flounder Platichth,ys Jesus. Diseases of
Aquatic Organisms 21, 145-150.
Wiklund, T . and Bylund, G. (1993) Skin ulcer disease of flounder
Platichthys Jesus in the northern Baltic Sea. Diseases of Aquatic
Organisms 17, 165-174.
Wiklund, T. and Dalsgaard, I. (1995) Atypical Aeromonas sal-
monicida associated with ulcerated flatfish species in the Baltic
Sea and the North Sea. Journal of Aquatic Animal Health 7,218-
224.
Wiklund, T., Dalsgaard, I., Erola, E. and Olivier, G. (1994) Charac-
teristics of ‘atypical’, cytochrome oxidase-negative Aeromonas sal-
monicida isolated from ulcerated flounders (Platichthyspesus (L.).
Journal of Applied Bacteriology 76, 5 1 1-520.
Wood, A.W., Johnston, B.D., Farrell, A.P. and Kennedy, C.J.
(1996) Effects of didecyldimethylammonium chloride (DDAC)
on the swimming performance, gill morphology, disease resist-
ance, and biochemistry of rainbow trout (Oncorhynchus mykiss).
Canadian Journal of Fisheries and Aquatic Sciences 53,2424-2432.
Ziemann, D.A., Walsh, W.A., Saphore, E.G. and Fulton-Bennett,
K. (1992) A survey of water quality characteristics of efluent from
Hawaiian aquaculture facilities. Jiiurnal of the World Aquaculture
Society 23, 18&191.