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CM 19961E: 17
International Council for the
Exploration ofthe Sea
Marine Environmental Quality Committee
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Fish disease monitoring - a valuable tool for pollution assessment ?
by
Thomas Lang & Volkert Dethlefsen
Bundesforschungsanstalt rur Fischerei
Institut rur Fischereiökologie
Deichstraße 12
27472 CuXhaven
Gerinany
Abstract
Studies on wild marine fish diseases have a long tradition in monitoring progriunmes carried out by
ICES Member Countries and methodologies applied have been intercalibrated and standardized to a
large extent. Since the beginning of more systematic studies in the 1970's, their major objectives have
been to assess .and monitor biological effects of contaminants by. using the prevalence and spatial
distribution of diseases as biological indicators ofpollution-associated environmental changes.
Although intensive fish disease studies have been carried out in the ICES area since almost two decades
and results and conclusions of these studies have becn discussed thoroughly, there is still no general
consensus as to whether changes in the prevalcnce of fish diseases can be uscd as a biological indicator
of effects of contammants and, consequently, whether fish disease studies are a valuable tool for
pollution assessment which should be integrated in international monitoring programmes.
In the light ofthe present discussion on the incorporation offish disease studies into the revised OSPAR
Joint Assessment and Monitoring Programnie (JAMP), the present paper provides abrief ovcrview of
the current status of fish disease monitoring in ICES Member Countries as weil as of the concept of a
cause-effect relationship bet\veen contaminants and fish diseases and the problems encountered with
demonstrating such a relationship. Further emphasis is given to weakneSses and strengths of fish disease
studies as compared to other techniques recommended for monitoring biological effcctS of contaminants.
Introduction
Conspicuous diseases and parasites of wild marine fishes have attracted scientists for' many
decades (for reviews see Sindermann 1970, Roherts 1982, \Vatennann & Kranz 1992). Apart
from natural or scientific curiosity, early and more comprehensive 'studies were mainly
dedicated to econornically significant diseases and parasites affecting fishery arid mariculture
(Roberts 1982).
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It was in the late 1960's and the early 1970's that first reports were published indicating a
possible link hetween anthropogenie contarninants and the occurrence of elevated prevalences
of certain diseases of wild marine fish and shellfish. First comprehensive epiderniological
studies commenced in the USA and focused on polluted coastal zones such as estuaries of
large rivers and waters elose to industries and ports. In these studies (reviews have been
published for instance by Sindermann 1979, 1989, 1993, Mix 1986, Malins et al.' 1988,
Overstreet 1988, Vethaak & ap Rheinallt 1992), a large number ofinfectious and putative noninfectious fish diseases have heen identified the prevalence and spatial distribution of which
corresponded with known or suspected pollution hot spots or gradients. \Vell-known examples
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of common diseases repeatedly considered to be pollution-associated are fin rot/erosion and •
ulcers, skeletal deformities, skin tumours, and liver tumours and their putative precursors.
In Europe, particularly Sindennan's reviews (1979, 1984) on pollution-associated diseases and
abnonnalities of fish and shellfish and on the impact of the environment on fish health received
much attention and stimulated systematie research/monitoring activites which mainly have
focused on the North Sea and adjacent waters (e.g. the lrish Sea) and on parts of the Baltie
Sea (a rather current compilation of European activities has been provided by Vethaak & ap
Rheinallt 1992). In Canada, a multidisciplinary monitoring programme of diseases in eastuarine
fishes ofthe southem Gulf of St. Lawrence in relation to pulp and paper mill eflluents is being
planned.
leES has been involved in the initiation and coordination of fish disease studies in relation to
marine pollution since the 1970's. In 1975, the ICES Worldng Group on Pollution Baseline
and Monitoring Studies in the Oslo Commission and ICNAF Area recommended to implement
a sub-group which was requested to review the present state of kriowledge of the effects of
marine pollution on livirig resources and to examine the experimental demonstration and
measurement of these effects and their interpretation and evaluation in field and monitoring
situations (Anonymous 1978). Whilst in the report of this sub-group, the term 'fish diseases'
did not even occur at all and only ver)! few 'morphological effects' (skeletal deformities,
tumours, gill damage) were considered useful parameters for biological effects monitoring
programmes, it was only a few years tater that at the 1979 ICES Workshop on Biological
Effects 0/ Marine Pollution a11d the Problems 0/ Monitoring a mimber of diseases (including
infectious diseases) of fish and shellfish were classified as potentially valuable tools for
pollution monitoring and detailed guidelines arid recommeridations were provided for the
design of pathobiological surveys for polh.itiori monitonng (Sindermann et al. 1980). In the
report, the shortcomings of many studies and the problems to .evaluate their results were
clearly identified and the rieed for more explariator)r work and data. accumulation
(epidemiological studies) was strongly emphasized.
The results of studies on the link between fish diseases and marine pollution initiated in that
period were reported to various ICES Working Groups and Committees and were presented at
several ICES Statutory Meetings (now,ICES Arinual Science Conferences). However, from
the beginning ofthese studies, their results and conclusions were debated quite controversially.
This was most evident in the 1980's when the discussion on possible biological effects of
anthropogenie contaminants in the sea - even in a scientific and independent organization such
as ICES - was more or less a political one and, therefore, rather controversial opinions were
expressed about the state of the marine environment. \Vith regard to findings of elevated fish
disease prevalences, particularly in the Noi-th Sea and its coastal areas, statements on their
aetiology were quite contradictory and ranged froin 'natural causes' to 'caused by
contaminants' (reasons for this disagreement will be discussed below). The discussion on this
issue is reflected in the repoi-ts ofvarious ICES Working Groups (e.g. the Working Grollp on
PathologjJ and Diseases 0/ Marine Organisms and the Working Group on Biological Effects
0/ Contaminallts) and the Advisory Committee on lv/arine Pollution and its successor, the
Advisory Committee 0;' the Marine Environment as weIl as in great number of scientific
publications (e.g. Sindenriann 1979, Möller 1985, Dethlefsen et al. 1987, Vethaak & ap
Rheinallt 1992, Bucke 1993, Anonymous 1995).
.
Despite the long-term experience with fish disease surveys, even today there is still no general
consensus in the scientific community regardirig the interpretation of field re~sults and it appears
as ifnot much progress has been made during the past 20 years in the understanding ofthe role
of contaminants in the aetiology of common diseases of wild marine fishes. Consequently,
there is also still no general agreement as to whether changes in the prevalence of fish diseases
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are a suitable indicator of biological effects of contaminants which should be incoI-porated in
national and international moiütoring programmes.
The discussion on the usefuiness of flsh clisease studies for monitoring purposes again was
intensified when it was decided to revise the former Joint MOI;itoring ProiJramme (.DvIP) of
the Oslo ~md Paris Cornritisions (OSPARCOM) ancl to implement the joint Assessme;ll a;ld
lvlonitoring Programme (JAMP) and to supplement the formerly more chemically onentated
monitoring with a biological effects monitoring section. In order to identify suitable biological
effe~ts techniques to be incorporated in such a prograinme, ICES has been requested by
OSPARCOM to recommend suitable biological effects techniques, to provide guidelines for
their applicatiori and to define, quality assurance requirements (Anonymous 1995). Within this
process, different opinions libout the suitability of fish diseases as a tool for pollution
assessment have been expressed and a number of statements were circulated which sometimes
were more confusing than helpful for understanding.
the authors of ihe preseni contributiori, being aciively involved in fish disease studies in the
North Sea, Baltic Sea and adjacent \vaters, therefore feIt that it could be useful for the present
discussion to provide. a ciIrrent overView briefly sunirnarizing the status of fish disease
monitoring in ICES Member Countries, to higWight the current uriderstanding of the basic
concept regarding the link between fish diseases and envirorUnental contaminants and to point
out weaknesses and strerigths of fish disease monitoring. It is, however, not the intention of
this paper to review new literature on particular fish diseases/parasites and their possible
association With coritarilinants and to compete with
the excellent reviews on this issue
published during the pasi !Wo decades (for iristance Sindermann 1979, 1984, 1989, Möller
1985, Mix 1986, Malins et al. 1988, Vethaak & ap Rheinallt 1992, Bucke 1993).
all
Status
of fish disease monitoring in the ICES area
.
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In many ICES Member Couritries, studies on the prevalenceand spatial distribution of diseases
of wild marine fish are an important componerit of national researchlmonitoring programrries
for the assessmerit of biological effects of contaminanis. Whilst mainly externally visible
diseases' were investigated in the beginnirig of these siudies, the gross and histological
examination for neoplastic and putative pre-neoplaStic liver lesions has increasingly been
included dunng the past decade. Studies on the link between contaminant exposure and fish
parasites are often not included although the potential value of parasites for pollutiori
monitoring pUI-poses has been repeatedly discussed (Möller i987, Khan & Thulin 1991,
MacKenzie et al. 1995).
In North Airierica, most activities during previous years have been carried in the USA. These
studies are still mainly coricentrating on coastal areas with. bcittom-dwelling fishes such as
English sole (Pleuronectes vet;,lus), starry flounder (Platichlhys stel/alus), and white croaker
(Genyonemus lineatus) along the Pacific coast arid Winter flounder (Pleuronectes americanus)
at the northeast Atlantic coast as main bioiridicator species (Myers et al. 1994 a). Since the
1980's, these studies mainly have beeri adressing the links between coritarilinants arid the
occurrence of neoplastic and rion-neoplastic liver lesions and related biomarkers (Malins et al.
1988, Murehelano & \Volke 1991, Myers et al. 1991, 1994 a,b, McCain et al. 1992, Moore &
Stegeman 1994).
'
In the European ICES area, particularly studies in the North Sea on ihe occurrerice of
externally visible fish diseases (e.g. Iymphocystis, epidermal hyperPlasia/papilloma, skin ulcer
disease) and, since the late 1980's, liver nodules/tumours of the common dab (Limallda
/imanda) have been part of national long-term monitoring programmes carried out. by all
bordenng countries since the end ofthe 1970's. Common diseases ofdab and other abundant
fish spedes occurring in the North Sea and adjacerit areas have been described for instarice by
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Bucke et al. (1996) and literature on epidemiological data has been thoroughly reviewed by .
Vethaak & ap Rheinallt (1992). Whilst, in the beginning, these programmes were restricted to ;;.
coastal areas, they have also been covering offshore regions in the entire North Sea since the
l'
1980's. Externally visible diseases of dab were also included in the list of biological effects '.~
techniques applied in the framework of the former Monitoring Master Plan (M1vfP) of the
North Sea Task Force (NSTF) (North Sea Task Force 1993). In coastal areas of the North
Sea, Dutch and German studies also investigated diseases and parasites of the European
flounder (Köhler 1990, 1995, Möller 1990, Anders & Möller 1991, Vethaak 1992, Lang 1994,
Vethaak & Jol 1996, Vethaak & Wester 1996). Other fish species frequently included in
disease monitoring in the North Sea are cod (Gadus morhua), whiting (Merlangius
merlangus), haddock (Melanogrammus aeglefinus), and plaice (Pleuronectes platessa).
In Table 1, the present status of fish disease monitoring programmes carried out by European
ICES Member Countries in the North Sea and adjacent waters is Iisted, containing information
on geographical areas, fish species and diseases. covered. Only those programmes are
mentioned which are related to the assessment of contaminant effects and which are being
carried out on a regular basis. Apart from these, there always has been a large number of more
scientificly orientated and temporally restricted research projects investigating contaminantinduced biological effects associated with pathology and diseases.
Table 1: Present status of fish disease monitoring programmes carried out by
European ICES l\lember Countries in the North Sea and adjacent waters
Belgium:
Belgian eontinental shelf and soutb-westem North Sca
dab, plaiee, flounder, sole, eod, whiting
extemally visible diseases and parasites, in dab Iiver nodulesltumours
Denmark:
no regular fish disease moiUtoring (tbe fonner extensive fish disease monitoring haS
been eompletely stopped only reeently)
Franee:
no regular fish disease monitoring
Gennany:
whole North Sea, English Channel, Irish Sea
dab, plaiee, eod, whiting, haddock, saithe
extemally visible diseases and parasites, in dab Iiver nodulesltumours
Iceland:
no regular fish diseäse monitoring
Ireland:
no regular fish disease monitoring
The Netberlands:
Duteh eoastal waters
.
dab and flounder
extemally visible diseases and parasites, in dab and flounder Iiver noduleslturnours
Norway:
no regular fish disease monitoring
Portugal:
no regular fish disease monitoring
Spain:
no regular fish discase monitoring
U.K.
- England:
eentral and western North Sea. English Channel, lrish Sea
dab, flounder, ead
extemally ,;sible discascs and parasites, in flatfishes Iiver nodulesltumours
- Scotland:
north-westem North Sea
dab,eod,haddoek
externaIly visible diseases and parasitcs, in dab Iivcr nodulesltumours
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Studies on the oeeurrenee of fish diseases are also eomponents of national researeh/monitoring ' :
programmes in the Baltie Sea. The major target fish species of larger-seale studies are
European flounder and cod arid, in addition, diseases of species such as fourhom sculpin
(Myoxocephalus qilcidricornis), herring (Clupea harengus), sprat (Sprattus sprattus), perch
(Perca fluviatilis), ruffe (Gymnocephalus cernua) and pike (Esox ludus) have been
investigated on a more loeal basis.
A current review of flounder diseases and parasites in the Baltic Sea is given by Bylurid &
LönnstrÖm (1994). Dethlefsen & Lang (1994) and Draganik et al. (1994) described the
abundance and spatial distribution of eod diseases in the south-westerri Baltie Sea, Bengtsson
(1988) and Bengtsson (1991) pollution-associated skeletal deformities of fourhom sculpin and
Lindesjöö (1992) diseases ofperch, ruffe and pike. related to pulp mill effiuents.
•
Information on Baltic Sea countries carrying out a regular wild fish disease monitoring
programme related to contaminant effects are given in Table 2. Again, there have been a
number of additional research projects in diverse Baltic Sea eountries foeusing on various
aspeets of contaminant-induced biological effeets including pathology and diseases.
Table 2: Present status of fish disease inonitoring programmes carried out by
ICES l\lember Countries in the Baltic Sea
Denmark:
no regular fish disease monitoring
Estonia:
Gulf of Finland
flounder
externally visible disCases and p:irasites, liver nodulesltumours
Finland:
no regular fish disease monitoring . .
Germany:
•
. whole south-western Baltic Sea
eod, flounder, plaiee, dab, whiting,
externally visible diseases and parasites, in flounder and dab Iiver nodules/tumours
Latvia:
Latvian waters
.
flounder, cod, herring, pike, pikepereh, roaeh
Poland:
Polish fishery zone
eod, flounder, herring, sprat
Russia:
no regular fish disease monitoring .
Sweden:
no regular fish disease monitoring
In a number of ICES Member Countries, the extent of fish disease monitoring programmes
has been corisiderably reduced during the past years whieh has' repeatedly been regretted by
lCES,. \Vorking Groups and Committees. Examples are Denmark and Sweden which
completely teiminated their formerly intensive efforts in the North Sea and Kattegat and the
Kattegat and Baltic Sea, respectively, The Netherlands, where the former programme which
had covered stations throughout the entire North Sea is now restricted to a few stations in
Dutch coastal waters, and Scotland, where the number of sampling sites has also been reduced
considerably. Also in the USA, some long-term monitoring programmes had to be suspended
due to a lack of funding.
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When results of early studies were discussed within relevant ICES-bodies in the 1980's, it '
became apparent that there was a lack of intercalibration and standardization of methodologies
applied and, therefore, results reported seemed not to be comparable. Therefore, the ICES ~:
Working Group on Patholoy and Diseases 0/ Jvfarilie Orgallisms (WGPDMO) started first .1.
attempts to solve this problem. Since that time, three sea-going workshops (1984 North Sea,
1988 Kattegat, 1994 Baltic Sea) were held under the auspices ofICES (in 1994 in cooperatiori
with the Baltic lvfarine Biologists (B}vfB)) in order to intercalibrate and standardize
methodologies for fish disease surveys and to establish practical guidelines for an integrated
international programme to determine long-term trends in fish disease prevalence levels. The
guidelines provided induded recommendations on minimum sampling requirements, target fish
species, types and intensity of diseases to be monitored, sampli~g stations and areas arid
additional measurements (Dethlefsen et ClI. 1986, Anonymous. 1989, Lang et al. 1995).
Additional preliminary guidelines were provided by \VGPDMO for rriacroscopic and
microscopic inspection of flatfish livers for the occurrence of neoplastic lesions. Attempts to'
further intercalibrate and standardize methodologies used for studies on liver patnology of
flatfish are underway and will be a major issue of the ICES Special Meetillg on the Use 0/
Live1- Patholog;, 0/ Flatjish tor Monitoring Biological Effects 0/ COlltaminal1ts whicn will be
held in October 1996 in Weymouth, UK.
Other ICES-activities related to fish diseascs were the ICES/IOC Workshop on Biological
Effects 0/ Contaminants in The North Sea (Vethaak et al. 1992) and the publication of a
training guide for the identification of common diseases and parasites of fish in the North
Atlantic (Bucke et al. 1996). In addition, diseases of marine finfish arid shellfish are being
described in the ICES ldentijication Leafletstor Diseases and Parasites 0/Fish and Shellfish,
a publication series prepared under the guidance ofthe \VGPDMO.
From the beginning of in situ fish disease studies, ICES Member Countries have been
requested to submit their diseuse prevalence data to ICES on an annual basis. At first, paper
formats collected by the \VGPDMO were used for this pUrPose, now a (recently revised) fish
disease format as weIl as a specific data entiy programme are available facilitating compatibility
with the other environmental data (for example contaminants in biota and sediments,
hydrography) stored in the ICES Environmental Databank. The fish disease prevalence data so
far submitted to ICES partly reach back until 1981 and represent an unique set of biological
long-term data. Only recently, standard procedures for the data submission, statistical analysis
and presentation of disease data have been developed by the ICES Sub-gr011P on Statisticcil
Analysis 0/Fish Disease Data inlvfarine Fish Stocks.
In conclusion, it can be stated that methodologies used for studies on diseases of wild fish in
the ICES area (in particular for dab, flounder and cod) are coordinated and standardized to a
large extent on an international level. Standard operating procedures including sampling
design, disease diagriosis and standard protocols for recordirig arid reporting' of fish diseases
data have been developed and applied successfuIly. All methodologies have now been
practically tested for a considerable period. During a number of sea-going. workshops, interlaboratory performance testing exercises regarding disease diagnosis have been. carried out.
Therefore, methodologies are readily applicable in fufure internatiomil monitoring programmes.
Disease data submitted to the ICES Envirorirriental Databank by institutes actively participating
in the above quality assurance procedures can be regarded to be of consistently high quality
and can be utilized as scientific baseline data for future rrionitoring programmes.
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Concept of a cause-efTeCt relationship between contaminants and fish diseases •
Ai a starting point, it may be useful to recall the definition of the term 'disease' and some ~:
associated principles:"Disease is a deviation /rom the state of complete physical or social ....
well-being of an organism involvilig a well-defined set of signs (md aetiology and leading to
an impairment of its normal filllction" (Bucke et al. 1996). According to Kinne (1980), the
deviation may be funetional or structural or both and may result from a single cause or from
several causes acting in concelt. The impairrnent should be quaritifiable in terms of a reduction
in the ecological potential (e.g. survival, groWth, reproduction, energy procurement, stress
endurance, competition). The degree of a deviation depends on the impact of the diseasecausing agent (entity) and the couriieractive potential of the iridividual affected, whereby. in
most cases, the relation betweeri impact and counteractive potential is subject to external
influences (Kirine 1980). In this context, the same author pointed out that demonstrable
deviations from the orgarusm's weIl-being requires that, the agent's effects surpass a certain
critical level which may happen if, for example, the host resistance is decreased due to
'envirorimental stress' (induding pollution) and other factors.
Since 'stress' plays such an essential role in the concept ofa relationship between coritaminants
and fish diseases, the terms 'stress', 'environmental stress', ,'stressor' which can be found in
nearlyall available reports on putative pollution-associated fish diseases and the use ofwhich is
sometimes inconsistent also deserve some more explanations. The concept of 'stress' was
introduced by Selye (1950) and stress has been originally defined by Selye as "the sum of all
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re-establish anormal
physiological responses by lt-'hich an animal tries to maintain
rnetabolism in the face oI a physical or chemical force". According to \Vedemeyer &
Goodyear (1984), this definition has evolved into the concept that "stress is the biological
ejfect ofanyforce (stressor) that challenges homeostatic stabilizing processes U11d extends
thern beYOlid their normal limits, at aliy lei'e/ of b'iologieal organizatioll - bidividual,
pop;,latioll, or ecosystem". Based on these definitions, the tenn 'envirorimental stress' is ofteri
0"
misused and should be replaced by 'environmental stressorls' since what is really meant in
most cases are the forces acting on the organism rather than the subsequent compensatory
physiological and well-defined responses of the organism. A 'stressor' is a force which is
severe enough to require physiological compensation (a 'stress response') by the affected
organism. If the stressor does not exceed certain tolerance limits, the stress resporise will
succeed in mairitaining health by re-establishing the equilibrium between the changed
environment arid the organism. Failure of an organism challenged by non-tolerable acute or
chroniC stressors to achieve compensation wiII lead to harmful stress effects either causing
imInediate death or sublethaI effects stich as increased susceptibility t6 diseases, redticed
tolerance to subsequent stressors, and reduced growth, longevity, and reproductive success
(Wedemeyer & Goodyear 1984) (more details on the stress cOII<:ept and its implications for
diseases ofmarine organisms have been provided by Sindermann 1984).
Based on the stress concept introduced by Selye, the role of stress on the disease resistance of
fishes was thoroughly described al ready in 1970 in a weIl-kriowri review paper by \Vedemeyer.
He also emphasized that stress may, besides its positive effects (increased probability of
survival), unfortunately, also contribute to iricreased susceptibility of the host to infection and
disease by affectirig both the host's specific humoral imri1unity as weIl as its non-specific
defence mechanisms directed against pathogens.
Regarding the relationship between fish diseases and contaminants, it was mainly Snieszko's
(1974) dassical review paper on the effects of environmental stress(ors) on outbreaks of
infectious diseases of fishes which constituted the coriceptual basis for the implementation of
more systematic studies on the prevalence and spatial distribution of fish diseases. AIthough a
major aetiological role of envirorimental factors in infectious fish diseases had been postulated
befere, Snieszko was probably the first who strongly emphasized the crucial role of (mainly
8
man-made) environmental changes. In his paper, he proposed a simple but eonvincing (and still •
generally accepted) model consisting of three essential interdependent factors (host, pathogen, ~
environment) the interaetions of which may ulimately result in the occurrence of infectious 10:
diseases. In the explanation of this model, Snieszko states:"An overt in/eetious disease oeeurs .. ~
when a suseeptible host is exposed to a vimle;lt pathogen WIder proper ellvironmental
conditions". The main essence of Snieszko's paper is that environmental stress(ors) (he
provided examples for temperature, oxygen and nitrogen deficiency arid excess, eutrophication,
sewage, metabolie products of fishes and industrial pollution) organism are exposed to may
predispose them to infectious diseases. .
.
.
From many studies the results ofwhich have for instance been reviewed by Sindermann (1979,
1984, 1989) there is evidence that pollution not only might contribute to infectious diseases
but also to non-infeetious diseases:"Ejfeets (of pollution) are often expressed as disease -
either in/eetious or ilOn-infectious. ln/eetious diseases may result from lowered resistallee to
primary pathogens, /rom invasion 0/ damaged tisSlle by/aeultative (secolldary) pathogens, or
from proliferation 0/ latent microbial in/ectiolls. Non-in/eetiolls diseases may reSlllt /rom
early genetie damage, or /rom ehemical modifieation 0/ bOlle and soft tisSlle, leading to
skeletal anomalies and tumours." (Sindermann 1984).
As possible conceptual basis for a cause-effect relationship between contaminants and
diseases, the following mechanisms have been considered repeatedly:
• Contaminants may act as unspecijic stressors causing stress associated with lowered disease
resistance (in this context, oßen the terms 'defence mechanisms', 'disease susceptibility',
'immunosupression' or 'immunocompetence' are being used) and. thus, either lead to a
decrease in the ability to prevent infection by pathogens (vimses, bacteria. metazoan parasites)
or to a decreased ability to deJeat already invaded pathogens. Both efJects may ultimately lead
to disease
• Contaminants may eause an increase in the abundanee andlor vinllence 0/ pathogens by
creating an environment which Javours the development 0/ pathogens (e.g. by increasing
nutrient coneentrations or changing hydrographie charaeteristies). It should be pointed out,
however, that eontaminants and other environmental changes mayaiso lead to an environment
un/avourableJor pathogens, thus, possibly resulting in a deerease 0/disease prevalenee
• Contaminants may eause specijic andlor zmspecijie changes on various levels 0/ biologieal
organization (moleeule. subcellular units, eells. tissues, organs) leading to disease without
involving pathogens (e.g. exposure to heavy metals and carcinogenie eontaminants such as
PAHs and/or PCBs may lead to skeletal deJormities and neoplastie liver ehanges. respectively)
• Contaminants may eause ehanges in the disease incidenee/prevalence via additive, synergistic
or antagonistie efJects o/the above aetiologicalJactors
• Contaminants may aet in eoncert with other anthropogenie/natural environmental stressors
afJecting the health status oJfish (concept oJa multiJactorial disease aetiology)
After long-term experience with in situ fish disease studies there is now a general consensus
that in most cases a direct cause-effect relationship between the exposure to contaminants and
the occurrence of elevated disease prevalences is only hard to establish due to the fact that
most common diseases have a multifactorial aetiology involving the impact of anthropogenie
and/or natural variations of host, pathogen and environment characteristics. However, there is
a number of cases where the increased occurrence of non-infectious diseases could clearly be
reIated to anthropogenic contaminants (e.g. fin erosion and skeIetal deformities in Baltic Sea
fishes exposed to pulp mill effiuents and other industrial discharges (Bengtsson 1988,
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Bengtsson 1991, Lindesjöö 1992), the occurrence of increasecl prevalences of liver tumours
and pre-neoplastie lesions iri polluted coastal areas in the North Sea (mainlyestuanes of the
River EIbe) (Köhler 1991, 1995) arid along the Atlaniie and Pacifie coasts ofthe USA (Malins
et al. 1988, Murchelano & \Volke 1991, Myers et al. 1991, 1994 a,b, 1-fcCain et al. 1992,
Moore & Stegeman 1994).
For infectious diseases of wild fish such as the lyrnphocystis disease of flatfishes, skin ulcer
disease of flatfishes and cod and other common diseases, there is still no evidence to what
extent environmental contarrunants contribute to observed spatial and temporal trends of
disease prevalences, althOligh a link between these diseases arid contaminants has been
postulated and discussed repeatedly (Sindermarin 1979, 1984, Dethlefsen et al. 1987).
However, there is now iricreasing information from long-term studies (e.g. for NOI-th Sea dab)
that temporal changes in the prevalence of different infectious diseases often are synchronized
iridicating that these changes are caused by the same underlying environmental factors
(possibly including contaminant exposure) which most likely affect the disease resistance ofthe
fish. Vethaak et al. (1992) found a significant positive correlation between the prevalence of
epidermal hyperplasia/papilloma (probably induced bY. viruses) ofthe cerumon dab sampled on
two cruises within aperiod of two weeks alorig a pollution gradient in the German Bight and
the liver residues of organochlorine contaminants. Furtherinore, from studies carried out in the
North Sea, there is indicatiori for elevated prevalences of probably virus-induced epidermal
hyperplasia/papilloma related to the dumping of wastes of the titanium dioxide production
(Dethlefsen
al. 1987, Vethaak & van der Meer 1991) and current statistical arialyses
revealed that changes in the prevalence of extemally visible diseases in dab from the German
Bight in the period 1984 -. 1994 were partly correlated with the contents of dab livers with
certain contamiriants (Dethlefsen & Lang, unpublished data). An example showing the
correlation between the summer prevalence of lymphocysiis arid the residue levels of HCB is
given in Figure 1 (annexed). Although these data should be considered preliminary arid,
therefore, treated with caution, they indicate that a cause-effect relationship inight exist.
et
•
Ariother example for effects of environmental changes with an anthropogenie contribution are
results of studies demonstrating a link between localized oxYgeri deficiency situations in the
Kauegat, probably at least partly due to eutrophicatiori, and the occurrence of increased
prevalences of infectious viral diseases of dab (lymphocystis and epidermal
hyperplasia/papilloma) in the same areas (Mellergaard & Nielsen 1995).
However, applying strict scientifie criteria, many studies' - independently of any conclusions
drawn - failed to establish circumstantial evidence for a causal relationship between
contamiriarits arid fish diseases. This does of course not implicate that such a relationship not
exists; it rather reflects the difficulties encountered with the identification of single aetiological
factors with a major impact on the pathogenesis of diseases (see above).
Apart from this general problem, the failure of showing links between diseases and
contaminants could in rriany cases be attributed to an insufficient study design (Vethaak & ap
Rheinal1t 1992) which actually did not al10w any scientifie conclusions at all. Nevertheless, in
quite a number of studies conclusions were drawn and examples exist for both sides: those
emphasizing and those disputing a major role of contaminants. However, these conclusions and
statements often were purely speculative and mairily based on the persorial view of the authors
about the eXtent of environmental pol1utiori rather than on scientifie criteria. A very illustrative
example highlighting the problem was given by Snieszko (1974):"We believe that the
aggra\!Gting effect
0/ stress,
/rom various types 0/ pollution, causes a high illcide/lce
0/
injectiozis diseases infishes. Unjortunately, this belief, which I also intuitively share, is not as
yei adequately documented'.
,:.
~
.
I
"
10
After aperiod of strong and contradictory statements in the late 1970's and .1980's about the'
presence or absence of any cause-effect relationships between contaminants and fish diseases _.
which stimulated fruitful discussions and initiated many studies and intemationally coordinated .\. ..
activities, the current and very popular approach is the concept of a multifactorial aetiology 0[' :
fish diseases (see above). Although there certainly can be no doubt that this concept contains a
lot of truth and reflects the complex situation marine organisms are facing under in Si/li
conditions, it also has some important disadvantages since it can be (mis)used to explain,
dispute or excuse everything form negative and positive to no findings regarding a relationship
between contaminants and fish diseases. Nevertheless, the good thing about the concept of a
multifactorial disease aetiology is that everyone can accept it. In contrast to the very lively
period in the 1970's and 1980's, it seems, however, that this concept has led to a decline in
scientific motivation and, consequently, research and monitoring activities. This is the case
particularly with the 'classical' extemally visible infectious and non-infectious fish diseases
which had been the starting point of all pollution-related fish disease research and monitoring
activities in the lCES area and the study of which, unfortunately, has been stopped or
drastically reduced in many leES Member Countries..
The situation is different with research/monitoring studies on contaminant-induced neoplastic
liver lesions of bottom-dweIIing fish which clearly were intensified during the past 10 years.
However, although these studies are undoubtedly important and promising, it has to be taken
into account that neoplastie liver lesions also have a multifactorial aetiology and represent only
a relatively small part of all possibly contaminant-associated fish diseases and can, in terms of
monitoring, only be used as biological indicator of the specifie group of carcinogenic
contaminants. For other non-carcinogenie anthropogenie contaminants entering the sea many
ofwhich are known to atTect the immune system (Wester et al. 1994), other diseases such as
infectious ones might be more suitable for monitoring purposes since they may reflect
immunotoxic in SÜll etTects of contaminants.
\Veaknesses of fish disease monitoring
The most significant weakness of many wild marine fish disease research/monitoring
programmes certainly is the fact that clear causes for recorded spatial and temporal variations
in the prevalence of diseases could only very seldom be demonstrated (see above). On the one
hand, this is due to the complex and multifactorial aetiology of most common diseases (see
previous chapter), the associated problem to identify and quantify single aetiological factors
out of a suite of many known and unknown factors having a potential impact on disease and
the fact that disease in most cases is an unspecific biological response to environmental change
and, therefore, its toxicological relevance is rather low as compared to molecular or cellular
biomarkers of contaminant exposure. On the other hand, as al ready being pointed out above, a
further reason for the weak evidence provided in many fish disease studies in favour of or
against a causal relationship often has been a poor survey design (Vethaak & ap Rheinallt
1992). Already in 1979, Sindermann highlighted basic requirements for in situ studies which
have to be met before any firm conclusions about the associations of a disease with
environmental pollution can be drawn:
• Knowledge ofthe history ofoccurrence ofthe disease in a partieular speeies in the geographie
area oJconcern
• Knowledge ofthe history ofoccurrence and levels ofparticular pol/utants in that area
• A review 0/ the biology, life history, and OCcurrence
species. and Imder diffirent environmental conditions
0/ the
disease in other areas, in other
e
11
• An intensive baseline survey 0/ the current disease and pollution situation, ,with attention to
statistical reliabi/ity o/sampling
• Laboratory andfield experimentation with the principle objective o/reproducing the disease by
exposure to known levels 0/ contaminants
• Resurveys 0/ the disease and pollution levels over several years looldng/or changes or trends.
.Ä1though it already would be a quite ambitious task to fulfil Sindermann's requirements, they
are according to our present knowledge still insufficient to fully understand mechanisms
involved in the aetiology and pathogenesis of diseases considered to be contaminantassociated. A thorough analysis would require much more information on host, disease and
'environment characteristics and their interactions and it is doubtful whether available resources
would perrnit such comprehensive studies. At best, this could be possible in specific research
projects but will probably never be possible on a routine basis in monitoring programmes.
However, thorough research programmes can provide scientific baseline information for
monitoring programmes and can identify parameters to be included in regular monitoring
programmes as minimum requirements.
From the available information on past and present fish disease monitoring programmes it can
be concluded that most of them even did or do not fullfil the requirements proposed by
Sindermann. The clearest cases which do fullfil these requirements at least in part and provided
circumstantial evidence for a causal relationship between environmental contaminants and fish
diseases are the studies being carried out in the USA since the 1980's on the occurrence of
increased prevalences of neöplastic liver lesions in bottom-dwelling fish species from polluted
coastal waters (briefly reviewed by Myers et al. 1994 a). Many other programmes suffer from
the weaknesses Iisted below or at least from some ofthem.
Frequently, there is a lack ofinformation on:
• Contaminant levels in sediments, water and biota (e.g.sometimes even in the jish examined/or
diseases) .and spatial trends thereo/
•
• Bioavai/abi/ity and metabolism 0/ contaminants
• Seasonal and long-term variations in contaminant levels which can be compared with
jluctuations 0/ the disease prevalence
• Host biology (growth pattern, sexual maturity. behaviour. migration, resistance to diseases,
immunocompetence)
• Disease characteristics (aetiology, pathogenesis. vertical and horizontal transmission
pathways. seasonal jluctuations, natural background levels, ejfects on individuals and whole
populations)
• Environment characteristics (physical and chemical hydrography. oceanography, climate
changes, seasonal and long-termjluctuations)
• Host-disease-environment interactions and seasonal dynamics thereo/
Repeatedly, it has been pointed out that field studies alone are not sufficient to establish causeeffect relationships (e.g. already by Sinde~ann et al. 1980). In 1994, the ICES Advisory
Committee on the Marine Environment (ACME), therefore, recommended that the best
strategy to elucidate possible relationships between fish diseases and pollution should comprise
an integrated approach combining field studies, mesocosm and laboratory studies. Due to the
.resources and efforts needed to meet this recommendation, the ACME noted that standardized
;; ...
..
..
12
research in this field should be encouraged and integrated between institutes involved'
(Anonymous 1994). Examples for a successful combination of field and experimental studies
;;.
again are the US studies mentioned above. An example for mesocosm studies providing ..
significant information is the Dutch project on the effects of contaminated harbour sludge on
diseases of flounder in which the development of early stages of liver tumours and associated
changes under simulated natural conditions in large tanks could clearly be demonstrated
(Vethaak 1994).
However, it should be emphasized that severe doubts were expressed repeatedly whether, even
if the above missing information can be obtained and the proposed strategies can be followed,
a scientific proof of cIear cause-effect relationships between specific dysfunctions (including
disease) and specific poIlutants will be possible at aII, particularly under in silll conditions
(Dethlefsen 1988, Sindermann 1989, 1993). According to Dethlefsen (1990), current methods
used for in silll studies can only describe regional and spatial coincidences between (known)
contaminants and biological effects but cannot provide unequivocal scientific proof for a causeeffect relationship. At best, only circumstantial evidence can be achieved the degree of which
depends on the degree of statistical correlation. Due to these uncertainties, scientists involved
in such studies will always have to face the fact that any statements on the presence or absence
of a cause-effect relationship will be disputed according to the personal belief of other
scientists and non-scientists. Furthermore, experimental laboratory and mesocosm studies of
course are also criticaI due to the confinement of the test organisms and the artificiaI holding
conditions. These conditions may per se impose such a stress on the test organisms that their
responses to experimental stressors can be far from being natural and therefore, such studies
may not clearly enough elucidate mechanisms involved in the aetiology and pathogenesis of
diseases or other biological effects of contaminants. Furthermore, results from experiments
attempting to reproduce natural conditions cannot be directly interpolated to the in Sitll
situation due to the same reasons (more information about the Iimitations of toxicity bioassays
is for instance given by McCarthy & Shugart 1990). AIthough there is not much hope that
these general problems can be resolved, scientists should of course seak possibilities to
minirnize uncertainties regarding the interpretation of their results by using an appropriate
study design taking into account the requirements detailed above.
Strengths of fish disease monitoring
In the foIlowing, some strenghts and advantages of fish disease monitoring are Iisted:
• The costs 0/ fish disease monitoring are low compared to many other biological efJects
techniques
• Target diseases identified are, with a certain degree oftraining, easy to recognize
• A large nllmber o/fish can be screened and resllits are immediately available
• Large geographical areas can be monitored
• No laborolls laboratOl'y work is needed
• Target fish species and diseases have been identified. methodologies to monitor externall.v
visible fish diseases and macroscopic liver lesions have been intercalibrated on an
international level and standard protocols taking into aCcollnt qllality assurance reqllirements
have already been established and tested
• A large database with long-term fish disease data /rom the North Sea and Baltic Sea sllbmitted
by ICES Afember COllntries is avai/able in the ICES Environmental Databank and can be llsed
as baseline informationfor future monitoring programmes
e
•
13
• Standard procedures Jor data submission (lCES provides a fish disease data reporting and a
fish disease data entry programme), statistical analysis and dafa presentation have recently
been developed in lCES
• Diseases are an overt and integrative biological endpoint o[physiological changes at different
levels oJbiological organization (molecular. subce//ular, ce//ular, tissue, organ, hole organism
level) a.fJecting the organism's homeostasis and being associated with environmental change
(including unspecijic, stress-mediated immunotoxic e.fJects and more specific. efficfs 0/
anthropogenie contaminants)
• Fish disease data provide inJormation on longer-term biological e.fJects o[ environmental
changes. lin concert with more specific early-waming techniques, e.g. biomarkers Jor
contaminarit exposure and[or contaminant-induced damage, they can be used more specifica//y
as indicatorJor efficts oJcontaminants
• Signijicant changes oJ the disease prevalence are a biologica//y and ecologica//y relevant
warning sign Jor adverse environmental changes since diseases may aiftct growth.
reproduction and survival o[ aiftcted individuals and may. there[ore. have imp/ications on the
population level and may even affict populationslcommunities oJprey/predator species
• Data on the prevalence and spatial distribution o[diseases (including parasites) o[commercial
fish species are oJ direct use Jor qua/ity controls o[ fish as [ood resource Jor human
consumption
The occurrence of significant changes in the prevalence of gross fish diseases can be
considered an unspecific and more general indicator for chronic rather than acute
(environmental) stress and it can be speculated that they might, therefore, be a more useful
indicator of the complex changes typically occurring under field conditions as compared to
specific biomarkers of subtle early changes on molecular or cellular level. However,
biomarkers of contaminant exposure and of contaminant-induced damage can be considered of
higher toxicological value than gross fish diseases and may, due to their more rapid response,
be a more important early warning signal of acute contaminant effects.
•
According to Kinne (1984), disease of an organism tends to reduce the energy available for
sustaining essential functions and structures, the resistance to concomittantly effective stressors
(natural and man-made), the capabilities for defence and escape and the potential for
competition and counteracting additional disease-causing entities. Therefore, high prevalences
of diseases might have serious implications on fish populations in terms of growth,
reproduction and survival and can, therefore, be c1assified as an indicator at a higher level of
biological organizatiori with a higher ecological relevance thari biomarkers of early change.
Howevei-, as McCarthy & Shugart (1990) have emphasized, a comprehensive and integrated
biological effects monitoring progamme needs to consider responses at several levels of
organization, incIuding biomarkers measured at the organismic and suborganismic level as weil
as population and community level indicators in order to answer two critical questions:
• Are orgallisms exposed to levels oJ toxica11ls that exceed the capacity oJ Ilormal
detoxification and repair systems?
• Jf there is evidence oJexposure,
thell is the chemical stress impacting the integrity 0/ the
populations 01'
communities ?
,
There can be no doubt that monitoring programmes using only single biological indicators of
contaminant effects would not be able the answer to the above questions. \Vhat is needed is an
integrated monitoring approach such as that recommended by leES (Anonymous 1995)
.
~
"
l~
compnsmg a combination of techniques measuring the presence of contaminants in the '
environment (chemical moni!oring), the exposure of organisms and bioavailability of ~.
contaminants (molecular and cellillar biomarkers 01 exposure), early toxicological effects
~
(molecular and celllllar biomarkers 01 damage), responses on the organismie level (e.g.
general cOllditiOll, growth, reprodllctioll capacity, diseases, survival) and responses on the
populationlcommunity level (changes in the abulldance alld diversity olfish alld other species,
e.g. more statiollary benthic species). These monitoring components ean be supplemented by
experimental studies (bioassays) investigating the toxie potential ofmarine compartments (e.g.
sediments, water, surface microlayer). Whilst the responses measured at lower levels of
biological organization (molecules, cells) can provide sensitive and specifie responses to
particular toxicants, their biological significance is, however, mostly unclear. Responses at
higher levels (populations communities) are direcdy relevant to concerns about ecological
effects of contaminants but can usually not be used to distinguish between effects of
contaminants and effects of other environmerital faetors (McCarthy & Shugart 1990).
Conclusions and prospect for future (fish diseäse) monitoring programmes
The main conclusion ofthe present paper is that fish disease monitoring can be a useful tool for
pollution assessment provided that an appropriate multidisciplinary study design is being used
taking into account and trying to avoid identified weaknesses of past and present fish disease
studies. There is sufficient evidence in the literature that anthropogenie contaminants - once
they exceed certain critical levels - can be major causal factors in the aetiology of infectious
and non-infectious diseases of wild marine fishes either by causing unspecifie biological
responses affecting the disease resistance or by causing more specifie effects or by causing
both. Therefore, studies on fish diseases should b6 incorporated in national and international
monitoring programines on biological effects of contaminants. However, it snould c1early be
stated that more research is needed since, in particular for infectious disease, there is still an
incomplete understanding of the natural functioning of ecological systems inc1uding the
relationship between host, disease causing agent and the environment. In this respect, we have
to admit that not much progress has been made since Sindermann identified the problem in
1979. Possibly the only exception are the studies on neoplastic Iiver lesions' of coastal fish
species in polluted environments where the linkages between contaminants and diseases could
increasingly be elucidated during the past 10 years.
It has to be emphasized that epidemiological studies on the links between anthropogenic
contaminants and diseases ofwild marine fishes can at best provide circumstaniial evidence but
no scientifie proof for a cause-effect relationship. The degree of evidence depends on the
degree of mathematical plausibility which is influenced by the design of the study. Using an
appropriate multidisciplinary study design would increase the probability to identify
associations between contaminants and disease.
Due to the problems encountered with interpretation of results of fish disease studies, fish
disease monitoring alone would certainly not be sufficient to assess the effects of contaminants
in the marine environment. It has to be pointed out, however, that the same holds for any other
biological effects technique used in isolation. For instance, only applying molecular and cellular
biomarker techniques would in most cases not provide information on ecologically relevant
biological effects. It is crucial that, in order to design a high quality environmental monitoring
programme meeting its objectives, biological effects of contaminants have to be measured on
various levels of biological organization. Only this kind of integrative approach cari provide
infomiation needed on the Iinkages between exposure to contaminants and the ecological
relevance and time scales ofbiological effects.
•
IS
Acknowledgement
Thanks are due to colleagues from ICES Member Countries who provided us additional
information on present national fish disease monitoring programmes (G. Bylund, Finland, D.
Declerck, Belgium, M. Myers, USA. I. Tabolina, Latvia, A.R. McVicar and S.\V. Feist, UK).
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Figure 1: Relationship between the prevalence of lyrnphocystis in North Sea dab (Limanda
limanda) from the German Bight and the residues of the organochlorine HeB in the Iivers of
dab in summer ofthe years 1984-1994 (Dethlefsen & Lang, unpublished data)
Dab, German Bight
prevalence of disease vs residues in livers
28 , - - - - - - - ; - - - - - - ; - - - - - - - , . - - - - - - . . . . . . - - - - - - - - - - - ,
....c:c:
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:..
24
i
:
:
:
19~8
.
.
.
,
,
~
5
5
~
20
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.-....
~
16
-+ \.------'"'---------........._ - - - _.. . . . . .- -----"""------"'---------'
10
20
30
40
HeB, Ilg!kg, Iiver, fat
50
60
•