External Fish Disease
Stressed organisms are more susceptible to disease and evaluating the health status of fish provides an integrated assessment of the effects of multiple stressors, including contaminant exposure. A regional assessment found that external fish disease, expressed as the Fish Disease Index (determined from incidences and severity of externally visible diseases and parasites in UK flatfish), was below the Environmental Assessment Criteria in all biogeographic regions, which indicates that overall, the fish health status was acceptable.
Background
UK target on biological effects of contaminants (external fish disease)
This indicator is used to supplement the target covering the biological effects of contaminants set out in the Marine Strategy Part One (HM Government, 2012), which requires that “the intensity of those biological or ecological effects due to contaminants agreed by OSPAR as appropriate for the UK Marine Strategy Part One purposes are below the toxicologically based standards”. Whilst this indicator has not yet been agreed by OSPAR, its assessment provides an integrated measure of fish health, which can be impacted by exposure to contaminants, although other environmental stressors may also lead to an increase in prevalence. It is a general health indicator and has therefore been included in the assessment of Good Environmental Status for Contaminants.
Key pressures and impacts
The key pressures associated with this indicator are the presence of environmental contaminants that can damage the immune system of organisms (such as polychlorinated biphenyls, dioxins, certain pesticides and some metals including mercury), and other environmental stressors including inadequate nutrition and sub-optimal physico-chemical conditions. In the UK Initial Assessment (HM Government, 2012), the main anthropogenic pressures responsible for the presence of contaminants in the sea were identified as being point sources (for example, industrial and sewage discharges and emissions) and diffuse sources (for example, agriculture, roads run-off, households and atmospheric deposition). No significant new pressures have since been identified.
Measures taken to address the impacts
There is a robust UK legislative framework in place for controlling pollution from the main sources of contaminants (energy production, transport, urban and industrial uses), including appropriate consenting and River Basin Management Plans described in the Marine Strategy Part Three (HM Government, 2015).
Further information
The incidence and severity of fish disease have been monitored in North Sea fish for over 35 years. Disease incidence is an indicator of stressor impacts upon a key part of the marine ecosystem and monitoring allows for the impact assessment of multiple stressors on fish health. Stressors include nutrition, environmental variability (such as temperature, pH, hypoxia) and exposure to anthropogenic contaminants that impact immuno-competence and make organisms more susceptible to infection by disease-causing agents.
In common dab (Limanda limanda), the incidence of epidermal hyperplasia/papilloma was found to decrease offshore along a pollution gradient in the southern North Sea (Vethaak and others, 1992), whilst viral lymphocystis was found to be elevated in flounder experimentally exposed to contaminated sediments (Vethaak and others, 1996). Increases in epidermal papilloma and lymphocystis in dab from Danish waters in the 1980s were thought to be stress related, following a period of oxygen deficiency (Mellergard and Nielsen, 1997), indicating the multifactorial nature of fish disease. Hyperpigmentation in North Sea dab has been increasing in prevalence and severity over the last two decades (Grütjen and others, 2013; Lang and others, 2017a). The cause(s) of hyperpigmentation remain unclear, although no infectious agents appear to be implicated (Noguera and others, 2013), and it has previously been associated with cadmium exposure (Tysklind and others 2013).
In order to allow a quantitative integration of fish disease incidence and severity data, the ICES Working Group on Pathology and Diseases of Marine Organisms developed the Fish Disease Index and established corresponding assessment criteria for use by OSPAR (Lang and Wosniok, 2008; ICES, 2012; Lang and others, 2017a). The Integrated Assessment of Contaminant Impacts on the North Sea workshop reported that the Fish Disease Index of dab was positively correlated with exposure to methylmercury (Lang and others, 2017a) and was highest in dab from the central North Sea (Dogger Bank, Ekofisk and offshore of the Firth of Forth), and at background levels in fish from Icelandic waters (Lang and others, 2017b).
Assessment method
UK target on biological effects
Within the United Kingdom, the Clean Seas Environment Monitoring Programme (CSEMP) is one way our national and international commitments to monitor marine biota in estuarine, near-shore and offshore marine waters are met (Nicolaus and others, 2016). The main drivers for the current programme are the OSPAR Co-ordinated Environmental Monitoring Programme and the Joint Assessment and Monitoring Programme (OSPAR Commission, 2014), together with the UK Marine Strategy Part One (HM Government, 2012). Within CSEMP, the UK monitors contaminants and their biological effects in flatfish (mainly dab but also flounder and plaice) and cod from UK seas. External fish disease is one of several indicators used to inform progress against the target for biological effects of contaminants set out in the Marine Strategy Part One (HM Government, 2012). The assessment of disease status provides an integrated measure of fish health, natural and anthropogenic stressors (including contaminants).
Assessment methodology for externally visible fish disease
Externally visible fish disease data were obtained for dab, flounder and cod from CSEMP monitoring cruises. Only dab data were included in the assessment; for flounder and cod the assessment methodology has not been finalised. Following collection, each fish was weighed, measured and carefully examined for external fish disease including, hyperpigmentation (Figure 1), epidermal hyperplasia/papilloma (Figure 2), lymphocystis, X-cell gill disease, fin rot, skin ulcerations and for the presence of parasites (Acanthochondria cornuta, Lepeophtheirus pectoralis and Stephanostomum baccatum). These conditions, including severity scoring, are described in the ICES TIMES protocol number 19 (Bucke and others, 1996). All analyses were quality assured through the Biological Effects Quality Assurance in Monitoring Programmes Fish Disease Measurement programme.
Figure 1. Common dab (Limanda limanda) showing hyperpigmentation and an acute skin ulcer.
Figure 2. Lymphocystis on common dab (Limanda limanda).
Fish Disease Index
The Fish Disease Index (FDI) summarises the disease status of each fish into a single number, based upon the presence and severity of 9 grossly observable diseases. Each disease is assigned a weighting for the calculation using a procedure based on expert judgement (Lang and Wosniok, 2008). The FDI of each individual fish was calculated based on the procedure developed by the ICES Working Group on Pathology and Diseases of Marine Organisms (Lang and Wosniok, 2008; ICES, 2012; Lang and others, 2017b) using a package for the R statistical software environment (ICES, 2018) provided by Dr Werner Wosniok (University of Bremen, Germany). The FDI combines observations of disease incidence and severity, disease weighting scores (raw FDI), and adjusts the output to reflect factors including sex, size and time of year (standardised FDI).
Assessment scales
Monitoring of contaminants and their effects in flatfish is undertaken for CSEMP at fixed stations in estuarine, coastal and offshore waters. For this assessment of external fish disease, the data from sampling stations in coastal and offshore waters (estuaries do not fall within the scope of the UK MS Part One), were aggregated and assessed at the level of the 8 UK biogeographical marine regions that were defined in the Charting Progress 2 report on the status of the seas (UKMMAS, 2010). The two Marine Strategy Part One sub-regions (Greater North Sea and Celtic Seas) were also considered (Figure 3).
Meta-analysis of status and trends of External Fish Disease
Monitoring data are assessed for status and trends following standard OSPAR approaches. Data was collected between 2010 and 2021. Assessments are made for many time series, each of a single determinand in a single species at a single monitoring station.
An individual time series of standardised FDI is assessed for status if:
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there is at least one year with data in the period 2016 to 2021
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there are at least three years of data over the whole time-series
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a parametric model can be fitted to the data and used to estimate the mean activity in the final monitoring year (or, occasionally, if a non-parametric test of status is applied)
An individual time series is assessed for trends if:
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there is at least one year with data in the period 2016 to 2021
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there are at least five years of data over the whole time-series
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a parametric model can be fitted to the data and used to estimate the trend in mean activity
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the station is representative of the area, rather than located at known impacted sites
The results of the individual time series are synthesised to assess status and trends at the UK biogeographic regional level. Locations of monitoring stations where there are suitable data are shown in Figure 3. The number of time series in each biogeographic region is given in Table 1.
Figure 3: Monitoring sites used to assess external fish disease in common dab in each Marine Strategy region (dark lines) and biogeographic subregion (light lines). The filled circles indicate sites where there are sufficient data to assess both status and trends; the open circles indicate sites where only status can be assessed. There are additional sites that are not shown because they were not sampled often enough.
Table 1: Number of stations within each sub-region used in the assessment of status and trends.
UK Marine Strategy sub-region |
Biogeographic region |
Status assessment |
Trend assessment |
Greater North Sea |
Northern North Sea |
11 |
8 |
Greater North Sea |
Southern North Sea |
8 |
6 |
Greater North Sea |
East Channel |
2 |
2 |
Celtic Seas |
Minches & West Scotland |
1 |
1 |
Celtic Seas |
Irish Sea |
10 |
6 |
Celtic Seas |
West Channel & Celtic Sea |
3 |
2 |
Assessment thresholds for External Fish Disease
Two assessment criteria (Table 2) are used to assess visible disease of fish:
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Background Assessment Criteria
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Environmental Assessment Criteria
Background Assessment Criteria (BAC) were developed by OSPAR for testing whether observed levels of external fish disease (expressed as the FDI) are near background levels. Mean values significantly below the BAC are said to be near background. Mean values not significantly below the Environmental Assessment Criteria (EAC) indicate environmental harm.
Table 2: Assessment criteria for Fish Disease Index including Background Assessment Criteria (BAC) and Environmental Assessment Criteria (EAC), values rounded to 2 decimal places.
Criteria |
Value |
BAC |
1.51 |
EAC |
6.72 |
BAC and EAC have been developed for measurements of FDI in common dab (Limanda limanda) and were calculated based on long-term prevalence data from the period 1986 to 2010 derived from the German fish disease monitoring programme (ICES, 2012). The BAC is the lowest 10th percentile of all mean FDI values per sampling campaign and area; the EAC is based on the relationship between the mean FDI and the mean Condition Factor of the population (Fulton's Condition Factor = weight*100/length3) and is equal to a reduction of the Condition Factor by 10%, which is regarded as an unacceptable health effect (ICES, 2012).
Methodological improvements
In the UK MS 2018 assessment, the same methodology to determine the standardised FDI was used, although the status assessment for the 8 UK biogeographic marine regions was based on the most recent year of data for each station compared to the BAC and EAC (Table 1). There was insufficient data for a trend assessment during that assessment. The methodology used in the current assessment is a significant improvement since it provides an objective regional assessment of both status and trend and therefore more in keeping with other UK MS and OSPAR Quality Status Report contaminant assessments.
Individual Time Series
Information on how the individual time series as assessed for status and trends is described in the OSPAR Hazardous Substances Assessment Tool (https://dome.ices.dk/ohat/?assessmentperiod=2023).
Results
Findings in the 2018 UKMS Assessment
The 2018 UKMS assessment for visible disease in fish concluded that dab had an acceptable health status (Robinson and Bignell, 2018). For the Greater North Sea, dab were assessed as having a disease status that is above background but below levels of significant concern. However, the Northern North Sea region was assessed as above Environmental Assessment Criteria in one of the years (2014). Overall, dab from the UK portion of the Celtic Seas were assessed as having a disease status above background but below levels of significant concern. Trend assessment was not possible.
2024 UK MS Assessment Results
External fish disease was assessed at 35 locations in UK marine waters, excluding estuarine sites (Figure 1). The time between sampling visits varied from annually to once every six years. The data used in the assessment was collected between 2010 and 2021.
Status Assessment
For regional assessment, only biogeographic regions with a minimum of three suitable stations with a reasonable geographic spread were included. There was insufficient data for regional analysis of the Scottish Continental Shelf, Minches & Western Scotland and Eastern Channel regions.
Levels of external fish disease, expressed as a standardised Fish Disease Index (FDI) were compared to OSPAR Background Assessment Criteria (BAC) and Environmental Assessment Criteria (EAC). The BAC determines if observed fish disease is at background or elevated. Furthermore, EAC identifies if the degree of fish disease is causing significant harm. A FDI below the EAC indicates an acceptable health status.
Regional assessment found that external fish disease, expressed as the FDI, was below the EAC in all biogeographic regions assessed (Figure 4) which indicates that overall, the fish health status was acceptable. However, when assessed individually, a number of stations are still above EAC, especially in the Northern North Sea region implying an unacceptable fish health status at some specific locations (Figure 5).
Figure 4: The mean standardised fish disease index (FDI) (coloured circles) in each biogeographic region. The horizontal line indicates the upper one-sided 95% confidence limit on the mean. The grey vertical lines are, from left to right, the Background Assessment Criterion (BAC) and the Environmental Assessment Criterion (EAC). The mean FDI is significantly below the BAC or EAC (p < 0.05) if its upper confidence limit is less than BAC or EAC respectively. The dark blue circles indicate that the mean FDI is significantly below the EAC (p < 0.05) but is not also significantly below the Background Assessment Criterion.
Figure 5: Status and trends of external fish disease, expressed as the standardised fish disease index (FDI), at each monitoring site. Light blue: the mean FDI is significantly below the Background Assessment Criterion (BAC) (p < 0.05). Dark blue: the mean FDI is significantly below the Environmental Assessment Criterion (EAC) (p < 0.05) but not the BAC. Red: the mean FDI is not significantly below the EAC (p > 0.05). Circle: no significant change in mean FDI (p > 0.05) or no trend assessment possible. Downward triangle: significant decrease in mean FDI (p < 0.05). Upward triangle: significant increase in mean FDI (p < 0.05).
Trend Assessment
Trends in external fish disease were assessed in biogeographic regions where there were at least five years of data from representative sites (Figure 6). There was insufficient data for regional analysis of the Scottish Continental Shelf, Minches & Western Scotland, Western Channel & Celtic Seas and Eastern Channel regions.
Figure 6: The yearly change (circles) in the mean standardised fish disease index in each biogeographic region. The horizontal line is the associated 95% confidence interval. There is a significant change in mean FDI (p < 0.05) if the confidence interval does not cut the vertical line at 0. The circle indicates that there is no significant change in mean FDI (p > 0.05).
When assessed at the biogeographic regional level, the level of external fish disease observed in the Northern North Sea, Southern North Sea and Irish Sea, was stable. However, when assessed at the individual station level, most stations were also stable, one downward trend was observed, and five stations had an upwards trend (Figure 5).
Further information
Individual Stations Status Assessment
Although the regional assessment of status for external fish disease (Figure 5) shows that four regions assessed were below the Environmental Assessment Criteria (EAC), a number of individual stations are above EAC, indicating an unacceptable status (Figure 7).
Figure 7: The mean standardised fish disease index (FDI) (coloured circles) at each monitoring site. The grey vertical lines are, from left to right, the Background Assessment Criterion (BAC) and the Environmental Assessment Criterion (EAC). The mean FDI is significantly below the BAC or EAC (p < 0.05) if its upper confidence limit (not displayed) is less than BAC or EAC respectively. Light blue: the mean FDI is significantly below the Background Assessment Criterion (p < 0.05). Dark blue: the mean FDI is significantly below the EAC (p < 0.05) but not the BAC. Red: the mean FDI is not significantly below the EAC (p > 0.05).
The biogeographic region with the highest number of stations with an unacceptable status was the Northern North Sea where 45% (5 out of 11) of assessments exceeded the EAC, and 55% (6 out of 11) of assessments were below the EAC. In the Southern North Sea only one station had an unacceptable status above the EAC, with the majority (88%) of stations below the EAC. The Eastern Channel had only two stations so a regional assessment here was not possible, although both stations were assessed as below the EAC. The Northern North Sea, Southern North Sea and Eastern Channel biogeographic regions constitute the Greater North Sea UKMS subregion. The UKMS sub-region with the highest number of stations with an unacceptable status was the Greater North Sea subregion, where 29% (6 out of 15) of assessments were above the EAC.
In comparison, all 14 stations within the Celtic Seas UKMS sub region (comprising the Minches & Western Scotland, Irish Sea and Western Channel & Celtic Seas biogeographic regions) were below the EAC, and one of these was also below the BAC. The Minches & Western Scotland region only had one station; therefore, a regional assessment was not possible. There are a lot of stations in the Irish Sea (10) and three in the Western Channel & Celtic Seas region.
Individual Stations Trend Assessment
Three stations from the Northern North Sea, one in the Minches & Western Scotland region and one in the Irish Sea showed an increasing trend (Figure 8). One station in the Western Channel & Celtic Sea had a downward trend. All other stations were stable – 81% (13 out of 16) and 67% (6 out of 9) stations were stable in the Greater North Sea and Celtic Seas sub regions respectively.
Figure 8: The yearly change (circle, triangle) in the mean standardised fish disease index (FDI) at each monitoring site. There is a significant change in mean FDI (p < 0.05) if its 95% confidence interval (not shown) does not cut the vertical line at 0. Circle: no significant change in mean FDI (p > 0.05). Downward triangle: significant decrease in mean FDI (p < 0.05). Upward triangle: significant increase in mean FDI (p < 0.05).
Conclusions
Overall, the regional assessments concluded that the fish health status of dab in UK marine environment was stable and at an acceptable level. However, there are still some fishing stations, mainly in the Northern North Sea, where external fish disease is elevated above the threshold which indicates significant harm. Furthermore, there are also some stations where external fish disease is increasing.
Further information
Twenty-nine per cent of fishing stations in the Northern North Sea have elevated fish disease above the EAC indicating an unacceptable health status. It was identified during development of the OSPAR assessment criteria that the North Sea is known to have a higher prevalence and severity of fish disease compared to the Baltic Sea (ICES, 2012). Fish health is complex with multiple contributing factors, including contaminant exposure. However, the elevated fish disease is not in keeping with the UKMS 2024 contaminant assessment where there are higher concentrations of contaminants in other areas like the Celtic Seas including the Irish Sea area. Therefore, it is plausible that the higher fish disease in the Northern North Sea is the result of additional factors other than contaminants.
Knowledge gaps
There were insufficient data for regional assessment of status and trends in four biogeographic regions (Scottish Continental Shelf, Minches and Western Scotland, Western Channel & Celtic Sea and Eastern Channel). Increasing sampling in these regions would enable this.
The assessment criteria were designed for use across all marine areas but were devised with data from the North Sea and the Baltic Sea only. The Baltic Sea is enclosed and has low salinity, and the North Sea is semi-enclosed. Refinement of the assessment criteria including analysis of data from other sea areas such as those that are influenced by open Atlantic waters, for example Western Scotland, would be beneficial.
Further information
Further analysis of which diseases are driving the elevated FDI in Northern North Sea and the increasing trends observed at some stations is required. Incorporating historical data from the North Sea into the analysis may bring further clarity to the trend assessment. External fish disease was monitored in the North Sea previously, before it was included in the UK Clean Seas Environment Monitoring Programme (CSEMP), so inclusion of this data in the analysis may be worth exploring. Further work into the links between FDI and contaminant exposure would be useful. Assessing the fish disease data against other environmental data including pH, salinity, dissolved oxygen and temperature would also be beneficial.
Although the meta-analysis used here was an improvement since UKMS 2018, further refinement of the statistical analysis is required.
References
Bucke D, Vethaak AD, Lang T, Mellergaard S (1996). Common diseases and parasites of fish in the North Atlantic: Training guide for identification. ICES Techniques in Marine Environmental Sciences number 19, 27 pages (accsessed on 6 July 2023).
Grütjen F, Lang T, Feist S, Bruno D, Nogeura P, Wosniok W (2013). Hyperpigmentation in North Sea dab Limanda limanda I Spatial and temporal patterns and host effects. Diseases of Aquatic Organisms, 103:9-24.
HM Government (2012). Marine Strategy Part One: UK Initial Assessment and Good Environmental Status. (accessed on 6 July 2023)
HM Government (2015). Marine Strategy Part Three: UK Programme of Measures. December 2015 (accessed on 6 July 2023).
ICES (2012). Report of the Working Group on Pathology and Diseases of Marine Organisms (WGPDMO). ICES CM 2012/SSGHIE:03, pages 48-61’ (accessed on 6 July 2023).
ICES (2018). Report of the Working Group on Pathology and Diseases of Marine Organisms (WGPDMO). 13-17 February 2018, Riga, Latvia. ICES CM 2018/ASG:01. 42 pages (accessed on 6 July 2023).
Lang T, Wosniok W (2008). The Fish Disease Index: a Method to Assess Wild Fish Disease Data in the Context of Marine Environmental Monitoring. ICES CM 2008/D:01, p 13.
Lang T, Kruse R, Haarich M, Wosniok, W (2017a). Mercury species in dab (Limanda limanda) from the North Sea, Baltic Sea and Icelandic waters in relation to host-specific variables. Marine Environmental Research, 124:32-40.
Lang, T, Fiest SW, Stentiford GF, Bignel JP, Vethaak AD, Wosniok, W (2017b). Diseases of dab (Limanda limanda): Analysis and assessment of data on externally visible diseases, macroscopic liver neoplasms and liver histopathology in the North Sea, Baltic Sea and off Iceland. Marine Environmental Research, 124: 61-69.
Mellergard S, Nielsen E (1997). Epidemiology of lymphocystis, epidermal papilloma and skin ulcers in common dab Limanda limanda along the west coast of Denmark. Diseases of Aquatic Organisms, 30: 151-163.
Nicolaus EEM, Wright SR, Bolam TPC, Barber JL, Bignell JP, Lyons B (2016).Spatial and temporal analysis of the risks posed by polychlorinated biphenyl and metal contaminants in dab (Limanda limanda) collected from waters around England and Wales Marine Pollution Bulletin, 112(1-2):399-405.
Noguera P, Feist SW, Bateman KS, Lang T, Grütjen F, Bruno DW (2013). Hyperpigmentation in North Sea dab Limanda limanda II Macroscopic and microscopic characteristics and pathogen screening. Diseases of Aquatic Organisms, 103: 25-34.
OSPAR Commission (2014). OSPAR Joint Assessment and Monitoring Programme (JAMP) 2014 – 2021. Ospar Agreement 2014-02 (accessed on 6 July 2023)
Robinson, C, Bignell, J. P, (2018). Status assessment for biological effects (visible diseases) in fish’ UK Marine Online Assessment Tool, available at: https://moat.cefas.co.uk/pressures-from-human-activities/contaminants/external-fish-disease/ (accessed on July 2023).
Tysklind N, Taylor MI, Lyons BP, Goodsir F, McCarthy ID, Carvalho, G (2013). Population genetics provides new insights into biomarker prevalence in dab (Limanda limanda L): a key marine biomonitoring species. Evolutionary Applications, 6: 891-909.
UKMMAS (2010). Charting Progress 2: An assessment of the state of the UK seas. Published by Defra on behalf of the UK Marine Monitoring and Assessment Strategy community (accessed on 4 January 2018).
Vethaak AD, Bucke D, Lang T, Wester PW, Jol J, Carr M (1992). Fish disease monitoring along a pollution transect: a case study using dab Limanda limanda in the German Bight. Marine Ecology Progress Series, 91:173-192.
Vethaak AD, Jol JG, Meijboom A, Eggens ML, ap Rheinallt T, Wester PW, van de Zande T, Bergman A, Dankers N, Ariese F, Baan RA, Everts JM, Opperhuizen A, Marquerie JM (1996). Skin and liver diseases induced in flounder (Platichthys flesus) after long-term exposure to contaminated sediments in large-scale mesocosms. Environmental Health Perspectives, 104: 1218-1229.
Authors
Hannah Anderson1
1Marine Directorate of the Scottish Government
Assessment metadata
Assessment Type | UK Marine Strategy Framework Directive Indicator Assessment |
---|---|
D8 Contaminants | |
D8.2. Effects of Contaminants | |
Point of contact email | marinestrategy@defra.gov.uk |
Metadata date | Sunday, June 1, 2025 |
Title | Biological effects (visible diseases) in fish |
Resource abstract | |
Linkage | |
Conditions applying to access and use | © Crown copyright, licenced under the Open Government Licence (OGL). |
Assessment Lineage | |
Indicator assessment results | |
Dataset metadata | |
Links to datasets identifiers | |
Dataset DOI | The Scottish Government, Marine Directorate. 2025. https://doi.org/10.7489/12541-1 |
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