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. The Fish Disease Index is determined from observations of the incidence and severity of externally visible diseases and parasites in UK flatfish, and indicates that dab have an acceptable health status.

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 Marine Strategy Framework Directive purposes are below the toxicologically-based standards”. Whilst this indicator has not yet been agreed by OSPAR for Marine Strategy Framework Directive (European Commission, 2008) purposes, its assessment provides an integrated measure of the health of fish, which can be impacted by exposure to contaminants and other environmental stressors 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 in the environment of 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).

Monitoring, assessment and regional co-operation

The monitoring and assessment of external fish disease is an OSPAR Candidate Indicator, as not all Contracting Parties currently include it in their monitoring programmes.

Areas that have been assessed

Status assessments were conducted for the UK biogeographic marine regions and aggregated to the UK-portions of the Greater North Sea and the Celtic Seas Marine Strategy Framework Directive sub-regions

Monitoring and assessment methods

Risk-based monitoring and assessment was conducted within the UK Clean Seas Environmental Monitoring Programme, using methods and principles set out by the OSPAR Coordinated Environmental Monitoring Programme. Data were assessed using methods developed by the International Council for the Exploration of the Seas Working Group on Pathology and Diseases of Marine Organisms.

Assessment thresholds

OSPAR and ICES have developed Environmental Assessment Criteria to assess whether significant harm is occurring, and Background Assessment Criteria to allow the assessment of whether the OSPAR objective of close-to-background levels of contaminants and their effects have been achieved. 

Further information

The incidence and severity of fish diseases 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 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 European Union Marine Strategy Framework Directive (European Commission, 2008) and Water Framework Directive (European Commission, 2000). Within the Clean Seas Environment Monitoring Programme, the UK monitors contaminants and their biological effects in flatfish (mainly dab but also flounder and plaice) 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). Monitoring and assessments are the scale of the 8 UK biogeographical marine regions that were defined in the Charting Progress 2 report on the status of the seas (UKMMAS, 2010). Assessments have been aggregated to report on the UK portions of the Marine Strategy Framework Directive Greater North Sea and the Celtic Seas sub-regions.

Assessment methodology for externally visible fish diseases

Externally visible fish disease data were obtained for dab, flounder and cod from Clean Seas Environment Monitoring Programme research cruises. Only dab data was assessed; for flounder the assessment methodology has not been finalised, and there were very few cod data available.

Following collection, each fish was weighed, measured and carefully examined for 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 green hyperpigmentation and an acute skin ulcer.

 

Figure 2. Epidermal hypoplasia/papilloma on common dab (Limanda limanda).

Assessment scales

Monitoring of contaminants and their effects in flatfish is undertaken for the Clean Seas Environment Monitoring Programme at fixed stations in estuarine, coastal and offshore waters. For this assessment of fish disease, the data from sampling stations in coastal and offshore waters that are representative of the area, rather than located at known impacted sites (estuaries do not fall within the scope of the Marine Strategy Framework Directive), were aggregated and assessed at the level of the 8 UK marine biogeographic regions. The assessments of the 8 UK regions were used as the basis of expert opinion when assessing status at the scale of the UK waters within the two Marine Strategy Framework Directive sub-regions (Greater North Sea and Celtic Seas).

Assessment thresholds for fish disease

Two assessment criteria are used to assess visible disease of fish:

  • Background Assessment Criteria
  • Environmental Assessment Criteria

Background Assessment Criteria were developed by OSPAR for testing whether observed levels of fish disease (expressed as the Fish Disease Index) are near background levels. Mean values significantly below the Background Assessment Criteria are said to be near background. Mean values not significantly below the Environmental Assessment Criteria indicate environmental harm.

Background Assessment Criteria and Environmental Assessment Criteria have been developed for measurements of Fish Disease Index in 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 Background Assessment Criteria is the lowest 10th percentile of all mean Fish Disease Index values per sampling campaign and area; the Environmental Assessment Criteria is based on the relationship between the mean Fish Disease Index 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).

Assessment of disease in fish

The Fish Disease Index summarises the disease status of each fish into a single number, based upon the presence and severity of 9 grossly observable diseases, which are assigned a weighting for the calculation using a procedure based on expert judgement (Lang and others, 2017a). The Fish Disease Index was determined for dab collected between 2010 and 2015. The Fish Disease Index of each individual fish was calculated using 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 Fish Disease Index combines observations of disease incidence and severity, disease weighting scores (raw Fish Disease Index), and adjusts the output to reflect factors including sex, size and time of year (standardised Fish Disease Index). Assessment of status for the 8 UK biogeographic marine regions involved determining the standardised Fish Disease Index for each marine region and comparing it with the Background Assessment Criteria and Environmental Assessment Criteria. The statistical package also allowed temporal trends of the Fish Disease Index to be assessed at the UK biogeographic region scale.

Results

The Fish Disease Index is not included as part of the UK Marine Strategy Framework Directive target for Good Environmental Status (often referred to as GES), although it can be used to provide additional confidence in the assessments of contaminants. Fish Disease Index responses below the Environmental Assessment Criteria indicate an acceptable health status for the monitored flatfish populations. Figure 3 shows the locations of the sampling stations and the results of the assessment of standardised Fish Disease Index for dab in the UK biogeographic marine regions for the most recent year available at each site.

Figure 3. Location of dab sampling stations (purple circles) and status assessment (coloured numbered regions) of the standardised Fish Disease Index in the most recent year sampled at each station, at the scale of the UK marine regions. Blue: the mean Fish Disease Index is significantly (p < 0.05) below the Background Assessment Criteria; green: the mean Fish Disease Index is significantly (p < 0.05) below the Environmental Assessment Criteria. Regions with coloured hatching are tentative assessments due to a limited number of sampling sites. Region 1 = northern North Sea; 2 = southern North Sea; 3 = eastern English Channel; 4 = western English Channel and Celtic Sea; 5 = Irish Sea; 6 = Western Scotland and the Minches; 7 = Scottish Continental Shelf; 8 = Atlantic North Western approaches (not assessed).

Status assessment

Greater North Sea

Overall, dab from the UK North Sea were assessed as having a disease status that is above background but below levels of significant concern. In the period 2010 to 2015, this status was stable for two of the three UK regions in the Greater North Sea, but disease incidence/severity increased in the Northern North Sea.

Celtic Seas

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. Disease status was stable for the period 2010 to 2015.

The number of stations assessed for status and for trends in each Marine Strategy Framework Directive sub-region and each UK biogeographic region are shown in Table 1.

Table 1. Number of time series within each UK biogeographic marine region used in the assessment of fish disease status and tends. Atlantic North West Approaches were not assessed.

MSFD Sub-region

UK marine region

Status

Trend

Greater North Sea

Northern North Sea

12

7

Southern North Sea

9

6

Eastern Channel

3

2

Celtic Seas

Western Channel & Celtic Sea

4

2

Irish Sea

10

5

West Scotland & the Minches

1

1

Scottish Continental Shelf

2

0

In the Greater North Sea, the standardised Fish Disease Index of the 3 UK marine regions was assessed as being above Background Assessment Criteria but below Environmental Assessment Criteria, in the last year of the time series, indicating that dab have a disease status that is poorer than background but not of significant concern (Figure 3). However, the Northern North Sea region was assessed as above Environmental Assessment Criteria in 2014 (Table 2).

Table 2. Status assessment of the standardised Fish Disease Index in each sampling year at the scale the UK marine regions. “<BAC”: the mean Fish Disease Index is significantly (p < 0.05) below the Background Assessment Criteria; “<EAC”: the mean Fish Disease Index is significantly (p < 0.05) below the Environmental Assessment Criteria; “≥EAC”: the mean Fish Disease Index is at, or above, the Environmental Assessment Criteria; * indicates that the status is tentative due to a limited number of sampling stations in that marine region. MSFD: Marine Strategy Framework Directive.

MSFD

Sub-region

UK Marine Region

2010

2011

2012

2013

2014

2015

Greater

North Sea

Northern North Sea

< EAC

< EAC

< EAC

< EAC

≥ EAC

< EAC

Southern North Sea

< EAC

< EAC

not assessed

< EAC

not assessed

< EAC

Eastern Channel

< BAC

< EAC

not assessed

<EAC

not assessed

<EAC

Celtic Seas

W Channel & Celtic Sea

< EAC

not assessed

<EAC

not assessed

< EAC

< EAC

Irish Sea

< EAC

< EAC

<EAC

<EAC

< EAC

< EAC

W Scotland & the Minches

< BAC *

< BAC *

< BAC *

not assessed

not assessed

not assessed

Scottish Continental Shelf

not assessed

not assessed

not assessed

not assessed

< BAC

not assessed

In the Celtic Seas, two UK regions (Western Scotland and the Minches, and Scottish Continental Shelf) were assessed as having background levels of disease below the Background Assessment Criteria (although there is only one sampling site in the former region and the assessment therefore tentative). The Irish Sea and the Western Channel and Celtic Sea regions are above Background Assessment Criteria but below Environmental Assessment Criteria.

There were no clear trends in the health status (mean standardised Fish Disease Index scores) of flatfish observed at the Marine Strategy Framework Directive sub-regional scale, although the Northern North Sea UK biogeographic marine region had an apparent increase in Fish Disease Index score over the period 2010 to 2015 (Figure 4). Of 41 timeseries, 21 could be assessed for trends (because they had been sampled at least three times during 2010 to 2015), of which only 3 showed clear trends in their Fish Disease Index score: Rye Bay and Newhaven (both stations in the eastern Channel) and the Outer Moray Firth (Northern North Sea). All 3 had upward trends in the standardised Fish Disease Index score with the Outer Moray Firth being above Environmental Assessment Criteria in 2014, whilst Rye Bay and Newhaven were below it in 2015.

Figure 4. Mean standardised Fish Disease Index in each sampling year (2010 to 2015) for the UK biogeographic marine regions. The blue horizontal line indicates the Background Assessment Criteria and the red line the Environmental Assessment Criteria.

It is not clear what is driving the increasing trend for Fish Disease Index in the Northern North Sea. Whilst hyperpigmentation has been reported as increasing in long-term datasets (Grütjen and others, 2013; Lang and others, 2017a), in this assessment of data from 2010 to 2015, there are no clear upward trends in the incidence/severity of any individual disease, and the increase is therefore a cumulative response. The Shetland site, with data available only between 2010 and 2012, had relatively low Fish Disease Index scores for the North Sea. However the subsequent absence of this site from the dataset does not explain why the Fish Disease Index shows a year-on-year increase from 2010 to 2014. Further analysis of data from a longer time series (including pre-2010 data) is required to investigate the reasons for this increase.

Conclusions

Fish disease did not exceed the Environmental Assessment Criteria for any marine region and thus dab disease status is acceptable for the UK portions of both the Marine Strategy Framework Directive Greater North Sea and Celtic Seas sub-regions. There were finer scale temporal and spatial variations within the assessment. It can be concluded that the disease status of dab is similar to the contaminant status of the UK seas: healthy in the North and West, but less healthy in the Irish Sea, North Sea and eastern Channel. This status also reflects the relative degrees of other anthropogenic pressure. Elevated disease prevalence is an ecologically relevant response to the impact of environmental stressors on fish immunocompetence. Health status monitoring of fish is an important component in assessing ecosystem health.

Knowledge gaps

  1. The upwards trends in the Fish Disease Index of dab from the Moray Firth and the Eastern Channel need verification, which can be achieved by extending the time series to include data collected before 2010.
  2. There are too few monitoring sites and/or years to provide good confidence in the status assessments for the Minches and western Scotland region and for the Scottish Continental Shelf region.
  3. Links between the Fish Disease Index and individual diseases with contaminants are tentative, and based upon association and correlation, rather than cause and effect. More mechanistic research approaches are required to investigate possible links between the two.
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 (viewed on 12 December 2018)

European Commission (2008a) ‘Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive)’ Official Journal of the European Union L 164, 25.6.2008, pages 19-40 (viewed on 16 November 2018)

European Commission (2000) ‘Directive 2000/60/EC of the European Parliament and of the Council establishing a framework for the Community action in the field of water policy’ Official Journal of the European Union L 327, 22.12.2000, pages 1–73 (viewed on 16 November 2018)

European Commission (2008a) ‘Directive 2008/56/EC of the European Parliament and of the Council of 17 June 2008 establishing a framework for community action in the field of marine environmental policy (Marine Strategy Framework Directive)’ Official Journal of the European Union L 164, 25.6.2008, pages 19-40 (viewed on 16 November 2018)

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 (viewed on 12 December 2018)

HM Government (2012) ‘Marine Strategy Part One: UK Initial Assessment and Good Environmental Status’ (viewed on 16 November 2018)

HM Government (2012) ‘Marine Strategy Part One: UK Initial Assessment and Good Environmental Status’ (viewed on 16 November 2018)

HM Government (2015) ‘Marine Strategy Part Three: UK Programme of Measures’ December 2015 (viewed on 16 November 2018)

ICES (2012) ‘Report of the Working Group on Pathology and Diseases of Marine Organisms (WGPDMO)’ ICES CM 2012/SSGHIE:03, pages 48-61’ (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

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 (viewed on 10 December 2018) (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

OSPAR Commission (2014) ‘OSPAR Joint Assessment and Monitoring Programme (JAMP) 2014 – 2021’ Ospar Agreement 2014-02 (viewed on 27 November 2018)

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 (viewed on 12 December 2018)

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 (viewed 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 (viewed on 12 December 2018)

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 (viewed on 12 December 2018)

Acknowledgements

Assessment metadata
Assessment TypeUK Marine Strategy Framework Directive Indicator Assessment
 

D8 Contaminants

 

D8.2.  Effects of Contaminants

 
Point of contact emailmarinestrategy@defra.gov.uk
Metadata dateWednesday, April 15, 2020
TitleBiological effects (visible diseases) in fish
Resource abstract
Linkage

Data shows the status and trends of external fish disease in common dab at monitoring stations in waters around the UK. A fish disease index (FDI) that 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) was calculated at an individual level.

Conditions applying to access and use

© Crown copyright, licenced under the Open Government Licence (OGL).

Assessment Lineage

Fish disease data were collected from various sampling stations in UK coastal and offshore regions as part of the Clean Seas Environment Monitoring Programme, winter cruise by Marine Scotland Science and Cefas trained operators following standardised ICES TIMES no. 19. 

Indicator assessment results
Dataset metadata

Please, see below

Links to datasets identifiers

https://portal.medin.org.uk/portal/start.php#details?tpc=012_Marine_Scotland_FishDAC_12111

Dataset DOI

https://doi.org/10.7489/12230-1

The Metadata are “data about the content, quality, condition, and other characteristics of data” (FGDC Content Standard for Digital Geospatial Metadata Workbook, Ver 2.0, May 1, 2000).

Metadata definitions

Assessment Lineage - description of data sets and method used to obtain the results of the assessment

Dataset – The datasets included in the assessment should be accessible, and reflect the exact copies or versions of the data used in the assessment. This means that if extracts from existing data were modified, filtered, or otherwise altered, then the modified data should be separately accessible, and described by metadata (acknowledging the originators of the raw data).

Dataset metadata – information on the data sources and characteristics of data sets used in the assessment (MEDIN and INSPIRE compliance).

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Indicator assessment metadata – data and information about the content, quality, condition, and other characteristics of an indicator assessment.

MEDIN discovery metadata - a list of standardized information that accompanies a marine dataset and allows other people to find out what the dataset contains, where it was collected and how they can get hold of it.

Recommended reference for this indicator assessment

Craig Robinson1 and John P. Bignell2 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/

1Marine Scotland

2Centre for Environment, Fisheries and Aquaculture Science