Table of Contents

{TOC}

Independent Expert Assessment of Unusual Crustacean Mortality in the North-east of England in 2021 and 2022

Compiled by a panel of independent experts convened by Defra’s Chief Scientific Adviser

17 January 2023

© Crown copyright 2023

This information is licensed under the Open Government Licence v3.0. To view this licence, visit www.nationalarchives.gov.uk/doc/open-government-licence/

This publication is available at: https://www.gov.uk/government/publications/assessment-of-unusual-crustacean-mortality-in-the-north-east-of-england-in-2021-and-2022

Any enquiries regarding this publication should be sent to us at ExternalAdvice@defra.gov.uk

Forward

This report documents the findings of an expert panel convened to consider the unusual mass mortality of crustaceans in the north-east of England starting in autumn 2021.

The panel was chaired by the Chief Scientific Adviser (CSA) of the Department for Environment, Food and Rural Affairs (Defra), Professor Gideon Henderson, with input from the Government CSA (GCSA) Professor, Sir Patrick Vallance. The crustacean mortality expert panel (CMEP) consisted of experts from academia and industry with a range of knowledge and experience spanning crustacean biology, marine eco-toxicology, sea-life histology/pathology, marine pollutants, algal blooms, chemical dispersion in the oceans, sediment and water chemistry, dredging, and coastal processes. The full CMEP met on three occasions between December 2022 and January 2023, with subgroups meeting to analyse aspects of the issue between meetings. The CMEP was tasked with providing an independent scientific assessment of all the possible causes of the mass crustacean mortality incident using all the relevant available data. The CMEP’s remit did not extend to consideration of government processes during the investigation of the mortality event(s), to food safety, nor to the economic implications of the deaths. This report represents the consensus views of the CMEP, has been produced by the CSA’s Office, and reviewed by the GCSA.

Membership of CMEP:

Gideon Henderson – Defra Chief Scientific Adviser

Eileen Bresnan – Marine Scotland

Jan Brooke – Environmental consultant

Keith Davidson – Scottish Association for Marine Science (SAMS)

Mike Dearnaley – HR Wallingford

Mark Fitzsimons – University of Plymouth

Alex Ford – University of Portsmouth

Tamara Galloway – University of Exeter

Crispin Halsall – University of Lancaster

Tammy Horton – National Oceanography Centre (NOC)

Mark Inall – Scottish Association for Marine Science (SAMS)

Marian Scott – University of Glasgow

David Wilcockson – Aberystwyth University

Executive summary

An unusually large number of dead or dying crustaceans started to be found along the coast of the north-east of England from early October 2021. This unusual mortality continued through October and November 2021, and continued periodically through 2022 (although it is difficult to distinguish reporting bias due to increased awareness). Crustacean wash-ups were found along at least 70 km of coastline, and dead or dying crustaceans were also reported by fishers over a wide region.

Some of these crustaceans displayed a twitching behaviour not normally observed in beach wash-ups, or during fishing activity. This unusual twitching was particularly apparent during the initial period of mortality (October to November 2021) and again during May 2022, and was observed along at least 70 km of the coastline.

Initial unusual wash-ups were dominated by crabs. There have been reports of a number of other species found dead on beaches in the area, but it is unclear these are more frequent than normal occurrences, with the possible exception of a large number of octopuses on one occasion.

The cause of this unusual crustacean mortality event has been controversial, with two prevailing theories being considered most closely: a harmful algal bloom, and toxicity from pyridine released by local dredging activity.

The Crustacean Mortality Expert Panel (CMEP) was convened in December 2022 to provide an independent scientific assessment of all the possible causes of the mass crustacean mortality incident using all relevant available data. The panel considered possible causes (including but not limited to the two previously dominant theories) and grouped their consideration into four sections: disease pathology, harmful algal bloom, chemical toxicity, and dredging.

Each potential cause was assessed for likelihood, as defined by the Intergovernmental Panel of Climate Change (IPCC) likelihood scale (italics are used to denote use of this scale).

Table 1: IPCC likelihood terminology.

|hl Terminology |hl Likelihood of the occurrence/outcome |

| Virtually certain | >99% probability of occurrence |

| Very likely | >90% probability |

| Likely | >66% probability |

| About as likely as not | 33 to 66% probability |

| Unlikely | <33% probability |

| Very unlikely | <10% probability |

| Exceptionally unlikely | <1% probability |

Disease pathology

The panel considered whether the mortalities could be caused by disease or parasites. There are pathogens that are known to cause similar symptoms to those observed in the north-east of England, including the unusual twitching behaviour. Such pathogens have caused mortality events and declines in crustacean populations around the world. An amoebic crustacean disease, belonging to a similar group of parasites causing mortalities in the USA, has recently been found for the first time in UK waters in crabs on the south coast. No significant pathogens were identified in the northeast crabs, but full molecular screening was not conducted. The panel consider it is about as likely as not, that a pathogen new to UK waters caused the unusual crustacean mortality.

Harmful algal bloom (HAB)

Coastal waters can, under certain conditions, experience a bloom of particular taxa that cause harm to the marine ecosystem or species. These harmful algal blooms (HABs) can cause mortality due to release of toxins from the algae in the bloom, or because they lead to depletion of oxygen in the water.

The expert panel assessed satellite data and water-column measurements and concluded that the presence of an algal bloom in the area during September 2021 was likely. The intensity and duration of this bloom is uncertain, but it is unlikely that the bloom persisted beyond a storm in early October 2021.

Karenia mikimotoi is the most likely species to cause mortalities of benthic organisms by an algal toxin in UK waters. There is some evidence for the presence of this species in the month before the mortality events, but a lack of measurements at the time and location of the mortality events prevent assessment of the role of algal toxins. The impacts of algal toxins are relatively indiscriminate and it would be anticipated that a widespread mortality of a broad range of organisms would also have been reported. This lack of evidence, and particularly the continuation of mortality beyond the time when a HAB is likely to be present, make it unlikely that a HAB toxin caused the unusual crustacean mortality. As the algae die oxygen levels in the benthic zone where crustaceans reside can decrease. Such conditions generally impact multiple bottom-dwelling species, but there is evidence that crustaceans are particularly vulnerable to lowering oxygen levels. Anoxia may therefore contribute to the unusual mortality of crustaceans, particularly in October 2021, but the panel could find no published evidence that low oxygen led to the twitching behaviour observed in some crabs, and mortalities of a more widespread range of taxa is normally seen during anoxia. These facts, along with the continuation of crab deaths for some time after the HAB is likely to be present, led the panel to consider it unlikely that anoxia associated with a HAB caused the unusual crustacean mortality. ==== Chemical toxicity (including pyridine) from shore-based sources and sediment ==== Teesside has a history of industrial activity, including a range of activities that have generated toxic chemical substances. These include pyridine which is known to be toxic to crabs at concentrations of around 10 mg/litre. There is evidence of historical production of pyridine on Teesside associated with industries including chemical production and steelworks. The panel considered these industries, including their waste disposal and demolition, and concluded that they could not be sources of any significant volume of pyridine during the period of crustacean mortality. Measurements of seawater by the Environment Agency and by York University, including but not limited to those during the incident period, could not detect pyridine, which supports this conclusion. Previous modelling of the dispersion of pyridine from a potential Tees source was considered by the panel. This modelling is based on release of a very large volume of pyridine but, even with this release, pyridine concentrations remain significantly below the level required for crab mortality. In the absence of any significant source of pyridine, the panel concluded that it is very unlikely that a point source of pyridine in Teesside caused the unusual crustacean mortality. Sediment measurements of pyridine, combined with assessment of the character and volumes of dredged material, indicate that the maximum pyridine release from sediment during dredging is several orders of magnitude lower than required to lead to watercolumn concentrations sufficient for crab mortality. The panel concluded that it is very unlikely that pyridine release from sediments led to toxicity and mortality for crabs. A range of other toxic chemicals, including persistent organic pollutants, heavy metals, and tri-butyl-tin are found in sediments in the Tees and are the result of long-term industrial activity in the region. These pollutants are measured and reported as part of usual regulated activities such as dredging and disposal. Measurements in the Tees region and existing knowledge about dispersion and behaviour of these pollutants and their toxicity enabled the panel to conclude that is very unlikely that a toxic pollutant other than pyridine caused the unusual crustacean mortality. Widely used chemicals such as pharmaceuticals and pesticides can enter seawater through normal river flow or from waste-water treatment. Although there is evidence for association of initial mortality with a period of sewage discharge, a suite of chemical measurements in waters, and the absence of any reason to expect the north-east of England to have greater fluxes of these chemicals than other parts of the UK, led the panel to conclude that it is very unlikely that chemicals associated with run-off from shore caused the unusual crustacean mortality. ==== Dredging ==== In dynamic estuaries and coastal areas, many ports and harbours need to dredge to provide and maintain safe navigable depths. Capital dredging excavates geological or historically accumulated sediments to create a new or deeper channel or berth. Maintenance dredging removes recent infill material to provide safe operating conditions in the context of the original or ‘declared’ channel (or berth) depth. No capital dredging was undertaken in the Tees area in the period before or during the unusual mortality event. The last capital dredging before this period was in December 2020, and the new capital dredging at Teesworks did not commence until September 2022. The panel therefore considers it exceptionally unlikely that capital dredging on the Tees caused the unusual crustacean mortality seen in this region between these dates. A larger than normal dredger was operating in the channel offshore Teesside during late September and early October 2021. The vessel was dredging recently mobilised sandy material deposited in the channel by storm events. Although larger than normal volumes of sediment were mobilised, maximum possible release of toxic chemicals, including pyridine, is significantly too small to cause crab mortality. Other routine dredging was also underway in the Tees Estuary by the port’s dredgers. This was similar to activity conducted every month to keep the port operational and followed normal regulatory procedures. Considering all available evidence about Teesside dredging the panel considers it very unlikely that release of any toxic chemical, including pyridine, due to maintenance dredging could have caused the deaths. This conclusion is supported by the broad geographic spread and long duration of crustacean mortality. ==== Summary ==== Overall, the panel was unable to identify a clear and convincing single cause for the unusual crustacean mortality. The key observations that any cause must be capable of explaining are: * Mortality over a sustained period and along at least 70 km of coastline; * The unusual twitching observed by dying crabs in many locations * The dominant mortality of crustaceans rather than a wider range of species A novel pathogen is considered the most likely cause of mortality (despite the lack of direct evidence of such a pathogen), because it would explain these key observations. The impact of an algal bloom would also explain the wide distribution of observed deaths and cannot be ruled out as a causative factor particularly early in the incident. It is unlikely, however, that an agal bloom can explain the twitching nor the long duration of mortality particularly during winter months. The presence of a toxic substance could explain the twitching, but no source of sufficient amount of any toxic material could be identified, despite a range of relevant sediment and water measurements, and based on expert assessment of this and literature evidence. Although a range of chemicals, including pyridine, are known to be toxic to crustaceans, the wide geographical spread and long duration of the event would require sustained release of very large volumes of the chemical which is considered very unlikely from point sources or due to dredging as a cause for unusual crustacean death. It is also possible that several of the stressors considered in this report operated together to degrade the marine environment and lead to the unusual mortality. ===== 1 Introduction ===== On the 4 of October 2021 bait collectors reported dying crabs on shores of Bran Sands in the north-east of England. This was followed by more sightings of morbid or moribund crustaceans over the course of the following weeks along the north-east coast of England, extending from Spittal Beach in the north to Scarborough in the south. At the time of writing, there have been 3 periods with notable numbers of wash-ups of crustaceans (October to November 2021, April to June 2022, September to December 2022) with the first two episodes including incapacitated live crabs with unusual twitching behaviour. Initial investigations by Defra Group, for the events of October to November 2021, could not definitively identify a cause, but concluded that algal blooms may be of significance. The local fishing community commissioned a study by leading Northeast Universities, led by Dr Caldwell of Newcastle University, to look further into probable causes. This group concluded that chemically toxic levels of pyridine, released by dredging in the area, was the most likely cause of the mortality event. In October 2022, the Environment, Farming & Rural Affairs (EFRA) Select Committee heard evidence from various relevant groups and wrote to the Defra Secretary of State requesting that an independent review was commissioned into the causes of the unusual deaths. In response, the Defra Chief Scientific Adviser (CSA), Professor Gideon Henderson was asked to set up a panel of independent experts, with oversight from the Government CSA (GCSA) Professor Sir Patrick Vallance. The resulting panel - The Crustacean Mortality Expert Panel (CMEP) - was established with experts from academia and industry with a range of knowledge and experience spanning crustacean biology, marine eco-toxicology, sea-life histology/pathology, marine pollutants, algal blooms, chemical dispersion in the oceans, dredging and coastal processes, and sediment and water chemistry. The CMEP was tasked with providing an independent scientific assessment of all the possible causes of the mass crustacean mortality incident using all the relevant available data, including the two prevailing theories of algal blooms and pyridine toxicity from dredging. The CMEP’s remit did not extend to consideration of government processes during the investigation of the mortality event(s), food safety, nor the economic implications of the deaths. The panel grouped their consideration into four sections: * Disease pathology: That the deaths were caused by a disease or parasite. * Harmful algal bloom: Including algal toxins released by the bloom, and oxygen depletion associated with the bloom. * Chemical toxicity: From chemicals (including pyridine) released by industry at the shore or by unusual run-off from the shore. * Dredging: The specific release of a toxic chemical (including pyridine) as a result of disturbance and resuspension by dredging or disposal of the dredged sediment. The structure of this report reflects this division. The panel also considered the combination effects of multiple stressors. As part of the panel’s inquiries, they sought and considered data from diverse sources, including from the Environment Agency (EA), Marine Management Organisation (MMO), Centre for Environment, Fisheries and Aquaculture Science (Cefas), the Newcastle University led research group, the Port Authority and Defra. All data considered is cited or listed in the accompanying document. This report represents the consensus views of the CMEP. ===== 2 Timing, locations, and nature of deaths ===== Observations of the locations and dates of crustacean deaths were compiled by the Environment Agency, along with other relevant associated observations. These are summarised in Figures 1 to 5. This compilation of data on mortality observations is used in consideration of the likelihood of all possible causes of mortality. Key aspects of the data on mortality are: the broad geographical extent (at least 70 km); the initial duration of deaths from early October to early December 2021 and subsequent periods of mortality in 2022; the twitching observed in dead crabs along much of the coastline; and the dominance of crustacea relative to other species. {html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 1 - Map of crab wash-ups.jpg” alt=“Figure 1” width=“100%” />{/html} Fig 1: Location map for the coastline from which unusual crab wash ups were reported between October and November 2021, adapted from the Environment Agency’s incident investigation summary. Locations with washups shown in Figures 2 to 5. Key industrial facilities considered as possible point source pollution are marked with black dots, and the extent of dredging in the Tees and dredging disposal site are outlined in black. (22_1BH_NEIFCA wash up incidents and logs record October 2021 to September 2022; 23_1BH_Wash Up Reports September to December 2022). {html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 2 - Animal wash-ups - 2109-2212 - possible hazards.jpg” alt=“Figure 2” width=“100%” />{/html} Fig 2: Observed locations of animal wash-ups between September 2021 and December 2022, colour coded by other information about possible hazards. Data from Hazards are the terms used by the public or officers who reported the incidence. The location distance is from the River Tees (in bold). (22_1BH_NEIFCA wash up incidents and logs record October 2021 to September 2022; 23_1BH_Wash Up Reports September to December 2022). {html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 3 - Locations of wash-ups - 2109-2212 - status.jpg” alt=“Figure 3” width=“100%” />{/html} Fig 3: Observed locations of animal wash-ups between September 2021 and December 2022, colour coded by status of the animal, including (in yellow) crabs and lobsters exhibiting the unusual twitching behaviour. The location distance is from the River Tees (in bold). Data from (22_1BH_NEIFCA wash up incidents and logs record October 2021 to September 2022; 23_1BH_Wash Up Reports September to December 2022). {html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 4 - Species wash-ups - 2109-2212 - possible hazards.jpg” alt=“Figure 4” width=“100%” />{/html} Fig 4: Species wash-ups between September 2021 and December 2022, colour coded by other information about possible hazards. Data from Animals are the terms used in reports from the public and officers, as a result crustaceans, crabs, lobsters, and shellfish should not be seen as distinctly separate categories. Hazards are the terms used by the public or officers who reported the incidence. (22_1BH_NEIFCA wash up incidents and logs record October 2021 to September 2022; 23_1BH_Wash Up Reports September to December 2022). {html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 5 - Species wash-ups - 2109-2212 - status.jpg” alt=“Figure 5” width=“100%” />{/html} Fig 5: Species wash-ups between September 2021 and December 2022, colour coded by status of the animal, including (in yellow) crabs and lobsters exhibiting the unusual twitching behaviour. Animals are the terms used in reports from the public and officers, as a result crustaceans, crabs, lobsters, and shellfish should not be seen as distinctly separate categories. (22_1BH_NEIFCA wash up incidents and logs record October 2021 to September 2022; 23_1BH_Wash Up Reports September to December 2022). ===== 3 Disease Pathology ===== Consideration was given to the following questions: 1. can a disease cause mass mortality of crustaceans at a regional scale? 2. what was the approach taken by Cefas to look at disease as a causative agent? 3. what was the pathology of the crabs observed off Teesside, and how does this relate to the possible causes? 4. what is meant by ‘twitching’ among the impacted crabs? 5. what symptoms would the potential causal factors exhibit in decapod crustaceans? ==== 3.1 Can disease cause mass mortality on crustaceans on a regional scale? ==== There is considerable evidence in the literature that large scale die-offs of crabs and lobsters have been attributed to disease (Messick and Sindermann, 1992; Mullen et al., 2004; Stentiford and Shields, 2005; Wang, 2011). For example, Mullen et al. (2004) reported that an estimated 11 million lobsters died off the coast of Long Island Sound (USA) in 1999. Initially their investigations looked into dredging, chemical contaminants, and disease. No significant amounts of trace elements, polycyclic aromatic hydrocarbons, polychlorinated biphenyl congeners, or pesticides were observed in lobster tissues and the study failed to isolate any bacteria from the hemolymph and hepatopancreas (Mullen et al., 2004). What the study did observe was considerable infection from a protozoan parasite throughout the nervous tissues of impacted lobsters, leading the authors to conclude that this parasite was the primary cause of mass mortality in 1999. These have been known to cause mortality events in other sea life including crabs and sea urchins (Newman and Ward, 1973; Jones and Scheibling, 1985; Bower et al., 1994; Bateman et al, 2022). Edible crabs and lobsters have been in decline along the south-east coast of England for the past 5 years (Sussex IFCA, 2021). The Manhood Peninsula Partnership, a regional collaborative, has initiated a project on Crustaceans, Habitat and Sediment Movement (Link to CHASM ). One particular line of inquiry for the CHASM project has been sedimentation following dredging in the local area, in particular capital dredging of 3 million m3 around Portsmouth Harbour in 2016 to allow access for new aircraft carriers. For example, Lobster landings have shown an annual decline (41 tonnes in 2017, 32 tonnes in 2018, 19 tonnes in 2019, 11 tonnes in 2020 to 8 tonnes in 2021) and edible crab landings have shown a similar trend (179 tonnes in 2018, 158 tonnes in 2019, 66 tonnes in 2020 to 48 tonnes in 2021). However, summary reports from several inshore fisheries and conservation authority (IFCA) regions (Devon, Cornwall, Southern, Northumberland) have seen declines in edible crab landings since 2017, even without the presence of dredging, indicating something more widespread might be occurring. Following the declines off the Sussex coast, Cefas investigated disease as a possible causal factor. The results, published in Bateman et al. (2022), report the finding of an amoebic crustacean disease (ACD) in edible crabs (Cancer pagurus) for the first time in UK waters, which belong to a similar group of parasites reported to have caused the lobster mortalities in the USA (Mullen et al., 2004). They go onto report “Data from previous edible crab health surveys conducted at Cefas between 2002 and 2021 (Stentiford et al., 2002, 2003, 2007, Bateman & Stentiford 2008, Feist et al., 2009, Bateman et al., 2011, 2016, Hartikainen et al., 2014) were re-evaluated to determine whether pathologies like those described here were present. A total of 620 edible crabs sampled directly from fisheries in the English Channel and 2860 juvenile edible crabs collected from the shoreline at 4 separate sites around the coast of England and Wales were examined over this period. None of these samples reported histological evidence of a paramoebid infection or associated pathologies consistent with paramoebiasis within the tissues”. Bateman et al. (2022) were able to conclude that the more recent finding of an ACD represents a novel parasite to the UK and suggest that further studies are required to investigate the potential role of ACD as a mortality driver in commercially exploited populations of C. pagurus in European waters. In a follow up email in response to a question from CMEP (20 December 2022) Cefas highlighted “that this emerging disease was unlikely to be responsible for the declines in the south coast crabs and it was not observed in the samples obtained in the north-east of England” (CEFAS, pers. comm., 20 December 2022). CMEP considered the possibility of an unidentified novel crustacean disease in the UK. They found research reporting on a number of viral and parasitic diseases that may not have been screened for by Cefas in the crab and lobster samples, for example viruses (Bateman and Stentiford, 2017; Zhao et al., 2021). These diseases include reoviruses which are known to infect a broad range of crustaceans (see review by Bateman and Stentiford, 2017) and which have sometimes been reported as causing similar symptoms to the crustaceans impacted by this event. For example, Johnson & Bodammer (1975) found that a Reo- like virus was responsible for mortality among Blue crab populations with a pathology associated with tremors and mortality within 3 days, at Chincoteague Bay, Virginia, USA. Zhao et al., 2021 report that the typical signs caused by reovirus infections in brachyuran crustaceans are “lethargy, anorexia, trembling and paralysis at late phases of the infection”. In their review they go on to outline that experimental infection can result in rapid and high mortality (Zhao et al., 2021). Wang and Gu (2002) reported that Chinese mitten crabs infected with a Rickettsia-like organism were “typically lethargic with loss of appetite and paroxysmal tremors of the pereiopod, hence the term ‘tremor disease’ given by the local fishermen. Infected crabs exhibited signs of weakness, anorexia, paroxysmal intense tremors and death in succession”. Therefore, the pathology of crabs associated with disease can be similar to the ‘twitching’ observed in the northeast of England. Knowledge of these viruses in UK crustacean populations is currently limited and hampered by limited molecular information on crabs (Bateman and Stentiford, 2017). Furthermore, many viruses are not found in isolation and act synergistically (Bateman and Stentiford, 2017). It is possible that there is a novel disease agent in the UK, similar to those thought to have caused the ‘uncontrolled convulsive twitching’ seen in the north-east mortality event. To further assess this possibility more information was sought from Cefas about the methods used in their disease screening and to specifically ask Cefas if they could be confident in ruling out novel disease agents to the UK through their standard histopathology disease screens. This is discussed in Section 3.2. Cefas confirmed that some pathogens would have been harder to see when samples were not screened from fresh or well preserved specimens. Therefore, Cefas highlighted that “it is possible there could be a novel pathogen not identified as yet and it is not likely that we can definitively eliminate the involvement of a potential novel pathogen”. Summary: There is a possibility of a novel pathogen causing declines in crustaceans in UK waters. ==== 3.2 What was the approach taken by Cefas ==== Cefas undertook histological and molecular analysis of a number of crab and lobster samples following the mass mortality event which included: Between 19 October and 24 November 2021 a total of 33 edible crab (Cancer pagurus), 11 native lobster (Homarus gammarus), and 5 shore crab (Carcinus maenas), a couple of Velvet swimming crabs (Necora puber; number unconfirmed), were also assessed for disease agents. Note that, when Cefas reports on molecular screening of known listed diseases, this refers only to White Spot Syndrome Virus (WSSV), because this is the only listed native crustacean disease they are statutorily obliged to screen (link to legislation ). Further analysis was conducted histologically. Table 2: Summary of Histological and molecular analysis of crab and lobster samples between 19 October and 24 November 2021 | Date | Species (number, location and presentation) | Test | Results | | 19 October 2021 | * Brown crab (7, Redcar) * Native lobsters (2, Bran Sands) * Shore crabs (5, Bran Sandsand Seaton) | Molecular screening WSSV | Negative | | 21 October 2021 | Brown crabs (16, merchant in Hartlepool) | Screened for known listed disease (WSSV) by molecular PCR techniques, and full disease screen for bacteria and histological analysis (all internal organs screened for disease including heart, gill, hepatopancreas, muscle, gonad, new shell). | Negative for WSSV, some bacteria present (Vibrio spp. and Marimonas aquiplantarum) but no pathology was observed in association with the bacteria. Histopathology reported no disease agent. | | 11 November 2021 | Lobsters (9) and histopathology edible crabs (8) (3 miles east of Redcar. Two of the lobsters were displaying lethargy/nonrighting behaviour and twitching) | PCR for WSSV, histopathology | All samples negative for WSSV. The 2 lobsters showing clinical symptoms were negative for any disease agent through histopathology. Presence of Hematodinium in 1 brown crab and 3 others infected with Paramikrocytos canceri. This pathogen is not considered consistent with the mortality event, nor was the pathogen detected in lobster (which were displaying clinical signs) | | 24 November 2021 | * Crabs (6, shore, edible and velvets; Runswick Bay; found moribund). * Edible crab (2, caught off Whitby (within 3 nautical miles); lethargic and dying) | PCR for WSSV Histopathology | All samples negative for WSSV, Low levels of Hematodinium sp. and Digenean, 1 brown crab showed low levels of Paramikrocytos canceri in the antennal gland | Cefas concluded that there was no evidence from the samples that there was an infectious disease agent responsible for the mortalities observed and they therefore did not believe that an aquatic animal disease was the likely cause of this event (from Ref: EW033-I-756 PM 41921, 41844, 42035, 42123). In response to a query from CMEP (email 22 December 16:47) on the extent of the molecular screens Cefas wrote “The initial disease screens covered only a small number of diseases. We have looked at histology for the amoebic disease but this only works well on freshly killed animals as the tissue degraded quickly after death”. It appears that samples they received were degraded making detection of some pathogens difficult histologically. It would therefore be useful for archived samples to be retrospectively screened for a broader range of potential pathogens, and to collect appropriate samples in the future to be able to screen for all potential pathogens. ==== 3.3 What was the pathology of the crabs observed off Teesside, and how does this relate to the possible causes? ==== Initial site reports from the Environment Agency (8 October 2021) highlight that officers reported 100s of crabs which were dead or in the process of dying and that they were “exhibiting a strange lethargic twitching behavior – either on their backs or on their fronts but not able to move in any controlled manner”. They go on to report that “this was true of crabs both submerged under the water and exposed/washed up at low tide. Dead lobsters washed up were also observed”. There was no other signs of pollution (smell, change in water colour or debris). All other marine organisms were seen still alive including mussels, lug worms, tube worms, periwinkles, barnacles and fish, it only seemed to be Crustacea affected.” (11_1BH_Crab investigation 8.10.2021.pdf). The EA incident investigation summary highlights that “only crabs (green shore, velvet swimming, edible, porcelain), and lobsters were observed as impacted (range of ages classes). On both shore visits crabs were either dead, or on their backs twitching/ very lethargic with no fight left in them.” (02_7EA_EA_Incident_Investigation_summary_Oct_Dec.doc). These observations are supported by videos which the panel has seen and verify claims of crabs twitching on their backs. The EA Stakeholder briefing document states: “Reports of other animals, including octopus, limpets and shrimp found dead in the area appear to be unconnected and are more likely to be a result of storms and bad weather in the area.” (03_7EA_Crab_deaths_Feb_stakeholder_update_final.doc). Furthermore, an Aquatic Environments consultancy report to the EA highlights “Having visited the six shores on the north-east coast of England in quick succession on the 20 and 21 January 2022, following the mortality event that occurred in the autumn of 2021, it appears that there has been a significant impact on the ‘true crab’ intertidal populations. No shore crabs or swimming crabs were recorded within the known zone of the event, whilst healthy populations were seen outside the area. Shore hermit crabs and possibly squat lobsters appear to have been less affected by the event, as their populations appear to be recovering and they were found (sometimes in good numbers) on the shores in the south of the area. From the limited observations made on these single post-event visits, it appears that the rest of the ‘rocky shore’ ecosystem has survived intact” (01_1BH_Aquatic Environments decapod mortality results.pdf). === 3.3.1 What is meant by ‘twitching’ among the impacted crabs? === The CMEP considered the ‘twitching’ reported among the washed up crabs as critical to ruling in or out various causal factors. Videos of this behavior show a variety of crabs in various habitats, including offshore trawl collected and shore collected specimens. The majority of the videos show moribund crabs either in low water or in buckets having been trawled, and it was difficult to assess the specimens. However, there were a few videos which stood out to the panel as providing good examples of what is likely meant by the observers using the term ‘twitching’. We refer to this hereafter as ‘uncontrolled convulsive twitching’ It should be noted that in some published literature this response is referred to as “paroxysmal intense tremors” (Wang and Gu, 2002). This behaviour is best indicated by the video log: GAWV0487.MP4 (Folder 03_21_1_BH_8th Oct 21). This shows a swimming crab in a small rockpool exhibiting ‘uncontrolled convulsive twitching’, with its legs moving in an uncontrolled manner, not seen in healthy specimens (see also IORV0148 – as above). Similar examples can also be seen in the ‘Vessel Surveys’ folder (07_22_1BH_Trawl videos 14_18.11.21; IMG_3230; IMG_3231 and 3232) showing the harbour swimming crab (Liocarcinus depurator) exhibiting uncontrolled convulsive twitching of swimming limbs. These should be compared with normal swimming crab behaviour, seen at the control site at Robin Hoods Bay (video IMG_3183). Further videos of uncontrolled convulsive twitching can be seen in the following folder: 05_22_1BH_Trawl images 18_19.01.22 (Off Seaton Carew All Crabs Video; 5. Skinningrove Wick L. holsatus Video 2 (also 1 x C. cassivelaunus); 7. Sea Off Saltburn All Crabs Video 1). Some of the other videos could be construed as ‘normal’ moribund/dying behavior. This can be seen in some videos of crabs lying on their backs exhibiting very little movement apart from the occasional twitch of a leg (for example video IMG_1476 in Folder 03_21_1_BH_8th October 21). The panel thought that these were inconclusive as there was no way to determine how long the crabs had been impacted, and could represent specimens that had previously been more actively ‘twitching’, but were now more advanced in pathology. In summary: There were definite signs of uncontrolled convulsive twitching in some of the video evidence. This presents differently to normal moribund or dying behaviour of crabs. ==== 3.4 What symptoms would the potential causal factors exhibit in decapod crustaceans? ==== === 3.4.1 Disease various - amoebic crab disease (ACD) specifically === Crabs and lobsters were observed moribund, limp and twitching which has been associated with some diseases (Newman and Ward, 1973; Jones and Scheibling, 1985; Bower et al., 1994; Mullen et al., 2004; Bateman et al., 2022). For example, Mullen et al., 2004 reported lobsters were “limp” which was interpreted clinically as paretic and flaccidly paralysed. Crabs/lobsters observed off Selsey were observed to be moribund and dead within pots (Bateman et al., 2022), but not twitching; however Cefas felt that the clinical similarities between those in the north-east of England were worth investigating for ACD. Cefas did not find any signs of the J. feistie (ACD) parasite, and felt that this emerging parasite had not caused the mass mortalities in the south to their knowledge, even though the clinical picture was similar. Twitching or tremors have been reported to be a symptom of several pathogens worldwide including reo or reo-like viruses, spiroplasma bacteria and amoebic crustacean disease (Johnson and Bodammer, 1975; Zhang et al., 2004; Wang, 2011; Zhang and Bonami, 2012). The CMEP considered that the symptoms described in the north-east of England, including autotomy and twitching (referred to as tremors in some literature), are consistent with a variety of diseases in crustaceans. === 3.4.2 Toxic pollutants various === The ‘uncontrolled convulsive twitching’ and autotomy evident from video footage (see Section 3.3) of the stranded crustaceans seem similar to the neurotoxic effects of some pesticide exposures. These are referred to in the ecotoxicology literature as ‘spasms’ or ‘spasming’. Schroeder-Spain et al., (2018) reported that blue crabs (Callinectes sapidus) exposed to two pesticides (Malathion and Carbaryl) had “Muscle spasms and uncontrolled limb movements in both pesticide treatments” resulting in an inability to right themselves and mortality at higher concentrations. Similar behavioural observations have been observed for blue crab exposed to pyrethroid pesticides (resmethrin; Schroeder-Spain and Smee, 2019) and neotropical crabs (Poppiana dentata) exposed to organophosphate insecticides (Singh et al., 2022). Twitching can also be induced by exposure to naturally occurring toxins in the mucus of nemertean-worms. Injection of mucus-derived peptides from the worm Lineus longissimus into Carcinus maenas results in rapid onset of involuntary tremors of the limbs, followed by hypertonus and paralysis via their action on voltage-gated sodium channels in the crab nervous system (Jacobssen et al., 2018). It is not suggested that nemertean toxins are the cause of the mass mortality in the north-east of England, but we draw on this published description of the neurotoxic effects of a marine toxin as a comparison to the ‘uncontrolled convulsive twitching’ pathology which was observed during the event. Further studies have demonstrated that injection from a wide variety of compounds such as monoamine neurotransmitters can induce tremors/twitching (Huddart and Batram 1984; Wood et al.,1995; Quesada et al., 2011). === 3.4.3 Algal bloom toxins === Naturally occurring algal toxins from harmful algal blooms (HABs) were measured and detailed in the reports (Testing of crustacean tissue samples report, June 2022). To the panel’s knowledge these agents have not been shown to induce the observed pathologies in invertebrates. A number of studies have indicated that crustaceans are immune to Paralytic and Diarrhetic Shellfish Poisoning toxins (PSPs and DSPs). For example, larvae of the American lobster (Homarus americanus) appear immune to PSP toxins (gonyautoxin II, -III and -IV, neosaxitoxin and saxitoxin) (Robineau et al., 1991), whilst adult lobsters fed with PSP toxins from the dinoflagellate Gonyaulax tamarensis (now Alexandrium catenella) were unaffected (Yentsch and Balch, 1975). Dungeness crabs (Cancer magister) can accumulate high levels of domoic acid (2.85 mg) over several weeks with no ill-effects reported (Lund et al., 1997). Lipophilic toxins, Azaspiracids, were elevated in some of the samples taken (up to 50 𝜇𝜇g/kg AZA1, Table 3, Testing of crustacean tissue samples report, June 2022), but have also been reported in Cancer pagurus tissues at 733 𝜇𝜇g/kg in Norway (Torgersen et al., 2008). No adverse effects to the crabs were reported in this Norwegian study. Okadaic acid (DSP) has also been found in Cancer pagurus tissues in Norway at 290 𝜇𝜇g/kg (Torgersen et al., 2005). None of the above studies mentions recorded pathology or mortality in the crustacean species investigated. Therefore, given that the concentrations of HAB toxins in the crustacean samples were not high, and that crustaceans are known to accumulate such toxins to much higher concentrations without the observed pathology, the panel thought HAB toxins as unlikely as a causal factor. === 3.4.4 Hypoxia === Under hypoxic conditions we would expect crustaceans to exhibit avoidance behaviour (Haselmair et al., 2010; Diaz & Rosenberg, 1995), eventually becoming more lethargic and moribund (if escape is not possible) as the health declines prior to death (Haselmair et al., 2010; Diaz & Rosenberg, 1995). Despite searching for reference to this behaviour specifically, the panel did not find any published evidence for ‘uncontrolled convulsive twitching’ in decapod crustaceans under hypoxic conditions. Uncontrolled convulsive twitching is not expected under hypoxic conditions. === 3.4.5 Conclusions === The twitching observed is consistent with a variety of diseases in crustaceans, or with a toxic agent. Algal bloom toxins and hypoxia are unlikely causative agents for the twitching observed. ==== 3.5 Does the fact that only crustaceans were impacted point to a causal factor? ==== This event only appeared to have effects on larger decapod crustaceans (including edible crabs, lobsters, common shore crabs and velvet swimming crabs, but not hermit crabs) (see Section 3.2: reports including: 02_7EA_EA_Incident_Investigation_summary_Oct_Dec.doc; 03_7EA_Crab_deaths_Feb_stakeholder_update_final.doc; 11_1BH_Crab investigation 8.10.2021.pdf). The panel, however, thought it was noteworthy that relatively large numbers of curled octopus (Eledone cirrosa) were observed washed up dead on the shore at similar locations, and approximately 1 month after the crabs. It was reported to IFCA on the 29th November 2021 by a number of the public that 100’s of octopus were washed up dead on Runswick Bay. An IFCA officer attended on the 1st December 2021 and spoke to dog walkers who also reported 100’s of dead octopus. The officer could not confirm if the numbers were in the hundreds, due to the rising tide cutting off parts of the beach, but did mention there were lots. On the 1 December a Facebook post, which included photos, reported a dozen dead octopus were washed up on Blast Beach and Hawthorn Beach (Seaham). In addition, on the 3 December 2021 IFCA officers received email reports of 30 to 40 dead octopus washed up on Hartlepool headland by a member of the public with some photo evidence. Also on the 3 December NE-IFCA logs an observation from Facebook that Littlehaven Beach (South Shields) “was littered with dead octopus”. CMEP felt that finding one or two washed up dead octopus might not be considered too unusual but 100’s, if correct, is unusual. The Environment Agency (EA) considered a number of theories to why this may have occurred from a natural die-off combined with a storm (as their lifespan is 2 years) and IFCA mentioned that Runswick Bay is the main habitat for octopus, to consideration of starvation given their main diet (crabs) had died. The counter argument is that food could well have been plentiful as it was dead and littering the seabed. It is also possible that octopus may have died from eating contaminated crabs, or died of the same things as the crabs. The CMEP also identified one study into high octopus mortality following storm discharges in Portugal which were attributed to urban runoff and found high levels of lead within tissues (Raimundo et al., 2017). The CMEP supports the EA conclusion that deaths of other species reported anecdotally (for example razor clams, seals, birds) are more likely to be natural storm wash ups or other naturally expected events. However, the large mortalities of a major food resource might have a knock-on effect through the food chain, so some deaths could be attributed as a secondary effect. ==== 3.6 Conclusions from pathological evidence, based on the available evidence ==== Based on the knowledge that a variety of crustacean diseases can induce a pathology similar to that observed off the north-east coast of England (particularly the uncontrolled convulsive twitching), and without further disease screening, the panel concluded that disease was about as likely as not (33 to 66% probability) to be the cause of the mass mortalities reported in the north-east of England. The panel agreed that this would move to either very unlikely (<10% probability) if results of molecular screening were confirmed as negative; or very likely (>10% probability) if a broad diagnostic screen of these potential pathogens proved positive.

Based on the available evidence, the CMEP came to the conclusion that the pathology seen in the dying organisms (‘uncontrolled convulsive twitching’) would also be consistent with a natural or anthropogenic stressor of the neural system. It was thought that this would be a likely cause of the observed pathology in the north-east of England if a source of such a neural stressor, for example, toxins, was present at sufficient levels.

4 Harmful Algal Blooms

4.1 Background

The marine phytoplankton community of coastal waters contain a relatively small number of genera and species that can under certain conditions cause harm to humans, our use of the marine ecosystem or other marine organisms. These harmful taxa are typically present at low background concentrations, but periodically increase in abundance to form harmful algal blooms (HABs). In UK waters most HABs are thought to occur naturally, promoted by a set of environmental conditions favourable to their development. However, anthropogenic factors can also promote blooms in certain circumstances.

A number of genera, principally the dinoflagellates Alexandrium, Dinophysis and the diatom Pseudo-nitzschia can produce a range of “shellfish toxins” that when accumulated within shellfish flesh make these shellfish harmful for human or other animal consumption. Most frequently toxicity events related to these species are associated with farmed shellfish (at which the bulk of monitoring is undertaken), but examples of wild crustacean mortality do exist (for example, Turner et al., 2018).

Mortalities of benthic organisms including crabs related to HABs have been reported in

Ireland and the UK since the 1970s (Bresnan et al., 2021). The majority of these events have been related to the dinoflagellate Karenia mikimotoi. The ecology and harmful properties of K. mikimotoi have been reviewed by Brand et al. (2012) and Li et al. (2019). Karenia mikimotoi can reach very high densities in the water column and senescence of the bloom can result in it sinking to the bottom and killing benthic organisms through resulting anoxia from smothering or bacterial degradation of the organic material. The toxicity of K. mikimotoi is complex but the species is thought to produce haemolytic and cytotoxic, compounds and generates reactive oxygen species. There is evidence to suggest that both mechanisms may result in mortalities during blooms potentially depending on the hydrography of the location (O’Boyle et al., 2016). It should be noted that the temperature tolerance and toxicity of K. mikimotoi is different to that of brevetoxin producing Karenia brevis that is not found in UK or European waters, but typically in warmer waters such as the Gulf of Mexico. In both contexts (anoxia, toxin production) a wide variety of benthic biota are typically impacted by K. mikimotoi and mortalities recorded are comprised of multiple species groups ranging from lug worms, star fish, sea urchins, crabs, lobsters to fish and more. Mass mortalities relating to K. miktmotoi typically require significantly elevated cell densities in the range of hundreds of thousands or millions of cells per litre (cells L-1) (see Table 1 of Li et al., 2009).

The panel considered the potential of the mortality event of 2021 in the context of a number of headings. These were:

1. What is the historic precedence for Karenia mikimotoi blooms and HAB related mortality events in region?

2. Was there an algal bloom in the waters along the north-east of England during September/October 2021?

3. Were the patterns of mortalities consistent with a HAB event?

4.2.1 //Karenia mikimotoi// and mortality events in UK and Irish waters

Historical incidents, in the UK and elsewhere are summarised by Li et al. (2019). There are a number of recent recorded incidents of K. mikimotoi blooms resulting in significant benthic mortalities in the waters surrounding the UK and Ireland. Silke et al. (2005) report of a large bloom of Karenia mikimotoi in Ireland in 2005. The bloom reached nears 4 x 106 cells L-1 and resulted in the mortality of a wide range of benthic species including crabs (Carcinus maenus, Portunus sp) as well as fish, star fish, lug worms and other benthic biota. This report noted that the only animals that seemed to be “hanging on” in the most impacted areas were the Common Hermit Crabs, Pagurus bernhardus, and the Organpipe Worm, Serpula vermicularis. The following year an extensive bloom of K. mikimotoi in Scottish waters resulted in benthic mortalities including annelids, molluscs and some species of fish (Davidson et al., 2009). Baptie and Swan (2017) report the mortality of “great variety” of organisms, including lugworms, urchins and crabs again from a K. mikimotoi bloom of approximately 3.5 x 107 cells L-1. Data from the Marine Scotland Scottish Coastal Observatory (SCObs) shows that cell densities of K. mikimotoi can exceed values of 1×10 6 cells L-1 at water temperatures ranging from 11.84 to 14.56 oC.

Karenia mikimotoi monitoring is limited in the north-east of England, but data from the Scottish regulatory biotoxin producing phytoplankton monitoring programme indicates that abundance of K. mikimotoi in the month of September have exceeded 100,000 cells L-1 in eight years since 2006. Elevated cell densities are therefore not unusual in September and in one year (2006) these elevated cell densities continued into October. Weekly phytoplankton monitoring by the SCObs shows with the exception of one record (3,500 cells L-1) reported values in November and December are very low (<600 cells L-1).

4.2.2 HAB mortality events in the north-east of England

While K. mikimotoi has been recorded in the north-east of England, to date there have been no records of mortalities of marine benthic biota as a result of a high biomass or Karenia mikimotoi bloom in the region. However, records of mortality events of marine organisms related to HABs in the north-east of England while rare, do exist. Reports in the literature come from the mortality of seabirds, particularly Shags (Phalacrocorax aristotelis) during June 1968 associated with the consumption of mussels contaminated with Paralytic Shellfish Toxins (PSTs) by the dinoflagellate Gonyaulax tamarensis (now Alexandrium catenella), an atypical event also associated with human illness (Coulson et al, 1968, Joint et al., 1997). There are also reports of Diarrhetic Shellfish Toxins (DSTs) in the livers of dead seabirds from the late 1990s in the IOC-ICES-PICES Harmful Algal Event Database (HAEDAT) although it is unknown if these toxins were the cause of death of these birds.

4.2.3 Shellfish toxin producing species in north-east of England

Regulatory monitoring of shellfish biotoxins and associated harmful phytoplankton for the

Retained EU Regulation 2017/625 occurs in England and Wales but at relatively low spatial and temporal frequency, overseen by the Food Standards Agency (FSA). The monitoring site in the north-east of England is at Holy Island. Data on K. mikimotoi cell concentration is not reported as part of that monitoring programme. No biotoxins were found above the limit of detection at this site during 2021.

4.3 Was there an algal bloom in the waters along the north-east of England during September to October 2021?

4.3.1 //Karenia mikimotoi// during September to October 2021

During 2021, high abundances >1 x 106 cells L-1 of Karenia mikimotoi were recorded in and offshore from Orkney throughout August and >500,000 cells L-1 in Shetland and

Moray Firth during late September. Anstruther in Fife reported a cell density of 5,760 cells L-1 on 6 September. Three EA monitoring sites in the north-east of England (Bamburg Castle, Northumberland and Beadnell Bay, The Bush) reported abundances of 306,033 cells L-1 (3 September), 358,309 cells L-1 (3 September) and 272,271 cells L-1 (4 September) respectively. While these data demonstrate that elevated K. mikimotoi were densities occurred on the east coast of the UK a month prior to the mortality event there is no phytoplankton cell count data immediately before or during the first week in October. Phytoplankton monitoring did not extend into October in the region, but phytoplankton cell densities typically decrease through October reaching low background values in November and the winter months (as was evident in the Scottish biotoxin producing phytoplankton monitoring that did continue during that part of 2021). It is therefore unlikely that a K. mikimotoi event would be responsible for the observed mortalities in late October or subsequently.

4.3.2 High biomass algal blooms

Chlorophyll concentrations are an indication of elevated phytoplankton biomass. High biomass might be expected to cause harm through deoxygenation when the bloom dies and sinks to the benthos, no matter the phytoplankton species involved. During the first week in September 2021, the EA directly measured (following acetone extraction) chlorophyll concentrations at a number of sites ranging from Bamburg Castle (8.4 µg L-1), Northumberland and Beadnell Bay (10.0 µg L-1), The Bush (2.0 µg L-1). Chlorophyll values >10 µg L-1 were also recorded at a number of sites earlier in the year between March and June 2021 but are not associated with this event.

{html}<img src=“./DEFRA/2301CEMP/Images/cemp-Figure 6 - Satellite image showing composite chlorophyll - wk 20-26 2109.jpg” alt=“Figure 6” width=“100%” />{/html}

Fig 6: Satellite Image showing composite chlorophyll values during week 20 to 26 September 2021.

These measurements are consistent with satellite derived (EMEMS Ocean Colour) data that showed patches of very high chlorophyll concentration from the 20 to 26 September (>30 mg m-3). These data (Figure 6) also demonstrate distinct offshore patches of chlorophyll (and hence algal blooms) that are very much dense enough to cause mortality should they relate to a K. mikimotoi (or potentially other phytoplankton) bloom that subsequently sank to the benthos. However, it must be noted that satellite derived chlorophyll estimates are less reliable in shallow, coastal waters such as these than offshore due to factors such as sediment resuspension. There is also no dissolved oxygen (DO) data from bottom waters in the region to support or counteract anoxia as a cause.

Plymouth Marine Laboratory applied a Karenia risk classifier to the area using satellite data from the NERC Earth Observation Date Acquisition and Analysis Service (NEODAAS) and processed following the methods outlined in Kurekin et al. (2014). This analysis identified the significant possibility that there was no bloom of Karenia present. High chlorophyll values detected could have been due to blooms of another phytoplankton species or suspended sediment. The limited phytoplankton monitoring prior to the mortalities being washed ashore mean there is insufficient information about the composition of the phytoplankton community during the period that high biomass was detected by satellite to ground truth the composition of this bloom.

4.3.3 Shellfish biotoxin blooms in the north-east of England

Data from the “Biotoxin and Phytoplankton official control monitoring programmes for England and Wales” operated by Cefas during 2021 (Coates et al., 2022) showed that Paralytic Shellfish Toxins, Lipophilic Shellfish Toxins (including Diarrhetic Shellfish Toxins) and Amnesic Shellfish Toxins were not detected above the limit of detection (LOD) in shellfish from the north-east of England. This monitoring programme employs “Trigger levels” of causative phytoplankton which are finite but relatively low abundances set to act as a potential early warning of harmful bloom development and possible subsequent toxin accumulation in shellfish. The associated causative organisms Alexandrium (PSTs), Dinophysis (DSTs) and Pseudo-nitzschia (ASTs) were not recorded above these “Trigger levels” during 2021. The benthic dinoflagellate Gonyaulax tamarensis, a DST producer is the only species recorded above its “Trigger level” of 100 cells L-1, but no DSTs above the LOD were recorded in shellfish at this site during the year.

4.4 Were the patterns of mortalities consistent with a HAB event?

4.4.1 //Karenia mikimotoi// or other high biomass bloom

Previous harmful Karenia mikimotoi and high biomass blooms have resulted in benthic mortalities that were broad and wide ranging (Silke et al., 2005, Davidson et al., 2009, Baptie and Swan 2017). The majority of reports are of mortalities in this event are of crabs and lobsters only. For example, a site visit to Bran Sands on 8 October by two EA officers reports 100s of dead crabs and many which were dying showing a lethargic twitching behaviour. Dead lobsters were also observed to be washed up. “All other marine organisms were seen still alive including mussels, lug worms, tube worms, periwinkles, barnacles and fish, it only seemed to be Crustacea affected”. Records of wash up and “twitching” behaviour observed in crabs and lobsters extend into mid/late November 2021. While the high algal biomass recorded by satellite at the end of September may have had an impact at the start of the event, given the storm in the area at the beginning of October 2021 and the expected die-off of phytoplankton at that time of year it is unlikely that an algal bloom caused an anoxia event that lasted for full duration of recorded mortalities.

These observations are a counter indicator to the event being related to an algal bloom either as (a) a K. mikimotoi bloom resulting in a toxic event or (b) K. mikimotoi or another high density algal bloom causing anoxia, as the negative effects of both of these bloom events are thought to be mostly indiscriminate rather than species specific (for example Silke et al., 2005). The weather and time of year suggest the sustained development of a high biomass algal bloom is unlikely.

We note that there is evidence that crustaceans are more susceptible to anoxic conditions than many other benthic organisms (Sunyer and Duarte 2008) (and see Section 4.4.2). This might help to explain the selective mortality. However, while there is published evidence of harmful blooms impacting crab larvae (for example Gravinese et al., 2019), we are unaware of any previous records of selective adult crustacean mortality resulting from a harmful algal bloom.

4.4.2 Are decapod crustaceans (crabs and lobsters) more sensitive to hypoxia events?

A review of the published literature was undertaken to assess what is known about decapod sensitivities to hypoxia (Tables 3, 4 and associated references). A recent reviewarticle (Vaquer-Sunyer and Duarte, 2008), indicates that decapod crustaceans are more sensitive than many other benthic marine invertebrates to reduced oxygen environments. It has also been reported that susceptibility to hypoxia/anoxia is heightened in the presence of hydrogen sulphide (Haselmair et al., 2010), which is often elevated in anoxic aquatic conditions. Hydrogen sulphide levels were not measured in the current investigation.

Noteworthy were several reports of ‘toxic/chemical’ smells within the NE-IFCA logs (8 and 25 October 2021; South Gare, Saltburn, Marske) from IFCA and EA officers plus the public and fishing community whereby efforts were made to differentiate these from rotting smells of the dead/dying material. These observations of toxic smells also included several reports of sewage related smells both onshore and offshore from fishers and picked up from IFCA officers through photos of sanitary products on the shoreline.

It is important to note that the affected taxa are benthic organisms and therefore measurements of dissolved oxygen (DO) at the seabed are critical to determining whether there was a deoxygenation event at the time. Sea surface or midwater oxygen levels will not necessarily be informative of what is occurring at the seabed.

The EA measured oxygen levels at the time of the event from surface water buoys were all high (95 to 100% DO; Link to Tees incident water data ). However, this does not provide evidence that there was no reduction of oxygen at the seabed at the time of the event. The EA did record at depth during vessel surveys (EA Vessel survey 15 to 17 November 2021) and also recorded high O2 readings (95% plus DO at approximately 10 m depth) although these were measured some time after the initial event.

As noted in Section 4.4.2 the onset of hypoxia in decapod crustaceans is unlikely to result in the ‘uncontrolled convulsive twitching’ as was seen in this event.

Table 3: Limits of hypoxia on decapod species relevant to the present case.

|hl Species |hl O2 (mgO2/L) |hl Measure of hypoxia |hl Reference |

| Cancer pagurus (European edible crab) | 3.65* | Critical oxygen tension (PcO2, 60 to 80 Torr at 10°C) | Bradford and Taylor, 1992 | | Liocarcinus depurator (Harbour swimming crab) | 2.43* | Critical oxygen tension (PcO2, 15 to 45 Torr at 14°C) | Gale , 1986 |

| Carcinus maenas (Common shore crab) | 1.43 | Sublethal threshold | Hill et al., 1991 |

| Homarus gammarus (European Lobster) | 0.7 to 1.33 | Tolerated with no adverse effects | Rosenberg et al., 1991 |