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Impacts of climate change on human health, HABs and bathing waters, relevant to the coastal and marine environment around the UK

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EXECUTIVE SUMMARY • Human health can be affected by toxin-producing phytoplankton, pathogenic Vibrio species (bacteria) and noroviruses (NoV) in UK waters. • The influence of climate change on toxin-producing phytoplankton is complex. This can be difficult to distinguish from shorter-term weather events and larger-scale circulatory processes. Confidence in current long-term prediction for harmful algal bloom (HAB) species is low. Data characterising the response of different HAB species to a broad range of environmental parameters are needed to improve short term (one to two week) forecasts and longer-term predictive models. • During the 2018 heatwave experienced in the UK (June-July), record water temperatures coinciding with elevated levels of pathogenic Vibrio species were identified from several sites along the southwest coast of the UK. • Climate change will modify the geographical distribution and seasonality of NoV. However, it is difficult to predict the effects of these changes on disease risk because NoV infectivity is determined by a complex set of factors, including host availability and susceptibility, emergence of new strains, and multiple environmental transmission pathways. • Surveillance studies indicate that NoV prevalence in water and shellfish is related to temperature, but it is not known how projected2020) Impacts of climate change on human health, HABs and bathing waters, relavant to the coastal and marine environment around the UK.
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Impacts of climate change on human
health, HABs and bathing waters, relevant
to the coastal and marine environment
around the UK
E. Bresnan 1, C. Baker-Austin 2, C.J.A. Campos 2*, K. Davidson 3, M.
Edwards 4,5, A. Hall 6, A. McKinney 7 and A.D. Turner 2
1 Marine Scotland Science, 375 Victoria Rd, Aberdeen AB11 9DB, UK
2 Centre for Environment, Fisheries and Aquaculture Science, The Nothe, Barrack
Road,Weymouth, Dorset DT4 8UB, UK
3 Scottish Association for Marine Science, Oban, PA37 1QA,UK
4 CPR Survey, Marine Biological Association, Plymouth, UK
5 School of Biological and Marine Sciences, University of Plymouth, Drake Circus,
Plymouth, UK
6 Sea Mammal Research Unit, W Sands Rd, St. Andrews, KY16 9XL, UK
7 Agri-Food and Biosciences Institute, 18a Newforge Lane, Belfast BT9 5PX
* Present address: Cawthorn Institute, 98 Halifax Street East, The Wood, Nelson 7010,
New Zealand
EXECUTIVE SUMMARY
Human health can be affected by toxin-producing phytoplankton,
pathogenic Vibrio species (bacteria) and noroviruses (NoV) in UK
waters.
The influence of climate change on toxin-producing phytoplankton is
complex. This can be difficult to distinguish from shorter-term
weather events and larger-scale circulatory processes. Confidence in
current long-term prediction for harmful algal bloom (HAB) species
is low. Data characterising the response of different HAB species to a
broad range of environmental parameters are needed to improve short
term (one to two week) forecasts and longer-term predictive models.
During the 2018 heatwave experienced in the UK (JuneJuly), record
water temperatures coinciding with elevated levels of pathogenic
Vibrio species were identified from several sites along the south-west
coast of the UK.
Climate change will modify the geographical distribution and
seasonality of NoV. However, it is difficult to predict the effects of
these changes on disease risk because NoV infectivity is determined
by a complex set of factors, including host availability and
susceptibility, emergence of new strains, and multiple environmental
transmission pathways.
Surveillance studies indicate that NoV prevalence in water and
shellfish is related to temperature, but it is not known how projected
Citation: Bresnan, E., Baker-
Austin, C., Campos, C.J.A,
Davidson, K., Edwards, M.,
Hall, A., McKinney, A. and
Turner, A.D. (2020) Impacts
of climate change on human
health, HABs and bathing
waters, relavant to the
coastal and marine
environment around the UK.
MCCIP Science Review
2020, 521545.
doi:
10.14465/2020.arc22.hhe
Submitted: 10 2019
Published online: 15th
January 2020.
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MCCIP Science Review 2020 521545
522
increases in sea-surface temperatures will affect the risk of illness.
Runoff from more frequent and intense extreme rainfall events will
increase NoV contamination from sewage sources and compromise
water quality, particularly in areas served by combined sewerage
infrastructure. Following sewer overflows, NoV concentrations in
nearshore waters can be 10 times higher than concentrations during
‘no discharge’ conditions.
A survey of tetrodotoxin (TTX) in shellfish from around the UK
revealed the toxin to be present in quantifiable amounts in shellfish
from southern England and in one sample from Scotland. Highest
TTX concentrations were recorded when water temperatures
exceeded 15°C (maximum concentration of total TTXs; 253 µg/kg)
although the toxin was also present at other times of the year. The role
of water temperature on the occurrence and distribution of this toxin
in UK shellfish and biota merits further investigation.
1. BACKGROUND
Climate change has the potential to impact coastal ecosystems in multiple
ways, altering human exposure to water-related contaminants that can cause
illness. The main groups of relevance to water-related illnesses in the UK
marine environment are toxin-producing phytoplankton and pathogenic
bacteria and viruses.
Harmful Phytoplankton
Marine phytoplankton are single-celled algae that inhabit the water column.
They play an important ecological role in the marine ecosystem as primary
producers, harvesting light energy from the Sun to produce food which gets
passed up through the marine food web (Chavez et al., 2011). A number of
marine phytoplankton species can produce toxins that can accumulate in the
flesh of shellfish and can pose a risk to human health if consumed. When
environmental conditions are favourable these toxin-producing
phytoplankton can increase in abundance. This is called a harmful algal
bloom’ (HAB). The main HAB genera of concern for human health in UK
waters are the dinoflagellates Alexandrium (associated with the production of
toxins responsible for paralytic shellfish poisoning (PSTs), Dinophysis
(toxins associated with diarrhetic shellfish poisoning (DSTs)) and the diatom
Pseudo-nitzschia (toxins associated with amnesic shellfish poisoning (ASTs);
Davidson and Bresnan, 2009). The dinoflagellates Azadinium (azaspiracid
toxins, AZAs), Protoceratium reticulatum, Lingulodinium polyedra and
Gonyaulax spinifera (yessotoxins, YTX) are less of an issue in UK waters
although AZAs have caused significant problems for the Irish shellfish
industry (Chevallier et al., 2015). The threat to human health from these
shellfish toxins is managed by the Food Standards Agency (in England,
Northern Ireland and Wales) and Food Standards Scotland who oversee a
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monitoring programme for shellfish and causative phytoplankton in
fulfilment of Food Hygiene Regulations (primarily Regulation (EC) No.
854/2004) to prevent the consumption of contaminated product.
Vibrio species and Noroviruses
One group of environmental bacteria (pathogenic Vibrio) are an increasingly
important cause of disease around the world. These bacteria can cause a range
of infections in humans, such as gastroenteritis, wound infections and sepsis
(blood poisoning). Transmission is mostly driven by the consumption of
contaminated seafood and/or exposure to seawater, often recreationally
through swimming. The species Vibrio vulnificus, V. parahaemolyticus and
V. cholerae are commonly implicated in human diseases. These bacteria grow
in warm, low-salinity waters and their abundance in the natural environment
mirrors ambient environmental temperatures.
Human noroviruses (NoV) are the most common pathogenic virus causing
epidemic infectious intestinal disease (IID) and a major cause of waterborne
illness worldwide. In the UK, approximately 17 million cases of illness and
one million general practice consultations due to IID occur annually (Tam et
al., 2012). The number of cases of shellfish-borne NoV in the UK has been
estimated to be approximately 21,000/year (Hassard et al., 2017). Norovirus
are highly contagious, rapidly and prolifically shed by symptomatic and
asymptomatic individuals, very stable in the environment outside the human
host and resistant to many forms of disinfection (Campos and Lees, 2014).
Human exposure to these organisms occurs through ingestion, inhalation or
direct contact with contaminated water and shellfish. Worldwide, the most
common manifestations of waterborne illness are gastrointestinal (nausea,
vomiting, diarrhoea). However, the effects can be more severe in persons who
are more vulnerable to illness (the young, the elderly, and the
immunocompromised). In the UK, there is no statutory mechanism for
reporting water-related disease and the evidence about the burden of disease
comes primarily from recording of outbreaks. It is widely accepted that the
total incidence of these diseases is largely underestimated. There is no
specific legislation to control risks from Vibrio and NoVs.
Assessing climate change impacts and human health
The complexity of how climate change impacts the marine environment is
increasingly acknowledged. The waters around the UK are showing a long-
term warming trend over the last 30 years. However, there has been some
short-term variability recorded with the period from 20082013 being cooler
than that from 20002008 and 20142017. Local and regional variations have
also been observed and the influence of cold ocean temperature anomalies in
the mid-high latitude North Atlantic has weakened the warming along the
UK’s south-west coast since the last relevant MCCIP Report Card (Tinker
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and Howes, 2020). The recent UK Climate Predictions (UKCP18) also
present a latitudinal aspect to predicted changes in air temperature and
precipitation (Lowe et al., 2018). Separation of climate-change impacts from
short-term fluctuations, such as weather events and long term multidecadal
cycles such as the North Atlantic Oscillation (NAO) and the Atlantic
Multidecadal Oscillation (AMO), are difficult and must be considered when
examining the impacts of climate change on biota. The impacts from
additional anthropogenic pressures on organisms harmful to human health,
such as ocean acidification is complex, in many cases potentially acting in
synergy with changes in other environmental parameters such as temperature
(Raven et al., in press).
To date, most research has focused on understanding how climate drivers
affect physical and ecological processes that act as key exposure pathways
for pathogens and toxins. There is currently much less information and fewer
methods with which to measure actual human exposure and incidence of
illness based on physical and ecological metrics from harmful events
(Berdalet et al., 2016). Studies examining societal impact in UK waters are
scarce (Willis et al., 2018). Furthermore, much of the related research is either
global or highly localised and therefore does not allow quantitative
projections of future health outcomes from water-related illnesses at temporal
and spatial scales appropriate for decisions to be made (Watts et al., 2015).
This review presents the current status of harmful phytoplankton, Vibrio
species and NoVs in UK waters, as well as providing an update on improved
understanding of the dynamics behind some of these issues since the last
update (Bresnan et al., 2017). Based on the available data and research, many
of the examples reported in the literature are site-specific. Environmental,
public health and food safety agencies in the UK maintain monitoring
programmes to reduce the risk of exposure to these hazards and water
companies undertake water quality investigations and implement
programmes of sewerage infrastructure upgrading to protect human health.
The scientific research community has also completed a number of studies
which contribute to improved understanding of the dynamics of the causative
organisms, essential to understanding and improving the ability to predict
impacts from climate change.
2. WHAT IS ALREADY HAPPENING?
Harmful Algae
Identification of climate change impacts on harmful algae is complex with
multiple factors such as temperature, water column stability, turbidity,
nutrients, grazing pressure, ocean acidification, wind mediated transport all
potentially influencing abundance, distribution and toxicity (Hallegraeff et
al., 2010, Wells et al., 2015, Trainer et al., 2019). HAB species in UK waters
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are diverse, observe a variety of different lifecycle and feeding strategies (e.g.
Alexandrium, obligate cyst formation, Dinophysis, complex mixotrophy,
Pseudo-nitzschia, chain forming autotroph) and are regionally distributed
around the UK coast (Davidson and Bresnan 2009, Bresnan et al., 2013,
Lewis et al., 2018). In some instances, information on species level diversity,
toxin production, distribution and ecology of these different HAB species is
still being collected in the UK. Since the last report card and update (Bresnan
et al., 2013; 2017) there has not been a dedicated investigation into the impact
of climate change on HABs in UK waters. A number of studies have
improved understanding of the diversity and distribution of selected HAB
species and how biological and physical drivers influence toxicity and bloom
formation in this region. These studies improve baseline understanding of the
dynamics of HABs in UK waters which is essential to understand the impacts
of environmental change on this group of organisms.
Analysis of historical data from the Continuous Plankton Recorder (CPR)
collected over the last 50 years provides evidence of the impact of changing
environmental conditions on the phytoplankton community in the seas around
the UK. These analyses have identified a ‘cold boreal’ anomaly in the late
1970s, a ‘warm temperate’ event resulting in a regime shift at the end of the
1980s, and an additional shift in the phytoplankton community in 2008
(Edwards et al., 2002; Alheit et al.,2005; Edwards et al., 2006; Wiltshire et
al., 2008; Alvarez-Fernandez et al., 2012). Analysis of this dataset has shown
a change in the abundance and distribution of selected HAB genera
(Dinophysis, Ceratium (renamed Tripos, Gomez 2013), Prorocentrum),
within the North Sea since the 1960s (Edwards et al., 2006). Sea-surface
temperature and changing wind speeds have been shown to influence
increases in the diatom Pseudo-nitzschia and decreases in the dinoflagellate
Tripos in the north east Atlantic since the mid-1990s (Hinder et al., 2012),
although there is some evidence of recovery in the latter over the last five
years (Edwards et al., 2020).
The influence of weather on HAB events has been confirmed in multiple
studies. A DST intoxication event in 2013 where human illness was recorded
after consumption of shellfish harvested from Shetland, was revealed to be
driven by a sudden change in wind direction, transporting a population of
Dinophysis onshore, resulting in a rapid increase in DSTs in Mytilus edulis
(Whyte et al., 2014). Wind direction and intensity has also been seen as a
driving factor behind prolonged DST events in Loch Fyne in Scotland (Morris
et al., 2010) as well as contributing to changes in phytoplankton community
composition over multiple decades recorded by the CPR (Hinder et al., 2012).
The establishment of HAB species from more southern waters (e.g.
Gymnodinium catenatum from the Iberian Peninsula) has yet to be recorded
in the UK (Bresnan et al., 2017). A dedicated study to establish the
methodologies for new and emerging HAB toxins (e.g. brevetoxins,
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pinnatoxins, cyclic amines) did not detect any in UK shellfish (Turner et al.,
2015a; Davidson et al., 2015).
There is a strong regional distribution in management actions (closure of
shellfish harvesting areas) and impacts associated with harmful
phytoplankton around the UK with the majority of management actions
recorded in Scotland (Figure 1). This is governed by the spatial distribution
of the causative phytoplankton and the location of shellfish harvesting
activities. Algal toxins have also been detected in marine mammals in
Scottish waters (Hall and Frame 2010, Jensen et al., 2015). Since the last
MCCIP Report Card (Bresnan et al., 2017) the incidence of closures of
shellfish harvesting areas due to the presence of algal toxins above the closure
limit has followed the regional pattern, but with an unusual record of PST in
shellfish in Swansea. An exceptional event was observed in December 2017
January 2018. A strong storm resulted in mass strandings of Dab (Limanda
limanda), and multiple species of crabs and starfish on the beaches of East
Anglia. A number of dogs who consumed these stranded fish and starfish
became ill and two died as a result of intoxication by PSTs (Turner et al.,
2018a). This is the first report of canine fatalities in the UK as a result of
PSTs. This result is surprising in this area due to the time of year this event
was recorded. Alexandrium has only been recorded occasionally and in low
abundance and PSTs have not been recorded in this region since chemical
testing began in 2008.
Since the last MCCIP Report Card, a review of the potentially PST producing
Alexandrium minutum suggest two different strains to be present in UK
waters, a non-toxic strain in Scotland and a toxic strain in the south coast of
England (Lewis et al., 2018). This review provides further support to the
regional distribution of PSTs detected in shellfish flagged in previous report
cards with A. catenella responsible for PSTs in shellfish in Scotland and A.
minutum in England (Collins et al., 2009; Turner et al., 2014). This also
highlights the complexity in examining the impacts climate change on
industries impacted by HABs given the regional diversity within the causative
genera.
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(A) ASTs (B) AZAs
(C) DSTs (D) PSTs
Figure 1: Number of years with management actions/negative impacts recorded at sites on
the UK coast as a result of algal toxins harmful to health during the period 20002017.
Data from the IOC-ICES-PICES Harmful Algal Event database (HAEDAT): (A) ASTs, (B)
AZAs, (C) DSTs and (D) PSTs. HAEDAT divides the UK coastline into 200 km strips and
summarises duration of shellfish closures and other impacts into ‘events’. See ICES-IOC
WGHABD (2017) for more information. Note: routine monitoring for AZAs began in the
UK in 2011.
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A review of the regional distribution of DST profiles associated with the
genus Dinophysis (Okadaic Acid (OA), Dinophysistoxins 1 (DTX1) and 2
(DTX2) between 2011 and 2016 was performed. This revealed the majority
of incidences to have been recorded in Scotland and laterally in the south-
west of England (Dhanji-Rapkova et al., 2018). A study of Dinophysis
species recorded in Scotland since 2001 showed D. acuminata to be present
during the summer months while D. acuta occurred more sporadically. The
presence of D. acuta was associated with a decrease of OA and DTX1 relative
concentrations and an increase of DTX2 in the toxin profiles within the
shellfish flesh (Swan et al., 2018). Investigation into the environmental
control of Dinophysis blooms in the Clyde Sea in Scotland highlighted the
role that temperature driven frontal systems can play in preventing
Dinophysis blooms being transported into sea lochs within the Clyde, thus
protecting aquaculture sites from the impacts associated with Dinophysis
toxins (Paterson et al., 2017). The concentration of AZAs in shellfish in the
UK have shown a high degree of interannual variability since monitoring
began in 2011. Since 2013 there have been no records of AZAs in shellfish
over the maximum permissible limit recorded in Scotland and only one record
in the south-west in 2015. Yessotoxins are rarely detected in UK shellfish and
records to date mainly come from the south-west of Scotland and Shetland.
Phytoplankton monitoring data associates Protoceratium reticulatum with
YTX in these areas (Dhanji-Rapkova et al., 2019).
A review of ASTs in UK shellfish from the last 10 years has showed that
while the concentration of Domoic Acid (DA) was below the maximum
permitted limit of 20 mg/kg in the majority of cases, an increase in the
frequency of occurrence of DA was observed, particularly in England during
2014 (Rowland-Pilgrim et al., 2019). A new study of the diversity of Pseudo-
nitzschia in the southern North Sea showed the presence of DA (the main
AST) in the water column to be associated with presence of P. delicatissima,
P. pungens and P. fraudulenta (Delegrange et al., 2018). This is in contrast
to recorded toxicity within this genus in Scotland, where these species were
found not to produce detectable concentrations of DA while DA production
was confirmed in P. australis and P. seriata (Fehling et al., 2006). Oomycete
parasites which have the potential to infect Pseudo-nitzschia cells have been
described from Scotland for the first time (Garvetto et al., 2018). This is the
first study of HAB parasites in UK waters, an additional biological factor
which may impact HABs by influencing bloom termination.
There is a global effort underway to investigate the global status of HABs
(Hallegraeff et al., 2017). In other parts of the world, extreme HAB events
have been recorded over the last number of years which have had devastating
impacts on local ecology and aquaculture industries (Trainer et al., in press);
a warm water anomaly in the eastern Pacific, which has persisted since 2014,
resulted in a significant Pseudo-nitzschia bloom, extended shellfish closures
as well as other multiple ecosystem impacts (Du et al., 2016; Trainer et al.,
in press) and a strong El Niño year resulting in catastrophic fish kills in Chile
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from blooms of Pseudochattonella and A. catenella (Clement et al., 2016).
Extreme events on such a scale have not been recorded in the UK.
Norovirus
Environmental factors such as temperature, rainfall and rising sea levels can
affect the abundance, distribution, growth and toxicity of the organisms which
can cause water-related illness. Heavy rainfall events are increasing in
frequency and intensity in parts of the UK (Jones et al., 2013; Otto et al.,
2018), however, the frequency and intensity of extreme events vary by region
and thus human health impacts will also vary accordingly. Air temperature in
the UK is generally increasing with greater increases in summer than winter,
and greater increases in the south than in the north (Watts et al., 2015; Lowe
et al., 2018) but there has been little research to examine the influence of air
temperature increases on coastal water quality.
Since the last MCCIP Report Card, a detailed analysis of environmental risk
factors for NoV in UK coastal areas has been carried out. These are water
temperature, number and volume of sewage discharges and river flows
(Campos et al., 2017). Further quantification of NoV concentrations in
sewage effluents subject to different treatment processes has been carried out
since the last report card. The results indicate no appreciable differences in
concentrations between untreated sewage and storm tank discharges (Campos
et al., 2016). Previous work had shown that following storm tank discharges,
mean NoV concentrations in oysters sampled in downstream waters can
increase 10 times relative to mean concentrations typically found during no-
discharge conditions (Campos et al., 2015). This indicates that, during rainfall
events, stormwater discharges can mobilise high concentrations of NoV to
rivers and coastal waters popular with bathing and other water-based
activities. There is very little information in the peer reviewed literature about
the frequency and duration of sewer overflows. However, reports based on
data for two UK water companies provided by the Environment Agency
indicate that 50% of overflows to rivers and 33% of overflows to coastal areas
are discharging more than once a month (WWF, 2017). This suggests that
despite the significant investment made by water companies in improving the
sewerage infrastructure, in parts of the UK a large number of overflows are
still spilling frequently.
The associations between weather and bathing water quality on infectious
intestinal disease were investigated using data from two Scottish National
Health Service Board areas (Eze et al., 2014). Monthly counts of viral and
non-viral gastrointestinal infections have been modelled as a smooth function
of temperature, relative humidity and average monthly counts of faecal
indicator organisms (adjusted for season and long-term trend effects) in
bathing waters in Scotland. In this study, humidity was used as a surrogate
for rainfall which was not available for the Board areas studied. In the context
of climate change modelling, changes in atmospheric humidity transport can
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be assumed to correlate well with daily rainfall totals (Lavers and Villarini,
2015). A significant negative association existed between weather
(temperature and humidity) and viral infection (Eze et al., 2014). Average
levels of non-viral gastrointestinal infections (e.g. salmonellosis,
campylobacteriosis) increased as temperature and relative humidity
increased. Peak viral gastrointestinal infection was in May while that of non-
viral gastrointestinal infections was in July. Increasing levels of faecal
indicator organisms in bathing waters were also associated with an increase
in the average number of viral and non-viral gastrointestinal infections at the
ecological level. UKCP09 projections for 2080–90 for a ‘medium emission
scenario’ indicate that sea-surface temperatures in the summer bathing season
will be 22.5 ºC warmer although in north and west of Scotland may be only
1ºC warmer (UKCP09, 2017). In theory, warmer waters and drier weather
create less favourable conditions for NoV to persist in the environment
outside human hosts. However, it has not been possible to quantify the effects
of these changes on disease prevalence because many water-related illnesses
are either undiagnosed or unreported. This is discussed further in Section 3
below.
Vibrio species
Pathogenic Vibrio species are a globally important cause of diseases in
humans and aquatic animals. There is growing evidence, based on laboratory,
environmental and clinical studies that demonstrate the clear association
between climate change and the incidence and disease impacts caused by
these bacteria. Because these Gram-negative bacterial pathogens, including
the species Vibrio vulnificus, Vibrio parahaemolyticus and Vibrio cholerae,
grow in warm, low-salinity waters, and their abundance in the natural
environment mirrors ambient environmental temperatures, they represent an
important marine sentinel species to study climate change impacts (Baker-
Austin et al., 2016a, b).
The lack of long-term datasets on Vibrio species precludes comparative
analyses (e.g. in both time and space) of the relationship between the role of
temperature and microbial diversity. However, studies carried out by Cefas
in 2018, including a recent analysis of low salinity (<30) estuarine systems in
southern England, demonstrate that pathogenic Vibrio spp. are present in
water and shellfish during summer months, often in very high concentrations.
These data augments previous studies carried out during 20122013 which
identified potentially pathogenic strains in two sites along the southern coast
of the UK. In particular, data from the survey carried out during June
September 2018 identified a mixture of human pathogenic strains including
Vibrio vulnificus, Vibrio alginolyticus, Vibrio parahaemolyticus and Vibrio
cholerae all four of which are considered important human pathogens
(Baker-Austin et al., 2018). As with previous work in 20122013, strains
carrying pathogenicity genes were regularly identified during this survey.
Record high water temperatures, exceeded 30oC in one site in July 2018 (and
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which were above 20oC from late June until the middle of August across all
sites), were observed through the summer of 2018. These unusual conditions
corresponded with a significant heatwave event in the UK from June to early
August, and may have played a role in driving the abundance of these
bacteria.
Analysis of archived Continuous Plankton Survey (CPR) samples has
investigated bacterial DNA in formalin-preserved plankton samples collected
over the past half-century (19582011) from the North Atlantic region. In
areas of warming, data from historic plankton sampling sites showed
increases in Vibrio bacteria abundance including the North Sea. The increases
in Vibrio abundance were related to changes to climate warming and the
Atlantic Multidecadal Oscillation (AMO). These changes parallel the rise in
Vibrio-related illnesses documented along the US Atlantic Coast and in
Northern Europe (Vezzulli et al., 2016).
Heatwave events appear to play a significant role in driving human health
risk. During the summer of 2018, a significant and sustained heatwave event
was observed across much of Northern Europe. As with previous heatwave
years in the region (e.g. 1994, 2006, 2010 and 2014) a large number of Vibrio
infections were subsequently reported associated with recreational water
exposures, and these infections have been reported in a number of countries,
including cases observed in Finland, Sweden, Norway and Germany. These
findings are of relevance because we have noticed an increase in heatwave
events in Northern Europe over the last two decades (Barriopedro et al.,
2011), with potential heatwave events likely to impact the UK similarly under
a warming climate system. A preliminary assessment of reported cases as well
as the environmental conditions driving these infections is currently ongoing,
however an analysis of the event of 2018 compared to the most significant
and recent heatwave observed in Northern Europe in 2014 (Baker-Austin et
al., 2016a, b) suggests a larger, more pronounced and longer-sustained
warming event. It is likely that this has corresponded with a noticeable
increase in the geographical spread over which Vibrio bacteria may flourish
(Semenza et al., 2017). In particular, infections have been reported
extensively this year in Norway, with several severe blood (sepsis) cases and
more than one fatality has also been reported by the media during the summer
of 2018 in this region.
It should also be noted that there are few domestically acquired Vibrio
infections reported each year, with the current risk deemed low. However, a
recent genomic study of pathogenic strains of Vibrio parahaemolyticus
reported in the UK, using isolates supplied from Public Health England’s
gastrointestinal unit has also shed some light onto potential Vibrio risk in the
UK. A small number of potentially domestically acquired infections were
identified from this work, including strains where no recent travel was
suspected. With the observation that previous V. parahaemolyticus infections
have been reported in the UK (Hooper et al., 1974), there remains the
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possibility that these unattributed infections, as well as many more based on
foodborne attribution studies (Scallen et al., 2011) are circulating in the UK.
Tetrodotoxin
Tetrodotoxin (TTX) is a highly potent neurotoxin known to accumulate in a
wide range of marine species (Turner et al., 2017). TTX is responsible for the
highest fatality rate of all marine intoxications, being associated most
commonly with accumulation in species of fish from the Tetraodontidae
family, such as puffer fish (Isbister et al., 2005). Unlike other marine
biotoxins, TTX is thought to be associated with production from a range of
marine bacteria, including most notably Vibrio species, although others have
postulated an association with certain specific phytoplankton species such as
P. cordatum (Turner et al., 2017). TTX is commonly encountered in tropical
and subtropical environments, and following the previous identification of
TTXs in shellfish from southern England in 2014 (Turner et al., 2015), a
recent survey of TTX in UK shellfish produce has been undertaken. Samples
were collected between 2014 and 2016 from around the UK, and results
showed the presence of TTX and associated analogues (TTXs) in a range of
shellfish species, including Pacific oysters (Crassostrea gigas), native oysters
(Ostrea edulis), common mussels (Mytilus edulis) and hard clams
(Mercenaria mercenaria), but not found to date in cockles (Cerastoderma
edule), razors (Ensis species) or king scallops (Pecten maximus). TTX-
positive bivalves have been almost exclusively detected from shellfisheries
along the south coast of England with one sample containing quantifiable
amounts of TTX from Scotland. The highest concentrations were quantified
in samples harvested during the warmer summer months, although TTXs
were still evident from some areas occasionally during the winter. A greater
level of risk was observed in areas of shallow, estuarine waters with
temperatures above 15°C (Turner et al., 2017), although more work is
required to elucidate the specific impacts of environmental parameters on
TTX presence in shellfish. Confirmation of the causative organism is critical
to begin to assess any impacts from climate change on this toxin. TTX has
also been identified recently in a non-native ribbon worm Cephalothrix
simula collected from west Cornwall. This presents another potential risk to
human health from exposure to TTX and more investigation is needed to
assess transfer of this toxin through different trophic levels (Turner et al.,
2018b).
3. WHAT COULD HAPPEN IN THE FUTURE?
Climate change can impact the physical environment in UK waters in
multiple ways. UKCP18 predict a move to warmer wetter winters and hotter
drier summers over the next century (although some variability will be
expected), increased coastal flood risk and sea level change, varying with
change scenario and geographic region (Lowe et al., 2018). Recent MCCIP
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updates show warming sea temperatures (Tinker and Howes, 2020), declining
oxygen concentrations in the North Sea (Mahaffey et al., 2020), with some
uncertainty around predictions for sea-level rise and storms and waves
(Horsburgh et al., 2019; Wolff et al., 2019) . The complexities in predicting
how climate change will impact harmful phytoplankton species have been
detailed in two key papers (Hallegraeff, 2010; Wells et al., 2015) with many
unknowns remaining and warranting further investigation.
Ocean acidification is also likely to affect marine biota, in synergy with
climate change impacts such as warming sea temperatures, thus making
identification of individual drivers of change difficult (Sommer et al., 2015;
Raven et al., in press) and a number of unknowns remain (Hallegraeff, 2010;
Wells et al., 2015). Ocean acidification impacts on the plankton community
was demonstrated in a recent mesocosm study where variable responses to
CO2 concentrations observed between different phytoplankton groups. The
nuisance phytoplankton Vicicitus globosus (class Dictyochophyceae, which
produces haemolytic cytotoxins that can cause fish mortalities) increased in
abundance and formed blooms as CO2 concentrations increased over 600
800 µatm. This subsequently disrupted the development of the micro- and
meso-zooplankton communities and impacted trophic transfer through the
food web (Riesbesell et al., 2018).
Modelling approaches have been used to examine the relationship of selected
HAB species with temperature. Gobler et al. (2017a, b) modelled an increase
in Dinophysis species growing period in the North Sea associated with
increases in sea surface temperature. However, the lack of inclusion of
additional drivers and phytoplankton loss terms into the model may result in
an over-estimation of the HAB populations (Dees et al., 2017). Townhill et
al. (2018) used species distribution models (SPDs) to reveal large shifts in the
distribution of selected harmful species from the Iberian Peninsula, along the
shelf edge and into the northern North Sea. While SPDs can show the
potential for range expansion, their application to plankton has been
questioned, with their accuracy reducing the further they project into the
future (Brun et al., 2016).
Changes in offshore circulation over multiple decades have great potential to
impact the dynamics of the North Sea. Large-scale modelling (Holt et al.,
2018) has shown the potential for climate change to reduce Atlantic inflow
into the North Sea. This will lead to a reduction in salinity and increased
influence from riverine input altering the nutrient regime and turbidity
particularly in the southern North Sea. This has the potential to impact the
distribution of HABs which already observes a regional distribution in this
region (ICES-IOC WGHABD, 2017).
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Norovirus
More frequent extreme rainfall events and associated runoff and storm surges
will exert greater pressure on the sewerage infrastructure and increase virus
loading, thus compromising the quality of the waters used for recreational
activities and shellfish harvesting (Hassard et al., 2017). Sewerage systems
in medium to highly urbanised catchments will be at greater risk of
exceedance of system capacity or failure due to damage. The risk of extreme
winter rainstorms in southern England, such as those that caused widespread
flooding in January 2014, has increased because of climate warming (Schaller
et al., 2016). In a large ensemble of climate model simulations, Schaller et al.
(2016) found that, as well as increasing the amount of moisture the
atmosphere can hold, anthropogenic warming caused a small but significant
increase in the number of January days with westerly flow, both of which
increased extreme precipitation. A significant risk of gastrointestinal illness
associated with contact with urban floodwater, particularly during clean-up
periods, has been demonstrated in two flood-related scenarios examined in
the UK (Fewtrell et al., 2011).
Some changing river flow regimes agree with future change projections,
while others are in apparent contradiction. Observed changes generally have
not been attributed to climate change, largely because of large direct human
disturbances on river flows and because river flow records are limited in
length and the identification of short-term trends is confounded by natural
variability (Hannaford, 2015).
Quantification of spill volume, duration and frequency for 19 combined sewer
overflows to coastal waters in the north-west of England under two climate
change scenarios (high and low emission scenarios) simulated by three global
climate models predicted an annual increase of 37% in total spill volume,
32% in total spill duration and 12% in spill frequency for the shellfish water
by 2080. The study further showed that CSO spill metrics are likely to reduce
substantially during the bathing season under both emission scenarios
(Abdellatif et al., 2015). A further study that used a high-resolution dynamic
climate model to estimate changes in UK rainfall intensities at short durations
(1, 3 and 6 hours) as a result of climate change found greater numbers of spills
on an annual basis and greater spill volumes during the bathing season than
previous projections based on UK climate change allowances for rainfall
intensity (Dale et al., 2015).
Changes in water temperatures will also alter the seasonality, abundance and
distribution of NoV in coastal waters. In UK coastal areas where increasing
temperatures lengthen the periods for bathing and other water-based
activities, exposure risks are expected to change. Current ‘regulatory’
microbial monitoring practices are time consuming, expensive and may not
reveal the actual health risk. Catchment-based modelling combining targeted
in situ monitoring and rainfall and temperature projections offer the potential
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for more accurate estimates of health risk (Coffey et al., 2014). Source
attribution, through quantified microbial source apportionment, linked with
appropriate use of microbial source tracking methods should, therefore, be
employed as an integral part of future epidemiological surveys (Fewtrell et al
2011).
Improvements in the predictive capability of global and regional climate
models (GCMs/RCMs) provide better insights into areas currently
undergoing change and areas where potential risks may greatly increase or
emerge in the future. While considerable work is underway to better
understand the capacity and resilience of sewerage networks and in planning
the investment in infrastructure required to take account of increasing
populations and climate change, information on the consequential reductions
of overflow events and associated microbial water quality improvements is
lacking in the peer-reviewed literature. This type of information is extremely
important for risk managers, clinicians and public health bodies as a proactive
means of ameliorating and managing changing risk, particularly in regions
where these types of pathogens may emerge in the short to medium term.
These future projections are allowing regions to be identified where it is
possible to provide detailed advice for risk assessment purposes.
Vibrio species
The environmental parameters that drive pathogenic Vibrio species in the
environment are well established. Pathogenic Vibrio grow well in warm
(>15°C) low salinity waters (<30), with their abundance in the environment
effectively tracking ambient sea surface temperatures. Validation of tools
such as those that use temperature and salinity datasets (Semenza et al., 2017;
Baker-Austin et al., 2013) have allowed us to predict when and where human
infections are likely to occur (Figure 2). In particular, sea surface
temperatures (SST) that exceed 18°C for sustained periods of time have
previously been implicated in disease emergence in Europe, in particular in
the Baltic Sea (Baker-Austin et al., 2013) (Figures 2 and 4).
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Figure 2: Variation of Vibrio: 1st August 2018. A significant swathe of warm, low salinity
(<30) water is apparent, stretching from the northern Baltic Sea to the transitional waters
of the North Sea/Baltic between southern Norway and Denmark. Based on data from
previous studies (Baker-Austin et al., 2013) these waters are capable of supporting vibrios
at high concentrations. (Data courtesy NOAA,
http://cwcgom.aoml.noaa.gov/cgom/OceanViewer/#)
Alongside general warming trends observed in northern latitude marine
systems (Lima and Wethey, 2012), the recent increase in the number, size,
length and severity of European heatwaves should also be noted (Barriopedro
et al., 2011), Figure 3. There is now a considerable body of research
providing climate projections of sea temperature for the UK waters and the
North-West European Shelf seas (NWS) (Tinker and Howes, 2020). For
instance, there is now good agreement on the sign of the temperature change
on the NWS among the end-of-century climate projection. However, there is
a spread in the magnitude of this warming. Most projections give a warming
between 14°C (Tinker and Howes, 2020). Irrespective of this, based on our
knowledge regarding the ecology of Vibrio pathogens, this increase in
warming is likely to greatly extend both the potential abundance as well as
risk window over which Vibrio infections are likely to occur in the UK and
NWS area. Such generalised warming trends can also be useful when
assessing potential risks from the presence of TTXs in shellfish, given the
widely accepted but not yet conclusively proven links between Vibrio and
other marine bacteria, and TTX (Turner et al., 2015a, b).
Daily Vibrio risk
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Figure 3: European summer temperatures for 15002010. Statistical frequency distribution
of best-guess reconstructed and instrument-based European ([35°N, 70°N], [25°W, 40°E])
summer land temperature anomalies (degrees Celsius, relative to the 19701999 period)
for the 15002010 period (vertical lines). The five warmest and coldest summers are
highlighted. (Reproduced with kind permission from Barriopedro et al., (2011), Science,
10.1126/science.1201224.)
Extreme localised warming of coastal areas has previously been associated
with seafood-related outbreaks in mid- and high-latitude areas, including V.
parahaemolyticus outbreaks in Alaska (McLaughlin et al., 2005) and
Northern Spain (Martinez-Urtaza et al., 2016). Critically, warmer summers,
predicted in the UKCP18 (Lowe et al., 2018) are likely to greatly moderate
Vibrio risk, especially heatwave events. For instance, using previously
employed temperature thresholds to define extremely hot summers, recent
studies have found that heatwave events that would occur twice a century in
the early 2000s (e.g. the 2003 European heatwave event) are now currently
expected to occur twice a decade. Critically, all RCPs indicate that by the
2040s a summer as hot as 2003 will be very common, and RCPs with the
strongest anthropogenic influence (e.g. RCP6.0 and RCP8.5) suggest the
2003 summer will be deemed an extremely cold event by the end of the
century (Christidis et al., 2015). Even a casual analysis of ‘Vibrio risk years’
(e.g. where elevated numbers of cases are reported) across Europe indicates
that the number and severity of extreme heatwave events has increased
recently (e.g. 2010, 2014, 2018 notable years with increased reports of
infections linked to heatwave events). Statistical analysis using past climate
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warming trends also suggests a longer ‘at risk’ period, with infections likely
to be reported earlier in the summer and into the autumn, correlating with an
increased time period over which these bacteria can flourish in the
environment (Baker-Austin et al., 2013). Other extreme climatic events have
also been linked to an increase in reported Vibrio infections (e.g. extreme
rainfall events reducing salinity, storm surges, etc.) (Baker-Austin et al.,
2016a), however the potential for these events to modulate risk is difficult to
ascertain. There is considerable uncertainty regarding future salinity around
the UK coastline, however most of the projections over the 21st Century
suggest that shelf seas and adjacent ocean will be fresher in the future than at
present (Dye et al., 2020). A freshening of marine waters is likely to
potentially increase Vibrio risk, however the interaction of salinity and
temperature in this regard is highly uncertain.
Figure 4: The relationship between Vibrio infections reported in the Baltic Sea and
maximum annual sea surface temperature (SST). Stars show observed data, dashed line
shows model predictions based on the influence of SST alone. Figure courtesy of Baker-
Austin et al. (2013a, b).
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4. CONFIDENCE ASSESSMENT
What is already happening?
NoV
HABs
Vibrio
What could happen in the future?
NoV
HABs
Vibrio
During the 2013 assessment HABs were assessed in a separate report card to
Human Health. HABs, pathogenic Vibrio species and NoV are three different
biological entities and thus their response to impacts of climate change and
confidence about them should not be expected to be the same. Analysis of
historical HAB data has shown evidence of change along with other members
of the phytoplankton community; however confidence in predicting change
remains low. As the causative organism of TTX in UK shellfish has yet to be
identified, this has not been assessed here. These different confidence
assessments flag the complexity of assessing the impacts of climate change
on human health. Efforts to provide field-based and retrospective
environmental data have greatly improved our understanding of how
environmental cues modulate Vibrio risk. However, data gaps still exist, in
particular the role of salinity in impacting these bacteria in the environment
Amount of evidence
Level of
agreement/consensus
H
M
L
H
M
L
Amount of evidence
Level of
agreement/consensus
H
M
L
H
M
L
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as well the lack of long-term environmental studies regarding these
pathogens. In addition, although the presence of pathogenic strains in the
environment has been observed, there has been a lack of clinical cases
reported in the UK.
5. KEY CHALLENGES AND EMERGING ISSUES
There is a lack of information and few methods with which to measure
actual human exposure and incidence of illness from HAB-related
toxins, Vibrios, NoV and TTX and studies of the societal impact
coming from these harmful events are scarce. Likewise, there is a need
to develop a framework for sharing of data between different
stakeholders involved with these emergent risks (e.g., clinicians,
scientists, microbiologists, risk assessors, etc.). Without supporting
data from the medical community, it will be difficult to quantitatively
project health outcomes from water-related illnesses resulting from
climate change.
Development of HAB models remains a challenge, both in the short
term (one to two week forecasts) to aid industry as well a longer term
projections into the future under different climate scenarios.
Expanding current models to include physical, chemical and
biological processes in addition to temperature will better recreate the
impacts of a changing climate in UK waters. Given the regional
diversity of HAB species in the UK, consideration to species level
differences may also be required.
Further research is needed on the development of wastewater
treatment processes for enhanced NoV removal, and on the likelihood
of human exposure to NoV in communities served by combined
sewerage infrastructure versus those served by separate infrastructure.
This should help better targeting of investment by water and sewerage
undertakers to reduce NoV loading to bathing and shellfish waters.
Improved understanding of how climatic factors affect the fate and
behaviour of NoV in the marine environment can facilitate the
development of predictive models for human health protection.
The ability to predict when and where different ‘at risk’ systems are
undergoing rapid warming using process-driven climate models will
greatly improve our understanding of future risk (Baker-Austin et al.,
2016a, b). In particular, models that can provide reliable data on areas
undergoing warming, with sufficient granularity to ascribe risk are
required, in particular using a range of different warming scenarios as
well as timescales. A key data gap in this regard in the availability of
salinity and temperature data at regional levels to feed into risk
assessment models. There are currently uncertainties regarding
modelling for salinity in many climate models. Regional model
projections are important because they will enable the scientific
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community to assess in greater detail over the UK how risks are
modulated by climate extremes.
The relatively recent discovery of TTX in European bivalves has
demonstrated a new threat to shellfish food safety, the causes of yet
which have yet to be confirmed. Studies on TTX-production
mechanisms, together with the experimental assessment of shellfish
uptake routes are urgently required to enable a full risk assessment of
the impacts of climate change on TTX-related risks.
REFERENCES
Abdellatif, M., Atherton, W., Alkhaddar, R.M. and Osman, Y.Z. (2015) Quantitative assessment of
sewer overflow performance with climate change in northwest England. Hydrological Sciences
Journal, 60(4), 636650.
Alheit J., Mollmann C., Dutz J., Kornilovs G., Loewe P., Mohrholz V. and Wasmund N. (2005)
Synchronous ecological regime shifts in the central Baltic and the North Sea in the late 1980s. ICES
Journal of Marine Science, 62, 12051215.
Alvarez-Fernandez, S., Lindeboom, H. and Meesters, E. (2012) Temporal changes in plankton of the
North Sea: community shifts and environmental drivers. Marine Ecology Progress Series, 462, 21
38.
Baker-Austin, C., Trinanes, J., Hartnell, R., Taylor, N., Siitonen, A. and Martinez-Urtaza, J. (2013)
Emerging Vibrio risk at high-latitudes in response to ocean warming. Nature Climate Change, 3,
73-77, doi:10.1038/nclimate1628
Baker-Austin, C., Trinanes, J.A., Gonzalez-Escalona, N. and Martinez-Urtaza, J. (2016a) Non-cholera
vibrios the microbial barometer of climate change. Trends in Microbiology, 25(1) pp. 7684, doi:
http://dx.doi.org/10.1016/j.tim.2016.09.008
Baker-Austin, C., Trinanes, J.A., Salmenlinna, S., Löfdahl, M., Siitonen, A. and Martinez-Urtaza, J.
(2016b) Heatwave-associated vibriosis in Sweden and Finland, 2014. Emerging Infectious
Diseases, 22 (7), 12161220.
Baker-Austin, C., Oliver, J.D., Alam, M., Ali, A., Waldor, M.K., Qadri, F. et al. (2018) Vibrio spp.
infections. Natuew Reviews Disease Primers [Internet] http://dx.doi.org/10.1038/s41572-018-
0005-8
Barriopedro, D., Fischer, E.M., Luterbacher, J., Trigo, R.M. and Garcia-Herrera, R. (2011) The hot
summer of 2010: redrawing the temperature record map of Europe. Science, 332(6026), 2204.
Berdelet E., Flemming L., Gowen R., and Davidson K. (2016) Marine harmful algal blooms, human
health and wellbeing: challenges and opportunities in the 21st century. JMBA, 96, 6191.
Bresnan, E., Davidson, K., Edwards M., Fernand, L., Gowen, R., Hall, A., Kennington, K., McKinney,
A., Milligan, S., Raine, R. and Silke, J. (2013) Harmful Algal Bloom Report Card. MCCIP Science
Review 2013, 236243, doi:10.14465/2013.arc24.236-243
Bresnan, E., Baker-Austin, C., Campos, C.J.A., Davidson, K., Edwards, M., Hall A., Lees, D.,
McKinney, A., Milligan, S., Silke, J. (2017) Human Health. MCCIP Science Review 2017,
doi:10.14465/2017.arc10.008-huh
Brun, P., Kiorbe, T., Licandro, P. and Payne, M.R. (2016) The predictive skill of species distribution
models for plankton in a changing climate Global Change Biology, 22, 31703181.
Campos, C.J.A. and Lees, D.N. (2014) Environmental transmission of human noroviruses in shellfish
waters. Applied and Environmental Microbiology, 80(12), 35523561.
Campos, C.J.A., Avant, J., Gustar, N., Lowther, J., Powell, A., Stockley, L. and Lees, D.N. (2015) Fate
of human noroviruses in shellfish and water impacted by frequent sewage pollution events.
Environmental Science & Technology, 49(14), 83778385.
Campos, C.J.A., Avant, J., Lowther, J. Till, D. and Lees, D.N. (2016) Human norovirus in untreated
sewage and effluents from primary, secondary and tertiary treatment processes. Water Research,
103, 224232.
Campos, C.J.A., Kershaw, S., Morgan, O.C. and Lees, D.N. (2017) Risk factors for norovirus
contamination of shellfish water catchments in England and Wales. International Journal of Food
Microbiology, 241, 318324.
Human health
MCCIP Science Review 2020 521545
542
Chavez, F.P., Messie, M. and Pennington, J.T. (2011) Marine Primary Production in Relation to
Climate Variability and Change [Carlson, C.A. and Giovannoni, S.J. (eds)]. Annual Review of
Marine Science, Vol 3, pp. 227260.
Chevallier, O.P., Graham, S.F.,Alonso, E., Duffy, C., Silke, J., Campbell, K., Botana, L.M. and Elliott,
C.T. (2015) New insights into the causes of human illness due to consumption of azaspiracid
contaminated shellfish. Scientific Reports, 5, 9818.
Christidis, N. et al. (2015) Dramatically increasing chance of extremely hot summers since the 2003
European heatwave, Nature Climate Change, 5, 4650.
Clement, A., Lincoquero, L., Saldivia, M., Brito, C.G., Munoz, F., Fernandez, C., Perez, F., Maluje,
C.P., Correa, N., Moncada, V., Contreras, G. (2016) Exceptional summer conditions and HABs
of Pseudochattonella in Southern Chile create record impacts on salmon farms. Harmful Algae
News, 53, 13.
Coffey, R., Benham, B., Krometis, L.-A., Wolfe, M. L. and Cummins, E. (2014) Assessing the effects
of climate change on waterborne microorganisms: implications for EU and U.S. water policy.
Human and Ecological Risk Assessment, 20, 724742.
Collins, C., Graham, J., Brown, L., Bresnan, E., Lacaze, J-P. and Turrell, E.A. (2009) Identification
and toxicity of Alexandrium tamarense (Dinophyceae) in Scottish waters. Journal of Phycology,
45, 692703.
Dale, M., Luck, B., Fowler, H.J., Blenkinsop, S., Gill, E., Bennett, J., Kendon, E.J. and Chan, S.C.
(2015) New climate change rainfall estimates for sustainable drainage. Proceedings of the
Institution of Civil Engineers, Paper 1500030.
Davidson K., Baker C., Higgins C., Higman W., Swan S., Veszelovszki A. and Turner A.D. (2015)
Potential Threats Posed by New or Emerging Marine Biotoxins in UK Waters and Examination of
Detection Methodologies Used for Their Control: Cyclic Imines. Marine Drugs, 13(12), 7087
7112, doi:10.3390/md13127057
Davidson, K. and Bresnan, E. (2009) Shellfish toxicity in UK waters: a threat to human health?
Environmental Health, 8, (Suppl 1), S12, doi: 10.1186/1476-069X-8-S1-S12
Delegrange A., Lefebvrec , A., Gohind , F., Courcot, L., Vincent D. (2018) Pseudo-nitzschia sp.
diversity and seasonality in the southern North Sea, domoic acid levels and associated
phytoplankton communities. Estuarine, Coastal and Shelf Science, 214, 194206.
Dees P., Bresnan E., Dale A., Edwards M., Johns D., Mouat B., Whyte C and Davidson K.
(2017), Harmful algal blooms in the Eastern North Atlantic Ocean. PNAS 114(46), 97639764.
Dhanji-Rapkova, M., O’Neill, A., Maskrey, B., Coates, L., Teixeira Alves, M., Kelly, R.J., Hatfield, R.
G., Rowland-Pilgrim, S. J., Lewis, A.M., Algoet, M. and Turner A.D. (2018) Variability and
profiles of lipophilic toxins in bivalves from Great Britain during five and a half years of
monitoring: Okadaic acid, dinophysis toxins and pectenotoxins. Harmful Algae, 77, 6680.
Dhanji-Rapkova, M. O’Neill A., Maskrey B., Coates L., Swan S.C., Teixeira Alves M., Kelly R. J.,
Hatfield R. G., Rowland-Pilgrim S. J., Lewis A. M., Turner A. D. (2019). Variability and profiles
of lipophilic toxins in bivalves from Great Britain during five and a half years of monitoring:
azaspiracids and yessotoxins. Harmful Algae, 87, 101629.
Du, X., Peterson, W., Fisher, J., Hunter, M. and Peterson, J. (2016) Initiation and Development of a
Toxic and Persistent Pseudo-nitzschia Bloom off the Oregon Coast in Spring/Summer 2015. PLoS
ONE, 11(10), e0163977, https://doi.org/10.1371/journal.pone.0163977
Edwards, M., Beaugrand, G., Reid, P.C., Rowden, A.A. and Jones, M.B. (2002) Ocean climate
anomalies and the ecology of the North Sea. Marine Ecology-Progress Series, 239, 110.
Edwards, M., Johns, D.G., Leterme, S.C., Svendsen, E. and Richardson, A.J. (2006) Regional climate
change and harmful algal blooms in the northeast Atlantic. Limnology and Oceanography, 51(2),
820829.
Edwards M., Atkinson, A., Bresnan, E., Hélaouët, P., McQuatters-Gollop A., Ostle C., Pitois, S.,
Widdicombe C. (2020) Plankton, jellyfish and climate in the North-East Atlantic, MCCIP Science
Review 2020, 322353.
Eze, J. I., Scott, E. M., Pollock, K. G., Stidson, R., Miller, C. A. and Lee, D. (2014) The association of
weather and bathing water quality on the incidence of gastrointestinal illness in the west of
Scotland. Epidemiology and Infection, 142, 12891299.
Fehling J., Davidson K., Bolch, C. J. and Tett, P. (2006). Seasonality of Pseudo-nitzschia spp.
(Bacillariophyceae) in western Scottish waters. Marine Ecology Progress Series, 323, 91105.
Fewtrell, L., Kay, D., Watkins, J., Davies, C. and Francis, C. (2011) The microbiology of urban UK
floodwaters and a quantitative microbial risk assessment of flooding and gastrointestinal illness.
Journal of Flood Risk Management, 4, 7787.
Garvetto, A., Nézan, E., Badis, Y., Bilien, G., Arce, P., Bresnan, E., Gachon, C.M.M and Siano, R.
(2018) Novel Widespread Marine Oomycetes Parasitising Diatoms, Including the Toxic
Human health
MCCIP Science Review 2020 521545
543
Genus Pseudo-nitzschia: Genetic, Morphological, and Ecological Characterisation. Frontiers in
Microbiology, 9, 2918.
Gobler, C.J., Doherty, O.M., Hattenrath-Lehmann, T., Griffith, A.W., Kang, Y. and Litaker, R. W.
(2017a) Ocean warming since 1982 has expanded the niche of toxic algal blooms in the North
Atlantic and North Pacific oceans. PNAS, 114(19), 49754980.
Gobler, C.J., Hattenrath-Lehmann, T. K., Doherty, O. M., Griffith, A. W., Kang, Y. and Litaker R.W.
(2017b) Reply to Dees et al., Ocean warming promotes species-specific increases in the cellular
growth rates of harmful algal blooms. PNAS, 114(46), E9765E9766.
Gomez, F. (2013). Reinstatement of the dinoflagellate genus Tripos to reinstate Neoceratium, marine
species of Ceratium (Dinophyceae, Alveolata). CICIMAR Oceánides, 28(1), 122.
Hall, A.J. and Frame, E. (2010) Evidence of domoic acid exposure in harbour seals from Scotland: A
potential factor in the decline in abundance? Harmful Algae, 9(5), 489493.
Hallegraeff, G.M. (2010) Ocean climate change, phytoplankton community responses and harmful
algal blooms: a formidable predictive challenge. Journal of Phycology, 46(2), 220235.
Hallegraeff, G.M., Bresnan, E., Enevoldsen, H., Schweibold, L. and Zingone, A. (2017) Call to
contribute to global harmful algal bloom status reporting. Ocean Biogeographic Information
System, https://obis.org/2017/11/03/hab-report/.
Hannaford, J. (2015) Climate-driven changes in UK river flows: a review of the evidence. Progress in
Physical Geography, 39(1), 2948.
Hassard, F., Sharp, J.H., Taft, H., LeVay, L., Harris, J.P., McDonald, J.E., Tuson, K., Wilson, J., Jones,
D.L. and Malham, S.K. (2017) Critical review on the public health impact of norovirus
contamination in shellfish and the environment: a UK perspective. Food and Environmental
Virology, 9(2), 123141.
Hinder, S.L., Hays, G.C., Edwards, M., Roberts, E.C., Walne, A.W. and Gravenor, M.B. (2012)
Changes in marine dinoflagellate and diatom abundance under climate change. Nature Climate
Change, 2(4), 271275.
Holt, J., Polton, J., Huthnance, J., Wakelin, S., O’Dea, E., Harle, J., Yool, A., Artioli, Y., Blackford, J.,
Siddorn, J. and Innall, M. (2018) Climate-driven change in the North Atlantic and Arctic Oceans
can greatly reduce the circulation of the North Sea. Geophysical Research Letters, 45(11), 827
11,836, https://doi.org/ 10.1029/2018GL078878
Hooper, W.L., Barrow, G.I., and McNab, D.J.N. (1974) Vibrio parahaemolyticus food poisoning in
Britain. Lancet, 7876, 11001102.
Horsburgh K., Rennie A. and Palmer M. (2020) Impacts of climate change on sea-level rise relevant to
the coastal and marine environment around the UK. MCCIP Science Review 2020, 116131.
ICES-IOC WGHABD (2017) Report of the ICES-IOC Working Group on Harmful Algal Bloom
Dynamics 2017, ICES CM 2017/SSGEPD:11.
Isbister, G.K. and Kiernan, M.C. (2005) Neurotoxic marine poisoning. Lancet Neurology, 2005, 219
228.
Jensen, S.-K., Lacaze, J.-P., Hermann, G., Kershaw, J., Brownlow, A., Turner, A. and Hall, A. (2015)
Detection and effects of harmful algal toxins in Scottish harbour seals and potential links to
population decline. Toxicon, 97, 114.
Jones, M.R., Fowler, H.J., Kilsby, C.G. and Blenkinsop, S. (2013) An assessment of changes in
seasonal and annual extreme rainfall in the UK between 1961 and 2009. International Journal of
Climatology, 33, 11781194.
Lavers, D.A. and Villarini, G. (2015) The relationship between daily European precipitation and
measures of atmospheric water vapour transport. International Journal of Climatology, 35, 2187
2192.
Lewis, A.M., Coates, L.N., Turner, A.D., Percy, L. and Lewis, J. (2018) A review of the global
distribution of Alexandrium minutum (Dinophyceae) and comments on ecology and associated
paralytic shellfish toxin profiles, with a focus on Northern Europe. Journal of Phycology, 54, 581
598.
Lima, F.P. and Wethey, D.S. (2012) Three decades of high-resolution coastal sea surface temperatures
reveal more than warming. Nature Communications, 3, 704,
http://www.nature.com/doifinder/10.1038/ncomms1713
Lowe, J.A., Bernie, D., Bett, P., Bricheno, L, Brown, S., Calvert, D. et al. (2018) UKCP18 Science
Overview Report November 2018, Version 2.0
https://www.metoffice.gov.uk/pub/data/weather/uk/ukcp18/science-reports/UKCP18-Overview-
report.pdf
Mahaffey, C., Palmer, M., Greenwood, N. and Sharples, J. (2020) Impacts of climate change on
dissolved oxygen concentration relevant to the coastal and marine environment around the UK.
MCCIP Science Review 2020, 3153
Human health
MCCIP Science Review 2020 521545
544
Martinez-Urtaza, J. et al. (2016) Pacific Northwest genotypes of Vibrio parahaemolyticus responsible
for seafood outbreak in Spain, 2012. SpringerPlus 5, 87
McLaughlin, J.B. et al. (2005) Outbreak of Vibrio parahaemolyticus gastroenteritis associated with
Alaskan oysters. The New England Journal of Medicine, 353, 14631470
Morris, S., Stubbs, B., Brunet, C. and Davidson, K. (2010) Spatial distributions and temporal profiles
of harmful phytoplankton, and lipophilic toxins in Common mussels and Pacific oysters from four
Scottish shellfish production areas (2009). Final project report to the Food Standards Agency
Scotland (FSAS), 57 pp.
Otto, F.E.L., van der Wiel, K., van Oldenborgh, G.J., Philip, S., Kew, S.F., Uhe, P. and Cullen, H.
(2018) Climate change increases the probability of heavy rains in Northern England/Southern
Scotland like those of storm Desmonda real-time event attribution revisited. Environmental
Research Letters, 13, 024006.
Paterson, R.F., McNeill, S., Mitchell, E., Adams, T., Swan, S.C., Clarke, D., Miller, P.I., Bresnan, E.
and Davidson, K. (2017) Environmental control of harmful dinoflagellates and 2 diatoms in a
fjordic system. Harmful Algae, 69, 117.
Raven, J., Gobler, C., Hansen, P.J. (in press) Dynamic CO2 and pH levels in coastal, estuarine, and
inland waters: Theoretical and observed effects on harmful algal blooms, Harmful Algae.
https://doi.org/10.1016/j.hal.2019.03.012
Riebesell, U., Aberle-Malzahn, N., Achterberg, E.P., Algueró-Muñiz, M., Alvarez-Fernandez, S.,
Arístegui, J. et al. (2018) Toxic algal bloom induced by ocean acidification disrupts the pelagic
food web. Nature Climate Change, 8 (12), 10821086.
Rowland-Pilgrim, S., Swan, S.C., O’Neill, A., Johnson, S., Coates, L., Stubbs, P., Dean, K., Harrison,
K., Teixeira Alves, M., Walton, A., Davidson, K., Turner, A.D. and Maskrey, B. H. (2019)
Variability of Amnesic Shellfish Toxin and Pseudo-nitzschia occurrence in bivalve molluscs and
water samples Analysis of ten years of the official control monitoring programme. Harmful Algae,
87, 101623.
Scallan, E. et al. (2011) Foodborne illness acquired in the United States-Major pathogens. Emerging
Infectious Diseases, 17, 715.
Schaller, N., Kay, A.L., Lamb, R., Massey, N.R., van Oldenborgh, G.J., Otto, F.E.L. et al. (2016)
Human influence on climate in the 2014 southern England winter floods and their impacts. Nature
Climate Change, 6(6), 627634.
Semenza, J.C., Trinanes, J., Lohr, W., Sudre, B., Lofdahl, M., Martinez-Urtaza, J. et al. (2017)
Environmental Suitability of Vibrio Infections in a Warming Climate: An Early Warning System.
Environmental Health Perspectives, 125(10), 107004.
Sommer, U., Paul, C., Moustaka-Gouni, M. (2015) Warming and Ocean Acidification Effects on
PhytoplanktonFrom Species Shifts to Size Shifts within Species in a Mesocosm Experiment.
PLoS ONE, 10(5), e0125239, doi:10.1371/journal. pone.0125239
Stubbs, B., Brunet, C. and Davidson, K. (2010) Spatial distributions and temporal profiles of harmful
phytoplankton, and lipophilic toxins in Common mussels and Pacific oysters from four Scottish
shellfish production areas (2009). Final project report to the Food Standards Agency Scotland
(FSAS), 57 pp.
Swan, S.A., Turner, A.D., Bresnan, E., Whyte, C., Paterson, R.F., McNeill, S., Mitchell, E. and
Davidson, K. (2018) Dinophysis acuta in Scottish Coastal Waters and Its Influence on Diarrhetic
Shellfish Toxin Profiles. Toxins, 10, 399, doi:10.3390/toxins10100399
Tam, C.C., Rodrigues, L.C., Viviani, L., Dodds, J.P., Evans, M.R., Hunter, P.R., Gray, J.J., Letley,
L.H., Rait, G., Tompkins, D.S. and O’Brien, S.J. (2012) Longitudinal study of infectious intestinal
disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut,
61, 6977.
Tinker, J.T. and Howes, E. (2020) The impacts of climate change on temperature (air and sea), relevant
to the coastal and marine environment around the UK. MCCIP Science Review 2020, 130.
Townhill, B.L, Tinker, J., Jones, M., Pitois, S., Creach, V., Simpson, S.D., Dye, S., Bear, E. and
Pinnegar, J. (2018) Harmful algal blooms and climate change: exploring future distribution
changes. ICES Journal of Marine Science, 75(6), 18821893.
Trainer, V.L., Moore, S.K., Hallegraeff, G., Kudela, R.M., Clement, A., Mardones, J.I. and Cochlan
W. P. (2019) Harmful algal blooms and climate change: Lessons from nature’s experiments with
extremes. Harmful Algae. https://doi.org/10.1016/j.hal.2019.03.009
Turner, A.D., Stubbs, B., Coates, L., Dhanji-Rapkova, M., Hatfield, R.G., Lewis, A.M., Rowland-
Pilgrim, S., O’Neil, A., Stubbs, P., Ross, S., Baker, C. and Algoet, M. (2014) Variability of paralytic
shellfish toxin occurrence and profiles in bivalve molluscs from Great Britain from official control
monitoring as determined by pre-column oxidation liquid chromatography and implications for
applying immunochemical tests, Harmful Algae, 31, 8799.
Human health
MCCIP Science Review 2020 521545
545
Turner, A.D., Powell, A., Schofield, A., Lees, D.N. and Baker-Austin, C. (2015a) Detection of the
pufferfish toxin tetrodotoxin in European bivalves, England, 2013-2014. Eurosurveillance, 20(2).
Turner, A., Higgins, C., Davidson, K., Veszelovszki, A., Payne, D., Hungerford, J. and Higman W.
(2015b) Potential threats posed by new or emerging marine biotoxins in UK waters and examination
of detection methodology used in their control: Brevetoxins. Marine Drugs, 13(3), 12241254,
doi:10.3390/md13031224
Turner, A.D., Dhanji-Rapkova, M., Coates, L., Bickerstaff, L., Milligan S., O’Neill A., Faulkner, D.,
McEneny, H., Baker-Austin, C., Lees, D.N. and Algoet, M. (2017) Detection of tetrodotoxin
shellfish poisoning (TSP) toxins and causative factors in bivalve molluscs from the UK. Marine
Drugs, 15(9), 277, doi: 10.3390/md15090277
Turner A.D., Dhanji-Rapkova, M., Dean, K., Milligan, S., Hamilton, M., Thomas, J., Poole, C.,
Haycock, J., Spelman-Marriot, J., Watson, A., Hughes, K., Marr, B., Dixon, A. and Coates, L.
(2018a) Fatal canine intoxications linked to the presence of saxitoxins in stranded marine
organisms following winter storm activity. Toxins, 10, 94. doi:10.3390/toxins10030094
Turner, A.D., Fenwick, D., Powell, A., Dhanji-Rapkova, M., Ford, C., Hatfield, R., Santos, A.,
Martinez-Urtaza, J. and Bean, T.P. (2018b) New invasive nemertean species (Cephalothrix simula)
in England with high levels of tetrodotoxin and a microbiome linked to toxin metabolism. Marine
Drugs, 16(452), 120.
UKCP09 (2017) UKCP09 Projections Change in sea surface temperature (ºC) by 2085, compared to
1975, medium emissions scenario summer. http://marine.gov.scot/maps/1452.
Vezzulli, L., Grande, C., Reid, P.C., Helaouet, P., Edwards, M., Hofle, M. G., Brettar, I., Colwell, R.
and Pruzzo, C. (2016) Climate influence on Vibrio and associated human diseases during the past
half centaur in the coastal North Atlantic. PNAS, 113(34), E5062E5071,
doi/10.1073/pnas.1609157113
Watts, G. et al. (2015) Climate change and water in the UK past changes and future prospects.
Progress in Physical Geography, 39(1), 628.
Wells, M.L., Trainer, V.L., Smayda, T.J., Karlson, B.S.O., Trick, C.G., Kudela, R.M., Ishikawa, A.,
Bernard, S., Wulff, A., Anderson, D.M. and Cochlan, W.P. (2015) Harmful algal blooms and
climate change: learning from the past and present to forecast the future. Harmful Algae, 49, 68
93.
Whyte, C., Swann, S. and Davidson, K. (2014) Changing wind patterns linked to unusually high
Dinophysis blooms around the Shetland Islands, Scotland. Harmful Algae, 39, 365373.
Willis, C., Papathanasopoulou, E., Russel, D. and Artioli, Y. (2018) Harmful algal blooms: the impacts
on cultural ecosystem services and human well-being in a case study setting, Cornwall, UK. Marine
Policy, 97, 232238.
Wiltshire, K. H., Malzahn, A. M., Greve, W., Wirtz, K., Janisch, S., Mangelsdorf, P., Manly, B. F. J.
and Boersma, M. (2008), Resilience of North Sea phytoplankton spring bloom dynamics: An
analysis of long-term data at Helgoland Roads. Limnol. Oceanogr., 53, 1294-302.
Wolf, J., Woolf, D. and Bricheno, L. (2020) Impacts of climate change on storms and waves relevant
to the coastal and marine environment around the UK. MCCIP Science Review 2020, 132157.
WWF (2017) Flushed away. How sewage is still polluting the rivers of England and Wales.
https://www.wwf.org.uk/sites/default/files/2017-12/Flushed%20Away__Nov2017.pdf
... HABs produce major economic impacts: damages on commercial fisheries, aquaculture and touristic industries, increasing monitoring and risk management costs, medical expenditure and productivity loss in case of large-scale impact on human health (Hoagland et al., 2002;Sanseverino et al., 2016). Despite increasing research, the extent and intensity of HAB outbreaks remain difficult to predict due to the complexity of processes involving multi-factor and multi-scale causes and effects (Kahru et al., 2020;Bresnan et al., 2020). However, this is of particular importance when considering the vulnerability of coastal industries to HABs. ...
... Two factors (DSP and ASP) linked to HABs explained nearly all closure decisions (90%) that were taken by the public authorities during the sample period. This would mean that HABs remain a hot issue for shellfish farmers and public managers, far beyond any other hazard, including oil spills or microbiological pollutants (McGowan 2016;Basti et al., 2018;Bresnan et al., 2020). ...
... Ecological and economic analyses of HAB events have been usually developed independently. The drivers of HAB occurrence and diffusion is left to ecological studies (O'Neil et al., 2012;Paerl et al., 2011;Lassus et al., 2016;Glibert and Burkholder 2018;Kahru et al., 2020;Bresnan et al., 2020), while economists are more interested in assessing the consequences in terms of welfare loss and employment (Hoagland et al., 2002;Sanseverino et al., 2016;Adams et al., 2018). The present research aims at looking at ecological phenomena through the eyes of public decision makers and shellfish farmers. ...
Chapter
This chapter provides the first overview of the disruptive impacts of HABs on the blue economy, with a particular focus on the application of science and technology in their management and mitigation. We present case studies of HABs in five different locations as examples of their effects on different sectors of the blue economy. We also review the main technological advances in recent decades, and current needs for improved understanding of HAB dynamics, monitoring, and forecasting. An evident gap in dealing with HABs in the frame of the blue economy is the inequity in resources available for monitoring worldwide. While developed countries count on advanced (and even impressive) tools for monitoring and early warning (e.g., automated tools, oceanographic moored instruments, forecast models), efficient monitoring in most developing countries is still missing and, when performed, mainly focused on seafood products intended for export. Basic research on HABs in these countries is also frequently deficient, with modeling capabilities for early warning virtually non-existent. Considering that many (truly) sustainable blue economy activities are developed precisely in vulnerable areas with low economic power, the need for the development of affordable and sustainable technologies becomes critical, allowing for the efficient monitoring of HABs.
... Although temperature is a key driver, the impact of climate change on HABs is complex due to the irregular influence of extreme weather events and nutrient runoff pollution from land, in addition to the potential influence of large-scale ocean currents (Wells et al., 2015). In recent years, the areas most affected include the south-eastern North Sea, west coast of Scotland and Northern isles, and some coastal waters of the Celtic Seas, although monitoring is often linked to risk management reporting for shellfish and aquaculture activities (Bresnan et al., 2020). Pollutant runoff and associated turbidity, both of which may be affected by increased heavy rainfall events, can also affect shallow-water seagrass habitats which have high biodiversity and ecosystem service value. ...
... For example, fish gill disease is a notable problem for aquaculture, and this can occur from parasite, virus, or bacterial sources, with elevated temperatures and high salinity noted as exacerbating risk factors (Boerlage et al., 2020). Increasing risks from problem species and pathogens have also been identified through their importance for human health protection (e.g., Vibrio bacteria in shellfish) and threats to commercially important marine species, especially bivalve shellfish (e.g., oysters) (Danovaro et al., 2011;Bresnan et al., 2020). ...
... It is also possible that increased runoff and discharge of pollutants from land (both point sources such as sewerage systems and diffuse sources as from agriculture) due to heavier rainfall events could increase risk from pathogens, as is occurring with excess nutrient runoff and Harmful Algal Blooms in coastal waters (Bresnan et al., 2020). In addition to biodiversity impacts this can have adverse impacts for fisheries, especially for shellfish. ...
Technical Report
Full-text available
The CCRA is a comprehensive assessment of the risks to the UK from climate change, as required by Act of Parliament every 5 years (Climate Change Act)
... This in turn leads to an increase in STX present in the water, which can reach concentrations high enough to impact human and animal health. Some of the changing environmental conditions linked with HAB initiation include temperature, water column stability, turbidity, nutrient input, grazing pressure, ocean acidification and wind mediated transport (Bresnan et al., 2020). It is currently unknown if individual cells contain different levels of STX, however toxin content appears to be linked to nutritional status (Han et al., 2016;Yang et al., 2011). ...
... Other coastal activities also suffer losses during HAB events, including tourism and recreation, with total global loses attributed to HABs in the marine environment estimated to be >US$2 billion annually (Kudela et al., 2015). In the UK during recent years when higher temperatures have been recorded, a coinciding increase in HAB species is expected (Bresnan et al., 2020). These changes have been linked to anthropogenic factors such as sea surface temperature, light, and nutrient input (nitrogen, phosphorous and silica). ...
... Additionally, it has been observed that a transition from succession of different species to a homogenised mix of species has occurred (Nohe et al., 2020). In addition, increased windspeeds shown to influence increases in diatom Pseudonitszchia and the dinoflagellate Tripos (Bresnan et al., 2020). Global extreme HAB outbreaks at been reported in recent years that have had major impacts on local ecology and aquaculture industries. ...
Thesis
Unsafe water, poor hygiene and inadequate sanitation are responsible for about 90% of diarrheal associated deaths worldwide, which are the second leading cause of death in children under five, globally (1.2 million deaths in 2005). The economic cost associated with unsafe water is also significant, with the World Bank estimating that a lack of access to safe water and sanitation amount to equivalent global economic losses of US$260 billion, annually. Coastal communities also face challenges from harmful algal blooms, which deplete oxygen and essential nutrients, and produce toxins that threaten human health; this impacts on locally important industries such as aquaculture, mariculture, leisure and tourism. Current, widely used methods for the detection of biological hazards in water sources rely on culturing or visual inspection of water samples via light microscopy. These techniques are time consuming, require well stocked laboratories and expensive equipment, are dependent on highly trained technical staff, and are often unable to differentiate morphologically similar organisms. Molecular techniques, on the other hand can provide better discrimination between related taxonomical groups, and are suited for miniaturisation and automation, enabling the analysis to be undertaken outside of the laboratory, and by minimally trained personnel. Recent advances in microfluidic technologies have demonstrated that molecular-biology techniques (e.g. genetic sequence amplification and detection) can be applied using lab-on-a-chip (LOC) systems for testing samples for the target organisms at the ‘point of sample’ or ‘point of care’. Nucleic acid sequence-based amplification (NASBA) and recombinase polymerase amplification (RPA) are particularly attractive for LOC applications as, unlike the current gold standard Polymerase Chain Reaction (PCR), they require simple, isothermal heating and a generally lower reaction temperature. NASBA is also attractive for LOC-based methods targeting RNA (e.g. RNA viruses) as it directly amplifies RNA removing the need for an additional reverse transcription step. This study indicates several, novel advances towards the provision of point of sample genetic testing for a range of harmful microorganisms and viruses. For the first time, the isothermal amplification of a fragment of the Hepatitis E virus using NASBA is reported with comparable sensitivity to a clinically relevant PCR-based assay. Further, amplification of a fragment of the Alexandrium minutum ITS1-5.8s-ITS2 rRNA gene region via RPA was achieved with a limit of detection of 10 cells exceeding the required sensitivity of 40 cells L-1 for statutory A. minutum surveillance in seawater. In addition to this, two methods for the long-term, dry storage of amplification reagents are presented. Trehalose and sucrose sugars combined with lyophilisation were sufficient to retain reagent activity after storage for four weeks at room temperature. Air drying in the presence of pullulan maintained reagent functionality for six weeks. Alongside these advances, a portable, handheld prototype concept for nucleic acid amplification was developed and tested, with the A. minutum ITS1-5.8s-ITS2 RPA assay being successfully performed on the handheld device achieving the same sensitivity as when performed on laboratory equipment. These advances demonstrate that nucleic acid amplification on a miniaturised device is possible, and that in future, rapid, specific and sensitive testing for harmful species may be able to be performed at the point of sample by non-technically trained operators.
... HABs produce major economic impacts: damages on commercial fisheries, aquaculture and touristic industries, increasing monitoring and risk management costs, medical expenditure and productivity loss in case of large-scale impact on human health (Hoagland et al., 2002;Sanseverino et al., 2016). Despite increasing research, the extent and intensity of HAB outbreaks remain difficult to predict due to the complexity of processes involving multi-factor and multi-scale causes and effects (Kahru et al., 2020;Bresnan et al., 2020). However, this is of particular importance when considering the vulnerability of coastal industries to HABs. ...
... Two factors (DSP and ASP) linked to HABs explained nearly all closure decisions (90%) that were taken by the public authorities during the sample period. This would mean that HABs remain a hot issue for shellfish farmers and public managers, far beyond any other hazard, including oil spills or microbiological pollutants (McGowan 2016;Basti et al., 2018;Bresnan et al., 2020). ...
... Ecological and economic analyses of HAB events have been usually developed independently. The drivers of HAB occurrence and diffusion is left to ecological studies (O'Neil et al., 2012;Paerl et al., 2011;Lassus et al., 2016;Glibert and Burkholder 2018;Kahru et al., 2020;Bresnan et al., 2020), while economists are more interested in assessing the consequences in terms of welfare loss and employment (Hoagland et al., 2002;Sanseverino et al., 2016;Adams et al., 2018). The present research aims at looking at ecological phenomena through the eyes of public decision makers and shellfish farmers. ...
Article
Harmful Algal Blooms (HAB) events may have serious economic consequences for shellfish farmers. When toxic algae blooms threaten human health, public authorities may decide to shut down the farming business for a while, i.e. ranging from a few days to several weeks or months, according to the severity of risks. The impact of closures being temporally and spatially distributed, shellfish farmers can avoid the risky zones or develop adaptive strategies to mitigate the economic consequences and therefore reduce significantly their business sensitivity to HABs. A sequential approach by optimal matching analysis is applied to an original data set of shellfish area closure decrees between April 2004 and December 2018 in Southern Brittany and Pays de la Loire (France) to build a typology of 79 aquaculture zones affected by various HAB and microbiological hazards (ASP, DSP, Norovirus, E. Coli, oil spills). The hypothesis is that the degree of exposure to the HAB hazard assessed by zonal closures may not be correlated to the level of sensitivity revealed by the economic results of the shellfish farming industry which can develop avoidance strategies.
... Algal Blooms (HABs) concern numerous species that are still under study to assess the complex co-effects of various environmental conditions (freshwater input, temperature increase, eutrophication) to either cells' proliferation or toxins production (Bresnan et al., 2020). For instance, climate change is being predicted to worsen eutrophication's impacts on water quality (Nazari-Sharabian et al., 2018) and to accentuate both intensity and frequency of HABs (Griffith & Gobler, 2020;Gobler, 2020 (Ulén et al., 2007;Tynkkynen et al., 2014;Grizzetti et al., 2021). ...
Thesis
Les écosystèmes côtiers font face à un environnement changeant qu’il soit d’origine naturelle ou anthropique. Le phytoplancton, à la base des réseaux trophiques marins, se situe au coeur du fonctionnement des écosystèmes. L’objectif de cette thèse s’intègre dans le cadre du projet S3-EUROHAB, et vise à évaluer la variabilité spatio-temporelle des communautés phytoplanctoniques au sein de divers systèmes de Manche Est, notamment en Baie de Seine. Pour répondre à ces objectifs, des approches allant de la physiologie à la communauté, et des unités taxonomiques aux caractéristiques fonctionnelles ont été explorées. Si l’approche communautaire permet de rendre compte du faible niveau de déviation inter-annuel au sein des assemblages phytoplanctoniques, elle révèle également des différenciations spatiales où chaque communauté est sous forte influence des facteurs environnementaux locaux. Ces patrons de variabilité spatiale sont également retrouvés au travers de l’approche fonctionnelle. Par ailleurs, la relation traits-environnement permet d’étudier l’adéquation entre stratégies fonctionnelles et distribution environnementale (niche écologique). Les résultats montrent que, malgré la forte diversité des organismes étudiés et le choix de traits, des taxons partageant des similarités fonctionnels partagent également des niches écologiques similaires. En complément d’une approche fonctionnelle communautaire, une approche expérimentale a été développée afin d’évaluer la plasticité du phytoplancton, notamment de contenus intracellulaires. Cette dernière révèle ainsi des adaptations spatiales et temporelles des teneurs en lipides et en chlorophylle-a des organismes phytoplanctoniques, en réponse aux besoins en lumière et pour le maintien du bon fonctionnement de la cellule selon les gradients environnementaux. Enfin, la relation entre les facteurs environnementaux et la dynamique de deux taxons toxiques Dinophysis sp. et Pseudo-nitzschia sp. a été étudiée. Dans un premier temps, cela met en évidence entre autre l’affinité de Dinophysis sp. avec l’augmentation de température et la stratification qu’elle induit au sein de deux environnements contrastés ; britannique et français. Dans un second temps, les circonstances des efflorescences de Pseudo-nitzschia sp. suggèrent l’existence de pressions biotiques contraignantes et possiblement causes des épisodes de toxicités observées de 2011 à 2014.
... The coincidence of geographical distribution of DSTs with nearby high precipitation quotas can also be observed on other North Atlantic coasts, such as the UK (Bresnan et al. 2020;Mayes and Wheeler 2013) and Ireland (Sweeney 2014;Salas and Clarke 2019). In Atlantic Spain, the Galician Rias are appropriate for large-scale mussel farming but are located in the rainiest part of peninsular Spain (Martinez-Artigas et al. 2020). ...
Article
Full-text available
In continental Portugal, high levels of diarrhetic shellfish poisoning toxins (DSTs) and paralytic shellfish poisoning toxins (PSTs) can be accumulated in bivalves. DSTs presented maxima during the dry summer season and were linearly related to precipitation accumulated over the previous months. Precipitation is highest on the northwest (NW) than on the southwest (SW) or south (S) coasts. An NW to S decreasing gradient in DSTs is commonly found. An NW to S decreasing gradient can also be found for some macronutrients (N, P and Si). Coastal fertilisation also favoured contamination with ASTs (amnesic shellfish poisoning toxins) and PSTs mainly on the NW coast, followed by the SW coast, with the lowest contaminations found on the S coast. Despite its marked autumnal seasonality, PSTs were unpredictable interannually. High PST’s contamination was coincidental with the last four solar minima periods of the 11-year sunspot cycle. On the opposite, ASTs increased slightly during maxima of geomagnetic activity (GMA). AST incidence in April and October was 2.7 times higher when GMA was above the monthly average (18.5 nT) in March and September, respectively. In the last two decades (2001–2020), average DST levels in June + July reduced after 2008, following a trend in the reduction of precipitation after 2003. Nevertheless, no trends were observed in the average percentage of samples exceeding annually the regulatory limit (PSEARL) for DSTs (18.4%) due to the high percentage of indicator-species analysed, which maintain DSTs for a prolonged time. Despite the low average PSEARL of 1.0% for ASTs during 2001–2013, it reduced to 0.4% in 2014–2020. This might have been coincidental with a global change in the northern hemisphere ocean temperature anomaly in 2014 or with weaker GMA stimulation during the weaker solar cycle 24. Due to the large interannual variability in PSTs associated with the solar cycle, no average PSEARL can be defined and no clear trends can be associated with global change.
... increasingly also being present (Bresnan et al., 2020;Davidson et al., 2012;Davidson et al., 2009;Touzet et al., 2010). Spatial and temporal variation in the patterns of HABs in the North Sea have also been reported (Bresnan et al., 2013;Edwards et al., 2006;Martino et al., 2020). ...
Article
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The marine nemertean Cephalothrix simula originates from the Pacific Ocean but in recent years has been discovered in northern Europe. The species has been associated with high levels of the marine neurotoxin Tetrodotoxin, traditionally associated with Pufferfish Poisoning. This study reports the first discovery of two organisms of C. simula in the UK, showing the geographical extent of this species is wider than originally described. Species identification was initially conducted morphologically, with confirmation by Cox 1 DNA sequencing. 16S gene sequencing enabled the taxonomic assignment of the microbiome, showing the prevalence of a large number of bacterial genera previously associated with TTX production including Alteromonas, Vibrio and Pseudomonas. LC-MS/MS analysis of the nemertean tissue revealed the presence of multiple analogues of TTX, dominated by the parent TTX, with a total toxin concentration quantified at 54 µg TTX per g of tissue. Pseudomonas luteola isolated from C. simula, together with Vibrio alginolyticus from the native nemertean Tubulanus annulatus, were cultured at low temperature and both found to contain TTX. Overall, this paper confirms the high toxicity of a newly discovered invasive nemertean species with links to toxin-producing marine bacteria and the potential risk to human safety. Further work is required to assess the geographical extent and toxicity range of C. simula along the UK coast in order to properly gauge the potential impacts on the environment and human safety.
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As the official control laboratory for marine biotoxins within Great Britain, the Centre for Environment, Fisheries and Aquaculture Science, in conjunction with the Scottish Association for Marine Science, has amassed a dec-ade's worth of data regarding the prevalence of the toxins associated with Amnesic Shellfish Poisoning within British waters. This monitoring involves quantitative HPLC-UV analysis of shellfish domoic acid concentration, the causative toxin for Amnesic Shellfish Poisoning, and water monitoring for Pseudo-nitzschia spp., the phy-toplankton genus that produces domoic acid. The data obtained since 2008 indicate that whilst the occurrence of domoic acid in shellfish was generally below the maximum permitted limit of 20 mg/kg, there were a number of toxic episodes that breached this limit. The data showed an increase in the frequency of both domoic acid occurrence and toxic events, although there was considerable annual variability in intensity and geographical location of toxic episodes. A particularly notable increase in domoic acid occurrence in England was observed during 2014. Comparison of Scottish toxin data and Pseudo-nitzschia cell densities during this ten-year period revealed a complex relationship between the two measurements. Whilst the majority of events were associated with blooms, absolute cell densities of Pseudo-nitzschia did not correlate with domoic acid concentrations in shellfish tissue. This is believed to be partly due to the presence of a number of different Pseudo-nitzschia species in the water that can exhibit variable toxin production. These data highlight the requirement for tissue monitoring as part of an effective monitoring programme to protect the consumer, as well as the benefit of more detailed taxonomic discrimination of the Pseudo-nitzschia genus to allow greater accuracy in the prediction of shellfish toxicity.