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Marine aquaculture relies on coastal habitats that will be affected by climate change. This review assesses current knowledge of the threats and opportunities of climate change for aquaculture in the UK and Ireland, focusing on the most commonly farmed species, blue mussels (Mytilus edulis) and Atlantic salmon (Salmo salar). There is sparse evidence to indicate that climate change is affecting aquaculture in the UK and Ireland. Impacts to date have been difficult to discern from natural environmental variability, and the pace of technological development in aquaculture overshadows effects of climatic change. However, this review of broader aquaculture literature and the likely effects of climate change suggests that over the next century, climate change has the potential to directly impact the industry. Impacts are related to the industry's dependence on the marine environment for suitable biophysical conditions. For instance, changes in the frequency and strength of storms pose a risk to infrastructure, such as salmon cages. Sea-level rise will shift shoreline morphology, reducing the areal extent of some habitats that are suitable for the industry. Changes in rainfall patterns will increase the turbidity and nutrient loading of rivers, potentially triggering harmful algal blooms and negatively affecting bivalve farming. In addition, ocean acidification may disrupt the early developmental stages of shellfish. Some of the most damaging but least predictable effects of climate change relate to the emergence, translocation and virulence of diseases, parasites and pathogens, although parasites and diseases in finfish aquaculture may be controlled through intervention. The spread of nuisance and non-native species is also potentially damaging. Rising temperatures may create the opportunity to rear warmer water species in the UK and Ireland. Market forces, rather than technical feasibility, are likely to determine whether existing farmed species are displaced by new ones.
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Review of climate change impacts on marine aquaculture in the UK
and Ireland
RUTH CALLAWAY
a,
*, ANDREW P. SHINN
d
, SUZANNE E. GRENFELL
c
, JAMES E. BRON
d
, GAVIN BURNELL
e
,
ELIZABETH J. COOK
f
, MARGARET CRUMLISH
d
, SARAH CULLOTY
e
, KEITH DAVIDSON
f
, ROBERT P. ELLIS
g
,
KEVIN J. FLYNN
a,b
, CLIVE FOX
f
, DARREN M. GREEN
d
, GRAEME C. HAYS
a
, ADAM D. HUGHES
f
,
ERIN JOHNSTON
e
, CHRISTOPHER D. LOWE
a
, INGRID LUPATSCH
b
, SHELAGH MALHAM
h
,
ANOUSKA F. MENDZIL
c
, THOM NICKELL
f
, TOM PICKERELL
i
, ANDREW F. ROWLEY
a
, MICHELE S. STANLEY
f
,
DOUGLAS R. TOCHER
d
, JAMES F. TURNBULL
d
, GEMMA WEBB
a,b,g
, EMMA WOOTTON
a
and ROBIN J. SHIELDS
b
a
Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea, SA2 8PP, UK
b
Centre for Sustainable Aquatic Research, Swansea University, Singleton Park, Swansea, SA2 8PP, UK
c
Department of Geography, College of Science, Swansea University, Singleton Park, Swansea, SA2 8PP, UK
d
Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK
e
Aquaculture & Fisheries Development Centre, University College Cork, Cooperage Building, Distillery Fields, North Mall, Cork, Ireland
f
Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, PA37 1QA, UK
g
Plymouth Marine Laboratory, Prospect Place, West Hoe, Plymouth, PL1 3DH, UK
h
School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, UK
i
Shellsh Association of Great Britain, FishmongersHall, London Bridge, London EC4R 9EL, UK
ABSTRACT
1. Marine aquaculture relies on coastal habitats that will be affected by climate change. This review assesses
current knowledge of the threats and opportunities of climate change for aquaculture in the UK and Ireland,
focusing on the most commonly farmed species, blue mussels (Mytilus edulis) and Atlantic salmon (Salmo salar).
2. There is sparse evidence to indicate that climate change is affecting aquaculture in the UK and Ireland.
Impacts to date have been difcult to discern from natural environmental variability, and the pace of
technological development in aquaculture overshadows effects of climatic change. However, this review of
broader aquaculture literature and the likely effects of climate change suggests that over the next century,
climate change has the potential to directly impact the industry.
3. Impacts are related to the industrys dependence on the marine environment for suitable biophysical
conditions. For instance, changes in the frequency and strength of storms pose a risk to infrastructure, such as
salmon cages. Sea-level rise will shift shoreline morphology, reducing the areal extent of some habitats that are
suitable for the industry. Changes in rainfall patterns will increase the turbidity and nutrient loading of rivers,
potentially triggering harmful algal blooms and negatively affecting bivalve farming. In addition, ocean
acidication may disrupt the early developmental stages of shellsh.
4. Some of the most damaging but least predictable effects of climate change relate to the emergence, translocation
and virulence of diseases, parasites and pathogens, although parasites and diseases in nsh aquaculture may be
controlled through intervention. The spread of nuisance and non-native species is also potentially damaging.
5. Rising temperatures may create the opportunity to rear warmer water species in the UK and Ireland. Market forces,
rather than technical feasibility, are likely to determine whether existing farmed species are displaced by new ones.
Copyright #2012 John Wiley & Sons, Ltd.
Received 30 September 2011; Revised 29 February 2012; Accepted 15 March 2012
KEY WORDS: aquaculture; climate change; pollution; water quality; disease; sh; invertebrates; algae; coastal; littoral; estuary; habitat
*Correspondence to: R. Callaway, Department of Biosciences, College of Science, Swansea University, Singleton Park, Swansea, SA2 8PP, UK.
E-mail: r.m.callaway@swansea.ac.uk
Copyright #2012 John Wiley & Sons, Ltd.
AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. 22: 389421 (2012)
Published online 7 May 2012 in Wiley Online Library
(wileyonlinelibrary.com). DOI: 10.1002/aqc.2247
INTRODUCTION
Aquaculture is the cultivation of aquatic organisms,
usually for the purposes of human consumption. It
implies a level of intervention in the rearing process
to enhance survival rates and production through a
combination of regular feeding, the provision of
substratum or through protection from predators
(FAO, 2002). Freshwater, brackish and seawater
environments are all exploited for aquaculture,
ranging from hatcheries located on freshwater
rivers, to estuaries, fjords, and open bays.
There is a close relationship between prevailing
environmental conditions and the success of
aquaculture production. This is largely because the
health of both nsh and shellsh is heavily
dependent on environmental conditions, such as
temperature, salinity, oxygen solubility and
dissolved waste products (Mydlarz et al., 2006).
Additionally, the physical processes of waves, tides,
rivers, and associated erosion or deposition may
alter the suitability of the abiotic environment. The
distribution of a specic species is limited by its
tolerance range to local environmental variables.
Towards the edge of its tolerance ranges, a species
may become immuno-compromised, such that
it becomes more susceptible to disease or to
predation. In addition, changes in the environment
may have direct or indirect effects on the abundance
of parasites and pathogens (Karvonen et al., 2010),
or the success of predatory and competitor species,
either native or introduced.
The success of aquaculture is fundamentally
dependent on the complex ecology of the aquatic
environment, which is a major concern considering
the wide ranging impacts of climate change (IPCC,
2007). Aquaculture facilities are often located in
areas which are likely to bear the brunt of climate
change impacts: coasts and estuaries are susceptible
to changes in water temperature, storm intensity or
frequency and sea level. On a more complex level,
shifts in the aquatic ecosystem will impact upon
relationships between prey, predators, parasites, and
pathogens. In rivers and estuaries, changes to ood
frequency and magnitude are an additional concern,
especially because of the sediments, nutrients,
pathogens and contaminants associated with run-off.
Extent, value and types of marine aquaculture in the
UK and Ireland
Marine aquaculture in the UK and Ireland can be
broadly divided into the shellsh and the nsh
sectors (Figure 1, Tables 1 and 2). Finsh
aquaculture sites are clustered towards the north
of the UK on the Western Scottish Highlands,
Argyll, the Hebrides and Northern Isles. The
western coasts of Ireland and Northern Ireland are
characterized by a high concentration of shellsh
sites as well as signicant nsh production, while
in England and Wales shellsh aquaculture
predominates (Figure 2).
Scotland leads marine nsh aquaculture,
producing over 90% of the UK and Irelands
marine nsh (Table 1; BIM, 2009; Cefas, 2011a).
Ireland is the second largest nsh producer. While
freshwater sh are cultivated in Northern Ireland
and England, marine nsh production is
negligible. In 2009, no marine nsh production
was recorded in offshore areas for Wales.
Ireland produces almost half of the UK and
Irelands shellsh (Table 2; BIM, 2009; Cefas,
2011b), followed by Wales with 20%. Northern
Ireland, England and Scotland share the
remaining 30% fairly evenly.
Dominant species cultivated vary from region to
region. In Scotland, Atlantic salmon (Salmo salar)
accounts for 98% of Scottish marine nsh
aquaculture at an estimated annual economic value
of £ 412 million (Scottish Government, 2010). In
addition to Atlantic salmon, small volumes of
halibut (Hippoglossus hippoglossus) and rainbow
trout (Oncorhynchus mykiss) are also produced in
offshore areas (Table 1). In terms of shellsh, the
Scottish industry is dominated by mussels (Mytilus
edulis), followed by lesser volumes of Pacicoysters
(Crassostrea gigas), native oysters (Ostrea edulis),
queen scallops (Aequipecten opercularis)and
scallops (Pecten maximus).
In contrast, Irish aquaculture produces far more
shellsh than marine nsh. Mussels accounted for
almost 80% of Irish shellsh production, followed
by Pacic oysters, native oysters, clams and scallops
(Table 2). Finsh produced were primarily Atlantic
salmon (96.23%) in addition to small volumes of sea
reared trout (3.77%). Although Ireland produces
more shellsh than nsh, the nsh sector has a
higher economic value. Irish nsh was valued at
72.0 million compared with 34.6 million for
shellsh (BIM, 2009).
England, Northern Ireland and Wales produce
very little marine nsh, and instead focus on
onshore rearing of freshwater nsh species such
as rainbow trout (Cefas, 2011a). As freshwater
species and onshore aquaculture are not the focus
of this review, they have been omitted here. In
R. CALLAWAY ET AL.390
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Table 1. Marine nsh production in the UK and Ireland (BIM, 2009; Cefas, 2011a)
Total volume (tonnes) by region
Total production by
species (tonnes)
Percentage of total
production by species (%)
England Wales Scotland Northern
Ireland
Ireland
Turbot 1 ... ... ... ... 1<0.01
Halibut ... ... 189 ... ... 189 0.1
Atlantic salmon ... ... 144 247 407 12 210 156 864 97.9
Rainbow trout or sea
reared trout*
... ... 2620 ... 478 3098 1.9
Total production
by region (tonnes)
1 0 147 056 407 12 688 160 152
Percentage of total
production by region (%)
<0.01 0.0 91.8 0.3 7.9
*This gure includes rainbow trout produced in cages in sea water in offshore areas, as well as Irish sea reared trout.
Table 2. Marine shellsh production in the UK and Ireland in 2009 (BIM 2009; Cefas, 2011b)
Total volume (tonnes) by region
Total production by
species (tonnes)
Percentage of total
production by species (%)
England Wales Scotland Northern
Ireland
Ireland
Pacic oyster 811 4 232 309 6,488 7,844 11.3
Native oyster 54 0 39 127 358 578 0.8
Scallops 0 ... 4... 55 59 0.1
Queen scallops ... ... 6... ... 6 0.0
Mussels 3800 13 812 6302 8015 26 502 58 431 84.5
Clams 13 ... ... 1 162 176 0.3
Cockles 2027 ... ... ... ... 2027 2.9
Total production by region (tonnes) 6705 13 816 6583 8452 33 566 69 122
Percentage of total production by
region (%)
9.7 20.0 9.5 12.2 48.6
Figure 1. In the UK and Ireland, mussels (Mytilus edulis) and Atlantic salmon (Salmo salar) are the most commonly farmed marine species. Conventional
cultivation and harvesting techniques are illustrated; (a) mussel dredge; (b) mussel raft; (c) salmon pens; (d) seaweed aquaculture (Saccharina latissima)
provides potential for expansion of the UK and Ireland aquaculture industries. (Source of images: Ruth Callaway a, b, c; Michele Stanley d.)
CLIMATE CHANGE AND MARINE AQUACULTURE IN THE UK AND IRELAND 391
Copyright #2012 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 22: 389421 (2012)
these parts of the UK marine aquaculture is
shellsh dominated, with mussels representing the
greatest proportion of production in all three
regions (Table 2).
Aim of review
The aim of this review is to establish the state of
knowledge with regards to the impact of climate
change on marine aquaculture in the UK and
Ireland, and to highlight areas where further
research is required to inform future policy and
decision-making (Figure 3). This review, initiated
by the UK Marine Climate Change Impact
Partnership (MCCIP), considers UK and Irish
aquaculture industries that utilize coastal habitats
to farm marine species for human consumption,
with a particular focus on Atlantic salmon and
blue mussel farming.
The level of human intervention varies between
farming processes. For instance, mussel farming
can be a relatively low intervention technique
limited to the relocation or settlement of wild spat
at sites suitable in terms of food supply and shelter
from storm and wave damage. There is though
an increasing requirement for management in
rope cultured mussel production as sites
increase in size and stock management becomes
more sophisticated to optimize growth, minimize
fouling and maximize spat fall. Salmon farming in
pens or cages is tightly managed as stock densities
and feeding is controlled, and sh are given
protection from predators. Although farmed
salmon are not dependent on natural resources,
successful aquaculture is completely reliant on the
abiotic environment in which it is conducted.
Marine species that are reared in land-based
recirculating aquaculture systems are not directly
affected by climate change and have not been
considered in this review.
The review begins by assessing the impact climate
change will have on culture environments, and
investigates what is known about effects of
ocean acidication. The physiology, health and
epidemiology of aquaculture species is then discussed
against a backdrop of environmental change. The
review also highlights how interactions between
nuisance and harmful species and aquaculture
species could change in future climates.
While this review focuses on the direct effects of
climate change on aquaculture, it is acknowledged
that indirect effects play an important role. The
aquaculture industry is driven by a complex set
of economic, operational and socio-economic
parameters, ranging from market demand to
nancial support, cost of energy, state of wild
sh stocks and land and property values
(Young, 2001; Whitmarsh and Palmieri, 2008).
Many of these factors are inuenced by climate
change and will in turn affect the progress of the
UK and Irish aquaculture industry. It is beyond
the scope of this paper to deal with all of these
issues, but given the importance of sh feed supply
for aquaculture, the last section of this review is
dedicated to the subject of global shmeal and sh
oil resources.
IMPACT OF CLIMATE CHANGE ON
ENVIRONMENTS SUITABLE FOR
AQUACULTURE
Marine aquaculture sites generally make use of
naturally existing coastal habitats that are suitable
for the target species. As such, species accustomed
to sea water and the daily rhythm of tides and
Figure 2. Geographical distribution of marine shellsh (blue symbols)
and nsh (black symbols) aquaculture production facilities in the
UK and Ireland.
R. CALLAWAY ET AL.392
Copyright #2012 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 22: 389421 (2012)
waves are typically grown in estuaries and shallow
coastal waters. Mussels may be farmed from
relocated spat or grown on racks or suspended
ropes, while salmon are reared in cages or pens.
The manner in which salmon and mussels are
cultivated exposes them to risks associated with
changes in ocean temperature, wave regime, storm
frequency or sea level.
Sea-level rise
Relative sea-level rise (RSLR) is the actual rate of
sea-level rise adjusted to include the impact of
isostatic change. The current relative rate of sea-level
rise in the south-west of England is about 2.5 mm yr
-1
,
while in Scotland sea-level rise attributed to climate
change is almost offset by uplift, with RSLR values of
between0.1and0.9mmyr
-1
(Shennan and Horton,
2002; Shennan et al., 2006). The rate of sea-level
change in Wales and the south-east of England is
between these values.
Over the next century, the effect of sea-level rise
on habitats suitable for aquaculture will be
spatially variable. In areas of isostatic uplift the
effect is minimized, while towards the south of the
UK subsidence enhances the impact of rising sea
levels. However, rates of sea-level rise are likely to
accelerate. Jenkins et al. (2009) indicate that the
projected range of absolute sea-level rise around
the UK, excluding land movements, is between 12
and 76 cm by 2095. This suggests an 8-fold
increase in current rates of sea-level rise toward
the turn of the century. At a rate approaching
1cm yr
-1
sea-level rise will easily outstrip rates of
isostatic uplift throughout the UK and Ireland.
One of the greatest challenges facing aquaculture
in coastal settings is understanding how coastal
habitats will respond to accelerating sea-level rise,
particularly as the shoreline morphology shifts. It
is currently assumed that the rate of coastal
habitat retreat will increase as the RSLR increases,
but this view may be challenged, with some
research indicating that the reorganization of the
shoreline has been sluggish during periods of rapid
sea-level rise in the past (Orford and Pethick,
2006). As a result, habitat types such as intertidal
mud ats, which are lost due to sea-level rise, may
not necessarily be replaced landward.
Of additional concern is the lack of sediment
available for reformation of coastal morphologies
at landward locations, impeding coastline recovery
and increasing coastal habitat vulnerability to
wave erosion (Orford and Pethick, 2006). In
estuaries, for instance, maintenance of depth as
sea level rises requires ne sediment deposition to
occur at an equal rate. If sufcient ne sediment is
Figure 3. Climate change can potentially affect many aspects of the UK and Ireland aquaculture industries; panels (a)(e) illustrate some of the impacts: (a)
jellysh blooms (Pelagia noctiluca) can kill farmed sh; (b) the non-native Pacicoyster (Crassostrea gigas) colonizeswild mussel beds; (c) blooms of harmful
microalgae can cause shellsh poisoning; (d) the development of mussel larvae may be affected by ocean acidication; (e) climate change affects wild sh
populations that are used in sh feed (source of images: Feargus Callagy a; Kerstin Kolbe b; Ruth Callaway c, e; Robert Ellis d).
CLIMATE CHANGE AND MARINE AQUACULTURE IN THE UK AND IRELAND 393
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not available, intertidal surface elevations will fall,
reducing the area for shellsh species such as cockles
(Cerastoderma edule) and mussels. However, deeper
inlets may be more suitable for mussel lays.
In addition to the rapid rate of sea-level rise
expected towards the end of the century and the
possibility of an insufcient supply of sediment to
redeposit coastal landforms, the assumption of
coastal habitats uniformly retreating is challenged
by coastal squeeze. Developments focused on the
coast provide a hard edge to retreating habitats,
and as a result, there may not be adequate space
for habitats to retreat landward. Crooks (2004)
suggested that increases in sea level will result in
the loss of intertidal habitats if ood defences are
maintained, unless a position of managed retreat is
adopted. Habitat loss in intertidal areas is likely
to impact shellsh cultivations, while nsh
aquaculture may be less affected. More research is
required regarding coastal sediment budgets and
the impact of accelerated sea-level rise on coastal
morphology and associated habitats.
Storm damage
Over the last 50 years there has been an
intensication of storm events in the north-east
Atlantic (Jones et al., 1999; Alexander et al., 2005;
Yan et al., 2006). The trend is predicted to
continue (Leckebusch et al., 2006), although the
rate of increase may be slow (Weisse et al., 2005).
Extreme wind speeds and wave conditions are
likely to increase concurrently (Grabemann and
Weisse, 2008). The severity of storms, their
frequency, the height of waves and storm surges
are all predicted to increase over the coming
decades (Frost et al., 2012).
Storm damage is a major concern to the
aquaculture industry. Mussel cultivations are
vulnerable to destruction by storms (Dankers,
1995), and in intertidal areas storms are a major
factor limiting the distribution of mussel beds to
sheltered parts (Nehls and Thiel, 1993).
A study of sh escapes in Scotland found that of
the 2.18 million sh that escaped during the seven
years covered by the research, 38% escaped during
a single storm event in 2005 (Taylor and Kelly,
2010). Similarly, during a summer ood in
Boscastle, southern England, one owner lost
40 000 salmon and brown trout (Salmo trutta)
(Handisyde et al., 2006). Storms cause large
waves, surges and ooding, all of which can
potentially result in structural damage to
infrastructure or the introduction of predators
(Handisyde et al., 2006). This leads to a loss of
stock, higher capital cost required to design
infrastructure that can withstand large events and
increased insurance costs.
Failure of cages and moorings is most likely to
occur during unsettled wave and wind conditions,
prompting Taylor and Kelly (2010) to suggest that
cages were under-designed for the environmental
conditions to which they were exposed. Storm
damage to marine salmon cages poses nancial
and welfare problems, as well as providing a route
for farmed salmon to escape into the environment
and interact with wild sh, causing hybridization
and loss of genetic diversity (Walker et al., 2006).
A greater frequency of extreme weather events is
also anticipated to facilitate disease epidemics
by causing ecological stress and thereby
compromising resilience (Epstein, 2001). However,
on the positive side, extreme weather events can
directly harm and reduce parasite populations
through environmental disturbance (Overstreet,
2007). Information regarding the impact of climate
change on storm surges, wave height and wave
frequency should be heeded when designing cages
for a specic return storm period.
The systematic recording of incidences of sh
escapes began in 2002 for Scottish sh farming,
and no similar records exist for regions outside of
Scotland. As such, it cannot be determined as to
whether the number of sh lost has increased,
whether incidents of escape are signicantly
correlated with storm incidence, or whether the
number of sh that escape correlates with storm
intensity. The greatest economic losses could
potentially occur in Scotland owing to the
concentration of salmon farming in this region.
However, the Scottish Government is in the
process of developing legislated engineering
standards for cages, and combined with a risk
analysis of previous incidents, this impact may be
mitigated in the future.
Precipitation, freshwater input and associated pollution
Evidence suggests that the intensity of precipitation
events will increase in the winter months, while
summers may become drier (Frost et al., 2012).
Lowe et al. (2009) predict that in the northern UK
where the majority of nsh aquaculture takes
place, there will be a reduction in summer rainfall
of up to 30% by 2098 compared with 19611990
values. An altered hydrology, characterized by
R. CALLAWAY ET AL.394
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more frequent oods and droughts, will have a
complex effect on the transport and concentration
of toxicants, nutrients and pollutants. This is
illustrated by a study in Portugal, which found
that during periods of lower than average rainfall,
episodes of diarrhetic shellsh poisoning increased
owing to reduced estuarine mixing (Vale and de
Sampayo, 2003).
Conversely, increases in peak river discharge
during winter are likely to present a major problem
to infrastructure developed in rivers and estuaries.
An increase in rainfall intensity during winter will
result in enhanced run-off and higher ood
discharge peaks (Roessig et al., 2004; Harley et al.,
2006). The impact of increased run-off on water
quality is three-fold: increased turbidity, increased
nutrient loads and increased contaminant loads.
Extreme precipitation events and ooding are often
associated with signicant nutrient pulses to the
near shore environment (Devlin and Brodie, 2004),
frequently as a result of sewage overows (Kay,
2008). Nitrogen-related pollution of coastal waters
has caused widespread hypoxia and anoxia, habitat
degradation, alteration of food-web structure and
loss of biodiversity (for review, see Howarth, 2008).
Data collected by the Scottish Environment
Protection Agency suggest that organic carbon
levels in Scotland have doubled within the last
20 years as a response to increases in run-off
(Sheahan et al., 2010).
The problem is likely to be severe for aquaculture
facilities located in the estuaries of rivers with large
catchments. Following an outbreak in the human
population, the norovirus may pass through the
sewage system. Heavy rainfall (or snow meltwater)
often results in tertiary treatment works being
bypassed, resulting in the discharge of efuent in a
raw or highly contaminated state. The Shellsh
Association of Great Britain has seen an increase
in the number of incidents of norovirus associated
with bivalves; in 2009 there were 12 outbreaks
with 24 positives from bivalve shellsh affecting
739 people (Pickerell, 2010).
The Intergovernmental Panel on Climate Change
(IPCC) (2007) suggest that the global oceans are
freshening. However, there is substantial uncertainty
and a lack of data concerning macro-scale and
long-term changes in salinity within UK coastal
waters as a result of climate change and the potential
impacts on UK aquaculture are even less dened.
For UK aquaculture, the most pressing needs are for
a long-term monitoring programme that studies
salinity changes at aquaculture sites, as well as an
enhanced understanding of the impacts of salinity
changes on UK aquaculture species.
OCEAN ACIDIFICATION
Ocean acidication is a recognized threat to marine
ecosystems (Frost et al., 2012). With atmospheric
carbon dioxide ( CO
2
) predicted to rise to between
550 ppmv and 958 ppmv by 2100, ocean pH is
predicted to fall by 0.30.5 units and carbonate
saturation states are projected to decline by about
45% before the end of this century (IPCC, 2007;
Andersson et al., 2008). Coastal and estuarine
ecosystems are expected to experience effects of
acidication earlier and more severely than other
systems (Orr et al., 2005; Feely et al., 2008, 2010;
Thomsen et al., 2010; Range et al., 2011). As
marine aquaculture industries utilize these
ecosystems for production, there are potentially
signicant socio- economic implications.
At present, few studies have measured the
biological effects as a result of the current decline
in ocean pH and carbonate ion concentration
from the pre-industrial levels (Talmage and
Gobler, 2010). There has, however, been a
signicant amount of research over the last decade
to determine the biological effects that ocean
acidication will cause by 2100. The response to
these levels of acidication varies between taxa,
with recent studies demonstrating inter-specic
variation between closely related species (Miller
et al., 2009), as well as intra-specic variation both
between and within populations (Parker et al.,
2011). Particular vulnerability has been observed
in the majority of marine calcifying groups,
principally through the reduced ability to produce
and maintain calcium carbonate (CaCO
3
)
structures under the declining ocean carbonate ion
concentrations. As such, the predominant impact
of ocean acidication on the marine aquaculture
industry is expected to occur in these marine
calcifying groups, primarily affecting the marine
shellsh aquaculture industries (Cooley and
Doney, 2009).
The principal biological effect is likely to occur
during the vulnerable early developmental stages
of bivalves; this is due to marine bivalves
producing a soluble amorphous CaCO
3
shell as a
transient precursor to the aragonite and calcite
shells that are secreted by adults (Weiss et al.,
2002; Fabry et al., 2008). This form of CaCO
3
is
CLIMATE CHANGE AND MARINE AQUACULTURE IN THE UK AND IRELAND 395
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signicantly less stable than the crystalline phases of
aragonite and calcite, rendering it more difcult for
larvae to produce their shells under the continuing
carbonate decline (Raven et al., 2005). Further, it
has been demonstrated that smaller post-larval
bivalves are less able to overcome dissolution
pressure at low pH (Waldbusser et al., 2010).
Subsequent impacts on shell formation can lead
to bivalves developing growth abnormalities
(Kurihara, 2008; Parker et al., 2010), declining
growth (Michaelidis et al., 2005; Talmage and
Gobler, 2009, 2010; Gazeau et al., 2010;
Bechmann et al., 2011) and reduced survival rates
(Watson et al., 2009; Talmage and Gobler, 2010).
In the wild, bivalve larvae naturally exhibit a high
mortality rate (>98%) during their transitional
phase from free swimming larvae to juveniles, and
therefore any additional stresses as a result of
ocean acidication could signicantly reduce the
number of individuals recruited (Green et al.,
2004). An example of this has already been
demonstrated in the wild, with signicantly lower
bivalve recruitment occurring at naturally low pH
sites (Cigliano et al., 2010). The supply of viable
spat could therefore be compromised by ocean
acidication conditions, which would potentially
impact mussel farms around the UK and Ireland.
This could force mussel farms to either rely more
heavily on hatchery produced seed in the future,
or to utilize a different mussel species that is more
tolerant to ocean acidication (Cooley and Doney,
2009; Bell et al., 2010).
Older life stages of bivalves have also shown to
be affected by the predicted future climate
scenarios. Adverse effects on calcication rates,
shell dissolution and the disruption of the internal
acidbase balance have been demonstrated. The
latter has been associated with a decreased
metabolic rate, declined tissue growth and
suppressed immune responses (Barry et al., 2005;
Michaelidis et al., 2005; Berge et al., 2006; Bibby
et al., 2007; Gazeau et al., 2007; Beesley et al.,
2008; Wood et al., 2008).
Selective breeding, such as that in the oyster
Saccostrea glomerta (Parker et al., 2011), could
potentially be used to obtain brood stock with an
increased tolerance towards the impacts of ocean
acidication. Further research could also be
applied to species which tolerate naturally high
CO
2 (aq)
levels, such as those inhabiting areas close
to hydrothermal vents (Fabry et al., 2008). If the
underlying physiological and genetic mechanisms
are isolated, it could enable shellsh industries to
produce climate proofspecies in the future
(Parker et al., 2011).
Economically lucrative species, such as lobsters
or crabs, are less likely to be affected through
the direct impacts of ocean acidication, in
comparison with marine bivalves. This is due to
decapodsability to strongly regulate their internal
ion concentration, which enables them to have a
high level of biological control over ionic
processes, e.g. calcication (Cooley and Doney,
2009), in addition to aiding the partial or full
compensation of internal acidbase disruption, e.g.
during hypercapnia induced acidosis (Spicer et al.,
2007; Small et al., 2010). Currently, culturing
production of crustaceans is negligible in the
UK and Ireland. However, there have recently
been successful developments to create lobster
hatcheries, predominantly aimed at re-stocking
natural populations (Burton, 2003). With this in
mind, focus should be directed to potential
energetic impediments in decapods as a result of
maintaining ionic homeostasis under ocean
acidication conditions.
Finsh are pre-adapted to some of the pressures
brought about by increased ocean acidication
(Ishimatsu et al., 2004, 2008; Portner, 2008). To
date, the majority of studies have not found any
direct effects on growth development (Munday
et al., 2009a), egg survival (Munday et al., 2009a;
Franke and Clemmesen, 2011), metabolic activity
(Melzner et al., 2009) or swimming performance
(Melzner et al., 2009; Munday et al., 2009a),
indicating limited direct effects of ocean
acidication for nsh farming in the near future.
Indirectly, ocean acidication could affect farming
through decreasing the olfactory responses of
marine sh larvae, thus increasing their susceptibility
to predators as they are less likely to be alerted to
their presence (Munday et al., 2009b, 2010).
Further research is needed to understand the
effects of ocean acidication on the calcareous
structures in nsh, such as otoliths, stratoliths
and gastroliths, to assess if there are any
developmental impacts on movement or feeding
throughout the life-cycle, which may affect both
natural and farmed populations (Cooley and
Doney, 2009).
In the short term ocean acidication is unlikely to
be of major concern for the UK and Irish
aquaculture industry. However, as a climate
change phenomenon it has the potential to change
entire food chains and community assemblages,
and it is therefore necessary to further understand
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the principal processes and effects of ocean
acidication on ecosystems. Since the response
to increased acidication is species specic,
aquaculture research needs to focus on the
commercially important species on a local scale.
Further research on economically important
shellsh is essential, with primary focus on larval
development and spat.
CLIMATE CHANGE AND THE PHYSIOLOGY
OF AQUACULTURE SPECIES
Most aquatic animals including sh are
poikilotherms. Their metabolic rate and energy
expenditure, and therefore their growth potential,
are strongly affected by water temperature.
Temperature increases that occur naturally during
summer increase growth rates up to the tolerance
limit of each species. Wild nsh avoid areas
where the temperature is outside their natural
temperature range, but farmed sh cannot, as they
are conned to their cages.
Elevated water temperature will impact on sh
directly through the inuence of temperature on
growth, and indirectly via specic nutritional and
physiological processes that affect growth.
Relationships between temperature and feed
intake, growth, and growth efciency have been
broadly researched in the past for several salmon
species and results show a bell shaped curve for
the response of both feed intake and growth to
increasing water temperature (Brett et al., 1969,
1982). Several studies followed this classical
approach to predict the optimum temperature for
Atlantic salmon (Figure 4) (Koskella et al., 1997;
Larsson and Berglund, 2006). Feed intake is a
critical factor. Feeding to satiation means that sh
will eat to meet their energy requirements, and
feed intake typically increases rapidly with
increasing temperature until appetite is inhibited at
higher temperatures (Figure 4). Here, energy
expenditure for maintenance increases and sh
may not be able to cover their requirements for
growth in addition to maintenance. As a
consequence climate change may reduce growth in
salmon in some areas due to a shift beyond the
speciesoptimum temperature range.
Principal studies following a bioenergetic
approach involving brown trout were conducted to
describe energy requirements for growth (Elliott,
1976, 1982). Temperature was a key variable
and its inuence on feed intake, growth, body
composition, nutrient retention efciency and
metabolic losses were modelled over a broad range
of temperatures. Following these early studies, it
was recognized that factorial approaches, which
compartmentalise requirements to components,
such as maintenance and growth, are essential
tools in dening feed requirements in aquaculture
(Bureau et al., 2002; Lupatsch, 2009). Thus, under
farming conditions, climate change related
increases in temperature might even have a
positive impact. It may result in enhanced growth
and production, provided that feed supply satises
the higher demand (Cho, 1992; Lupatsch, 2009).
Concepts and approaches developing growth
models for salmon have been published (Iwama
and Tautz, 1981; Jobling, 2003), but they need to
be updated regularly, especially as genetic
selection of farmed Atlantic salmon has improved
the growth potential considerably. In Norway, for
example, farmed Atlantic salmon have been
selected for increased growth rate since 1975.
Together with improvements in nutrition this has
reduced the production cycle by approximately
1.5 years (Thodesen et al., 1999; Gjedrem, 2010).
Generally, information about the impacts of
higher temperatures on the life-cycle of Atlantic
salmon is incomplete, since most studies focus on
smaller, juvenile stages (Brett et al., 1982; Elliott,
1991). There is little information about the impact
of warmer waters on the nutritional requirements
of large salmonids held in sea cages. Some
understanding of nutritional physiology can be
gained from the Tasmanian salmon farming
industry (Carter et al., 2005), as temperatures in
those waters are on average higher than in the
northern hemisphere. However, information on
growth for salmonids reared in cages under
Figure 4. Predicted (dashed line) and observed (black dots) feed intake
of age 1+ salmon (Salmo salar) reared at ve different temperatures
(after Koskella et al., 1997).
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farming conditions can rarely be found in the
publically available literature. Currently, the best
datasets on ration and growth, and probably the
most sophisticated models, are those owned
commercially by farms or feed companies.
Salmonids favour fairly low temperatures and the
normal range for salmon farms lies within 519 C.
Fast, efcient growth is best achieved in water
temperatures of 1317 C. Outside this range,
production becomes less efcient, either due to
slower growth or to temperature stress problems.
Thus, a rise in water temperature of about 4 C
(IPCC, 2007) could exceed the optimal temperature
range of salmon. In addition, seasonal extreme
values may be equally or even more important than
changes in annual average temperature. Morgan
et al. (2001) found improved growth in rainbow
trout during winter with a 2 Ctemperature
increase, but decreased growth in summer when the
2C increase was added to already high
temperatures. Warming waters could open up new
sites further north, or deeper waters, which are
currently not suitable for aquaculture. However,
areas may also become unsuitable. Currently
salmon farming is concentrated in Scotland
(Figure 2), where water temperatures range from
615 C (Baxter JM et al., 2011). Increasing water
temperatures may limit the southern expansion of
salmon farms, although the main limitation for the
foreseeable future is still likely to be the availability
of suitable sites for cultivation.
A compounding factor is the decrease of water
solubility of oxygen with increasing temperature.
The worst combination is high water temperature
and low water ow. This effect is more pronounced
in sea water than in fresh water, as oxygen solubility
is dependent on salinity. Pörtner and Knust (2007)
suggested that the main physiological effects of
climate change will be due to thermal limitation
of oxygen. While many studies focus on juvenile
life-history stages of salmonids, larger individuals
might be at even greater risk, as they may reach
their thermal aerobic limit sooner than smaller
individuals (Pörtner and Knust, 2007). Thus,
oxygen limitation could potentially affect larger sh
in sea cages.
At present, most salmon hatcheries and
broodstock facilities in Scotland rely on relatively
simple ow-through systems with limited control
of temperature and water quality. A combination
of economic and environmental concerns is driving
the industry towards the use of some land based
recirculating systems which allow full control of
water temperature and quality. Impacts of climate
change may necessitate that the majority of this
production takes place in such systems to ensure
the supply of good quality smolts, as high
temperatures have been shown to detrimentally
impact on egg quality and production (King and
Pankhurst, 2004).
Opportunities for farming warmer water species
such as sea bass (Dicentrarchus labrax) and turbot
(Scophthalmus maximus) may emerge from rising
seawater temperatures, as has been envisaged for
Norwegian waters (Bergh et al., 2007). However,
much of this farming is expected to be carried out
in land-based recirculating aquaculture systems in
the vicinity of the coast, as already widely
practised in the Mediterranean for hatchery and
nursery stages. Hence, issues such as the price of
energy, land-use and market demand are likely to
be of greater importance for the development of
these new industries than changes in seawater
temperature.
An increase in sea surface temperature is also
likely to affect the growth of farmed shellsh.
Ferreira et al. (2008) examined the potential
effects of global climate change on shellsh growth
by considering an increase in water temperature of
1C and 4 C above the mean annual seawater
temperature of Strangford Lough (N. Ireland,
UK); the 1 C increase scenario was based on near
future predictions, and 4 C is the maximum
increase predicted for the year 2100 (IPCC, 2007).
Using the ShellSim model of Hawkins et al.
(2002), they predicted that an increase in water
temperature would lead to a reduction in
aquaculture productivity and a decrease in the
mean weight and mean length of both oysters and
mussels. These decreases would have a dramatic
effect on the blue mussel, and lesser consequences
for the Pacic oyster population. An increase of
1C in the water temperature would lead to a
reduction of about 50% in mussel production and
less than 8% in Pacic oyster production. An
increase of 4 C would result in a reduction of 70%
in mussel production and less than 8% in Pacic
oyster production.
HEALTH AND EPIDEMIOLOGY
Effects of climate change on the health of nsh and
shellsh are currently not quantiable. There are
plenty of examples of emerging, or at least newly
discovered, diseases in the marine or freshwater
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environment (Lafferty et al., 2004). However, the
evidence that climate change is a major driver
behind the emergence of diseases is thin (Lafferty,
2009). Cook et al. (1998) demonstrate a link
between increasing sea temperature and spread of
Perkinsus marinus in the eastern oyster Crassostrea
virginica,asdoHofmannet al. (2001) for MSX
disease Haplosporidium nelsoni in the same host
species, although it is difcult to conclusively
demonstrate causality in such observational studies.
It has been suggested that global warming at best
contributes to (viral) disease emergence and that
translocation of hosts and vectors is the more
important factor (Zell et al., 2008).
Epidemic spread, a process driven by positive
feedback, provides a noisy system which is
relatively difcult to analyse robustly compared
with other branches of biology. Surveillance of
aquaculture diseases is further complicated by the
large numbers of species involved for both hosts
and parasites (Tables 3 and 4), and the
comparative youth of the industry compared with
terrestrial farming. The scarcity of long-term
datasets hampers analysing and understanding the
impacts of climate change on disease levels in situ
(Karvonen et al., 2010).
Fish parasites and pathogens
The potential impact of climate change on marine
aquaculture in the UK and Ireland, in terms of
health and epidemiology, depends on its impacts
upon the key drivers for disease emergence
(Figure 5). These drivers can be broadly grouped
into parasite and microbial pathogen change and
introduction, host change and introduction, and
changes in contact and interaction between hosts
and pathogens.
Parasites are subject tomany of the environmental
constraints experienced by other free-living
organisms. However, they may also require
extremely narrowly dened local environmental
conditions, which are provided by a specichost,or
several hosts, according to a given parasites host
specicity. At the same time the host environment
may buffer parasites, particularly endoparasites,
against wider environmental changes. Climate
change will therefore affect parasites both directly
through the ambient environment and indirectly via
effects on host parameters such as distribution,
behaviour, physiology, and mortality. The more
complex the life-cycle in terms of the number of
hosts and parasite stages involved, the more likely it
Table 3. Parasitic diseases in aquaculture species relevant to the UK and Ireland*
Aquaculture species Parasite Type Comments Key references
Salmo salar (Atlantic salmon) Lepeophtheirus salmonis Caligidae Sea lice are a year round problem and are controlled through
the administration of various bath and in-feed treatments.
The efciency of these may be reduced by altered
environmental conditions, i.e. elevated water temperature,
organic loading, reduced oxygen content, etc.
Johnson et al. (1993)
Caligus elongatus (sea lice)
Mytilus edulis (blue mussel) and M. galloprovincialis Marteilia spp. Protozoan Berthe et al. (2004)
Mytilicola spp. (red worm) Copepod Bignell et al. (2008)
Ostrea edulis (native oyster) Bonamia ostreae Haplosporidian Causes signicant mortalities when introduced Culloty and Mucalhy (2007)
Bonamia exitiosa Abollo et al. (2008)
Crassostrea gigas (Pacic oyster) Various trematodes Trematoda
Haplosporidium armoricanum Haplosporidian Renault et al. (2000)
Hine et al. (2007)
Homarus gammarus (European lobster) Nicothoë astaci Copepod May be intermediate host Wootton et al. (2011)
*This table shows main parasites affecting UK and Irish aquaculture species; it is not an exhaustive review of all diseases.
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is to be affected by environmental change, as each
link in the life-cycle may be subject to different
requirements (Overstreet, 1993). Effects on host
parameters are relevant not only to cultured species
but also to wild host reservoirs and vector species,
which are common sources of infection for farmed
animals.
There is evidence to show that specic
environmental changes, whether naturally
occurring or anthropogenic, can have substantial
impacts upon both protistan and metazoan
parasites, affecting the identity of key parasite
species within a host community, the dynamics of
infection and the outcome of infection for the
host (MacKenzie et al., 1995; Williams and
MacKenzie, 2003; Sures, 2004; Overstreet, 2007).
While considerable work has been undertaken to
predict the effects of climate change on parasitic
diseases of terrestrial species, little work has
been carried out to examine the potential effects
of climate change on aquatic parasites
(Marcogliese, 2001, 2008; Karvonen et al., 2010).
Moreover, the specialized, often highly simplied
environment created by current aquaculture
practices, particularly the high intensity
monoculture systems frequently employed in the
UK and Ireland, mean that predictions made for
the impacts of environmental change upon
parasitism of wild host populations may not hold
true for cultured nsh,evenwithinthesamesh
species.
Higher levels of parasitism in wild sh populations
might be expected to increase host mortality, and
thereby act to control parasite numbers. In contrast,
parasites are controlled through interventions and
Table 4. Viral and bacterial diseases in aquaculture species relevant to the UK and Ireland*
Aquaculture species Disease and agent Type Comments Key references
Salmo salar (Atlantic salmon) Amoebic gill disease
(AGD)
Neoparamoeba
pemaquidensis
Amoebae Reported from Scottish and Irish farms. Environmental changes
predispose salmon to colonisation by amoebae and ciliates
Rodger and McArdle (1996)
Bermingham and Mulcahy
(2004)
Mytilus edulis (blue mussel) Vibriosis Bacterial Anguiano-Beltrán et al. (2004)
Crassostrea gigas (Pacic oyster) Vibrio splendidus Bacterial Mass mortalities usually during the summer Le Roux et al. (2002)
Herpes virus
(Ostreid herpesvirus 1
mvar)
Viral Increasing importance in UK and Ireland as a major cause
of disease.
Segarra et al. (2010)
Mercenaria mercenaria (hard-shelled
clam)
Vibriosis (vibrios) Bacterial Temperature dependent, more likely to affect larval stages
and juveniles
Venerupis philippinarum (Manila clam) Vibrio tapetis Bacterial Brown ring disease in Manila clams Paillard (2004)
Herpes virus Viral
Homarus gammarus (European lobster) Gaffkaemia (Aerococcus
viridians var. homari )
Bacterial No evidence of climate related changes in prevalence or severity/
susceptibility
Cawthorn (2011)
Shell disease syndrome Bacterial
(uncertain)
Possibility of epizootic shell disease spread to European lobsters Vogan et al. (2008)
*This table shows main viral and bacterial diseases affecting UK and Irish aquaculture species; it is not an exhaustive review of all diseases.
Figure 5. Disease susceptibility model for sh and shellsh.
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management strategies in aquaculture, rather than
through parasite-associated mortality.
Effects of changes in temperature on parasites
Aquatic parasites show temperature optima for the
successful completion of their life-cycle, and an
extension of the season over which temperatures
are amenable to survival and development will
provide a longer window of infection for infectious
stages. It will also provide more time for the
proliferation of parasites to occur, both on and off
hosts, and it will lead to more generations of
parasites over the farm cycle through faster
development times.
Higher temperatures may have direct
implications for the level and nature of pathology
experienced by hosts, where the speed of
development of individual stages, the increase in
numbers within the host or the nal size and state
of development reached are affected. With higher
winter temperatures some parasites that would
normally be dormant or present in negligible
numbers, may continue to pose a problem over the
winter months.
Since changes in water temperatures may
affect movements of wild hosts, this may affect
the introduction of parasites into aquaculture
environments. The copepod parasite Caligus
elongatus for instance, which principally infects
marine cultured Scottish and Irish Atlantic salmon
over summer and autumn, is brought into the
aquaculture environment by wild marine sh
species migrating into coastal waters to feed (Bron
et al., 1993; Revie et al., 2002). The seasonal
appearance and disappearance of this species
from farm sites means that development of
chemotherapeutant resistance is limited, in
contrast to the salmon louse Lepeophtheirus
salmonis, which is often present year-round.
Longer residence times for migrating wild host
species could therefore increase parasite incidence
on farms, thereby affecting both sh health and
parasite biology.
Increase in water temperature will also affect the
ability to successfully treat parasite pathogens, with
some chemotherapeutants being less suitable for
treatment at higher temperatures. For example,
the efcacy of hydrogen peroxide, used to remove
caligid parasites from marine farmed Atlantic
salmon, varies with temperature. It needs to be
applied at lower concentrations for efcacy against
lice at warmer temperatures, but it becomes
increasingly toxic to sh, with 7.7% mortality of
Atlantic salmon reported at 14 C and 100%
mortality at 18 C (Johnson et al., 1993).
Effects of changes in water quality on parasites
Changes in precipitation patterns and the associated
build-up of nutrients may lead to eutrophication
and increased water turbidity. In farmed
Atlantic salmon gill damage caused by elevated
ammonium, nitrite and chlorophyll levels was
suggested to be a predisposing factor for amoebic
gill disease in Ireland, while temperature increase
is itself a risk factor for the disease (Bermingham
and Mulcahy, 2004). It has been suggested that the
deteriorating quality of estuarine waters, combined
with higher temperatures, may provide a risk in
terms of numbers of the parasitic and toxic
dinoagellate Pesteria sp. (Burkholder and
Glasgow, 1997; Rublee et al., 2005), although this
has yet to be reported as an issue for aquaculture.
The species has nevertheless been documented in
Northern European waters (Jakobsen et al., 2002),
suggesting that it could become a problem if
coastal conditions change.
Deterioration in water quality or site hygiene
will similarly increase ambient levels of many
opportunistic pathogens (e.g. Trichodina sp.). The
same will be true for bacterial pathogens, and
opportunistic parasites may appear as secondary
pathogens following bacterial infection, or they
may themselves promote secondary infection by
bacteria.
Changes in coastal salinity associated with
changes in precipitation may also affect the
survival and infection success of some marine
parasites. The infective copepodid of L. salmonis,
for instance, shows compromised survival at
<29 ppt (Bricknell et al., 2006) and it has been
noted that sites with periods of high freshwater
run-off experience loss of sea lice during low
salinity ushing events (authorsobservations).
Effects of changes in temperature on sh hosts
Changing climate may lead to some sh species
extending their presence into new areas. These
species will be exposed to the full spectrum of
parasites present in the new environment. They
may also carry their own parasites to add to the
parasite load of native aquatic species, both
farmed and wild. This could include harmful
non-native species. The invading wild hosts might
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act as host reservoirs for existing aquaculture
pathogens.
Although parasites are introduced along with their
exotic hosts, in general these hosts appear to be less
infected than native species (Torchin et al., 2003),
possibly due to the stochastic extinction of small
founder populations or the lack of local vectors.
With higher seawater temperatures the immune
function of farmed sh species may increase
within their optimal temperature range (Bly et al.,
1997; Bowden et al., 2007). However, higher
temperatures are associated with falls in oxygen
levels, which is likely to increase stress in sh.
This potentially compromises immune capacity
and provides increased scope for opportunistic
infections.
Parasite-host contact
Climate change may affect the pattern of contact
between parasite and host populations, i.e. the
routes of transmission. Changing physical factors
may alter the spatial overlap between hosts and
parasites. The contact could be accelerated or
disrupted through altered ocean currents, changes
in precipitation patterns or, in the long term,
through sea-level change. One feature of climatic
change that could affect UK and Irish
aquaculture, and which was highlighted for the
terrestrial environment by Hudson et al. (2006), is
the possibility of increased spatial synchrony, i.e.
the development of extensive areas sharing a
similar climate or environment. It was suggested
that under such conditions large-scale outbreaks of
disease might follow through disease transmission
across large areas. The timing of events in host
and parasite life-cycles, such as hatching and
migration, may shift to accommodate changes in
the environment (Marcogliese, 2001). Because of
the often complex interactions between parasites
and hosts this may act to break or create
conditions of spatial overlap, depending on
circumstances, and levels of infection in wild or
cultured hosts may increase or decrease.
While the above discussion principally deals with
events occurring within the lifetime of hosts and
parasites it is also critical to consider longer term
evolutionary change. The genetics of both hosts
and parasites have already been affected by
culture environments and practices, for example
breeding for desired farm traits such as disease
resistance in salmon and the emergence of
resistance to chemotherapeutant in bacteria and
sea lice (Treasurer et al., 2000; Bravo et al., 2008;
Lees et al., 2008a, b). The inevitable adaptations
to climate change by hosts and parasites may
result in unpredictable knock-on effects on
resistance or virulence, depending on trade-offs
between the traits under selection.
Microbial infections of sh
Climate change has a number of possible impacts on
the infection of nsh by microbial and viral
pathogens in aquaculture, both in terms of source
and effects. Changes in rainfall and water
temperature can inuence the loading of pathogens
within sh farms, as well as the species composition
of those pathogens and the infection rates of the sh
in the farm. Any increase in these infections would
have a direct effect on the protability of
aquaculture.
Generally, in waters of the UK and Ireland
pathogen infection rates are affected by water
temperature in marine systems as a result of three
factors:
(i) Supply: bacteria and fungi both experience
positive correlations between temperature and
production. Therefore the reservoir of pathogens
present in the environment is generally higher
under warmer conditions, leading to increased
infection risk.
(ii) Active period: many diseases are only present in
the population during warm, summer periods
and are not active during the cooler winter
months (Harvell et al., 2002). Warmer waters
will prolong the warmer periods and therefore
extend the season during which sh will be
susceptible to infection.
(iii) Host susceptibility: climate change may shift
conditions outside the biological optima of
organisms. This is likely to place them under
greater stress thus suppressing their immune
system (Snieszko, 1974; Bowden et al., 2007),
resulting in an increased rate of microbial infection.
Reduced precipitation in the northern UK in
summer (Lowe et al., 2009) would reduce the
frequency and loading of bacteria and fungi
washed into the areas around nsh farms.
However, for seasons where precipitation is
predicted to increase and areas where rainfall
events are going to intensify, the reverse will be
the case, i.e. bacterial loading will increase and
cultured animals will be more heavily affected by
microbial pathogens. Species that are farmed
near the border of their optimal biological niche
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could experience stress and, hence, increased
susceptibility to disease. This could be particularly
problematic for cultured sh populations which
lack the genetic diversity to counter new
pathogens (FAO, 2011).
Several bacterial and viral infections of farmed
sh in the UK are known to be inuenced by
temperature. Viral hemorrhagic septicemia virus
(VHSV), infectious haematopoietic necrosis (IHN)
and Oncorhynchus masou virus (OMV) are viral
infections that show higher rates of infection at
low water temperatures (815 C) (Amend, 1970;
Yoshimizu et al., 2005; Arkush et al., 2006). The
risk of these diseases may decrease with increasing
water temperature. Conversely, the bacterial
infection enteric red mouth (ERM) becomes
signicantly more lethal at temperatures above
about 10 C, particularly when the host organism
is stressed (Defra, 2011). Levels of furunculosis
also increase at higher temperatures (Nordmo and
Ramstad, 1999).
As has already been observed in larger marine
organisms (Stebbing et al., 2002; Nye et al., 2009),
increasing water temperature is likely to shift the
range of pathogens northward. Until now some
pathogens may have been unable to survive in UK
and Irish waters, but are increasingly able to gain
a foothold either through natural migration with
the poleward spread of warm water species, or
through the accidental introduction of organisms
through stock movement (Birkbeck et al., 2011). A
documented example of the northward spread of a
pathogen, although in shellsh rather than nsh,
is that of the expansion of range of the Eastern
Oyster Disease on the USA Eastern Seaboard in
the 1980s (Ford, 1996). This expansion was linked
to a series of relatively warm winters, which meant
that the usual repression of the pathogen in the
water during the cold months was not as effective
as usual, and the infection was able to spread.
Should a long-term change in water temperature
take place, these expansions could become
commonplace and also result in greater disease
burdens in farmed nsh.
Shellsh
The form of shellsh aquaculture varies
dramatically with different species and this will
affect the likely changes in disease prevalence and
severity following climate change. For example,
mussels are either grown on ropes or seeded as
mussel lays to be later harvested in offshore areas
around the coast and are therefore subject to the
potential changes associated with climate change.
At the opposite extreme, lobsters, although not
currently produced commercially, have recently
been subject to feasibility studies for production
using land-based re-circulating aquaculture systems
(RAS). These are not subject to primary
environmental effects of climate change such as
temperature change, acidication, and emerging
diseases, because such systems have a high level of
biosecurity and environmental control.
Many shellsh are susceptible to bacterial
diseases such as vibriosis, especially during early
stages of development (Table 4). Vibrios are
ubiquitous in sea water and their growth is
dependent on the temperature of the surrounding
environment (Hsieh et al., 2008). In simple terms,
a rise in water temperature will usually result
in higher bacterial growth leading to more
disease. At the same time the host may be
immune-compromised as a result of the increase in
water temperature and associated changes in
oxygen tension (Cheng et al., 2003, 2004). Vibrios
are often found living in association with the
cuticle of crustaceans. For example, in the case of
Vibrio cholerae a major environmental reservoir of
such bacteria is a variety of zooplankton and
phytoplankton (Colwell et al., 2003; Pruzzo et al.,
2008). Therefore changes in plankton distribution
as a result of climate change may affect the
distribution of chitin-binding vibrios in seawater.
Although there is little evidence of how climate
change may affect the distribution of vibrios in the
coasts around the UK and Ireland, in the warmer
waters of the Mediterranean recent studies have
shown a demonstrable link between Vibrio
infections related to seasonality and temperature
change (Vezzulli et al., 2010).
Shellsh are also susceptible to rickettsia-like
diseases. These bacteria are obligate intracellular
parasites that can only multiply within the cells of
their hosts. A recent study on a rickettsia-like
disease, termed milky-disease, in the shore crab,
Carcinus maenas, showed that increased water
temperature during transport and storage and a
general decay in environmental conditions (e.g.
reduced oxygen solubility, nitrogenous waste
products) resulted in high levels of disease that
caused mortality (Eddy et al., 2007). Hence, such
diseases may also be inuenced by changes in the
temperature of surface waters and we would
predict that the prevalence and severity of such
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conditions may increase in temperate waters in the
coming decades.
Several species of crustaceans are susceptible to
shell disease syndrome a condition thought to be
associated with bacterial growth on the outer
cuticle (Vogan et al., 2008). In the USA, an
emerging form of this disease, called epizootic
shell disease, has caused major losses in
lobster (Homarus americanus) populations. One of
the factors that may be associated with this
emerging disease is temperature, although other
environmental factors may also be involved
(Castro et al., 2006; Glenn and Pugh, 2006).
The major parasitic diseases of shellsh are shown
in Table 3. It is extremely difcult to predict how
climate change may affect both the prevalence and
severity of such diseases under different forms of
aquaculture. In some cases, e.g. Hematodinium in
crustaceans, the distribution of the host species may
change the prevalence of disease, because there are
other hosts or vectors as part of the parasites
life-cycle (Hamilton et al., 2011). Hence, stocking
an aquaculture facility with larval or juvenile
animals may bring such diseases into the facility.
The recent global emergence of dinoagellate
parasites within the genus Hematodinium (Morado,
2011) makes this a worrying condition both for
sheries and any planned development of
crustacean aquaculture in the UK and Ireland.
There is some evidence that responses to climate
change in terms of shellsh health and disease is
species specic. Where species are on the edge of
their boundaries and the prevailing conditions alter
to more favourable conditions for diseases and
parasites, or to more stress for the host, then
epidemiologically the parasite or disease will have
the upper hand and the host species could suffer
high mortalities. Recent observations of Mytilus
edulis and the red worm, Mytilicola,haveshown
that mussels high up the shore are exposed to higher
temperatures and have higher levels of this parasite.
They suffer high mortality compared with mussels
lower down the shore. It is possible that increased
temperatures would encourage higher Mytilicola
numbers in animals further down the shore with
economic consequences. However, where the
conditions alter to be more favourable to the host,
the disease or parasite is likely to be kept in check.
MACROALGAE
Currently the cultivation of algae in the UK
and Ireland is negligible. There is, however,
tremendous interest in the expansion of the
industry, primarily for the production of biofuel
and for sh feed production (Spolaore et al., 2006;
BioMara, 2011), and hence climate change effects
on algae need to be considered.
Macroalgae live in highly dynamic and
hydrodynamically complex environments (Gaylord,
2000), experiencing forces that can often result in
structural failure of the plants, reducing macroalgae
cover over winter periods (Pratt and Johnson,
2002). These forces can be a major structuring
driver of natural macroalgae communities (Menge,
1976; England et al., 2008) and will be a
determining factor on which species can be
produced at any production site. Higher energy
sites will be more suitable for kelp species such as
Alaria esculentus and Laminaria digitata as opposed
to Saccharina latissima, which favours less exposed
situations (Lüning, 1990). If the frequency and
strength of storms is going to increase there may be
a shift to the production of species more tolerant of
high energy environments. In addition to the
increased risk of losing seaweed biomass through
direct damage, change in storm patterns would also
increase the hydrodynamic loading on the seaweed
farm infrastructure, for example longlines and
moorings. This could potentially lead to a further
loss of the cultivated biomass through mechanical
failure.
An alteration in nutrient loading of coastal
waters due to increased extreme precipitation
events will affect near-shore environments.
Temporal variability in load can play a signicant
role in determining the response of macroalgae to
nutrient enrichment (Worm and Sommer, 2000).
The response to this temporal heterogeneity is
species (Pedersen and Borum, 1996) and life stage
(Bergstrom et al., 2003) dependent. Increased
variability in nutrient loading has been shown to
benet the dispersal, survival and growth of
invasive algae (Incera et al., 2009; Vermeij et al.,
2009), but may have little effect on slower
growing kelp species (Pster and Van Alstyne,
2003). It may retard the growth of some fucoids
due to an increase of epiphyte growth (Pedersen
and Borum, 1996). While there is generally little
knowledge about the impacts of extreme
precipitation events on kelp species, increased
precipitation and increased temperature have
been associated with a reduction of kelp cover in
natural and articial habitats of southern
California (Grove et al., 2002).
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The effects of raising seawater temperatures as a
result of climate change on macroalgal cultivation
are not yet clear. It has been predicted that higher
temperatures, coupled with lower wind velocities
at certain latitudes, may result in a reduction of
vertical mixing and a decreased supply of nutrients
from deep waters, which in turn could lead to a
drop in productivity (Bakun, 1990; Diffenbaugh
et al., 2004; Issar and Neori, 2010). As a
consequence some areas may become unsuitable
for the cultivation of macroalgae without the
addition of extra nutrients. The boreal species
Ascophyllum nodosum, for example, has its
southern limit in the UK and the north of France.
It has been in decline along the English coast close
to Plymouth since the 1930s, but it ourishes in
Brittany where strong tidal mixing reduces
seawater temperatures and increases supplies of
inorganic nutrients (Hiscock et al., 2001). Similar
supplies of nutrients are not present in the
Plymouth area, and any changes in tidal mixing
due to the impacts of climate change are likely to
result in the decline of A. nodosum.
Many species of macroalgae are restricted
geographically by the temperature ranges in which
they will grow. There is some evidence of a shift in
natural populations northward in the US due to
increased seawater temperatures, particularly with
regard to kelps (Graham et al., 2007). For the UK
and Ireland there are still many unknowns.
Reports by the Environment and Heritage Service
of Northern Ireland (2007) and Hiscock et al.
(2001) suggested that there will be a decline in the
distribution of some cold-water species of
seaweeds as a result of climate change in Ireland,
south-west England and Wales, with Scotland
largely unaffected. Some of the cold water species
found within the waters of the UK and Ireland are
already at their geographical temperature limits,
and if domesticated for a new aquaculture
industry this industry is likely to be limited to
regions were the effects of increased seawater
temperature due to climate change are minimal
(Environment and Heritage Service of Northern
Ireland, 2007).
There has been considerable interest in the
potential for macroalgae to sequester carbon on
relatively short time scales (Gao and McKinley,
1994; Tang et al., 2011; Chung et al., 2011).
Macroalgae in general contain approximately 30%
dry matter, and at the current levels of cultivation
the macroalgal industry removes nearly 0.7 million
tons of carbon from the sea annually (Turan and
Neori, 2010). This represents only a very small
impact on total carbon emissions, and for the
offsets to be signicant there would have to be a
dramatic increase in the levels of cultivation
(Turan and Neori, 2010). Potentially, a 1000 km
2
area of seaweed could sequester up to 1 million
tons of CO
2
per year (Issar and Neori, 2010;
Kraan, 2010). The impacts of increased
atmospheric CO
2
on macroalgae cultivation will
depend on the species that are being grown. Many
macroalgae species, including commercial kelps,
have CO
2
concentrating mechanisms (Axelsson
et al., 2000). These mechanisms ensure that the
macroalgae are not carbon limited during normal
growth. Growth rates of 13 species of macroalgae
did not show any increase during experimental
CO
2
enrichment (Israel and Hophy, 2002).
However, there is evidence that the gross chemical
composition of macroalgae may change (Zou
and Gao, 2010) and this may be an important
consideration for macroalgae cultivation, depending
on the eventual utilization. As such, climate change
will probably have a limited impact on the
macroalgal cultivation industry of the UK and
Ireland. The majority of impacts over the next
30 years are likely to come from changes in species
composition of culture macroalgae and the need to
develop engineering solutions; both as a result of
increased storminess.
ABUNDANCE OF NUISANCE AND
HARMFUL SPECIES
Climate change will potentially affect fundamental
biological processes and would therefore inuence
the distribution, spread, abundance, and impact of
invasive species (Gritti et al., 2006), including
harmful algal blooms (Hinder et al., 2012). While
not all invasive species will be nuisance species or
cause harm, some taxa will exert substantial
negative impact on native biota and economic
values. Most marine aquaculture enterprises are
vulnerable to nuisance and harmful species, which
can have direct negative effects on the cultured
species to the extent that they kill entire stocks
within days.
Non-native species
Non-native species are those that have been
intentionally or unintentionally introduced outside
their native range (Maggs et al., 2010). If these
species become established and then threaten
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biodiversity or cause economic damage, they are
referred to as invasive(Wilcove et al., 1998).
Climate change and invasive species present two
of the greatest global threats to biodiversity and
the provision of ecosystem services (Halpern et al.,
2008; Burgiel and Muir, 2010). There is growing
evidence that in combination the threats have a
compounding effect, particularly the increasing
seawater temperatures and invasive species (Byers
et al., 2002; Stachowicz et al., 2002). They can
cause massive economic and ecological damage,
and the estimated cost of non-native species to the
economy in Great Britain is £1.7 billion a year
(Vitousek et al., 1997; Pimentel et al., 2005;
Williams et al., 2010). The annual cost to the
aquaculture industry in the UK and Ireland is
estimated to be £7.1 million, although it was
stressed that this is probably an underestimate as
there is little distinction by the industry between
native and non-native species during pest control
operations (Williams et al., 2010).
However, the damage to the UK and Irish
aquaculture by non-native species, and the extent
to which this may be attributed to climate change,
is currently unknown. Widespread economic
repercussions by non-native species to the UK
aquaculture industry have not been reported to
date, and there is little evidence at present to
suggest that climate change is either exacerbating
or suppressing the impacts that non-native species
are currently having on the UK and Ireland
aquaculture industry.
There are, however, examples from outside the
UK and Ireland, which suggest that climate
change could lead to an increase in the rate of
invasions (Dukes and Mooney, 1999), particularly
in marine habitats at higher latitudes (Reid et al.,
2009; Ruiz and Hewitt, 2009). The northward
expansion of neo-tropical and temperate species
has been seen across multiple taxa (Huntley et al.,
1995; Parmesan and Yohe, 2003; Hickling et al.,
2005; Sharma et al., 2007; Ling and Johnson,
2009; Reid et al., 2009).
Once a non-native species arrives in the UK or
Ireland, its impact on the aquaculture industry
could be extensive, either through the fouling of
nets, cages, buoys, moorings, boat hulls and the
cultured species themselves (Williams et al., 2010),
or through their competition for resources. There
are several examples of non-native tunicates
already present in the UK and Ireland, which have
had a signicant economic impact in other
countries on aquaculture industries through
fouling: Didemnum vexillum (see Coutts and Forrest,
2007), Ciona intestinalis (see Ramsay et al., 2008),
Styela clava (see Thompson and MacNair, 2004)
and Botrylloides violaceus (see Bock et al., 2011).
Stachowicz et al. (2002) found that Botrylloides sp.
not only recruited earlier in years with warmer
winters, but also grew at a faster rate than native
tunicate species when the temperature was near the
maximum observed in the summer months. They
concluded that climate change may facilitate a shift
in dominance of non-native species, some of which
could prove costly for the aquaculture industry in
the UK and Ireland.
Concerns for the aquaculture industry include
the competition of non-native species for
resources. This may be competition for space and
food, or predation and parasitism by non-native
species. The Pacic oyster Crassostrea gigas, for
example, was introduced for aquaculture purposes
in the 1960s, and has since colonized northern
European Atlantic coasts. This has been linked to
a decline in farmed oyster performance over the
last 10 years in France (Cognie et al., 2006). The
range expansion coincided with increasing summer
seawater temperatures in the region, and C. gigas
can now be found in uncultivated regions on the
south coast of England, north-east coast of
Ireland, the French Atlantic coast, Norway and
the Wadden Sea, where the dense intertidal
hummocks of shell and live oysters can cause
signicant changes to the habitat structure
(Figure 3b) (Nehls et al., 2006; Syvret et al., 2008;
Dutertre et al., 2010; Wrange et al., 2010).
The distribution of non-native species is
predicted to experience signicant changes in
response to climate change, with many already
established species expected to spread northwards
into new areas (Smith et al., 2012). Improving
early detection and long-term monitoring
capabilities is urgently required, in conjunction
with increasing research on the interaction
between climate change and non-native species
and the effect on maritime industries, such as
aquaculture.
Jellysh
The term jellyshdescribes various types of
gelatinous zooplankton including scyphozoa,
siphonophores and hydrozoa (Richardson et al.,
2009). Jellysh tentacles contain toxic stinging
cells or nematocysts which are used to immobilize
planktonic and nektonic prey. Since jellysh
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numbers can also increase rapidly under the right
conditions, blooms of jellysh can cause serious
problems for nsh held in sea cages (Purcell
et al., 2007).
Damage is caused by small jellysh entering
through cage meshes, or by tentacles of larger
species breaking off and entering the cages. There
is evidence that the major impacts of jellysh to
caged nsh come from damage to the gills
(Baxter EJ et al., 2011). A recent study
demonstrated that even relatively short-term
exposure (2 to 48 h) to macerated Aurelia aurita
tissue could cause persistent gill damage to salmon
(Baxter EJ et al., 2011). Damage to the epidermis,
necrosis of the gills (Bruno and Ellis, 1985),
hypersensitivity to jellysh toxin (Seaton, 1989)
and secondary infections with pathogenic bacteria
introduced via the jellysh (Delannoy et al., 2011)
have all been implicated as causal agents in sh
mortalities. Additional problems can be low
oxygen caused by clogging of cage nets leading to
stress in the sh which will affect food conversion
and growth.
There are many examples of various jellysh
species causing sh kills, although they are often
anecdotal and in some cases the species
responsible was not identied (Purcell et al., 2007).
In August 1984, the leptomedusa Phialella
quadrata was reported to have caused the death of
1500 Atlantic salmon smolts at an unnamed
location in Shetland (Bruno and Ellis, 1985;
Seaton, 1989). This appears to be the rst
documented case of salmonid mortality related to
jellysh in Scottish waters in the scientic
literature. In November 2007, the small jellysh
Pelagia noctiluca swamped the cages of a salmon
farm in Northern Ireland, killing an estimated
250 000 sh (Doyle et al., 2008). Large blooms of
this species have been reported many times,
particularly in Ireland (Doyle et al., 2008), and the
implication is that jellysh impacts on sh farms
should be considered a real ever-present threat.
Different species of jellysh are of concern.
The lions mane jellysh (Cyanea capillata), the
moon jellysh (Aurelia aurita), the narcomedusa
Solmaris corona, Phialidium sp., Leuckartia
raoctona and Catablema vesicarium have all
caused problems for aquaculture businesses
(Seaton, 1989; Båmstedt et al., 1998; Purcell et al.,
2007). Caged sh cannot escape a jellysh bloom,
and in some cases amelioration measures such as
bubble curtains can make the situation worse if
the jellysh are broken up before they interact
with sh pens, and then the small fragments are
able to pass through the net mesh into the cage.
Whether incidence of jellysh induced sh kills
are increasing due to climate change is equivocal.
There is certainly growing concern over the
negative impacts of jellysh in marine systems.
Central to this issue is the suggestion that
overshing may lead to a proliferation of jellysh.
Termed shing down the food chain, it has
been argued that the progressive removal of
the largest sh in marine systems through
overshing, will eventually lead to an endpoint of
marine ecosystems dominated by jellysh and
other invertebrates (for review see Richardson
et al., 2009).
In addition to the concerns of shing down the
food chain, climate change may also be affecting
jellysh abundance. There have been a number of
studies in which time-series of jellysh abundance
spanning many years have been linked to various
climate indices such as the North Atlantic
Oscillation Index as well as water temperature and
precipitation (Lynam et al., 2004, 2011). Lynam
et al. (2011) suggested that climate change was
causing an increase in jellysh abundance, and
rising sea temperatures were cited as a factor
(Graham, 2001; Mills, 2001). However, there are
other potential causes for increases in jellysh,
including changes in the strength of inux of
oceanic water to shelf sea areas (Lynam et al.,
2010), eutrophication (Arai, 2001) and even
increases in hard surfaces, such as aquaculture
rafts and dock walls, which can provide settlement
sites for the benthic stages of some jellysh species
(Holst and Jarms, 2007; Lo et al., 2008). In some
regions, such as the Irish Sea, Japan, and
Mediterranean, there is empirical evidence that
warming conditions as part of climate change are
leading to increased abundance of certain jellysh
species (Richardson et al., 2009). However, in
other areas, such as the North Sea, fewer jellysh
have been found in warmer years. Furthermore
sometimes long-term trends in jellysh abundance
have not been sustained as time-series have
lengthened, such as in the Bering Sea (Brodeur
et al., 2008). Owing to these varying long-term
trends, generalizations about the impact of climate
change on jellysh abundance are hard to make
(Richardson et al., 2009).
In areas, such as the west coast of Ireland, where
climate change is expected to cause an increased
abundance of harmful jellysh in the future, then
increased sh kills at aquaculture farms are likely
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to result. For example, the jellysh P. noctiluca,
which caused the sh kill in Northern Ireland, is
generally considered a warm-water species that is
periodically advected to the more northern
latitudes of the UK and Ireland (Doyle et al.,
2008). For such warm water species we might
expect that the progressive ocean warming of the
last few decades in the NE Atlantic (Hobson et al.,
2008) will cause increased jellysh occurrence at
high latitudes. However, robust data to examine
this prediction are lacking. Furthermore, current
patterns may also be important in inuencing the
distribution of some jellysh (Purcell et al., 2007),
and the interplay of ocean warming in addition to
changing currents will need to be considered when
assessing likely future trends in jellysh abundance.
Jellysh have been a component of the pelagic
marine fauna that has generally been neglected by
scientists, compared for example with crustacean
zooplankton and sh. Hence there is a general
lack of data on long-term trends in jellysh
abundance in UK and Irish waters. Jellysh
populations are naturally highly variable; many
species respond to favourable conditions by rapid
population increases, making them difcult to
monitor (Boero et al., 2008; Gibbons and
Richardson, 2009). Observations of increases in
jellysh abundance over a limited time may only
show a part of a cycle and may be followed by a
subsequent decline (Brodeur et al., 2008). These
issues create problems for quantitative sampling of
jellysh populations, which are further exasperated
by their patchy distribution. Hence large-scale
efforts are usually required to produce robust
time-series of jellysh abundance (see Lynam
et al., 2011 for an example).
In Scotland individual farms and companies
record incidents, but there has been little attempt
to collate these data in order to identify regional
or temporal patterns (Nickell et al., 2010). There is
therefore a clear requirement for improved
monitoring to identify trends and to ascertain
whether outbreaks occur in specic localities.
Methods need to be developed that will allow
routine estimation of abundance to reproducible
standards at reasonable cost by farm operatives
(Purcell, 2009). Promisingly, jellysh surveys have
been conducted using sheries survey vessels that
were simultaneously undertaking sh stock
assessments, providing some of the best jellysh
time-series datasets to date in areas as diverse as
the Gulf of Alaska, North Sea and Irish Sea
(Lynam et al., 2004, 2011; Brodeur et al., 2008).
Continuation of existing surveys and initiation of
new surveys to other areas and seasons is a central
requirement to understanding the impact of
climate change on jellysh (see, for example,
Bastian et al., 2011). These surveys may also lead
to an understanding of the physicalchemical
conditions favoured by different species. In this
way it may be possible to model the climate
envelopeof conditions that species favour, and
hence model both historical and future ranges, as
has been done for other types of zooplankton
where better survey data exists (e.g. copepods;
Reygondeau and Beaugrand, 2011). The
availability of such models could eventually
provide warnings to the industry of impending
blooms, allowing industry to take precautionary
actions, such as harvesting or moving sh or
employing physical barriers around cages.
Development of new farm sites should also take
account of the potential for jellysh blooms.
Current sh-farm husbandry practices need to be
reviewed to ensure that they are not encouraging
localized blooms by providing additional polyp
substrate.
While jellysh pose serious threats to
aquaculture, in many Asian countries they are a
resource for commercial harvesting (You et al.,
2007). Jellysh may be cultured in ponds, often as
part of a polyculture of other harvested taxa (e.g.
sea cucumbers). In addition, jellysh may be
grown in articial conditions and then seeded
into semi-enclosed bays where they grow in
natural conditions prior to harvesting for human
consumption. The global trend is for increased
commercial harvesting of jellysh, although such
harvesting has yet to start in the UK or Ireland.
Harmful algal blooms
Harmful algal blooms (HABs) are a generic
description for any algal growth that is considered
by humans as being deleterious. Often such
harmful or toxic bloom species are actually
represented by a small fraction of the total algal
(phytoplankton) biomass. Although typied by
classic shellsh poisoning species, such as
Alexandrium, many tens of genera have deleterious
effects (Hinder et al., 2011). Potentially any algal
bloom, if large enough, can cause problems for
aquaculture. In addition, most HAB species are
not simply phototrophic phytoplankton, but are
mixotrophic protists that can not only
photosynthesize but also feed on dissolved and
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particulate matter (including other plankton as well
as detritus). As a consequence, their growth may be
promoted by factors other than supply of inorganic
nutrients. HABs are of particular concern for
mussel cultivation and the rearing of caged sh.
Some HABs are more appropriately termed
ecosystem disruptive algal blooms (EDABs)
(Sunda et al., 2006). These EDABs are formed
by phytoplankton which is indigestible by
zooplankton and hence block the normal ow of
energy and elements through the food chain.
Examples are large, mucus and foam-producing
forms, such as Phaeocystis. Any prolic
phytoplankton growth may potentially generate an
EDAB, by becoming inedible (probably due to
accumulation of noxious secondary metabolites)
when they become nutrient starved (Mitra and
Flynn, 2006). These organisms may also provide
poor feed for bivalves, and when dying, EDABs
cause further damage through decay (e.g.
hypoxia). Here the term HAB will be taken to
include EDABs.
The review of Bresnan et al. (2010) describes in
some depth many UK-centric issues relating to
climate change and HABs formation, and much of
the information is relevant for the shellsh industry.
HABs include dinoagellates such as Alexandrium,
associated with the production of paralytic
shellsh poisoning (PSP), Dinophysis producing
lipophillic shellsh toxins (LST), and diatoms such
as Pseudo-nitzschia linked to amnesic shellsh
poisoning (ASP). Incidences leading to closures of
shellsh harvesting areas are reported from Scottish
and Irish waters (Bresnan et al., 2010).
The relationship between climate change and
HABs is highly complex. Most HAB related
events are near-shore, although they may originate
off-shore through seeding and advection. In
general, however, they are greatly affected by
terrestrial processes, which are often linked to
anthropogenic activity. For instance, nutrient
inputs, changes to local marine ecosystems
affected by land use and human population
growth all have an impact on the occurrence of
HABs. More signicantly, increases in run-off,
either via changes to catchment land use or by
climatic drivers and climate change, also
contribute to the occurrence of HABs. While
eutrophication is a major driver in phytoplankton
growth, an imbalance in N:P ratios within the
organisms will promote toxicity (Youlian et al.,
1998). The emphasis on P removal in sewage
treatment, coupled with the looming predicted
crisis in P-fertilizer supply beyond the next two
decades, provides a high N:P supply ratio.
The ways in which climate change may affect N
and P run-off is associated primarily with the
pattern of rainfall, especially if ash oods
overwhelm sewage treatment works. Changes in
rainfall patterns may also have another impact
associated with HABs, as a decrease in run-off
may bring in less Si. Si stress is implicated with
toxicity for the diatom Pseudo-nitzschia australis,
now a common species off the UK (Youlian et al.,
1998).
However, marine processes equally affect
phytoplankton growth and succession. The
formation of algal blooms in coastal waters is
associated primarily with sunny, warm, and stable
water conditions. Elevated water temperatures
enhance growth rates, creating a knock-on effect
on zooplankton growth rates. The extent to which
primary and secondary productions are enhanced
pro rata, or whether HABs may proliferate, is not
clear. In local situations where bivalves are
important consumers of phytoplankton, factors
affecting these and members of the meroplankton
could be important. This may be especially so for
the growth of mixotrophic species, which depend
on the growth of other more benign organisms,
such as the Diuretic Shellsh Poisoning (DSP)
producing Dinophysis, which feeds on cryptomonads.
While terrestrial and marine processes have so far
been the focal points of explaining HAB formation,
ocean acidication is increasingly being recognized
as a contributing factor. Algal bloom formation
results in the alkalinization of water, as CO
2
,
nitrate, and phosphate are consumed. The more
eutrophic the water, the greater the biomass
development (elevating pH), and the calmer the
water conditions, the more rapid and higher the
pH rises. This pH rise is detrimental to algal
growth and is reported to affect species succession
(Hansen, 2002). Through ocean acidication the
starting pH for this process is lower, and hence the
succession events may be expected to be altered.
With the expected warming of the water,
succession may be affected further. On collapse of
the bloom the warmer waters and the lower nal
pH of the bulk water may also affect decay
processes leading to changes in water quality
beyond those experienced in recent centuries.
There is a long history of attempts to explain the
apparent increased frequency in HABs on a
global scale, with a corresponding continuing
international research effort (GEOHAB, 2011). In
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the UK, establishing whether such events are
increasing has been hindered by uncoordinated
and incomplete record keeping of plankton
composition (Bresnan et al., 2010). In addition,
the form of the heavily indented western coastline
can support locally important blooms which may
go unnoticed. Unfortunately, remote sensing to
detect algal blooms in UK and Irish waters is
often problematic due to cloud cover, necessitating
increased use of semi-automated samplers in
near-shore waters to cover this gap in knowledge.
Bresnan et al. (2010) suggest that condence
in the UK science base is medium, but that our
predictive ability is low. They identify a paucity
of experimental and modelling studies of
HABs species of UK importance as a problem
and recommend enhancing our autecological
understanding of the HAB species. In addition, we
should improve our understanding of EDABs in
general, while further investigating major UK and
Ireland blooming phytoplankton. While the link
to nutrient-status (water and phytoplankton),
temperature and ocean acidication do need to be
claried, there is also a need for information on
their competitors and consumers, both planktonic
and benthic. Recent work has shown a profound
shift in the relative abundance of diatoms and
dinoagellates in UK waters (Hinder et al., 2012).
Dinoagellates (both HAB and non-HAB taxa)
have declined markedly in abundance, while
diatoms (both HAB and non-HAB taxa) have
increased (Figure 6). These patterns have been
linked to the combined effects of rising water
temperatures and increasingly windy conditions
(Hinder et al., 2012).
EFFECTS ON GLOBAL FISHMEAL AND FISH
OIL RESOURCES
Much of UK aquaculture, particularly salmonid, is
currently dependent upon feeds formulated with
relatively high levels of marine shmeal (FM) and
sh oil (FO) derived from industrial, feed-grade
(reduction) sheries of small pelagic species. The
reduction sheries are at their sustainable limits
and, over the last 30 years, around 2025 million
tonnes (Mt) of feed sh have been caught
annually, which reduce to about 67MtofFM
and 1.01.4 Mt of FO (IFFO, 2011). Aquaculture
is the fastest growing food sector with production
increasing by an average of almost 9% per
year (FAO, 2009). Between 1992 and 2006,
consumption of FM and FO for aquaculture
increased from around 15% and 20% of global
supplies, respectively, to around 68% and almost
89%, respectively (Tacon, 2005; Tacon and
Metian, 2008). There is no realistic prospect of
FM and FO production being increased in the
future, and indeed, there is increasing competition
for these small pelagic species for direct human
consumption (Tacon and Metian, 2009a, b).
Therefore, the global FM and FO market is one
Figure 6. There have been profound changes in the abundance and
distribution of dinoagellates and diatoms in the NE Atlantic region
(including the North Sea) related to increasing water temperatures
and increasingly windy conditions. Dinoagellates (both HAB and
non-HAB taxa) have shown a marked decrease in abundance in
Continuous Plankton Recorder (CPR) samples while diatoms (both
HAB and non-HAB taxa) have tended to increase, so that the relative
abundance of diatoms to dinoagellates has increased. The plots show
changes in the distribution and abundance of one diatom taxa
(Thallasiosira) and one dinoagellate (Ceratium furca) derived from
the CPR survey (modied from Hinder et al., 2012). Colour scale is
based on log transformed numbers of cells per CPR sample and
provides a relative measure of the abundance of taxa. Image shows a
CPR being deployed in the North Sea.
R. CALLAWAY ET AL.410
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of nite and strictly limited supply and ever-rising
demand. It is accepted that climate change is likely
to play a signicant role in changing the
productivity, seasonality and distribution of marine
ecosystems and their resources in the future (Glantz,
2005). For instance, there are increased captures of
boarsh (Capros aper) in the NE Atlantic off
Ireland that may be related to climate change
affecting stocks. This species is contributing to FM
(although not FO) production, but they may simply
be displacing other pelagic species, mainly sandeel,
rather than representing an increased resource.
Therefore, looking forward, global FM and FO
supplies are uncertain and currently our capacity to
predict and respond to these impacts is limited
(Merino et al., 2010a, b).
The largest reduction shery is on the eastern
South Pacic seaboard (Chile/Peru; anchovies and
sardines), with other major sheries in Asia
(Thailand and Japan), North America (USA,
Mexico and Canada; menhaden, capelin) and
Scandinavia (blue whiting, herring, mackerel, etc.).
Climatic events are well-known to affect FM and
FO supplies. The El Niño-Southern Oscillation
(ENSO), which occurs periodically across the
tropical Pacic Ocean, is characterized by
variations in surface ocean temperature (El Niño,
warming and La Niña, cooling), which can
dramatically affect the reduction sheries. El Niño
reduces the upwelling of cold, nutrient-rich water
decreasing the phytoplankton that sustains the
large sh populations, and in the 1972 event the
Peruvian anchoveta reduction shery collapsed.
The last major El Niño in 19971998 reduced
production of FO to under 0.8 Mt and of FM to
around 5 Mt (IFFO, 2011), which affected
aquaculture through increased prices. If repeated
now, a similar reduction in global FO stocks
would have severe supply implications as well.
Climate change impacts are likely to amplify these
natural variations and to exacerbate existing
stresses on marine sh stocks. Studies of global
warming in the ocean have shown that the
south-east Pacic region has not registered a sea
surface temperature increase during the last
50 years, as has happened in most other regions.
However, Peru has initiated a major study to
assess the impact of climate change on the sardine
and anchovy sheries in the Northern Humboldt
current system, the Peru Ecosystem Projection
Scenarios project (PEPS, 2009). Effects of climate
change on other sheries are under similar
investigation, and the UK project, QUEST-Fish, is
currently investigating how climate change would
potentially affect future production of global
sheries resources (Barange et al., 2010a, b).
Although there is a slight but denite downward
trend in global captures of feed sh in the
last 30 years (IFFO, 2011), there is no direct
evidence that this is solely due to climate change,
and other factors, not least shing pressure, could
be the cause.
Within the aquaculture sector, the continued use
of FM and FO as major feed ingredients has been of
considerable concern for many years. The nite,
limited supply and rising demand for global FM
and FO has resulted in generally increasing prices
with climatic variability introducing further
instability and pressure on supply and prices
(Mullon et al., 2009). There are also increasing
concerns over the use of marine products for
animal feeds, with aquaculture especially perceived
to be driving exploitation of marine sheries
(Naylor et al., 2000). Regulation of the permitted
levels of contaminants in animal feeds is also a
concern restricting the use of FM and, especially,
FO from specic geographical locations such as
the Baltic (Tocher, 2009). All these factors have
dictated that, for aquaculture to continue to
expand, solutions to the problems of FM and FO
supply must be found and this has prompted
considerable research (Naylor et al., 2009). Most
of this effort has been directed towards
developing other, more sustainable alternatives as
replacements for FM and FO as feed ingredients
(Tocher, 2009). Alternative marine resources such
as exploiting lower trophic levels (zooplankton) to
produce meals and oils, and/or the use of sheries
by-products (white sh and aquaculture wastes)
have signicant ecological, health and other
worries (Olsen et al., 2010). Therefore, the current
favoured solution is the use of terrestrial plant
meals and vegetable oils as replacements for
FM and FO, respectively. Maximal levels of
replacement that can be applied without affecting
production and nutritional quality vary with
species, with salmonids allowing greater levels of
replacement than marine species such as cod, sea
bream, and sea bass. Levels of replacement also
vary with region, with replacement of FM and FO
in Atlantic salmon farming, being higher in Chile
and Norway than in the UK. These efforts along
with improvements in farming practices have
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greatly increased the efciency of aquaculture
activities in converting dietary nutrients into
human food, often calculated as a sh-in sh-out
(FIFO) ratio (Kaushik and Troell, 2010). Thus,
the FIFO ratio is decreasing for all species
across all aquaculture sectors (Tacon and Metian,
2009a, b).
The FM/ FO debate has also focused attention
on the great differences within global aquaculture,
with the greatest use of FM and especially FO for
the high-value, high-trophic level carnivorous
species generally farmed in the economically
developed countries (Tacon et al., 2010). This has
prompted the suggestion that future aquaculture
development should focus more on farming of
species of lower trophic level and less dependent
upon dietary FM and FO. This would require
some change in consumer perception and
acceptance of new, less familiar, farmed species. A
similar situation exists with another possible
long-term solution such as the use of transgenic
approaches, primarily the engineering of plant
crops to suit aquaculture needs, but also the
possibility of engineering farmed sh to suit the
alternative feeds (Tocher, 2009).
CONCLUSION
Direct effects of climate change on the UK and
Ireland aquaculture sector have so far not been
quantiable, and current evidence of impact is
speculative. There are several potential reasons for
this.
First, it is possible that climate change has indeed
so far not translated into measurable effects on the
UK and Ireland aquaculture sector. Impacts such
as storms, diseases or temperature variations are
continuously dealt with by the industry, and it is
difcult to separate climate change from natural
variations in environmental conditions. Also, the
aquaculture sector is relatively young in the UK
and Ireland and the pace of technological progress
has been rapid, as illustrated by developments
in cage design, feed formulation, and
pharmaceuticals. Swift adaptations and high
resilience of the industry may have outweighed the
comparatively slow pace of climate change thus
far. Although future problems with parasites and
diseases in nsh aquaculture may be controlled
through intervention, it will be at increasing cost.
Importantly, measuring the effects of climate
change demands systematically collected monitoring
data. This is a pre-condition for establishing
baselines and discovering signicant trends against
which new observations can be compared. While
such long-term data exists for wild sh populations
from stock assessments, information is sparse for
the aquaculture sector. Some relevant data on, for
example, storm damage, growth rates, availability
of spat or fouling of cages, is held by individual
enterprises, but little of this is publicly available, nor
is it collated systematically.
The level of threat from climate change depends
on the degree of reliance that individual sections
of the aquaculture industry place on prevailing
environmental conditions. Bivalve farming, which
depends on wild spat for stock, plankton for food
and water quality for health, is highly susceptible
to various effects of climate change. In
comparison salmon farming is more independent
from the natural environment since feed supply
and offspring are managed. Nonetheless, cages are
vulnerable to storm damage and fouling, and the
sh are exposed to parasites and pathogens
occurring in the surrounding water. At the other
end of the spectrum, marine aquaculture systems
can be engineered to completely isolate livestock
from the surrounding environment, e.g. land-based
recirculating aquaculture systems. It is anticipated
that this form of aquaculture will increase in the
future to enable continued supplies of established
aquaculture species, irrespective of changing
environmental conditions.
In terms of opportunities arising from warming
coastal waters, it is compelling to envisage the
possibilities of rearing warmer water species. For
the bivalve industry climate change could open
opportunities for rearing the Pacicoysterinwaters
currently unsuitable for the species, although in the
wild this non-native species is likely to compete with
mussels or native oysters. Similarly, warmer water
nsh species, e.g. sea bass, could potentially
displace salmon farming in certain locations. While
this is technically a valid argument, market forces
are more likely to determine whether or not a new
species is cultured. Salmon production meets
consumer demand; the industry is established and
protable. If environmental conditions became
unsuitable for salmon cultivation, it is considered
more likely that measures will be taken to overcome
the emerging obstacles, rather than endeavouring to
substitute the species.
However, demands do change. New opportunities
may arise by shifts and changes in wild sh stocks in
R. CALLAWAY ET AL.412
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response to climate change. If, for example, cod
landings were to decline substantially while the
consumer demand remained, higher prices would
open opportunities to expand the rearing of this
species. Further opportunities may arise from
hatching early development stages of shellsh and
nsh for the restocking of wild populations.
Small-scale experiments are already underway for
lobsters and bivalves, but this process could gain
importance for other species. Hence, the effects of
climate change on wild sh stocks and sheries may
indirectly have a greater effect on the UK and
Ireland aquaculture sector than direct effects on
currently farmed species.
Invading species and particularly jellysh pose a
real threat because they can wipe out entire
salmon cage sites within days. Since jellysh
blooms are suspected to be affected by climate
change, and their abundance is possibly linked to
developments in the wild sheries, efforts to
improve the monitoring of jellysh should be
supported.
Possibly the greatest challenge for marine sh
farming lies in the replacement of shmeal and sh
oil as a main ingredient in formulated feeds.
Climate change plays a part in the declining stocks
of small pelagic sh species such as anchovies and
sardines, although shing pressure is likely to be of
greater importance. Furthermore, shmeal and
sh oil is a nite resource and limits the expansion
of the aquaculture sector. Terrestrial plant meal
and vegetable oils are currently being evaluated as
replacements, but their production competes
with other farming and land-use interests. An
opportunity for the UK and Irish aquaculture
sector arises from the production of omega-3 rich
oils from microalgae and other microorganisms.
Improving understanding about the degree to
which climate change affects aquaculture in the
UK and Ireland requires research that addresses
large spatial and temporal scales. In order to gain
scientically rigorous insight into effects of climate
change on the aquaculture sector, publically
available nationwide information needs to be
collected, at least for the most pressing threats
to the industry. However, while long-term
monitoring is desirable, this may be unlikely to be
resourced in the current and foreseeable economic
climate. There may have to be reliance upon an
iterative development of predictive models, which
are validated using a patchwork of data emerging
from experimental and observational studies.
In the near term, priority should be given to
elucidating the impact of climate change on
bivalve aquaculture, as this sector has fewer
technological and pharmaceutical tools to respond
to challenges. In addition, the effects of changing
rainfall and run-off patterns on coastal water
quality need clarication. This is particularly
important in mussel growing areas that are located
in shallow waters and estuaries, such as is
common in England and Wales. Understanding
the likelihood of deteriorating water quality due to
climate change is an urgent challenge.
ACKNOWLEDGEMENTS
The following authors were funded by the ERDF
funded project SEACAMS: R Callaway, SE
Grenfell, KJ Flynn, AF Mendzil and R Shields.
GC Hays was supported by the ERDF Interreg
IVa project EcoJel and by the Climate Change
Consortium for Wales (C3W). The ERDF
INTERREG IVA, Highlands and Islands
Enterprise, Crown Estate, Northern Ireland
Executive, Scottish Government and Irish
Government funded BioMara project supported
MS Stanley. C Fox, K Davidson and T Nickell
acknowledge the support of the Crown Estate. The
ERDF Interreg IVa project SUSFISH supported
AF Rowley, S Malham, E Wootton and S
Culloty. Sites of aquaculture enterprises in
Northern Ireland were kindly provided by Jenny
Smyth of Aquaculture and Fish Health, DARD.
Miranda Walker (Swansea University) assisted in
producing Figure 5. The paper was commissioned
by the Marine Climate Change Impact Partnership
(MCCIP) and we thank the members for their
encouragement and continuous support. The
partnership also provided invaluable comments to
an earlier draft of the manuscript. We thank the
editor John Baxter and two anonymous reviewers
for their constructive comments on the manuscript.
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