Environmental Research 251 (2024) 118561

Contents lists available at ScienceDirect

Environmental Research
journal homepage: www.elsevier.com/locate/envres

Review article

Climate change impacts on oyster aquaculture - Part I: Identification of

key factors
Emmanuel Okine Neokye a, b, Xiuquan Wang a, b, *, Krishna K. Thakur c, Pedro Quijon d,
Rana Ali Nawaz a, b, Sana Basheer a, b
a
Canadian Centre for Climate Change and Adaptation, University of Prince Edward Island, St. Peter’s Bay, Prince Edward Island C0A 2A0, Canada
b
School of Climate Change and Adaptation, University of Prince Edward Island, Charlottetown, Prince Edward Island C1A 4P3, Canada
c
Department of Health Management, Centre for Veterinary Epidemiological Research (CVER), Atlantic Veterinary College, University of Prince Edward Island,
Charlottetown, Prince Edward Island C1A 4P3, Canada
d
Coastal Ecology Laboratory, Department of Biology, University of Prince Edward Island, Charlottetown, Prince Edward Island C1A 4P3, Canada

A R T I C L E I N F O A B S T R A C T

Keywords: Oysters are enriched with high-quality protein and are widely known for their exquisite taste. The production of
Climate change oysters plays an important role in the local economies of coastal communities in many countries, including
Oyster aquaculture Atlantic Canada, because of their high economic value. However, because of the changing climatic conditions in
Oyster production
recent years, oyster aquaculture faces potentially negative impacts, such as increasing water acidification, rising
Climate factors
Greenhouse gas emissions
water temperatures, high salinity, invasive species, algal blooms, and other environmental factors. Although a
few isolated effects of climate change on oyster aquaculture have been reported in recent years, it is not well
understood how climate change will affect oyster aquaculture from a systematic perspective. In the first part of
this study, we present a systematic review of the impacts of climate change and some key environmental factors
affecting oyster production on a global scale. The study also identifies knowledge gaps and challenges. In
addition, we present key research directions that will facilitate future investigations.

1. Introduction grazers (Kluger et al., 2017). They are crucial in controlling the depth of
light penetration and the quality of the water because of their filtration
Oysters are highly preferred species in aquaculture because of their activities (Petersen et al., 2016). Energy flow patterns from the pelagic
resilience to severe environmental conditions. However, they are sus­ environment to the benthos are altered by oysters. Oysters are widely
ceptible to climate change and its induced hazards. Oysters are highly distributed across the globe. For example, the eastern oyster (Crassostrea
valued for their economic, cultural, nutritional, and ecological impor­ virginica) has a wide geographical and latitudinal distribution. They are
tance. With an estimated 9 billion people on the planet by 2050, oyster found in the Gulf of St. Lawrence, the Caribbean, and the Gulf of Mexico
cultivation will guarantee food security (Shumway et al., 2003; Godfray according to Lazoski et al. (2011). Oysters are ectotherms and euryha­
and Charles, 2010). Over the past decades, the production of oysters has line, however, they thrive in shallow estuaries where water temperature
been steadily increasing and is expected to continue (FAO, 2019, 2023). varies seasonally between − 1.5 ◦ C and 22 ◦ C.
They are regarded as both keystone species and ecosystem engineers in At both the regional and global levels, there has been substantial
the aquatic environment (Gutiérrez et al., 2003; Han et al., 2017). research and review on how climate change will impact oyster aqua­
Oysters engage in top-down and bottom-up interactions with their en­ culture (Okon et al., 2023; Gabrielle et al., 2021). However, these
vironments (Coen et al., 2007). However, the top-down control via studies focused on climate change impacts on oyster diseases and
filter-feeding could dramatically reduce phytoplankton populations oyster-predator dynamics. Also, the study used increasing water tem­
(Cranford et al., 2003; Newell, 2004; Forsberg et al., 2017) potentially perature as a key factor to the susceptibility of disease and predator
affecting oyster performance itself (Bacher et al., 2003; Strohmeier interaction in the oyster ecosystem. From the broader perspective,
et al., 2005). Additionally, they also impact other filter-feeders and comprehensive research has been done regarding the potential impact of

* Corresponding author. Canadian Centre for Climate Change and Adaptation, University of Prince Edward Island, St. Peter’s Bay, Prince Edward Island C0A 2A0,
Canada.
E-mail addresses: [email protected], [email protected] (X. Wang).

https://doi.org/10.1016/j.envres.2024.118561
Received 22 December 2023; Received in revised form 23 February 2024; Accepted 25 February 2024
Available online 2 March 2024
0013-9351/© 2024 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-
nc/4.0/).
E.O. Neokye et al. Environmental Research 251 (2024) 118561

Fig. 1. Global aquaculture production from 1950 to 2020.

(Source: FAO, 2020).

climate change on aquaculture in general (De Silva and Soto, 2009;

Table 1
Bueno and Soto, 2017; Clements and Chopin, 2016; Yazdi and Shakouri,
Oyster species and their geographical distributions around the world.
2010; Chung et al., 2017; Froehlich et al., 2017; Handisyde et al., 2006;
Harvey et al., 2017; Kluger et al., 2017; Dabbadie et al., 2018). Also, the Common Name Scientific Name Geographical Distribution
present literature studies do not examine how climate change scenarios American cupped Crassostrea USA, Canada, Dominica Rep.
are utilized to forecast future oyster production. Therefore, this review is oyster virginica
Pacific cupped Crassostrea gigas China, Japan, Korea, Thailand, Australia,
essential to promote producers’ preparedness and help minimize the
oyster NZ, Malaysia, Canada, US, Mexico,
risks and impacts of climate change on oyster aquaculture. Such infor­ France, Ireland, Netherlands, Channel Is.,
mation is particularly helpful in determining the best climate change UK Spain, Portugal.
actions aimed at sustainable management of oyster resources. European flat Ostrea edulis France, Ireland, Netherlands, UK, Spain,
Therefore, the objective of part 1 of this study is to systematically oyster Portugal, Channel Islands.
Hooded oyster Saccostrea Mauritius
review and summarize (i) the impacts of climate change on oyster
cuccullata
aquaculture production, and (ii) Identify key environmental factors Gasar cupped Crassostrea Senegal, Gambia
affecting oyster production. More significantly, this review also iden­ oyster gasar
tifies the research gaps, challenges, and future directions for the oyster Cortez oyster Crassostrea Mexico, Chile
corteziensis
aquaculture industry.
Chilean flat oyster Ostrea chilensis Chile
Mangrove cupped Crassostrea Cuba, Puerto Rico, Jamaica
2. Global aquaculture and oyster production oyster rhizophorae
Olympia oyster Ostreola USA
conchaphilia
2.1. Global aquaculture production
Indian backwater Crassostrea India, Sri Lanka
oyster madrasensis
Globally, the aquaculture industry is expanding and now accounts Slipper cupped Crassostrea Philippines
for a larger portion of fisheries production. Asia and particularly China oyster iredalei
account for the majority of the world’s aquaculture production. Aqua­ Sydney rock oyster Saccostrea Australia
glomerata
culture plays an important role in the livelihoods of people from diverse
Portuguese oyster Crassostrea Portugal
backgrounds. There are about 9.5 million aqua culturists in Asia and angulata
many more people will likely be involved in supplying a range of goods West African Crassostrea West Africa (Ghana)
and services to the sector FAO (2020). Although the average rate of mangrove oyster tulipa
growth in the aquaculture sector appears to have slowed in recent years
compared with the rapid growth seen during the 1980s and 1990s,
production from 1950 to 2020.
continued expansion is predicted for the coming decades as a result of
increasing demand for fish and the limited production capacity of cap­
2.2. Global distribution of oyster species
ture fisheries. As a result of economic pressures and the increased
development and spread of aquaculture technologies, it seems likely that
Oysters are widely distributed and can be found throughout the
a general trend towards more intensive cultural practices will occur.
world. In North America alone, there are at least 150 varieties of oysters.
According to the FAO (2020), the total fisheries and aquaculture pro­
Globally, farmed oysters include over twelve different species both
duction have had a significant growth in the past seven decades going
native and introduced as shown in Table 1. Most of the oyster species
from 19 million tonnes (live weight equivalent) in 1950. This increased
used in aquaculture farming can be found naturally in shallow depths in
to a record of about 179 million tonnes in 2018. Additionally, the
marine and brackish areas that are closer to the coast. In principle,
aquaculture sector expanded at a 3.3% annual rate. Aquaculture pro­
oyster can close their shells during harsh environmental conditions. This
duction declined marginally in 2019 (a fall of 1 % compared with 2018)
includes changes in salinity and water temperature. Most critically, they
but increased by a mere 0.2 % to reach 178 million tonnes in 2020. The
become exposed during low tide when salinity declines. Their ability to
total combined value of fisheries and aquaculture production in 2020
adapt makes oysters a good species for aquaculture. More importantly,
was estimated at USD 406 billion. However, aquaculture production
they can be farmed in locations that are accessible at low tide.
alone had a value of USD 265 billion. Furthermore, the marginal decline
since 2018 could be due to the impact of the novel COVID-19 as sug­
gested by FAO (2020). Fig. 1 is an illustration of global aquaculture

2
E.O. Neokye et al. Environmental Research 251 (2024) 118561

Fig. 2. Global oyster production (Metric tonnes) and key oyster-producing countries in 2018.
(Source: FAO, 2019).

Fig. 3. The life cycle of oyster (Crassostrea virginica).

2.3. Global oyster aquaculture production days to reach the d-hinge veliger stage. Then two shells (“bi-valves”) and
the “velum” an organ for movement and eating develop. The free-
Since 1990, oyster aquaculture production has grown significantly, swimming larval oyster grows a foot (ped) after about 2–4 weeks and
from 1.2 million tonnes to 6 million tonnes in 2018 with a value of US becomes ready to firmly attach itself to a hard surface, typically an old
$7.46 billion. China consumes almost all of its production, accounting oyster shell, during the pediveliger stage. A spat develops once the
for about 85% of the world’s oyster production (FAO, 2019). In addition, pediveliger is firmly attached and begins to grow for about six months.
around 50,000 tonnes of oysters are traded annually on the global From this permanent spot, the young spat filters algae from the water
market. Countries like Korea, France, and China are major exporters of and grows quickly. After a few months, the spat grows to a size of about
oysters. The top three EU nations for oyster imports are France, Spain, 5 mm long and 4 mm wide and reaches the juvenile stage. The oyster
and Italy, although France is also one of the top exporters (FAO, 2019). grows throughout the juvenile stage until it becomes an adult. Once the
Oysters have a relatively short shelf life, which hinders large-scale in­ oyster reaches the adult stage, it can reproduce, and the life cycle con­
ternational trade because consumers frequently prefer live, in-shell tinues in the next generation. However, the majority of oysters are male
oysters or freshly shucked meats. Furthermore, value-added and con­ when they first reach adulthood and change to female as they age. Fig. 3
venience products, including canned oysters and frozen or is an illustration of the life cycle of oyster species.
vacuum-packed oysters prepared with various sauces, can potentially be
distributed globally. Fig. 2 shows the leading oyster-producing (Nations, 3. Environmental factors affecting oyster production
2018).
3.1. Effects of CO2 and global percentage share of emissions

2.4. The life cycle of oyster species According to Maulu et al. (2021), the absorption and increasing
amounts of anthropogenic activities that release CO2 into the oceans and
The first stage of the oyster’s life cycle begins when the gametes are water bodies result in acidification. This has detrimental impacts on
fertilized and the cells divide into an embryo. It takes about 2 days to shell-forming aquatic life, especially oysters. Since the industrial revo­
reach the trochophore stage. Then hair-like structures called “cilia” lution, there has been about a 26% increase in water acidity. However,
develop allowing it to move through the water column. It takes about 20

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E.O. Neokye et al. Environmental Research 251 (2024) 118561

Fig. 4. Pathways through which climate change will affect oyster aquaculture.

services needed by oyster farmers. Fig. 4 is an illustration of how

increasing concentration of greenhouse gas (GHG) emissions in the at­
mosphere will impact on oyster culture production.
Although aquaculture activities, such as power input, transportation,
and feed production are considered the main pathways of the sector’s
contribution to GHGs, its contribution is relatively minimal. This is
because when compared to other food production sectors it is signifi­
cantly less. For example, the effect of aquaculture on carbon dioxide and
other global warming gas emissions in 2010 was estimated at 385
million tons. This was about 7 % of the agricultural sector’s contribution
that year (Maulu et al., 2021). Fig. 5 displays the global emissions dis­
aggregated by species group. In addition, the geographical pattern of
emissions closely mirrors production. Also, the aquaculture farm energy
usage and N2O emissions account for the majority of the non-feed
emissions.
MacLeod et al., 2019, did a comprehensive analysis of CO2 emission
by specific species with a focus on a global perspective. His analysis was
based on the total emissions disaggregated by species group,
geographical region, and emission category.
Fig. 5. Global percentage share of calculated CO2 emissions by species in 2019.
The majority of emissions originated in the areas with the highest
(Source: MacLeod et al., 2019). productivity (e.g., East Asia and South Asia). For the majority of species
groups, emissions and production are also highly correlated, e.g., cyp­
rinids are responsible for 34 % of emissions and 32 % of production.
this trend is expected to continue in warmer low and mid-latitudes
However, there are some exceptions. For instance, from the global
(FAO, 2019). For about two decades, long-term dramatic decreases in
perspective, shrimp account for 18 % of emissions but only 9 % of
ocean pH have been observed throughout the North Atlantic. In addi­
production, while bivalves produce 9 % of emissions but represent 23 %
tion, it has been predicted that the pH of both oceans and water bodies is
of production (Fig. 5).
expected to decline further. In principle, this will affect commercial
shellfish or the early life stages of cultured oyster species and this has a
repercussion on their survival rate (FAO, 2019). The increasing acidity 3.2. Global emission of aquatic N2O
of coastal water bodies is a threat to oyster aquaculture. This is because
the absorption of CO2 and partial pressure of CO2 (pCO2) is higher in Several factors are accounting for the increasing amount of N2O gas
coastal waters than in the open ocean (FAO, 2019). The impacts of in aquaculture systems. They include the type of feeding rate, water
climate change on aquaculture production are both direct and indirect. exchange rate, dissolved oxygen, pH, water temperature, etc. Microbial
The physical state and physiology of finfish and shellfish production activities such as nitrification and denitrification on a fish farm result in
systems are among the immediate effects. Additionally, indirect conse­ N2O emissions according to Hu et al. (2012). In principle, nitrous oxide
quences could result from changes to input supplies, ecosystem struc­ (N2O), stays in the atmosphere and is then converted to nitrogen oxide
ture, and secondary production. This may affect product prices, (NO2) which in turn depletes the stratospheric ozone layer and exposes
especially spat feed (formulated algae) as well as other goods and the earth to more solar radiation resulting in warmer temperatures.

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E.O. Neokye et al. Environmental Research 251 (2024) 118561

However, it is challenging to quantify the emissions from the surface of a brackish water culture which are of high economic value species
pond or estuary to the atmosphere. N2O emissions from fish farms Handisyde et al. (2006); Kibria et al. (2017). In recent years, the sea
depend on pH and dissolved oxygen content and both fluctuate greatly level has increased by an average of 3.1 mm/year as a result of climatic
(Bosma et al., 2011). For calculation purposes, Hu et al. (2012) included and non-climatic factors (Dangendorf et al., 2017). The rate of increase
the N2O emissions from ponds to illustrate their likely contribution to varies greatly by region, with Western Pacific having values up to three
the total emissions, and to allow the comparison of the GHGs associated times the global average and Eastern Pacific having values of either zero
with aquaculture products. In their analysis, they were able to determine or negative. Over the past century from 1901 to 2010, the sea level rose
the amount of N2O. This was done by multiplying the production by by a global average of 0.19 m. It is projected that between 2000 and
emission factor per kg of production (i.e., 1.69 gN2O–N per kg of pro­ 2100, the global mean sea level rise (SLR) will very likely (90 % prob­
duction, or 0.791 kgCO2e/kgLW production). Furthermore, this is ability) reach between 0.5m and 1.2m under RCP8.5, 0.4m–0.9m.
greater than the 0.71% utilized by Henriksson et al. (2014) in the Furthermore, under RCP4.5, 0.3m–0.8m under RCP2.6 (Kopp et al.,
calculation, which translates to a conversion rate of N to N2O–N of 1.8 2014).
%.

3.3. Water temperature 3.5. Changes in precipitation patterns

The physiology, gene expression, distribution, as well as health of Changes in rainfall patterns will affect oyster production and sus­
oysters, are influenced by water temperature (Zippay and Helmuth, tainability in two different ways. The increase in rainfall will cause
2012; Shelmerdine et al., 2017). The ectothermic nature of oysters flooding while low periods or no rainfall will eventually result in
makes their internal body temperature match that of external water drought. According to the IPCC et al. (2018), risks resulting from
temperatures. This is exceptional for intertidal species which are subject drought events are likely to be higher at 2 ◦ C compared with 1.5 ◦ C of
to aerial exposure. Although the effect of temperature on physiology is global warming in a given region, while flooding event patterns are
species-specific, generally, as water temperature increases, physiolog­ difficult to predict with certainty. Studies have shown that increased
ical rates will increase until a threshold is met, and this will eventually patterns of rainfall, particularly in low-lying coastal areas will cause
result in a performance decrease (Kooijman, 2010). The relationship production risks in aquaculture farms (Bell et al., 2010). Some of the
between physiological functions such as dissolved oxygen consumption risks include losing cages during floods. Secondly, the invasion of cages
and filtration rates, and variations in temperature over short periods will by unwanted species. Thirdly, damage to cages and washing away
inevitably affect how long they can survive (Malham et al., 2009). In (Rutkayova et al., 2017). The excessive influx of rainwater in oyster
addition, the long-term changes (years) will impact their reproductive farms, especially those in the wild, could negatively affect environ­
timing and effort, and consequently their spatial distribution (Kittner mental sustainability. Furthermore, this could also lead to water quality
and Riisgård, 2005; Filgueira et al., 2014). The impact of climate change deterioration and high turbidity due to runoff. Additionally, losses from
and the relationship between water temperature and the physiology of cages pose a challenge to the social and economic aspects of aquaculture
oysters is very crucial. Most importantly, high-temperature intervals sustainability by reducing the financial rewards for the farmers. How­
may favor the growth of aquatic species. This is more prevalent in ever, drought may lead to water shortage and cause stress to oysters.
temperate locations. Specifically, this will favor the production of Furthermore, this could lead to water quality deterioration and may
warmer aquatic species, such as the giant tiger prawn, tilapia, oysters, have negative effects on aquaculture production (Hambal et al., 1994).
and mussels (Pickering et al., 2011; Guyondet et al., 2018; Colden and Shortage of water through changes in the pattern of precipitation is
Lipcius, 2015). Along with the increasing water temperature due to likely to cause disputes among users especially those engaged in aqua­
global warming, the IPCC et al. (2021) has predicted extreme climate culture, and agriculture, as well as domestic and industrial users
phenomena such as heavy rains, heat waves, and droughts. Seasonal and (Handisyde et al., 2006; Barange et al., 2018).
interannual variations in water temperature and salinity caused by these
occurrences will have a considerable impact on organism survival and
behaviors in the aquatic ecosystem. Therefore, species inhabiting the 3.6. Ice surface layer formation
coastal and intertidal areas, especially oysters, will be vulnerable to such
changes. However, the stress induced by temperature and salinity fluc­ Although, there is little scientific information on the effects of snow
tuations are distinct from each other (Woodin et al., 2020). on oyster aquaculture. Ice surface layer formation in winter can be a
serious threat to aquatic organisms especially those cultured in ponds,
3.4. Sea level rise bays, and estuaries. Ice surface layers can inhibit the rate of photosyn­
thesis and dissolved oxygen during the winter season. Furthermore, it
Sea level rise will negatively impact oyster aquaculture breeding may impede respiration of the aquatic organisms. Additionally, the ice
programs and the economic sustainability of the sector. The influx of surface layer depending on the depth can hinder the filter-feeding ability
saline water caused by sea level rise is projected to have an impact on of oysters. Furthermore, it poses a significant threat to the life cycle of
aquaculture production infrastructure, including ponds, cages, and oysters. In principle, the mortality of cultured species is highly probable
pens, especially in lowland areas (Kibria et al., 2017). Oyster aquacul­ in such situations. At extremely low temperatures oysters may hiber­
ture production and freshwater fisheries resources are known to be nate. This will result in retardation in growth and affect the quality of
negatively impacted by salinization (Handisyde et al., 2006; Kibria meat and the market price. Oysters living in their natural environment
et al., 2017). Additionally, changes in species composition, organism are more likely to be affected by the ice surface layer than those
abundance and distribution, ecosystem productivity, and phenological cultured. This is because cultivated oysters are more carefully controlled
shifts are likely to be brought on by sea level rise, particularly in farms during their early life stages before they are released into farms. For
located near estuaries. As a result, this could endanger the growth of instance, oyster farmers, particularly in Prince Edward Island (PEI),
cultured oysters in low-lying coastal areas (Doney et al., 2012). There Canada lower their cages deeper in the water column in winter condi­
are associated benefits with aquaculture activities that are social and tions when an ice surface layer is formed. Ice layers also increase pro­
environmental which are explored by coastal communities. However, duction costs since, particularly in PEI, producers must use chainsaws to
these activities are directly and indirectly affected by rising sea levels, cut through the ice before they can harvest oysters in winter. Future
thereby endangering the production and sustainability of the sector. On research could therefore concentrate on the effects of snow ice on the life
the positive side, sea-level rise may increase the areas suitable for cycle of oysters.

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Fig. 6. The effects of GHG emissions (N2O, CO2) and other factors affecting oyster production.

3.7. Siltation and sedimentation can decrease light penetration needed for photosynthesis. Therefore,
decreasing food production and dissolved oxygen solubility to levels
High levels of siltation are known to be deleterious, especially to that are harmful to oyster populations. In principle, eutrophication is
eastern oysters (Crassostrea virginica), and the collective effect of sus­ one of the primary causes of increased turbidity in marine environments
pended and bedded sediment is understudied from the perspective of (GESAMP, 1990). Turbidity also affects the ecosystems of oyster reefs by
oyster farming and bed restoration (Poirier et al., 2021). Sediments may altering interactions between predators in the food web. According to
cover the cages of oysters and prevent water flow through the cages. (Lunt and Smee, 2014), it affects the distribution of mobile species and
Oysters are ecosystem engineers, therefore the detrimental impacts of alters predation levels and the abundance of intermediate predators,
siltation on both larval and adult oysters may eventually have cascading which indirectly alters food webs. Turbidity is known to have an indirect
repercussions on the surrounding biological population. Sediments from effect on juvenile eastern oysters, an important ecosystem engineer in
floods due to erosion and rains in aquaculture sites cause high turbidity. estuarine systems.
According to Carriker (1986), excessive amounts of suspended silt may
negatively affect oyster larvae by interfering with their ability to feed.
3.9. Salinity
Additionally, oysters that live in turbid conditions in their natural
habitats have developed a filtering system to distinguish inorganic
Salinity is considered one of the most consequential environmental
particulates from food in suspension. Moreso, oysters reject inorganic
stressors for the culture of oysters along coastal areas (Miller et al., 2007;
particulates through the production of pseudofeces. Even though juve­
de Albuquerque, Ferreira, Salvador and Turini, 2012). Salinity is seen as
nile and adult oysters can survive under moderately turbid environ­
a variable parameter reflecting the input of freshwater from precipita­
ments, the deposition of sediment may have a detrimental effect on the
tion, ice melting, river runoff, and loss of water through evaporation.
survival and development of oysters (Lenihan, 1999) and can prevent
Additionally, the mixing and circulation of surface water with under­
natural reef-building processes (Colden and Lipcius, 2015). In addition,
ground water (Koblinsky et al., 2003; Cochrane et al., 2009). Evapora­
the infilling of interstitial voids in the bed structure caused by increased
tion is anticipated to increase with the increase in global temperatures,
sedimentation lowers the quality of the habitat. Most critically, oyster
causing variations in water surface salinity. Rodrick (2008) reported
spat settlement rates can be lowered by sediment deposition. Addi­
that at lower salinity levels, oysters are susceptible to bacteria invasion.
tionally, Mackenzie (1983) showed that even a small amount of silt can
He further discovered that the differences in salinity may have an impact
prevent the substrate from being used for spat attachment. Increased
on oyster immunological function, specifically the capacity of hemo­
sediment accumulation has the potential to bury some oyster cages
cytes (blood cells) to resist foreign bacterial invasion.
partially or completely, creating dangerous hypoxic conditions and
In general, there is a prediction of high mortalities for several species
catastrophic oyster mortality (Colden and Lipcius, 2015).
including cultured oysters due to increased variation in water salinity.
The result will be an adverse effect on the economic and social sus­
tainability of the sector through increased loss of species and higher
3.8. Turbidity
management costs. There is a need for future research to focus on the
effect of salinity at levels lower than an optimal requirement on oyster
According to Sandèn and Håkansson (1996), turbidity levels in water
aquaculture. However, few studies have been done on how various
bodies are rising due to human activity in coastal areas. The total sus­
commercially significant species like oysters react to variations in
pended particulate matter generally inhibits the growth of oysters by
salinity as a result of climate change. This scientific knowledge would be
diluting the organic matter at high levels (Barange et al., 2018).
very useful for adaptation strategy for aquaculture, as changes in salinity
Turbidity rarely exceeds aquatic organism tolerance levels relative to
may favor some species that are more saline tolerant (Jahan et al.,
other abiotic factors like salinity, temperature, and dissolved oxygen.
2019).
Instead, turbidity impairs predators’ vision and changes top-down
forcing (Liljendahl-Nurminen et al., 2008). In addition, the increasing
nutrient input and erosion are the two primary sources of turbidity that 3.10. Algal blooms
are significantly influenced by human activities (Candolin et al., 2008);
and cause siltation in lakes and streams (Khan and Ali, 2003). Moreso, it The term “harmful algal blooms” (HABs) refers to naturally

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occurring accumulations of microscopic algae in water bodies. They are Table 2

distributed worldwide and pose threats to the aquatic ecosystem. About Some observed diseases and parasites of oyster species (FAO, 2019).
2% are known to be harmful. Blooms of harmful algae can have varied Disease Agent Type Syndrome Measure
impacts on marine ecosystems, depending on suspension filter-feeding
Denman Island Mikrocytos Protozoan None Restricted
oysters who show size-selective feeding on phytoplankton. Therefore, Disease mackini parasite modified
algal bloom under thermal stimulation could be controlled. However, in culture
oyster farming, this would cause the phytoplankton community to be practices
altered. Both Marshall et al. (2009) and Li et al. (2015) reported that Nocardiosis Nocardia Bacterium None Modified
crassostreae culture
HABs occur more frequently in the mesohaline and polyhaline regions, practices
most especially in major tributaries and estuaries in coastal regions. Herpes-type virus None Virus None None
These same geographical areas, however, are particularly favorable for disease of C.
the growth of oyster reefs (Smith et al., 2005; Carnegie and Burreson, gigas larvae
Oyster velar virus None Virus None Unknown
2011). The U.S. government and shellfish growers from Maryland and
disease
Virginia together performed research and surveys in the mid-2000s, (OVVD)
which revealed several needs for the shellfish sector. The establish­
ment and maintenance of good water quality, specifically for the shell­
fish species being cultivated, was one of the most crucial and significant 2004; de Lorgeril et al., 2018), which is triggered by the herpes virus
findings (Oesterling and Luckenbach, 2008). To adequately assess the (Segarra et al., 2010; Martenot et al., 2011). According to Pernet et al.
hazards posed by algal blooms on aquaculture production, farmers need (2014), this disease, also known as Pacific oyster mortality syndrome,
to utilize the use of technologies that would identify such occurrences appears during specific seasons when there is a drastic change in water
and respond to them. Fig. 6 gives an illustration of the effects of GHG temperatures from 16 ◦ C to 24 ◦ C. In oyster farms, mortality is seen in
emissions (N2O, CO2) and other factors that contribute to the prolifer­ summer, especially on the French Atlantic coast, and in the spring and
ation of algal blooms. autumn on the Mediterranean coast, which is characterized by warmer
seawater temperatures. The detection of virulence factors constitutes an
3.11. Dissolved oxygen essential part of the risk assessment for human pathogenic Vibrio species
(Food and Agriculture Organization of the United Nations/World Health
Dissolved oxygen (DO) is an important component of aquatic eco­ Organization (FAO/WHO), 2011), some of which have been identified
systems. Changes in its content have a significant effect on the global in populations belonging to the Splendidus clade. In addition, the recent
nitrogen and carbon cycles (IPCC et al., 2014). The existence of bacteria, discovery of virulence factors in V. tasmaniensis and V. crassostreae has
plants, fish, and other invertebrates depends on the presence of dis­ enabled more accurate monitoring of splendidus clade populations
solved oxygen in the aquatic ecosystem. Excessive algal growth and potentially pathogenic to oysters. Splendidus clade populations are
decomposition result in low dissolved oxygen in the aquatic environ­ potentially pathogenic to oysters. In addition, domoic acid, commonly
ment. Low DO is known to create physiological stress on oysters (Diaz known as Amnestic Shellfish Poison (ASP), is also produced by the
and Rosenberg, 1995; Vaquer-Sunyer and Duarte, 2008) by impairing diatom pseudo-nitzchia sp. Being microscopic algae, they cause diseases
growth, reproduction, and immune functions, and reducing available in oysters after ingestion. It further causes cardiovascular, instability
habitat. Accordingly, low DO has been associated with the loss and seizures, and permanent short-term memory loss in humans. Table 2
unsuccessful rehabilitation of numerous oyster reefs (Cheney et al., shows some observed diseases and parasites of oyster species.
2001, Beck et al., 2011). Oysters can tolerate low DO conditions. In
addition, the ephemeral and episodic nature of its low DO conditions 3.13. Predation
(Breitburg, 1992; Johnson et al., 2009), makes it challenging to compare
how low DO affects the growth and survival of oysters and other Oyster aquaculture farmers have more control over predation
commercially important species (Hoback and Barnhart, 1996; Carmi­ depending on the design of their farms. The use of cages and longline
chael et al., 2004, Keppler et al., 2005). Furthermore, C. virginica can culture protects them from predators. In some farms, oysters are pro­
survive hypoxia (<1 mg/L) for 3 to >28 days (Stickle et al., 1989; Gray tected from invertebrate predators using mesh sacks. In addition, the off-
et al., 2002). The potential effects of low DO on oysters include changes bottom culture technique elevates the oysters from the water column,
in stress protein expressionPatterson et al., 2014, and reduced feeding, preventing predators from having access to them. Additionally, oysters
settlement, growth, and reproduction (Wallace et al., 2002). The can be raised in hatcheries until they reach an appropriate size and
improvement of fundamental knowledge of oyster physiology requires become less vulnerable to predators before being transferred to farms
the detection of sub-lethal and cumulative effects of DO on oysters. This (FAO, 2019). The physiological reactions of oysters to the changing
will also help with site selection for continuing restoration and man­ environment could make them more vulnerable to predators. Oysters
agement efforts ongoing worldwide (Beck et al., 2009; Schulte et al., are very adaptive to their environment and can grow in a highly variable
2009). Furthermore, understanding how low DO concentrations spe­ way depending on the conditions in the exact location. As a result of
cifically affect oysters could provide an early physiological indicator of increased predator presence in the aquatic environment, the growth of
stress to avoid mortality. individual species could be altered in response to defense (Lord and
Whitlatch, 2012). Oyster spat are vulnerable to predation from star­
3.12. Pathogens and diseases fishes, especially those cultured in bays and estuaries. Additionally,
some of the major predators of oysters include fish species and in­
The culture of oyster is associated with some pathogens, Vibrio spe­ vertebrates, such as crabs and snails. Many species respond to climate
cies which are responsible for epidemics, and zoonoses (Austin, 2010; Le change by moving into different areas as the current habitat becomes
Roux et al., 2015). Vibrio aestuarianus strains as well as a group of the unsuitable and new areas become preferable. Therefore, prey living in
Splendidus clade have been linked to mortality in farmed oysters during areas that provide habitat from predators will become more vulnerable
the past two decades (Soletchnik et al., 1999; Gay et al., 2004; Lemire as a result of the shift of predator species (Doney et al., 2012). Predators
et al., 2015). Vibrio aestuarianus has also been identified as a serious of oysters generally prefer a higher salinity environment. Therefore,
pathogen for adult oysters (Travers et al., 2017), whilst Vibrio tasma­ increased estuary salinity which is driven by the decrease in river
niensis and Vibrio crassostreae strains of the Splendidus clade are linked discharge may leave oysters without low-salinity refuge habitat (Kimbro
to a multifactorial sickness affecting spats and juveniles (Gay et al., et al., 2017). This may impair their capacity to protect themselves

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E.O. Neokye et al. Environmental Research 251 (2024) 118561

Fig. 7. Some environmental factors affecting oyster aquaculture production.

against increasing the relative danger of predation. impacting oyster production. Climate change is causing an increase in
acidification and water temperature, adversely affecting its production.
3.14. Chlorophyll a concentration To ensure maximum sustainability of oyster aquaculture, climate
change, and its induced hazards must be addressed globally and at the
The concentration of chlorophyll a in water can be used to charac­ regional level. This will ensure food security for countries that are
terize the biomass of phytoplankton, preliminarily determine the dependent on aquaculture for subsistence and for resource management
eutrophication degree of water, and reflect the water quality of lakes purposes.
(Kim et al., 2021). Therefore, chlorophyll a concentration is closely This study recommends that future research should focus on climate-
related to environmental factors, which is an indicator of primary pro­ induced hazards such as hurricanes, floods, and storm surges, on oyster
ductivity in the aquatic ecosystem. In principle, culturing oysters in an aquaculture. Consequently, future research should examine the regional
area with high chlorophyll a concentration is likely to produce quality dynamics of climate change to identify locations where oysters or
and marketable size compared with an area with low concentrations. shellfish may be vulnerable to climate change impacts. Additionally, in
Eutrophic water habitats, particularly those near the ocean such as bays, part 2 of the continuation of this paper, we focused on assessing climate
estuaries, and salt lakes, have high primary productivity output, making change impacts on oyster production, a framework for modeling oyster
them better suited for oyster farming and providing phytoplankton production. Lastly, we document mitigation and adaptation measures
(Umehara et al., 2018). Therefore, oyster farming is frequently carried and knowledge gaps, to be published later.
out in coastal areas due to the rich food availability and convenience.
According to Hallegraeff (1993), the consumption of phytoplankton by CRediT authorship contribution statement
oysters inhibits excessive phytoplankton growth, including harmful
algal blooms (HABs). High primary production is facilitated by the Emmanuel Okine Neokye: Writing – review & editing, Writing –
abundant supply of nitrogen and phosphorus input from coastal runoff original draft, Visualization, Methodology, Conceptualization. Xiuquan
water emanating from land-based sources. High nutrient loads, how­ Wang: Writing – review & editing, Visualization, Validation, Supervi­
ever, might cause excessive eutrophication and lead to frequent red sion, Funding acquisition, Conceptualization. Krishna K. Thakur:
tides. Therefore, continuing efforts to reduce organic matter and nutri­ Writing – review & editing. Pedro Quijon: Writing – review & editing.
ents such as nitrogen and phosphorus is a serious concern for aquacul­ Rana Ali Nawaz: Software. Sana Basheer: Visualization.
ture farmers. Furthermore, net zooplankton, and suspension-feeding
oysters compete directly for food (Gerritsen et al., 1994). Therefore, in
an estuary where primary production is generally high, zooplankton Declaration of competing interest
density and biomass per unit volume tend to be ten times higher than in
the offshore area (Magalhães et al., 2006; Walkusz et al., 2009). The authors declare the following financial interests/personal re­
lationships which may be considered as potential competing interests:
4. Conclusion and future directions The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
Fig. 7 illustrates some of the key environmental factors affecting the work reported in this paper.
oyster production globally. Oysters are vital natural resources that sus­
tain humans and the aquatic ecosystem. However, climate change and Data availability
some key factors have impacted its potential for maximum production in
many regions. This article discussed the various ways climate change is No data was used for the research described in the article.

8
E.O. Neokye et al. Environmental Research 251 (2024) 118561

Acknowledgments Scientific Knowledge. FAO Fisheries and Aquaculture Technical Paper. No. 530.
FAO), Rome, pp. 151–212.
Diaz, R., Rosenberg, R., 1995. Marine benthic hypoxia: a review of its ecological effects
This research was supported by the Natural Science and Engineering and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. Annu.
Research Council of Canada, the New Frontiers in Research Fund, Nat­ Rev. 33, 245–303.
ural Resources Canada (NRCan), the Government of Prince Edward Is­ Doney, S.C., Ruckelshaus, M., Duffy, J.E., Barry, J.P., Chan, F., English, C.A., et al., 2012.
Climate change impacts on marine ecosystems. Ann. Rev. Mar. Sci 4, 11–37. https://
land, and the Atlantic Computational Excellence Network (ACENET). doi.org/10.1146/annurev-marine-041911-111611.
FAO, 2019. Cultured Aquatic Species Information Programme: Crassostrea Virginica.
References Food & Agriculture Organization of the United Nations, Fisheries and Aquaculture
Department. http://www.fao.org/fishery/culturedspecies/Crassostrea_virginica/en.
SummaryandTechnicalReport. Microbiological Risk Assessment Series No. 16. Rome:
Austin, B., 2010. Vibrios as causal agents of zoonoses. Vet. Microbiol. 140, 310–317. FAO, 193.
https://doi.org/10.1016/j.vetmic.2009.03.015. FAO 2023. Magallana gigas. Cultured Aquatic Species Information Programme. Text by
Bacher, C., Grant, J., Hawkins, A., Fang, J., Zhu, P., Duarte, P., 2003. Modeling the effect Helm, M.M. Fisheries and Aquaculture Division [online]. Rome. Updated 2006-06-
of food depletion on scallop growth in Sungo Bay (China). Aquat. Living Resour. 16, 08 [Cited Tuesday, November 7th, 2023]. https://www.fao.org/fishery/en/culture
10–24. https://doi.org/10.1016/S0990-7440(03)00003-2. dspecies/crassostrea_gigas.
Barange, M., Bahri, T., Beveridge, M.C.M., Cochrane, K.L., Funge-Smith, S., Poulain, F. Filgueira, R., Guyondet, T., Comeau, L.A., Grant, J., 2014. A fully spatial ecosystem-DEB
(Eds.), 2018. Impacts of Climate Change on Fisheries and Aquaculture: Synthesis of model of oyster (Crassostrea virginica) carrying capacity in the Richibucto Estuary,
Current Knowledge, Adaptation and Mitigation Options. FAO, Rome, p. 628. FAO Eastern Canada. J. Mar. Syst. https://doi.org/10.1016/j.jmarsys.2014.03.015.
Fisheries and Aquaculture Technical Paper No. 627. Food and Agriculture Organization, 2020. The state of world fisheries and aquaculture.
Beck, M., et al., 2009. Shellfish Reefs at Risk: a Global Analysis of Problems and Sustainability in action. Rome. https://doi.org/10.4060/ca9229en.
Solutions. Nature Conservancy, Arlington, Virginia, USA. Food and Agriculture Organization of the United Nations, 2018. Globefish: Information
Beck, M.W., et al., 2011. Oyster reefs at risk and recommendation for conservation, and Analysis on Markets and Trade of Fisheries and Aquaculture products.
restoration, and management. Bioscience 61, 107–116. Forsberg, P.L., Lumborg, U., Bundgaard, K., Ernstsen, V.B., 2017. Impact of mussel
Bell, J., Batty, M., Ganachaud, A., Gehrke, P., Hobday, A., Hoegh-Guldberg, O., et al., bioengineering on fine-grained sediment dynamics in a coastal lagoon: a numerical
2010. Preliminary assessment of the effects of climate change on fisheries and modeling investigation. J. Mar. Syst. 176, 1–12. https://doi.org/10.1016/j.
aquaculture in the Pacific. In: Gillett, R. (Ed.), Fisheries in the Economies of the jmarsys.2017.07.008.
Pacific Island Countries and Territories. Pacific Studies Series. Asian Development Froehlich, H.E., Gentry, R.R., Halpern, B.S., 2017. Conservation aquaculture: shifting the
Bank), Manila, pp. 451–469. narrative and paradigm of aquaculture’s role in resource management. Biol.
Bosma, R., Thi Anh, P., Potting, J., 2011. Life cycle assessment of intensive striped catfish Conserv. 215, 162–168. https://doi.org/10.1016/j.biocon.2017.09.012.
farming in the Mekong Delta for screening hotspots as input to environmental policy Gabrielle, L., Shirley, B., Edward, C., 2021. Oyster-predator dynamics and climate
and research agenda. Int. J. Life Cycle Assess. 16, 903–915. change. Environ. Data Inf. Serv. https://doi.org/10.32473/edis-fa228-2020.
Breitburg, D., 1992. Episodic hypoxia in Chesapeake Bay: interacting effects of Gay, M., Renault, T., Pons, A.-M., LeRoux, F., 2004. Two Vibrio splendidus-related
recruitment, behavior, and physical disturbance. Ecol. Monogr. 62, 525–546. strains collaborate to kill Crassostrea gigas: taxonomy and host alterations. Dis.
Bueno, P.B., Soto, D., 2017. Adaptation Strategies of the Aquaculture Sector to the Aquat. Organ. 62, 65–74. https://doi.org/10.3354/dao062065.
Impacts of Climate Change. FAO, Rome. Gerritsen, J., Holland, A.F., Irvine, D.E., 1994. Suspension-feeding bivalves and the fate
Candolin, U., Engström-Öst, J., Salesto T, T., 2008. Human-induced eutrophication of primary production: an estuarine model applied to Chesapeake Bay. Estuaries 17,
enhances reproductive success through effects on parenting ability in sticklebacks. 403–416.
Oikos 117, 459–465. https://doi.org/10.1111/j.2007.0030-1299.16302.x. GESAMP, 1990. IMO/FAO/UNESCO/WMO/IAEA/UN/UNEP; Joint group of experts on
Carmichael, R., Shriver, A., Valiela, I., 2004. Changes in shell and soft tissue growth, the scientific aspects of marine environmental protection. In: The State of the Marine
tissue composition, and survival of quahogs, Mercenaria, and softshell clams, Mya Environment. GESAMP.
arenaria, in response to eutrophic-driven changes in food supply and habitat. J. Exp. Godfray, H., Charles, J., et al., 2010. Food Security. The Challenge of Feeding 9 Billion
Mar. Biol. Ecol. 313, 75–104. People. Science 327, 812–818.
Carnegie, R.B., Burreson, E.M., 2011. Declining impact of an introduced pathogen: Gray, J.S., Wu, R.S., Or, Y.Y., 2002. Effects of hypoxia and organic enrichment on the
haplosporidium nelsoni in the oyster Crassostrea virginica in Chesapeake Bay. Mar. coastal marine environment. Mar. Ecol. Prog. Ser. 238, 249–279.
Ecol. Prog. Ser. 432, 1–5. Gutiérrez, J.L., Jones, C.G., Strayer, D.L., Iribarne, O., 2003. Mollusks as ecosystem
Carriker, M.R., 1986. Influence of suspended particles on the biology of oyster larvae in engineers: the role of shell production in aquatic habitats. Oikos 101, 79–90. https://
estuaries. American Malacalogical Bulletin Special Edition 3, 41–49. doi.org/10.1034/j.1600-0706.2003.12322.x.
Cheney, D., Elston, R., MacDonald, B., Kinnan, K., Suhrbier, A., 2001. The roles of Guyondet, T., Comeau, L.A., Bacher, C., Grant, J., Rosland, R., Sonier, R., et al., 2018.
environmental stressors and culture methods on the summer mortality of the Pacific Climate change influences carrying capacity in a coastal embayment dedicated to
oyster Crassostrea gigas. J. Shellfish Res. 20, 1195. shellfish aquaculture. Estuar. Coasts 38, 1593–1618. https://doi.org/10.1007/
Chung, I.K., Sondak, C.F.A., Beardall, J., 2017. The future of seaweed aquaculture in a s12237-014-9899-x.
rapidly changing world. Eur. J. Phycol. 52, 495–505. https://doi.org/10.1080/ Hallegraeff, G.M., 1993. A review of harmful algal blooms and their apparent global
09670262.2017.1359678. increase. Phycologia 32, 79–99. https://doi.org/10.2216/i0031-8884-32-2-79.1.
Clements, J.S., Chopin, T., 2016. Ocean acidification and marine aquaculture in North Hambal, H., Mohd Akhir, A., Saniah, Y., 1994. Environmental Issues on aquaculture
America: potential impacts and mitigation strategies. Rev. Aquac. 9, 326–341. development in Malaysia. In: Working Papers of the Fisheries. Research Institute,
https://doi.org/10.1111/raq.12140. Department of Fisheries, Kuala Lumpur, Malaysia.
Cochrane, K., De Young, C., Soto, D.T., Bahri, D.T., 2009. Climate Change Implications Han, D., Chen, Y., Zhang, C., Ren, Y., Xue, Y., Wan, R., 2017. Evaluating impacts of
for Fisheries and Aquaculture: Overview of Current Scientific Knowledge. FAO, intensive shellfish aquaculture on a semi-closed marine ecosystem. Ecol. Model. 359,
Rome. FAO Fisheries and Aquaculture Technical Paper No. 530. 193–200. https://doi.org/10.1016/j.ecolmodel.2017.05.024.
Coen, L.D., Brumbaugh, D.R., Bushek, D., Grizzle, R., Luckenbach, W.M., Posey, M.W., Handisyde, N.T., Ross, L.G., Badjeck, M.C., Allison, E.H., 2006. The effects of climate
Powers, S.P., Gregory, S.T., 2007. Ecosystem services related to oyster restoration. change on world aquaculture: a global perspective. Final technical report. In:
Mar. Ecol. Prog. Ser. 341, 303–307. Stirling: DFID Aquaculture and Fish Genetics Research Programme. Stirling Institute
Colden, A.M., Lipcius, R.N., 2015. Lethal and sublethal effects of sediment burial on the of Aquaculture.
eastern oyster Crassostrea virginica. Mar. Ecol. Prog. Ser. 527, 105–117. Henriksson, P.J.G., Zhang, W., Nahid, S.A.A., Newton, R., Phan, L.T., Dao, H.M., Zhang,
Cranford, P.J., Dowd, M., Grant, J., Hargrave, B., McGladdery, S., 2003. Ecosystem level Z., Jaithiang, J., Andong, R., Chaimanuskul, K., Vo, N.S., Hua, H.V., Haque, M.M.,
effects of marine bivalve aquaculture. Sci. Rev. Potential Environ. Effects Aquacult. Das, R., Kruijssen, F., Satapornvanit, K., Nguyen, P.T., Liu, Q., Liu, L., Wahab, M.A.,
Aqua. Ecosyst. 1, 51–95, 10.1.1.566.4625. Murray, F.J., Little, D.C. & Guinée, J.B. 2014. Final LCA case study report—results of
Dabbadie, L., Aguilar-Manjarrez, J.J., Beveridge, M.C.M., Bueno, P.B., Ross, L.G., LCA studies of Asian aquaculture systems for tilapia, catfish, shrimp, and freshwater
Soto, D., 2018. Chapter 20: Effects of Climate Change on Aquaculture: Drivers, prawn. SEAT Deliverable Ref: D 3.5.
Impacts and Policies. FAO, Rome. Hoback, W., Barnhart, M., 1996. Lethal limits and sublethal effects of hypoxia on the
Dangendorf, S., Marcos, M., Wöppelmann, G., Conrad, C.P., Frederikse, T., Riva, R., amphipod Gammarus pseudolimnaeus. J. North Am. Benthol. Soc. 15, 117–126.
2017. Reassessment of 20th century global mean sea level rise. Proc. Natl. Acad. Sci. Hu, Z., Lee, J.W., Chandran, K., Kim, S., Khanal, S.K., 2012. Nitrous oxide (N2O) emission
USA 114 (23), 5946–5951. https://doi.org/10.1073/pnas.1616007114. from aquaculture: a Review. Environ. Sci. Technol. 46 (12), 6470–6480. https://doi.
De Albuquerque, M.C.P., Ferreira, J., Gustavo, C.S., Turini, C., 2012. Influence of org/10.1021/es300110x.
Temperature and Salinity on Survival and Growth of the Pearl Oyster Larvae Pteria IPCC, 2014. In: Pachauri, R.K., Meyer, L.A. (Eds.), Climate Change 2014: Synthesis
hirundo, vol. 38. Boletim do Instituto de Pesca, pp. 189–197. Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of
De Lorgeril, J., Escoubas, J.M., Loubiere, V., Pernet, F., Le Gall, P., Vergnes, A., et al., the Intergovernmental Panel on Climate Change [Core Writing Team. IPCC, Geneva,
2018. Inefficient immune response is associated with microbial permissiveness in Switzerland, p. 151.
juvenile oysters affected by mass mortalities on field. Fish Shellfish Immunol. 77, IPCC, 2018. Global warming of 1.5◦C. An IPCC special report on the impacts of global
156–163. https://doi.org/10.1016/j.fsi.2018.03.027. warming of 1.5◦C above pre-industrial levels and related global greenhouse gas
De Silva, S.S., Soto, D., 2009. Climate change and aquaculture: potential impacts, emission pathways. In: Masson-Delmotte, V., Zhai, P., Pörtner, D.H.O. (Eds.), The
adaptation and mitigation. In: Cochrane, K., De Young, C., Soto, D., Bahri, T. (Eds.), Context of Strengthening the Global Response to the Threat of Climate Change,
Climate Change Implications for Fisheries and Aquaculture: Overview of Current Sustainable Development, and Efforts to Eradicate Poverty.

9
E.O. Neokye et al. Environmental Research 251 (2024) 118561

IPCC, 2021. Summary for policymakers. In: R, Y., Masson-Delmotte, B.Z., Zhai, V.P., aquaculture production: sustainability implications, mitigation, and adaptations.
Pirani, A., Connors, S.L., Péan, C., Berger, S., Caud, N., Chen, Y., Goldfarb, L., Front. Sustain. Food Syst. 5, 609097 https://doi.org/10.3389/fsufs.2021.60909.
Gomis, M.I., Huang, M., Leitzell, K., Lonnoy, E., Matthews, J.B.R., Maycock, T.K., Miller, A. Whitman, Ruiz, Gregory M., Minton, Mark S., Ambrose, Richard F., 2007.
Waterfield, T., Yelekçi, O. (Eds.), Climate Change 2021: the Physical Science Basis. Differentiating successful and failed molluscan invaders in estuarine ecosystems.
Contribution of Working Group I to the Sixth Assessment Report of the Mar. Ecol. Prog. Ser. 332, 41–51.
Intergovernmental Panel on Climate Change. Newell, R.I., 2004. Ecosystem influences of natural and cultivated populations of
Jahan, A., Nipa, T.T., Islam, S.M.M., Uddin, M.H., Islam, M.S., Shahjanan, M., 2019. suspension-feeding bivalve molluscs: a review. J. Shellfish Res. 23, 51–62.
Striped catfish (Pangasianodon hypophthalmus) could be suitable for coastal Oesterling, M., Luckenbach, M., 2008. Best Management Practices for the Virginia
aquaculture. J. Appl. Ichthyol. 35, 994–1003. https://doi.org/10.1111/jai.13918. Shellfish Culture Industry. Marine Resource Report No. 2008-10. NOAA, Silver
Johnson, M., Powers, S., Senne, J., Park, K., 2009. Assessing in situ tolerances of Eastern Spring, MA, p. 12.
Oysters(Crassostrea virginica) under moderate hypoxic regimes: implications for Okon, E.M., Birikorang, H.N., Munir, M.B., Kari, Z.A., Téllez-Isaías, G., Khalifa, N.E.,
restoration. J. Shellfish Res. 28, 1–8. Abdelnour, S.A., Eissa, M.E.H., Al-Farga, A., Dighiesh, H.S., et al., 2023. A global
Keppler, C., Hoguet, J., Smith, K., Ringwood, A., Lewitus, A., 2005. Sublethal effects of analysis of climate change and the impacts on oyster diseases. Sustainability 15,
the toxic alga Heterosigma akashiwo on the southeastern oyster (Crassostrea 12775. https://doi.org/10.3390/su151712775.
virginica). Harmful Algae 4, 275–285. Patterson, H.K., Boettcher, A., Carmichael, R.H., 2014. Biomarkers of dissolved oxygen
Khan, A.A., Ali, S.B., 2003. Effects of erosion on indus river bio-diversity in Pakistan. stress in oysters: a tool for restoration and management efforts. PLoS One 9 (8),
Pakistan J. Biol. Sci. 6, 1035–1040. https://doi.org/10.3923/pjbs.2003.1035.1040. e104440. https://doi.org/10.1371/journal.pone.0104440.
Kibria, G., Haroon, Y.A.K., Dayanthi, N., 2017. Climate change impacts on tropical and Pernet, F., Lagarde, F., Jeannee, N., Daigle, G., Barret, J., Le Gall, P., et al., 2014. Spatial
temperate fisheries, aquaculture, and seafood security and implications–a review. and temporal dynamics of mass mortalities in oysters is influenced by energetic
Livest. Res. Rural Dev. 29, 22. reserves and food quality. PLoS One 9, e88469, 10.1371/journal. pone.0088469.
Kim, H.G., Hong, S., Chon, T.-S., Joo, G.-J., 2021. Spatial patterning of chlorophyll a and Petersen, J.K., Saurel, C., Nielsen, P., Timmermann, K., 2016. The use of shellfish for
water-quality measurements for determining environmental thresholds for local eutrophication control. Aquacult. Int. 24, 857–878. https://doi.org/10.1007/
eutrophication in the Nakdong River basin. Environ. Pollut. 268, 115701. s10499-015-9953-0.
Kimbro, D.L., White, J.W., Tillotson, H., Cox, N., Christopher, M., Stokes-Cawley, O., Pickering, T.D., Ponia, B., Hair, C.A., Southgate, P.C., Poloczanska, E.S., Della
Yuan, S., Pusack, T.J., Stallings, C.D., 2017. Local and regional stressors interact to Patrona, L., et al., 2011. Vulnerability of aquaculture in the tropical Pacific to
drive a salinization-induced outbreak of predators on oyster reefs. Ecosphere 8 (11), climate change. In: Bell, J.D., Johnson, J.E., Hobday, A.J. (Eds.), Vulnerability of
e01992. https://doi.org/10.1002/ecs2.1992. Tropical Pacific Fisheries and Aquaculture to Climate Change. Noumea: Secretariat
Kittner, C., Riisgård, H.U., 2005. Effect of temperature on filtration rate in the mussel of the Pacific Community), pp. 647–731.
Mytilus edulis: No evidence for temperature compensation(2005). Mar. Ecol. Prog. Poirier, L.A., Clements, J.C., Coffin, M.R.S., Craig, T., Davidson, J., Miron, G.,
Ser. 305, 147–152. https://doi.org/10.3354/meps305147. Davidson, J.D.P., Hill, J., Comeau, L.A., 2021. Siltation negatively affect settlement
Kluger, L.C., Filgueira, R., Wolff, M., 2017. Integrating the concept of resilience into an and gaping behaviour in eastern oysters. Mar. Environ. Res. 170, 105432.
ecosystem approach to bivalve aquaculture management. Ecosystems 20, 1–19. Rodrick, G.B., 2008. Effects of temperature, salinity and pesticides on oyster hemocyte
https://doi.org/10.1007/s10021-017-0118-z. activity. Florida Water Resour. J 4, 14.
Koblinsky, C.J., Hildebrand, P., LeVine, D., Pellerano, F., Chao, Y., Wilson, W., et al., Rutkayova, J., Vácha, F., Maršálek, M., Beneš, K., Civišová, H., Horká, P., et al., 2017.
2003. Sea surface salinity from space. Sci. Goals Meas. Approach Radio Sci. 38, 7. Fish stock losses due to extreme floods–findings from pond-based aquaculture in the
https://doi.org/10.1029/2001RS002584. Czech Republic. J. Flood Risk Manage. 11, 351–359. https://doi.org/10.1111/
Kooijman, S.A.L.M., 2010. Dynamic Energy Budget Theory for Metabolic Organization, jfr3.12332.
third ed. Cambridge University Press, Cambridge. Sandèn, P., Håkansson, B., 1996. Long-term trends in secchi depth in the baltic sea.
Kopp, R.E., Horton, R.M., Little, C.M., Mitrovica, J.X., Oppenheimer, M., Rasmussen, D. Limnol. Oceanogr. 41, 346e351.
J., Strauss, B.H., Tebaldi, C., 2014. Probabilistic 21st and 22nd century sea-level Schulte, D., Burke, R., Lipcius, R., 2009. Unprecedented restoration of a native oyster
projections at a global network of tide-gauge sites. Earth’s Future 2, 383–406. metapopulation. Science 325, 1124–1128.
https://doi.org/10.1002/2014EF000239. Segarra, A., Pépin, J.F., Arzul, I., Morga, B., Faury, N., Renault, T., 2010. Detection and
Le Roux, F., Wegner, K.M., Baker-Austin, C., Vezzulli, L., Osorio, C.R., Amaro, C., et al., description of a particular Ostreid herpesvirus 1 genotype associated with massive
2015. The emergence of Vibrio pathogens in Europe: ecology, evolution, and mortality outbreaks of Pacific oysters, Crassostrea gigas, in France in 2008. Virus
pathogenesis (Paris, 11-12th March 2015). Front. Microbiol. 6, 830. https://doi.org/ Res. 153, 92–99, 10.1016/j.virusres.2010. 07.011.
10.3389/fmicb.2015.00830. Shelmerdine, R., Mouat, B., Shucksmith, R., 2017. The most northerly record of feral
Lemire, A., Goudenege, D., Versigny, T., Petton, B., Calteau, A., Labreuche, Y., et al., Pacific oyster Crassostrea gigas (Thunberg, 1793) in the British Isles. Bioinvasions
2015. Populations, not clones, are the unit of vibrio pathogenesis in naturally Rec 6, 57–60. https://doi.org/10.3391/bir.2017.6.1.09.
infected oysters. ISME J. 9, 1523–1531. https://doi.org/10.1038/ismej.2014.233. Shumway, S.E., Davis, C., Downey, R., Karney, R., Kraeuter, J., Parsons, J., et al., 2003.
Lenihan, H.S., 1999. Physical–biological coupling on oyster reefs: how habitat structure Shellfish aquaculture–in praise of sustainable economies and environments. World
influences individual performance. Ecol. Monogr. 69 (3), 251–275. Aquacult. 34, 8–10.
Li, J., Gilbert, P.M., Gao, Y., 2015. Temporal and spatial changes in Chesapeake Bay Smith, G.F., Bruce, D.G., Roach, E.B., Hansen, A., Newell, R.I.E., McManus, A.M., 2005.
water quality and relationships to Prorocentrum minimum, Karlodinium veneficum, Assessment of recent habitat conditions of Eastern Oyster Crassostrea virginica bars
and CyanoHAB events, 1991-2008. Harmful Algae 42, 1–14. in mesohaline Chesapeake Bay. N. Am. J. Fish. Manag. 25, 1569–1590. https://doi.
Liljendahl-Nurminen, A., Horppila, J., Lampert, W., 2008. Physiological and visual org/10.1577/m04-058.1.
refuges in a metalimnion: an experimental study of effects of clay turbidity and an Soletchnik, P., Le Moine, O., Faury, N., Razet, D., Geairon, P., Goulletquer, P., 1999.
oxygen minimum on fish predation. Freshw. Biol. 53, 945–951. https://doi.org/ Summer mortality of the oyster in the Bay Marennes-Oleron: spatial variability of
10.1111/j.1365-2427.2008.01952.x. environment and biology using a geographical information system (GIS). Aquat.
Lord, J.P., Whitlatch, R.B., 2012. Inducible defenses in the eastern oyster Crassostrea Living Resour. 12, 131–143. https://doi.org/10.1016/S0990-7440(99)80022-9.
virginica gmelin in response to the presence of the predatory oyster drill Urosalpinx Stickle, W.B., Kapper, A.M., Li-Lian, L., Gnaiger, E., Wang, Y.S., 1989. Metabolic
cinerea say in long Island sound. Mar. Biol. 2012 (159), 1177–1182. https://doi.org/ adaptations of several species of Crustaceans and molluscs to hypoxia: tolerance and
10.1007/s00227-012-1896-7. microcalorimetric studies biol. Bull. (Arch. Am. Art) 177, 303–312.
Lunt, J., Smee, L.D., 2014. Turbidity influences trophic interactions in estuaries Limnol. Strohmeier, T., Aure, J., Duinker, A., Castberg, T., Svardal, A., Strand, Ø., 2005. Flow
Oceanogr 59 (6), 2014. reduction, seston depletion, meat content and distribution of diarrhetic shellfish
Mackenzie, C.L., 1983. To increase oyster production in the northeastern United States. toxins in a long-line blue mussel farm. J. Shellfish Res. 24, 15–24. https://doi.org/
US Natl. Mar. Fish. Serv. Mar. Fish. Rev. 45, 1–22. 10.2983/0730-8000(2005)24[15:FRSDMC]2.0.CO;2.
MacLeod, M., Hasan, M.R., Robb, D.H.F., Mamun-Ur-Rashid, M., 2019. Quantifying and Travers, M.A., Tourbiez, D., Parizadeh, L., Haffner, P., Kozic-Djellouli, A.,
Mitigating Greenhouse Gas Emissions from Global Aquaculture. FAO, Rome. FAO Aboubaker, M., et al., 2017. Several strains, one disease: experimental investigation
Fisheries and Aquaculture Technical Paper No. 626. of Vibrio aestuarianus infection parameters in the Pacific oyster. Crassostrea gigas.
Magalhães, A., Costa, R.M., Liang, T.H., Pereira, L.C.C., Ribeiro, M.J.S., 2006. Spatial and Vet. Res. 48, 32, 3256 10.1186/s13567-017-0438-1.
temporal distribution in density and biomass of two pseudodiaptomus species Umehara, A., Asoka, S., Fuji, N., Otani, S., Yamamoto, H., Nakai, S., Okuda, T.,
(copepoda: calanoida) in the caeté river estuary (amazon region - North of Brazil). Nishijima, W., 2018. Biological Productivity Evaluation at Lower Trophic Levels
Braz. J. Biol. 66 (2a), 421–430, 2006. with Intensive Pacific Oyster Farming of Crassostrea gigas in Hiroshima Bay, vol.
Malham, S.K., Cotter, E., O’Keeffe, S., Lynch, S., Culloty, S., King, J., Latchford, J., 495. Japan, Aquaculture, pp. 311–319.
Latchford, J., Beaumont, A., 2009. Summer mortality of the Pacific oyster, Vaquer-Sunyer, R., Duarte, C., 2008. Thresholds of hypoxia for marine biodiversity. Proc.
Crassostrea gigas. In: The Irish Sea: the Influence of Temperature and Nutrients on Natl. Acad. Sci. USA 105, 15452–15457.
Health and Survival, vol. 287. Aquaculture, pp. 128–138. https://doi.org/10.1016/j. Walkusz, W., Kwasniewski, S., Petersen, S.F., Hop, H., Tverberg, V., Wieczorek, P., Jan
aquaculture.2008.10.006. Marcin Weslawski, J.M., 2009. Seasonal and spatial changes in the zooplankton
Marshall, N.A., Marshall, P.A., Tamelander, J., Obura, D., Malleret-King, D., Cinner, J.E., community of Kongsfjorden, Svalbard. Polar Res. 28 (2), 254–281. https://doi.org/
2009. A Framework for Social Adaptation to Climate Change: Sustaining Tropical 10.1111/j.1751-8369.2009.00107.x.
Coastal Communities [SIC] and Industries. Wallace, R., Rikard, F., Howe, J., Rouse, D., 2002. Optimum Size for Planting Hatchery
Martenot, C., Oden, E., Travaillé, E., Malas, J.P., Houssin, M., 2011. Detection of Produced Oyster Seed. Final Technical Report Grant No. NA86RG0073.
different variants of ostreid herpesvirus 1 in the pacific oyster, Crassostrea gigas
between 2008 and 2010. Virus Res. 160, 25–31, 10.1016/j.virusres.2011. 04.012.
Maulu, S., Hasimuna, O.J., Haambiya, L.H., Monde, C., Musuka, C.G., Makorwa, T.H.,
Munganga, B.P., Phiri, K.J., Nsekanabo, J.D., 2021. Climate change effects on

10
E.O. Neokye et al. Environmental Research 251 (2024) 118561

Woodin, S.A., Wethey, D.S., Olabarria, C., Vázquez, E., Domínguez, R., Macho, G., et al., Yazdi, S.K., Shakouri, D., 2010. The effects of climate change on aquaculture. Int. J.
2020. Behavioral responses of three venerid bivalves to fluctuating salinity stress. Environ. Sci. Dev. 1, 378–382. https://doi.org/10.7763/IJESD.2010.V1.73.
J. Exp. Mar. Biol. Ecol. 522, 151256, 10.1016/j. jembe.2019.151256. Zippay, M.L., Helmuth, B., 2012. Effects of temperature change on mussel. Mytilus.
Integr. Zool. 7, 312–327. https://doi.org/10.1111/j.1749-4877.2012.0031.

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