Surviving the cold: a review of the effects of cold spells on bivalves and mitigation measures

Abstract

Cold spells, characterized by prolonged periods of low temperature, have become increasingly frequent, intense, and prolonged due to the ongoing effects of climate change, resulting in devastating consequences for marine ecosystems and significant socio-economic impacts. As ectothermic organisms, bivalves are dependent on their environment for regulating body temperature, and thus, cold spells can disrupt their normal functioning, leading to mass mortalities. This review comprehensively summarizes the effects of cold spells on bivalves and proposes mitigation measures to be considered in future bivalve farming and management plans. Scientific evidence has indicated that cold spells can alter bivalve metabolism, leading to an increase in stress protein production and a decrease in the activity of energy metabolism-related enzymes, which can negatively impact the bivalve immune system and increase the risk of disease. To mitigate the effects of cold spells on bivalves, a number of strategies can be employed, including the use of thermal shelters such as floating covers, selective breeding of more cold-tolerant bivalves, and genetic engineering to enhance the expression of heat-shock proteins in bivalves. The impacts of cold spells on bivalves are significant, affecting both their physiological and molecular processes. Through the implementation of thermal shelters, selective breeding, and genetic engineering, the effects of cold spells on bivalves can be reduced, improving their survival and growth. Further research is required to fully understand cold spells’ impacts on bivalves and develop effective mitigation measures.

Full text

Surviving the cold: a review of
the effects of cold spells on
bivalves and mitigation measures
Fortunatus Masanja
1
, Yang Xu
1
,KeYang
1
, Robert Mkuye
1
,
Yuewen Deng
1
and Liqiang Zhao
1,2
*
1
Fisheries College, Guangdong Ocean University, Zhanjiang, China,
2
Guangdong Provincial Key
Laboratory of Aquatic Animal Disease Control and Healthy Culture, Guangdong Ocean University,
Zhanjiang, China
Cold spells, characterized by prolonged periods of low temperature, have
become increasingly frequent, intense, and prolonged due to the ongoing
effects of climate change, resulting in devastating consequences for marine
ecosystems and significant socio-economic impacts. As ectothermic organisms,
bivalves are dependent on their environment for regulating body temperature,
and thus, cold spells can disrupt their normal functioning, leading to mass
mortalities. This review comprehensively summarizes the effects of cold spells
on bivalves and proposes mitigation measures to be considered in future bivalve
farming and management plans. Scientific evidence has indicated that cold spells
can alter bivalve metabolism, leading to an increase in stress protein production
and a decrease in the activity of energy metabolism-related enzymes, which can
negatively impact the bivalve immune system and increase the risk of disease. To
mitigate the effects of cold spells on bivalves, a number of strategies can be
employed, including the use of thermal shelters such as floating covers, selective
breeding of more cold-tolerant bivalves, and genetic engineering to enhance the
expression of heat-shock proteins in bivalves. The impacts of cold spells on
bivalves are significant, affecting both their physiological and molecular
processes. Through the implementation of thermal shelters, selective
breeding, and genetic engineering, the effects of cold spells on bivalves can be
reduced, improving their survival and growth. Further research is required to fully
understandcoldspells’impacts on bivalves and develop effective
mitigation measures.
KEYWORDS
cold spells, bivalve, physiology, mitigation, climate change
1 Introduction
As climate change progresses, extreme climatic events such as heat waves, droughts,
cyclones, and cold spells are expected to become more frequent and intense (Weilnhammer
et al., 2021). Bivalve species, a crucial component of marine environments, are frequently
exposed to such fluctuations and are vulnerable to the impacts of these events (He et al.,
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Vladimir Laptikhovsky,
Centre for Environment, Fisheries and
Aquaculture Science (CEFAS),
United Kingdom
REVIEWED BY
Xizhi Huang,
Johannes Gutenberg University Mainz,
Germany
Yuan Wang,
Dalian Ocean University, China
*CORRESPONDENCE
Liqiang Zhao
lzhao@gdou.edu.cn
SPECIALTY SECTION
This article was submitted to
Marine Fisheries, Aquaculture and Living
Resources,
a section of the journal
Frontiers in Marine Science
RECEIVED 04 February 2023
ACCEPTED 10 April 2023
PUBLISHED 21 April 2023
CITATION
Masanja F, Xu Y, Yang K, Mkuye R, Deng Y
and Zhao L (2023) Surviving the cold: a
review of the effects of cold spells on
bivalves and mitigation measures.
Front. Mar. Sci. 10:1158649.
doi: 10.3389/fmars.2023.1158649
COPYRIGHT
© 2023 Masanja, Xu, Yang, Mkuye, Deng and
Zhao. This is an open-access article
distributed under the terms of the Creative
Commons Attribution License (CC BY). The
use, distribution or reproduction in other
forums is permitted, provided the original
author(s) and the copyright owner(s) are
credited and that the original publication in
this journal is cited, in accordance with
accepted academic practice. No use,
distribution or reproduction is permitted
which does not comply with these terms.
TYPE Review
PUBLISHED 21 April 2023
DOI 10.3389/fmars.2023.1158649

2023). Extreme low water temperatures, specifically cold spells, can
significantly affect the various levels of biological organization in
bivalves, leading to declines or cessation of vital activities (Gosling,
2015). Moreover, in aquaculture and natural waters, extreme cold
spells can even cause substantial mortality among bivalve
populations (Ferreira et al., 2021). Bivalves are of vital importance
to marine ecosystems, both ecologically and economically. As a vital
food source for many species and a key element in aquaculture,
understanding their responses to environmental stressors, such as
cold spells, is crucial. Although much has been studied about high-
temperature stress responses in bivalves, knowledge about their
response to cold stress is limited (Liu et al., 2016).
The effects of cold stress on bivalves have been investigated at
different levels of biological organization, and the advances in
molecular-genetic, physiological, and biochemical methods have
improved our understanding of these effects (Figure 1). This review
aims to synthesize the current knowledge on the physiological and
molecular mechanisms underlying the effects of cold spells on
bivalve species. The focus will be on the changes that occur in
various levels of biological organization in response to cold stress
and on identifying adaptation and mitigation strategies to cope with
these events.
1.1 Cold spells
Marine cold spells are regional and prolonged instances of
anomalously cold ocean water (Schlegel et al., 2021;Figure 2).
Although these events have profound ecological and economic
impacts, including shifts in species distribution and declines in
coastal fisheries (Schlegel et al., 2021), they have received less
attention compared to marine heatwaves, which are characterized
by elevated ocean temperatures and have been linked to global
warming (Hobday et al., 2016). Notably, severe cold spells have
resulted in significant fish mortalities, coral bleaching, and
macroinvertebrate mortalities in areas such as the North Atlantic
Subtropical Gyre (Josey et al., 2018) and the Taiwan Strait (Chang
et al., 2013).Theseeventshaveresultedineconomiclosses
estimated at USD 10 million (Schlegel et al., 2021).
1.1.1 Ecological impacts
The effects of cold spells on bivalves have become an
increasingly important area of investigation in the field of
ecology. Cold spells have been shown to have a detrimental
impact on bivalve development and reproduction, with studies
demonstrating reduced growth rates and a decrease in the
number of juveniles produced (Cheng et al., 2018;Boroda et al.,
2020). This is particularly evident in areas such as China and the
North Atlantic coast, where high mortality rates of oysters and
mussels have been observed in response to cold spell events (Liu
et al., 2016;Baden et al., 2021). The impacts of cold spells on
bivalves also have indirect effects on other species within the
ecosystem. For example, a cold spell event in China resulted in a
reduction in the populations of fish and crabs that rely on bivalves
as a food source, potentially leading to a cascading effect throughout
the ecosystem (Wakelin et al., 2021). It is clear that the impact of
cold spells on bivalves represents a critical issue with far-reaching
ecological consequences. Further research is necessary to fully
comprehend the effects of cold spells on bivalve populations and
the ecosystems in which they reside.
1.1.2 Economic impacts
The impact of cold spells on bivalve populations has far-
reaching economic consequences, as bivalves, particularly oysters
and mussels, are a critical component of the global aquaculture
industry valued at over $10 billion (FAO, 2018). Cold spells can
result in a significant decline in the growth and reproduction of
bivalves, thereby reducing yields for commercial bivalve fisheries
and leading to economic losses for both fishers and the fishing
industry. Studies by Möllmann (2019) and Whitfield et al. (2016)
FIGURE 1
Effects of cold spells on bivalve species physiology, aquaculture yield, and adaptation/mitigation strategies. This figure summarizes the impact of
cold spells on bivalve aquaculture, focusing on their effects on the physiology of bivalve species, and aquaculture yield, as well as the various
adaptation and mitigation strategies employed to mitigate these impacts.
Masanja et al. 10.3389/fmars.2023.1158649
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have reported that cold spells in the Baltic Sea and Western Cape,
South Africa, respectively, caused reductions in the growth of the
common Baltic clam (Macoma balthica), Western Cape rock lobster
(Jasus lalandii) by up to 50% and 20% respectively; The Pacific
oyster (Crassostrea gigas) has been extensively studied in terms of
the impacts of marine cold spells, and studies have indicated that
prolonged cold spells can cause decreased growth and increased
mortality in oysters (Büttger et al., 2011), leading to reduced yields
for oyster aquaculture operations and economic losses for farmers
and related industries. An extensive literature search was conducted
using the terms “cold spell,”“cold wave,”“cold event,”“cold water,”
“cold-extreme,”“cold shock,”“cold stress,”and “cold temperature”
in Google Scholar, Research Gate, and Semantic Scholar to provide
a comprehensive examination of the topic.
2 Impacts of cold spells on
bivalve physiology
The impact of cold spells on bivalve physiology, with significant
findings indicating alterations in growth, reproduction, decrease in
immunity, and metabolism (Carneiro et al., 2020). Studies by Lesser
et al. (2010) and Brumbaugh et al. (2010) have shown that cold
spells can reduce the growth rate of the blue mussel (Mytilus edulis)
and decrease the number of eggs produced by the Atlantic oyster
(Crassostrea virginica) by up to 80%, respectively. These impacts
can negatively affect the species’population size and, thus, the
ecosystem. The reduction in fertility observed in bivalves during
cold spells has been attributed to changes in the production of
reproductive hormones, such as estrogen and testosterone (Liu
et al., 2016). The disruption of hormone production is linked to
the down-regulation of genes involved in their synthesis and
alterations in the signaling pathways that regulate reproduction,
including the hypothalamic-pituitary-gonadal axis (Yan
et al., 2018).
The decrease in immunity leading to higher disease incidence is
an important physiological effect of the cold spell on bivalves. Cold
exposure can suppress several components of the immune response.
This can make bivalves more vulnerable to infections by pathogens,
such as bacteria, viruses, and parasites. For example, a study on the
clam (Mactra veeriformis) showed that clams underwater
temperature stress change at 10°C, 20°C, or 30°C for 24 h. Viable
bacterial counts (VBC), total haemocyte count (THC), phagocytic
activity, lysozyme activity, Neutral red retention (NRR) times, and
superoxide dismutase (SOD) activity were assessed in three different
water temperature groups. Clams held at 10°C decreased in THC,
lysozyme activity, and NRR (Yu et al., 2009). Another study on
Mussel (Mytilus galloprovincialis) kept at 10°C shows lower
phagocytic activity than at 20°C and 30°C (Carballal et al., 1997).
Therefore, cold spell events can have significant impacts on the
health and survival of bivalve populations. In conclusion, cold spells
significantly impact the physiology of bivalve species, particularly
regarding growth, reproduction, immunity, and hormone
production. Further research is necessary to better understand the
mechanisms behind these impacts and the potential
ecological consequences.
3 Impacts of cold spells on bivalve
molecular level
3.1 Gene expression
The alteration of gene expression is a significant effect of cold
spells on bivalves. Exposure to low temperatures can activate a
multitude of molecular pathways, including those involved in stress
response, immunity, and metabolism. For instance, Zhu et al.
(2016) reported a substantial increase in the expression of genes
related to stress response, such as heat shock proteins (HSPs) and
antioxidant enzymes, in Pacific oysters (Crassostrea gigas) after 24
hours of exposure to cold temperatures. This modulation of gene
expression may play a role in the oysters’coping mechanisms
against cold stress by offering cellular protection and facilitating
repair and recovery.
Similarly, a study by Li et al. (2020) demonstrated a significant
increase in the expression of genes related to immunity, including
FIGURE 2
An example of a marine cold spell (MCS). The metrics shown are duration (D; days), maximum intensity (imax; °C), and cumulative intensity (icum; °C
days) (Schlegel et al.,2021).
Masanja et al. 10.3389/fmars.2023.1158649
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antimicrobial peptides and lectins, in blue mussels (Mytilus edulis)
after 48 hours of exposure to cold temperatures. This change in gene
expression could help mussels defend against more prevalent
pathogens in cold environments. In conclusion, these findings
highlight the importance of further investigating the molecular
mechanisms underlying the effects of cold spells on bivalves, as
they may provide insight into the adaptation strategies of
these organisms.
3.2 Biochemical composition
Cold stress in bivalves is characterized by alterations in
temperature-sensitive enzymes and increased production of HSPs
(Boroda et al., 2020). HSPs are a group of proteins that are activated
in response to stress and play a crucial role in safeguarding cells
from damage (Kregel, 2002). The expression of HSPs is a
widespread response to stress in various organisms, including
bivalves (Fabbri et al., 2008). One of the essential physiological
responses to cold stress in bivalves is the synthesis of antifreeze
proteins (AFPs) (Storey and Storey, 2013). These proteins bind to
ice crystals, inhibiting their growth and thereby protecting cells
from freezing damage (Storey and Storey, 2013). Bivalves have been
shown to produce several types of AFPs, including type I and type II
(Dong et al., 2022). The effects of cold stress on bivalves also involve
changes in biomolecule levels, such as lipids and carbohydrates
(Margesin et al., 2007). For instance, the levels of certain lipid types,
such as wax esters and phospholipids, increase in response to cold
stress (Copeman and Parrish, 2003;Margesin et al., 2007). This is
believed to aid bivalves in maintaining cell membrane integrity and
shielding against freezing damage (Storey and Storey, 2013). In the
blue mussel (Mytilus edulis), cold stress has been observed to
increase the expression of HSP70 and HSP90, which are involved
in protein folding and repairing damaged proteins (Ioannou et al.,
2009). Similarly, the Pacific oyster (Crassostrea gigas) experiences
an increase in the expression of HSP70 and HSP60 during cold
stress, which protects cellular proteins from damage (Chen et al.,
2018). Besides HSP activation, bivalves utilize other molecular
mechanisms to cope with cold stress. For example, the expression
of antioxidant enzymes, such as superoxide dismutase (SOD) and
catalase, is elevated in response to cold stress to protect cells from
oxidative damage (Storey and Storey, 2013;Boroda et al., 2020).
Additionally, bivalves increase the expression of cold-shock
proteins (CSPs) to adapt to low temperatures. CSPs are a family
of proteins that counteract some harmful effects of temperature
downshift and thus help the cells to adapt example is Ybox (Karlson
et al., 2002;Kohno et al., 2003), which regulates mRNA translation
and protect cellular proteins from damage (Dong et al., 2020). The
study on the long-term effects of low temperature on mussel species
revealed significant changes in the gill membrane composition,
which were found to be associated with alterations in the fatty acid
profile. Specifically, the analysis showed an increase in the levels of
unsaturated fatty acids, including non-methylene-interrupted ones
(NMIFA), and a decrease in the concentration of saturated fatty
acids in the gills of the mussels (Chao et al., 2020). Moreover, we
observed a notable rise in the cholesterol level in mussels exposed to
a temperature of 5°C (Chao et al., 2020). These findings suggest that
low temperatures can significantly impact the biochemical
composition of mussel gills, potentially affecting their
physiological functions. Further research is needed to explore the
mechanisms underlying these changes and their potential
ecological implications.
3.3 Impacts on immune responses
Several investigations have evaluated the effects of marine cold
spells on the immune system of bivalves. Findings indicate that such
events can impair the immune function of bivalves and increase
their vulnerability to diseases. Tan et al. (2020) observed a decrease
in the expression of immune genes in the (Chlamys farreri) scallop
due to a marine cold spell. In addition to gene expression changes,
cold spells can also affect the levels of immune proteins. Chen et al.
(2007) reported a reduction in the hemocyte lysate protein levels in
(Chlamys farreri) scallops following a cold spell. The reduced
immune response of bivalves resulting from marine cold spells
may result in increased disease incidence, as demonstrated by Tan
et al. (2020) in the (Chlamys farreri) scallop, where a cold spell
resulted in a higher occurrence of (Vibrio splendidus) disease. Long-
term exposure to low temperatures can have significant impacts on
the immune response and gene expression of bivalves, potentially
leading to changes in their physiological functions and survival.
One study on the blue mussel (Mytilus edulis) found that exposure
to cold temperatures caused changes in the expression of immune-
related genes, including genes involved in immune recognition,
phagocytosis, and oxidative stress response (Boroda et al., 2020).
The current review highlights the detrimental effects of marine cold
spells on the immune response of bivalves, causing an increase in
their susceptibility to diseases. However, further research is
necessary to comprehend the underlying mechanisms. Future
studies should particularly focus on exploring the effects of cold
spells on diverse bivalve species.
4 Mitigation and adaptation strategies
to reduce the impacts of cold spells
4.1 Mitigation strategies
Mitigation strategies aim to reduce the negative impacts of cold
spells on bivalve populations by preventing or reducing the
occurrence of cold spells. Some potential mitigation strategies
include mitigating the impacts of cold spells on bivalves,
including using thermal blankets, heated water systems, and
insulation of ponds and tanks. Thermal blankets, made of
materials such as polyethylene or fiberglass, can be placed on the
surface of ponds or tanks to reduce heat loss. Heated water systems
can also be used to maintain water temperatures at optimal levels
for bivalve growth. Insulation of ponds and tanks can also help to
reduce heat loss and maintain optimal water temperatures. In
addition, habitat restoration can increase the resilience of bivalve
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populations to cold spells by creating more suitable conditions for
bivalves to survive and grow. This can be achieved through the
restoration of seagrass beds, oyster reefs, and other habitats that
provide protection from cold temperatures. For example, seagrass
beds can act as a thermal buffer, reducing the effects of cold spells on
bivalve populations (McCay and Rowe, 2003). Finally, temperature
monitoring can provide early warning of cold spells, allowing for
proactive management of bivalve populations. For example, by
monitoring the temperature in oyster aquaculture sites, farmers
can take measures to protect their stock from cold spells (Mark
et al., 2003;Atindana et al., 2020).
4.2 Adaptation strategies
Adaptation strategies for reducing the impacts of cold spells on
bivalves include selecting cold-tolerant species and using genetic
improvement programs (Aarset,1982;Paget et al., 2014). Cold-
tolerant species, such as the Pacific oyster (Crassostrea gigas) and
the European flat oyster (Ostrea edulis), are better able to withstand
cold temperatures and are, therefore, less susceptible to cold-related
mortality. Genetic improvement programs, such as selective
breeding, can also be used to improve the cold tolerance of
bivalve populations. Overwintering is when some organisms
survive the winter season by either passing through it or waiting
it out. During this time, conditions such as cold temperatures, ice,
snow, and limited food supplies make survival difficult, notably in
insects (Bale and Hayward, 2010), birds (Latta and Faaborg,2009),
and plants (Adams et al., 2004), this a strategy that can be used to
protect bivalve populations from cold spells. This can be achieved
by moving the bivalves to a location where the water temperature is
warmer or by providing them with a suitable overwintering habitat.
Mitigating the impacts of cold spells on bivalves is a critical issue for
the aquaculture industry, as these events can result in significant
mortality and reduced growth rates.
5 Conclusion
In conclusion, cold events have a substantial impact on bivalve
species, leading to reductions in growth and reproductive capacity,
feeding and metabolic rates, and heightened mortality rates. To
cope with these adverse conditions, bivalves have evolved
mechanisms such as burrowing into the sediment, altering the
composition of their bodily fluids, and modulating their
physiology and molecular pathways. However, the effects of cold
events on bivalve species are variable and contingent upon the
severity, duration, and physiological and molecular resilience.
While global trends suggest a decline in the frequency of cold
events, additional research is required to fully comprehend the
effects on bivalve populations and to devise more effective research
and management strategies that mitigate these impacts.
Author contributions
We hereby declare the credited author states as follows: FM:
Writing –original draft, data curation, investigation, validation. YX:
Data curation, Writing –review & editing, Validation. KY: Data
curation, Writing –review & editing, Validation. RM: Writing –
review & editing. YD: Conceptualization, Resources. LZ:
Conceptualization, Writing-original draft preparation, Project
administration. Kind regards, LZ on behalf of all other co-
authors. All authors contributed to the article and approved the
submitted version.
Funding
The current research has been facilitated by funding from the
following organizations: Department of Education of Guangdong
Province (grant numbers 2020KTSCX050 and 2022ZDZX4012),
Guangdong Zhujiang Talents Program (grant number
2021QN02H665), National Science Foundation of China (grant
numbers 42076121, M-0163, and 42211530423), Modern Agro-
industry Technology Research System (earmarked fund CARS-49),
and the Scientific Research Start-up Funds program of Guangdong
Ocean University.
Conflict of interest
The authors declare that the research was conducted in the
absence of any commercial or financial relationships that could be
construed as a potential conflict of interest.
Publisher’s note
All claims expressed in this article are solely those of the authors
and do not necessarily represent those of their affiliated
organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
claim that may be made by its manufacturer, is not guaranteed or
endorsed by the publisher.
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