
==== Front
iScience
iScience
iScience
2589-0042
Elsevier

S2589-0042(24)02063-7
10.1016/j.isci.2024.110838
110838
Review
Diseases of marine fish and shellfish in an age of rapid climate change
Rowley Andrew F. a.f.rowley@swansea.ac.uk
1∗
Baker-Austin Craig 2
Boerlage Annette S. 3
Caillon Coline 4
Davies Charlotte E. 1
Duperret Léo 5
Martin Samuel A.M. 6
Mitta Guillaume 7
Pernet Fabrice 4
Pratoomyot Jarunan 8
Shields Jeffrey D. 9
Shinn Andrew P. 1011
Songsungthong Warangkhana 12
Srijuntongsiri Gun 13
Sritunyalucksana Kallaya 12
Vidal-Dupiol Jeremie 5
Uren Webster Tamsyn M. 1
Taengchaiyaphum Suparat 12
Wongwaradechkul Ratchakorn 10
Coates Christopher J. christopher.coates@universityofgalway.ie
114∗∗
1 Biosciences, Faculty of Science and Engineering, Swansea University, Swansea SA2 8PP, Wales, UK
2 Centre for Environment, Fisheries and Aquaculture Science, Weymouth, UK
3 Centre for Epidemiology and Planetary Health (CEPH), SRUC School of Veterinary Medicine, Inverness, Scotland, UK
4 Université of Brest, Ifremer, CNRS, IRD, LEMAR, Plouzané, France
5 IHPE, Université of Montpellier, CNRS, Ifremer, University Perpignan Via Domitia, Montpellier, France
6 Scottish Fish Immunology Research Centre, School of Biological Sciences, University of Aberdeen, Aberdeen, Scotland, UK
7 Ifremer, ILM, IRD, UPF, UMR 241 SECOPOL, Tahiti, French Polynesia
8 Institute of Marine Science, Burapha University, Chonburi 20131, Thailand
9 Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA
10 INVE Aquaculture (Thailand), 471 Bond Street, Bangpood, Pakkred, Nonthaburi 11120, Thailand
11 Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, QLD, Australia
12 National Center for Genetic Engineering and Biotechnology (BIOTEC), National Science and Technology Development Agency (NSTDA), Bangkok 10400, Thailand
13 School of Information, Computer, and Communication Technology, Sirindhorn International Institute of Technology, Thammasat University, Pathum Thani, Thailand
14 Zoology and Ryan Institute, School of Natural Sciences, University of Galway, H91 TK33 Galway, Ireland
∗ Corresponding author a.f.rowley@swansea.ac.uk
∗∗ Corresponding author christopher.coates@universityofgalway.ie
28 8 2024
20 9 2024
28 8 2024
27 9 110838© 2024 The Author(s)
2024
https://creativecommons.org/licenses/by-nc/4.0/ This is an open access article under the CC BY-NC license (http://creativecommons.org/licenses/by-nc/4.0/).
Summary

A recurring trend in evidence scrutinized over the past few decades is that disease outbreaks will become more frequent, intense, and widespread on land and in water, due to climate change. Pathogens and the diseases they inflict represent a major constraint on seafood production and yield, and by extension, food security. The risk(s) for fish and shellfish from disease is a function of pathogen characteristics, biological species identity, and the ambient environmental conditions. A changing climate can adversely influence the host and environment, while augmenting pathogen characteristics simultaneously, thereby favoring disease outbreaks. Herein, we use a series of case studies covering some of the world’s most cultured aquatic species (e.g., salmonids, penaeid shrimp, and oysters), and the pathogens (viral, fungal, bacterial, and parasitic) that afflict them, to illustrate the magnitude of disease-related problems linked to climate change.

Graphical abstract

Environmental science; Global change; Aquatic science; Oceanography; Zoology; Microbiology; Aquaculture; Aquaculture diseases

Subject areas

Environmental science
Global change
Aquatic science
Oceanography
Zoology
Microbiology
Aquaculture
Aquaculture diseases
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pmcIntroduction

Earth’s human population is projected to exceed nine and 11 billion by 2050 and 2100, respectively,1 placing inordinate pressure on terrestrial and aquatic environments for greater food production. For millennia, coastal communities have relied on the seas for food and feed. Although this resource was considered boundless by some, we now understand that overfishing has decimated wild stocks, resulting in economic decline and environmental degradation. Aquaculture is also an ancient practice, e.g., freshwater carp husbandry in China is some 2,000 years old,2 and more recently, the increasing demand for quality food rich in protein, omega 3 polyunsaturated fatty acids, and minerals, has triggered the development of intensive aquaculture (freshwater, brackish, and marine) such that it now exceeds yields from capture fisheries.3 Examples of marine/brackish fish and shellfish produced globally for human consumption include Atlantic salmon (Salmo salar), milkfish (Chanos chanos), gilthead seabream (Sparus auratus), Pacific whiteleg shrimp (Penaeus vannamei), crawfish such as Procambarus clarkii, and oysters (e.g., Crassostrea virginica and C. gigas).3 In the oceans, ∼17% of production comes from mariculture4 although this may develop in future years with improvements in culture methods and openings in global markets for seafood. As an illustration of the current situation of capture fisheries vs. mariculture, data show that 90.3 million tonnes (live weight equivalent) of global marine capture fishery production were reported in 2020 down from 96.5 million tonnes in 2018 while during the same period mariculture increased production from 30.9 to 33.1 million tonnes.3 Recent analyses of food production from the oceans conclude that reform in fisheries policies and processes, together with the sustainable expansion of mariculture, could increase production even after considering the diverse and complex challenges that climate change brings.4,5

Intensification of fish farming (freshwater, brackish, and marine) comes at a price with consequences linked to environmental damage, fish meal extraction from wild fish, waste product toxicity, eutrophication below sea pens, and various pharmaceuticals (e.g., antibiotics and antiparasitic drugs) leeching into the benthos.6 In contrast, the cultivation of bivalve molluscs has little environmental footprint as these do not require feed at later stages of development. Regardless of the form of cultivation or the target species, disease limits productivity and increases wastes. Furthermore, spread of pathogens/parasites from captive to wild fish and shellfish (and vice versa) is a major consequence of the expansion of aquaculture, as it is impossible to fully control biosecurity in open water systems (e.g., pens/cages housing fish and trestles and ropes for growing bivalve molluscs). An illustration of this problem comes from the infestation of Atlantic salmon (Salmo salar) by ectoparasitic copepods, the salmon louse Lepeophtheirus salmonis, and species of Caligus, where there is the potential transfer of these to wild fish in the surrounding waters.7,8 Parasitism by lice such as Caligus spp. and L. salmonis is endemic in wild fish and, in the case of the latter, is found all year long, but numbers of lice per fish is generally low such that they do not cause significant mortality. Approaches employing chemical control of lice using various organophosphates are effective but can also have detrimental effects on non-target species9,10 and lice have become increasingly resistant to certain agents.11,12,13,14 Alternative approaches to chemicals include the use of cleaner fish to consume the lice,15 mechanical devices such as high-pressure water jetting (e.g., Hydrolicer) for dislodging lice,16 a suite of physical barriers17 and novel cage designs to minimize contact with lice; and yet the management of lice in farmed salmon persists among the most prominent issue of parasitic infections in aquaculture. For example, in autumn 2023, an outbreak of L. salmonis in cultured salmon in Iceland resulted in the culling of large numbers of grossly affected fish and was reported widely in the media (e.g., https://www.theguardian.com/environment/2023/nov/03/sea-lice-outbreak-icelandic-salmon-farm-welfare-disaster-footage).

Both infectious and non-infectious diseases in wild and captive fish, shellfish, and macroalgae (seaweeds), can devastate production. For instance, economic losses in shrimp production in the Mekong Delta of Vietnam due to the bacterial disease, acute hepatopancreatic disease, and the viral disease, white spot syndrome, were estimated at >US$ 26 million and >US$ 11 million, respectively, in one year.18 For finfish, parasitic diseases result in the loss of 5.8–16.5% of the total value from aquaculture production in the U.K. alone.19 In fisheries, the effects of disease can vary in severity from catastrophic collapse of stocks through to reduced growth, fecundity, and at the lowest level, loss of marketability. Regarding the latter, a disease of marine crabs in fisheries caused by the dinoflagellate parasites, Hematodinium spp.20,21 exemplifies this condition. Over 50 species of decapod crustaceans worldwide are infected by these parasites, which can retard growth, discolor the carapace,22 and lead to mortality. In species including Tanner crabs (Chionecetes bairdi) and snow crabs (C. opilio), the infected muscle has a bitter taste (termed “bitter crab disease”) making it unmarketable.23,24

While climate change has been reviewed comprehensively in terms of general effects on fisheries and aquaculture,4,5,25,26,27,28,29,30,31 there are fewer contemporary overviews directed at infectious disease.32,33 Hence, we aim to evaluate the potential effects of climate change on infectious diseases of fish and shellfish in marine and brackish environments. By means of several “case studies” of notable diseases and their globally dispersed hosts, we also illustrate the potential magnitude of the problems faced with increasing production of high-quality food for an ever-growing population in a time of rapid environmental change. Finally, we briefly explore how these diseases can be mitigated through new approaches to farming fish and shellfish now and in the future.

What is the effect of disease on the production of food from the sea?

It is difficult to gauge the economic effects of both infectious and non-infectious diseases on wild populations of marine fish and shellfish but there is the potential for serious losses.34 Mortality in wild fish can be hidden as they are rapidly subject to predation and may decompose before they can be observed.35 Major fish kills, such as those caused by algal toxins (harmful algal blooms) become apparent when they wash onto the shoreline, but autopsy of such individuals may fail to determine the etiology of the condition that resulted in their death. Pertinent examples of diseases of fisheries with known economic consequences include ichthyophoniasis of herring36,37 and in Chinook salmon (Oncorhynchus tshawytscha) in the Yukon River38 caused by the oomycete, Ichthyophonus hoferi. In this former example, the reduction of populations of Pacific herring (Clupea pallasii) in Alaska after 1993 was attributed to a few diseases but principally to ichthyophoniasis. For shellfish, epizootic shell disease outbreaks in New England American lobsters (Homarus americanus) coincided with the collapse of the southern New England stock.39 Similarly, the decline in populations of velvet swimming crabs (Necora puber) caught in Brittany, France after 1984 was thought to be linked to the occurrence of hematodiniosis caused by dinoflagellate parasites, Hematodinium spp.40

In terms of aquaculture, diseases are more readily observed and identified, and the associated economic losses are easier to calculate despite being highly variable in severity across locations, the species affected, and in different seasons. There has been a revolution in molecular “tools” available for pathologists to identify and track the spread of disease-causing agents41 and these complement traditional approaches such as microscopy and histopathology. Advances in epidemiology, including the modeling of disease dynamics and transmission, are also important when preparing for emerging diseases, and forecasting outbreaks.42,43,44

Elevated temperature and changes in the prevalence and severity of infectious diseases in the oceans

This last year, 2023, was the warmest since modern records began in 1850.45 Global climate data for January–December 2023 show that oceans were 0.91°C higher than average making this the warmest since 1850.45 (Figure 1). Similarly, land and ocean + land temperature anomalies, were +1.79 and +1.18°C, respectively, with sea surface temperatures hotter than average in several areas of the world including parts of North and South America, Europe, Africa, Oceania, and Asia.45Figure 1 Global ocean temperature trends

Derived from the HadCRUT5 (ensemble means and uncertainties) dataset of Morice et al. (2021)46 that uses a combination of sea-surface temperatures and near-surface air temperatures over land and compared against the 1961–1990 reference period.

The gradual increase in global temperatures varies geographically, as such, there is a crucial need to examine local temperature trends in each major aquaculture-producing country together with the temperature and thermal tolerance ranges of both pathogens/parasites and their fish and shellfish hosts (Table 1). Such information will allow refined predictions of future changes in disease prevalence and severity.Table 1 Pertinent examples of pathogens and parasites affecting marine aquaculture and their temperature ranges, optimal conditions, and critical thresholds affecting their environmental survival

Disease	Pathogen/Parasite (taxonomy)	Hosts	Temperature range (°C)	Optimum temperature (°C)	Thermal tolerances (°C)	
AHPND	Vibrio parahaemolyticus (G- bacterium)	Shrimp	5–37	20–35	<5–10 & >35-40	
Bacterial kidney disease	Renibacterium salmoninarum (G+ bacterium)	Salmonid fish	5–22	15–18	<0–4 & >20-25	
Bonamiasis	Bonamia ostreae (Haplosporidia)	Bivalve molluscs	4–25	12–20	<5–10 &>25-30	
Dermo disease	Perkinsus marinus (alveolate)	Oysters	>2-28	25	<2	
Infectious salmon anemia	ISA virus	Salmonid fish	3–24	10–15	>25	
MSX disease	Haplosporidium nelsoni (Haplosporidia)	Oysters	5–20	20–22	<4 & >20	
Necrotizing hepatopancreatitis	Hepatobacter penaei (G-bacterium)	Shrimp	25–32	28–30	<20–25 & 35-40	
Salmon louse	Lepeophtheirus salmonis (copepod)	Salmonid fish	3–24	10	<3 & >24 (high loss)	
White spot disease	White spot syndrome virus	Shrimp	0–50	25–28	>50	

Increased temperatures are the best understood consequences of climate change in terms of aquatic diseases.47,48 Higher temperatures have effects on both host and parasite/pathogen normally to the detriment of the host and the relationship is exacerbated if outside their thermal range; Figure 2). In terms of pathogenic bacteria, higher temperatures often stimulate multiplication rates and may also lead to higher virulence (i.e., disease causing ability) caused by changes in the expression profiles of virulence factors such as hemolysins, siderophores, and a variety of endo- and exo-toxins (e.g., refer to studies by Lages M.A. et al., Lopez-C.G. et al., and Lee Y. et al.49,50,51). Hosts may become immune suppressed by direct effects on immune cells or indirectly, as dysbiotic changes in their microbiomes can potentially inhibit the immune system (e.g., refer Liang Q. et al. and Hembron P.S. et al.,52,53 see also Case study #1 in this review). As a rise in winter sea surface temperatures may permit pathogen multiplication, this can result in all-year round infections,47 perhaps initiating emerging diseases, or, infectious agents changing their host and geographic ranges.Figure 2 Environmental, host and pathogen/parasite features that co-exist to promote disease outbreaks

Examples of how elevated temperature associated with climate change can affect the prevalence and severity of aquatic diseases in fish, shellfish, and seaweeds are shown in Table 2. Three of these examples are discussed further in the following text and in Case studies #2–6. For salmonid fish, the interaction between temperature and ectoparasitic sea lice, L. salmonis has been investigated using a range of approaches from experimental through to modeling (Table 2).54,55 Considering the interaction between the parasite, host, and environmental temperature using an experimental approach revealed that increasing temperatures between 10°C and 22°C reduce the growth, condition, and survival of Atlantic salmon post-smolts exposed to varying infestation levels of lice/fish ranging from zero, low (1.4 lice per fish) to high (ca. 6.8 lice per fish) levels.55 Collectively, these and other data may suggest that control of lice affecting salmon farming in warming waters in the Northern hemisphere may become increasingly difficult in coming years.Table 2 Examples of changes in disease prevalence and/or severity linked to high environmental temperatures

Host(s)	Disease and (causative agent)	Location	Change reported	Key reference(s)	
Various marine fish and abalones (Haliotis rubra and H. laevigata)	Gill damage in fish (diatom, Chaetoceros coarctatus)	South Australia	High (ca. 27°C) and variable water temperatures (5°C above average) causing mortalities in fish and abalone. Causative agent may be associated with algal blooms. Fish affected in shallow waters near and/or above thermal tolerances	Roberts et al.56	
Atlantic salmon (Salmo salar)	Salmon louse (parasitic copepod, Lepeophtheirus salmonis)	Tank-based experiment	Increases in temperature result in faster development of infective stages of parasite	Hamre et al.54	
Salmon (wild and farmed)	L. salmonis	Pacific coast, B.C., Canada	Climate change models show future increase in abundance of sea lice resulting in current control strategies becoming ineffective	Godwin et al.55	
Salmon (S. salar)
(migrating wild smolts)	L. salmonis	Model based on wild smolt from river Vasso in Norway migrating in coastal waters	Models predict that with increasing temperature lice will cause more damage to migrating salmon smolts and that those fish at the southernmost margins are therefore most vulnerable to the effects of sea lice.	Vollset et al.57	
Atlantic salmon (S. salar)	Gill disease (several non-infectious and infectious conditions)	Various including Chile, Canada and N. Europe	Prevalence of gill damage linked to high water temperatures. See Case study #6	Foyle et al.,58 Jones and Price59	
Striped bass (Morone saxatilis)	Dermal mycobacteriosis (Mycobacterium spp.)	Chesapeake Bay region, USA	Both healthy and diseased bass show a 3-fold increase in mortality with rises in summer surface temperatures of 26°C–28ºC inferring that these fish are close to their thermal tolerance	Groner et al.60	
Eastern oyster (Crassostrea virginica)	Dermo disease (Perkinsus marinus)	Gulf of Mexico to Chesapeake Bay, USA	Northwards spread of Dermo linked to increased winter sea surface temperatures	Cook et al.61	
Pacific oyster (Crassostrea gigas)	Summer mortality (Vibrio sp.)	Aquarium based experiments with oysters from the Wadden Sea, Germany	Thermal stress and spawning status decrease the disease resistance to vibriosis resulting in higher mortality at 21°C than 17°C	Wendling and Wegner62	
Pacific oyster (C. gigas)	Mass summer mortality (Vibrio alginolyticus)	Shandong Province, China	High summer temperatures result in >60% mortality linked to more rapid growth and upregulation of virulence genes in vibrios. No evidence of involvement of other pathogens such as ostreid herpes virus 1	Yang et al.,63 Li et al.64	
Pacific oyster (C. gigas)	Pacific oyster mortality syndrome (POMS)
(polymicrobial, ostreid herpes virus 1 and Vibrio spp.)	Europe	A polymicrobial condition where initial infection by the virus causes immune suppression resulting in individuals being more susceptible to secondary bacterial infections by vibrios. Epizootics occur between 16°C and 24°C (See Case study #4)	Petton et al.,65 Petton et al., 2021,66 de Lorgeril et al.,67 Combe et al.,68 Destoumieux-Garzón et al.,69 and Oyanedei et al.70	
Abalone (Haliotis tuberculata)	Vibriosis (Vibrio harveyi)	Normandy & Brittany, France	Long term higher summer temperatures associated with abalone mortality. Increase in temperature above 17°C associated with vibriosis	Travers et al.71	
Black abalone (Haliotis cracherodii)	Withering syndrome (Rickettsiales-like bacteria; Candidatus Xenohaliotis californiensis)	Laboratory and field-based (California coast)	Animals exposed to high temperature showed disease in tank-based experiments. Extreme environmental temperatures favor disease progression in intertidal zone	Ben-Horin et al.72	
American lobster (Homarus americanus)	Epizootic shell disease (bacterial dysbiosis)	Massachusetts, USA	Increase in temperature results in microbial dysbiosis on shell resulting in erosion, cuticular damage and mortality. (See Case study #5)	Groner et al.,73 Ishaq et al.,74 Rowley and Coates,75 and Shields76	
Shrimp (including Penaeus vannamei)	Acute hepatopancreatic necrosis disease [AHPND, = early mortality syndrome]
(Vibrio spp. including V. parahaemolyticus)	Mexico, Thailand, USA	Strains of vibrios that produce the toxins PirABvp cause this disease that is characterized by high mortality. Both salinity and high temperature modify the expression of the PirA gene responsible for toxin generation that cause AHPND (See Case study #3)	Estrada-Perez et al.,77 Lee et al.,78 and Tran et al.79	
Shrimp (Penaeus setiferus and Penaeus aztecus)	Shrimp black gill (ciliate, Hyalophysa lynni)	Texas Gulf coast, USA (Gulf of Mexico)	High temperatures (>20°C) and lower salinity (<10 ppt) caused by precipitation events, are environmental drivers of this condition	Swinford et al.80	
Blue crab (Callinectes sapidus)	(dinoflagellate, Hematodinium perezi)	Atlantic seaboard, USA	Water temperatures of >25°C and salinity (>30 ppt) favor parasite development in its host. Milder winters facilitate parasite survival	Shields,76 Huchin-Mian et al.,81	
Snow crab (Chionoecetes opilio)	Bitter crab disease (dinoflagellate, Hematodinium sp.)	Newfoundland, Eastern Canada	Warm water masses raising temperatures from −1.4°C to 2.0°C spurred epizootics	Shields et al.82	
Red seaweed (Delisea pulchra)	Bleaching (bacterial dysbiotic condition associated with appearance of Alteromonas sp., Aquimarina sp. and Agarivorans)	Subtidal habitats near Sydney, Australia	High summer temperatures result in bleaching events especially in shallow water. High temperatures appear to drive reduction in levels of host’s antibacterial chemicals (halogenated furanones) resulting in bacterial dysbiosis and possible immune suppression	Campbell et al.,83 Kumar et al.,84 and Hudson et al.,85	
Seaweeds (various species)	Ice-ice disease (bacterial dysbiotic condition?)	Widespread including India, China and Zanzibar	Disease appears in hot and dry season. Aquarium based studies show temperatures between 33°C and 35°C trigger disease above thermal tolerance level of some seaweeds	Largo et al.,86 Largo et al.,87 Arasamuthu et al.,88 and Ward et al.,89	

Abalone populations in the Pacific Ocean from Mexico to California have been decimated by a condition termed withering syndrome (Table 2). The cause of this disease is an intracellular bacterium that is rickettsiales-like.90,91,92 Abalone farming can be a highly lucrative venture as these are some of the highest value shellfish and declines in the populations of black and red abalones of the Californian coastline are attributed, at least partially, to this chronic condition that occurs as epizootics following abnormally high-seawater temperatures associated with El-Niño-southern oscillation (e.g., refer to studies by Tissot B.N. and Moore J.D. et al.93,94). Abalones adapted to cool water temperatures are more susceptible to withering syndrome than those with higher thermal ranges.95

Putative effects of temperature on multicellular parasites can be difficult to assess as some have multiple life history stages to enable them to finally reach their definitive host, or they may employ reservoirs of infection. For example, digenean parasites of marine animals often have sea birds or fish as their definitive host and various invertebrates, including crustaceans and molluscs, as intermediate hosts. The trematode Microphallus similis is a parasite of sea birds (e.g., gulls) and has two intermediate hosts normally littorinid snails and various crabs including the common shore crab, Carcinus maenas.96,97 Changes in the distribution of these intermediate hosts resulting from climate change, or the appearance of newly arrived non-native snails or crabs, could interrupt the life cycle of the parasite.98 This is likely to occur as the parasite is a host generalist. There are reports of temperature effects on parasite emergence in marine trematodes—for example, Thieltges and Rick99 examined the life history of the trematode, Renicola roscovita, a parasite of bivalves in the North Sea. The periwinkle, Littorina littorea, is the first intermediate host of R. roscovita and bivalves, such as mussels and cockles, are the second intermediate host that become infected when cercariae are released. Mesocosm experiments revealed that cercariae infectivity is optimal at 20°C (August temperatures) and the authors concluded that warmer summers in this region will enhance the transmission of R. roscovita with resulting ecosystem effects.

Magalhães et al.100 examined how predicted changes in climate (salinity, pH, and temperature) in Europe may affect the echinostome Himasthla elongata in its second intermediate host, the edible cockle, Cerastoderma edule. Overall, higher infection success in cockles was found in all three variables under climate change predictions. For example, parasitized cockles at the higher temperature regime of 22°C showed a greater amount of cellular damage because of reduction in their antioxidant levels than those held at 17°C.

Although the focus of this review are diseases of fish and shellfish, brief mention is made of other mariculture products, namely seaweeds, and environments where juvenile fish reside such as coral reefs and seagrass meadows, which are also impacted by climate-driven diseases (Table 2). Seaweed cultivation and harvesting are of increasing importance as sources of various chemicals (e.g., agar and carrageenan), nutraceuticals, cosmetics and feed supplements,101 and as a tool for carbon sequestration. Disease limits production of seaweeds and examples of pathogens can be found in all the major taxonomic groups including bacteria.89,102 Two such conditions probably caused by bacteria have been linked to unusually high temperatures including bleaching in the red alga Delisea pulchra83 and “ice-ice” disease in numerous seaweeds.88 In D. pulchra, the disease is associated with dysbiosis where opportunistic bacterial pathogens including Alteromonas sp., Aquimarina sp., and Agarivorans sp. prevail.84,103 Notably, Aquimarina spp. are involved in epizootic shell disease in lobsters that is also triggered by raised sea temperatures (See Table 2 and Case study #5 for further detail). These observations suggest that opportunists such as Aquimarina spp. and other members of the phylum Bacteroidota could emerge as threats to a wide range of marine organisms in response to changes in oceanic conditions.75,104

Seagrass meadows are vital nurseries for juvenile fish and shellfish105 and disease-attributed losses can affect these animals. Seagrasses are declining worldwide, and higher temperatures are considered the proximal driver of disease outbreaks, e.g., Labyrinthula zosterae, a protistan pathogen of common eelgrass, Zostera marina.106

Coral reefs provide key habitat to many species of fish and invertebrates and their loss due to climate change and other anthropogenic stressors can have a knock-on effect on fisheries. Coral reef deterioration and bleaching (both microbial and stressor induced) are linked intimately with increased temperatures and predicted to become more prevalent and intense with climate change. Between 1992 and 2018, coral disease prevalence trebled to ∼9.9% globally according to a meta-analysis of disease prevalence, coral coverage, and sea surface temperatures.107 In the same study, 76.8% of global coral reefs are modeled/predicted to be infected/diseased by 2100. If realized, such levels of disease in coral reefs would have devastating consequences for many ecosystem services, notably food provision (biodiversity and productivity108) and carbon sequestration.109

Of course, not all diseases are likely to become more prevalent in a changing climate as some pathogens/parasites are negatively affected by rising temperature. For example, winter ulcer disease of Atlantic salmon caused by a bacterial consortium (e.g., Moritella viscosa, Aliivibrio wodanis, and Tenacibaculum sp.) occurs in water at 7–8°C or below in Norway110 and so changes in water temperature now and in the future, may decrease its significance as a key disease in winter months. Other diseases in temperate-Arctic regions that affect fish during the winter include cold water vibriosis caused by Vibrio salmonicida.111 The disease does not typically occur at temperatures above 10°C, which correlates with the temperature profile for siderophore (iron-binding) production—a key virulence factor for this bacterium.112

Changes in other environmental parameters and their potential effect on prevalence and severity of infectious diseases

Beyond temperature, climate change has other profound effects including sea level rises, ocean acidification, deoxygenation, and increased frequency of storms resulting in storm surges, precipitation resulting in freshwater runoff changing salinity, and pollutants leeching from the land into coastal regions (Figure 2). These are likely to fuel changes in disease occurrence particularly in vulnerable coastal regions, but they are much less understood as drivers than temperature.113

White spot disease of crustaceans is an indisputable threat to shrimp cultivation worldwide, and by 2012, was estimated to have cost US$ >18 billion in losses.114 Shinn et al.18 attribute annual losses of US$ 4 billion per year between 2009 and 2018. This disease is caused by the white spot syndrome virus (WSSV) that has a wide host range including shrimp and crabs.115 Higher temperatures favor viral multiplication in general; however, a recent overview concluded that temperatures between 25°C and 28°C favored multiplication of WSSV but above 30°C caused declines in this process.116 A further observation was that stress caused by rapid temperature and salinity fluctuations was the principal predisposing factor to disease progression rather than higher temperatures alone. Because climate change can alter salinity levels rapidly due to increased incidence of storm activity, such events may be more common in future. Other drivers such as eutrophication, may also play a part in promoting this disease especially in coastal/photic zones.

Bivalves are vulnerable to acidification as their calcium carbonate containing shells are a major barrier to disease-causing agents gaining entry to internal tissues and as a defense to predation.117 Shells lacking strength and rigidity are potentially more likely to be damaged by wave action resulting in opportunistic pathogens gaining entry to soft underlying tissues116 although this requires experimental evidence of such correlations. While there are numerous studies examining various scenarios of ocean acidification including changes in physiological processes, only a few have attempted to determine the likely effects of predicted changes to disease susceptibility and/or resistance (e.g., refer to studies by Schwaner C. et al. and Clements J.C. et al118,119).

Climate change and immune system modulation in fish and shellfish

The phagocytosis and subsequent intracellular destruction of pathogens and parasites is a fundamental defense mechanism of all multicellular animals. In shellfish (crustaceans and molluscs), the cells involved are termed haemocytes (because they are housed in the main body cavity the haemocoel) while in fish the equivalents are granulocytes, monocytes/macrophages and other professional phagocytes. Shellfish also depend on a range of antimicrobial factors including antimicrobial peptides (AMPs), lectins, lysozymes, and in some cases, the products of the prophenoloxidase activating system.117,120 Fish also produce AMPs, lectins, and lysozymes but have additional molecules including immunoglobulins (antibody), a range of immunoregulatory cytokines, and terminal factors of the complement system such as the membrane attack complex, to deal with invasive pathogens and parasites.121,122

As fish and shellfish are poikilotherms, their immune systems are influenced by environmental changes such as temperature, salinity, and pH and so climate change is likely to affect their health status. In general, abnormally high and low temperatures act as immune suppressors but this depends on the duration of stress (acute, subacute, and chronic), the thermal tolerance ranges of individual species, and the presence of other environmental stressors such as rapid fluxes in salinity caused by storms and chemical contaminants in runoff.123 Changes in temperature124,125,126, pH127, and salinity128,129 have been shown to adversely affect the immune systems of both fish and shellfish and the literature (especially that pertaining to teleost fish) is replete with examples that have been reviewed in detail elsewhere.130,131,132,133,134 Some pertinent examples are highlighted in Table 3 to illustrate how climate change may affect the immune capacity of shellfish, while examples in fish are discussed in the following text.Table 3 Examples of environmental immune modulation in shellfish

Model species	Environmental parameter(s)	Immune and other assays	Overall conclusions	Reference	
European abalone (green ormer) (Haliotis tuberculata)	Increased temperature as found in summer months	• Phagocytic activity

• Phenoloxidase activity

• Superoxide dismutase (marker of intracellular antimicrobial generation)

	High summer water temperatures coinciding with gametogenesis, causing lower immune capacity, as evidenced by assays, resulting in higher chance of vibrio infections	Travers et al.71	
Pacific oyster (Crassostrea gigas)	Temperature stress (17°C–19°C)	• Phagocytic activity of hemocytes

• Survival following vibrio infections

	Post-gametogenesis oysters are more susceptible to vibriosis due to immune depression caused by gametogenesis exacerbated by higher temperatures	Wendling and Wegner62	
Thick shell mussel (Mytilus coruscus)	Short term pH and salinity stress	• Hemocyte mortality and counts

• Phagocytic activity

• Lysosomal content of hemocytes

	Decrease in pH results in lower hemocyte counts, phagocytosis and lysosomal content. Overall, high and low salinities and low pH have negative effects on hemocytes	Wu et al.135	
Blue mussel (Mytilus edulis)	Combinations of acidification (apparent pH 7.99 reduced to 7.65) and long term (6 months) temperature stress (12 increased to 15°C)	• Total hemocyte counts

• Phagocytic ability

• Hemocyte respiratory burst assay

	Increase in hemocyte number (a marker of stress?) at higher temperatures. Acidification has limited effects on own or in combination	Mackenzie et al.127	
American lobster, (Homarus americanus)	Temperature stress (16 vs. 24°C)	• Phagocytic activity

• Hemocyte viability in vitro

	Immune system compromised above 21°C. Temperature affects viability of hemocytes in vitro.	Steenbergen et al.136	

Most fish have body temperatures that are isothermal with the surrounding environment. In general, fish at low temperatures, such as those in Arctic-temperate winter, rely more on their non-specific defenses (e.g., phagocytosis, complement fragments, lysozyme, and AMPs) than those as part of their specific defenses (e.g., antibody generation and cell mediated immunity delivered by T cells). Hence antibody levels and some other key regulatory immune molecules, such as cytokines, decrease with declining temperatures in a wide range of fish including those in Arctic, temperate, and tropical climes.134 With an impaired specific immune system, vaccination in winter temperatures becomes impractical and several cold-water adapted pathogens, including cold-water vibriosis, exploit the impaired immune system.

Fish within their optimal thermal range are more likely to have a “balanced” immune system relying on both non-specific and specific reactions to maintain homeostasis. Short-term (hours-days) sudden elevation in temperature triggers a stress response, while in the longer-term, high temperatures lead to immune suppression particularly associated with specific immunity.137 Temperature shifts in terms of immune reactivity have been extensively studied in a wide range of fish of both commercial and non-commercial significance (see Table 1 in Scharsack and Franke; 134 for examples). There are, however, only a relatively small number of long-term studies likely to reflect climate change scenarios simply because of the difficulty in conducting such experiments in many research aquaria. A valuable example of such long-term studies is that of Magnadottir et al.137 who carried out an extensive 12-month aquarium-based study on the effect of temperature on Atlantic cod (Gadus morhua) where one group of fish was held at 1°C (winter temperature), a second group at 7°C (the optimum temperature for cod), and another at 14°C (at the margins of thermal tolerance for this species). As expected, antibody levels were highest in the 14°C group but hemolytic activity (a marker for the complement activated part of the non-specific immune system) was lowest in this same group and highest in fish at 7°C. As these data were only collected at the end of the experiment (i.e.,12 months) there is no temporal information on the dynamics of these parameters. Nonetheless, fish in both the 1°C and 7°C groups showed the highest growth rates and the overall conclusion was that 7°C was the optimum temperature for Atlantic cod in terms of their immune capacity.

Fish at high temperatures, including those near or above their thermal range, also show evidence of immunosuppression with a generalization of higher dependence of such individuals to rely on their non-specific, as opposed to their specific, defenses.134 For example, to simulate the effects of climate change, Zanuzzo et al.138 placed Atlantic salmon (S. salar) in aquaria with incremental temperature increases of 1°C per week from 12°C to 20°C and 4 weeks later measured multiple parameters associated with non-specific defenses. They found no evidence of major deleterious effects of these high temperatures on several markers of non-specific immunity (e.g., plasma lysozyme and complement activity) but the short-term nature of their study and lack of infection trials (pathogen challenge), are potential limitations in their experimental design.

Case studies

This section of our review employs six examples of how climate change may affect aquatic diseases taken from diverse geographic areas, pathogen types and hosts.

Case study #1: Will climate change increase disease susceptibility in fish and shellfish via microbiome perturbation?

In fish and shellfish, host-associated microbiomes are abundant within the intestinal tract and are also associated with all other mucosal surfaces (i.e., gills and skin) and with hemolymph (blood) in invertebrates.135,139 Microbiota broadly influence host physiology, including nutrient acquisition, metabolism, immune function, and pathogen defense.140 Relationships between microbiota, the host immune system, and pathogenic agents are complex, dynamic, and can strongly influence disease outcomes.141 In fish, commensal microbes influence the immune system development and maturation130,142 while diverse interactions between immune cells and microbiota maintain their symbioses.141,143 Less is known for shellfish, although crustacean hemolymph microbiota interact with host immune response144 and microbial metabolites can influence the immune system of crustaceans.145

Healthy microbiomes are generally diverse, ecologically stable, and respond dynamically to environmental and host fluctuations.140,141,146 Commensal and mutualist microbiota can inhibit pathogen colonization, including via competition, niche modification, and/or production of antimicrobial agents.143 Microbiomes, however, are sensitive to disruption by environmental stressors, often leading to reduced diversity and impaired function (dysbiosis), which can subsequently allow potential pathogens to colonize and proliferate.147 Pathobiomes can be highly complex, consisting of multiple potential pathogens, and their products, rather than single causative agents of disease.148 Signatures of dysbiosis have been identified in fish microbiomes following exposure to antimicrobial agents and environmental stressors.149 These typically include reduction in microbiome diversity and beneficial (anti-inflammatory) bacteria, together with an increased abundance and/or pathogenic activity of opportunistic microbes, influenced by species and mucosal surface.147,149,150,151

Stressors associated with climate change are likely to induce microbiome perturbation and disrupt the critical relationship between microbiome and immune system, subsequently increasing disease risk particularly in aquaculture settings. There is considerable evidence that finfish and shellfish microbiomes are highly sensitive to temperature changes across a range of species. Within poikilothermic hosts, in particular, external temperature directly impacts the microbiome, imposing differential selection pressures within the community and altering microbe physiology and function.149,152 In addition, temperature-induced changes in host metabolism, immune system, gut function, cortisol, and mucous production, for example, are likely to influence the microbiome indirectly. The effects of temperature change on fish and shellfish microbiomes vary depending on the nature of the stressor. Relatively small thermal fluctuations often cause transitory microbiome changes, whereas more chronic, mild temperature change can induce alternative, but stable, microbiome states.149,152 Notably, microbiomes have an extensive capacity to develop tolerance of temperature stress, which may also confer benefits to the host.153 More severe thermal stressors, such as those associated with heatwaves or prolonged temperature elevation, however, are likely to overwhelm this resiliency and induce dysbiotic transitions characterized by reduced diversity and increased presence of opportunistic pathogens.147,148,149,151

Only a small number of studies have to date directly linked temperature stress with dysbiotic transition and increased pathogen abundance in the microbiome and even fewer have documented clinical signs of disease. Some of these studies with shellfish and fish are briefly discussed in the following text. A rapid rise in temperature simulating a heat wave induced changes in the microbiome of Pacific oysters (C. gigas) with significant increases in vibrios including V. harveyi that resulted in high levels of host mortality.154 Also, Pacific oysters that had been acclimated to high temperatures, were protected against subsequent rapid temperature stress resulted in lower mortality and vibrio loads than those seen in controls.155 In another mollusc, the Yesso scallop, Mizuhopecten yessoensis, heat stress increased the abundance of pathogenic bacteria, Tenacibaculum and Mycoplasma in the gut microbiome as well as intestinal pathologies.156 In fish, increased temperature elevated several opportunistic pathogens in the gut of greater amberjack (Seriola dumerili) and this was directly associated with reduced host productivity.157 Similarly, heat stress in chum salmon (Oncorhynchus keta) increased the abundance of several opportunistic Vibrio spp.,158 while estuarine Eastern striped grunters (Helotes sexlineatus) exposed to thermal pollution showed evidence of gut dysbiosis including increased prevalence of pathogenic Photobacterium.159 Other studies have demonstrated that heat stress both disrupts the microbiome and exacerbates the effects of experimental pathogen exposure. For example, in the Pacific oyster, hard-shelled mussels and sea cucumbers, elevated temperatures increase susceptibility to experimental Vibrio infection and simultaneously induce dysbiosis in gut and hemolymph microbiomes.160,161,162,163 These studies, however, have shown that dysbiotic microbiome changes rarely simply facilitate proliferation of a given target pathogen (i.e., Vibrio) but, rather, tend to be characterized by increased abundance of a number of opportunistic pathogens typical of the complex pathobiome state.148 As such, causal mechanisms linking temperature stress to disease via microbiome disruption are not well established.

Aquaculture microbiomes are also likely to be sensitive to other environmental stressors directly or indirectly associated with climate change, including acidification, hypoxia, salinity, pollution, and nutrient availability. Although these stressors are known to alter fish and shellfish microbiomes (e.g. refer to studies by Xavier R. et al, Dang X. et al., Khan B. et al., and Zhong K.X. et al.147,164,165,166), research examining how microbiome disruption could enhance disease susceptibility has been scarce.147,166 Interactive effects of combined stressors, newly emerging pathogens, as well as stressor-impacts on other aspects of host physiology all increase complexity and will likely exacerbate disease risk. Ultimately, research is required to better understand how functional changes during microbiome to a dysbiotic pathobiome affect host physiology, such as mucosal surface integrity and inflammatory and immune responses, which subsequently determine disease pathology. This knowledge may help us to better predict and mitigate disease risk in a changing world.

Case study #2: Vibrios are barometers of climate change in the oceans

Climate change influences the dynamics of Vibrio bacteria, a genus that includes pathogens of humans such as those causing cholera (e.g., toxigenic V. cholerae) and vibriosis (non O1/O139 V cholerae, V. parahaemolyticus, V. vulnificus, and V. alginolyticus)167 and opportunistic pathogens in fish and shellfish (refer to Mohamad N. et al.168; see also Case studies #3 and 4 in this review). Vibrios are natural inhabitants of estuarine, coastal, and marine environments and play an important role in the aquatic ecosystem and biogeochemical cycles.169 They produce various macromolecule-degrading extracellular enzymes (including chitinase, proteases, and lipases) that degrade carbon substrates into nutrients.170 Such characteristics allow for their rapid growth such as when climate change increases the level of river discharge with terrestrial nutrients.171 Rising global temperatures, especially in oceans and coastal regions, create favorable conditions for the proliferation of vibrios relevant to human and animal health. Because these bacteria tend to grow and proliferate in warm, low-salinity conditions, and because vibrios are among the fastest growing bacteria studied to date, they have been dubbed a microbial “barometer” of climate change.171 Changes in oceanic factors like salinity and sea surface temperatures impact the distribution and abundance of various Vibrio species, and compelling long term molecular studies underpin how climate influences the presence and abundance of these bacteria across global scales.172,173 Life cycles of vibrios can also be complex. They can be found either free living in the water or surface attached to plankton and marine animals.174 An increase in ocean temperature also increases the abundance of vibrios in plankton-associated bacterial community.174,175,176

As a result of these changes, we are now witnessing the emergence of what were once considered tropical bacterial pathogens into many colder temperate areas. Extreme weather events such as hurricanes177 and heatwaves178 can introduce Vibrio species into new areas and can greatly increase their concentration in the environment, where they can initiate infections of humans and other animals. Contact between humans and Vibrio-contaminated raw shellfish during times of higher-than-normal sea surface temperatures leading to disease appear to be increasing in occurrence.179,180 Understanding the interplay between Vibrio and climate change is crucial for anticipating and mitigating potential human health risks and species under aquaculture cultivation such as oysters and shrimp. Comprehensive surveillance, research, and public health measures are essential to address the emerging challenges posed by the complex relationship between Vibrio bacteria and climate-driven environmental changes.

Case study #3: Climate change effects on Vibrio infections of shrimp

Acute hepatopancreatic necrosis disease (AHPND) is an emerging disease of shrimp in culture resulting in high mortality. It first emerged in China in 2009 and spread to Vietnam in 2010, Malaysia in 2011, Thailand in 2012, and Mexico in 2013181 causing a substantial economic loss of USD 44 billion in 2010–2016.181 Vibrio parahaemolyticus was the first species identified to be associated with AHPND. Genome analysis revealed that various V. parahaemolyticus isolates recovered from shrimp and pond water during AHPND outbreaks are genetically diverse, indicating that the disease-causing isolates are not clonal.182 AHPND pathology is brought about by Photorhabdus insect-related (Pir) toxins encoded by the pVA1-type plasmid.78,79,183 Vibrio spp. carrying such plasmids can cause AHPND including V. parahaemolyticus, V. harveyi, V. campbellii, V. owensii, and V. punensis.184,185,186 Two toxin homologues to Pir toxins (A and B) are produced and secreted from these species and cause severe cell necrosis in the hepatopancreas (Figures 3A and 3B).Figure 3 Damage to the hepatopancreas (HP) of shrimp infected with V. parahaemolyticus caused by toxins

(A) Normal histological structure of the hepatopancreas.

(B) Appearance of damaged hepatopancreas. Note tubule disruption.

Environmental changes can have profound effects on toxin generation by these vibrios associated with AHPND. Expression of the PirA toxin is altered upon changes in temperature and salt concentration, suggesting the involvement of environmental factors to virulence and pathogenicity.187 Interestingly, the pVA1-type plasmid spreads horizontally across the Vibrio genus by conjugative type IV secretion system encoded on the VA1-type plasmid.188 The efficacy of conjugation is also regulated by environmental factors such as bacterial density, temperature, and nutrient levels.188 In addition to impacting the abundance, spread, and species composition of vibrio community, climate change also seems to influence the spread of virulence plasmid like pVA1. Virulence-related genes, including genes involved in adhesion, biofilm formation, toxins, and type III secretion systems, are responsive to climate-dependent environmental cues like temperature, salinity, and pH. For instance, an increase in seawater temperature (from 21 to 27°C and 31°C) upregulates virulence gene expression, enhancing adhesion and biofilm formation in V. parahaemolyticus.189 Expression of a thermostable direct hemolysin, a virulence factor with hemolytic and cytotoxic activity, is also upregulated in V. parahaemolyticus upon an increase in seawater temperature.189 Expression of type III secretion system 2, essential for host colonization and immune modulation, in V. parahaemolyticus is also regulated by temperature and salt responsive histone-like nucleoid-structuring protein.190 Taken together, the occurrence of AHPND during shrimp cultivation seems to be a result of complex interaction of multiple factors—species composition, virulence factors, environmental signals such as temperature and salinity, and host immunity.189,190

Case study #4: Pacific oyster mortality syndrome—A polymicrobial and multifactorial disease

Since 2008, massive mortality events have occurred yearly with the emergence of a disease called Pacific oyster mortality syndrome (POMS) severely affecting the oyster industry.191,192,193 Within the two following decades, this disease has become panzootic affecting Pacific oyster populations all around Europe, North America, Asia, and the South Pacific.194,195,196,197,198,199,200,201 POMS is associated with the recurrent detection of Ostreid herpesvirus type 1 μVar (OsHV-1 μVar) in moribund oysters191,192,193 as well as strains of the bacterial genus Vibrio.67,70,202,203,204 Infection by OsHV-1 is the initial step that leads the animal to an immunocompromized state resulting in a bacterial dysbiosis followed by a bacteraemia responsible for oyster death.67 Several bacterial genera are involved in this secondary infection67,205; among them vibrios that behave as opportunistic pathogens causing hemocyte lysis.70,204

The risk of POMS outbreaks is dependent on complex interactions between host, pathogens, and environmental factors.191,206,207,208,209,210 Among the environmental factors that influence POMS, temperature and pH are directly related to climate change. Other factors, indirectly linked to climate change must also be considered including food availability (primary production), energetic status of the host, and salinity. Here, we review how these factors individually affect POMS.

Temperature, ocean warming, and marine heatwaves

In Europe, POMS epizootics occur when the seawater temperature is between 16°C and 24°C206 Below 16°C, OsHV-1 infections can persist in latent forms or low-replication rates, as reported in other herpesviruses.211,212 Then, reactivation of the virus can occur several weeks or even months after initial exposure, in response to increases in temperature above 16°C207,213 Increased temperature results in increased viral replication and shedding by the host, reflecting increased growth metabolism.214 When the seawater temperature reaches 24°C or more, epizootics are halted in different countries.206,215,216,217,218 Consequently, seawater temperature clearly sets the start and the end of the epizootics in Europe. In Australia, the window of POMS permissiveness is higher, between 18°C and 26°C, even if the upper limit has never been established as clearly as in Europe.215,216 Finally, in laboratory conditions, viral infections and mortality of oysters occur up to 30°C, which suggests that laboratory conditions differ from those encountered in the natural environment.207,210

Ocean warming primarily manifests through species poleward migration. On average, marine species have shifted approximately 30–60 km per decade since 1950.219 In Europe, the Pacific oyster, originally introduced south of the river Loire in France, now extends its range to the southern regions of Norway, a putative consequence of global warming or translocation of living organisms.220 In theory, the lower temperature limit is anticipated to be reached earlier in the year, thereby expanding the time window of POMS permissiveness. Conversely, in even more southerly regions of Europe, the upper temperature limit should be surpassed earlier and for more extended periods throughout the year, resulting in a contraction of the time window for POMS permissiveness. Hence, although POMS may advance northward, there is a potential for its gradual decline in southern regions attributed to excessively high temperatures during certain parts of the year. Marine heatwaves, which consist of prolonged periods of abnormally warm water at a particular location,221 can also influence the expression of POMS. For example, mortality risk is associated with the rate of temperature increase in the weeks before reaching 16°C.222 Given that marine heatwaves are also associated with rapid increases in temperature, they could increase POMS-related mortality risk as reported in other marine diseases;223 however, this assumption needs further examination.

Ocean warming and marine heatwaves may increase POMS-related mortality risk through increased growth metabolism. In ectothermic organisms like oysters, increased temperature accelerates growth within the thermal tolerance window of the species. When these organisms are exposed to obligate intracellular parasites that depend on the cellular machinery of the host to replicate and proliferate, like viruses, it is likely that increased temperature promotes viral proliferation. This is clearly what happens with OsHV-1μVar.207,210,214 Ocean warming and marine heatwaves may also disturb or modulate oyster physiology when the temperature is reaching the upper limit of thermotolerance. C. gigas can withstand a wide seawater temperature range. This process was characterized at the transcriptome level with an increase in immune defense genes expression and a drop of metabolomic activities after acclimatization at high temperature.210 Catabolism, cell growth, and metabolites transport are impaired at 29°C when compared to 21°C. A non-optimal metabolomic environment for virus proliferation, combined with a higher antiviral response to the OsHV-1 μVar infection, leads to a decrease to POMS susceptibility (Duperret et al. unpublished). Furthermore, an overexpression of antiviral functions combined with DNA repair ability in animals acclimated at high temperature offering a better protection against virus exposure (Duperret et al. unpublished). Alternatively, ocean warming, and marine heatwaves, may increase POMS-related mortality risk through dysbiosis. For instance, increased temperature may influence the abundance or the virulence of opportunistic bacterial pathogens responsible for the secondary infection occurring during the disease.160

pH and ocean acidification

There is scant evidence of the impact of ocean acidification on the susceptibility of oysters to POMS. Indeed, the only study published to date suggests that short-term exposure to low pH increases the susceptibility of oysters to OsHV-1, and this coincides with lower activity of superoxide dismutase and basal activity of nitric oxide synthase—two enzymes that are involved in the host immune response.224 This study leads to the conclusion that acute acidification of seawater is likely to induce modulation of immune response in oysters infected by OsHV-1μVar. However, longer-term experiments failed to reproduce this result (F. Pernet personal communication). Further developments should consider long-term acclimation and multi-generational effects and examine other combined factors such as temperature to fully explore the impacts of ocean acidification POMS-related mortality risk.

Food availability and energetics

Bivalves are filter-feeders which directly rely upon phytoplankton for growth and reproduction. However, phytoplankton community composition and primary production is likely to decline under the effect of climate warming which favors ocean stratification and drought episodes.225 These two phenomena limit nutrient supplies to phytoplankton in both the open ocean and the coastal zone.226 The availability of phytoplanktonic food, directly influencing the energetic status of organisms, is one of the most influential factors on susceptibility to POMS214 and on the biological responses of organisms to global climate change.227,228,229

Unrestricted food supply improves the physiological condition of oysters and lowers their susceptibility to disease, probably reflecting an allocation trade-off between energy available to mount immune response and energy for other fitness-related functions.214,229 Food scarcity slows the growth and metabolism of the host on which the pathogen depends to proliferate, thus limiting viral proliferation, shedding and host mortality. Reduced primary productivity may mitigate POMS-related mortality risk by reducing host growth metabolism and impeding the ability of the virus to proliferate. However, if energy reserves are severely impaired, this protective effect can be overwhelmed, rendering the organism unable to mount an effective defense against the disease. Therefore, the indirect effect of climate change on primary production on POMS-related mortality risks remains unpredictable and will depend on the intensity of the induced stress. Beyond the quantity of food, the quality of food must also be considered. However, the effect of diet quality on susceptibility to POMS is unknown.

Salinity

Coastal areas where oyster farming is practiced are becoming more saline, reflecting decreasing freshwater inputs, and increasing sea-surface temperature fostering evaporation.230 The potential impact of hyper-salinity on POMS-related risk of mortality is not fully understood. There is no relationship between the salinity gradient and OsHV-1μVar-associated oyster mortality risk in the field, regardless of the spatial scale of investigation and salinity ranges.223,231,232 Nonetheless, findings from a laboratory experiment where oysters were acclimated to a range of salinities and subsequently exposed to OsHV-1μVar, reveal that the survival rate of oysters facing OsHV-1μVar at 35‰ is approximately 20% greater than those at 25‰.233

Developmental plasticity and rapid adaptation to POMS in a global change context

Recent work demonstrates that genetic and epigenetic mechanisms contribute significantly to oyster’s resistance to POMS.234,235 While epigenetics contribute alone to developmental even transgenerational plasticity,234 genetic and epigenetic lead to rapid adaptation.235 These phenomena will continue but global change brings new stressors leading to the needs of multidirectional adaptation for which it is difficult to predict the outcome. Interestingly, several works performed on various models showed that exposure to one stressor can promote an enhanced response toward other stressors.236 This mechanism of cross-tolerance is still misunderstood but may rely on molecular pathways sharing key actors enabling the upregulation of several pathways in response to a single stressor.236 These processes would be pre-adaptive in the global change context but this needs to be further studied in the context of oyster/POMS/global change interaction.

Conclusions

The fate of POMS in the face of climate change remains uncertain for three reasons. Firstly, certain climate change factors affecting POMS, such as deoxygenation, have not been examined, and others like ocean acidification and salinity lack comprehensive studies for robust conclusions. Secondly, existing research has predominantly analyzed individual factors in isolation, despite their simultaneous occurrence and potential interactions impacting POMS. Lastly, assessments of climate change factors on POMS have predominantly focused on short-term effects, emphasizing acclimation, without addressing the potential for long-term adaptation. Consequently, it is imperative to embark on a future research path that integrates multiple drivers and adopts a long-term perspective under ecologically realistic conditions.

Case study #5: Epizootic shell disease in the American lobster

The American lobster (Homarus americanus) is afflicted by an environmental disease known as epizootic shell disease (ESD). It is caused by bacterial dysbiosis (i.e., an altered bacterial community) on the cuticle that results in severe chitinoclastic damage to the shell of afflicted animals (Figure 4A). The disease is strongly correlated with increasing temperature from climate change and is exacerbated by environmental contaminants known as alkylphenols.76,237 A recurring suite of bacteria is associated with the disease. This includes Aquimarina macrocephali var. homari and several other bacterial taxa (Jannaschia, Hirschia, Pseudalteromonas, and Thalassobius) that are present at higher prevalence and relative abundance levels on diseased lobsters.238,239 These bacteria are chitinoclastic, but they appear to require a portal of entry through the cuticle to effect disease.240 Our current understanding of the etiology is that increased temperatures due to climate change negatively affect host defensive responses, with widespread contaminants (alkylphenols, such as bis-phenol A) interfering with tyrosine-crosslinking (i.e., sclerotisation), thereby lengthening the hardening process after moulting by as much as three times longer than normal.241,242Figure 4 American lobsters (Homarus americanus) with epizootic shell disease

(A) Lobster from Rhode Island with a light infection manifesting as pinprick like lesions on the dorsal carapace.

(B) Lobster from Rhode Island, USA with a heavy infection manifesting as coalesced lesions covering >30% of the carapace and limbs.

(C) Histological section through the dorsal carapace of a lobster from the Gulf of Maine showing a large “pseudomembrane” (unlabelled arrows) and intensive cellular infiltration (∗) by hemocytes below the affected cuticle (C).

With the longer shell hardening time, the weakened cuticle becomes highly susceptible to colonization by chitinoclastic bacteria which then grow into the exocuticle to form a dysbiotic community. Longer hardening times also make lobsters more susceptible to injury, thereby increasing the likelihood of creating a portal of entry for invading bacteria. Ultimately, the dysbiosis can survive at 4°C, thrive at 12°C, and proliferates rapidly at temperatures ≥18°C.243 Lobsters die at moult presumably from the adherence of pseudomembranes that form on to epidermis prior to ecdysis (Figure 4C). The pseudomembranes form in areas of damage to the shell, where the resulting lesions can form over more than 30% of the cuticle (Figures 4A and 4B).

ESD has seriously impacted the commercial lobster landings in the southern New England fishery, the third largest lobster fishery for the American lobster, after the Gulf of Maine and Canadian fisheries. The southern New England fishery has not recovered from the influence of this disease. The disease imposes substantial mortality risk to egg-bearing females, which experience a 12× to 16× higher risk of mortality than unaffected lobsters.244 Female lobsters do not moult annually and, therefore, cannot moult out of the disease before it progresses to an advanced state. This results in a sharp, sustained decline in females, their egg production, and recruitment over time.73,237,245,246

ESD has been found at low levels in the Gulf of Maine where sea temperatures are much lower than in the Southern New England fishery. Nonetheless, it has been steadily increasing over the last two decades and is now found at modest levels, <10%, in legal-sized females in the region.247 Its prevalence in “oversize” females (>126 mm carapace length), however, has been reported at 10–20% and these females may moult less frequently than legal (89–126 mm carapace length) females. The strong association between rising temperature and ESD has promoted surveillance of the disease in the Gulf of Maine. Temperature projections indicate that bottom temperatures ≥12°C are already present in many shallow reaches in the Gulf, particularly in the “Down East” region closest to the Bay of Fundy, and these areas should be targeted for additional surveillance over time.248

Case study #6: Gill health in Atlantic salmon in a warming world

Fish gills are an organ of only one cell layer, consisting of epithelial and mucus producing cells that separates the external environment from the internal bloodstream. They have many critical functions, including respiration, osmoregulation, excretion of nitrogenous waste, pH regulation, hormone production, and protection of internal fish organs against the environment.249 In parallel to their physiological functions, the gill is recognized as an important immune organ because of its role as a major mucosal barrier. Gill mucus is rich in antibodies, antimicrobial peptides, and signaling molecules that can regulate local immune responses. The interactions between salmon physiology, immunology, the environment, and infectious and non-infectious agents are complex and often not restricted to a single organ such as the gills. Gills are in many cases the primary location of negative effects from the environment due to their small barrier between the fish and the surrounding ocean.

This case study discusses effects of climate change on Atlantic salmon gills. These are the main fish species produced in many countries including the U.K, Norway, and Chile. Atlantic salmon in their sea water stage are mainly cultured in open-net pens and are thus constantly exposed to the ocean and everything in it, therefore we focus on the saltwater production stage because this is most relevant for climate and environmental change.

Gill disease and salmon management

Compromised gill health, or gill disease, occurs when infectious or non-infectious agents result in a detectable change affecting the functionality of the gill (Figure 5). Many inefficiencies in gill functions start with insults to the gills that then lead to colonization of infectious agents, reduced functionality in gills, and in many cases follow-up effects in other organs of the fish. Gill disease in Atlantic salmon can be caused by, or are associated with, many different infectious agents such as the amoeba Neoparamoeba perurans, other types of parasitic gill diseases including Desmozoon lepeophtherii, bacterial pathogens including Candidatus Branchiomonas cisticola and Tenacibaculum spp., and viruses including salmon gill pox virus.250,251,252 Non-infectious gill diseases are caused by cnidarian nematocysts in zooplankton and jellyfish, gill disease by harmful algae, and chemical/toxin-associated gill disease.253 The primary interaction with fish is often an insult by a spikey (i.e., irritative/abrasive) agent, which is sometimes followed up by the release of toxins, e.g., by certain plankton species, and secondary infections. Often principal pathological changes are non-specific, often multifactorial and a primary cause is not known. Then, it is referred to as “complex gill disease”.250 Gill disease affects salmon in fresh and saltwater stages, for example Salmon Gill Pox Virus can lead to high mortalities in both of these stages.254Figure 5 Gross gill appearance—an example of gill disease in Atlantic salmon, Salmo salar

The wide variety of causes for gill disease (if known) and clinical signs makes it challenging to standardize the relation between clinical signs, diagnostic test results, and gill health into a single case definition for gill disease that can be quantified. Surveillance for gill disease is most commonly through generic diagnostic tests such as gill scores from gross gill observations (Figure 5), normally assessed on the farm site, histopathology, and molecular tests when specific pathogens are suspected, or where information on underlying molecular mechanisms for gill inflammation is required.255

Climate change and salmon gill health

Perhaps the most important consequences of climate change to most salmon producing countries are warmer summers and less cold winters. Warmer summers in which problems arise, and less cold winters in which diseases are not cleared and instead become chronic. Two well-described temporal studies of gill pathogens and gill health have followed fish through a production cycle in commercial Scottish sites256 and in Norway.257 In both cases, increases in gill disease and pathology were found to peak in late summer, autumn, and early winter, which then cleared by spring. When season was removed from the analysis a significant relationship was found with water temperature.256 The impacts of warmer winter temperatures experienced in salmon production areas has meant the fish have been unable to clear their gill parasites and this results in increase gill pathology and hence higher mortalities.

Increased temperatures can affect salmon directly. For example, extreme summer temperatures have been associated with mass mortalities of salmon as was observed off the coast of Newfoundland during 2019 where some sites had 100% mortality.258 These authors examined salmon physiology and behavior in sea cages during natural warm water events demonstrating increased heart rate with increased water temperature, which reflects increase metabolic activity at warmer water temperature. Any inefficiency in gill function would have a negative outcome under such stress. Warm water also holds less oxygen than cold water, at the same time as fish are cold blooded as water temperature increases, as does their metabolic rate and hence oxygen demand.

Changing environmental conditions can affect salmon gills indirectly through effects on infectious agents of salmon such as amoebic gill disease which grow better at higher temperatures and salinities.259,260 For instance, fish held at 15°C compared with 10°C showed increased severity of infections, and it has been suggested that the causative agent of amoebic gill disease, N. perurans, may be more able to attach to the gills and grow faster at the higher temperature.261

Non-infectious agents that can affect salmon gills are zooplankton and phytoplankton blooms, which are correlated with seawater temperatures.261,262 In temperate regions where Atlantic salmon are farmed warmer waters almost always are reflected by a concurrent increase in planktonic species, often seen as the spring bloom. This increase in productivity also has the potential of increasing the pathogen load. As fish gills become infected and the resulting pathology occurs due to inflammation, the capacity of fish to function physiologically is compromised. Harmful zooplankton and harmful phytoplankton blooms are most likely to be a problem in summer-autumn with higher water temperatures.263

Impact of gill disease now and in the future

Given the variety in causes it can be difficult to assess the impact of climate change on overall gill health of Atlantic salmon. Most information comes from public fish mortalities data given the label “due to gill disease”, and often these are combined with viral conditions such as cardiac myopathy syndrome. Such data have, however, shown dramatic increases in relation to mortality due to gill health.264,265,266 However, they are an underrepresentation of the effects of gill health, because physiological processes in the salmon body can be affected before the fish dies, resulting in reduced productivity, e.g., by poor growth. Little is known about the direct and indirect costs of gill disease and this is needed to better understand the extent of this disease and how this may change because of increased environmental temperature.

Mitigation and adaptation strategies against disease

Predicting the precise impact of climate change on the frequency and severity of disease episodes in aquaculture and fisheries is inherently complex due to various factors. On a positive note, aquaculture husbandry practices have continuously evolved, encompassing changes in system design, stocking densities, on-site biosecurity protocols, and in management and control strategies. Concurrently, advancements have been made in genetics, enhancing the ability of aquaculture species to resist or tolerate pathogen challenges. Progress has also been evident in diagnostics, pathogen detection and identification, nutrition, including the use of functional feeds and probiotics to bolster the immune status of cultured aquatic species, and the overall health management of the culture environment. This section provides a summary of some of these strategies used to promote health and/or to circumvent the adverse effects of climate change on both fish and shellfish diseases.

Improved biosecurity

Biosecurity measures aim to limit the contact between pathogen/parasite and host such that infection cannot occur. These are superior to control/treatment approaches including use of antimicrobials and anti-parasitic agents as they have less direct impact on the environment. For example, recirculating aquaculture systems (RAS) allow fish cultivation in-land in indoor facilities where the quality of the water in terms of partial sterility, temperature, salinity, and levels of nitrogenous waste products, can be controlled in isolation to inhospitable conditions (e.g., disease-causing agents) in other natural waters. Such systems, though, are expensive to construct, can have high-energy needs and produce greenhouse gas emissions.267 They do allow a higher stocking density than other flow through systems but despite this advantage they may be economically unworkable based on the price and market demand of the final product.

Improved treatment and control strategies for infectious diseases of fish and shellfish

The development of vaccines and the practical methods for delivery of these has been a success story for fish cultivation over the last few decades. However, despite these successes, some conditions have proven difficult to control. For example, early attempts to develop vaccines to control fish ectoparasites such as L. salmonis were disappointing in terms of their efficacy and so alternate strategies (e.g., chemical control) have been developed that may not be as benign as vaccines. Use of new approaches for vaccines including subunit peptides, DNA and RNA-based vaccines (next generation), and new adjuvants show future promise.268,269 Other emerging approaches to control diseases of both fish and shellfish include biofloc technology,270 phage delivery,271,272 and novel immune stimulants.273,274

Improved disease surveillance in the oceans

Groner et al.275 and Maynard et al.248 argue for an improved approach to disease surveillance in the marine environment utilizing advances in detection and reporting of diseases, management strategies, and developing models to predict outbreaks of disease. However, the practicalities of such improvements by governments and interested parties are unclear.

Genetic selection and breeding of resistant strains

Selective breeding of resistant populations of fish and shellfish to disease has been practiced for nearly a century with some success. Given the scale of available literature on both fish and shellfish in terms of selective breeding programmes, here, we simply point the reader to key reviews on fin-fish and shellfish selective breeding.276,275,277,278,279,280,281,282 Of particular note here is the finding that triploid oysters (widely used in oyster farming) display enhanced susceptibility to heatwaves in comparison to non-triploids.283

Relocation of aquaculture sites

Climate change may make it impossible to culture fish and shellfish in traditional locations especially if water temperatures regularly exceed the physiological buffering capacity of fish and shellfish that leave them vulnerable to infectious and non-infectious diseases. Examples of strategies to move production vary in complexity from simple movement of trestles containing developing Pacific oysters and salmon in cages into deeper water hence avoiding higher summer air temperatures when exposed by the tide through to closure of existing sites and their relocation. Finally, movement of C. virginica pre-harvesting from low to high salinities can reduce the risk of vibrio contamination causing food poisoning.284,285

Concluding remarks

It is 20 years since the publication of the first broad exploration of whether diseases are increasing in the oceans.286 Their analysis based on Web of Science citations concluded that while the occurrence of disease was increasing in some groups (e.g., corals, marine mammals, urchins, and molluscs) in some there was no apparent change (e.g., crustaceans) while in others, such as bony fish, levels were decreasing. A subsequent analysis in 2019 using available data from 1970 to 2001 and 2001 to 2015, also found increases in disease in corals and urchins and apparent decreases in similar conditions in bony fish and decapod crustaceans.33 This reduction in disease reporting in bony fish was attributed to population declines (i.e., overfishing) resulting in a lower chance of density dependent disease transmission between individuals of the same species. Our review shows that while these two “broad brush stroke” approaches to changes in disease occurrence in marine dwelling organisms suggest no increase in fish and shellfish in general, there are examples of increased occurrence and severity of diseases in fish and shellfish both in the wild and under cultivation. Episodes of sudden increases in both aerial and sea surface temperature can push animals close to, or beyond, their thermal tolerance resulting in physiological and immunological changes leaving them vulnerable to opportunistic pathogens (Figure 2).76,127 Sessile animals, such as mussels, oysters, and seaweeds, are at particular risk especially if they are in the intertidal region where temperature extremes can be rapid, severe, and prolonged in the summer months. Of course, the impact(s) of climate-driven cooling on marine disease dynamics remains largely unknown.

The projected increase in humankind population in the coming years will require all our ingenuity in an era of unstable climate if we are to feed ourselves and, at the same time, protect our ecosystems from pervasive, and perhaps irreversible, damage.287

Acknowledgments

A.F.R and C.J.C. acknowledge funding from BBSRC/NERC (BB/P017215/1 ) and the Ireland-Wales ERDF Interreg project, Bluefish. The POMS studies reported in Case study 4 were supported by the ANR projects DECIPHER (ANR-14-CE19-0023 ) and DECICOMP (ANR-19-CE20-0004 ), by Ifremer project GT-huitre, and by the Fond Européen pour les Affaires Maritimes et la Pêche (FEAMP, GESTINNOV project no. PFEA470020FA1000007 ). These studies are set within the framework of the "Laboratoires d'Excellences (LABEX)" TULIP (ANR-10-LABX-41 ). W.S. and G.S. acknowledge funding from the National Science, Research and Innovation Fund, 10.13039/501100017170 Thailand Science Research and Innovation (grant no. 4709364 ). K.S. and S.T. acknowledge funding from the 10.13039/501100004704 National Research Council of Thailand: High-Potential Research Team Grant Program (grant no. N42A650869 ). S.A.M.M. was funded by 10.13039/501100019915 Scottish Aquaculture Innovation Centre (SAIC grant SL 2017 Nutritional Aspects of Gill Disease in Atlantic Salmon and SAIC grant SL 2020 Spatial and temporal drivers of gill pathology in Atlantic salmon. Case study 6 was supported by the “Gill health in Scottish farmed salmon” project (SAIC grant SL_2017_07 ).

Author contributions

Initial conceptualization: A.F.R. and C.J.C.; collected and reviewed literature and writing original draft manuscript: All authors.; final editing: A.F.R. and C.J.C.; all authors have read and approved this article.

Declaration of interests

The authors declare no competing interests.
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