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Modeling Pathogen Dispersal in Marine Fish and Shellfish
Abstract
In marine ecosystems, oceanographic processes often govern host contacts with infectious agents. Consequently, many approaches developed to quantify pathogen dispersal in terrestrial ecosystems have limited use in the marine context. Recent applications in marine disease modeling demonstrate that physical oceanographic models coupled with biological models of infectious agents can characterize dispersal networks of pathogens in marine ecosystems. Biophysical modeling has been used over the past two decades to model larval dispersion but has only recently been utilized in marine epidemiology. In this review, we describe how biophysical models function and how they can be used to measure connectivity of infectious agents between sites, test hypotheses regarding pathogen dispersal, and quantify patterns of pathogen spread, focusing on fish and shellfish pathogens.
... 94,95 This toolkit from physical oceanography has been successfully applied to biologically relevant dispersal of, for example, passively and actively drifting propagules (larvae, eggs, and seeds) 49,96-100 or pathogens. 101,102 An advantage of the proposed method over, for example, genetic methods of assessing spatial connectivity between populations is the potential for high-throughput and fast application to several locations at a time. Further, simulations are non-invasive and can be applied without much a priori knowledge of a region if a hydrodynamic model is available (e.g., Copernicus Marine Service provides an open-access platform for various hydrodynamic models of the global ocean 103 ). ...
... One example is sea louse infection in salmon aquaculture farms, demonstrating that, with increasing distances between farms, cross-infection would be reduced. 77,78,102 The Scottish government even successfully adopted particle dispersal simulations for spatial management of salmon aquaculture to define ''farm management areas'' for which diseases have to be reported. 104 Although the importance of diseases has also been discussed earlier in the context of aquaculture CC, 39 particle dispersal simulations have only recently been used as a tool to inform CC decisions. ...
... The potential risk of effluent carried SARS-CoV-2 into the ocean has not aroused public concern, partly due to its vast dilution capability. Biophysical model simulating dispersion of virus in the marine environment after direct release can be a powerful tool providing with a reliable prediction of the spreading and path of the pathogens (Cantrell et al., 2020). In this study, we simulated the scope of SARS-COVID-2 from outfalls and estimated its potential threat in an inland sea, the Bohai Sea of China. ...
... While viruses are generally perceived the 'simplest' to model, dispersion processes can still be quite sophisticated; inclusion of transfer by asymptomatic host species or sediment adsorption (Cantrell et al., 2020). For convenience of calculations, we assumed that viruses are passively moved by simulated currents and followed for a predetermined length of time. ...
A novel coronavirus (SARS-CoV-2) has caused more than 150 million confirmed infections worldwide, while it is not clear whether it affects the coastal waters. This paper proposed a biophysical model based on 16 scenarios with different virus half-life parameters to assess potential viral contamination from 25 municipal sewage outfalls into the Bohai Sea. Viral concentration maps showing spatial and temporal changes are provided based on a biophysical model under multiple scenarios. Results demonstrate that adjacent sea areas can become exposed to SARS-CoV-2 via water-borne transport from outfalls, with a higher risk in winter, because SARS-CoV-2 can be highly stable at low temperature. As coastal waters are the ultimate sink for wastewater and the epidemic will last for long time, this work is of great importance to raise awareness, identify vulnerable areas for marine mammals, and avoid the risk of exposure of tourists at bathing beach.
... Most dispersal models of waterborne pathogens typically simulate one average or one worst case scenario of infection as a simplifying assumption without integrating the epidemic progression of the disease (Olivares et al. 2015;Foreman et al. 2015b;Cantrell et al. 2020b). Infection and viral shedding are dynamic processes, evolving over the course of an outbreak, with variable viral abundance released into the water, and dispersed in turn by ocean conditions. ...
Pathogen dispersal from infected aquaculture sites into the surrounding ocean poses risks of infection to wild and farmed species, but is difficult to predict. This study aimed to build a framework using an ocean circulation and a particle tracking model in conjunction with a dynamic infection model and a virus inactivation model to simulate the dispersal of the infectious salmon anemia virus (ISAV) from Atlantic salmon farms. Simulated particles were released from hypothetically infected farms and advected by modelled currents. Inactivation of viral cohorts by ambient ultraviolet radiation and natural microbial communities was simulated during advection. Simulations showed that ISAV concentration varied spatiotemporally with the progression of the outbreak, current speed and direction, tidal elevation amplitude, and environmental decay. Connec-tivity among aquaculture sites varied in relation to seaway distances, though simulations showed that connectivity can also be asymmetrical between farm sites. Sensitivity analyses showed that the dispersal of ISAV was moderately sensitive to uncertainty associated with the viral decay model, highlighting the importance of obtaining accurate estimates of inactivation rates of ISAV. This framework provides an approach to simulate waterborne viral transmission that considers the biology and epidemic features of significance for pathogens and the dynamic conditions of the ocean.
... However, these frameworks differ in their underlying principles and the contextual factors that they emphasize [e.g. (19)(20)(21)(22)(23)(24)]. In addition, most simulation models have been developed for terrestrial rather than aquatic animals, which can be problematic when they are directly used in aquaculture sites due to the big environmental differences. ...
The sustainable development of the aquaculture sector is at risk due to the significant challenges posed by many emerging infectious diseases. While disease prevention and control measures are becoming increasingly critical, there is a dearth of studies on the epidemiological aspects of disease transmission in aquatic ecosystems. This study aims to forecast the spread of a bacterial disease between fish farms in two regions, Romsdalsfjord in Norway and Gujwa in South Korea by applying a DTU-DADS-Aqua spatiotemporal hybrid simulation model. The simulation model assessed the pattern of disease transmission between fish farms under different degrees of transmission power based on the distance between farms (ScalingInf), host susceptibility (RelSusceptibility), the origin site of disease, and the capacity of culling fish. The distance between fish farms was found to have significant associations with disease transmission. In most simulation conditions, the disease transmission between different bay management areas (BMAs) was not evident in Romsdalsfjord. In the Guwja region, where there are relatively narrow distances between fish farms, the spread of infectious disease was greatly affected by ScalingInf. The impact of RelSusceptibility on disease transmission patterns is a critical factor to consider in simulation modeling. When RelSusceptibility ranges from 0.5–1, there is little impact on the likelihood of disease transmission. Conversely, lower ranges (0.2 and 0.05) of RelSusceptibility result in a significant decrease in the area affected by the spread of disease. Eradication measures could control the patterns of infectious disease transmission, but the effectiveness of the depopulation strategy can be dramatically changed depending on the geographical environment. In conclusion, through a comparative analysis of the disease transmission and management scenarios, this study demonstrates the potential use of existing simulation models in predicting the spread of infectious diseases under different epidemiological circumstances and quarantine actions.
... These efforts can leverage recent advances in forecasting human disease outbreaks [61]. New approaches to epidemiological modelling are making it increasingly possible to predict the emergence and trajectory of aquatic disease events, including under climate changefor example, physical oceanographic models coupled with biological models for fish and shellfish pathogens [62]. Databases of disease incidence v can be exploited to parameterise models that correlate likelihood of disease emergence against a range of climatic, anthropogenic, and stochastic factors [63][64][65]. ...
Resolving the cause of disease (= aetiology) in aquatic organisms is a challenging but essential goal, heightened by increasing disease prevalence in a changing climate and an interconnected world of anthropogenic pathogen spread. Emerging diseases play important roles in evolutionary ecology, wildlife conservation, the seafood industry, recreation, cultural practices, and human health. As we emerge from a global pandemic of zoonotic origin, we must focus on timely diagnosis to confirm aetiology and enable response to diseases in aquatic ecosystems. Those systems' resilience, and our own sustainable use of seafood, depend on it. Synchronising traditional and recent advances in microbiology that span ecological, veterinary, and medical fields will enable definitive assignment of risk factors and causal agents for better biosecurity management and healthier aquatic ecosystems.
... Disease-causing pathogens can also spread at a faster rate in aquatic environments compared to terrestrial environments (McCallum et al., 2003). In aquatic settings, water serves as the medium that carries the pathogens between hydrodynamically linked populations (Amundrud and Murray, 2009;Cantrell et al., 2020) with the spreading distance of viable pathogen by the passive dispersal through the water body reaching to 50 km or more (Kragesteen et al., 2018). Disease outbreaks can be critical in these tropical waters because they are highly vulnerable to climate change. ...
Nanotechnology is an area of science, engineering, and technology that deals with nanoscale dimensions and tolerances, specifically the manipulation of single atoms and molecules with diameters ranging from 1 to 100 nm. Carbon-based nanoparticles, ceramic nanoparticles, metal nanoparticles, semiconductor nanoparticles, polymeric nanoparticles, and lipid-based nanoparticles are some of the numerous types of nanoparticles that can be classified on the basis of their size, shape, physical, and chemical properties. Probiotics are live, nonpathogenic bacteria that are given to help maintain microbial balance, particularly in the gastrointestinal tract. These probiotics, which can be found in fermented foods and come in the form of capsules, pills, packets, or powders, are made up of lactic acid bacteria such as Lactobacillus and Bifidobacterium species, as well as Saccharomyces boulardii yeast. The applications of biosynthesis of nanoparticles from marine sources such as marine plants, marine animals, and marine microbes are discussed in this chapter. Probiotics can be found in a variety of forms, including dietary supplements, medicines, and medical foods. For more effective probiotic therapy for microbiota-related ailments, a greater understanding of the interplay between genetic, microbial, and environmental impacts within individuals is expected.
... The density of livestock is often linked to pathogen spread (Cantrell et al., 2020;Craft, 2015;Tildesley et al., 2019) and the density of poultry farms in southwest France was found to be associated the occurrence of outbreaks in the case of the French HPAI 2016-2017 epidemic . To test the role of poultry density in driving viral spread, we considered the densities of duck and chicken farms per département as predictors. ...
In 2016–17, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analysed the spatio‐temporal dynamics of the epidemic using a structured‐coalescent‐based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within‐département transmission intensity. We extended the phylodynamic analysis with a generalised linear model to assess the impact of multiple factors—including large‐scale preventive culling and live‐duck movement bans—on viral migration rates and Ne. We showed that the large‐scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within‐département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short‐distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterising the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast‐evolving livestock pathogens. This article is protected by copyright. All rights reserved
... On the other hand, as air is typically a much harsher medium for pathogens than water, the sea is expected to host a large number of pathogens (viruses, bacteria and parasites) for a relatively long time. The longer life span of pathogens in a water medium, together with the increased buoyancy arising from the different physical properties of seawater and air, coupled to the existence of marine currents that can transmit pathogens for long distances away, allows diseases to spread faster and reach further distances in marine environments compared to epidemics in terrestrial systems (Cantrell et al., 2020). As a result, the possible long-term transmission of parasites by currents in marine environments make them more prone to suffer from persistent zoonotics compared to terrestrial ecosystems, where for an epidemic outbreak to occur the presence of an initial infected host (or vector) is necessary within a susceptible population. ...
The state of the art of epidemic modelling in terrestrial ecosystems is the compartmental SIR model and its extensions from the now classical work of Kermack-Mackendrick. In contrast, epidemic modelling of marine ecosystems is a bit behind, and compartmental models have been introduced only recently. One of the reasons is that many epidemic processes in terrestrial ecosystems can be described through a contact process, while modelling marine epidemics is more subtle in many cases. Here we present a model describing disease outbreaks caused by parasites in bivalve populations. The SIRP model is a multicompartmental model with four compartments, three of which describe the different states of the host, susceptible (i.e. healthy), S, infected, I, and removed (dead), R, and one compartment for the parasite in the marine medium, P, written as a 4-dimensional dynamical system. Even if this is the simplest model one can write to describe this system, it is still too complicated for both direct analytical manipulation and direct comparison with experimental observations, as it depends on four parameters to be fitted. We show that it is possible to simplify the model, including a reduction to the standard SIR model if the parameters fulfil certain conditions. The model is validated with available data for the recent Mass Mortality Event of the noble pen shell Pinna nobilis, a disease caused by the parasite Haplosporidium pinnae, showing that the reduced SIR model is able to fit the data. So, we show that a model in which the species that suffers the epidemics (host) cannot move, and contagion occurs through parasites, can be reduced to the standard SIR model that represents epidemic transmission between mobile hosts. The fit indicates that the assumptions made to simplify the model are reasonable in practice, although it leads to an indeterminacy in three of the original parameters.
... Several other transmission modes are considered in the VDMP and may contribute to the viral spread (Wade, 2017); these include boat-movement networks, sharing of equipment and personnel between farms of the same company, and stocking practices (St-Hilaire et al., 2002). While hydrodynamic data have been used in other aquatic modelling studies in BC to inform connectivity between marine farm sites (Cantrell et al., 2018(Cantrell et al., , 2020Foreman et al., 2009Foreman et al., , 2015aForeman et al., , 2015b the models that produce these data have only been developed for the Kyuquot Sound, Broughton Archipelago, and Discovery Islands region (Foreman et al., 2015a). These represent around one-third of the MZs in BC, which limits the application extent of such models and data thereof in the region, as opposed to the use of seaway distance between farm sites, as presented in this study. ...
Infectious hematopoietic necrosis (IHN) virus is a rhabdovirus of significant concern to the salmon aquaculture industry in British Columbia (BC). IHN epidemic events in BC have historically resulted in high mortalities and economic losses among farmed salmon populations. A viral disease management plan (VDMP) was developed by salmon companies in BC in, 2010 and implemented during the 2012 IHN outbreak in BC with a positive outcome; however, to date the effectiveness of VDMP practices in managing IHN epidemics on a coast-wide scale has not been formally evaluated. Therefore, we developed a model to simulate the waterborne incursion and spread of IHN virus into salmon farms across the BC coast. The model was developed using the DTU-DADS-Aqua modelling framework and model processes were designed to reflect the epidemiology of IHN, along with farm management and disease mitigation protocols currently implemented in BC. The model was used to assess effectiveness of the VDMP compared with alternative mitigation approaches. Model results quantified the combined and individual effects of disease surveillance, detection efforts, depopulation measures, and vaccine efficacy in reducing IHN virus transmission. Model outputs indicated the need for use of multiple mitigation measures in combination for a highly effective reduction in spread. Furthermore, the use of an IHN vaccine with high population coverage and efficacy, and the implementation of surveillance zones and pre-emptive depopulation of all net-pens in IHN-infected farms are crucial to contain IHN epidemics. A comparison between simulated model scenarios showed that current VDMP practices were effective in both limiting the spread and mitigating IHN epidemics across the BC coast. The model can be used to inform policy decisions in aquaculture and siting of marine farms, and provides insights to limit the magnitude of IHN epidemics in farmed salmon populations.
... 5 Some terrestrial pathogens, mainly viruses, seem to spread rapidly. 6 Lagomorphs host several fast-spreading terrestrial pathogens, such as the rabbit haemorrhagic disease virus (RHDV) or the myxoma virus. 4 The outbreaks of the myxoma virus in the 1950s and the RHDV in the 1980s-1990s caused severe rabbit population declines altering the equilibrium of the Iberian Mediterranean ecosystem. ...
Background:
Fast-spreading diseases affecting wildlife populations threaten biodiversity. Two caliciviruses, Lagovirus europaeus/GI.1 and Lagovirus europaeus/GI.2, caused rabbit haemorrhagic disease virus (RHDV) in wild rabbits. Despite having different characteristics, these variants spread quickly, posing a threat to wild rabbit populations.
Methods:
In this study, we conducted a thorough review of the scientific literature and reports of international organisations of first detections of both variants of RHDV in the Euro-Mediterranean region. We concentrated on this area to avoid bias due to intentional human introductions.
Results:
The estimated mean spread rate of GI.2 was higher than that of GI.1 (GI.2: 479 km/year, range: 47-7346; GI.1: 330 km/year, 37-6248). These differences were not statistically significant. This lack of difference may be due to the interactions between each variant's virulence characteristics. Humans may have a dominant effect on their spread. Potential limitations associated with the observational process could have hindered our ability to identify statistical differences.
Conclusions:
The lack of difference in the spread patterns of the two variants could be due to a biological cause, human facilitation or a lack of statistical power. Adapting protocols to detect diseases in wildlife using homogeneous criteria will be indispensable in the coming years.
... On the other hand, as air is typically a much harsher medium for pathogens than water, the sea is expected to host a large number of pathogens (viruses, bacteria and parasites) for a relatively long time. The longer life span of pathogens in a water medium, together with the increased buoyancy arising from the different physical properties of seawater and air, coupled to the existence of marine currents that can transmit pathogens for long distances away, allows diseases to spread faster and reach further distances in marine environments compared to epidemics in terrestrial systems (Cantrell et al., 2020). As a result, the possible long-term transmission of parasites by currents in marine environments make them more prone to suffer from persistent zoonotics compared to terrestrial ecosystems, where for an epidemic outbreak to occur the presence of an initial infected host (or vector) is necessary within a susceptible population. ...
The state of the art of epidemic modelling in terrestrial ecosystems is the compartmental SIR model and its extensions from the now classical work of Kermack–Mackendrick. In contrast, epidemic modelling of marine ecosystems is a bit behind, and compartmental models have been introduced only recently. One of the reasons is that many epidemic processes in terrestrial ecosystems can be described through a contact process, while modelling marine epidemics is more subtle in many cases. Here we present a model describing disease outbreaks caused by parasites in bivalve populations. The SIRP model is a multicompartmental model with four compartments, three of which describe the different states of the host, susceptible (i.e. healthy), S, infected, I, and removed (dead), R, and one compartment for the parasite in the marine medium, P, written as a 4-dimensional dynamical system. Even if this is the simplest model one can write to describe this system, it is still too complicated for both direct analytical manipulation and direct comparison with experimental observations, as it depends on four parameters to be fitted. We show that it is possible to simplify the model, including a reduction to the standard SIR model if the parameters fulfil certain conditions. The model is validated with available data for the recent Mass Mortality Event of the noble pen shell Pinna nobilis, a disease caused by the parasite Haplosporidium pinnae, showing that the reduced SIR model is able to fit the data. So, we show that a model in which the species that suffers the epidemics (host) cannot move, and contagion occurs through parasites, can be reduced to the standard SIR model that represents epidemic transmission between mobile hosts. The fit indicates that the assumptions made to simplify the model are reasonable in practice, although it leads to an indeterminacy in three of the original parameters. This opens the possibility of performing direct experiments to be able to solve this question.
... However, there may be discrepancies between abundances of sea lice measured at sites and from sentinel cages (Salama et al., 2018). Alternatively, investigating the genetic parentage of individual sea lice could improve the knowledge of lice dispersion locally (Cantrell et al., 2020). ...
The objective of this study was to estimate the impact of infestation pressures on the abundance of the parasitic sea louse, Lepeophtheirus salmonis, in the Bay of Fundy, New Brunswick (NB), Canada, using the Fish‐iTrends database for the years 2009–2018. Infestation pressures were calculated as time‐lagged weighted averages of the abundance of adult female (AF) sea lice within a site (internal infestation pressure: IIP) and among sites (external infestation pressure: EIP). The EIP weights were calculated from seaway distances among sites and a Gaussian kernel density for bandwidths of 5 to 60 km. The EIP with a bandwidth of 10 km had the best fit, as determined with Akaike's information criterion, and historical AF sea lice abundance. This estimated dispersal distance of 10 km was similar to previous studies in Norway, Scotland and in New Brunswick. The infestation pressures estimated from empirical AF sea lice abundance within and among sites significantly increased the abundance of AF sea lice (p < .001). This study concludes that sea lice burdens within Atlantic salmon farms in the Bay of Fundy, NB, are affected by within site management and could be improved by synchronizing treatments between sites.
... As in other environments, the impact that the T6SS has upon these fierce inter-bacterial competitions is substantial and likely relevant to human disease. Many Vibrio species are pathogenic to shellfish or coral (Sussman et al. 2008;Cantrell et al. 2020), and they can have a major impact on human health through contamination of seafoods (Elbashir et al. 2018). It has been shown that several Vibrios utilize their T6SS to dominate local microbiotas and displace some of its members. ...
Bacteria inhabit all known ecological niches and establish interactions with organisms from all kingdoms of life. These interactions are mediated by a wide variety of mechanisms and very often involve the secretion of diverse molecules from the bacterial cells. The Type VI secretion system (T6SS) is a bacterial protein secretion system that uses a bacteriophage-like machinery to secrete a diverse array of effectors, usually translocating them directly into neighbouring cells. These effectors display toxic activity in the recipient cell, making the T6SS an effective weapon during inter-bacterial competition and interactions with eukaryotic cells. Over the last two decades, microbiology research has experienced a shift towards using systems-based approaches to study the interactions between diverse organisms and their communities in an ecological context. Here, we focus on this aspect of the T6SS. We consider how our perspective of the T6SS has developed and examine what is currently known about the impact that bacteria deploying the T6SS can have in diverse environments, including niches associated with plants, insects and mammals. We consider how T6SS-mediated interactions can affect host organisms by shaping their microbiota, as well as the diverse interactions that can be established between different microorganisms through the deployment of this versatile secretion system.
... Thus, lice larvae can potentially drift several tens of kilometres away from the source Johnsen et al., 2014;Samsing et al., 2015), and therefore contribute to an elevated infection pressure over a large geographic area. Hydrodynamic models are a widely used tool for simulating dispersion of planktonic matter (Stucchi et al., 2011;Adams et al., 2016;Salama et al., 2018;Cantrell et al., 2020b;Rabe et al., 2020;Toorians and Adams, 2020). Combined with individual-based models (IBMs) where known behaviour and development parameters have been implemented, it is possible to quantify the number of salmon lice and their infectivity with high resolution in both space and time (Sandvik et al., , 2020cMyksvoll et al., 2018;Johnsen et al., 2020a). ...
Climate change can hamper sustainable growth in the aquaculture industry by amplifying and adding to other environmental challenges. In Norway, salmon lice-induced mortality in wild salmonid populations is identified as a major risk factor for further expansion. Higher temperatures will induce increased production of salmon lice larvae, decreased developmental time from non-infective nauplii to infectious copepods, and higher infectivity of copepodids. In a warmer climate, a modelling exercise shows how these three factors lead to a significant increase in the infection pressure from farmed to wild salmonids, where the infectivity of copepodids is the term with the highest sensitivity to temperature changes. The total infection pressure gradually increases with increasing temperature, with an estimated twofold if the temperature increases from 9°C to 11°C. Thus, making it even harder to achieve a sustainable expansion of the industry with rising water temperature. This study demonstrates how bio-hydrodynamic models might be used to assess the combined effects of future warmer climate and infection pressure from salmon lice on wild salmonids. The results can be used as an early warning for the fish-farmers, conservation stakeholders and the management authorities, and serve as a tool to test mitigation strategies before implementation of new management plans.
... Aquaculture management strategies implemented to combat water-born pathogens (Groner et al., 2016;Kragesteen et al., 2018;Nekouei et al., 2018;Gallardo-Escárate et al., 2019) can often be informative and transferred between countries. In particular, model-based management tools, similar to the one described in this article, can easily be exchanged among countries running bio-hydrodynamic model (Adams et al., 2016;Cantrell et al., 2020;Toorians and Adams 2020;Rabe et al., 2020), and further be used to test mitigation strategies before management plans are implemented. ...
Aquaculture is providing an increasingly larger proportion of the world’s protein for human consumption; however, its environmental impact is a bottleneck for sustainable expansion. In Norway, the government has enacted a framework where salmon lice-induced mortality in wild salmonid populations is used for assessing the environmental sustainability in production zones. Direct measurements of the level of lice-induced mortality on wild salmonids are difficult to acquire, thus comprehensive sustainability assessments are based on a set of evidence-based proxies. One such proxy is the infestation pressure from a bio-hydrodynamic model, from which we develop an index that summarize the sustainability of aquaculture in terms of lice infestation. This index is based on the proportion of areas with elevated lice loads, and is a novel approach used to investigate how sustainability could be achieved through scenario testing of different management strategies. The analyses identified a mismatch between legal and sustainable lice levels, but also a beneficial effect of reducing lice levels on farms. This study’s approach demonstrated how bio-hydrodynamic models might be used to assess sustainability and to predict the necessary reduction of lice larvae from farms to classify the entire Norwegian aquaculture industry as environmentally sustainable.
... For example, terrestrial runoff may decrease recovery rates of infected individuals by introducing pollutants and affecting osmoregulation, thus suppressing immune responses to parasites [73]. For aquatic species, this phenomenon has been studied with particular interest in fisheries and aquaculture, with models aiming to detect host density thresholds that could result in disease outbreaks [53,74,75]. We used population distance from closest watershed as a proxy for this possibility in our model. ...
Parasites are an integral part of coral reef ecosystems due to their influences on population dynamics, biodiversity, community structure, and food web connectivity. The Phylum Apicomplexa contains ubiquitous animal associates including the causative agents of globally important human diseases such as malaria and cryptosporidiosis. Despite their ubiquity, little is known about the biology, ecology, or distribution of these microorganisms in natural animal populations. In the US Virgin Islands, the dusky damselfish (Stegastes adustus) had a high but variable incidence of a Haemohormidium-like blood apicomplexan among 30 sites sampled. Microscopic analyses of blood smears allowed us to group these fish as infected, having low intensity infections, or uninfected. Regression analyses detected no significant differences in the condition indices (expressed as length–mass ratio). However, infection was clearly associated with potentially extremely high leukocyte counts among infected S. adustus that were not seen in uninfected fish. These results suggested the potential for some impact on the host. Linear mixed effects models indicated that S. adustus population density and meridional flow velocity were the main predictors of apicomplexan prevalence, with presence of other Stegastes species, population distance from watershed, zonal flow velocity, the complexity of the surrounding habitat, and season not showing any significant relationship with fish infection.
... Additionally, as climate change leads to warming oceans, the geographic ranges may change for both hosts and infectious agents. Biophysical models will be key for identifying susceptible host populations, predicting disease transmission pathways across larger areas, exploring the impacts of future climatic scenarios on transmission processes, and developing intervention strategies (Cantrell et al. 2020b). ...
Sea lice are one of the most economically costly and ecologically concerning problems facing the salmon farming industry. Here, we validated a coupled biological and physical model that simulated sea lice larvae dispersal from salmon farms in the Broughton Archipelago (BA), British Columbia, Canada. We employed a concept from ecological agent-based modeling known as ‘pattern matching’, which identifies similar emergent properties in both the simulated and observed data to confirm that the simulation contained sufficient complexity to recreate the emergent properties of the system. One emergent property from the biophysical simulations was the existence of sub-networks of farms. These were also identified in the observed sea lice count data in this study using a space-time scan statistic (SaTScan) to identify significant spatio-temporal clusters of farms. Despite finding support for our simulation in the observed data, which consisted of over a decade’s worth of monthly sea lice abundance counts from salmon farms in the BA, the validation was not entirely straightforward. The complexities associated with validating this biophysical dispersal simulation highlight the need to further develop validation techniques for agent-based models in general, and biophysical simulations in particular, which often result in patchiness in their dispersal fields. The methods utilised in this validation could be adopted as a template for other epidemiological dispersal models, particularly those related to aquaculture, which typically have robust disease monitoring data collection plans in place.
... Taking into account that knowledge of water currents and the dispersion of lice is important to assess their regional distribution, several coupled dispersion modelling systems have been developed (e.g. Murray and Gillibrand, 2006;Foreman et al., 2012;Asplin et al., 2014;Johnsen et al., 2014;Adams et al., 2016;Samsing et al., 2017;Krangesteen et al., 2018;Myksvoll et al., 2018;Asplin et al., 2020;Cantrell et al., 2020;Rabe et al., 2020). These models have previously assumed that sea lice nauplii and copepodites are passive particles, but they are becoming increasingly sophisticated with the particles possessing more realistic biological behaviours (e.g. ...
... A key difference between the terrestrial and marine ecosystem that facilitates the existence of these novel life forms, is that transmission is enabled in the latter because cancerous cells are released in the environment and are dispersed by oceanic currents. [22] This mode of transmission allows for infection over relatively long distances (as observed and modelled for other marine pathogens [45,46] ) and the cancer cells are known to be able to survive typical estuarine conditions for at least two days with a relatively low mortality. [47] It is also possible that the dispersal of infected individuals, for example mussels, colonising drifting debris [48] allows for the dispersal of transmissible cancers in distant bivalve populations (but also more recently by boats as suggested by Yonemitsu et al. [7] ). ...
Transmissible cancers are elusive and understudied parasitic life forms caused by malignant clonal cells (nine lineages are known so far). They emerge by completing sequential steps that include breaking cell cooperation, evade anti-cancer defences and shedding cells to infect new hosts. Transmissible cancers impair host fitness, and their importance as selective force is likely largely underestimated. It is, therefore, crucial to determine how common they might be in the wild. Here, we draw a parallel between the steps required for a transmissible cancer to emerge and the steps required for an intelligent civilisation to emerge in the Milky Way using a modified Drake equation. Using numerical analyses, we estimate the potential number of extant marine and bivalve species in which transmissible cancers might exist. Our results suggest that transmissible cancers are more common than expected, and that new lineages can be found by screening a large number of species.
The potential risk posed by infectious agents (IAs) associated with netpen aquaculture to wild fishes is determined based on the “release” of IAs from netpens into the environment, the “exposure” of the wild fish to those released agents, and the “consequence” for wild fish experiencing infection by those agents. Information available to characterize these three factors is often lacking, and the occurrence of transmission from aquaculture to wild fish as well as potential consequences of such transmission are difficult to observe. In this study, we utilized environmental DNA (eDNA) to characterize the release of dozens of IAs from, and exposure of Pacific salmon to, Atlantic salmon aquaculture. We combined these factors with the consequence of infection, as determined by the literature, to identify IAs that may pose a risk to wild salmon exposed to aquaculture in British Columbia, Canada. Over an 18-month period, eDNA samples were collected from seven active and four inactive netpen aquaculture sites in the Broughton Archipelago, BC. A meta-analytical mean across 22 IAs showed that the odds of IA detection at active sites was 4.3 (95% confidence interval = 2.3:8.1) times higher than at inactive sites, with 11 IAs in particular demonstrating a pattern consistent with elevated release. Oncorhynchus tshawytscha was the only Pacific salmon species presenting eDNA detections more likely to occur around and within active netpens relative to inactive sites. After considering the evidence of negative consequences of infection (from previous literature) in tandem with release model results, we determined that Tenacibaculum maritimum, Tenacibaculum finnmarkense, Ichthyobodo spp., and Piscine orthoreovirus are potential risks to Pacific salmon exposed to marine netpen aquaculture. These IAs, and others demonstrating patterns consistent with release but with insufficient prior research to evaluate the consequences of infection, require further studies that identify the factors influencing the intensity of release, the spatial extent of release around netpens, and the prevalence of infection in wild fish within known distances from netpens.
Marine parasites are strongly linked to marine diseases; they negatively impact fish farming by reducing production and hindering sustainable industry development. However, there is less research on infectious diseases in marine environments compared to terrestrial systems. In this paper, we investigate the mathematical modeling and dynamics of marine diseases caused by parasites, incorporating memory effects. We propose a fractional-order Susceptible-Infectious-Parasite (SIP) model featuring a non-linear general incidence rate. The computation of the basic reproduction number is provided, along with discussions on positivity, boundedness, and the existence and uniqueness of solution. We also explore the local stability of equilibrium states and conduct a sensitivity analysis of parameters to identify those most significant in the model. Our findings show that when the basic reproduction number is less than 1, the disease-free equilibrium is locally asymptotically stable, and when it exceeds 1, the endemic equilibrium point is asymptotically stable. Key parameters influencing disease transmission by marine parasites include the rates of parasite production by infected hosts, and transmission from susceptible to infectious individuals. Numerical simulations validate theoretical results, demonstrating that incorporating memory effects provides more realistic disease dynamics, influencing the time required to reach stable states. We find that the number of marine parasites peaks in correlation with the formula of the incidence rate.
Sustainability of aquaculture, an important component of the blue economy, relies in part on ensuring assessment of environmental impact and interactions relating to sea lice dispersing from open pen salmon and trout farms. We review research underpinning the key stages in the sea lice infection process to support modelling of lice on wild salmon in relation to those on farms. The review is split into five stages: larval production; larval transport and survival; exposure and infestation of new hosts; development and survival of the attached stages; and impact on host populations. This modular structure allows the existing published data to be reviewed and assessed to identify data gaps in modelling sea lice impacts in a systematic way. Model parameterisation and parameter variation is discussed for each stage, providing an overview of knowledge strength and gaps. We conclude that a combination of literature review, empirical data collection and modelling studies are required on an iterative basis to ensure best practice is applied for sustainable aquaculture. The knowledge gained can then be optimised and applied at regional scales, with the most suitable modelling frameworks applied for the system, given regional limitations.
Fresh fish remain the dominant forms and preservation technologies have enabled them to access ever more distant markets. In this study, we used metabarcoding of the 16S rRNA gene to generate gill microbiomes from Scomber scombrus bought at fishmonger’s stores as fresh products but whose labels showed they had been harvested in the Atlantic or Mediterranean FAO fishing areas. The microbial data were analysed with the aim of evaluating their ability to maintain signals from their different geographical origins and the presence of taxa which can potentially act as spoilers, foodborne pathogens, or histamine producers. Results revealed that microbiota, at the end of the wild fish supply chain, had differences related to the two FAO fishing areas (Atlantic vs Mediterranean).
Despite the presence of microbial genera potentially associated with spoilage, histamine-production or foodborne pathogens, their patterns confirmed that low-temperature storage is a traditional but effective method of preservation. However, the ongoing spoilage processes were more evident in fresh non-local specimens, dominated by psychrophilic Gram-negative bacteria, whereas fresh local specimens contained Planctomycetes taxa. Therefore, despite the current limitations mainly related to time and cost of the method, our study highlighted that microbiome-based applications are an emergent tool for food system transformation.
Recent Advances in Aquaculture Microbial Technology
2023, Pages 65-102
Chapter 5 - Microbes and fish diseases
Author links open overlay panelChou-MinChong1Jiun-YanLoh2
https://doi.org/10.1016/B978-0-323-90261-8.00009-2
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Abstract
The relationship between microorganisms and fish can be either mutualistic or pathogenic. In the majority of cases, fish diseases caused by pathogenic bacteria are among the most prevalent epidemics in the aquaculture industry. These bacterial infections are often associated with primary and secondary infections, caused postinfectivity by parasites or fungus. Bacterial diseases can cause significant production losses and economic devastation to an industry. Therefore, an in-depth understanding of their interrelationship and stress-related environmental factors is crucial for effective disease prevention and control. This book chapter depicts the importance of microbes, bacteria-related diseases in various water bodies, as well as the potential contribution of microbes to the aquaculture industry. Alternative disease prevention and control strategies such as immunostimulants, vaccines, RNA, and phage therapies, antimicrobial peptides (AMPs), phytotherapeutical compounds, as well as pre-, pro-, and postbiotics have been discussed to address fish disease issues. With the rapid development of technology, products, and techniques, the identification of the causative agents and the development of new therapies are no longer strenuous tasks. Despite these advancements, farm or facility biosecurity followed by good aquaculture practices are still considered effective prevention options than the cure.
Aims
This study examined and characterized the extract for metabolites of Halobacillus marinus HMALI004 to understand their antibacterial activities against opportunistic marine pathogens, that is, Vibrio parahaemolyticus and Vibrio cholerae.
Methods and Results
The bacterial strain HMALI004 was characterized as H. marinus, and an antibacterial spectral test revealed its inhibition against two opportunistic marine pathogens (V. parahaemolyticus and V. cholera). Fermentation broth of strain HMALI004 was subjected to column chromatography and high-performance liquid chromatography to separate antibacterial substances. Two compounds were successfully isolated and identified as 1H-pyrrole-2-carboxylic acid and 4-chloro-1H-pyrrole-2-carboxylic acid by mass spectrometry (MS) and nuclear magnetic resonance. The minimal inhibition concentration (MIC) values of 1H-pyrrole-2-carboxylic acid and 4-chloro-1H-pyrrole-2-carboxylic acid for V. parahaemolyticus were 25 μg/ml, while their MIC values for V. cholerae were 50 and 100 μg/ml, respectively. The reactive oxygen species (ROS) production of two pathogen strains treated with 1H-pyrrole-2-carboxylic acid and 4-chloro-1H-pyrrole-2-carboxylic acid were detected to investigate the antimicrobial mechanism. The results suggested that 4-chloro-1H-pyrrole-2-carboxylic acid exerted enhanced ROS production in V. parahaemolyticus, whereas 1H-pyrrole-2-carboxylic acid had a weaker effect. Both compounds caused a significant rise in ROS production in V. cholerae, causing severe damage to the cell wall and cytoplasm, leading to cell death.
Conclusions
The bacterium H. marinus HMALI004 was isolated from a shrimp pond and was found to produce antimicrobial compounds, which could inhibit the growth of opportunistic marine pathogens V. parahaemolyticus and V. cholerae by increasing ROS.
Significance and Impact of the Study
Successfully isolated antibacterial-producing strain, H. marinus HMALI004, and its antimicrobial compounds could be used as biological control agents for marine pathogens.
The incidence of emerging infectious diseases (EIDs) has increased in wildlife populations in recent years and is expected to continue to increase with global environmental change. Marine diseases are relatively understudied compared with terrestrial diseases but warrant parallel attention as they can disrupt ecosystems, cause economic loss, and threaten human livelihoods. Although there are many existing tools to combat the direct and indirect consequences of EIDs, these management strategies are often insufficient or ineffective in marine habitats compared with their terrestrial counterparts, often due to fundamental differences between marine and terrestrial systems. Here, we first illustrate how the marine environment and marine organism life histories present challenges and opportunities for wildlife disease management. We then assess the application of common disease management strategies to marine versus terrestrial systems to identify those that may be most effective for marine disease outbreak prevention, response, and recovery. Finally, we recommend multiple actions that will enable more successful management of marine wildlife disease emergencies in the future. These include prioritizing marine disease research and understanding its links to climate change, improving marine ecosystem health, forming better monitoring and response networks, developing marine veterinary medicine programs, and enacting policy that addresses marine and other wildlife diseases. Overall, we encourage a more proactive rather than reactive approach to marine wildlife disease management and emphasize that multidisciplinary collaborations are crucial to managing marine wildlife health.
Despite culturing the fastest-growing animal in animal husbandry, fish farmers are often
adversely economically affected by pathogenic disease outbreaks across the world. Although there are
available solutions such as the application of antibiotics to mitigate this phenomenon, the excessive
and injudicious use of antibiotics has brought with it major concerns to the community at large,
mainly due to the rapid development of resistant bacteria. At present, the use of natural compounds
such as phytocompounds that can be an alternative to antibiotics is being explored to address the issue
of antimicrobial resistance (AMR). These phytocompounds are bioactive agents that can be found in
many species of plants and hold much potential. In this review, we will discuss phytocompounds
extracted from plants that have been evidenced to contain antimicrobial, antifungal, antiviral and
antiparasitic activities. Further, it has also been found that compounds such as terpenes, phenolics,
saponins and alkaloids can be beneficial to the aquaculture industry when applied. This review will
focus mainly on compounds that have been identified between 2000 and 2021. It is hoped this review
will shed light on promising phytocompounds that can potentially and effectively mitigate AMR.
Rapid identification of marine pathogens is very important in marine ecology. Artificial intelligence combined with Raman spectroscopy is a promising choice for identifying marine pathogens due to its rapidity and efficiency. However, considering the cost of sample collection and the challenging nature of the experimental environment, only limited spectra are typically available to build a classification model, which hinders qualitative analysis. In this paper, we propose a novel method to classify marine pathogens by means of Raman spectroscopy combined with generative adversarial networks (GANs). Three marine strains, namely, Staphylococcus hominis, Vibrio alginolyticus, and Bacillus licheniformis, were cultured. Using Raman spectroscopy, we acquired 100 spectra of each strain, and we fitted them into GAN models for training. After 30,000 training iterations, the spectra generated by G were similar to the actual spectra, and D was used to test the accuracy of the spectra. Our results demonstrate that our method not only improves the accuracy of machine learning classification but also solves the problem of requiring a large amount of training data. Moreover, we have attempted to find potential identifying regions in the Raman spectra that can be used for reference in subsequent related work in this field. Therefore, this method has tremendous potential to be developed as a tool for pathogen identification.
Warming waters are changing marine pathogen dispersal patterns and infectivity worldwide. Coupled biological–physical modelling has been used in many systems to determine the connectivity of metapopulations via infectious disease particles. Here we model the connectivity of sea lice larvae (Lepeophtheirus salmonis) among salmon farms in the Broughton Archipelago, British Columbia, Canada, using a coupled biological–physical model. The physical model simulated pathogen dispersal, while the biological component influenced the survival and developmental rates of the sea lice. Model results predicted high temporal variability in connectivity strength among farms, an emergent effect from the interacting parts of the simulation (dispersion versus survival and development). Drivers of temporal variability were disentangled using generalized additive modeling, which revealed the variability was most strongly impacted by the spring freshet, which can act as a natural aid for sea lice control in the Broughton Archipelago. Our results suggest that farm management strategies can benefit by accounting for short-term spikes in regional pathogen connectivity among farms. Additionally, future scenarios of a warming climate with reduced snowpack can make sea lice control more challenging.
Larval dispersal is a critically important yet enigmatic process in marine ecology, evolution, and conservation. Determining the distance and direction that tiny larvae travel in the open ocean continues to be a challenge. Our current understanding of larval dispersal patterns at management-relevant scales is principally and separately informed by genetic parentage data and biological-oceanographic (biophysical) models. Parentage datasets provide clear evidence of individual larval dispersal events, but their findings are spatially and temporally limited. Biophysical models offer a more complete picture of dispersal patterns at regional scales but are of uncertain accuracy. Here, we develop statistical techniques that integrate these two important sources of information on larval dispersal. We then apply these methods to an extensive genetic parentage dataset to successfully validate a high-resolution biophysical model for the economically important reef fish species Plectropomus maculatus in the southern Great Barrier Reef. Our results demonstrate that biophysical models can provide accurate descriptions of larval dispersal at spatial and temporal scales that are relevant to management. They also show that genetic parentage datasets provide enough statistical power to exclude poor biophysical models. Biophysical models that included species-specific larval behaviour provided markedly better fits to the parentage data than assuming passive behaviour, but incorrect behavioural assumptions led to worse predictions than ignoring behaviour altogether. Our approach capitalises on the complementary strengths of genetic parentage datasets and high-resolution biophysical models to produce an accurate picture of larval dispersal patterns at regional scales. The results provide essential empirical support for the use of accurately parameterised biophysical larval dispersal models in marine spatial planning and management.
As a biodiverse region under a Mediterranean climate with a mix of highly developed and natural watersheds, coastal Santa Barbara County (SB), located in southern California, is susceptible to the hydrologic impacts of climate change. This study investigates the potential changes in hydro-meteorological variables in this region as well as their societal and ecological implications for projected climate conditions during the twenty-first century. Daily streamflow ensembles from 135 coastal watersheds for the period 2021–2100 are developed using the Hillslope River Routing (HRR) model forced with downscaled precipitation and temperature projections derived from 10 climate models in the Coupled Model Inter-Comparison Project, Phase 5, and two emission scenarios (Representative Concentration Pathways, RCP, 4.5 and 8.5). Analysis of the projected ensemble precipitation and streamflow series relative to historical conditions (1961–2000) shows (i) minimal change in annual precipitation (median change within ±3%); (ii) an altered seasonal rainfall distribution with a decrease in rainfall at the beginning of the rainy season (Oct–Dec), an increase during the Jan–Mar period, and a decrease at the end of the season (Apr–Jun); (iii) increases in the magnitude and frequency of large storms (> 36 mm/day) which combined with a shorter rainy season, lead to increases in annual peak flows; and (iv) the propagation of the altered precipitation characteristics resulting in nonlinear changes in the magnitude and variability of annual maximum discharges (i.e., mean, standard deviation, skew) impacting estimated return period discharges (e.g., estimated 100-year flood discharges for the period 2061–2100 under 8.5 increase by up to 185%). While these results are specific to southern coastal California, the nature of nonlinear hydrologic response to altered precipitation characteristics underscores the value of regional studies investigating potential impacts of climate projections on streamflow dynamics.
Connectivity in an aquatic setting is determined by a combination of hydrodynamic circulation and the biology of the organisms driving linkages. These complex processes can be simulated in coupled biological-physical models. The physical model refers to an underlying circulation model defined by spatially-explicit nodes, often incorporating a particle-tracking model. The particles can then be given biological parameters or behaviors (such as maturity and/or survivability rates, diel vertical migrations, avoidance, or seeking behaviors). The output of the bio-physical models can then be used to quantify connectivity among the nodes emitting and/or receiving the particles. Here we propose a method that makes use of kernel density estimation (KDE) on the output of a particle-tracking model, to quantify the infection or infestation pressure (IP) that each node causes on the surrounding area. Because IP is the product of both exposure time and the concentration of infectious agent particles, using KDE (which also combine elements of time and space), more accurately captures IP. This method is especially useful for those interested in infectious agent networks, a situation where IP is a superior measure of connectivity than the probability of particles from each node reaching other nodes. Here we illustrate the method by modeling the connectivity of salmon farms via sea lice larvae in the Broughton Archipelago, British Columbia, Canada. Analysis revealed evidence of two sub-networks of farms connected via a single farm, and evidence that the highest IP from a given emitting farm was often tens of kilometers or more away from that farm. We also classified farms as net emitters, receivers, or balanced, based on their structural role within the network. By better understanding how these salmon farms are connected to each other via their sea lice larvae, we can effectively focus management efforts to minimize the spread of sea lice between farms, advise on future site locations and coordinated treatment efforts, and minimize any impact of farms on juvenile wild salmon. The method has wide applicability for any system where capturing infectious agent networks can provide useful guidance for management or preventative planning decisions.
Temperature is hypothesized to alter disease dynamics, particularly when species are living at or near their thermal limits. When disease occurs in marine systems, this can go undetected, particularly if the disease is chronic and progresses slowly. As a result, population‐level impacts of diseases can be grossly underestimated. Complex migratory patterns, stochasticity in recruitment, and data and knowledge gaps can hinder collection and analysis of data on marine diseases. New tools enabling quantification of disease impacts in marine environments include coupled biogeochemical hydrodynamic models (to hindcast key environmental data), and multievent, multistate mark–recapture (MMSMR) (to quantify the effects of environmental conditions on disease processes and assess population‐level impacts). We used MMSMR to quantify disease processes and population impacts in an estuarine population of striped bass (Morone saxatilis) in Chesapeake Bay from 2005 to 2013. Our results supported the hypothesis that mycobacteriosis is chronic, progressive, and, frequently, lethal. Yearly disease incidence in fish age three and above was 89%, suggesting that this disease impacts nearly every adult striped bass. Mortality of diseased fish was high, particularly in severe cases, where it approached 80% in typical years. Severely diseased fish also had a 10‐fold higher catchability than healthy fish, which could bias estimates of disease prevalence. For both healthy and diseased fish, mortality increased with the modeled average summer sea surface temperature (SST) at the mouth of the Rappahannock River; in warmer summers (average SST ≥ 29°C), a cohort is predicted to experience >90% mortality in 1 year. Regression of disease signs in mildly and moderately diseased fish was <2%. These results suggest that these fish are living at their maximum thermal tolerance and that this is driving increased disease and mortality. Management of this fishery should account for the effects of temperature and disease on impacted populations.
Growth in salmon aquaculture over the past two decades has raised concerns regarding the potential impacts of the industry on neighboring ecosystems and wild fish productivity. Despite limited evidence, sea lice have been identified as a major cause for the decline in some wild Pacific salmon populations on the west coast of Canada. We used sea lice count and management data from farmed and wild salmon, collected over 10 years (2007–2016) in the Muchalat Inlet region of Canada, to evaluate the association between sea lice recorded on salmon farms with the infestation levels on wild out-migrating Chum salmon. Our analyses indicated a significant positive association between the sea lice abundance on farms and the likelihood that wild fish would be infested. However, increased abundance of lice on farms was not significantly associated with the levels of infestation observed on the wild salmon. Our results suggest that Atlantic salmon farms may be an important source for the introduction of sea lice to wild Pacific salmon populations, but that the absence of a dose response relationship indicates that any estimate of farm impact requires more careful evaluation of causal inference than is typically seen in the extant scientific literature.
Sea lice infestations are an increasing challenge in the ever-growing salmon aqua-
culture sector and cause large economic losses. The high salmon production in a small area cre-
ates a perfect habitat for parasites. Knowledge of how salmon lice planktonic larvae disperse and
spread infection between farms is of vital importance in developing treatment management plans
to combat salmon lice infestations. Using a particle-tracking model forced by tidal currents, we
show that Faroese aquaculture farms form a complex network. In some cases as many as 10% of
the infectious salmon lice released at one farm site enter a neighboring fjord containing another
farm site. Farms were characterized as emitters, receivers or isolated, and we could identify 2 clus-
ters of farms that were largely isolated from each other. These farm characteristics are a valuable
input for the development of management plans for the entire Faroese salmon industry.
Vibrio parahaemolyticus is the leading cause of seafood-related infections with illnesses undergoing a geographic expansion. In this process of expansion, the most fundamental change has been the transition from infections caused by local strains to the surge of pandemic clonal types. Pandemic clone sequence type 3 (ST3) was the only example of transcontinental spreading until 2012, when ST36 was detected outside the region where it is endemic in the U.S. Pacific Northwest causing infections along the U.S. northeast coast and Spain. Here, we used genome-wide analyses to reconstruct the evolutionary history of the V. parahaemolyticus ST36 clone over the course of its geographic expansion during the previous 25 years. The origin of this lineage was estimated to be in ~1985. By 1995, a new variant emerged in the region and quickly replaced the old clone, which has not been detected since 2000. The new Pacific Northwest (PNW) lineage was responsible for the first cases associated with this clone outside the Pacific Northwest region. After several introductions into the northeast coast, the new PNW clone differentiated into a highly dynamic group that continues to cause illness on the northeast coast of the United States. Surprisingly, the strains detected in Europe in 2012 diverged from this ancestral group around 2000 and have conserved genetic features present only in the old PNW lineage. Recombination was identified as the major driver of diversification, with some preliminary observations suggesting a trend toward a more specialized lifestyle, which may represent a critical element in the expansion of epidemics under scenarios of coastal warming.
ContextSea lice are the most significant parasitic problem affecting wild and farmed salmon. Larval lice released from infected fish in salmon farms and their transport by water masses results in inter-farm networks of lice dispersal. Understanding this parasite connectivity is key to its control and effective management. Objectives
Quantify the spatial and seasonal patterns in sea lice (Lepeophtheirus salmonis) dispersal in an area with intensive salmon farming. Identify emergent clusters in the network, where associated salmon farms could be used for coordinated management and spatial planning of the industry. Methods
We used a biophysical model to simulate lice dispersal from 537 salmon farms along the Norwegian coastline for two seasons (spring and winter) from 2009 to 2014. We used network analysis to characterize dispersal pathways and quantify the spatial and temporal patterns in connectivity. ResultsLice dispersal patterns and network metrics varied greatly between seasons, but differences were consistent amongst years. Winter networks presented more connections, and links were on average two times longer (average winter median = 36.5 ± 7.6 km, mean ± SE; average spring median = 17.8 ± 1.7 km). We identified 12 emergent farm clusters, which were similar across seasons and with the production areas for salmon aquaculture proposed by the Norwegian government. Conclusions
Seasonal variations in lice development times, oceanographic processes and the topological arrangement of salmon farms affect lice dispersal patterns. We have identified a biologically meaningful and politically tractable alliance structure for sea lice management consisting of closely-associated clusters of farms.
Sea turtles found stranded on beaches are often rehabilitated before being released back into the wild. The location and date of release is largely selected on an informal basis, which may not maximize the chance of survival. As oceanic conditions have a large influence on the movements of neonate sea turtles, this study aimed to identify the best locations and months to release rehabilitated sea turtles that would assist in their transport by ocean currents to the habitat and thermal conditions required for their survival. A particle tracking model, forced by ocean surface velocity fields, was used to simulate the dispersal pathways of millions of passively drifting particles released from different locations in Western Australia. The particles represented rehabilitated, neonate turtles requiring oceanic habitats [green (Chelonia mydas), hawksbill (Eretmochelys imbricata) and loggerheads (Caretta caretta)] and flatback turtles (Natator depressus) which require neritic habitats. The results clearly identified regions and months where ocean currents were more favorable for transport to suitable habitats. Tantabiddi, near Exmouth on the north-west coast, was consistently the best location for release for the oceanic species, with dominant offshore-directed currents and a very narrow continental shelf reducing the time taken for particles to be transported into deep water. In contrast, release locations with more enclosed geography, wide continental shelves, and/or proximity to cooler ocean temperatures were less successful. Our results produced a decision support system for the release of neonate marine turtles in Western Australia and our particle tracking approach has global transferability.
Transmission is a fundamental step in the life cycle of every parasite but it is also one of the most challenging processes to model and quantify. In most host?parasite models, the transmission process is encapsulated by a single parameter ?. Many different biological processes and interactions, acting on both hosts and infectious organisms, are subsumed in this single term. There are, however, at least two undesirable consequences of this high level of abstraction. First, nonlinearities and heterogeneities that can be critical to the dynamic behaviour of infections are poorly represented; second, estimating the transmission coefficient ? from field data is often very difficult. In this paper, we present a conceptual model, which breaks the transmission process into its component parts. This deconstruction enables us to identify circumstances that generate nonlinearities in transmission, with potential implications for emergent transmission behaviour at individual and population scales. Such behaviour cannot be explained by the traditional linear transmission frameworks. The deconstruction also provides a clearer link to the empirical estimation of key components of transmission and enables the construction of flexible models that produce a unified understanding of the spread of both micro- and macro-parasite infectious disease agents.
This article is part of the themed issue ?Opening the black box: re-examining the ecology and evolution of parasite transmission?.
Salmonid alphavirus subtype 3 (SAV3) causes pancreas disease (PD) and adversely affects salmonid aquaculture in Europe. A better understanding of disease transmission is currently needed in order to manage PD outbreaks. Here, we demonstrate the relationship between viral dose and the outcome of SAV3 infection in Atlantic salmon post-smolts using a bath challenge model. Fish were challenged at 12 °C with 3 different SAV3 doses; 139, 27 and 7 TCID50 L⁻¹ of seawater. A dose of as little as 7 TCID50 L⁻¹ of seawater was able to induce SAV3 infection in the challenged population with a substantial level of variation between replicate tanks and, therefore, likely represents a dose close to the minimum dose required to establish an infection in a population. These data also confirm the highly infectious nature of SAV through horizontal transmission. The outcome of SAV3 infection, evaluated by the prevalence of viraemic fish, SAV3-positive hearts, and the virus shedding rate, was positively correlated to the original SAV3 dose. A maximal shedding rate of 2.4 × 10⁴ TCID50 L⁻¹ of seawater h⁻¹ kg⁻¹ was recorded 10 days post-exposure (dpe) from the highest dose group. The method reported here, for the quantification of infectious SAV3 in seawater, could be useful to monitor PD status or obtain data from SAV3 outbreaks at field locations. This information could be incorporated into pathogen dispersal models to improve risk assessment and to better understand how SAV3 spreads between farms during outbreaks. This information may also provide new insights into the control and mitigation of PD.
Electronic supplementary material
The online version of this article (doi:10.1186/s13567-016-0385-2) contains supplementary material, which is available to authorized users.
Salmonid alphavirus subtype 3 (SAV3) causes pancreas disease (PD) and adversely affects salmonid aquaculture in Europe. A better understanding of disease transmission is currently needed in order to manage PD outbreaks. Here, we demonstrate the relationship between viral dose and the outcome of SAV3 infection in Atlantic salmon post-smolts using a bath challenge model. Fish were challenged at 12 °C with 3 different SAV3 doses; 139, 27 and 7 TCID50 L−1 of seawater. A dose of as little as 7 TCID50 L−1 of seawater was able to induce SAV3 infection in the challenged population with a substantial level of variation between replicate tanks and, therefore, likely represents a dose close to the minimum dose required to establish an infection in a population. These data also confirm the highly infectious nature of SAV through horizontal transmission. The outcome of SAV3 infection, evaluated by the prevalence of viraemic fish, SAV3-positive hearts, and the virus shedding rate, was positively correlated to the original SAV3 dose. A maximal shedding rate of 2.4 × 104 TCID50 L−1 of seawater h−1 kg−1 was recorded 10 days post-exposure (dpe) from the highest dose group. The method reported here, for the quantification of infectious SAV3 in seawater, could be useful to monitor PD status or obtain data from SAV3 outbreaks at field locations. This information could be incorporated into pathogen dispersal models to improve risk assessment and to better understand how SAV3 spreads between farms during outbreaks. This information may also provide new insights into the control and mitigation of PD.
Temperatures regulate metabolism of marine ectotherms and thereby influence development, reproduction, and, as a consequence, dispersal. Despite the importance of water temperatures in the epidemiology of marine diseases, for the parasitic copepod Lepeophtheirus salmonis, the effect of high and low temperatures has not been methodically investigated. Here, we examined the effects of a wide temperature range (3–20 °C) on L. salmonis larval development, adult body size, reproductive outputs, and infestation success. Further, we tested if dispersal of salmon lice differed with two temperature-dependent development times to the infective stage (30 and 60 degree-days) using an individual-based dispersal model. Development times followed universal models of temperature dependence described for other marine ectotherms. Water temperatures had a negative relationship with development times, adult body size, and reproductive outputs, except at 3 °C, where larvae failed to reach the infective stage and all parameters were decreased, indicating low temperatures are more detrimental than high temperatures. The predictable effect of temperatures on lice development and reproduction will have important applications, such as predicting dispersal and population connectivity, to assist in controlling lice epidemics.
Sea lice are common ectoparasites of farmed and wild salmonids and can cause substantial morbidity and mortality in their hosts. While sea lice infections are common in estuarine areas with variable salinity, the effects of salinity on population dynamics are poorly understood. We used existing literature to parameterize salinity-dependent logistic mortality curves for different life stages of sea lice. We then used population matrix models to characterize the effects of temperature and salinity on sea louse population growth. Our models showed that low salinity decreases survival, while low temperature retards sea louse development. In contrast with the linear effects of temperature on sea louse development, salinity has a nonlinear effect on sea louse survival; values below 20 psu cause mortality, while values above 20 psu have little effect on survival. Simulations showed that sea louse population growth can be greatest in zones that are intermediate between estuarine and oceanic. In these cases population growth is not limited by the low salinities found in more estuarine sites or the low temperatures found in more oceanic sites.
Fjordic coastlines provide sheltered locations for finfish and shellfish aquaculture, and are often subject to harmful algal blooms (HABs) some of which develop offshore and are then advected to impact nearshore aquaculture. Numerical models are a potentially important tool for providing early warning of such HAB events. However, the complex topography of fjordic shelf regions is a significant challenge to modelling. This is frequently compounded by complex bathymetry and local weather patterns. Existing structured grid models do not provide the resolution needed to represent these coastlines in their wider shelf context. In a number of locations advectively transported blooms of the ichthyotoxic dinoflagellate Karenia mikimotoi are of particular concern for the finfish industry. Here were present a novel hydrodynamic model of the coastal waters to the west of Scotland that is based on unstructured finite volume methodology, providing a sufficiently high resolution hydrodynamical structure to realistically simulate the transport of particles (such as K. mikimotoi cells) within nearshore waters where aquaculture sites are sited. Model–observation comparisons reveal close correspondence of tidal elevations for major semidiurnal and diurnal tidal constituents. The thermohaline structure of the model and its current fields are also in good agreement with a number of existing observational datasets. Simulations of the transport of Lagrangian drifting buoys, along with the incorporation of an individual-based biological model, based on a bloom of K. mikimotoi, demonstrate that unstructured grid models have considerable potential for HAB prediction in Scotland and in complex topographical regions elsewhere.
Background
Pancreas disease (PD), caused by salmonid alphavirus (SAV), is an important disease affecting salmonid aquaculture. It has been speculated that Atlantic salmon post-smolts are more prone to infections in the first few weeks following seawater- transfer. After this period of seawater acclimatization, the post-smolts are more robust and better able to resist infection by pathogens. Here we describe how we established a bath immersion (BI) model for SAV subtype 3 (SAV3) in seawater. We also report how this challenge model was used to study the susceptibility of post-smolts to SAV3 infection in two groups of post-smolts two weeks or nine weeks after seawater - transfer. Methods
Post-smolts, two weeks (Phase-A) or nine weeks (Phase-B) after seawater- transfer, were infected with SAV3 by BI or intramuscular injection (IM) to evaluate their susceptibility to infection. A RT-qPCR assay targeting the non-structural protein (nsP1) gene was performed to detect SAV3-RNA in blood, heart tissue and electropositive-filtered tank-water. Histopathological changes were examined by light microscope, and the presence of SAV3 antigen in pancreas tissue was confirmed using immuno-histochemistry. ResultsVirus shedding from the Phase-B fish injected with SAV3 (IM Phase-B) was markedly lower than that from IM Phase-A fish. A lower percentage of viraemia in Phase-B fish compared with Phase-A fish was also observed. Viral RNA in hearts from IM Phase-A fish was higher than in IM Phase-B fish at all sampling points (p < 0.05) and a similar trend was also seen in the BI groups. Necrosis of exocrine pancreatic cells was observed in all infected groups. Extensive histopathological changes were found in Phase-A fish whereas milder PD-related histopathological lesions were seen in Phase-B fish. The presence of SAV3 in pancreas tissue from all infected groups was also confirmed by immuno-histochemical staining. Conclusion
Our results suggest that post-smolts are more susceptible to SAV3 infection two weeks after seawater-transfer than nine weeks after transfer. In addition, the BI challenge model described here offers an alternative SAV3 infection model when better control of the time-of-infection is essential for studying basic immunological mechanisms and disease progression.
Infectious marine diseases can decimate populations and are increasing among some taxa due to global change and our increasing reliance on marine environments. Marine diseases become emergencies when significant ecological, economic or social impacts occur. We can prepare for and manage these emergencies through improved surveillance, and the development and iterative refinement of approaches to mitigate disease and its impacts. Improving surveillance requires fast, accurate diagnoses, forecasting disease risk and real-time monitoring of disease-promoting environmental conditions. Diversifying impact mitigation involves increasing host resilience to disease, reducing pathogen abundance and managing environmental factors that facilitate disease. Disease surveillance and mitigation can be adaptive if informed by research advances and catalysed by communication among observers, researchers and decision-makers using information-sharing platforms. Recent increases in the awareness of the threats posed by marine diseases may lead to policy frameworks that facilitate the responses and management that marine disease emergencies require.
The human-pathogenic marine bacteria Vibrio vulnificus and V. parahaemolyticus
are strongly correlated with water temperature, with concentrations
increasing as waters warm seasonally. Both of these bacteria can be concentrated
in filter-feeding shellfish, especially oysters. Because oysters are often
consumed raw, this exposes people to large doses of potentially harmful bacteria.
Various models are used to predict the abundance of these bacteria in
oysters, which guide shellfish harvest policy meant to reduce human health
risk. Vibrio abundance and behaviour varies from site to site, suggesting that
location-specific studies are needed to establish targeted risk reduction strategies.
Moreover, virulence potential, rather than simple abundance, should
be also be included in future modeling efforts.
Emerging diseases pose a recurrent threat to bivalve aquaculture. Recently, massive mortality events in the Pacific oyster Crassostrea gigas associated with the detection of a microvariant of the ostreid herpesvirus 1 (OsHV- 1mVar) have been reported in Europe, Australia and New Zealand. Although the spread of disease is often viewed as a governance failure, we suggest that the development of protective measures for bivalve farming is presently held back by the lack of key scientific knowledge. In this paper, we explore the case for an integrated approach to study the management of bivalve disease, using OsHV-1 as a case study. Reconsidering the key issues by incorporating multidisciplinary science could provide a holistic under- standing of OsHV-1 and increase the benefit of research to policymakers.
Since the mid-1980s, clinical inspections of aquaculture sites carried out on a regular basis by authorized veterinarians and fish health biologists (known as fish health services: FHS) have been an essential part of aquatic animal health surveillance in Norway. The aims of the present study were (1) to evaluate the performance of FHS routine clinical inspections for the detection of VHS and (2) to explore the effectiveness of risk-based prioritisation of FHS inspections for demonstrating freedom from VHS in marine salmonid sites in Norway. A stochastic simulation model was developed to estimate site sensitivity (SeS), population sensitivity (SeP), and probability of freedom (PFree). The estimation of SeS takes into consideration the probability that FHS submit samples if a site is infected, the probability that a sample is tested if submitted, the effective probability of infection in fish with clinical signs, laboratory test sensitivity, and the number of tested samples. SeP and PFree were estimated on a monthly basis over a 12 month period for six alternative surveillance scenarios and included the risk factors: region, species, area production density, and biosecurity level. Model results indicate that the current surveillance system, based on routine inspections by the FHS has a high capability for detecting VHS and that there is a high probability of freedom from VHS in Norwegian marine farmed salmonids (PFree >95%). Sensitivity analysis identified the probabilities that samples are submitted and submitted samples are tested, as the most influential input variables. The model provides a supporting tool for evaluation of potential changes in the surveillance strategy, and can be viewed as a platform for similar exotic viral infectious diseases in marine salmonid farming in Norway, if they share similar risk factors.
Teleost fish possess an adaptive immune system associated with each of their mucosal body surfaces. Evidence obtained from mucosal vaccination and mucosal infection studies reveal that adaptive immune responses take place at the different mucosal surfaces of teleost. The main mucosa-associated lymphoid tissues (MALT) of teleosts are the gut-associated lymphoid tissue (GALT), skin-associated lymphoid tissue (SALT), the gill-associated lymphoid tissue (GIALT) and the recently discovered nasopharynx-associated lymphoid tissue (NALT). Teleost MALT includes diffuse B cells and T cells with specific phenotypes different from their systemic counterparts that have co-evolved to defend the microbe-rich mucosal environment. Both B and T cells respond to mucosal infection or vaccination. Specific antibody responses can be measured in the gills, gut and skin mucosal secretions of teleost fish following mucosal infection or vaccination. Rainbow trout studies have shown that IgT antibodies and IgT(+) B cells are the predominant B cell subset in all MALT and respond in a compartmentalized manner to mucosal infection. Our current knowledge on adaptive immunity in teleosts is limited compared to the mammalian literature. New research tools and in vivo models are currently being developed in order to help reveal the great intricacy of teleost mucosal adaptive immunity and help improve mucosal vaccination protocols for use in aquaculture.
Finite volume ocean circulation and particle tracking models are used to simulate waterborne
transmission of infectious hematopoietic necrosis virus (IHNV) among Atlantic
salmon (Salmo salar) farms in the Discovery Islands region of British Columbia, Canada.
Historical simulations for April and July 2010 are carried out to demonstrate the seasonal
impact of river discharge, wind, ultra-violet (UV) radiation, and heat flux conditions on nearsurface
currents, viral dispersion and survival. Numerical particles released from infected
farm fish in accordance with IHNV shedding rates estimated through laboratory experiments
are dispersed by model oceanic flows. Viral particles are inactivated by ambient UV
radiation levels and by the natural microbial community at rates derived through laboratory
studies. Viral concentration maps showing temporal and spatial changes are produced and
combined with lab-determined minimum infectious dosages to estimate the infective connectivity
among farms. Results demonstrate that neighbouring naïve farms can become
exposed to IHNV via water-borne transport from an IHNV diseased farm, with a higher risk
in April than July, and that many events in the sequence of farm outbreaks in 2001-2002 are
consistent with higher risks in our farm connectivity matrix. Applications to other diseases,
transfers between farmed and wild fish, and the effect of vaccinations are also discussed.
Population connectivity, which is essential for the persistence of benthic marine metapopulations, depends on how life history traits and the environment interact to influence larval production, dispersal and survival. Although we have made significant advances in our understanding of the spatial and temporal dynamics of these individual processes, developing an approach that integrates the entire population connectivity process from reproduction, through dispersal, and to the recruitment of individuals has been difficult. We present a population connectivity modelling framework and diagnostic approach for quantifying the impact of i) life histories, ii) demographics, iii) larval dispersal, and iv) the physical seascape, on the structure of connectivity and metapopulation dynamics. We illustrate this approach using the subtidal rocky reef ecosystem of Port Phillip Bay, were we provide a broadly-applicable framework of population connectivity and quantitative methodology for evaluating the relative importance of individual factors in determining local and system outcomes.
The spatial characteristics of marine population connectivity are primarily influenced by larval mortality, the duration of the pelagic larval stage, and the settlement competency characteristics, with significant variability imposed by the geographic setting and the timing of larval release. The relative influence and the direction and strength of the main effects were strongly consistent among 10 connectivity-based metrics.
These important intrinsic factors (mortality, length of the pelagic larval stage, and the extent of the precompetency window) and the spatial and temporal variability represent key research priorities for advancing our understanding of the connectivity process and metapopulation outcomes.
Vibrio cholerae is a globally distributed water-borne pathogen that causes severe diarrheal disease and mortality, with current outbreaks as part of the seventh pandemic. Further understanding of the role of environmental factors in potential pathogen distribution and corresponding V. cholerae disease transmission over time and space is urgently needed to target surveillance of cholera and other climate and water-sensitive diseases. We used an ecological niche model (ENM) to identify environmental variables associated with V. cholerae presence in marine environments, to project a global model of V. cholerae distribution in ocean waters under current and future climate scenarios. We generated an ENM using published reports of V. cholerae in seawater and freely available remotely sensed imagery. Models indicated that factors associated with V. cholerae presence included chlorophyll-a, pH, and sea surface temperature (SST), with chlorophyll-a demonstrating the greatest explanatory power from variables selected for model calibration. We identified specific geographic areas for potential V. cholerae distribution. Coastal Bangladesh, where cholera is endemic, was found to be environmentally similar to coastal areas in Latin America. In a conservative climate change scenario, we observed a predicted increase in areas with environmental conditions suitable for V. cholerae. Findings highlight the potential for vulnerability maps to inform cholera surveillance, early warning systems, and disease prevention and control.
Dinoflagellate blooms are frequently observed under temporary eutrophication of coastal waters after heavy rains. Growth of these opportunistic microalgae is believed to be promoted by sudden input of nutrients and the absence or inefficiency of their natural enemies, such as grazers and parasites. Here, numerical simulations indicate that increasing nutrient availability not only promotes the formation of dinoflagellate blooms but can also stimulate their control by protozoan parasites. Moreover, high abundance of phytoplankton other than dinoflagellate hosts might have a significant dilution effect on the control of dinoflagellate blooms by parasites, either by resource competition with dinoflagellates (thus limiting the number of hosts available for infection) or by affecting numerical-functional responses of grazers that consume free-living parasite stages. These outcomes indicate that although both dinoflagellates and their protozoan parasites are directly affected by nutrient availability , the efficacy of the parasitic control of dinoflagellate blooms under temporary eutrophication depends strongly on the structure of the plankton community as a whole.
In studies of the population dynamics of parasitic sea lice and the implications of outbreaks for salmon farms, several types of mathematical models have been implemented. Delay differential equation models describe the temporal dynamics of average adult lice densities over many farm sites. In contrast, larval transport models consider the relative densities of lice at farm sites by modelling larval movements between them but do not account for temporal dynamics or feedbacks created by reproduction. Finally, several recent studies have investigated spatiotemporal variation in site lice abundances using statistical models and distance-based proxies for connectivity. We developed a model which integrates connectivity estimates from larval transport models into the delay differential equation framework. This allows representation of sea lice developmental stages, dispersal between sites, and the impact of management actions. Even with identical external infection rates, lice abundances differ dramatically between farms over a production cycle (dependent on oceanographic conditions and resulting between-farm connectivity). Once infected, lice dynamics are dominated by site reproduction and subsequent dispersal. Lice control decreases actual lice abundances and also reduces variation in abundance between sites (within each simulation) and between simulation runs. Control at sites with the highest magnitude of incoming connections, computed directly from connectivity modelling, had the greatest impact on lice abundances across all sites. Connectivity metrics may therefore be a reasonable approximation of the effectiveness of management practices at particular sites. However, the model also provides new opportunities for investigation and prediction of lice abundances in interconnected systems with spatially varying infection and management.
Context Parasite transmission between captive and wild fish is mediated by spatial, abiotic, biotic, and management factors. More effective population management and conservation strategies can result from multivariable assessments of factors associated with spatial dynamics of parasite spillover. Objective Our study characterised spatial patterns of sea lice (Lepeophtheirus salmonis, Caligus clemensi) infection on out-migrating chum (Oncorhynchus keta) and pink (O. gorbuscha) salmon in an area with Atlantic salmon (Salmo salar) farming. Methods A multivariable statistical model for sea louse parasitism of out-migrating chum and pink salmon was developed from 166,316 wild salmon sampled in the Broughton Archipelago, British Columbia, Canada from 2003 to 2012. We assessed for factors hypothesized to influence sea lice infection levels, at the non-motile life stage, including spatial scales of infection sources. Results Fish length, sampling year and method were strong explanatory factors. Infection was greatest in higher salinity water. Farmed and wild juvenile salmon infection levels were correlated, on average, within 30 km. Except for 2004, sea lice infection on farms were typically well below the regulatory level (3 motiles per fish). Average intensity of non-motile infections observed on the wild fish were 6.36 (SD = 9.98) in 2004 compared to 1.66 (SD = 1.25) for the other years. Conclusions Accuracy of future model estimates will benefit by including hydrodynamic data accounting for anisotropic spread of sea lice from sources. Multivariable statistical modelling over long time series data strengthens understanding of factors impacting wild juvenile salmon infection levels and informs spatial patterns of aquatic epidemiology.
Vibrio
parahaemolyticus is an important human pathogen whose transmission is associated with the consumption of contaminated seafood. Consistent multilocus sequence typing for V. parahaemolyticus has shown difficulties in the amplification of the recA gene by PCR associated with a lack of amplification or a larger PCR product than expected. In one strain (090–96, Peru, 1996), the produced PCR product was determined to be composed of two recA fragments derived from different Vibrio species. To better understand this phenomenon, we sequenced the whole genome of this strain. The hybrid recA gene was found to be the result of a fragmentation of the original lineage-specific recA gene resulting from a DNA insertion of approximately 30 kb in length. This insert had a G+C content of 38.8%, lower than that of the average G+C content of V. parahaemolyticus (45.2%), and contained 19 ORFs, including a complete recA gene. This new acquired recA gene deviated 24% in sequence from the original recA and was distantly related to recA genes from bacteria of the Vibrionaceae family. The reconstruction of the original recA gene (recA3) identified the precursor as belonging to ST189, a sequence type reported previously only in Asian countries. The identification of this singular genetic feature in strains from Asia reveals new evidence for genetic connectivity between V. parahaemolyticus populations at both sides of the Pacific Ocean that, in addition to the previously described pandemic clone, supports the existence of a recurrent transoceanic spreading of pathogenic V. parahaemolyticus with the corresponding potential risk of pandemic expansion.
The salmon louse Lepeophtheirus salmonis is a major parasite of salmon, and is able to travel between farms during its pelagic phases. We investigated the spatial dispersion of L. salmonis planktonic stages in the Hardangerfjord, Norway, using an individual-based model and a fjord circulation model. The models allowed us to investigate how assumptions about swimming responses to environmental cues affect vertical distribution, development and horizontal transport. The rules governing vertical distributions include passive particles remaining fixed at constant depths, but also prescribed responses of active particles to environmental cues such as ambient light level, salinity and temperature. Horizontal dispersion was affected by the vertical distribution scheme (rules) of the particles (each representing an individual planktonic-stage L. salmonis). When particles were held fixed in the surface layer, the horizontal dispersion and the area potentially affected by a source of lice decreased relative to the distribution that was predicted when lice had vertical migration behaviours. The simulations also showed that swimming triggered by both light and temperature may result in a diel migration pattern. If the particles sought out the warmest areas during juvenile stages, development to the infectious stage was reduced by up to 1 d. Better information is required on the actual response of lice to a set of vertical environmental factors to improve predictions of lice dispersal in fjords.
We report the development of a prototype tool for modeling the risks of
spreading of non-indigenous invasive species via ballast water. The tool constitutes of
two types of models: a 3D hydrodynamical model calculates the currents in the North
Sea and Danish Straits, and an agent-based model estimates the dispersal of selected
model organisms with the prevailing currents calculated by the 3D hydrodynamical
model. The analysis is concluded by a postprocessing activity, where scenarios of
dispersal are combined into an interim estimate of connectivity within the study area.
The latter can be used for assessment of potential risk associated with intentional or
unintentional discharges of ballast water. We discuss how this prototype tool can be
used for ballast water risk management and outline other functions and uses, e.g., in
regard to ecosystem-based management and the implementation of the EU Marine
Strategy Framework Directive.
Temperature is hypothesized to contribute to increased pathogenicity and virulence of many marine diseases. The sea louse (Lepeophtheirus salmonis) is an ectoparasite of salmonids that exhibits strong life-history plasticity in response to temperature; however, the effect of temperature on the epidemiology of this parasite has not been rigorously examined. We used matrix population modelling to examine the influence of temperature on demographic parameters of sea lice parasitizing farmed salmon. Demographically-stochastic population projection matrices were created using parameters from the existing literature on vital rates of sea lice at different fixed temperatures and yearly temperature profiles. In addition, we quantified the effectiveness of a single stage-specific control applied at different times during a year with seasonal temperature changes. We found that the epidemic potential of sea lice increased with temperature due to a decrease in generation time and an increase in the net reproductive rate. In addition, mate limitation constrained population growth more at low temperatures than at high temperatures. Our model predicts that control measures targeting preadults and chalimus are most effective regardless of the temperature. The predictions from this model suggest that temperature can dramatically change vital rates of sea lice and can increase population growth. The results of this study suggest that sea surface temperatures should be considered when choosing salmon farm sites and designing management plans to control sea louse infestations. More broadly, this study demonstrates the utility of matrix population modelling for epidemiological studies.
Since 2008, mass mortalities of 1-yr-old Crassostrea gigas associated with the ostreid herpesvirus OsHV-1 μVar have occurred along all the coasts of France when seawater temperature reaches 16 to 17°C. The present study aimed to characterize the effect of temperature on oyster survival in combination with OsHV-1 DNA quantification by standard real-time PCR and total vibrio population levels in oyster tissues. To examine the effect of seawater temperature on disease transmission and related mortality of oysters, cohabitation experiments were conducted between healthy naïve oysters and oysters previously exposed to field conditions in areas where mortalities were occurring. Oysters initially maintained in controlled conditions (free of mortality and negative for OsHV-1), and then transferred to an area where high mortalities were occurring among farmed stocks, became infected with OsHV-1 and exhibited high loads of vibrios followed by significant mortalities. When previously exposed oysters were maintained indoors at 13.0°C for 40 d and then at 20.6°C, they exhibited no mortality, were negative for OsHV-1 detection, and did not transmit the disease to healthy oysters. Survival of previously exposed oysters maintained indoors at 8 temperatures ranging from 13.4 to 29.0°C varied from 25 to 48% and was negatively correlated with holding temperature. Concomitantly, survival of naïve cohabiting animals (62 to 98%) decreased with increasing seawater temperature until a plateau was reached between 16.2 and 21.9°C, and increased at higher temperatures. Therefore, the optimal temperature range for disease transmission from field-exposed to naïve animals was between 16.2 and 21.9°C. Our results suggest that a long-term period (40 d) at low temperature (13°C) may offer a method of mitigating mortalities in oysters that have been exposed to an infective environment.
White spot syndrome virus (WSSV) is the pathogen behind white spot disease (WSD) in shrimp and many other crustaceans. It is a highly contagious virus capable of causing total mortality in 3-10 days of outbreak in normal culture conditions. Since the first report of occurrence in China and Taiwan between 1991 and 1992, WSD outbreak caused tremendous losses at farm level throughout the world. Most of the published reviews on WSSV emphasize advanced genetic studies and biosecurity measures in terms of disease management. Recently, some new technologies such as greenhouse, polyculture, biofloc and minimal water exchange have been proposed for WSD management, which is the trigger for this review. However, further research is needed on those new technologies enhancing their efficient application.
Marine ecosystems are beset by disease outbreaks, and efficient strategies to control dispersal of pathogens are scarce. We tested whether introducing no-farming areas or ‘firebreaks’ could disconnect dispersal networks of a parasitic disease affecting the world's largest marine fish farming industry (∼1000 farms). Larval salmon lice (Lepeophtheirus salmonis) are released from and transported among salmon farms by ocean currents, creating inter-farm networks of louse dispersal. We used a state-of-the-art biophysical model to predict louse movement along the Norwegian coastline and network analysis to identify firebreaks to dispersal. At least one firebreak that fragmented the network into two large unconnected groups of farms was identified for all seasons. During spring, when wild salmon migrate out into the ocean, and louse levels per fish at farms must be minimised, two effective firebreaks were created by removing 13 and 21 farms (1.3% and 2.2% of all farms in the system) at ∼61°N and 67°N, respectively. We have demonstrated that dispersal models coupled with network analysis can identify no-farming zones that fragment dispersal networks. Reduced dispersal pathways should lower infection pressure at farms, slow the evolution of resistance to parasite control measures, and alleviate infection pressure on wild salmon populations.
Sea lice are a constraint on the sustainable growth of Scottish marine salmonid aquaculture. As part of an integrated pest management approach, farms coordinate procedures within spatial units. We present observations of copepodids being at relatively greater density than nauplii in upper waters, which informs the development of surface layer sea lice transmission modelling of Loch Linnhe, Scotland, for informing farm parasite management. A hydrodynamic model is coupled with a biological particle-tracking model, with characteristics of plankton sea lice. Simulations are undertaken for May and October 2011–2013, forced by local wind data collected for those periods. Particles are continually released from positions representing farm locations, weighted by relative farm counts, over a 2-week period and tracked for a further 5 days. A comparison is made between modelled relative concentrations against physical and biological surveys to provide confidence in model outputs. Connectivity between farm locations is determined in order to propose potential coordination areas. Generally, connectivity depends on flow patterns in the loch and decreases with increased farm separation. The connectivity indices are used to estimate the origins of the sea lice population composition at each site, which may influence medicinal regimens to avoid loss of efficacy.
Background:
Salmon lice (Lepeophtheirus salmonis) are the most important parasite of farmed salmon. Infective larvae position themselves in the upper part of the water column to increase encounter probabilities with potential hosts. Previous studies have shown that a 'snorkel' sea-cage technology protects salmon from infection in surface waters. We tested whether deep snorkels would more effectively reduce lice infestation than shallow snorkels and still uphold adequate conditions for the fish. Five sea-cages (12 m × 12 m) each holding approximately 3000 Atlantic salmon (Salmo salar) (53 ± 10 g) were fitted with snorkels that gave protection from infection for 0, 4, 8, 12 or 16 m. We tested if reductions in the settlement of new salmon lice copepodids were consistent among 4 separate infection periods.
Results:
Lice infestation decreased exponentially with depth in all time periods. Infection levels in shallow snorkels (0 and 4 m) were consistently four to ten times higher than those in deep snorkels (12 and 16 m). Key welfare and production performance indices were similar across all snorkel depths.
Conclusion:
Deeper snorkels dramatically and consistently reduced infection levels of salmon lice compared to shallow snorkels without consequences for fish welfare and production performance. Therefore, reducing salmon sea lice encounters using a depth-based barrier is a powerful management tool for salmon farming.
The ability to infect a host is a key trait of a virus, and differences in infectivity could put one virus at an evolutionary advantage over another. In this study we have quantified the infectivity of two strains of infectious hematopoietic necrosis virus (IHNV) that are known to differ in fitness and virulence. By exposing juvenile rainbow trout (Oncorhynchus mykiss) hosts to a wide range of virus doses, we were able to calculate the infectious dose in terms of ID50 values for the two genotypes. Lethal dose experiments were also conducted to confirm the virulence difference between the two virus genotypes, using a range of virus doses and holding fish either in isolation or in batch so as to calculate LD50 values. We found that infectivity is positively correlated with virulence, with the more virulent genotype having higher infectivity. Additionally, infectivity increases more steeply over a short range of doses compared to virulence, which has a shallower increase. We also examined the data using models of virion interaction and found no evidence to suggest that virions have either an antagonistic or a synergistic effect on each other, supporting the independent action hypothesis in the process of IHNV infection of rainbow trout.
Markov chain analysis was recently proposed to assess the time scales and preferential pathways into biological or physical networks by computing residence time, first passage time, rates of transfer between nodes and number of passages in a node. We propose to adapt an algorithm already published for simple systems to physical systems described with a high resolution hydrodynamic model. The method is applied to bays and estuaries on the Eastern Coast of Canada for their interest in shellfish aquaculture. Current velocities have been computed by using a 2 dimensional grid of elements and circulation patterns were summarized by averaging Eulerian flows between adjacent elements. Flows and volumes allow computing probabilities of transition between elements and to assess the average time needed by virtual particles to move from one element to another, the rate of transfer between two elements, and the average residence time of each system. We also combined transfer rates and times to assess the main pathways of virtual particles released in farmed areas and the potential influence of farmed areas on other areas. We suggest that Markov chain is complementary to other sets of ecological indicators proposed to analyse the interactions between farmed areas - e.g., depletion index, carrying capacity assessment. Markov chain has several advantages with respect to the estimation of connectivity between pair of sites. It makes possible to estimate transfer rates and times at once in a very quick and efficient way, without the need to perform long term simulations of particle or tracer concentration.
White plague is one of the most devastating coral diseases in the Caribbean, and yet important aspects of its epidemiology, including how the disease transmits, remain unknown. This study tested potential mechanisms and rates of transmission of white plague in a laboratory setting. Transmission mechanisms including the transport of water, contact with macroalgae, and predation via corallivorous worms and snails were tested on the host species Orbicella annularis. Two of the tested mechanisms were shown to transmit disease: water transport and the corallivorous snail Coralliophila
abbreviata. Between these transmission mechanisms, transport of water between a diseased coral and a healthy coral resulted in disease incidence significantly more frequently in exposed healthy corals. Transmission via water transport also occurred more quickly and was associated with higher rates of tissue loss (up to 3.5 cm d−1) than with the corallivorous snail treatment. In addition, water that was in contact with diseased corals but was filtered with a 0.22-μm filter prior to being introduced to apparently healthy corals also resulted in the transmission of disease signs, but at a much lower rate than when water was not filtered. This study has provided important information on the transmission potential of Caribbean white plague disease and highlights the need for a greater understanding of how these processes operate in the natural environment.
Ballast water is one of the most important vectors for the transport of non-native species to new aquatic environments. Due to the development of new ballast water quality standards for viruses, this study aimed to determine the taxonomic diversity and composition of viral communities (viromes) in ballast and harbor waters using metagenomics approaches. Ballast waters from different sources within the North America Great Lakes and paired harbor waters were collected around the Port of Duluth-Superior. Bioinformatics analysis of over 550 million sequences showed that a majority of the viral sequences could not be assigned to any taxa associated with reference sequences, indicating the lack of knowledge on viruses in ballast and harbor waters. However, the assigned viruses were dominated by double-stranded DNA phages and sequences associated with potentially emerging viral pathogens of fish and shrimp were detected with low amino acid similarity in both ballast and harbor waters. Annotation-independent comparisons showed that viromes were distinct among the Great Lakes, and the Great Lakes viromes were closely related to viromes of other cold natural freshwater systems but distant from viromes of marine and human designed/managed freshwater systems. These results represent the most detailed characterization to date of viruses in ballast water, demonstrating their diversity and the potential significance of ship-mediated spread of viruses.
The combination of wide-ranging spatial and temporal scales associated with the oceanic environment, together with processes intrinsic to the biology of marine organisms, makes the quantitative study of population connectivity a formidable challenge. Sampling over all scales, except for targeted field efforts that focus on selected processes of life stages in limited domains,is presently not possible. As such, modeling approaches that simultaneously include key physical dynamics and biological traits provide a way forward to investigate general ecological questions as well as provide qualitative assessments regarding connectivity of specific regions and populations. In some instances, model results have provided information of relevance to deci- sion-makers in determining marine protected areas and other management strategies. At a minimum, models can be used to generate hypotheses for empirical studies. Overall, coupled biological-physical models are critical tools for addressing the complex processes driving population connectivity in marine systems.
In 1993 an unusual sabellid polychaete was brought to our attention. It grossly deformed the shells of cultured abalones in some of the California abalone mariculture facilities. This worm is not native to California and was subsequently found in rocky intertidal and subtidal habitats in southern Africa, where it had not previously been recognized. The worm is hermaphroditic and has benthic larvae that are competent to settle within 12 h and soon secrete a mucous sheath. Development of the tentacular crown occurs within a week and generation time can be short, about one month. The worm has a unique association with host gastropods. Unlike all other known shell-fouling organisms, the sabellid routinely settles inside the aperture at the growing edge of the shell. The host responds by secreting a layer of nacre over the mucous sheath to form a tube enclosing the worm, whose crown of tentacles extends through the opening of the tube to the outer surface of the shell. Heavy infestations cause the cessation of linear growth of the host as prismatic shell deposition cannot be resumed after repeated settlement of larvae. The sabellid is not very host specific; many other California native gastropods are readily infested. Bivalves do not appear to be susceptible. Efforts to find a native California predator of the adult worms were not successful. The sabellid has caused great economic damage to some facilities commercially culturing abalones. An established population of this worm has been detected in California, and further risk of establishment and spread of this worm is great. Its unique biology suggests that it may be a useful experimental probe for studies of molluscan shell deposition and may also serve to reveal how molluscs defend themselves against organisms attempting to settle in and foul their apertures.
The PaV1 virus infects spiny lobsters (Panulirus argus) throughout most of the Caribbean, where its prevalence in adult lobsters can reach 17% and where it poses a significant risk of mortality for juveniles. Recent studies indicate that vertical transmission of the virus is unlikely and PaV1 has not been identified in the phyllosoma larval stages. Yet, the pathogen appears subclinically in post-larvae collected near the coast, suggesting that lobster post-larvae may harbour the virus and perhaps have aided in the dispersal of the pathogen. Laboratory and field experiments also confirm the waterborne transmission of the virus to post-larval and early benthic juvenile stages, but its viability in the water column may be limited to a few days. Here, we coupled Lagrangian modelling with a flexible matrix model of waterborne and post-larval-based pathogen dispersal in the Caribbean to investigate how a large area with complex hydrology influences the theoretical spread of disease. Our results indicate that if the virus is waterborne and only viable for a few days, then it is unlikely to impact both the Eastern and Northwestern Caribbean, which are separated by dispersal barriers. However, if PaV1 can be transported between locations by infected post-larvae, then the entire Caribbean becomes linked by pathogen dispersal with higher viral prevalence in the North. We identify possible regions from which pathogens are most likely to spread, and highlight Caribbean locations that function as dispersal "gateways" that could facilitate the rapid spread of pathogens into otherwise isolated areas. © 2014 International Council for the Exploration of the Sea 2014. All rights reserved. For Permissions, please email: [email protected]
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Pancreas disease (PD) is a viral disease causing negative impacts on economy of salmon farms and fish welfare. Its transmission route is horizontal, and water transport by ocean currents is an important factor for transmission. In this study, the effect of temperature changes on PD dynamics in the field has been analysed for the first time. To identify the potential time of exposure to the virus causing PD, a hydrodynamic current model was used. A cohort of salmon was assumed to be infected the month it was exposed to virus from other infective cohorts by estimated water contact. The number of months from exposure to outbreak defined the incubation period, which was used in this investigation to explore the relationship between temperature changes and PD dynamics. The time of outbreak was identified by peak in mortality based on monthly records from active sites. Survival analysis demonstrated that cohorts exposed to virus at decreasing sea temperature had a significantly longer incubation period than cohorts infected when the sea temperature was increasing. Hydrodynamic models can provide information on the risk of being exposed to pathogens from neighbouring farms. With the knowledge of temperature-dependent outbreak probability, the farmers can emphasize prophylactic management, avoid stressful operations until the sea temperature is decreasing and consider removal of cohorts at risk, if possible.
The outbreak, persistence, and eradication of infectious diseases often depend on the density of hosts. In coastal seas, many fisheries are fully or over-exploited; meanwhile, farmed populations are increasing rapidly with aquaculture growth. Marine aquaculture facilities are typically open to the surrounding ecosystem and, therefore, wild and farmed populations are connected by their shared parasites. At the core of epidemiological theory are host density thresholds, above which diseases can persist or invade and below which diseases can be eradicated. Host density thresholds in aquaculture-fishery interactions likely function at regional scales that encompass multiple farms, which are connected by pathogen dispersal and the movement of wild hosts. Sudden outbreaks of parasitic copepods in wild-farmed salmon systems may be linked to aquaculture growth exceeding host density thresholds. Abiotic (e.g. temperature and salinity), management (e.g. husbandry and farm siting), and biotic factors (e.g. migrations of wild hosts) likely affect threshold values. A connected wild-farmed host population can exceed a host density threshold due to an influx of wild hosts via migration, increases in aquaculture production, or environmental change such as climate warming. Coastal management and policy should heed the disease implications of climate warming, aquaculture growth, and fisheries restoration that suggest increasing host densities and decreasing threshold values.