Over recent years the growth in aquaculture, accompanied by the emergence of new and transboundary diseases, has stimulated epidemiological studies of aquatic animal diseases. Great potential exists for both observational and theoretical approaches to investigate the processes driving emergence but, to date, compared to terrestrial systems, relatively few studies exist in aquatic animals.
Research using risk methods has assessed routes of introduction of aquatic animal pathogens to facilitate safe trade (e.g. import risk analyses) and support biosecurity. Epidemiological studies of risk factors for disease in aquaculture (most notably Atlantic salmon farming) have effectively supported control measures.
Methods developed for terrestrial livestock diseases (e.g. risk-based surveillance) could improve the capacity of aquatic animal surveillance systems to detect disease incursions and emergence. The study of disease in wild populations presents many challenges and the judicious use of theoretical models offers some solutions.
Developing Aquatic Epidemiology
It has been argued that fish health research has focused on isolating and characterising pathogens, at the expense of host and environmental factors.
Only relatively recently have epidemiological studies investigated causes of aquatic animal diseases under field conditions. Inevitably the development of epidemiological methodology has focused firstly human, and secondly terrestrial livestock health issues. As a consequence the development of aquatic epidemiology has lagged behind its terrestrial counterparts, however in recent years the field has developed rapidly. Epidemiological studies of aquatic animals systems are becoming more common place and the techniques used have increased in complexity.
The beginning of aquatic animal epidemiology mirrored the evolution of modern epidemiology in terrestrial livestock. The first risk factor study was published by Thorburn, who applied approaches previously used in terrestrial systems to investigate mortality due to vibriosis in farmed rainbow trout.
Intensive Atlantic salmon (the first large scale commercially produced fish) production was pioneered in Norway in the 1970s. Inevitably, disease problems emerged, most notably infectious salmon anaemia (ISA). ISA and other diseases stimulated epidemiological research to support cost-effective control strategies in farmed Atlantic salmon.
Subsequently, other important diseases have emerged in aquaculture, some with serious economic and environmental consequences. Gyrodacytlus salaris emerged in Norway in the early 1970s causing serious declines in many wild Atlantic salmon populations. Farmed Atlantic salmon may act as a reservoir for infection, thus contributing to populations declines in wild salmon.
A number of viral diseases, notably white spot syndrome virus (WSSV), have emerged in the nascent paenid shrimp farming sector, with devastating economic consequences in some countries. Cold water strawberry disease emerged in 2006 in the UK, causing financial losses to trout producers. Disease emergence has clearly provided an important spur to the application of epidemiology.
The growth of aquatic animal epidemiology is illustrated by an analysis of the number and type of studies presented at the International Society of Veterinary Epidemiology and Economics (ISVEE) conferences, held every three years since 1976 (Table 1). The number of aquatic abstracts and the species being studied have increased, the questions addressed and the techniques used have become more diverse (the location of the conference may influence the number of aquatic animal submissions).
Shellfish (molluscs and crustacea) production accounts for over a quarter of the aquatic animals consumed annually, but have been the subject of comparatively few studies (which are predominantly of cultured shrimp). This may be explained by the limited options for disease control.
Transboundary and emerging diseases
A key role for epidemiology is to identify and assess exotic and emerging disease threats. Transboundary diseases are a major threat to both farmed and wild terrestrial and aquatic animal populations.
In recent years, a number of aquatic animal diseases have emerged and spread rapidly across international political boundaries, causing serious financial and ecological impacts. WSSV emerged in shrimp (Paenus monodon) culture in China (Fuijan Province) in 1992 and subsequently spread to Taiwan and Japan and then became panzootic. The main route of transmission was the movement of live animals. G. salaris emerged in Norway in the early 1970s, and is hypothesised to have been introduced from Sweden with the introduction of a Baltic strain of Atlantic salmon.
A new variant of oyster herpes virus recently emerged in European oyster production and has spread rapidly through live animals movements. Koi herpesvirus achieved widespread distribution across the globe within a few years of emerging through movements of carp, mainly destined for the ornamental trade industry. The movements of bullfrogs (as pets, food and for laboratory use) has been implicated in the spread of the fungal disease, chytridiomycosis in wild amphibia.
Movements of animals drive disease emergence not only through extending the geographic range of known diseases but by moving species outside of their natural ranges, thus providing the opportunity for putative pathogens to find new hosts. The scale and diversity of aquatic animal movements, mainly for the ornamental trade but also for food and aquaculture, far outweighs international terrestrial movements, and presents important challenges to epidemiologists.
Import risk analysis (IRA)
IRA assesses the risk of disease spread through trade in animals or their products. In aquatic animal health they have been undertaken for a variety of reasons (reviewed by Peeler et al.,), but mainly to support animal health policy making with respect to trade and biosecurity. Epidemiological approaches are used within the import risk analysis framework.
Consistent, defensible and scientifically sound assessments of disease threats and disease freedom are required to fulfil the requirement of the Agreement on the Application of Sanitary and Phytosanitary (the SPS agreement) of the World Trade Organisation (WTO) (which was enacted to allow Members to adopt measures to protect human, animal or plant life or health, whilst preventing restrictions on international trade disguised as sanitary measures).
Thus this application of epidemiology, for both terrestrial and aquatic animal diseases, have developed in response to both requirements of international trade agreements and the real threat of transboundary diseases. One of first aquatic animal IRA was Biosecurity Australias assessment of the risk of disease introduction with the import of wild caught salmon carcasses from Canada.
IRA requires information on the epidemiology of the diseases in the exporting country, biophysical characteristics of the pathogen and product information to be integrated. As part of the consequence assessment epidemiological and economic modelling are needed to assess disease spread and impact on local industries and wild populations.
More broadly, an assessment of routes of introduction (through trade, movement of shipping, lorries etc.) is the necessary basis on which to review a countrys biosecurity measures. However, there are constraints to IRA, as currently practised. Frequently, relevant information is not available. IRA cannot account for unidentified hazards; this is particularly relevant for aquatic animal health in general and the trade in ornamental aquatic animals in particular.
Aquaculture and disease emergence
The same risk framework which has been used for examining disease spread through trade in live animals and animal products have also been applied to disease emergence. Murray and Peeler and Bridges et al. used risk models to investigate drivers for the emergence of disease in aquaculture.
However, disease emergence in terrestrial systems has been studied in greater depth, in particular the evolution of virulence, the importance of animal reservoirs and multiple hosts. These studies have in large part been driven by the emergence of zoonotic pathogens.
Epidemiological studies need to more fully explore the conditions under which putative pathogens spread between wild and farmed aquatic animals. The introduction of non- native species has been fundamental to the expansion of aquaculture. Rainbow trout, a native of North America, is the most important freshwater finfish species in Europe and is cultured across the globe.
Paenus monodon and other species have been shipped internationally to establish shrimp aquaculture. A recent review demonstrated that the introduction of non-native aquatic animal species underpinned many instances of disease emergence in Europe and this is likely to be true for other parts of the world.
It is likely that the culture of new species, the expansion of aquaculture into new areas and the global trade in both live aquatic animals and commodity will continue to increase as the demand for animal protein increases with the growth in human population and the decline of wild capture fisheries.
Diseases which emerge in farmed populations invariably originate in wild populations. Thus interaction between wild and farmed populations facilitated by the open design of many aquaculture systems and the current fish farming practices is fundamental to disease emergence. Additionally, restrictions in the use of chemicals or the development of resistance could lead to the re-emergence of old diseases that had previously be controlled.
Applying the epidemiological modelling approaches which have been used to study disease emergence in terrestrial systems may provide insights into the processes driving disease emergence in the aquatic environment, and inform the development of improved mitigation measures.
Climate change and disease emergence
Climate change will influence the development of aquaculture and the epidemiology of aquatic animal diseases. Many important aquatic animal pathogens have temperature thresholds, above or below which disease or infection does not occur.
A risk assessment model to screen pathogens, to identify those whose threat will increase under established climate change scenarios has been developed for freshwater fish diseases and applied to the UK, which identified Lactococcus garvieae and Anphanomyces invadans as the exotic diseases whose threat will increase most with rising water temperatures. Epidemiological modelling and the application of geographic information systems (GIS) have been used to good effect to assess the likely impact of climate change scenarios on terrestrial livestock diseases (especially vector borne diseases such as blue tongue virus and trypanosomiasis), and huge scope exists to apply these approaches to aquatic animal diseases.
Outbreak investigation is a core activity for epidemiologists and uses key methods of modern epidemiology: measurement of disease frequency in time and space and in different populations. More recently molecular analyses have been incorporated into outbreak investigations in order to aid source tracking. Outbreak investigations of transboundary diseases are generally undertaken by the veterinary services and generally remain unpublished. However, research papers investigating the origin of transboundary diseases have been published.
Investigations of infectious haematopoietic necrosis virus (IHNV) in Europe have attributed its introduction to imported rainbow trout eggs from the US. This hypothesis has been supported by molecular epidemiology studies showing that all European IHNV isolates belong to one of the four N. American genogroups. Conversely, genotyping demonstrated that viral haemorrhagic septicaemia virus (VHSV) in N. America strain had emerged separately from a marine reservoir with no epidemiological link to Europe (where the disease first emerged). Similarly genotyping of ISAV demonstrated emergence from the marine reservoir on separate occasions in Norway, Scotland and N. America.
However, genetic analysis of the isolate from the recent outbreak in Chile is identical to Norwegian isolates suggesting spread via imported eggs in 1996.
Despite its growing use and popularity, aquatic molecular epidemiology is yet to reach the level of sophistication applied to terrestrial systems. Examples of the potential power of molecular epidemiology can be seen in studies such as Cottam et al. who, in studying the transmission of foot and mouth disease virus (FMDV) used small mutations found in the entire viral sequence to identify possible previously unidentified contacts in the 2001 epidemic.
The availability of technologies that allow for rapid, large-scale sequencing, such techniques provide exciting potential to develop aquatic epidemiology, and may provide a powerful tool to enhance our ability to accurately trace the source and course of infections.