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Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe
Microbes and Infection 8 (2006) 1358e1364 www.elsevier.com/locate/micinf
Review
Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe Rodolphe E. Gozlan a,*, Edmund J. Peeler b, Matt Longshaw b, Sophie St-Hilaire c, Stephen W. Feist b a b
Centre for Ecology and Hydrology, Winfrith Technology Centre, Winfrith Newburgh, Dorchester DT2 8ZD, United Kingdom Centre for Environment Fisheries & Aquaculture Science, The Nothe, Barrack Road, Weymouth DT4 8UB, United Kingdom c Department of Biological Sciences, Idaho State University, Pocatello, ID 83209, USA Available online 9 February 2006
Abstract The expansion of aquaculture and the demand for ornamental fish have resulted in the large-scale movements of aquatic animals and their pathogens. Here we review the most important non-native fish and shellfish pathogens in European waters and their global impacts on wild fish host populations. The role of theoretical models in the study of the impact of microbial pathogens is discussed, including its integration into risk assessments. Ó 2006 Elsevier SAS. All rights reserved. Keywords: Fish diversity; Microparasites; Freshwater; Risk assessment; Pathogen introductions
1. Introduction The decline of fish stocks around the world has been attributed to habitat loss, over fishing, and more recently, pathogens [1,2]. The following review will examine the sources of pathogen transfer into na€ıve wild fish populations, a few examples where pathogen introduction is responsible for loss of aquatic biodiversity, and methods which could be utilised to reduce, at least anthropogenic, translocation of fish pathogens. There are several ways for novel pathogens to be introduced into a na€ıve population. For example, a benign organism can undergo a genetic change that renders it more pathogenic [3,4]. A pathogen can also be introduced via the range expansion of wild fish to new geographic areas as a result of global warming or removal of natural barrier (i.e. canals, habitat management). However, the main pathway of pathogen introduction is through the movement of animals for trade and recreation. The sheer volume of international trade,
* Corresponding author. Tel.: þ44 01305 213574; fax: þ44 01305 213600. E-mail address: [email protected] (R.E. Gozlan). 1286-4579/$ - see front matter Ó 2006 Elsevier SAS. All rights reserved. doi:10.1016/j.micinf.2005.12.010
facilitated by the drive for free trade and tourism, has increased the likelihood of the intentional or unintentional movement of aquatic species and their associated pathogens. In fact, most literature examples of population effects from introduced novel pathogens link anthropogenic movement (intentional or unintentional) of aquatic species. In many cases, customs and quarantine practices that were developed to protect countries from aquatic diseases provide inadequate safeguards against species that threaten native inland water biodiversity [5]. More than 80% of aquatic animal introductions are freshwater and these introductions are mainly for aquaculture (53%), fisheries support (18%), recreational fishing (12%) and aquarium trades (10%) [6]. The growth in intensive modern aquaculture has been followed by increased introduction and translocation of infectious pathogens in European freshwater ecosystems; at least 94 known pathogenic agents from 13 different taxonomic groups (Virus, Bacteria, Eumycota, Ascetospora, Dermocystida, Ciliophora, Microspora, Myxozoa, Monogenea, Digenea, Cestoda, Nematoda, and Crustacea) have been introduced into European waters. The main geographical source of pathogen introduction into Europe is Asia, 64% of the total number of sourced
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introductions, followed by North America (22%) and only 9% accounted for European translocations. Africa and South America together represented less than 1% [7]. However, this account is possibly biased towards pathogens of aquaculture species due to limited knowledge of wild fish pathogen fauna. The strong correlation between source of host and source of pathogen indicates that aquaculture not only facilitates disease emergence but also may act as a source of pathogen introduction. In addition, there are well-established examples of the movement of live fish for farming resulting in disease translocation (discussed in detail in Section 4). The link between movement of live fish and translocation of pathogens might become more obvious when developments in sampling protocols and diagnostic techniques enable better characterisation of emerging infectious pathogens [1]. Many believe that intensive aquaculture conditions such as high stocking densities, accumulation of waste, handling, and poor water quality all serve to compromise immunity and favour disease emergence [7]. Recent increased awareness of potential disease transfer from aquaculture farms to wild ecosystems originates from the great discrepancies between the high prevalences of infection in farmed fish when compared to apparently low prevalences in wild populations. The introduction and establishment of animals into a new geographical region (biological pollution), often through human involvement, can introduce novel pathogens (pathogen pollution) to the native fauna. When an introduced host acts as a reservoir population from which infection can ‘spill-over’ to sympatric wildlife, pathogen pollution which would otherwise fail to persist instead underpins the emergence of disease in na€ıve populations. A recent example is the introduction of topmouth gudgeon (Pseudorasbora parva) into an English fish farm. This fish is a host for the rosette-like agent [1], an intracellular eukaryotic parasite and has now escaped into the connected river system, with the potential to introduce the pathogen to na€ıve native wild populations. Whirling disease caused by the myxozoan parasite Myxobolus cerebralis is another example of spill over (spill-back) that shows aquaculture not only as a revealer of diseases but also principally as a source and dispersal mechanism. Trade in ornamental fish, with its large taxonomic diversity of species, raised or captured in natural environments from geographically widespread origins, remains a potential source of pathogen pollution, especially in areas where the water temperature is conducive to the survival of exotics. Their real contribution to the introduction of pathogens is largely unknown as they are not subject to specific sanitary surveillance in Europe [7,8]. Although there are numerous examples of disease emergence after species introduction, there are undoubtedly many more that have not been identified. Epidemics in the wild that cause high mortality or changes in species behaviour are easily characterised, but less easily identified when they cause long-term gradual population declines. It is relatively complex to link fish population decline and pathogen infection in wild populations because diseased or dead animals are rapidly destroyed by predators or necrophages. This is one of the reasons why the impact of an introduced pathogen might very
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often go unnoticed. However, it is only with a clear understanding of the impact of pathogen pollution on wild fish population that risk assessment policies [8] can be properly adapted to prevent disease outbreaks and preserve biodiversity. Few examples of the impact of pathogen introduction on wild fish population exist [7]. Some of the most convincing cases are the impact of Anguillicola crassus on eel (Anguilla anguilla) populations in Lake Balaton, the impact of a ciliate parasite Ichthyophthirius multifiliis on a pupfishes species (Orestia sp.) population in Lake Titicaca where the link between the ciliate introduction and the mass mortalities of fish was established after 30 years and finally, the impact of the monogenean parasite Gyrodactylus salaris on Norwegian Atlantic salmon (Salmo salar) populations. The cost of global biodiversity loss due to disease is yet to be assessed; however, an economic cost is associated with introduced species and emerging infectious diseases in wildlife. For the United States alone this cost has been recently estimated at more than $137 billion per year [9]. 2. Pathogen detection Routinely, the presence of a pathogen in a population will be detected based on clinical signs shown by infected specimens, but recent research has shown that the host specificity as well as the level of virulence of certain pathogens could be extremely variable [1]. For particular pathogens, the range of possible hosts across various taxonomic groups is unknown and therefore contributes to the difficulty in their detection. Also, the detection of healthy carrier or sub-clinical carriers is not done systematically and the techniques or means set up for the diagnosis are not always sensitive enough for routine detections [1]. This highlights the complexity of legislating on the import of live fish with a multiple host-species scenario [8]. Advances in diagnostic methods have considerably altered the level of perception of pathogens and diseases; this has notably influenced health legislation and is likely to result in the review of measures to reduce introductions. The recent findings on the carrier of the rosette-like agent [1] highlight the limitations of the screening programmes currently used internationally to detect pathogens in carrier fish populations. Although the minimum detection limits of molecular tests are very low, it is only one factor involved in the detection of a carrier population. Other factors, such as the prevalence of carrier fish within the population, the concentration of the pathogen within the fish and the amount and type of tissue sampled play a very important role in the ‘sensitivity’ of the sampling scheme [10]. Often these other factors are forgotten and the lack of pathogen detection is associated to a pathogen free population. In cases where carrier states are suspected and difficult to detect and there is no good medical history to corroborate mortality events, regulators may advise the use of more conventional methods such as cohabitation studies with susceptible species, stress testing, or antibody tests for assessing the health of populations. The drawback to these techniques is the cost; however, the benefits may outweigh the costs if pathogen transfer is prevented.
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Nevertheless, the detection of pathogens calls for ever more sophisticated identification techniques. Developments in molecular biology have led to rapid growth in new diagnostic methods (e.g. polymerase chain reaction, amplification of nucleic acids, restriction enzyme digestion, probe hybridisation and nucleotide sequencing). These techniques have lower detection limits and are considered more rapid than the traditional methods such as culture, serology and histology; however, they do not address the limitations of sampling carrier populations. Carrier populations generally have low numbers of infected individuals, and those infected have low levels of pathogens. In some cases (i.e. herpes viruses) the target tissue in carrier fish is not clearly known. Even with the use of molecular diagnostic tests it is sometimes difficult to detect carrier populations without extensive testing, which is not economical. One recent example of where routine testing of fish from carrier populations did not detect the pathogen until a cohabitation study was conducted is that of on topmouth gudgeon [1]. An advantage of molecular techniques when compared to immunochemical and other approaches is the potential to compare pathogen genetically, which has benefited taxonomy, pathogen evolution, pathogenic mechanisms and epidemiology [3]. Aquatic health specialists are able to distinguish between introductions of pathogens and native agents in emergence with increasing accuracy, thus revealing the considerable diversity of pathogens and their hosts. 3. Examples of pathogen establishment in European waters There are numerous reports of the detection of ‘new’ fish and shellfish pathogens throughout Europe [7]. However, most of these are relatively innocuous and most likely reflect the diligence of statutory authorities and research workers involved in aquatic animal health. There are relatively few examples of the introduction and spread of pathogens that either were already well recognised as serious pathogens or have become so (Table 1). This section provides some examples of such pathogens which have resulted in serious disease in wild or farmed stocks. Crayfish plague is the best known example of the spread of an infectious aquatic disease infecting freshwater Crustacea. The oomycete fungus Aphanomyces astaci causes the disease. Native crayfish species throughout Europe are highly susceptible to this pathogen which has eradicated populations in affected areas. The spread of crayfish plague, from initial outbreaks in Italy in the 1860s to many European countries, was described by Alderman [11]. It is thought that the plague was introduced into Europe via imports of North American signal crayfish which are naturally resistant to the pathogen. Subsequently, commercial transfers of crayfish and natural migrations facilitated the spread of the plague. This disease remains of concern and is notifiable to the ‘‘Office Internationale des Epizooties’’ (OIE). Proliferative kidney disease (PKD) of salmonids caused by the myxozoan parasite Tetracapsuloides bryosalmonae is one
amongst the most important diseases affecting cultured salmonids in many European countries as well as in North America [12]. The parasite causes significant economic loss in rainbow trout farms and affects wild salmonid, although the impact on wild populations is unclear. The first reports of proliferative kidney disease were from Germany at the turn of the twentieth century and reports of the disease increased throughout Europe as salmonid aquaculture expanded. However, it is now recognised that the parasite is a natural host of freshwater bryozoans and that the stages released from the bryozoans are infective to fish [13]. It is thought that the parasite can be spread naturally by waterfowl vectors [12], dispersing infected bryozoan statoblasts trapped in their feathers which give rise to new colonies when deposited in new water bodies. Water bodies lacking susceptible fish species have been shown to harbour infections in bryozoan colonies. Introduction of salmonids to these areas has resulted in disease. Whether salmonids can release stages infective to bryozoa, thereby increasing pathogen concentration in the environment, has yet to be confirmed. Recently the discovery of a disease agent implicated in the decline of the cyprinid fish the endangered sunbleak Leucaspius delineatus [1] has highlighted the potential for the spread of fish pathogens by colonisation of invasive fish species and commercial activities. The pathogen, currently referred to as ‘rosette-like agent’ (RLA) is similar if not identical to Sphaerothecum destruens affecting North American salmonids. The pathogen causes a chronic disease which prevents spawning of wild fish such as L. delineatus. The decline of L. delineatus across Europe appears to be linked to the spread of P. parva which originated from China during the 1960s. P. parva appears to be a healthy carrier for the pathogen and susceptible species held in the same water as carrier infected with the rosette-like agent exhibits spawning inhibition, emaciation and eventually dies. Further work is required to determine the distribution of the pathogen in Europe, transmission mechanisms and potential threats to other fish species. A number of bacterial pathogens have similarly come to prominence through their recognition as disease agents in aquaculture situations, but which also have affected wild fish, notably bacterial kidney disease (Renibacterium salmoninarum) and furunculosis (Aeromonas salmonicida sub sp. salmonicida). Bacterial kidney disease was first reported in wild salmon in Scotland in 1933 and soon afterwards in cultured fish in North America. It has a very wide geographic distribution, effectively having been found wherever susceptible salmonids are farmed with the exception of Australasia. Bacterial kidney disease has been spread through the movement of live fish and gametes (it is vertically transmitted) for aquaculture. Furunculosis, caused by A. salmonicida, is thought to have been introduced into the UK in the 1920s with imported trout [14]. It caused disease and mortality in wild salmonids in the UK [15]. The disease spread to Norway on two occasions, with live salmon exports from Denmark and Scotland [16]. Shellfish diseases have also shown their ability to spread via anthropogenic intervention and two of the most important are notifiable disease within the European Union. Marteilia
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Table 1 Examples of important transboundary diseases of farmed fish Disease
Susceptible species
Country where introduced
Year
Potential route
Viruses Infectious haemopoeitic necrosis White spot virus of shrimp Pilchard herpes virus Sleeping disease Koi herpes virus
Salmonids Shrimps (Penaeus spp.) Pilchards (Sardinops sagax) Rainbow trout (Oncorhynchus mykiss) Carp (Cyprinus carpio)
Europe Asia and Americas Australia UK Japan
1976 1990s 1995 2002 2003
Fish eggs Live crustacean Fish carcasses Fish carcasses Live fish
Bacteria Red pest (Listonella anguillarium) Furunculosis (Aeromonas salmonicida) Gaffkaemia (Aerococcus viridans)
Eels (Anguilla spp.) Salmonids European lobster (Homarus gammarus)
Japan and US UK Europe
1780s 1920s 1978
Live fish Live fish Live lobsters
Fungal infections Crayfish plague (Aphanomyces astaci)
European crayfish (Astacus fluviatilis)
Europe
1865
Live signal crayfish
Coarse fish Salmonids Native European oysters (Ostrea edulis) Atlantic salmon European eel (Anguilla anguilla)
Europe US France and Spain
2005 1960s 1970s
Live fish Fish carcasses Live oysters
Norway Europe
1973 1980s
Live fish Live fish
Parasites Rosette-like agent Whirling disease (Myxosoma cerebralis) Bonamia oestrae Gyrodactylus salaris Anguillicola crassus
refringens, a paramyxean parasite has caused mass mortalities in the European flat oyster Ostrea edulis since its discovery in France in the 1960s where it caused significant economic loss [17]. Subsequently the disease occurred in Spain and The Netherlands. Movements of shellfish appear to have been the principle mechanism of spread. However, there is strong evidence that the parasite requires an intermediate host (possibly the copepod Paracartia grani). Bonamiasis caused by the haplosporean parasite Bonamia ostreae is another disease of O. edulis which has caused significant losses to the European aquaculture industry. Other intracellular ‘microcell’ parasites cause similar diseases in bivalve molluscs elsewhere and are regarded as major threats to oyster stocks around the world [18]. B. ostreae is thought to have reached Europe via introduction of infected O. edulis from North America with the first disease outbreaks occurring firstly in France in 1979 and spreading to neighbouring countries over the following decades, reaching the United Kingdom and Ireland. The source of infection and whether there is an intermediate host for the parasite are currently unknown. G. salaris, a freshwater, monogenean ectoparasite, is one of a number of gyrodactylids that infect salmonids. The parasite was first described as a commensal parasite of Atlantic salmon in Sweden [19]. However, when the parasite was introduced into Norway in the early 1970s with the importation from Sweden of juvenile salmon for aquaculture, its impact was dramatic [20]. Atlantic salmon in Norway (Atlantic strains of Atlantic salmon) appeared to be considerably more susceptible to G. salaris, compared with their Baltic cousins (Baltic strains of Atlantic salmon) [19]. In susceptible strains of salmon, reproduction is unchecked by an immune response and death normally results. G. salaris feeds by removing plugs of flesh, which results in secondary infections and compromises osmoregulation. The parasite has been introduced into a total of 45 Norwegian rivers,
mainly through the movement of salmon for farming [20]. The distribution of G. salaris in Europe is unknown but it is likely to be widespread due to the movement of rainbow trout from Finland [16]. G. salaris is arguably one of the most important disease threats to Atlantic salmon populations outside of the Baltic watershed. 4. The impacts of introduced microbial pathogens on wild fish populations Few studies have been conducted on the impact of pathogens on free-living hosts. Furthermore, the number of studies examining the role of disease on structuring fish populations is even more limited, in particular in relation to introduced pathogens. Those pathogens that are studied tend to be ones that impact immediately and negatively on host population dynamics, usually in the form of epidemics. A number of examples in the literature that have shown that pathogens can have a significant and deleterious effect on fish populations, but these have tended to be very localised and are often associated with a combination of adverse environmental conditions. Since disease can act not only directly through mortality events but also indirectly (e.g. reduced fecundity, alterations in host behaviour, reductions in swimming speeds, and increased risk of predation [21]) the total impact can be difficult to assess. Additionally, it would be expected that ‘‘diseased’’ individuals would be quickly removed from the ecosystems, thus providing an underestimate on the role of disease in structuring populations. Intuitively it would be expected, given the plethora of information on diseases in aquaculture, that diseases would have an impact on fish populations. However, the influence of disease on population structure has rarely been considered in the management of fisheries, which may in part be due to the lack of
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examples of diseases in wild fish and an overemphasis on the role of stressors in captive fisheries compared with those present in wild fisheries. Arguably, one of the most studied infections of farmed and wild fish is whirling disease caused by the myxozoan M. cerebralis. Originally described from Europe in 1898 [22], it is now recognised as a major pathogen of North American salmonids, in particular Oncorhynchus mykiss. Its translocation from Europe and its subsequent establishment in the USA demonstrates the importance of understanding the fauna of hosts in their natural environment and the impact of moving these apparently innocuous pathogens into new and na€ıve environments and hosts. Unfortunately, even with such an extensively studied pathogen, the true effect on populations remains unclear. Despite the number of studies, there is still uncertainty about the complex interactions between host, pathogen and environment, which constrains the development of management strategies to control the parasite in wild fish [22]. In addition, there is a lack of absolute and clear evidence that the parasite can impact on all populations [22]. This may be due to differences in host susceptibility, variations in exposure routes and doses and environmental conditions prior to and after introduction of the parasite. Indeed, the apparent lack of statistical and mathematical models that clearly demonstrate a correlation between disease severity and population declines gives cause for concern. Two other major pathogens of concern in wild salmonids are T. bryosalmonae and G. salaris, both of which have been implicated in population declines. Native salmon parr population density was reduced to approximately 50% 2 years after the introduction of G. salaris into Norwegian rivers and after 7 years, salmon parr density was as low as 5% [20]. Subsequent reductions in migrating smolts have led to reductions in returning adult salmonids in subsequent years and thus severe population declines. Proliferative kidney disease is recognised as a pathogen of farmed salmonids, causing upwards of 40% mortality on a farm, but its role in population success has been, until relatively recently, less well defined. It is known that the severity of PKD infections is exacerbated by poor water quality [23]. Moreover, recent findings indicate unequivocally that a combination of poor water quality and the presence of PKD was responsible for reductions of brown trout populations in Swiss rivers. A major issue in determining the impact of microbial pathogens on population diversity is that most publications do not consider the community per se when examining diseases. The impact of any disease is usually considered singularly and over a short period of time. Mortality is usually the outcome measured and body condition, fecundity, swimming and other host behaviour are seldom examined over a long period of time. Establishing the multiple interactions between environment and pathogens is also difficult to achieve. Furthermore, the effect of the loss of, or reduction in, numbers of individuals from that population on the wider community structure is often not considered. Future studies should seek to consider the role of disease on individuals, populations and communities. The types of studies required for assessing the role of pathogens on aquatic biodiversity are difficult to accomplish because
they require the study of populations over long periods of time, multiple watershed for comparisons, and are therefore very expensive. The introduction of a non-native pathogen into a population with low genetic variation has rarely been considered outside of aquaculture facilities. Such effects can have catastrophic consequences. Heterozygous populations are often better able to contend with any new or existing disease threat than homozygous populations, which are at greater risk of extinction from an introduced pathogen. Hedrick et al. [24] showed that inbred populations of the endangered Gila topminnow Poeciliopsis occidentalis occidentalis were at greater risk of extinction when exposed to Gyrodactylus turnbulli when compared to a heterozygous population. Whilst such events would appear detrimental to host populations, parasites themselves may preferentially infect host populations with low levels of genetic variation [25]. Irrespective of whether or not microbes are detrimental to their native host in their normal range, it is important that the microbial fauna of the introduced host species is characterised and any potential impacts on the communities of the receiving ecosystems are considered prior to any movements into that system. 5. Theory and risk assessments Theoretical studies of the impact of microbial pathogens on fish populations encompass mathematical disease models (deterministic or stochastic) and risk modelling. Models provide a method to conceptualise complex systems and an environment in which to examine interactions; they are, therefore, appropriate to the study of the impact of microbial pathogens on the diversity of fish populations. In the field of aquatic animal health, mathematical models have been used to study the epidemiology of sealice: Lepeophtheirus salmonis [26] and Caligus elongatus [27]. Models of larval lice production in Norwegian [28] and Scottish [29] waters have demonstrated that a very large proportion of larval lice originate from farmed fish, substantially altering sealice epidemiology, compared with the pre-aquaculture period. Other diseases which have been investigated by modelling include the impact of bacterial kidney disease [30] and furunculosis [31] on chinook salmon (Oncorhynchus tshawytscha) populations and epidemics of pilchard herpes virus in Sardinops sagax along the Australian coast [32,33] and Ichthyophonus hoferi (a mesomycetozoan disease) in herring (Clupea harengus) [34]. Two theoretical papers have produced generic models for the impact of disease on wild salmon populations [35,36]. During a disease outbreak it is possible that the high replication rate of the pathogen favours the evolution of a more virulent strain [11]. Not only this could be the source of a novel pathogen into a na€ıve population but also it could result in a larger effect on biodiversity. Theoretical models of the evolution of virulence have been developed [4,37] and can be incorporated into models to estimate the impact of disease in wild populations.
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In risk analysis terminology, risk is defined as both the probability and consequences of an adverse event (e.g. pathogen introduction) and, therefore, consequence assessment is an important element of the process. The use of risk assessment in aquatic animal health has largely been restricted to investigating disease transmission and, in particular, transboundary spread (i.e. import risk analysis e IRA). A review of the ‘import risk analysis’ found that the consequence assessment was frequently omitted or highly restricted in scope and depth. Mathematical modelling needs to be used for consequence assessment for significant progress in estimating the likely ecological impact of disease introduction to be achieved. Theoretical studies have been used to study the impact of endemic diseases (e.g. bacterial kidney disease) and epidemic (e.g. pilchard herpes virus) diseases on individual wild fish host populations. The integration of epidemiological and ecological models is required to extend studies of single populations to the level of the fish community and, therefore, diversity. In addition to methodological constraints, the further application of theoretical approaches is limited by a lack of epidemiological data. 6. Effect of climate change Climate change will influence the effect of microbial pathogens on fish populations. Firstly, increasing water temperatures will change the geographic distribution of marine species, with potential disease consequences. In freshwater, increasing water temperature will increase the ability of exotic fish species, introduced into Europe as a result of international trade, to establish and spread, thereby increasing the probability that pathogens spread to native fish populations. In addition, some introduced pathogens, such as koi herpes virus, may survive better and exert greater impact at higher water temperatures. A change in climate will also affect the epidemiology of endemic diseases. The incidence and geographic range in Europe of Lactococcus garvieae have increased in recent years as the water temperature has risen. There is evidence from Switzerland that the prevalence of proliferative kidney disease in wild grayling (Thymallus thymallus) increased with water temperature. Furthermore, increases in temperature may affect the behaviour of native species and result in exposure to pathogens that would not necessarily have been exposed to. Assessing the likely influence of climate change on disease epidemiology will inform the development of policies to mitigate its impact on fish diversity. 7. Discussion and conclusion This review has assessed how microbial pathogens may affect the diversity of fish populations in Europe. The role of aquaculture and the translocation of fish species have been highlighted. Whilst aquaculture has been practised for more than 2000 years, and movements of live fish have taken place for almost as long, the rapid expansion of fish farming over the last 40 years, in terms of volume, number of species and geographic location, has been accompanied by significant
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international movements of live fish [8]. In addition, the demand in the West for fish as companion animals creates large-scale movements of warm and coldwater ornamental fish. This review clearly demonstrates that introduced pathogens and parasites, invariably associated with live fish movements, have affected the diversity of wild fish populations. Macroparasites provide the best examples: the impact of G. salaris on Atlantic salmon in Norway and A. crassus in European eels. Some will argue that the threat of transboundary diseases based on the precautionary principle should lead to the restriction of free trade in aquatic animals and their products. However, this would be contrary to international trade agreements. The Sanitary and Phytosanitary Agreement of the World Trade Organisation offers a middle way. A country can impose measures over and above those set out in international agreements, if supported by an import risk analysis (IRA). In this review it is argued that methodological developments in IRA, notably the application of mathematical modelling, are needed to ensure that the potential impact of microbial pathogens is properly assessed. IRA will always be limited by our ability to identify hazards as hazard identification for many aquatic animal pathogens is constrained by the lack of data. An IRA of Atlantic salmon smolts to Norway from Sweden in the early 1970s would probably not have identified G. salaris as a hazard. The problem of unidentified hazards has led some to argue that, using historical data, an estimate of the likelihood of an unidentified hazards could be calculated and included in a commodity IRA [38]. Biosecurity Australia have considered linking undiagnosed mass mortality incidents in cultured bivalve molluscs, which occur quite regularly, to known hazards to improve the hazard identification process. Compared with exotic pathogens, there is less evidence of endemic microbial pathogens influencing the diversity of fish populations. However, the problems of detecting demographic and genetic impacts in wild fish populations are severe. It is likely that studies reviewed would not have been able to detect subtle influences of pathogens on population diversity. A greater use of mathematical and statistical modelling approaches is needed to improve our ability to detect the impact of disease in wild fish populations, and to improve the design of future surveys. The aquaculture industry, governments and international organisations have the shared responsibility to ensure that aquacultural development causes minimal environmental impact. Inevitably, transfers of live fish will continue, therefore, it is crucial that IRA methodology is developed so that potential disease hazards are reliably identified and the consequences of disease introduction adequately assessed. The expansion of fish farming, either in new geographic areas or by bringing new species into farmed production, must be carefully evaluated for its potential environmental impacts. Inevitably, the majority of fish farming will operate in open systems that allow interaction with wild populations, therefore, minimum biosecurity levels should be established to minimise the risk of escapes and pathogen transfer to the wild. Assessments of the risks associated with live fish movements and aquaculture must be securely based on scientific evidence.
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The design of future fish disease studies should, in part, be determined by the data required for risk assessments. References [1] R.E. Gozlan, S. St-Hilaire, S.W. Feist, P. Martin, M.L. Kent, Biodiversity e disease threat to European fish, Nature 435 (2005) 1046. [2] P. Daszak, Emerging infectious diseases of wildlife e threats to biodiversity and human health, Science 287 (2000) 443e449. [3] C.O. Cunningham, Molecular diagnosis of fish and shellfish diseases: present status and potential use in disease control, Aquaculture 206 (2002) 19e55. [4] J.J. Bull, Perspective e virulence, Evolution 48 (1994) 1423e1437. [5] A. Ricciardi, Facilitative interactions among aquatic invaders: is an ‘‘invasional meltdown’’ occurring in the Great Lakes? Can. J. Fish. Aquat. Sci. 58 (2001) 2513e2525. [6] D.M. Bartley, R.P. Subasinghe, Historical aspects of international movement of living aquatic species, Rev. Sci. Tech. Off. Int. Epizoot. 15 (1996) 387e400. [7] G. Blanc, in: A. Uriarte, B. Basurco (Eds.), Environmental Impact Assessment of Mediterranean Aquaculture Farms, CIHEAM-IAMZ, Zaragoza, 2001, pp. 37e56. [8] G.H. Copp, R. Garthwaite, R.E. Gozlan, Risk identification and assessment of non-native freshwater fishes: a summary of concepts and perspectives on protocols for the UK, J. Appl. Ichthyol. 21 (2005) 371e373. [9] D. Normile, Invasive species e expanding trade with China creates ecological backlash, Science 306 (2004) 968e969. [10] S. St-Hilaire, C. Ribble, G. Traxler, T. Davies, M.L. Kent, Evidence for a carrier state of infectious hematopoietic necrosis virus in chinook salmon Oncorhynchus tshawytscha, Dis. Aquat. Org. 46 (2001) 173e179. [11] D.J. Alderman, Geographical spread of bacterial and fungal diseases of crustaceans, Rev. Sci. Tech. 15 (1996) 603e632. [12] M. Henderson, B. Okamura, The phylogeography of salmonid proliferative kidney disease in Europe and North America, Proc. R. Soc. Lond. B. 271 (2004) 1729e1736. [13] S.W. Feist, M. Longshaw, E.U. Canning, B. Okamura, Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae, Dis. Aquat. Org. 45 (2001) 61e68. [14] A.J. Mitchell, Finfish health in the United States (1609e1969): historical perspective, pioneering researchers and fish health workers, and annotated bibliography, Aquaculture 196 (2001) 347e438. [15] A. Irianto, B. Austin, Probiotics in aquaculture, J. Fish Dis. 25 (2002) 633e642. [16] T.A. Bakke, P.D. Harris, Diseases and parasites in wild Atlantic salmon (Salmo salar) populations, Can. J. Fish. Aquat. Sci. 55 (1998) 247e266. [17] F.C.J. Berthe, F. Le Roux, R.D. Adlard, A. Figueras, Marteiliosis in molluscs: a review, Aquat. Living Resour. 17 (2004) 433e448. [18] R.B. Carnegie, N. Cochennec-Laureau, Microcell parasites of oysters: recent insights and future trends, Aquat. Living Resour. 17 (2004) 519e528. [19] G. Malmberg, M. Malmberg, Species of Gyrodactylus (Platyhelminthes, Monogena) on salmonids in Sweden, Fish Res. 17 (1993) 59e68. [20] B.O. Johnsen, A.J. Jensen, The Gyrodactylus story in Norway, Aquaculture 98 (1991) 289e302.
[21] I. Barber, D. Hoare, J. Krause, Effects of parasites on fish behaviour: a review and evolutionary perspective, Rev. Fish Biol. Fish. 10 (2000) 131e165. [22] J.L. Bartholomew, P.W. Reno, in: J.L. Bartholomew, J.C. Wilson (Eds.), The History and Dissemination of Whirling Disease, Amer Fisheries Soc, Bethesda, 2002, pp. 3e24. [23] M. El-Matbouli, R.W. Hoffmann, Influence of water quality on the outbreak of proliferative kidney disease e field studies and exposure experiments, J. Fish Dis. 25 (2002) 459e467. [24] P.W. Hedrick, T.J. Kim, K.M. Parker, Parasite resistance and genetic variation in the endangered Gila topminnow, Anim. Conserv. 4 (2001) 103e109. [25] R. Poulin, L.J. Marshall, H.G. Spencer, Metazoan parasite species richness and genetic variation among freshwater fish species: cause or consequence? Int. J. Parasitol. 30 (2000) 697e703. [26] C.W. Revie, G. Gettinby, J.W. Treasurer, G.H. Rae, N. Clark, Temporal, environmental and management factors influencing the epidemiological patterns of sea lice (Lepeophtheirus salmonis) infestations on farmed Atlantic salmon (Salmo salar) in Scotland, Pest Manag. Sci. 58 (2002) 576e584. [27] C.W. Revie, G. Gettinby, J.W. Treasurer, G.H. Rae, The epidemiology of the sea lice, Caligus elongatus Nordmann, in marine aquaculture of Atlantic salmon, Salmo salar L. in Scotland, J. Fish Dis. 25 (2002) 391e400. [28] P.A. Heuch, T.A. Mo, A model of salmon louse production in Norway: effects of increasing salmon production and public management measures, Dis. Aquat. Org. 45 (2000) 145e152. [29] J.R.A. Butler, Wild salmonids and sea louse infestations on the west coast of Scotland: sources of infection and implications for the management of marine salmon farms, Pest Manag. Sci. 58 (2002) 595e608. [30] O.S. Hamel, J.J. Anderson, Relationship between antigen concentration and bacterial load in Pacific salmon with bacterial kidney disease, Dis. Aquat. Org. 51 (2002) 85e92. [31] H. Ogut, P.W. Reno, D. Sampson, A deterministic model for the dynamics of furunculosis in chinook salmon Oncorhynchus tshawytscha, Dis. Aquat. Org. 62 (2004) 57e63. [32] A.G. Murray, The use of simple models in the design and calibration of a dynamic 2D model of a semi-enclosed Australian bay, Ecol. Model. 136 (2001) 15e30. [33] A.G. Murray, D.J. Gaughan, Using an age-structured model to simulate the recovery of the Australian pilchard (Sardinops sagax) population following epidemic mass mortality, Fish. Res. 60 (2003) 2e3. [34] A.L.S. Munro, A.H. McVicar, R. Jones, The epidemiology of infectious diseases in commercially important wild marine fish, Rapp. P.V. Re´un. Cons. Int. Explor. Mer. 182 (1983) 21e32. [35] D.A. Levy, C.C. Wood, Review of proposed mechanism for sockeye salmon population cycles in Fraser River, Bull. Math. Biol. 54 (1992) 241e262. [36] S. des Clers, Modelling the impact of disease-induced mortality on the population size of wild salmonids, Fish. Res. 17 (1993) 237e248. [37] S.A. Frank, Models of parasite virulence, Quart. Rev. Biol. 71 (1996) 37e78. [38] D.J. Gaughan, Disease-translocation across geographic boundaries must be recognized as a risk even in the absence of disease identification: the case with Australian Sardinops, Rev. Fish Biol. Fish. 11 (2002) 113e123.
Review
Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe Rodolphe E. Gozlan a,*, Edmund J. Peeler b, Matt Longshaw b, Sophie St-Hilaire c, Stephen W. Feist b a b
Centre for Ecology and Hydrology, Winfrith Technology Centre, Winfrith Newburgh, Dorchester DT2 8ZD, United Kingdom Centre for Environment Fisheries & Aquaculture Science, The Nothe, Barrack Road, Weymouth DT4 8UB, United Kingdom c Department of Biological Sciences, Idaho State University, Pocatello, ID 83209, USA Available online 9 February 2006
Abstract The expansion of aquaculture and the demand for ornamental fish have resulted in the large-scale movements of aquatic animals and their pathogens. Here we review the most important non-native fish and shellfish pathogens in European waters and their global impacts on wild fish host populations. The role of theoretical models in the study of the impact of microbial pathogens is discussed, including its integration into risk assessments. Ó 2006 Elsevier SAS. All rights reserved. Keywords: Fish diversity; Microparasites; Freshwater; Risk assessment; Pathogen introductions
1. Introduction The decline of fish stocks around the world has been attributed to habitat loss, over fishing, and more recently, pathogens [1,2]. The following review will examine the sources of pathogen transfer into na€ıve wild fish populations, a few examples where pathogen introduction is responsible for loss of aquatic biodiversity, and methods which could be utilised to reduce, at least anthropogenic, translocation of fish pathogens. There are several ways for novel pathogens to be introduced into a na€ıve population. For example, a benign organism can undergo a genetic change that renders it more pathogenic [3,4]. A pathogen can also be introduced via the range expansion of wild fish to new geographic areas as a result of global warming or removal of natural barrier (i.e. canals, habitat management). However, the main pathway of pathogen introduction is through the movement of animals for trade and recreation. The sheer volume of international trade,
* Corresponding author. Tel.: þ44 01305 213574; fax: þ44 01305 213600. E-mail address: [email protected] (R.E. Gozlan). 1286-4579/$ - see front matter Ó 2006 Elsevier SAS. All rights reserved. doi:10.1016/j.micinf.2005.12.010
facilitated by the drive for free trade and tourism, has increased the likelihood of the intentional or unintentional movement of aquatic species and their associated pathogens. In fact, most literature examples of population effects from introduced novel pathogens link anthropogenic movement (intentional or unintentional) of aquatic species. In many cases, customs and quarantine practices that were developed to protect countries from aquatic diseases provide inadequate safeguards against species that threaten native inland water biodiversity [5]. More than 80% of aquatic animal introductions are freshwater and these introductions are mainly for aquaculture (53%), fisheries support (18%), recreational fishing (12%) and aquarium trades (10%) [6]. The growth in intensive modern aquaculture has been followed by increased introduction and translocation of infectious pathogens in European freshwater ecosystems; at least 94 known pathogenic agents from 13 different taxonomic groups (Virus, Bacteria, Eumycota, Ascetospora, Dermocystida, Ciliophora, Microspora, Myxozoa, Monogenea, Digenea, Cestoda, Nematoda, and Crustacea) have been introduced into European waters. The main geographical source of pathogen introduction into Europe is Asia, 64% of the total number of sourced
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introductions, followed by North America (22%) and only 9% accounted for European translocations. Africa and South America together represented less than 1% [7]. However, this account is possibly biased towards pathogens of aquaculture species due to limited knowledge of wild fish pathogen fauna. The strong correlation between source of host and source of pathogen indicates that aquaculture not only facilitates disease emergence but also may act as a source of pathogen introduction. In addition, there are well-established examples of the movement of live fish for farming resulting in disease translocation (discussed in detail in Section 4). The link between movement of live fish and translocation of pathogens might become more obvious when developments in sampling protocols and diagnostic techniques enable better characterisation of emerging infectious pathogens [1]. Many believe that intensive aquaculture conditions such as high stocking densities, accumulation of waste, handling, and poor water quality all serve to compromise immunity and favour disease emergence [7]. Recent increased awareness of potential disease transfer from aquaculture farms to wild ecosystems originates from the great discrepancies between the high prevalences of infection in farmed fish when compared to apparently low prevalences in wild populations. The introduction and establishment of animals into a new geographical region (biological pollution), often through human involvement, can introduce novel pathogens (pathogen pollution) to the native fauna. When an introduced host acts as a reservoir population from which infection can ‘spill-over’ to sympatric wildlife, pathogen pollution which would otherwise fail to persist instead underpins the emergence of disease in na€ıve populations. A recent example is the introduction of topmouth gudgeon (Pseudorasbora parva) into an English fish farm. This fish is a host for the rosette-like agent [1], an intracellular eukaryotic parasite and has now escaped into the connected river system, with the potential to introduce the pathogen to na€ıve native wild populations. Whirling disease caused by the myxozoan parasite Myxobolus cerebralis is another example of spill over (spill-back) that shows aquaculture not only as a revealer of diseases but also principally as a source and dispersal mechanism. Trade in ornamental fish, with its large taxonomic diversity of species, raised or captured in natural environments from geographically widespread origins, remains a potential source of pathogen pollution, especially in areas where the water temperature is conducive to the survival of exotics. Their real contribution to the introduction of pathogens is largely unknown as they are not subject to specific sanitary surveillance in Europe [7,8]. Although there are numerous examples of disease emergence after species introduction, there are undoubtedly many more that have not been identified. Epidemics in the wild that cause high mortality or changes in species behaviour are easily characterised, but less easily identified when they cause long-term gradual population declines. It is relatively complex to link fish population decline and pathogen infection in wild populations because diseased or dead animals are rapidly destroyed by predators or necrophages. This is one of the reasons why the impact of an introduced pathogen might very
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often go unnoticed. However, it is only with a clear understanding of the impact of pathogen pollution on wild fish population that risk assessment policies [8] can be properly adapted to prevent disease outbreaks and preserve biodiversity. Few examples of the impact of pathogen introduction on wild fish population exist [7]. Some of the most convincing cases are the impact of Anguillicola crassus on eel (Anguilla anguilla) populations in Lake Balaton, the impact of a ciliate parasite Ichthyophthirius multifiliis on a pupfishes species (Orestia sp.) population in Lake Titicaca where the link between the ciliate introduction and the mass mortalities of fish was established after 30 years and finally, the impact of the monogenean parasite Gyrodactylus salaris on Norwegian Atlantic salmon (Salmo salar) populations. The cost of global biodiversity loss due to disease is yet to be assessed; however, an economic cost is associated with introduced species and emerging infectious diseases in wildlife. For the United States alone this cost has been recently estimated at more than $137 billion per year [9]. 2. Pathogen detection Routinely, the presence of a pathogen in a population will be detected based on clinical signs shown by infected specimens, but recent research has shown that the host specificity as well as the level of virulence of certain pathogens could be extremely variable [1]. For particular pathogens, the range of possible hosts across various taxonomic groups is unknown and therefore contributes to the difficulty in their detection. Also, the detection of healthy carrier or sub-clinical carriers is not done systematically and the techniques or means set up for the diagnosis are not always sensitive enough for routine detections [1]. This highlights the complexity of legislating on the import of live fish with a multiple host-species scenario [8]. Advances in diagnostic methods have considerably altered the level of perception of pathogens and diseases; this has notably influenced health legislation and is likely to result in the review of measures to reduce introductions. The recent findings on the carrier of the rosette-like agent [1] highlight the limitations of the screening programmes currently used internationally to detect pathogens in carrier fish populations. Although the minimum detection limits of molecular tests are very low, it is only one factor involved in the detection of a carrier population. Other factors, such as the prevalence of carrier fish within the population, the concentration of the pathogen within the fish and the amount and type of tissue sampled play a very important role in the ‘sensitivity’ of the sampling scheme [10]. Often these other factors are forgotten and the lack of pathogen detection is associated to a pathogen free population. In cases where carrier states are suspected and difficult to detect and there is no good medical history to corroborate mortality events, regulators may advise the use of more conventional methods such as cohabitation studies with susceptible species, stress testing, or antibody tests for assessing the health of populations. The drawback to these techniques is the cost; however, the benefits may outweigh the costs if pathogen transfer is prevented.
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Nevertheless, the detection of pathogens calls for ever more sophisticated identification techniques. Developments in molecular biology have led to rapid growth in new diagnostic methods (e.g. polymerase chain reaction, amplification of nucleic acids, restriction enzyme digestion, probe hybridisation and nucleotide sequencing). These techniques have lower detection limits and are considered more rapid than the traditional methods such as culture, serology and histology; however, they do not address the limitations of sampling carrier populations. Carrier populations generally have low numbers of infected individuals, and those infected have low levels of pathogens. In some cases (i.e. herpes viruses) the target tissue in carrier fish is not clearly known. Even with the use of molecular diagnostic tests it is sometimes difficult to detect carrier populations without extensive testing, which is not economical. One recent example of where routine testing of fish from carrier populations did not detect the pathogen until a cohabitation study was conducted is that of on topmouth gudgeon [1]. An advantage of molecular techniques when compared to immunochemical and other approaches is the potential to compare pathogen genetically, which has benefited taxonomy, pathogen evolution, pathogenic mechanisms and epidemiology [3]. Aquatic health specialists are able to distinguish between introductions of pathogens and native agents in emergence with increasing accuracy, thus revealing the considerable diversity of pathogens and their hosts. 3. Examples of pathogen establishment in European waters There are numerous reports of the detection of ‘new’ fish and shellfish pathogens throughout Europe [7]. However, most of these are relatively innocuous and most likely reflect the diligence of statutory authorities and research workers involved in aquatic animal health. There are relatively few examples of the introduction and spread of pathogens that either were already well recognised as serious pathogens or have become so (Table 1). This section provides some examples of such pathogens which have resulted in serious disease in wild or farmed stocks. Crayfish plague is the best known example of the spread of an infectious aquatic disease infecting freshwater Crustacea. The oomycete fungus Aphanomyces astaci causes the disease. Native crayfish species throughout Europe are highly susceptible to this pathogen which has eradicated populations in affected areas. The spread of crayfish plague, from initial outbreaks in Italy in the 1860s to many European countries, was described by Alderman [11]. It is thought that the plague was introduced into Europe via imports of North American signal crayfish which are naturally resistant to the pathogen. Subsequently, commercial transfers of crayfish and natural migrations facilitated the spread of the plague. This disease remains of concern and is notifiable to the ‘‘Office Internationale des Epizooties’’ (OIE). Proliferative kidney disease (PKD) of salmonids caused by the myxozoan parasite Tetracapsuloides bryosalmonae is one
amongst the most important diseases affecting cultured salmonids in many European countries as well as in North America [12]. The parasite causes significant economic loss in rainbow trout farms and affects wild salmonid, although the impact on wild populations is unclear. The first reports of proliferative kidney disease were from Germany at the turn of the twentieth century and reports of the disease increased throughout Europe as salmonid aquaculture expanded. However, it is now recognised that the parasite is a natural host of freshwater bryozoans and that the stages released from the bryozoans are infective to fish [13]. It is thought that the parasite can be spread naturally by waterfowl vectors [12], dispersing infected bryozoan statoblasts trapped in their feathers which give rise to new colonies when deposited in new water bodies. Water bodies lacking susceptible fish species have been shown to harbour infections in bryozoan colonies. Introduction of salmonids to these areas has resulted in disease. Whether salmonids can release stages infective to bryozoa, thereby increasing pathogen concentration in the environment, has yet to be confirmed. Recently the discovery of a disease agent implicated in the decline of the cyprinid fish the endangered sunbleak Leucaspius delineatus [1] has highlighted the potential for the spread of fish pathogens by colonisation of invasive fish species and commercial activities. The pathogen, currently referred to as ‘rosette-like agent’ (RLA) is similar if not identical to Sphaerothecum destruens affecting North American salmonids. The pathogen causes a chronic disease which prevents spawning of wild fish such as L. delineatus. The decline of L. delineatus across Europe appears to be linked to the spread of P. parva which originated from China during the 1960s. P. parva appears to be a healthy carrier for the pathogen and susceptible species held in the same water as carrier infected with the rosette-like agent exhibits spawning inhibition, emaciation and eventually dies. Further work is required to determine the distribution of the pathogen in Europe, transmission mechanisms and potential threats to other fish species. A number of bacterial pathogens have similarly come to prominence through their recognition as disease agents in aquaculture situations, but which also have affected wild fish, notably bacterial kidney disease (Renibacterium salmoninarum) and furunculosis (Aeromonas salmonicida sub sp. salmonicida). Bacterial kidney disease was first reported in wild salmon in Scotland in 1933 and soon afterwards in cultured fish in North America. It has a very wide geographic distribution, effectively having been found wherever susceptible salmonids are farmed with the exception of Australasia. Bacterial kidney disease has been spread through the movement of live fish and gametes (it is vertically transmitted) for aquaculture. Furunculosis, caused by A. salmonicida, is thought to have been introduced into the UK in the 1920s with imported trout [14]. It caused disease and mortality in wild salmonids in the UK [15]. The disease spread to Norway on two occasions, with live salmon exports from Denmark and Scotland [16]. Shellfish diseases have also shown their ability to spread via anthropogenic intervention and two of the most important are notifiable disease within the European Union. Marteilia
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Table 1 Examples of important transboundary diseases of farmed fish Disease
Susceptible species
Country where introduced
Year
Potential route
Viruses Infectious haemopoeitic necrosis White spot virus of shrimp Pilchard herpes virus Sleeping disease Koi herpes virus
Salmonids Shrimps (Penaeus spp.) Pilchards (Sardinops sagax) Rainbow trout (Oncorhynchus mykiss) Carp (Cyprinus carpio)
Europe Asia and Americas Australia UK Japan
1976 1990s 1995 2002 2003
Fish eggs Live crustacean Fish carcasses Fish carcasses Live fish
Bacteria Red pest (Listonella anguillarium) Furunculosis (Aeromonas salmonicida) Gaffkaemia (Aerococcus viridans)
Eels (Anguilla spp.) Salmonids European lobster (Homarus gammarus)
Japan and US UK Europe
1780s 1920s 1978
Live fish Live fish Live lobsters
Fungal infections Crayfish plague (Aphanomyces astaci)
European crayfish (Astacus fluviatilis)
Europe
1865
Live signal crayfish
Coarse fish Salmonids Native European oysters (Ostrea edulis) Atlantic salmon European eel (Anguilla anguilla)
Europe US France and Spain
2005 1960s 1970s
Live fish Fish carcasses Live oysters
Norway Europe
1973 1980s
Live fish Live fish
Parasites Rosette-like agent Whirling disease (Myxosoma cerebralis) Bonamia oestrae Gyrodactylus salaris Anguillicola crassus
refringens, a paramyxean parasite has caused mass mortalities in the European flat oyster Ostrea edulis since its discovery in France in the 1960s where it caused significant economic loss [17]. Subsequently the disease occurred in Spain and The Netherlands. Movements of shellfish appear to have been the principle mechanism of spread. However, there is strong evidence that the parasite requires an intermediate host (possibly the copepod Paracartia grani). Bonamiasis caused by the haplosporean parasite Bonamia ostreae is another disease of O. edulis which has caused significant losses to the European aquaculture industry. Other intracellular ‘microcell’ parasites cause similar diseases in bivalve molluscs elsewhere and are regarded as major threats to oyster stocks around the world [18]. B. ostreae is thought to have reached Europe via introduction of infected O. edulis from North America with the first disease outbreaks occurring firstly in France in 1979 and spreading to neighbouring countries over the following decades, reaching the United Kingdom and Ireland. The source of infection and whether there is an intermediate host for the parasite are currently unknown. G. salaris, a freshwater, monogenean ectoparasite, is one of a number of gyrodactylids that infect salmonids. The parasite was first described as a commensal parasite of Atlantic salmon in Sweden [19]. However, when the parasite was introduced into Norway in the early 1970s with the importation from Sweden of juvenile salmon for aquaculture, its impact was dramatic [20]. Atlantic salmon in Norway (Atlantic strains of Atlantic salmon) appeared to be considerably more susceptible to G. salaris, compared with their Baltic cousins (Baltic strains of Atlantic salmon) [19]. In susceptible strains of salmon, reproduction is unchecked by an immune response and death normally results. G. salaris feeds by removing plugs of flesh, which results in secondary infections and compromises osmoregulation. The parasite has been introduced into a total of 45 Norwegian rivers,
mainly through the movement of salmon for farming [20]. The distribution of G. salaris in Europe is unknown but it is likely to be widespread due to the movement of rainbow trout from Finland [16]. G. salaris is arguably one of the most important disease threats to Atlantic salmon populations outside of the Baltic watershed. 4. The impacts of introduced microbial pathogens on wild fish populations Few studies have been conducted on the impact of pathogens on free-living hosts. Furthermore, the number of studies examining the role of disease on structuring fish populations is even more limited, in particular in relation to introduced pathogens. Those pathogens that are studied tend to be ones that impact immediately and negatively on host population dynamics, usually in the form of epidemics. A number of examples in the literature that have shown that pathogens can have a significant and deleterious effect on fish populations, but these have tended to be very localised and are often associated with a combination of adverse environmental conditions. Since disease can act not only directly through mortality events but also indirectly (e.g. reduced fecundity, alterations in host behaviour, reductions in swimming speeds, and increased risk of predation [21]) the total impact can be difficult to assess. Additionally, it would be expected that ‘‘diseased’’ individuals would be quickly removed from the ecosystems, thus providing an underestimate on the role of disease in structuring populations. Intuitively it would be expected, given the plethora of information on diseases in aquaculture, that diseases would have an impact on fish populations. However, the influence of disease on population structure has rarely been considered in the management of fisheries, which may in part be due to the lack of
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examples of diseases in wild fish and an overemphasis on the role of stressors in captive fisheries compared with those present in wild fisheries. Arguably, one of the most studied infections of farmed and wild fish is whirling disease caused by the myxozoan M. cerebralis. Originally described from Europe in 1898 [22], it is now recognised as a major pathogen of North American salmonids, in particular Oncorhynchus mykiss. Its translocation from Europe and its subsequent establishment in the USA demonstrates the importance of understanding the fauna of hosts in their natural environment and the impact of moving these apparently innocuous pathogens into new and na€ıve environments and hosts. Unfortunately, even with such an extensively studied pathogen, the true effect on populations remains unclear. Despite the number of studies, there is still uncertainty about the complex interactions between host, pathogen and environment, which constrains the development of management strategies to control the parasite in wild fish [22]. In addition, there is a lack of absolute and clear evidence that the parasite can impact on all populations [22]. This may be due to differences in host susceptibility, variations in exposure routes and doses and environmental conditions prior to and after introduction of the parasite. Indeed, the apparent lack of statistical and mathematical models that clearly demonstrate a correlation between disease severity and population declines gives cause for concern. Two other major pathogens of concern in wild salmonids are T. bryosalmonae and G. salaris, both of which have been implicated in population declines. Native salmon parr population density was reduced to approximately 50% 2 years after the introduction of G. salaris into Norwegian rivers and after 7 years, salmon parr density was as low as 5% [20]. Subsequent reductions in migrating smolts have led to reductions in returning adult salmonids in subsequent years and thus severe population declines. Proliferative kidney disease is recognised as a pathogen of farmed salmonids, causing upwards of 40% mortality on a farm, but its role in population success has been, until relatively recently, less well defined. It is known that the severity of PKD infections is exacerbated by poor water quality [23]. Moreover, recent findings indicate unequivocally that a combination of poor water quality and the presence of PKD was responsible for reductions of brown trout populations in Swiss rivers. A major issue in determining the impact of microbial pathogens on population diversity is that most publications do not consider the community per se when examining diseases. The impact of any disease is usually considered singularly and over a short period of time. Mortality is usually the outcome measured and body condition, fecundity, swimming and other host behaviour are seldom examined over a long period of time. Establishing the multiple interactions between environment and pathogens is also difficult to achieve. Furthermore, the effect of the loss of, or reduction in, numbers of individuals from that population on the wider community structure is often not considered. Future studies should seek to consider the role of disease on individuals, populations and communities. The types of studies required for assessing the role of pathogens on aquatic biodiversity are difficult to accomplish because
they require the study of populations over long periods of time, multiple watershed for comparisons, and are therefore very expensive. The introduction of a non-native pathogen into a population with low genetic variation has rarely been considered outside of aquaculture facilities. Such effects can have catastrophic consequences. Heterozygous populations are often better able to contend with any new or existing disease threat than homozygous populations, which are at greater risk of extinction from an introduced pathogen. Hedrick et al. [24] showed that inbred populations of the endangered Gila topminnow Poeciliopsis occidentalis occidentalis were at greater risk of extinction when exposed to Gyrodactylus turnbulli when compared to a heterozygous population. Whilst such events would appear detrimental to host populations, parasites themselves may preferentially infect host populations with low levels of genetic variation [25]. Irrespective of whether or not microbes are detrimental to their native host in their normal range, it is important that the microbial fauna of the introduced host species is characterised and any potential impacts on the communities of the receiving ecosystems are considered prior to any movements into that system. 5. Theory and risk assessments Theoretical studies of the impact of microbial pathogens on fish populations encompass mathematical disease models (deterministic or stochastic) and risk modelling. Models provide a method to conceptualise complex systems and an environment in which to examine interactions; they are, therefore, appropriate to the study of the impact of microbial pathogens on the diversity of fish populations. In the field of aquatic animal health, mathematical models have been used to study the epidemiology of sealice: Lepeophtheirus salmonis [26] and Caligus elongatus [27]. Models of larval lice production in Norwegian [28] and Scottish [29] waters have demonstrated that a very large proportion of larval lice originate from farmed fish, substantially altering sealice epidemiology, compared with the pre-aquaculture period. Other diseases which have been investigated by modelling include the impact of bacterial kidney disease [30] and furunculosis [31] on chinook salmon (Oncorhynchus tshawytscha) populations and epidemics of pilchard herpes virus in Sardinops sagax along the Australian coast [32,33] and Ichthyophonus hoferi (a mesomycetozoan disease) in herring (Clupea harengus) [34]. Two theoretical papers have produced generic models for the impact of disease on wild salmon populations [35,36]. During a disease outbreak it is possible that the high replication rate of the pathogen favours the evolution of a more virulent strain [11]. Not only this could be the source of a novel pathogen into a na€ıve population but also it could result in a larger effect on biodiversity. Theoretical models of the evolution of virulence have been developed [4,37] and can be incorporated into models to estimate the impact of disease in wild populations.
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In risk analysis terminology, risk is defined as both the probability and consequences of an adverse event (e.g. pathogen introduction) and, therefore, consequence assessment is an important element of the process. The use of risk assessment in aquatic animal health has largely been restricted to investigating disease transmission and, in particular, transboundary spread (i.e. import risk analysis e IRA). A review of the ‘import risk analysis’ found that the consequence assessment was frequently omitted or highly restricted in scope and depth. Mathematical modelling needs to be used for consequence assessment for significant progress in estimating the likely ecological impact of disease introduction to be achieved. Theoretical studies have been used to study the impact of endemic diseases (e.g. bacterial kidney disease) and epidemic (e.g. pilchard herpes virus) diseases on individual wild fish host populations. The integration of epidemiological and ecological models is required to extend studies of single populations to the level of the fish community and, therefore, diversity. In addition to methodological constraints, the further application of theoretical approaches is limited by a lack of epidemiological data. 6. Effect of climate change Climate change will influence the effect of microbial pathogens on fish populations. Firstly, increasing water temperatures will change the geographic distribution of marine species, with potential disease consequences. In freshwater, increasing water temperature will increase the ability of exotic fish species, introduced into Europe as a result of international trade, to establish and spread, thereby increasing the probability that pathogens spread to native fish populations. In addition, some introduced pathogens, such as koi herpes virus, may survive better and exert greater impact at higher water temperatures. A change in climate will also affect the epidemiology of endemic diseases. The incidence and geographic range in Europe of Lactococcus garvieae have increased in recent years as the water temperature has risen. There is evidence from Switzerland that the prevalence of proliferative kidney disease in wild grayling (Thymallus thymallus) increased with water temperature. Furthermore, increases in temperature may affect the behaviour of native species and result in exposure to pathogens that would not necessarily have been exposed to. Assessing the likely influence of climate change on disease epidemiology will inform the development of policies to mitigate its impact on fish diversity. 7. Discussion and conclusion This review has assessed how microbial pathogens may affect the diversity of fish populations in Europe. The role of aquaculture and the translocation of fish species have been highlighted. Whilst aquaculture has been practised for more than 2000 years, and movements of live fish have taken place for almost as long, the rapid expansion of fish farming over the last 40 years, in terms of volume, number of species and geographic location, has been accompanied by significant
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international movements of live fish [8]. In addition, the demand in the West for fish as companion animals creates large-scale movements of warm and coldwater ornamental fish. This review clearly demonstrates that introduced pathogens and parasites, invariably associated with live fish movements, have affected the diversity of wild fish populations. Macroparasites provide the best examples: the impact of G. salaris on Atlantic salmon in Norway and A. crassus in European eels. Some will argue that the threat of transboundary diseases based on the precautionary principle should lead to the restriction of free trade in aquatic animals and their products. However, this would be contrary to international trade agreements. The Sanitary and Phytosanitary Agreement of the World Trade Organisation offers a middle way. A country can impose measures over and above those set out in international agreements, if supported by an import risk analysis (IRA). In this review it is argued that methodological developments in IRA, notably the application of mathematical modelling, are needed to ensure that the potential impact of microbial pathogens is properly assessed. IRA will always be limited by our ability to identify hazards as hazard identification for many aquatic animal pathogens is constrained by the lack of data. An IRA of Atlantic salmon smolts to Norway from Sweden in the early 1970s would probably not have identified G. salaris as a hazard. The problem of unidentified hazards has led some to argue that, using historical data, an estimate of the likelihood of an unidentified hazards could be calculated and included in a commodity IRA [38]. Biosecurity Australia have considered linking undiagnosed mass mortality incidents in cultured bivalve molluscs, which occur quite regularly, to known hazards to improve the hazard identification process. Compared with exotic pathogens, there is less evidence of endemic microbial pathogens influencing the diversity of fish populations. However, the problems of detecting demographic and genetic impacts in wild fish populations are severe. It is likely that studies reviewed would not have been able to detect subtle influences of pathogens on population diversity. A greater use of mathematical and statistical modelling approaches is needed to improve our ability to detect the impact of disease in wild fish populations, and to improve the design of future surveys. The aquaculture industry, governments and international organisations have the shared responsibility to ensure that aquacultural development causes minimal environmental impact. Inevitably, transfers of live fish will continue, therefore, it is crucial that IRA methodology is developed so that potential disease hazards are reliably identified and the consequences of disease introduction adequately assessed. The expansion of fish farming, either in new geographic areas or by bringing new species into farmed production, must be carefully evaluated for its potential environmental impacts. Inevitably, the majority of fish farming will operate in open systems that allow interaction with wild populations, therefore, minimum biosecurity levels should be established to minimise the risk of escapes and pathogen transfer to the wild. Assessments of the risks associated with live fish movements and aquaculture must be securely based on scientific evidence.
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