SOCIAL, ECONOMIC AND BIODIVERSITY IMPACTS OF EPIZOOTIC ULCERATIVE SYNDROME (EUS)

J.H. Lilley¹, R.B. Callinan² and M.H. Khan³

¹Institute of Aquaculture, University of Stirling
Stirling FK9 ⁴LA, Scotland, UK

²Regional Veterinary Laboratory, Wollongbar Agricultural Institute
Wollongbar, NSW 2477, Australia

³Bangladesh Fisheries Research Institute
Mymensingh-2201, Bangladesh

Lilley, J.H., R.B. Callinan and M.H. Khan. 2002. Social, economic and biodiversity impacts of epizootic ulcerative syndrome (EUS). p. 127-139. In: J.R. Arthur, M.J. Phillips, R.P. Subasinghe, M.B. Reantaso and I.H. MacRae. (eds.) Primary Aquatic Animal Health Care in Rural, Small-scale, Aquaculture Development. FAO Fish. Tech. Pap. No. 406.

ABSTRACT

Few surveys have been conducted that accurately assess the impacts of epizootic ulcerative syndrome (EUS) on fish populations and associated fishing communities. A review of past information on the disease is hampered by the fact that a pathology-based diagnosis of EUS was not used in most studies prior to 1994, and many accounts of ulcerative fish diseases in Asia may be unrelated. Data from the Bangladesh Flood Action Plan 17 (FAP17) Project, from October 1992 to March 1994, showed that 26% of 34,451 freshwater fish examined had lesions of some sort. A recent cross-sectional survey in Bangladesh revealed that 80% of 471 fish with lesions sampled from 84 sites were diagnosed as EUS-positive. This indicates that studies of EUS in Bangladesh that just examined fish with lesions were not grossly overestimating the prevalence of the disease.

Outbreaks of EUS have subsided in many areas, but new occurrences are being reported in previously unaffected areas and in newly developed farming and fisheries management systems. There is recent evidence that EUS does not always occur in seasonal outbreaks or always cause high mortalities, but may be prevalent at low levels throughout the year. It may, therefore, have an effect on productivity that cannot be measured in terms of mortalities alone. Communities that are heavily dependent on local fisheries have been affected by outbreaks of EUS. Social impacts may extend beyond persons directly affected by fish losses. Estimates of direct economic losses due to EUS-caused mortalities in several affected countries are given, and further estimates are calculated from recent survey data; however, losses due to lowered productivity may be of greater significance. Reduced aquaculture and fisheries production can be demonstrated during times of serious EUS outbreaks, although it cannot be positively determined that EUS was the factor that caused the decline. Anecdotal evidence suggests that during times of severe outbreaks highly susceptible species may be difficult to locate. The long-term effects on aquatic ecology have not been investigated.

INTRODUCTION

There is a great deal of anecdotal information on outbreaks of epizootic ulcerative syndrome (EUS) and extrapolated data on EUS-related losses, but relatively little survey data that provide actual randomised counts of mortalities or of fish with lesions. Even fewer studies have defined the lesions caused by EUS and confirmed the diagnosis in each case, or in a proportion of cases. Scientists at the Aquatic Animal Health Research Institute (AAHRI) in Bangkok, Thailand, the only diagnostic reference laboratory for EUS approved by the Office International des Épizooties (OIE), define an EUS case as: a fish with necrotising granulomatous dermatitis and myositis associated with hyphae of Aphanomyces invadans. This is a slightly modified definition of that given in Roberts et al. (1994), and requires processing of histological preparations with haematoxylin and eosin (H&E) and Grocott's stain in order to make a positive diagnosis (OIE 2000).

The severity of EUS outbreaks has subsided in many areas, but there remain occurrences of lesions on fish that do not fit with the conventional view of EUS, as they are not associated with large-scale fish kills. Nonetheless, a cross-sectional survey in Bangladesh conducted during the winter of 1998-99 revealed that 80% of 471 fish with clinical lesions, sampled from 84 sites, were diagnosed as EUS-positive (Khan and Lilley 2001). This indicates that EUS is still the largest cause of lesions on freshwater fish in Bangladesh, and that studies that just examined fish with lesions were not grossly overestimating the prevalence of the disease.

A review of some previous EUS surveys in Bangladesh is given here, indicating whether a diagnosis fitting with that given above was provided. These surveys give information on the social, economic and biodiversity impacts of EUS at that time.

EUS PREVALENCE SURVEYS IN BANGLADESH

The Bangladesh Flood Action Plan 17 Fisheries Studies and Pilot Project (FAP17 1995) accumulated data on the occurrence of lesions on about 35,000 wild freshwater fish. Summary of this data (Figs. 1-5 and Table 1) demonstrates a surprisingly high prevalence of lesions on these fish. More than half of the fish examined comprised the whole population of fish in the water body, which eliminates the danger of selecting sub-samples of less healthy fish (Fig. 1). Whole population samples had only a slightly lower percentage of lesions (24%) than population sub-samples (28%).

The higher occurrence of lesions in winter (Fig. 2), and on species that are generally considered to be most EUS-susceptible (Table 1), provides further evidence that the lesions are predominantly the result of EUS infections. The prevalence data on individual species (Table 1) equate well with unpublished data collected by M.H. Khan and co-workers on species affected during the 1998-99 winter period. The latter study confirmed which species were EUS affected.

The FAP17 database includes comments on the severity of the infections in each sample. These were coded from X (mild) to XXXXX (severe lesion), and the average severity is given in Table 1. Again, the most affected species were those recorded as highly susceptible to EUS (e.g., Puntius spp., Channa spp. and Mastacembelus spp.). It is interesting to note any differences in susceptibility within genera for fish that are being considered as candidate species for aquaculture development. For example, Puntius terio is listed as one of the worst affected species, whereas no lesions were recorded on any P. phutuio sampled.

Some regional differences in the occurrence of lesions are given in Figure 3, although these cannot be accounted for by flooding or the other risk factors considered. Variations in lesion occurrence between habitat (Fig. 4) support findings by Khan and Lilley (2001) that EUS is less likely to occur in actively flowing waters.

Table 1. Prevalence of lesions on 34,612 wild fish in Bangladesh (calculated from unpublished FAP17 survey data 1992-94, arranged in order of % with lesions).

As with the whole- versus sub-sample analysis (Fig. 1), the fish that were collected using less selective fishing methods (e.g., seine net) had a lower prevalence of lesions than fish collected using methods that were likely to select for weaker fish (e.g., spear, scoop net) (Fig. 5).

FAD = fish aggregation device.

A study of the prevalence of EUS in three floodplain areas was undertaken by Subasinghe and Hossain (1997) using a histological diagnosis of the disease (see Box 1). They showed that prevalence was generally lower in artificially stocked fish sampled from natural waters than in wild fish. It is unlikely that fry reared in hatcheries within Bangladesh pose a significant EUS risk to wild fish, as there are few accounts of EUS in carp hatcheries, and EUS has now been shown to be endemic in natural waterways throughout most of Bangladesh (Khan and Lilley 2001). It is the wild fish themselves that are considered risk factors for EUS. Khan and Lilley (2001) also showed that sites that were artificially stocked showed no significant association with occurrence of EUS.

There has been a decreasing occurrence of EUS in both wild (Box 1) and farmed fish (Box 2) in Bangladesh over the last 10 years. The reduced severity of outbreaks has been even more evident. EUS-affected ponds netted during initial outbreaks commonly revealed that certain fish species were 100% infected, with high rates of mortality (Barua et al. 1991, Ahmed and Rab 1995). These susceptible species now usually show lower rates of infection, and lesions often heal as temperatures rise (M.H. Khan and co-workers. unpubl. data). An ADB/NACA (1995) questionnaire survey of carp farmers in Bangladesh showed that 17% of extensive farmers and 53% of intensive and semi-intensive farmers reported resolution of the EUS problem from 1992-95 (see Tables 2 and 3). Similarly, Hossain (1998) reported that 85% of Thana Fisheries Officers (TFOs) indicated that the general aquatic animal disease situation improved from 1994-96, and that 91% of the TFOs indicated an improvement from 1996-98.

Table 2. Losses in semi-intensive and intensive carp farms reporting EUS from 1992-95 (source: ADB/NACA 1995, M.J. Phillips pers. comm).¹

Table 3. Losses in extensive carp farms reporting EUS from 1992-95 (source: ADB/NACA 1995, M.J. Phillips pers. comm).¹

PRESENT STATUS OF EUS

Although EUS outbreaks have subsided in Bangladesh and other areas, new occurrences are being reported in previously unaffected areas, and in newly developed farming systems and fisheries management systems. A summary of recent outbreaks is given in Box 3.

The recent outbreaks show that EUS is not always strictly seasonal, or always causes high mortalities, but may be prevalent at a low level throughout the year. It may, therefore, have an effect on productivity that cannot be measured in terms of mortalities alone.

This year, several occurrences of EUS in juvenile giant gourami and climbing perch in Thailand have been confirmed at AAHRI. These have occurred at times outside the usual "EUS season."

EUS in Australia remains an important issue in estuarine wild fish and in cultured silver perch (Bidyanus bidyanus) in New South Wales, Queensland and the Northern Territory. The disease has occurred almost all year round and at prevalences of 20-90% in farmed silver perch (R.B. Callinan, unpubl. data).

In 1998, EUS occurred for the first time in the Philippine island of Mindanao (J. Albadladejo unpubl. data) Earlier, in January 1996, there was up to 30% prevalence in EUS-susceptible fish from both Laguna Lake and Mangabol Swamp in central Luzon.

SOCIAL IMPACTS

Communities that are heavily dependent on local fish catches have been most affected by outbreaks of EUS. For example, 10,650 fishing families are dependant on fisheries production from Batticaloa Lagoon in eastern Sri Lanka, and any fluctuations in catch levels have a severe socio-economic impact on the local community (P. Vinobaba, S.T. George and N. Kandasamy unpubl. data). Disease outbreaks have occurred in the lagoon in 1989, 1993 and 1994, and Vinobaba and Vinobaba (1999, and unpubl. data) clearly demonstrated EUS mycotic granulomas in samples of a number of lagoon fish species. P. Vinobaba and colleagues (unpubl. data) suggest that flooding and agricultural run-off may be risk factors for disease. They believe that there is an urgent need to protect and develop fisheries resources in Batticaloa District, which has 168,300 ha of inland waterways, and should be capable of sustaining the local communities.

Similarly, Laguna Lake and Mangabol Swamp in Luzon, Philippines support capture fisheries and pond and cage aquaculture. Some 75,000 people depend on fish from these areas as a source of food and income. EUS first occurred in Laguna Lake in 1985, and by 1992, the disease was considered the most important factor determining the size of the fish harvest. In 1989, over 50% of the harvest of susceptible fish was lost due to EUS; and in 1990, over 40% was lost (R.B. Callinan unpubl. data).

In Kerala State, India, Kurup (1992) reported that between the first appearance of EUS in August 1991, and by April 1992, the disease had caused serious loss of income to 25,000 full-time and 7,000 part-time fisherfolk.

Bhaumik et al. (1991) surveyed the effects of EUS on fish producers, traders and consumers in West Bengal (see Box 4). Virtually all of the farmers interviewed (97%) were allocated as having "marginal" or "small" farms. Of the EUS-affected farms, 48% were low-input traditional farms, compared to 35% that were described as "semi-scientific" and 16% as "scientific" farms.

The effect of EUS on traders and consumers was skewed towards poorer rural communities. A higher percentage of people from rural areas (53%) preferred the more susceptible snakehead and "miscellaneous fish species" compared with 18% of urban dwellers. Fewer rural people were able to eat fish often, but after an EUS outbreak, demand for fish was not much reduced in rural areas, largely because prices were reduced (Box 4). Similarly, despite high consumer resistance to diseased fish, they were more likely to be bought in rural areas. Das and Das (1993) reported that women fish vendors suffered particular hardship after EUS outbreaks and often had to seek alternative employment.

In contrast to the above situations, other communities that do not rely heavily on susceptible fish have not been badly affected by EUS outbreaks. For instance, snakehead and other wild fishes in Punjab, Pakistan are not widely fished for local consumption. Of the freshwater fishes that are eaten in Pakistan, the preferred species are usually EUS-resistant common and Chinese carps.

The social impacts of EUS may extend beyond persons directly affected by fish losses. For example, one of the main constraints to aquaculture development in Nepal is an ongoing fear of disease, largely a result of previous EUS outbreaks. People are reluctant to start aquaculture activities due to the perceived high risk of disease and a lack of knowledge of how to deal with fish disease (Callinan et al. 1999). Conversely, Little et al. (1996) noted that in Thailand, the decimation of wild fish stocks, particularly snakehead, due to EUS in the early 1980s, was a major stimulus to the culture of herbivorous fish.

In Thailand, a questionnaire survey of snakehead farms is being undertaken to determine the present impacts of the disease. Mortalities in intensive snakehead culture accounted for most of the recorded economic losses due to EUS in Thailand in the 1980s. It is suspected that losses are currently not high, but one early reply stated that the farmer had given up the business due to disease problems in 1994, when significant EUS outbreaks occurred.

With regard to control of diseases in rural aquaculture, managing the risk of disease is usually a cheaper and more effective means of control than treatment. Gopal-Rao et al. (1992) pointed out that in Andhra Pradesh, an average of 10% of the production cost is spent on disease treatment. They called for an integrated approach to fish health by combining management techniques with chemotherapy.

ECONOMIC IMPACTS

Published estimates of direct economic losses due to EUS mortalities in several affected countries are listed by Lilley et al. (1998). Further estimates of economic loss during early outbreaks in Bangladesh are given by Hossain (1993), who reported that the 1988 EUS epizootic caused an average loss in each district of Taka (Tk) 405,960 (US$8,300); and by Collis (1993), who recorded the loss of 18 mt of fish at Tk 430,000 (US$8,800) from 240 ponds in six thanas between 1991-93. More recent estimates of the economic loss to carp culture in the region are given in a revised edition of the ADB/NACA (1995) data and are listed in Tables 2 and 3. Projecting future losses, the most conservative estimate of the cost of fish losses due to EUS in Australia, the Philippines and Indonesia until the year 2027 has been calculated at US$63 million (ACIAR 1998).

Freshwater aquaculture in Asia is generally not a major foreign exchange earner, and production is mainly for local or domestic consumption. Therefore, the more significant impacts of EUS on local micro-economies are probably not reflected within economic loss data.

As EUS lesions in most affected areas do not appear to be causing mortalities on the scale of previous outbreaks, it may also be the case that economic loss due to lower productivity is of greater significance than direct mortalities. A survey in Andhra Pradesh in the early 1990s combined the effects of disease-induced growth loss with mortality, in an estimated annual loss due to disease of 40 million Indian rupees (US$860,000) (Gopal-Rao et al. 1992).

There are further concerns for the future, as several countries in the region attempt to diversify the species used for aquaculture to include fishes known to be susceptible to EUS. For example, snakehead culture is being developed in southern India, and the associated dangers of EUS should be considered during this process (Callinan et al. 1999).

BIODIVERSITY IMPACTS

The idea that a pathogenic fungus can have significant biodiversity impacts on aquatic animals is not unique to the case of EUS. A very similar species of fungus, Aphanomyces astaci, devastated European crayfish populations at the end of the last century and, when it hit Scandinavia in the early part of this century, Sweden was transformed from the world's largest crayfish exporter to the world's largest crayfish importer (Swahn 1994). More recently, a chytridiomycete fungus has caused massive population declines and possible extinctions of amphibians. It is considered to be the single greatest cause of amphibian declines in the western hemisphere and Australia (Munkacsi 1999).

Outbreaks of ulcerative mycosis (UM) in the 1980s had a significant impact on the productivity of the estuarine fisheries of the eastern United States (Noga et al. 1988). Recent evidence indicates that the invasive Aphanomyces involved in those outbreaks may be A. invadans, the EUS fungal pathogen (Blazer et al. 1999).

Reductions in aquaculture and fisheries production can be demonstrated during times of serious EUS outbreaks. For example, within the past decade, India showed an increase in aquaculture production in every year other than 1990. Subasinghe (1997) speculated that this might be due to EUS losses in that year.

Data provided by Das (1994) on wild fish landings from the Brahmaputra River show massive declines in EUS-susceptible species at the time of first EUS outbreaks in that water system. Landings of Channa striata decreased by 88%, from 22 mt in 1987-88 to 3 mt in 1988-99, and remained at a similar level until 1991. Catches of Channa punctata declined by 85%, from 30 mt to 5 mt over the same period, and further declined to 3 mt by 1991. Data on one species that is not generally considered susceptible (Gudusia chapra) are given, and this showed an 880% rise in landings, from 0.1 mt to 0.9 mt over the period 1987 to 1989.

Similarly, scientists in Kerala are convinced that populations of susceptible fish have declined as a result of the EUS outbreaks, although no data were given (Callinan et al. 1999). However, it cannot be positively determined that EUS was the major factor that caused these declines in overall fish production.

Anecdotal evidence suggests that during times of severe outbreaks some susceptible species disappeared from fish markets altogether. In Bangladesh, Channa spp., Nandus spp. and Mastacembelus spp. were said to be difficult to locate in 1988-89, but Table 1 indicates that by 1992-94, reasonable numbers were being caught. Puntius sophore, a highly susceptible fish, appears to have been present in large numbers throughout the outbreaks.

CONCLUSIONS

• Randomisation and a pathology-based case diagnosis are essential for disease prevalence studies, and should be employed in studies monitoring EUS prevalence.

• There has been decreased severity and prevalence, but continued widespread occurrence, of EUS in Bangladesh and many other affected areas.

• EUS has continued to affect new areas and new systems.

• In Asia, EUS generally has more significant impacts in extensive, low-input systems and wild fisheries, than in controlled intensive fish culture.

• In South and Southeast Asia, rural traders and consumers are more affected than urban/suburban communities.

• Fear of disease is an important constraint to aquaculture development in some areas.

• Managing risk of disease losses from EUS is usually a cheaper and more effective means of control than treatment.

• EUS has probably affected the diversity of species in certain areas, but the long-term effect of this is unknown.

ACKNOWLEDGEMENTS

The authors thank the Department for International Development of the United Kingdom (DFID), the Australian Centre for International Agricultural Research (ACIAR) and the British Council for their financial support.

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