It is now becoming apparent that many of the introductions and movements of aquatic animals have been responsible for the introduction, establishment and spread of aquatic animal pathogen species (parasites, viruses, bacteria and fungi) into new geographic areas and hosts. Once established in natural waters (and often aquaculture facilities) and hosts, such pathogens are almost impossible to eradicate.
In most cases, fishery managers and governments have not properly considered pathogen transfer when contemplating transboundary movements of aquatic animals, or have been slow to react to such introductions directly by the private sector either with or without approval. With proper planning, it may have been possible to avoid introduction of these pathogens and there now exist a number of international codes of practice and guidelines to assist this process. These include international efforts led by the International Council for the Exploration of the Sea (ICES), Cartagena Protocol of the Convention on Biological Diversity (CBD), the World Organisation for Animal Health (OIE) Sanitary and Phytosanitary Agreement of the World Trade Organization (WTO/SPS), and the FAO Code of Conduct for Responsible Fisheries (CCRF). In Asia, the latest initiative is the FAO/NACA Regional Technical Cooperation Programme (TCP/RAS/ 6714(A) and 9605(A)) “Assistance for the Responsible Movement of Live Aquatic Animals”, which led to agreement on the “Asian Technical Guidelines on Health Management for the Responsible Movement of Live Aquatic Animals” (Global Aquaculture Alliance Web site13; FAO/NACA/ OIE, 1998; Fegan et al., 2001).
Despite the existence of these codes, protocols and guidelines, governments and particularly the private sectors in both Asia and Latin America continue to introduce new shrimp species with limited consideration of potential disease consequences. They have thus generally been caught unprepared by the recent epizootic outbreaks involved with shrimp transboundary movements. Additionally, their immediate responses have been largely ineffective in preventing or reducing disease losses which may exceed US dollars one thousand million/year in direct production losses worldwide and considerably more in total.
Countries that have actively enforced live shrimp importation bans, with some success include:
Direct, involuntary importation of new pathogens with their imported hosts has been shown to be even difficult to quantify, including transfer of new strains of established pathogens specific to the host, the potential for interbreeding with, and displacement of, native species, and unknown effects on the genetic diversity and ecology of native fauna. Each of these has the potential to cause unexpected and far-ranging adverse effects on host populations and commercial and sport fisheries, with accompanying severe socio-economic impacts on human populations.
In some countries, the private sector has adopted so called “better” or “best” management practices (BMPs), which may have contributed to the prevention of on-farm disease problems. Although the state sector has also assisted these efforts through the development of expertise, infrastructure and capacity for health management, shrimp culture and capture fisheries in most countries remain vulnerable to further introductions of transboundary diseases. There is much further work that can be done however, and this report includes recommendations as to what this might comprise.
Little is currently known about the effects of cultured shrimp on wild populations and biodiversity. The fears are that alien cultured shrimp could escape to the wild and then either displace native shrimp populations by out-competing them, interbreeding with them, or killing them through contamination with fatal pathogens (i.e. viruses) to which they are susceptible.
Some of the scant research done in this area has indicated that much of the genetic structure of wild populations appears to reflect historical events on large biogeographical scales, rather than resulting from patterns of present-day dispersal. Benzie (2000) found no conclusive evidence that aquaculture escapees had altered the genetic constitution of wild stocks of P. monodon in Thailand. However, this research was conducted before the introduction of P. vannamei, so the effects of escapees of this species (in Thailand at least) remain unknown.
The escape of P. vannamei from shrimp farms into the surrounding environment can be expected as a result of accidental release during harvesting as well as mass escape during flooding events. Some release from hatcheries may also be expected unless comprehensive measures are taken to reduce escapes. In Thailand, floods in Surat Thani and Pranburi in 2003 for example led to several million P. vannamei escaping to the coastal environment. Not surprisingly, P. vannamei therefore has been reported in fisherfolk's catches on Andaman and Gulf of Thailand coasts. No detailed information on catches is available, but numbers have not been reported as large. There are also no reports from fisherfolk or Thai Department of Fisheries officers that escapes of P. vannamei have led to any perceivable impact on wild shrimp populations in any Thai coastal area. However, further ecological research is needed on P. vannamei in the wild and its impacts on fisherfolk's catches and native species.
Native penaeid shrimp species support fisheries of commercial importance in several Asian countries, and crustaceans and shrimp are also significant in artisanal coastal fisheries.
The main risk would be if competition occurs with native species where P. vannamei occupies the same “ecological niche” or in other ways cause competition for habitat (space), feed or adversely interfere with breeding behaviour or breeding success. If P. vannamei occupies a “vacant” niche (which is unlikely), or the abundance of other shrimp species is limited by other factors, (which is possible), then P. vannamei has the potential to add to shrimp catches. However, if £vannamei does not breed and become established in the wild any impacts are likely to be localized and limited in time.
Some instances of cultured shrimp escaping to and becoming established in the wild are known from the United States of America. Penaeus monodon (originally from Hawaii) were introduced accidentally into the Atlantic coast of the United States of America when they were accidentally released by the Waddell Mariculture Center in 1988. Commercial shrimpers have subsequently captured P. monodon as far south as Florida, although it is not believed to be established in the United States of America (McCann, Arkin and Williams, 1996). Similarly, P. monodon, P. vannamei, P. stylirostris and P. japonicus are all known to have escaped culture facilities in Hawaii, although none are known to be locally established (Brock, 1992; Eldridge, 1995).
Taura Syndrome Virus (TSV) has been documented in wild PL (in Ecuador in 1993) and adult (off the Pacific coast of Honduras, El Salvador and southern Mexico since 1994) P. vannamei. The infected adults showed high mortalities and developed diagnostic lesions from the disease. Thus, viruses such as TSV have been proven to infect and cause mortality in wild shrimp populations, but their effects on commercial penaeid shrimp fisheries remain unstudied and unknown (Lightner and Redman, 1998b).
In the Pacific Islands, P. japonicus has escaped culture facilities, but has failed to become established, although P. merguiensis is known to have escaped and become established in the wild off Fiji (Eldridge, 1995). The effects of this on the wild shrimp populations, however, remain unknown.
If there is establishment of breeding populations of P. vannamei in the wild, then competition with native species will be sustained and the potential for longer-term impacts on aquatic biodiversity in coastal waters will become more significant. The risks of such consequences do exist and suggest the need for great caution.
Despite the fact that the species has been widely introduced, a comprehensive study of the literature carried out for this report and the information available from other countries in Asia and in the Americas did not find any evidence of P. vannamei becoming established in the wild outside of its range (i.e. it may not become an easily “invasive” species). However, there is a need for further field research, as there was insufficient information available on the natural breeding habits of P. vannamei to make any further assessment of this issue, or the degree of potential competition or interaction with native species. Thus, in the absence of good scientific evidence, a precautionary approach should be adopted to Penaeus vannamei farming, if animals are to be introduced.
Penaeus vannamei is tolerant of a wide range of salinities, especially very low salinity. This means that it is currently cultured in both inland and coastal areas. Just as with the farming of other Penaeid species, this raises a number of potential environmental issues. Environmental concerns for P. vannamei culture include potential impacts on: (1) natural and agricultural habitats, caused by poorly sited or managed shrimp farms; and (2) effects of farm effluents on water quality in inland and coastal areas14.
Although there are differences in the locations where P. vannamei and native Penaeid species are farmed, there are likely to be no major differences in the impacts on habitats. In Asia, Penaeus vannamei is commonly farmed in shrimp farms that have previously produced P. monodon. Therefore, no significant new impacts on the habitats of coastal or agriculture areas are anticipated. Although there has been some expansion of P. vannamei into new farming areas, impacts of such farming on the surrounding natural environment is not considered significant, provided adequate measures are taken. As in the case of P. monodon, particular care is essential when culturing P. vannamei in areas with seasonal freshwater. Normal siting practices and good farm management for reducing impacts on surrounding habitats should be followed. Where farms practice limited water exchange, recycling of pond water or use of effluent treatment, then impacts on the surrounding environment can be reduced or eliminated. The trend in farming of P. vannamei in Asia and the Americas is towards the use of limited water exchange and closed or semi-closed farming systems, thus the impacts on the environment are less.
One potentially positive environmental impact of farming of P. vannamei concerns the differences in behaviour and feeding habits compared to P. monodon. Penaeus vannamei spends more time in the water column, and tends not to burrow into the bottom sediment allowing it to be harvested more easily than P. monodon. It is possible to harvest without complete draining of the pond, thereby avoiding the stirring up of poor quality bottom sediments. Harvesting using the non-draining method offers an opportunity to avoid the discharge of harvesting effluent that is high in nutrients and organic matter.
Another significant advantage of P. vannamei is its feeding habits and requirements for lower protein diets compared to P. monodon, which will reduce pressure on fishmeal and fish oil requirements. Penaeus vannamei requires a lower protein (and hence cheaper) diet in culture than P. monodon and is more able to utilize the natural productivity of shrimp ponds, even under intensive culture conditions, and with better feeding efficiency. In Thailand, typical commercial grow-out feeds for P. vannamei contain 35 percent protein and cost 10–15 percent less than the 40–42 percent protein feeds for P. monodon.
More efficient feeding practices and reduction in the use of fish meal can lead to reduced problems of nitrogen discharge and more efficient use of natural feed resources, per unit of production. Nutrient budgets in the literature for P. vannamei and P. monodon culture show that P. vannamei farming makes more efficient use of nitrogen than P. monodon culture, principally due to the lower protein requirements of P. vannamei.
In 1989, six viruses were known to affect Penaeid shrimp, but by 1997 more than 20 viruses were identified as having affected wild stocks and commercial production (Hernández-Rodríguez et al., 2001). The OIE now lists seven viral diseases of shrimp in the Aquatic Animal Health Code (OIE, 2003), which are considered to be transmissible and of significant socio-economic and/or public health importance. These viral diseases are: white spot disease (WSSV), Yellow Head disease (YHV), Taura syndrome virus (TSV), spawner-isolated mortality virus disease (SMV), tetrahedral baculovirosis (Baculovirus penaei - BP), spherical baculovirosis (Penaeus monodon-type baculovirus) and Infectious hypodermal and haematopoietic necrosis (IHHNV) (OIE, 2003; OIE Web site15). All OIE member countries are obliged to report these diseases so that disease spread can be monitored and legislation instituted to prevent disease spread. However, the member countries do not always comply with these requirements.
Penaeus vannamei and P. stylirostris are known to be carriers of the following viral diseases: WSSV, BP, IHHNV, REO, LOVV and TSV. These viruses can be transmitted to native wild penaeid shrimp populations (Overstreet et al., 1997; JSA, 1997; Timothy Flegel, per. com.).
Penaeus monodon are known carriers of: WSSV, YHV, MBV, IHHNV, BMNV, GAV, LPV, LOVV, MOV and REO (Lightner, 1993; Flegel, 2003).
Perhaps the biggest concern to Asian countries already or currently wanting to import P. vannamei is the possibility of introducing TSV. Despite original work suggesting Taura syndrome (TS) was caused by a toxic pesticide, it is now known that a single or perhaps several very closely related strains (mutations) of the Taura syndrome virus (TSV) are responsible for the TS pandemic in the Americas (Brock et al., 1997; OIE Web site). TSV is a single strand RNA virus and hence susceptible to mutations, causing more concern, and is closely related to other insect viruses (Gulf States Marine Fisheries Commission Web site16; Flegel and Fegan, 2002).
Taura Syndrome Virus was first identified from farms around the Taura river in Ecuador in 1992 and subsequently spread rapidly to the whole of Latin and North America within three years. TSV spread first throughout Ecuador and to Peru (1993), Colombia (Pacific and Atlantic coasts), Honduras, Guatemala, El Salvador, Nicaragua, Hawaii, Florida and Brazil (1994), Mexico, Texas, South Carolina and Belize (1995/96) (Brock et al., 1997; Lightner and Redman, 1998; GSMFC Web site), and subsequently Asia including Mainland China and Taiwan Province of China (from 1999) (OIE Web site; Flegel and Fegan, 2002a), and most recently Thailand (2003) (Timothy Flegel, per. com.), probably through the regional and international transfer of live PL and broodstock P. vannamei.
Taura syndrome caused serious losses in revenue throughout Latin America in the 1990s. It has been suggested that TSV caused direct losses (due to shrimp mortality) of US$1–1.3 thousand million in the first three years in Latin America. However, indirect losses due to loss of sales, increased seed cost and restrictions on regional trade were probably much higher (Brock et al., 1997; Hernández-Rodríguez et al., 2001).
In 1992, Ecuador was producing close to 100 000 tonnes of P. vannamei worth some US$880 million (FAO FISHSTAT estimate is US$551 million). Lightner (1996a) estimated that a 30 percent reduction in production (to 70 000 tonnes) in subsequent years represented a loss of up to US$400 million per year from Ecuador alone (Figure 2). However, P. vannamei, even without the benefit of selective breeding (still in its infancy at that stage) were quickly able to gain some tolerance to TSV, so that Ecuador had recuperated to a production of 129 600 tonnes worth US$875 million by 1998 (FAO Fishstat figure is US$648 million). Then in late 1999, WSSV hit Ecuador and production rates declined once again (Rosenberry, 2000).
Little is known regarding the prevalence of TSV in wild shrimp populations, and although it has been detected in wild P. vannamei from the Americas and in wild P. monodon in Taiwan Province of China, there is no evidence that it has impacted wild shrimp populations (Brock, 1997; GMFS Web site; OIE Web site). Taura syndrome so far appears to occur largely as a sub-clinical infection in populations of wild shrimp (Brock et al., 1997). Although P. monodon and P. japonicus appear largely unaffected, the potential impact of TSV on native stocks of P. indicus and P. merguiensis in Asia remains unknown, but a definite cause for concern.
The mechanism of spread of TSV is still uncertain, although initial theories concentrated on the spread through contaminated PL and broodstock between farms (Lightner, 1995 and 1996b; Garza et al., 1997). Limited data have shown that TSV was introduced to Colombia and Brazil through contaminated broodstock from Hawaii (Brock et al. 1997). These broodstock were untested for TSV since it was not yet known that Taura syndrome had a viral cause. Such cases demonstrate once again more of the problems involved with transboundary movements of animals, even supposedly SPF ones. Recent research has shown that mechanical transfer through insect and avian vectors may be an equal or even more likely route of infection. TSV has sometimes been found in tissue bioassays of the water boatman (Trichocorixa reticulata), an estuarine insect common worldwide, and virus-containing extracts of this insect have been shown to induce infection in SPF P. vannamei under laboratory conditions (Lightner, 1995). Patterns of the spread and mortality of P. vannamei in Texas have also suggested that the ingestion of infected insects is the probable mechanism of spread of TSV (Thompson et al., 1977).
Exports of shrimp (tonnes) from Ecuador (1979–2002) and environmental/disease events
Source: Cámara Nacional de Acuacultura Web site - http://www.cna-ecuador.com
Infective TSV has also been demonstrated in the faeces of shrimp-eating seagulls (Larus atricilla) collected near ponds infected with TSV in Texas, United States of America (Lightner, 1996a; Garza et al., 1997). Experimental results have also shown that healthy shrimp can be infected through injection of cell-free homogenates prepared from infected shrimp, and by direct feeding on infected shrimp (Brock et al., 1995; Hasson et al., 1995). Taura syndrome virus has also been shown to remain infective after one or more freeze-thaw cycles, indicating the possibility of regional transmission through infected frozen shrimp (Lightner, 1995; Brock et al., 1997). With proper disinfection procedures and controls, however, this route is currently considered to be low-risk (Flegel and Fegan, 2000b; Flegel, 2003).
Taura syndrome virus is highly infective for P. vannamei, P. setiferus and P. schmitti. Penaeus stylirostris can be infected by injection, but appear to be highly refractory to TSV and have demonstrated tolerance to TS in growing areas affected by this disease. Other species including P. aztecus, P. duorarum, P. monodon, P. japonicus and P. chinensis have been experimentally infected, developed the disease and remained carriers, but show some resistance (Lightner, 1996a; Brock et al., 1997; Overstreet et al., 1997; GSMFC Web site; OIE Web site). Interestingly, like P. stylirostris, P. monodon and P. japonicus appear highly refractory to TSV, and although it retards growth rates, they remain asymptomatic and the virus has not yet been demonstrated to cause mortality in these species (Timothy Flegel, per. com.; Brock et al., 1997; OIE Web site). However, since TSV is an RNA virus, with a high propensity to mutate, there is no guarantee that it will not mutate into a more virulent form for native Asian shrimp (as it did in Central America) (Flegel and Fegan, 2002; Lightner, 2002).
Taura Syndrome Virus has already been detected in P. vannamei in Mainland China (starting in 1999/2000) and Taiwan Province of China (from 1999) (OIE Web site; Tu et al., 1999; Yu and Song, 2000) with 19 cases reported to OIE from Taiwan Province of China in 1999, ten (resulting in 700 000 cases and 200 000 deaths) in 2000, and seven (resulting in 500 000 cases and 50 000 deaths) in 2001. Recently, TSV has been identified in Thailand (Timothy Flegel, per. com.), but not officially reported to OIE, despite being a listed disease. TSV has not yet (in 2003) been reported from Viet Nam, Indonesia (Taw, Srisombat and Chandaeng, 2002), India or Malaysia (Dato Mohamed Shariff, per. com.).
The Taura syndrome virus tends to infect juvenile shrimp within two to four weeks of stocking ponds or tanks (0.1–1.5 g body weight) and occur largely within the period of a single moult cycle. In the acute phase of the disease, during pre-moult the shrimp are weak, soft-shelled, have empty digestive tracts and diffuse expansion of the red chromatophores, particularly in the tail (hence the common name - red tail disease) (Lightner, 1995). Such animals will usually die during moulting (5–95 percent), although the reasons for the large variability in survival rates remains unknown; adult shrimp are known to be more resistant than juveniles (Brock et al., 1997). Those shrimp that survive will show signs of recovery and enter the chronic phase of the disease. Such shrimp will show multiple, randomly distributed, irregular, pitted, melanised lesions of the cuticle. These gross or microscopic lesions will persist, but may be lost during moulting, the shrimp thereafter appearing and behaving normally. However, although the shrimp may then be resistant to recurrence of the disease, they often remain chronic, asymptomatic carriers of TSV for life (Lightner, 1996b; Brock et al., 1997; GSMFC Web site; OIE Web site), as has been shown by bioassays (Brock et al., 1995).
Standard histological and molecular methods may be used for detection, diagnosis and surveillance, although specific DNA probes applied to in situ hybridization assays with paraffin sections currently provide the greatest diagnostic certainty of this virus (OIE Web site). RT-PCR assays can also be used providing advantages of larger sample sizes and non-lethal sampling for broodstock. Additionally, live shrimp bioassays and serological methods with monoclonal antibodies can also be used for diagnosing infections with TSV. The full set of current diagnostic procedures using all of these methods is found in the OIE Diagnostic Guide available on the OIE Web site.
Eradication methods for TSV in culture facilities are possible and depend upon total destruction of infected stocks, disinfection of the culture facility, avoidance of reintroduction of the virus (from nearby facilities, wild shrimp and carriers) and restocking with TSV-free PL produced from TSV-free broodstock (Lotz, 1997; Lightner and Redman, 1998a; OIE Web site).
Other methods suggested for controlling the virus include: switching to the refractory P. stylirostris, and (similar to those suggested for other viruses): maintenance of optimal environmental conditions, weekly applications of hydrated lime (CaOH) at 50 kg/ha, polyculture with fish (to consume dying and dead carriers) and development of TSV resistant lines of P. vannamei (Brock et al., 1997). In the past few years, considerable success has been achieved in the development of families and lines of P. vannamei which are resistant to TSV (Argue et al., 2002).
Most of the SPF P. vannamei suppliers from Hawaii and Florida now offer stocks of P. vannamei which have demonstrated resistance to TSV (SPF and SPR) (Table 7). Genetic selection programmes run throughout the Americas have also resulted in the production of SPR lines for TSV. The use of such SPR lines enabled the Latin American industry to recuperate from the worst of the TSV pandemic within three to four years. However, importation of such lines must be done with caution, since non-SPF animals, even though resistant to TSV, may still act as carriers and can result in the introduction of TSV into areas of Asia currently free from the disease.
In the latest edition of the OIE aquatic animal health code, guidelines are offered for countries currently declared free from TSV for importations of shrimp. These guidelines suggest that the competent authority of such countries should only import live P. vannamei and P. stylirostris (eggs, nauplius, PL, juveniles or broodstock) from either countries or certified regions or aquaculture establishments declared free from TSV (OIE, 2003). The competent authority of the importing country should require that each shipment be accompanied by an international aquatic animal health certificate issued by the competent authority of the exporting country. This certificate must certify, on the basis of an official crustacean health surveillance scheme (run according to the OIE manual) that the country, region or establishment is officially declared TSV-free. The same guidelines exist for importation of dead shrimp.
Aquaculture establishments, zones within countries, or countries that are considered TSV-free, are those which: have been tested in an official crustacean health surveillance scheme for a minimum two years using the procedures described in the OIE manual, without detection of TSV in any susceptible host species of shrimp17. Additionally for aquaculture establishments, they must be supplied with water that has been suitably disinfected and have barriers preventing contamination of the establishment and its water supply. New or disinfected facilities, may be declared free from TSV in under two years if all other requirements are met (OIE Web site).
While this degree of control may be possible in large-scale highly organized shrimp farms, the reality is that most farms are too small or disorganized to undertake such comprehensive measures. The lack of supporting infrastructure in regulation, testing and diagnosis is an additional constraint. This problem is not confined to Asia where farms are typically very small, but also occurs in Latin America where farms are far larger.
This virus was first discovered in P. vannamei and P. stylirostris in the Americas in 1981, starting in Hawaii (Lightner, 2002). However, it was probably not an indigenous virus, but was thought to have been introduced along with live P. monodon from Asia. IHHNV has probably existed for some time in Asia without detection due to its insignificant effects on P. monodon, the major cultured species in Asia, meaning that nobody was looking for it. Recent studies have revealed geographic variations in IHHNV isolates, which suggested that the Philippines were the source of the original infection in Hawaii, and subsequently in most shrimp farming areas of Latin America (Tang et al., 2002).
IHHNV is a small single-stranded DNA-containing parvovirus, which is only known to infect only penaeid shrimp. “Natural” infections are known to have occurred with P. stylirostris, P. vannamei, P. occidentalis and P. schmitti, while P. californiensis, P. setiferus, P. aztecus and P. duorarum were proven susceptible experimentally in Latin America. Penaeus monodon, P. semisulcatus, P. japonicus and P. chinensis and others are known to be susceptible in Asia (OIE Web site).
Catastrophic epidemics and multi-million dollar losses in shrimp culture have been attributed to IHHNV (GSMFC Web site) and it has had significant negative consequences for cultured P. vannamei in the Americas during the 1990s (Lightner, 1996a). Some indication of its impact may be gauged from work done in intensive culture systems in Hawaii, which improved yields by 162 percent through the stocking of shrimp bred specifically to be IHHNV resistant (Flegel and Fegan, 2002).
IHHNV did not cause significant problems in Ecuador until the warm waters and abundant wild seed (acting as latent carriers of the disease) associated with the strong El Niño of 1987/88 caused an epidemic from 1987 onwards (Jiménez et al., 1999) (Figure 4). Recent use of domesticated and selected strains of P. vannamei instead of wild PL has more recently reduced the severity of the epidemic, indicating the utility of such selections in combating viral pathogens such as IHHNV.
IHHNV was also largely responsible for the temporary cessation of Mexican commercial shrimp fishing for several years once it escaped from farms into the wild shrimp populations (Lightner, 1996). IHHNV is now commonly found in cultured and wild penaeid on the Pacific coast of Latin America from Mexico to Peru, but not yet from the eastern coast of Latin America. It has also caused problems for the Hawaiian broodstock and farm-based culture industries. IHHNV has also been reported from both cultured and wild Penaeid from throughout the Indo-Pacific region (OIE Web site).
IHHNV is fatal to P. stylirostris (unlike P. vannamei), which, although highly resistant to TSV (leading to its comeback in the culture industry of Mexico in the late 1990s), are extremely sensitive to IHHNV (causing 90 percent mortality), especially in the juvenile stages (Lightner, 1996; OIE Web site). However, IHHNV has not been associated with mass mortalities of P. stylirostris in recent years (Tang et al. 2002b), probably due to the selection of IHHNV-resistant strains (i.e. the so-called “supershrimp” P. stylirostris, Tang and Lightner, 2001). This emphasizes the potential benefits offered from the domestication and genetic selection of cultured shrimp.
Penaeus vannamei are fairly resistant to this disease with certain modifications in management practices. In P. vannamei, IHHNV can cause runt deformity syndrome (RDS), which typically results in cuticular deformities (particularly bent rostrums), slow growth, poor feed conversion and a greater spread of sizes on harvest, all combining to substantially reduce profitability. These effects are typically more pronounced where the shrimp are infected at an early age, so strict hatchery biosecurity including checking of broodstock by PCR, or the use of SPF broodstock, washing and disinfecting of eggs and nauplii is essential in combating this disease. Even if IHHNV subsequently infects the shrimp in the grow-out ponds, it has little effect on P. vannamei if the PL stocked can be maintained virus free (Centre for Tropical and Subtropical Aquaculture, 1996).
Some strains of IHHNV, however, have recently been found to be infectious for P. vannamei, including a putative strain collected from Madagascan P. monodon (Tang et al., 2002) and a putative attenuated strain in an American laboratory (Larramore et al. 2002). In addition, recent laboratory studies with P. stylirostris has shown that juveniles that are highly infected with IHHNV (by feeding them with IHHNV-infected tissue) were able to show 28–91 percent survival three weeks after subsequent infection with WSSV (by feeding them with WSSV-infected tissue), while control animals suffered 100 percent mortality within five days (Tang et al., 2002b). Surviving shrimp were found to be heavily infected by IHHNV, but had at most only light infection with WSSV which was not enough to kill all of them. Similar trials showed that neither IHHNV pre-infected P. vannamei nor IHHNV-resistant P. stylirostris (SPR “Supershrimp”) were able to tolerate subsequent WSSV infections. Nonetheless, these results raise the question whether exposing shrimp to putative strains of IHHNV may prevent them from getting infected by an infectious strain of IHHNV or possibly WSSV.
IHHNV typically causes no problems for P. monodon since they have developed a tolerance to it over a long period of time, but they may suffer from runt deformity syndrome (RDS) (OIE Web site). Penaeus merguiensis and P. indicus meanwhile appear refractory to the disease (Flegel and Fegan, 2002). They are, however, life-long carriers of the disease and so could easily pass it onto P. vannamei, which typically suffer from slow growth (RDS) when exposed to IHHNV. This presents a potential problem if the two species are cultured in close proximity at any phase of their life cycle (Timothy Flegel, per. com.). This should be a cause for great concern for P. vannamei farms that are currently being established throughout Asia.
As with most important shrimp viruses, transmission of IHHNV is known to be rapid and efficient by cannibalism of weak or moribund shrimp, although water-borne transfer due to cohabitation is less efficient. Vertical transmission from broodstock to larvae is common (OIE Web site) and has been shown to originate from the ovaries of infected females (while sperm from infected males was generally virus-free). Although the embryos of heavily infected females may abort, this is not always true and selection of IHHNV-free broodstock (by nested PCR) and disinfection of eggs and nauplii would help ensure production of virus-free PL (Motte et al., 2003).
As with TSV, IHHNV may be transmitted through vectors such as insects, which have been shown to act as carriers for the disease. However, their mode of action is thought to be mechanical rather than real, as insect extracts do not react to in situ hybridisation tests for IHHNV (Timothy Flegel, per. com.).
The probability that IHHNV in frozen shrimp can cause problems is suggested from OIE data that IHHNV remains infectious for more than 5 years of storage at minus 20°C (OIE Web site).
Gross signs of disease are not specific to IHHNV, but may include: reduced feeding, elevated morbidity and mortality rates, fouling by epicommensals, bluish coloration, while larvae PL and broodstock rarely show symptoms (OIE Web site).
Diagnosis and detection methods include DNA probes for dot blot and in situ hybridisation and PCR techniques (including real-time PCR, Tang and Lightner, 2001) as well as histological analysis of H&E-stained sections looking for intracellular, Cowdrey type A inclusion bodies in ectodermal and mesodermal tissues. The full procedures for all these tests can be found in the OIE Web site.
One of the big problems with IHHNV is its eradication in facilities once they have been infected. The virus has been shown to be highly resistant to all the common methods of disinfection including chlorine, lime, formalin and others in both ponds and hatcheries (CTSA, 1996; Scurra, per. com.). Complete eradication of all stocks, complete disinfection of the culture facility and avoidance of restocking with IHHNV-positive animals, i.e. through the use of screened or SPF animals, has been recommended (OIE Web site).
This virus is now and has for some time been the most serious threat facing the shrimp farming industry in Asia (since 1992) and Latin America (since 1999). It is an extremely virulent pathogen with a large number of host species (Flegel, Boonyratpalin and Withyachumnarnkul, 1997; Lightner and Redman, 1998b).
This disease is probably the major cause of direct losses of up to US$1 thousand million per year since 1994 in Asia. Similarly, in Latin America, losses due to WSSV have been substantial. For example, in the first six months of its first appearance in Ecuador, it was estimated to have caused a loss of 63 000 tonnes of cultured P. vannamei and P. stylirostris, worth some US$280 million. In addition, indirect losses in hatchery, feed and packing plant capacities and so on resulted in lost earnings and the loss of 150 000 jobs in the sector (Alday de Graindorge and Griffith, 2000). Data from the Ecuadorian Camara Nacional de Acuacultura (CNA) show that due to WSSV, shrimp exports fell from 115 000 tonnes in 1998 to 38 000 tonnes in 2000, and have only recovered slightly to 47 000 tonnes in 2002, and perhaps 50 000 tonnes in 2003 (CNA Web site) (Figure 2). This equates to a total direct loss (alone) of some 267 000 tonnes of shrimp worth nearly US$1.8 thousand million (if production had remained static at 1998 levels) between 1999 and mid-2003.
Similar problems have occurred throughout Central and South America, with the exception of Brazil and Venezuela, which remain WSSV-free due to the prompt and effective closure of their borders to all crustacean imports in 1999. The United States also managed to eradicate WSSV from its shrimp culture industry in 1997 after initial losses through implementation of biosecurity measures, including the use of all SPF broodstock (Lightner, 2002), although there are reports of its recent re-emergence in Hawaii in 2004 (Shrimp News Web site18).
WSSV is a large double-stranded DNA baculovirus (Lightner, 1996). Other names for probably the same viral complex include Chinese baculovirus (CBV), White spot syndrome baculovirus complex (WSBV), Mainland China's Hypodermal Hepatopoietic Necrosis Baculovirus (HHNBV), Shrimp Explosive Epidermic Disease (SEED), Penaeid Rod-shaped DNA Virus (PRDV), Japan's Rod-shaped Nuclear Virus (RV-PJ) of P. japonicus, Thailand's Systemic Ectodermal and Mesodermal Baculovirus (SEMBV) of P. monodon, red disease and white spot virus or disease (GSMFC Web site).
WSSV was first reported in farmed P. japonicus from Japan in 1992/93, but was thought to have been imported with live infected PL from Mainland China. At roughly the same time, it was discovered in cultured P. monodon, P. japonicus and P. penicillatus in Taiwan Province of China and then in P. monodon in southern Thailand (Lightner and Redman, 1998b). WSSV then spread rapidly throughout most of the shrimp growing regions of Asia, probably through infected broodstock and PL P. monodon. Then, in 1995, it was detected for the first time in farmed P. setiferus in Texas. It was also shown to be infective experimentally to both P. vannamei and P. stylirostris (Tapay et al., 1996). WSSV did not reach the Philippines, which had an effective government ban on live imports, until an illegal introduction of Chinese PL P. monodon in 2000 (Flegel and Fegan, 2002).
Other susceptible host species include the shrimp species P. merguiensis, Metapenaeus ensis, Metapenaeus monoceros and various crab species, while Palaemon setiferus, Euphausia superba, Metapenaeus dobsoni, Parapenaeopsis stylifera, Solenocera indica, Squilla mantis, Macrobrachium rosenbergii and a range of crab species can act as latent carriers, although Artemia appear unsusceptible (Flegel et al., 1997; Hossain et al. 2001).
Later, in 1999, WSSV began affecting Latin America from Honduras, Guatemala, Nicaragua and Panama in Central America to Ecuador and Peru in the south and later to Mexico. The only shrimp farming countries to remain free of WSSV in Latin America are Brazil and Venezuela, who (like the Philippines) both placed immediate and effective bans on the importation of live crustaceans and developed their domestication programmes for producing virus-free seedstock.
The mode of transmission of WSSV around Asia was believed to be through exports of live PL and broodstock. The outbreaks in Texas in 1995 and then Honduras in 1999, followed by Spain and Australia in 2000–2001, were thought to be due to the virus escaping from processing plants which were importing and processing frozen shrimp from infected parts of Asia, although this has never been proven (Lightner, 1996a and 2002; GSMFC Web site). Regardless of their origin, isolates of WSSV have shown little genetic or biological variation, suggesting that the virus emerged and was spread from a single source (Lightner, 2002).
WSSV, as with most viral diseases, is not thought to be truly vertically transmitted, because disinfection of water supplies and the washing and/or disinfection of the eggs and nauplius is successful in preventing its transmission from positive broodstock to their larvae. Instead, it is generally believed that the virus sticks to the outside of the egg, since, if it gains entry to the egg, it is rendered infertile and will not hatch. Thus, using proper testing and disinfection protocols, vertical transmission can be prevented in the hatchery, as proven by the Japanese who to date have successfully eliminated WSSV from captive stocks in the country through disinfection and PCR checking of broodstock and nauplii (Timothy Flegel, per. com.).
Using mathematical epidemiology modelling, Soto and Lotz (2001) showed that WSSV was more easily transmitted through ingestion of infected tissues than through cohabitation with infected hosts, and that P. setiferus was much more susceptible than P. vannamei to infection.
Although it is clear that live Penaeids can carry the virus and infect new hosts through reproduction (transmission from broodstock to larvae), consumption or cohabitation with diseased or latent carriers, and that it is possible for frozen shrimp to be infective, other modes of transmission are also possible. For example, Australia is considered WSSV (and YHV)-free, although WSSV was detected in the Northern Territories in 2000 associated with imported bait shrimp, before being eradicated (East et al., 2002).
Data regarding the presence and effects of WSSV in wild shrimp populations in infected countries is scarce, but it is known to be present in wild shrimp in both Asia and Latin America.
WSSV infects many types of ectodermal and mesodermal tissues, including the cuticular epithelium, connective, nervous, muscle, lymphoid and haematopoietic tissues. The virus also severely damages the stomach, gills, antennal gland, heart and eyes. During later stages of infection, these organs are destroyed and many cells are lysed. The shrimp then show reddish colouration of the hepatopancreas and the characteristic 1–2 mm diameter white spots (inclusions) on their carapace, appendages and inside surfaces of the body. They also show lethargic behaviour and cumulative mortality typically reaches 100 percent within two to seven days of infection (GSMFC Web site).
Increasingly, since the late 1990s, it has become clear that the presence of WSSV in a pond does not always lead to disaster. Work in Thailand has shown that outbreaks are usually triggered from latent P. monodon carriers by some environmental changes, probably related to osmotic stress through changes in salinity or hardness or rapid temperature changes (Flegel, Boonyaratpalin and Withyachumnarnkul, 1997). Similarly in Latin and North America, fluctuations in temperature have been shown to induce mortalities of infected P. vannamei. However, there have been conflicting reports about constant temperatures which have been reported to: limit mortality due to WSSV at 18 °C or 22 °C and induce 100 percent mortality at 32 °C in the United States of America (Overstreet and Matthews, 2002), yet induce mortality at less than 30 °C and protect from it at greater than 30 °C in Ecuador (Matthew Briggs and Neil Gervais, per. com.).
Additionally, three to four years of genetic selection work (selection of shrimp surviving WSSV outbreaks) on the domesticated stocks of P. vannamei appear to have resulted in enhanced resistance to WSSV in Ecuador (Matthew Briggs and Neil Gervais, per. com.). Thus the culture industries for P. vannamei in Central and South America have been slowly recuperating since the start of the WSSV epidemic in 1999. For example, Ecuador was exporting 115 000 tonnes in 1998, which dropped to only 38 000 tonnes in 2000 after the arrival of WSSV in 1999. Subsequently, Ecuador has recovered to export an estimated 50 000 tonnes in 2003 (INP and CAN [Ecuador] Web sites).
Prevention methods are similar to those with TSV. All live and frozen shrimp should be checked by PCR prior to importation from infected areas to those currently disease-free. Broodstock should be PCR screened before breeding. PL should also be PCR screened before stocking into ponds, as this has been proven to result in a higher percentage of good harvests (Pornlerd Chanratchakool, per. com.). PCR is not an infallible method for detection of WSSV, but it is the best diagnostic procedure currently available. Washing and disinfection of eggs and nauplii has also been shown to prevent vertical transmission of WSSV from infected broodstock to larval stages. Feeding with fresh crab and other crustaceans to broodstock should be avoided. Polyculture techniques with mildly carnivorous fish species (such as tilapia) has also proven effective at limiting the virulence of WSSV in ponds, as the fish can eat infected carriers before they become available to the live shrimp.
The white spot virus only remains viable in water for 3–4 days, so disinfection of water used for changes and fine screening is effective in preventing transmission. Dose rates of 70 ppm formalin have been shown to prevent transmission and not cause any harm to shrimp (Flegel et al., 1997). In addition, all effluent from farming or processing operations with the possibility of WSSV infections should be disinfected (i.e. with formalin or chlorine) prior to discharge (Flegel, Boonyaratpalin and Withyachumnarnkul, 1997).
WSSV can be detected by using PCR, or with probes for dot-blot and in situ hybridisation tests. It can also be visually diagnosed through the presence of the characteristic white spots (although these are not always present in infected animals). WSSV can be confirmed histologically (particularly for asymptomatic carriers) by the presence of large numbers of Cowdrey A-type nuclear inclusions and hypertrophied nuclei in H&E-stained sectioned tissues, or simply by rapid fixation and staining of gill tissue and microscopic examination (Flegel, Boonyaratpalin and Withyachumnarnkul, 1997). Standard diagnostic techniques are provided on the OIE Web site.
Yellow Head Virus was the first major viral disease problem to affect Asian shrimp farms when it was diagnosed as causing extensive losses in Thailand starting in 1990/91. YHV and its close relatives GAV and LOVV are single stand RNA viruses, similar to TSV.
The first records of this virus were from P. monodon ponds in Eastern Thailand in 1990/91. By 1992, it had moved to Southern Thailand and was causing substantial mortality. YHV is prevalent wherever P. monodon are cultured, including Thailand, Taiwan Province of China, Indonesia, Malaysia, Mainland China, the Philippines and Viet Nam. It may also have been responsible for the first major crashes in Taiwan Province of China in 1987 (GSMFC Web site; Flegel, Boonyaratpalin and Withyachumnarnkul, 1997; Lightner and Redman, 1998b).
Losses due to YHV continued, although the severity and frequency of outbreaks declined sharply by 1994 when WSSV became the prime cause of mortality in cultured P. monodon. Although research has shown that YHV is still present in culture ponds, the shrimp now rarely show gross symptoms and are latently infected. There thus appears to be a currently unknown mechanism for rapid tolerance or resistance to RNA-type viruses (such as YHV in Asia, and TSV in Latin America) in penaeid shrimp (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977).
It is known that YHV occurs in wild shrimp, but there is no data on the extent or effects of YHV on populations of wild shrimp in Asia and its impacts are thus currently unknown.
The primary mechanism of spread of YHV in pond culture appears to be from water and mechanical means or from infected crustacean carriers (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977). Some infected carriers appear to have latent infections (i.e. P. merguiensis, Metapenaeus ensis, Palaemon styliferus and Acetes spp.), while others may die from it (i.e. Euphausia superba). Other crustaceans, such as Macrobrachium rosenbergii and many crab species and Artemia appear unsusceptible (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977).
Since, like most viruses, the viability of the free virus in seawater is not more than a couple of hours, the most serious threat to farmers is latent or asymptomatic carriers, from which the virus can be spread either by ingestion or cohabitation. In addition, infected broodstock can pass on the virus to larvae in the maturation/hatchery facilities if thorough disinfection protocols are not strictly adhered to (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977).
Although a distinct possibility, YHV has not yet been reported from Latin America apart from some probably spurious results from Texas in 1995 (Lightner, 1996). However, from work in Hawaii, YHV is known to cause high mortality in P. vannamei, P. stylirostris, P. setiferus, P. aztecus and P. duorarum when it is injected as viral extracts (Lu et al., 1994; Lightner, 1996). Despite this, there are still no reports of “natural” infections in shrimp farms of P. vannamei and P. stylirostris with YHV in Asia. There is a strong possibility, however, that YHV may cause problems for the new culture industries for P. vannamei and P. stylirostris in Asia. This will probably be true at least until these species can gain some degree of tolerance or resistance to the virus as P. monodon appears to have done. In the meantime, the large number of latent infected hosts (including P. monodon) will serve as a potential reservoir of infection and should not be permitted to come into contact with cultures of P. vannamei or P. stylirostris.
YHV principally affects pond reared P. monodon in juvenile stages from 5–15 g (Lightner, 1996). Shrimp typically feed voraciously for two to three days and then stop feeding abruptly and are seen swimming near the pond banks. YHV infections can cause swollen and light yellow coloured hepatopancreas in infected shrimp, and a general pale appearance, before dying within a few hours. Total mortality of the crop is then typically seen within three days. Experimentally infected shrimp develop the same signs as those naturally infected, indications of the disease are noted after two days and 100 percent mortality results after three to nine days (Lu et al., 1995; GSMFC Web site).
Yellow head virus can be detected by RT-PCR or with a new probe for dot-blot and in situ hybridisation tests. It can also be diagnosed histologically in moribund shrimp by the presence of intensely basophilic inclusions, most easily in H&E-stained sectioned stomach or gill tissue, or simply by rapid fixation and staining of gill tissue and microscopic examination. Exact protocols for all of these techniques are given in the OIE Web site and by Flegel, Boonyaratpalin and Withyachumnarnkul, 1977.
Eradication methods in ponds are much the same as for other viruses and involve a package including: pond preparation by disinfection and elimination of carriers, storage and/or disinfection of water for exchange with chlorine (30ppm active ingredient), filtering water inlet to ponds with fine screens, avoidance of fresh feeds, maintenance of stable environmental conditions, disinfection of YHV infected ponds before discharge, and monitoring (by PCR) and production of virus free broodstock and PL for pond stocking (Flegel et al., 1997). Various immunostimulants, nutrient supplements and probiotics have been tried, but there remains a paucity of conclusive evidence of the benefits of such treatments.
The rapid tolerance gained by P. monodon to YHV provoked theories as to its mechanism (Pasharawipas et al., 1997). Whether this theory is correct or not, field data has indicated that shrimp surviving a YHV epidemic are already infected and thus are not killed by subsequent infections, suggesting that some type of “vaccination” (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977) with a dead or attenuated virus might provide some resistance. Some commercial products are already being marketed and trials have been partially successful. YHV is not causing much loss at present in Asia, but general management practices as described above (to maintain optimal environmental conditions and minimize viral loadings) are still required to help prevent infections (Flegel, Boonyaratpalin and Withyachumnarnkul, 1977).
Lymphoid Organ Vacuolization Virus was first noted in P. vannamei farms in the Americas in the early 1990s (Brock and Main, 1994). In P. vannamei, LOVV has been shown to result in limited localized necrosis of lymphoid organ cells, but has never been shown to impact production. It was later discovered in Australia, along with the other TSV-like virus GAV (Lightner and Redman, 1998b).
Due to the coincidence in dates, it is possible that the main cause of the problems with P. monodon, was a result of the introduction of viral pathogens carried by P. vannamei. A RNA viral pathogen very similar to LOVV in P. vannamei has recently been discovered in Thailand in the lymphoid organ of P. monodon (December 2002, by D.V. Lightner). This new type of LOVV might be the causative agent of this slow growth phenomenon. Evidence for this was provided by Timothy Flegel (per. com.), who found that juvenile P. monodon injected with this virus grew to only four grams after two months, while those injected with a placebo reached eight grams in the same time. Injections of the same virus into P. vannamei caused no obvious effects, suggesting that it probably originated from this species.
There are a number of other viruses in the Asia-Pacific region. Penaeus monodon from Australia have been found to be hosts for a number of viruses not yet present in other Asian countries. These include two viruses closely related to YHV: GAV (only 20 percent genetically different to YHV) and MOV (only 10 percent genetically different from GAV), which are quite recently discovered viruses that are already prevalent in 100 percent of £monodon from Queensland (Timothy Flegel, per. com.). MOV was only discovered in 1996, but has already been found in P. japonicus and is associated with disease episodes in P. monodon farms in Australia and elsewhere in Asia (IQ2000 Web site19). The strong possibility for the introduction of these viruses into Asia exists due to frequent shipments of P. monodon broodstock from Australia into Thailand, Viet Nam and other Southeast Asian countries.
Many of the viruses infecting shrimp are hidden or cryptic and, although present in their host, may produce no gross signs of disease or notable mortality. Many of these viruses, without methods of diagnosis, are probably being harboured unknown within the wild and cultured populations of shrimp throughout the world. It may not be until shrimp species from one location are moved to another and their viral flora comes into contact with new and/or naive or intolerant hosts that disease epidemics begin. Crustaceans may be particularly problematic since they tend to have persistent, often multiple, viral infections without gross or even histological signs of disease (Flegel and Fegan, 2002).
Examples of this problem include the transfer of IHHNV from the tolerant P. monodon in Asia to the susceptible white shrimp P. vannamei and P. stylirostris in Latin America. Another possibility in this category is the LOVV virus thought to be causing the slow growth phenomenon in P. monodon around Asia. This virus may have been imported with live P vannamei broodstock and PL brought to Asia from the Americas in the mid 1990s. For this reason, extreme caution should be placed on the transboundary movements of live shrimp.
Necrotizing hepatopancreatitis is caused by a Rickettsia-like intracellular bacterium and has been an important disease in Texan shrimp culture since its first diagnosis in 1985. It has resulted in mass mortalities (20–90 percent) of £vannamei in highly saline commercial grow-out ponds nearly every year since then (Thompson et al., 1997). By 1993, NHP had spread to Ecuador and Peru, and by 1995, coinciding with warm waters with high salinity associated with El Nino, was causing severe mortalities (60–80 percent mortality) of P. vannamei and P. stylirostris throughout Ecuador (Jiménez, Barniol and Machuca, 1997). It is believed that NHP was spread with infected PL from Central America to Peru and Ecuador (Jiménez, Barniol and Machuca, 1997).
NHP has not yet been reported in Asia, but could cause significant damage were it to be transferred here with untested shrimp from Latin America (Fegan, 2002).
There are few rigorous analyses of the costs of disease on aquaculture and capture fishery activities. Most of the estimates that have been made were based on the estimated value of production which was presumed lost due to disease with reference to national production figures pre and post-epidemic. For shrimp culture, “native” viruses causing problems have been largely due to WSSV and YHV in Asia and TSV and IHHNV in Latin America.
Estimates for Asia include: a loss of over US$250 million for 1993 (continuing every year) in Mainland China, loosing 120 000 tonnes of production of P. chinensis, P. japonicus and P. monodon to WSSV (Jiang, 2000); US$400 million in direct economic loss due to all shrimp diseases in 2002 (Chen Aiping, per. com.); US$300 million since 1992 for lost production in Indonesia due to YHV and WSSV (Rukyani, 2000); US$30–40 million/year due to YHV in 1992 and 1993, rising to 240–650 million/year between 1994 and 1997 due to WSSV and THV inn Thailand (Chanratchakool, Fegan and Phillips, 2000); US$100 million in 1993 due to WSSV, YHV and MBV in Viet Nam (Khoa, Hao and Huong, 2000); US$25 million/year due to WSSV in Malaysia (Yang et al., 2000); Rp4–5 thousand million annually in India to WSSV and YHV (Mohan and Basavarajappa, 2000); up to Rp1 thousand million per year since 1996 in Sri Lanka to WSSV and YHV; and US$32.5 million between 1994–1998 in Australia due to “Mid Crop Mortality Syndrome” (MCMS) (Walker, 2000).
Total losses in Asia over the past decade may thus reach close to US dollars one billion a year due to the direct effects of “native” viruses on shrimp production. However, none of these figures takes into account ancillary industry losses including: unemployment and social upheaval, reduced requirements for feed, chemicals and other supplies, closure of hatcheries and capture fisheries for broodstock and wild seed, reduced requirements for packing, processing, export and shipment of shrimp produced, reduced investor confidence and so on.
Latin American shrimp farmers have also suffered huge economic and social problems related to outbreaks of native viral disease epidemics, especially TSV and IHHNV since 1993 (Figure 2). For example, Ecuador lost up to US$400 million per year from 1992 to 1997 to TSV (Lightner, 1996a); Honduras lost 18, 31 and 25 percent of its shrimp due to TSV in 1994, 1995 and 1996 respectively (Corrales, Watson and Wigglesworth, 2000); Panama lost 30 percent of its production to TSV in 1996 (Morales, Bercerra and Lara, 2000); Peru lost US$2.5 million to TSV in 1993 (Talavera and Vargas, 2000); and Mexico lost US$25 million due to IHHNV infections in P. stylirostris in the late 1980s/early 1990s (SEMERNAP, 2000). It has been suggested that TSV caused direct losses (due to shrimp mortality) of US$1–1.3 thousand million in the first three years in Latin America. However, as in Asia, indirect losses due to loss of sales, increased seed costs and restrictions on regional trade were probably much higher (Brock et al., 1997; Hernández-Rodríguez et al., 2001).
To date, in Asia, the introduction of infected broodstock of P. vannamei from Latin America from 1996 onwards is known to have resulted in the introduction of TSV into Mainland China and Taiwan Province of China (from 1999). TSV is now believed to be causing mass mortalities in cultured P. vannamei in both countries (Tu et al., 1999; Yu and Song, 2000; Chen Aiping, per. com.). Estimates of the economic and social losses have not yet been made. TSV is also now known to be present in Thailand and is reported to be beginning to cause heavy mortalities to the P. vannamei being cultured there (Timothy Flegel, per. com.).
In Latin America, although P. monodon and P. japonicus have been imported at various times, their culture has never been successful, so that losses of these species due to the diseases brought with them have never reached a high level of economic significance.
Introduced WSSV has resulted in significant loss of production of penaeid shrimp in Latin America since 1999. In Ecuador for example, within the first year of the WSSV epidemic in 1999, the disease caused a direct financial loss of US$280 million (42 percent of production capacity, or 63 000 tonnes of P. vannamei and P. stylirostris) (Alday de Graindorge and Griffith, 2000). Data from the CNA of Ecuador suggest a direct loss of US$1.7 billion between 1999 and the first half of 2003 (CNA Web site, Figure 2). Other problems resulting from the WSSV epidemic have been seen in Honduras (13 percent reduction in workforce) (Corrales, Watson and Wigglesworth, 2000), and 40 percent (4 400 tonnes) of lost production worth US$40 million in 1999 in Panama with P. vannamei (Morales, Bercerra and Lara, 2000). Every other Latin American country, with the exception of Brazil and Venezuela, including United States of America, had also suffered serious problems due to WSSV since 1999.
No problems have yet been encountered with TSV infecting native cultured shrimp species (i.e. P. monodon) in Asia, although P. monodon and P. japonicus appear to be largely refractory to TSV (Brock et al., 1995). Penaeus chinensis (and others) have been experimentally infected with TSV (Overstreet et al., 1997). Together with the mutative capacity of RNA viruses like TSV, this illustrates the potential for infection of native species and is a major cause for concern.
It has been reported that pathologic viruses could be transmitted to native wild penaeid shrimp populations (Overstreet et al., 1997; Joint Subcommittee on Aquaculture [J.S.A.], 1997), thus introduced alien shrimp viruses may be capable of infecting native wild shrimp populations.
Taura Syndrome Virus has been detected in wild P. vannamei escapees in the United States, but appears to have had minimal impact on wild shrimp populations (Brock, 1997; GMFS Web site; OIE Web site). Taura Syndrome Virus appears to occur largely as a sub-clinical infection in populations of wild shrimp (Brock et al., 1997).
There is some evidence of TSV in the wild populations of P. monodon around the southwest coast of Taiwan Province of China during 2000, although pathological effects on its new host were not noted and they appear largely unaffected (IQ2000 Web site). Penaeus japonicus is also known to be refractory to TSV, but the effects of TSV on native stocks of wild Asian P. indicus and P. merguiensis are not known and are a definite cause for concern. This is especially worrying since TSV is a highly mutable RNA virus and could mutate into a more virulent form for native Asian shrimp, as it has done in Latin America (Flegel and Fegan, 2002; Lightner, 2002).
There are speculations that IHHNV originating from United States culture facilities may have caused the closure of the Mexican shrimp fishery from 1987 to 1994 and the loss of millions of dollars, since wild P. stylirostris (and other less prevalent native species) proved highly susceptible to IHHNV (Lightner, 1996b; J.S.A., 1997). IHHNV is commonly found in wild shrimp on the Pacific coast of Latin America and throughout Asia, from where it probably originated (OIE Web site; Lightner, 2002). In Asia, IHHNV is not thought to cause many problems, since P. monodon, P. indicus and P. merguiensis are all refractory to the disease, having spent a long time cohabitating with it (Flegel and Fegan, 2002).
Since WSSV was first reported in the United States of America in 1995, it has been found in cultured and wild shrimp, crabs and freshwater crayfish at multiple sites in the eastern and south-eastern United States including Texas (Lightner, 1999). WSSV-positive shrimps and crabs have been found regularly in Texas from 1998, although the effects of WSSV on these wild populations remain unquantified (APHIS Web site). Despite the fact that WSSV was reported as eradicated from shrimp farms in the United States in 1997, it is still found in wild stocks in the Gulf of Mexico and the southeast Atlantic states and so is probably now established (Lightner, 2002).
WSSV is also found in wild shrimp throughout Asia, but again, its effects on the wild stock remain unclear. However, since WSSV is easily passed from spawners to their larvae (if the eggs and nauplius are not thoroughly disinfected), its effects in the wild population could be greatly affecting the Asian P. monodon culture industry.
Similarly, LOVV was found in wild spawners from the Andaman Sea off Thailand by Donald Lightner in 2002. It is thought that this virus might be the cause of the slow-growth phenomenon currently affecting cultured P. monodon in Asia (Timothy Flegel, per. com.), and if so, it is having a huge economic impact on the Asian shrimp culture industry.
In addition to direct effects on production, the impacts of diseases are particularly felt by small-scale farmers who, especially in Asia, represent the backbone of many coastal communities. Their very livelihoods are threatened through reduced food availability, loss of income and employment, social upheaval and increased vulnerability. Crop losses to disease for this sector of society may determine whether or not those families are below the United Nations poverty threshold (Fegan et al., 2001). In Mainland China, for example, the WSSV epidemic in 1993 affected the lives of 1 million people, and has continued to have effects to this day (Jiang, 2000).
Similar effects have been noted from Latin American countries. In Ecuador for example, within the first year of the WSSV epidemic in 1999, the disease also lead to the loss of 26 000 jobs (13 percent of the labour force), the closure of 74 percent of the hatcheries, a 68 percent reduction in sales and production for feed mills and packing plants, 64 percent layoffs at feed mills and a total of 150 000 jobs lost in the shrimp farming industry (Alday de Graindorge and Griffith, 2000). Although production has been slowly increasing since then, the Ecuadorian industry remains at less than 45 percent of its maximum in 1998 prior to the WSSV epidemic, effectively putting production levels back 16 years, to those achieved in 1987 (Figure 2).
14 The consortium on shrimp farming and the environment has produced numerous thematic reviews and case studies related to this subject to more information please visit http://www.enaca.org
15 See http://www.oie.int/
17 A new FAO document on surveillance and zoning provides advice and guidance for countries to establish surveillance and zoning programmes to reduce disease risks. Subasinghe, R.P.; McGladdery, S.E.; Hill, B.J. (eds.). Surveillance and zoning for aquatic animal diseases. FAO Fisheries Technical Paper. No. 451. Rome, FAO. 2004. 73p.