The rise of the syndrome – sub-optimal growth disorders in farmed shrimp

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The condition described as monodon slow growth syndrome (MSGS) has been reported from many countries. Though not leading to mortality, retarded growth at the pond level results in significant economic losses. This review focused on several key syndromic conditions that the sector is facing and discuss how new approaches to detection and description of (particularly) syndromic conditions are both now require.

Several potential pathogens have been identified from affected shrimp; however, no confirmed causal relationship has yet been established. Moreover, it has been well recognised for quite long that diseases in aquaculture are an expression of a complex interaction between host, pathogen and environment.

The major bacterial pathogens/diseases affecting farmed shrimp include acute hepatopancreatic necrosis disease (AHPND) caused by toxins encoded by plasmid-bearing genes of Vibrio parahaemolyticus, septic hepatopancreatic necrosis (SHPN) or ‘vibriosis’, caused by Vibrio harveyi, V. parahaemolyticus, V. alginolyticus and other species, necrotising hepatopancreatitis (NHP) caused by an intracellular bacterium, Hepatobacter penaei.

Although not a new phenomenon, shrimp aquaculture is currently affected by several syndromic diseases of unknown etiology. The elucidation of these etiologies is necessary to determine the pathogen(s) involved, other potential causes, and necessary preconditions for detection and control of disease.

Further, it will be important to determine which diseases can be categorised as ‘trade-limiting’ (disease caused by pathogens having international trade implications) and ‘yield/production-limiting’ (chronic syndromic conditions leading to significant production losses but not having direct bearing on international trade). This review focuses on the various manifestations of slow/retarded growth in penaeid shrimp species.

Sub-optimal growth disorders (SoGD) in farmed shrimp

During 2002, MSGS recorded in shrimp-growing areas across Thailand associated with approximately 36% (approximately USD 300 million) losses in annual production volume of farmed P. monodon. At that time, among the most serious disease problems affecting P. monodon farming, MSGS was ranked third after WSSV and YHV.

Almost simultaneously (mid 2004), a similar occurrence of unusual slow growth was reported from a commercial P. monodon farm in East Africa. The occurrence was characterised by wide variation in size, without abnormal mortality and slow growth (mean body weight of retarded animals was reported to be 30% less than expected) Penaeus monodon farmed in India also displayed differential growth which hampered production significantly.

In a study conducted on the economic impact of diseases (during 2006–2008), Kalaimani et al. (2013) estimated that slow growth syndrome and ‘white gut disease’ in P. monodon in India resulted in a production loss of 5726 MT, equating to Rs.1.2 billion (USD 21.64 million) annually.

Pathogens associated with suboptimal growth in P. monodon. Known shrimp viruses and other pathogens.

Retarded growth in shrimp has been reported to be associated with several pathogens. Before MSGS was reported from farmed shrimp in Thailand, hepatopancreatic parvovirus (HPV) was suggested to cause slow growth in P. monodon. Flegel et al. (1999) also reported HPV in retarded shrimp, and they found negative statistical correlation between severity of HPV and length of shrimp.

Retardation of growth in farmed shrimp has been noticed as one of the outcomes of PmNV infection. Further, as the route of PmNV to the grow-out system is through contaminated post-larvae derived from virus infected broodstock, trans- mission may be prevented through screening of broodstock and post-larvae

Studies have revealed that multiple viral infections are common in normal and stunted shrimp, suggesting that identifying known pathogens from affected shrimp constitutes only one approach and a single pathogen aetiology for slow growth in shrimp is unlikely.

Chayaburakul et al. (2004) suggested that MSGS was independent of the intensity of infection of the viruses but dependent on some other overriding factors such as unknown pathogens, non- pathogenic factor or genetic variants of known pathogens tentatively named monodon slow growth agent (MSGA).

Reports indicate the wide range of disease-causing agents identified/isolated/associated with retarded/slow/ stunted growth in P. monodon from different parts of the world, though no conclusive evidence of their association could be proved.

Laem-Singh virus.

Laem Singh virus has been observed by in situ hybridisation (ISH) in both normal and MSGS-affected shrimp, reinforcing that LSNV is unlikely to be the sole cause of MSGS.

TEM and ISH analyses showed that LSNV could be detected in tissues of the eye in only small shrimp from MSGS ponds, and an association (but not the reason for it) was demonstrated between pond level retarded growth and LSNV in eyestalks, but that eyestalks/brain tissue was not infected in LSNV-positive ponds with normal CV.

It is important to acknowledge that LSNV which has been reported from India and other countries in Asia has no conclusive causal relationship with slow growth.

After the discovery of LSNV, Flegel (2008) proposed that LSNV is a ‘necessary but insufficient’ cause of MSGS; with other pathogens or environmental factors also important in the manifestation of the condition. It is essential to consider the CV of shrimp size/weight in the pond in question when determining whether that pond is subject to MSGS.

The case definition for MSGS is a pond definition, not an individual shrimp description, as it has to meet the condition that the shrimp population it contains has a CV for 35% or more for weight distribution shifted to less than marketable size.

Some authors attributed the growth retardation reported in MSGS to the suppression of the release of CHH peptide in the optic lobe, which results in decreased hepatopancreatic glycogenolysis and persistent hypoglycaemia. The observations made in this study are of significance in that it can be further explored for using these parameters as biomarkers of retardation in shrimp.

Relation of abiotic and other factors in sub-optimal growth.

Despite identification of several pathogens including viral, bacterial and eukaryotic from MSGS-affected P. monodon, a single-agent aetiology remains elusive. It is reasonable to discount a specific environmental parameter responsible for the retarded growth, as MSGS occurred over a wide geographical range.

Slow growth in Penaeus vannamei

Though a range of factors have been suggested as the cause of RDS in P. vannamei, which included excessive antibiotic use in hatcheries, nature of post-larvae originated from captive, ablated broodstock, deteriorating pond conditions due to accumulation of unknown pollutants, poor quality feed, genetic factor etc., Kalagayan et al.

(1991) showed that the major factor responsible for RDS was IHHNV It is recognized that two of the most powerful determinants of profitability are shrimp growth rates and market value and, therefore, factors which are having negative impact on the growth rate and size of the animal and, thereby, the market value, will significantly affect the profitability.

Slow growth and hepatic microsporidian infection EHP had been recorded from shrimp collected from ponds not exhibiting WFS as well as the shrimp collected from ponds that have recovered from WFS. These, along with oral challenge tests, indicated that EHP is not the sole causative agent of WFS in P. vannamei. EHP in combination with other enteric pathogens responsible for septic hepatopancreatic necrosis (SHPN) and potentially other unknown factors likely underlie the clinical syndrome described as WFS.

“EHP infections have also been associated with other disfunctions of the gut system, including AHPND and, septic hepatopancreatic necrosis (SHPN) proposing that EHP infection may be a risk factor for both of these other diseases.”

EHP was initially considered to be a minor disease threat in shrimp farming regions due to its initial low prevalence and lack of severe disease outbreaks leading to mortality. However, high prevalence and higher disease intensity status are now more commonplace, associated with poor performance in grow-out.

Although some microsporidians are ubiquitous in nature and do always associate with disease and mortality, reports from farmers as well as researchers indicate that the hepatic infection with EHP results in significant growth retardation and a resultant increased variability in shrimp size that is not evident until 2–3 months of cultivation.

The contribution of pathogens that are ‘necessary but insufficient causes’ to sub-optimal disease at the pond level is not necessarily predictable.

New insights

Although significant attention has been paid to viral pathogens such as WSSV and YHV over the past two-and- a-half decades due to their virulent nature and sudden and large scale mortality, it may be equally important to pay attention to chronic slow growth conditions which have the potential to significantly affect production metrics in the shrimp sector.

A critical examination of research carried out on these slow growth syndromes, as provided here, reveals not only significant potential for contradictory interpretation of evidence associated with specific observations of slow growth syndromes but also a lack of consistency in the associated diagnostics that are applied when attempting to define aetiology

Although the majority of studies on MSGS (in P. monodon) point to the involvement of multiple viral or virus like agents, especially LSNV and hepatopancreatic viruses such as HPV or MBV, the only viral pathogen that has been proposed as the potential cause of slow growth in P. vanammei is IHHNV. However, a common pathogen identified in both shrimp species is the hepatopancreatic microsporidian EHP.

Another consistent observation made in MSGS cases is the presence of bacterial lesions and, in certain cases, marked haemocytic inflammation and nodule formation characteristic of bacterial infection (similar to the septic hepatopancreatic necrosis (SHPN) caused by Vibrio sp.

“The evidence for bacterial co-infection indicates that multiple or concomitant infection could be a possible cause of slow growth syndromes in shrimp”

The ‘one pathogen-one disease’ paradigm has increasingly been realised as insufficient to explain many disease scenarios, and the pathobiome concept has recently been developed to promote a more multi- factorial perspective on disease aetiologies. The slow/retarded growth problem in shrimp clearly demonstrates the serious limitations of the conventional single pathogen approach and the need for more comprehensive approach to deal with such chronic conditions.

It also highlights the need for looking beyond viral pathogens and the standard requirement of complementing the PCR-based screening of post-larvae with conventional evaluation protocols of health status.

This is a summarized version developed by the editorial team of Aquaculture Magazine based on the review article titled “THE RISE OF THE SYNDROME – SUBOPTIMAL GROWTH DISORDERS IN FARMED SHRIMP” developed by: RAJENDRAN KOOLOTH VALAPPIL, GRANT D. STENTIFORD, AND DAVID BASS. The original article was published on FEBRUARY 2021, through REVIEWS IN AQUACULTURE under the use of a creative commons open access license. The full version can be accessed freely online through this link: https://www.researchgate.net/publication/349721825.

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