1995, 18, 263-271

Factors affecting outbreaks of epizootic uleerativesyndrome in farmed fish in Bangladesh*

M. A H M E D ' & M. A . R A B ' 'Internationat Center for Living Aquatic Resources Management

(ICLARM). Metro Manila. Philippines, atut 'Departtnent of Econotntcs. Istatnic University. Kusttna. Bangladesh

Abstract. Among 257 Bangladesh fish ponds investigated, 46% were affected by epizooticuleerative syndrome (EUS) either fully or partially. Thai silver barb, Puntius gonionottis(Bleeker), eulture ponds were worst affected (64%) by EUS, while all Nile tilapia,Oreochromis nilotictts (L.), monoeulture ponds remained unaffected. Stocking of silver barbfor eulture, use of piseiddes as a means of removing predators or unwanted species prior tostoeking of cultured species, and eulture of fish in previously derelict ponds are factorswhich significantly affected the probability of occurrence of EUS. Choice of species otherthan silver barb and use of lime during the post-stocking period signifieantly affected theprobability of pond stocks being less adversely affected by EUS.

Introduction

Outbreaks of epizootic ulcerative syndrome (EUS) have become a common phenomenon bothin high-density commercial and less-intensive farm aquaculture in Asia, adding an element ofrisk to investment. The economic impact of fish lost because of disease outbreaks has beetisevere in recent years in countries like Bangladesh, Thailand and the Philippines (Lilley,Phillips & Tonguthai 1992). Improving the understanding of EUS and analysis of underlyingphysico-chemical and environmental factors in existing aquaculture systems is critical for mostof the Asian countries, where development of aquaculture is seen as a complementary meansof increasing food production, income and employment from small-scale family farms.

Under a collaborative project between the Government of Bangladesh and the InternationalCenter for Living Aquatic Resources Management (ICLARM), operators in 257 out of 634small waterbodies (ponds and ditches) in four target unions of Kapasia Thana in GazipurDistrict were provided with extension services during 1991-1992 (Ahmed 1992; Ahmed, Rab& Bimbao 1993). Farmers received technical assistance on pond preparation, technologyselection, stocking rates, rearing and harvesting. Three general culture systems: Thai silverbarb, Puntius gonionotus (Bleeker); Nile tilapia, Oreochromis niloticus (L.); and polycultureof rohu, Labeo rohita (Hamilton), catla, Catla catla (Hamilton), mrigal, Cirrhimis mrigala(Hamilton), silver carp, Hypophthalmichthys molitrix (Valenciennes), common carp, Cyprinuscarpio L., and grass carp, Ctenopharyngodon idella (Valenciennes), were recommended, basedon individual preferences and consistent with the waterbody characteristics and resources ofindividual farmers (Gupta 1992). All these technologies were designed as low cost and lessreliant on commercial feed and fertilizers, promoting the use of on-farm resources andby-products (Lightfoot, Gupta & Ahmed 1992). While large-size (more than 600m') perennialponds were used for carp polyculture, most of the silver barb and tilapia culture ponds weresmall (less than 600m^) and shallow seasonal ponds (Ahmed, Rab & Bimbao 1995). Thedistribution of ponds under the three culture choices were: 124 carp polyculture ponds, 112

* ICLARM Contribution No. 1022.Correspondence: M. Ahmed, c/o ICLARM, MC PO Box 2631, 0718 Makati, Metro Manila, Philippines

264 M. Ahmed and M. A. Rab

silver harb ponds and 23 lilapia ponds. However, 42 ponds under carp polyculture wereadditionally stocked with silver barb, while eight ponds with silver barb culture were additionallystocked with Nile tilapia.

All of the ponds were stocked during July and August 1991 following pond preparation thatincluded removal of predators and unwanted species, application of organic and inorganicmanures, and treatment with lime (calcium carbonate). During the course of culture operations,many farmers reported the occurrence of EUS. The outbreaks took place toward the onset ofwinter (November-December 1991). This paper gives an account of the prevalence of thedisease in the cooperating farmers' ponds and discusses the factors related to the outbreak ofEUS.

The occurrence of fish disease is commonly linked to the deterioration of the aquaticenvironment (Asian Development Bank and Network of Aquaculture Centres in Asia 1991).Certain environmental factors are believed to be important in the case of EUS outbreaks infarmer-operated ponds in the Asian region (Lilley et al. 1992). Remedies have been soughtthrough improvements and maintenance of a better environment for fish. An attempt has beenmade in this paper to investigate important aspects of pond management, soil characteristicsand farming history to determine their influence (in a probability sense) on the occurrence ofEUS as well as the extent of damage of stocks in EUS-affected ponds.

Materials and methods

Information regarding the outbreak of EUS and intensity of damage to fish stocks in the pondswere compiled for 257 cooperating farmers' ponds located in several clustered villages ofKapasia Thana in Gazipur District of Bangladesh under the above mentioned project. Disease-related information, such as number of ponds affected by EUS, intensity of the disease in theaffected ponds, species affected and assessment of damage to the fish stocks in the affectedponds were collected by the project extension staff. Some of the variables such as previoushistory of disease, culture status and age of ponds were pooled from a previous survey of smallwaterbodies (ponds and ditches) in the area (Ahmed 1992).

Analytical methods

Factors affecting the chances of EUS occurrence in fish ponds or the extent of loss of fish stockcaused by EUS can be analysed with binary choice models, an econometric analysis that hasbeen found appropriate when the dependent variable assumes a choice between two alternatives(Pindyck & Rubenfield 1981). Several authors [e.g. Maddala (1983) and Capps & Kramer(1985)] pointed out a number of deficiencies in the linear probability estimation of this kind ofmodel, suggesting instead the use of a monotonic transformation such as logit or probitspecification. Logit and probit specifications produce comparable results and guarantee thatpredictions lie within unit intervals (Capps & Kramer 1985). However, the difference is thatthe probit model assumes a normal probability distribution, while the logit model assumes aIo2istic or lo£ normal distribution. The choice between the two is usvialiy arbitrary and islargely a question of convenienee (Hanushek & Jackson 1977). A logit model was selected forthe present analysis and maximum likelihood was considered a preferred estimation technique(Capps & Kramer 1985).

EUS in fartned fish in Bangladesh 265

Using the logit analytical tool, two separate models were specified for the analysis of factorsrelated to EUS in farmed fish ponds in Bangladesh. Model I analyses the factors affecting theprobability of occurrence of EUS, while Model II analyses the factors explaining the extent ofdamage to fish stocks in the EUS-affected ponds.

Model I assumed the outcome occurrence and non-occurrence of EUS as a dependentvariable (Y,), which is dichotomous (1 for occurrence and 0 for non-occurrence). Model IIdealt only with the EUS-affected ponds and its dependent variable (Yz) is also dichotomous(1 for fully damaged ponds and 0 for partially damaged ponds). For the purpose of the presentanalysis, EUS-affected ponds in which most of the fish were infected, leading to death or lossof at least 75% of the stock, were considered fully affected. The number of samples for ModelI was 257 ponds and for Model II 107 ponds.

The explanatory variables identified for the two models were defined as follows:Xi = technology type

Model I(1) if adopted technology was silver barb (includes ponds in which some Nile tilapia

were added)(0) otherwise (Nile tilapia or earp polyculture, including ponds in which some silver

barb were also added)Model II(1) if adopted technology was silver barb (includes ponds in which some Nile tilapia

were added)(0) otherwise (carp polyculture ponds, including ponds in which some silver barb were

additionally stocked)X2 = technology type

Model I(1) if adopted technology was Nile tilapia(0) otherwiseModel II(1) if adopted technology was carp polyculture in which silver barb were additionally

stocked(0) otherwise

X3 = technology typeModel I(1) if adopted technology was carp polyculture(0) otherwise (including ponds in which some silver barb were added)Model II(1) if adopted technology was carp polyculture (excluding ponds in which some silver

barb were additionally stocked)(0) otherwise (silver barb ponds, including those in which Nile tilapia were additionally

stocked; or carp polyculture ponds in which silver barb were additionally stocked)X4 = method used to clear predators prior to stocking

(1) if piscicide was used(0) otherwise

X5 = effects of flooding(1) if pond was affected by flooding(0) otherwise

X^ = previous farming status

(I) if the pond was farmed(0) otherwise

X7 = previous history of disease(1) if affected by disease in the past(0) otherwise

Xs = pre-stocking application of lime(1) asers(0) non-users

Xc, = post-stoeking application of lime(1) users(0) non-users

Xm = age of the pond(1) newly excavated(0) otherwise

Xii=soil type(1) reddish sandy soil (lateritic soils)(0) otherwise

Nine of the eleven variables defined above were used by each of the two models. Model Idropped variable X,, while Model II excluded variable Xj to avoid a singular matrix. Also,Model 1 excluded variable Xy, while Model II excluded variable X ,̂ Both the models wereestimated using the computer software LIMDEP (Limited Dependent Variable). To find themaximum likelihood values for the coefficients, LIMDEP uses Newton's method in whichvariance matrix is estimated with second derivatives of the log likelihood.

Results

There were 117 ponds (46%) affected by EUS, either fully (18%) or partially (28%) during the1991-1992 production cycle. In terms of area, EUS-affected ponds occupied nearly 8-8ha(43%) of total waterbodies under fish culture. Amongst the three culture systems practised,silver barb culture ponds were worst affected. As much as 64% of silver barb monocultureponds were affected by EUS compared to only 35% of carp polyculture and none of the tilapiamonoculture ponds (Table 1).

Ponds that were cleared of predators and unwanted species by use of piseieides (phostoxyn)prior to stocking of cultured species, showed the highest occurrence (58%) of EUS, On theother hand, only 17% of newly excavated ponds were affected by EUS (Table 1), Applicationof lime was suggested by extension workers during preparation of ponds prior to stocking andduring rearing as a means of reducing turbidity and maintaining good water quality. Nosignificant difference was observed between the users and non-users of lime during pondpreparation in terms of occurrence of EUS and extent of damage of fish stock in EUS-affectedponds (Table 2). Average application of lime during pond preparation was higher for theunaffected ponds (0-71 kg 40m^') than the partially affected ponds (0-59kg 40m^-) or fullyaffected ponds (0 52kg 40m^'), although the differences were not statistically significant.Amongst the EUS-affected ponds, lime use was significantly greater in the partially affectedponds than the fully affected ponds (Table 2),

Some 56% of the flooded ponds were affected by EUS, against 45% for the ni-freeponds (Table 3). Ponds which had a previous history of disease were found to be ai ,-d byEUS in higher proportions. Out of 117 ponds affected by the disease, 64% had a ious

EUS in farmed fish in Bangladesh 267

cthods, Kapasia Tliana, Gazipur District, Bangladesh, 1991-1992

with liveadded"

Predator re:

pi cieide use'-

not cleaned

Theseadditioi

prcvale'These

" Remc

were pondiall> tockedp polyculturncc of EUSponds were

lally stocked

unde:1 howeponithan tundei.

r silver barb cultuever, none of the

he major carp.: carp polyculture

re wiitilapi

with

th a sm:a weren carp <

a small

all numaffecte(

numbe

/ated ni

ber of tilapiai by EUS,

T of silver bar

onds

history of disease. Also, ponds that were previously derelict (physically unsuitable for fishculture because of silted bottom, high abundance of aquatic weeds or broken dykes) showed ahigher occurrence of EUS than those that were farmed or were in farmable condition. Eighty-three per cent of the previously derelict ponds that were brought under fish culture during1991-1992 suffered from EUS (Table 3),

The summary statistics of logit regression analysis for the two models specified are shown inTable 4, The log likelihood tests indicate that the amount of variation explained in each modelis significantly different from zero. Table 4 shows two separate measures of goodness of fit forthe two models. The first is the likelihood ratio index (LRI) or McFaddan's R^ (Harper,Rister, Mjeldc, Drees & Way 1990), although this is not comparable to R- reported inordinary least squares (OLS) regressions. The values of McFadden's R^ are 0-16 and 0-34 forModels I and II, respectively. These are typical for logit models (Sonka, Hornbaker & Hudson1989; Harper et al. 1990), The second measure shows the predictive power of the modelsdefined by the proportion of correctly predicted outcomes. The logit regression correctlypredicted almost 71% of the cases in Model 1 and 81% in Model II,

Influences of the explanatory variables on the probability of outcomes in both the models

Tabi t 2. DisiribDislriei, Bangl;)«

used (kg 40m -)

During pond preparati

Mean use (kg)

D u n n g rearing

non-userMoan use (kg)

Combined mca

period:

n ( k g )

* Significant at 1% leve** Significant at 2% levet Figures in parentheses

U32

0-5((1.4

0 1(0-30-7

18-37)

1125

99*•28)17**

(0-626)

5516

0-587(0-463)

120-504*

(0-583)1-130**

(0-818)

0-706(1-626)

5981

0-376(1-25)1-080

(2-82)

4663

0-653(1-295)

128 100129 100

0-411(1-03)1-060

(2-24)

Table i. Prevalence of disease by oeeurrence of flooding, previous disease history and physicponds in Kapasia Thana , Gazipur District, Bangladesh, 1991-1992

No. % No. % No. % No . %

Occurrence of flood:yes 9 39 4 17 10 44 23 100no 37 16 67 29 130 55 234 100

Previous history ofdisease:

yes 31 20 44 29 77 51 152 100no 15 14 27 26 63 60 105 100

Previous physieal

farmed/farmable 43

are shown in Table 5 in terms of coefficients and f-values. Of the nine variables analysed, theprobability of fish ponds in Kapasia during the 1991-1992 produetion period being affected byEUS was significantly associated with six of these variables: (a) the silver barb technology(Xi), (b) the tilapia technology (X,), (c) method of removal of predators and unwanted species(X4), (d) previous farming status (Xs), (e) age of pond (X,o), and (f) soil char . ristics ofthe pond (Xj,)-

It appears that the adoption of silver barb culture was directly associated RUS,increasing the probability of occurrence of EUS. On the other hand, the relationshi .genEUS and tilapia culture was negative. The probability of EUS increased with t of

EUS in farmed flsh in Batigladesh 2(iS

lil

Va

X,

X2

X j

x,X,

x<,Xy

Xs

Statistics

Nutnber of iterationsLog likelihoodRestrieted (slopes = 0) log-LLikelihood ratio index (LRI)"Likelihood ratio test''Correetly predicted (%)

" Equivalent to MeFadden's R^ (i" Test that all slope eocffieietits a;are significant at 1% level; degre

cehhood estimates for Models I and

Model I

jiable Coefficient /-vak

1-084 3-66*(0-296)

-2-963 2-78*(1-066)

M49 4-15*(0-359)0-682 1-30

(0-524)-1-218 3-24*(0-376)0-325 1-05

(0-309)0-064 0-21

(0-306)

Model I

5-148-65-176-32

0-15755-3471-48

Model il

5-48-811-74-018

0-34150-41580-53

iee Harper ei al. 1990).re equal to zero (both modelses of freedom = 8).

1 II in Kapasia Thar

Ml

le Coefficient

0-488(0-635)

-1-513(0-891)

** -0-522(0-645)

-0-177(0-807)

** -0-242(0-698)0-413

(0-574)

la, Gazipur Di

adel II

: f-value

0-77

1-70**

0-81

0-22

0-35

0-72

-1-971(0-522)

1-U3(1-35)1-042

(0-552)

*** Significant at 1% level.** Significant at 5% level.* Significant at 10% level.

' Harper et al. (1990) used a 20% level of signifieanee based onMandersheid's (1965) justification for use of higher signifieanee levels incases where relationships are less known.

piscicide (phostoxyn) as means of removing predators and unwanted species from the ponds

prior to stocking of cultured species. Inclusion of ponds previously not farmed or in derelict

condition inereased the probability of EUS. Fish culture in newly exeavated ponds lowered

the probability of occurrence of EUS, while ponds having reddish sandy soil inereased the

probability of EUS.

In the ease of probability of extent of damage to fish stocks in the EUS-affeeted ponds

270 M. Ahmed and M. A. Rah

(Model II) only (hree variables: (a) carp polyculture (X,), (b) use of lime post-stocking (X9)and (c) soil characteristics (X,,) were statistically significant. The negative sign of the variableX, implies that the intensity of damage to stocks due to EUS would be expected to be higheriov ponds using silver barb. Likewise, the negative relationship between the use of lime duringpost-stocking management of the pond (Xy) implies that lime would contribute to control ofspread of infection, thereby lowering the probability of damage to fish stocks. The significantpositive coefficient for the variable X,, implies higher probability of EUS in the ponds thathave reddish sandy soils. Within the project area, it was observed that ponds having reddishsandy soil suffered from water turbidity, exhibiting a less than ideal environment for fishstocks.

Discussion

A broad class of variables determining fish pond environment appears relevant to the prevaleneeand effects of EUS in farmed ponds in Bangladesh. Species selection also made a majordifference between ponds in terms of prevalence and effects of EUS. Silver barb appeared tobe most susceptible to EUS, followed by major earp (L. rohita, C. catla and C. mrigala) andChinese and common carp. Lilley et al. (1992) also reported that Chinese and common carpshowed some resistance against EUS.

Post-stocking management of ponds such as correct and timely use of lime could reduce theseverity of EUS to a large extent, especially in terms of death rates of fish. The benefits of theuse of lime, particularly during the post-stocking phase, was apparent. Its eontribution as adisinfectant agent, means of increasing pH or reducing acidity, and above all, redueing waterturbidity had an overall effect on control of infectious agents and produced a better responseto fertilizer use (Boyd 1990). Moreover, newly excavated ponds whose water quality andmanagement were expected to be obviously better, suffered little from EUS. Cleaning ofponds by drying and netting were more desirable (i.e. less harmful to ponds environmentally)than the use of piscicide.

Flooding, though a common phenomenon, particularly for ponds located in marginal lands,did not show any significant influence on the probability of occurrence of EUS. Generally,flooding brings the risk of water quality deterioration through introduction of carrier fish or bydirectly introducing infectious agents. Since EUS occurs during the dry season, the effects offlood-related water quality deterioration may have been less detrimental.

In the context of Bangladesh aquaculture development, the effects of flooding, history ofdisease, physical condition of ponds and species selection on the likelihood of EUS need moreanalysis. Recent trends in aquaculture development have shown the potential for utilizingmarginal lands and seasonal waterbodies, where short-cycle fish species sueh as silver barbcould be easily grown. Therefore, the apparent suseeptibility of silver barb to EUS will requiremore careful investigation. The investigation of EUS is also more important in polyculturesystems, which are very common in Bangladesh. The farms may run the risk of EUS becauseof the presenee of one or more EUS-prone species as carriers in the ponds.

Finally, the procedure used in this paper is useful for a wide range of data colleeted byresearch and extension professionals. The resulting information will be useful in selectingappropriate technologies and imparting education and training programmes at the fish farmerlevel. Extension specialists can analyse survey data to identify those characteristics of fishponds most likely to influence the oecurrence of EUS and quantify the risks from EUS inaquaculture.

EUS in fartned fish in Bangladesh 271

paper. The assistance of Messrs M, Rahman and B, Mia in computerization and data analysesis acknowledged.

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