review of literature -...

Chapter II

Review of Literature

2.1 International status of intergrated farming

2.2 National status of integrated farming

2.3 Resident bacterial flora of fishes

2.4 Prevalence of fish diseases in aquaculture fish farms

2.5 Nutrient cycling by bacteria in aquatic systems

2.6 Degradation of organic materials by bacterial enzymes in

aquatic system

2.7 NPK profile of aquaculture farms

2.8 Multiple drug resistance among bacteria of integrated

farms

2.9 Serological characteristics bacteria from integrated farms

2.10 Influence of physico chemical parameters on aquatic

ecosystem

References

Chapter 2

Review of Literature

In recent years intensive fish culture is being practiced in the

brackish water, coastal water and fresh water impoundments of India and

aquaculture has been expanding rapidly, in an attempt to increase the

economy of our nation. This chapter aims to review the empirical and

theoretical information available from similar and related studies. A review

was conducted on the international and national status of integrated paddy

cum fish farming, diversity of bacteria from the different body parts of

cultured carps and wild fishes, bacterial load of water and sediment and its

diversity in aquatic system, prevalence of bacteria in nutrient enrichment in

integrated paddy cum fish farming, enzymatic activity of bacteria in

recycling of nutrients, characterization of the bacterial isolates from various

sources like fishes, water and sediment for their multiple drug resistance

and other serological properties and physico-chemical parameters of water

and soil in aquatic system.

2.1 International status of intergrated farming Integrated farming systems are new farming enterprises worldwide,

and the most efficient way of increasing self sufficiency of farm holdings

by increased resource utilization and thereby maximizing yields and

diversifying products. Stahl (1979) noted that decomposition of straw and

stubbles served as detrital supplements to prawns in aquatic ecosystems.

Khoo and Tan (1980) observed that introduction of herbivorous fish in rice

fields controlled weeds and reduced feeding cost. They also reported that

integration of fish farming with agriculture in Malaysia that the income

18 Chapter 2

from fish culture constituted 22 to 60 percent of farm income in single

cropped area of rice and 4 to 19 percent in double cropped area. They

concluded that fish formed a significant part of the total income of at least

60 percent of tenant farmers interviewed. According to them efficient

management was of utmost importance in increasing the profit margin. Nie

and Wang (1981) studied the relationship between rice and fish and found

that both benefit from each other. He called this mutualistic association and

this provided the theoretical basis for the expansion of rice-fish culture in

China. The Chinese were the pioneers of integrated farming and integration

of aquatic plant cultivation and fish farming has been in since the second

and first century B.C. (CFFCEB, 1982).

Guerrerro et al., (1982) reported the beneficial effects of fresh water

prawn as a stocking component in rice-fish integrated situation and noted

that when Macrobrachium rosenbergii was cultured along with rice, rice

plants provided feeding surfaces essential for the species. Miltner et al.,

(1983) found that rice straw detritus were good feed supplements for

prawns. Sevilleja and Lopez (1986) noted a significant saving in fertilizer

cost in rice production fields previously utilized for fish production.

Sevilleja (1986) demonstrated that rice fish integrated farming yielded

about 40% more income as compared to monoculture of rice. FAO (1988)

reported the observations of Chinese scientists on the apparent advantages

of rice-azolla-fish system and noted the increased grain yield, fish biomass,

and soil fertility, decreased incidence of pests, weeds and diseases.

Hu Bantong (1990) reported that 50kg of fish can produce enough

pond humus to fertilize six hectare of cropland. Light foot et al., (1990)

observed that integrated rice-fish system offered the possibilities of

Review of Literature 19

increasing rice yields by as much as 15% while continuous monocropping

of rice led to a decline in soil microbial biomass and fertility.

Identifying the importance of fish in Asian Rice Farming System, a

net work to popularize this practice had been mooted by IRRI and

ICLARM (Lightfoot et al., (1990). Costa Pierce (1992) reviewed the rice

fish farming practices of Indonesia and reported an annual yield of 63, 218

tones of fish from this system. Moody (1992) observed that under rice-fish

system, Cyprinus carpio not only eradicated weeds and algae in the rice

fields but also saved the cost on ploughing and harrowing. Nie et al.,

(1992) traced the mutualism of rice and fish farming and concluded that

grass carp controlled weeds thoroughly as compared to hand weeding and

herbicides. Wang (1992) suggested that, one of the most important farming

models suited for rice-fields is azolla-rice-fish integration.

The common carp Cyprinus carpio appeared to be better suited to

rice field environments of Philippines than Nile tilapia. Role of fish in pest

control in rice farming has been studied by Yuan (1992) in China and

reported that rice plant hoppers were reduced from a maximum of 104,000

to 70,776/hectare. Rice leaf rollers decreased from 210,000 to 120,000 per

hectare and grass carp (Ctenopharyngodon idella) were particularly

effective in controlling sheath blight. Experiments conducted with grass

carp (Ctenopharyngodon idella) in a rice-fish system in China showed that

they increased rice yields generally by 10% or more. C.idella controlled

weeds and harmful insects. By eating grass, they reduced the need for

farmers labour for weeding. C. idella faeces also helped to fertilize the rice

fields, Nie et al., (1992).

20 Chapter 2

Halwart (1994) reported that the rice crop benefits from the

presence of fish in terms of reduced pest incidence. Li and Paw (1994)

described that the rice fish culture in China is in the process of development

from extensive culture to semi intensive culture, from monoculture to

polyculture, and from self sufficient natural economy to commercial

economy.

Studies conducted by Halwart (1994) in Philippines on the potential

of biological control of common carp (Cyprinus carpio) and Nile tilapia

(Oreochromis niloticus) has reported that although fishes are not the single

solution to insect pest problems in rice fields, they do contribute to limiting

pest abundance and support the army of natural enemies of rice pests.

Common carps are found to be effective biocontrol agents against apple

snail pomacea (Pila globosa), the paddy pest in Philippines. Grass carps in

rice fields when polystocked with other species were found to manure and

fertilise pond water and generate natural food to filter feeders and

omnivores (Yang et al., 1994).

Fagi and Syamsiah, (1994) postulated that under optimum stocking

intensities in rice-fields, Cyprinus carpio enhanced availability of

phosphorus to rice. Fang et al., (1994) in the studies of pond water and

sediments of polyculture fish ponds observed the correlation between the

load of bacteria in fish pond and several environmental factors monitored.

Israel and Sevilleja (1995) reported that in Philippines rice fish culture

leads to higher rice production compared to rice monoculture. Shehadeh

and Feidi (1996) reported in Egypt, which is the second country in terms of

rice-fish area after China with 172. 800ha, almost 32% of the total

aquaculture production was contributed through rice-fish systems. The


potentials of the integrated farming technology for transforming existing

traditional farming systems to become more sustainable in Ghana has been

reported by Lightfoot et al., (1996).

The integrated farming technology has became an appropriate

method for replenishment of decimated fish populations in the rice fields

with improvement of incomes, nutrition and environment for sustainable

operations and resource management to support healthy human life in

Bangladesh (Mazid and Hussain, 1996). Aldon (1997) reported the practice

of simultaneous rearing of crustaceans such as giant fresh water prawn M.

rosenbergii along with rice during the non saline phase in coastal fields of

Vietnam. He observed that approximately 80% of farm households in

Vietnam have their own small pond garden and canal for aquaculture.

Cagauan et al., (2000) reported from their case studies in Philippines that

fish and the nitrogen fixing aquatic fern Azolla and ducks integrated with

rice farming can result in nutrient enhancement, pest control, feed

supplementation and biological control.

2.2 National status of integrated farming Integrated farming system that depends on natural processes that

can convert organic wastes of one farming enterprise into useful byproducts

has been studied extensively by various authors, (Ardiwinata, 1957; Hora

and Pillay, 1962; Mears et al., 1974; Rabanal, 1974; Huat and Tan, 1980;

Chambers and Ghildyal, 1985; Richards, 1985; and Fresco and Poats,

1986). Country overviews on this system of farming have also been

provided for Bangladesh (Arce, 1985), China (Li, 1988) and India (Ghosh,

1992).

22 Chapter 2

Asia is considered to be the cradle of integrated crop-livestock -

fish farming and Sinha (1986) observed that the system helps to diversify

the income base of poor fisherman and small farmers. Reviews on

historical, socio-economic and ecological aspects of rice-fish farming by Li

(1988), Fernando (1993a), Halwart (1994), Mackay (1995), Choudhary

(1995) and Little et al., (1996) are available.

Ghosh (1980) while reviewing the prospects on integrated rice-fish

resource of 2.3 million hectare of deep water rice plots in the fresh water

sector, which would be used for rice-fish culture. According to his study

monocropped area under high monsoon precipitation is also potential areas

for utilization as fish/prawn culture systems during the summer fallow

period, particularly for raising prawns. Feasibility of monosex culture of

male tilapia (Oreochromis mossambicus) along with paddy in pokkali field

has been studied along the central coastal belt of Kerala and it was reported

that under the peculiar conditions of pokkali fields, Nile tilapia

(Oreochromis mossambicus) alone was found to be suitable for

simultaneous rice-cum-fish culture (Rajendran et al., 1981).

Muraleedharan (1981) in his article on “Resource use efficiency in

rice cultivation in low lying lands of Kerala” observed that inputs such as

human labour, bullock labour and fertilizers were not efficiently used in

cultivation of rice. Rajendran et al., (1981) conducted experiments in rice-

fish simultaneous culture in Pokkali fields of Kerala during 1977-78 and

observed that under ideal conditions production up to 183kg/hectare could

be achieved within 109 days period with Etroplus species. Since paddy

cultivation was not so economical, additional income gained through fish

culture was a great help to the farmers. There was also possibility of


increasing production of paddy as Etroplus had helped in removing

Hydrilla.

Purushan (1986) in his study on recent advances in paddy cum fish

culture observed that the culture of fish and paddy together could

potentially increase and stabilize income on rice farms and also paddy post

fish culture increased the total annual yield. The fish could be beneficial in

eliminating weeds, molluscs and mosquitoes thus reducing labour cost. He

also studied the scope of paddy cum fish culture in Kerala and found that

the rate of fish production in paddy fields stood much better and suggested

the introduction of this practice in Kayal lands of Kuttanad and Kole, in

addition to 26,000 hectare of Pokkali Fields.

The apparent advantages of the Chinese practice of rice Azolla-fish

system in terms of increased grain yield, fish biomass, soil fertility and

decreased incidence of pest, weeds and disease have also been highlighted

by FAO and SIDA, (1988). Lightfoot et al., (1990) observed that integrated

rice-fish systems offer possibilities of increasing rice yields by as much as

15%. According to him, fish not only contribute to nitrogen accumulation

through their faecal excrements in the rice fields but also reduce nitrogen

loss. Fish can convert food into body tissues more efficiently than any other

farm animals. The food conversion rate is known to be 1-5 times more in

fish. The practice of utilization of rice fields for sequential farming of fish

and prawn is an age old practice in the pokkali rice fields of Kerala. These

are brackish water fields adjoining the Vembanad Lake. The practice is

popularly known as Chemmeenkettu or prawn filtration.

Studies conducted by the Kerala Agricultural University at the

Regional Agricultural Research Station, Kumarakom indicated that in

24 Chapter 2

addition to rice production averaging three tons per hectare, fish yield

ranging from 600 to 1000 kg/hectare could be obtained by simultaneous

farming of rice and fish.

As compared to the practice of simultaneous farming which requires

several modifications to the rice fields to protect the fish from the inherent

risk of pesticide applications, rotational farming of rice and fish was shown

to be more advantageous as it permitted better management practices for

both rice and fish (Padmakumar et al., 1990). In their investigations, where

in Indian major carps, common carps and Etroplus and the giant fresh water

prawn Macrobrachium rosenbergii were polycultured, yield touched

1005kg per hectare without any additional expenditure on feeding or

manuring. The integrated rice-fish rotational farming system for low lying

rice fields tested and developed by the Kerala Agricultural University at its

Regional Research Station, Kumarakom and introduced in Kuttanad a few

years ago as demonstration trial in farmer’s fields has become an instant

success. As a result there has been even an increase, though marginal, in

the area under rice in the low lying fields of Kottayam between 1997-98

and 1998-99 from 13754 hectare to 14393 hectare.

The study conducted by Padmakumar et al., (1990) indicated that

integrated farming of giant prawns (Macrobrachium rosenbergii) in

channels of coconut garden in the wetland area, adjoining southern portion

of Vembanad Lake is economically viable.

Identifying the importance of fish in Asian rice farming system, a

network to popularise rice-fish farming has been mooted by IRRI and

ICLARM (Lightfoot et al., 1990). Ghosh and Chakrabarti (1990) reviewed

the different works on farming of fish in rice fields in India and observed


that monocrop rice fields under high monsoon precipitation and deep water

rice fields are ideal zones for integrated farming.

Kerala has extensive weed-checked water areas with low dissolved

oxygen suitable for the cultivation of air breathing fishes like Clarias

batrachus, Heteropneustes fossils, Channa striatus and Channa punctatus,

which have many cultural traits. Several culture fishes like Catla, Mrigal,

Rohu, Cyprinus has been widely cultured in fresh water bodies including the

paddy fields with supplementary organic feed (Sinha and Srivastava, 1991).

Growing the Chinese grass carp C. idella in integrated rice cum fish

farming system in eastern India increased the yield of rice by about 20%

and 35% and is attributed to the direct and indirect benefits of the control of

aquatic weeds and also to the additional manuring of the plots by grass carp

faeces. In the studies on the economic viability of poultry-rice and fish in

the lowland rice fields in Tamil Nadu, Rangaswamy et al., (1992) reported

an increase in profit margin by 60 per cent as compared to the conventional

farming practice.

Mukhopadhyaya et al., (1992) studied the relative advantages of

rice-fish integration in the deep water rice fields of West Bengal and

reported fish yields ranging from 263-1215kg/hectare. Tiwari (1993)

observed that a farming system involving flooded rice, poultry and fish had

a high degree of complementarity. The integration of fish and the nitrogen

fixing aquatic fern Azolla show promise for increasing the production

potential of the system.

Dube (1995) studied integrated aquaculture and found that, through

fish-paddy crop integration the production cost can be reduced to one third.

26 Chapter 2

It also reduced land erosion by 57 per cent. Weeds and insects were

controlled by fish as they feed on it. Fish cum crop integration led to

increased efficiency of resource utilization, reduced investment risk

through crop diversification and served as additional resource of food and

income. Influence of organic and inorganic fertilization on the growth and

nutrients of rice and fish in a dual culture system in Kharagpur, West

Bengal, India has been studied by Ghosh et al., (1995) and reported that the

total number of phytoplankton species as food for the fish under organic

manuring was more than under inorganic fertilization.

The integrated farming technology has become an appropriate

method for replenishment of nutrition and environment for sustainable

operations and resource management to support healthy human life in

Bangladesh (Mazid and Hussain, 1996). The potentials of the integrated

farming technology for transforming existing traditional farming system

into more sustainable system has been highlighted by Lightfoot et al.,

(1996). Singh and Swami (1998) in their studies in Punjab revealed that by

the integration of aquaculture with agriculture and use of supplementary

feed, a sustainable fish production of over 10 tones per hectare can be

easily obtained.

2.3. Resident bacterial flora of fishes The bacterial flora of living fish generally reflects the microbial

content of water, environmental factors, feeding habits and seasonal

changes. Colwell (1962) suggested that the methods of handling fish and

their pre capture environment influence the composition of the skin flora.

Lindsay (1986), Peleteiro and Richards, (1985) and Shewan (1961)

recorded Pseudomonas, Achromobacter, Flavobacter and Vibrio species in


descending order of frequency on gills of marine fish from the north sea

and Norwegian water, whereas only Bacillus and Micrococus were isolated

from gills of fish from warmer waters of India. These differences probably

reflect differences in environmental temperatures, with more psychrophiles

and fewer mesophiles in the cold north sea water.

The intestinal microflora of fish reflects the bacterial content of

ingested food and water, Seki (1969), Horsley (1977) and Tanasomwang

and Muroga (1988). Horsley (1973) examined bacteria from the skin of

Atlantic salmon in marine, estuarine and fresh waters. The frequency of

genera isolated varied at different sampling sites, and the major

components of the skin flora were similar to those present in the water,

again indicating that the external flora of fish are a reflection of their

environment. Sera and Ishida, (1972) studied that the stomach and

intestinal content of fish closely reflects the bacterial flora of their diet.

An investigation of the aerobic and anaerobic heterotrophic intestinal

flora of gold fish Carassius aurates demonstrated that the intestinal microflora

became relatively stable at about 67 days after hatching and consisted of

Aeromonas hydrophila, Pseudomonas, Clostridium, Bacteroides type A,

Enterobacteriaceae, Plesiomonas, Shigelloides and Moraxella. These

transients were also detected in fish diets and fish eggs, and in water or

sediment, but did not become established in the intestines.

Horsley (1973) studied the bacterial genera on the gills of Atlantic

salmon migrating up the Dec River in Aberdeenshire, Scotland showed that

the relative numbers of the different genera changes with changes in the

environment of the fish from the marine to fresh water. Trust and Sparrow

(1974) found that numbers of bacteria in fresh water Salmonoids increased

28 Chapter 2

between the stomach and the posterior portion of the intestine. They

suggested that these numbers must represent active multiplication in the

tract as they could not be accounted for by ingestion.

Trust and Sparrow (1975) calculated that the area of gills covered

by bacteria would be only 0.02%. Yoshimizu et al., (1976) determined that

the intestinal microflora was simpler than those of the surrounding waters,

consisting of Aeromonas and Enterobacteriaceae in fresh water reared fish

and Vibrio in fish from sea water. A study in Finland by Niemi and

Thaipalinen, (1982) showed that effluents from two fish farms had elevated

numbers of total coliforms and fecal coliforms and on one farm effluent

had more fecal Streptococci than the influent. The majority of coliforms

identified were Enterobacter and Citrobacter and Aeromonas hydrophila

were quite common. The percentages of Gram-positive bacteria including

Bacilli, Cocci and Coryneform bacteria were markedly higher in natural

fish than in cultured ones, Clostridium and sulphate reducing bacteria were

commonly isolated from natural fishes (Sakata et al., 1984).

Quantitative and qualitative studies on the bacterial flora of freshly

caught pearl spot Etroplus suratensis from Cochin backwaters revealed that

the microflora of skin, gills and intestine consisted mainly of asporogenous

rods (Surendran and Iyer, 1985). Sugita et al., (1988) reported that the

permanent intestinal microflora consisted of bacteria which were also

present in the surroundings but which were able to persist and grow in the

environment provided by the intestinal tract.

Austin (1988) isolated the surface micro flora from the skin of

healthy turbot was Photobacterium angustum, Photobacterium loga,

Alcaligens feacalis, Pseudomonas fluorescens and Bacillus firmus. These


bacteria may also have been present in the water as a result of being shed

from fish, but in numbers too low. The mucus of the gills, gut and skin of

fish contains lysozyme and immunoglobulins which presumably act as

defense mechanisms against bacteria.

Various aspects of the normal microbial flora associated with fish

have been studied by Cahill (1990). Generally the range of bacterial genera

isolated is related to the aquatic habitat of the fish and varies with factors

such as the salinity of the habitat and the bacterial load in the water.

In integrated farming system, the contribution of bacteria as major

feed source for fish filter feeding and omnivorous species has been

illustrated by Guo et al., (1994). Importance of biofilms in fish processing

and aquaculture industry is being increasingly recognized and the role of

bacterial biofilms as a source of pathogens has been reported by

Karunasagar et al., (1994) and Tonguthai (1995). Geldreich and Clarke

(1996) reported that bacterial flora of aquatic animals especially that of fish

and shell fish is a reflection of their environmental flora. Aquatic animals

take up various kinds of bacteria from food, water and sediments which

may become constituent of bacterial flora of the digestive tract (Yoshisuke

et al., 2000). The aquaculture products can also be a source of various

bacterial, viral and protozoan pathogens. The contamination can occur

from various sources such as water, feed, pond, soil, bird droppings and

other live forms of surrounding ecosystems (Hus et al., 2000).

The composition of the bacterial flora of Black clam Villorita

cyprinoids from Vembanadu Lake in Kerala reveals a total of 55 bacterial

strains. The mesophilic flora was dominated by genera Vibrio, Aeromonas

and Pseudomonas. The total bacterial flora of clam consisted of about 72%

30 Chapter 2

gram-negative and 28% gram-positive genera (Lalitha and Surendran,

2005). The percentage contribution of different bacterial groups in the

biofilms of water seemed to be fluctuating, but Vibrio, Aeromonas,

Pseudomonas and Bacillus were isolated on most of the occasions (Das et

al., 2007).

2.4 Prevalence of fish diseases in aquaculture fish farms Fish disease is one of the most important problems that severely

affect the economic balance of aquaculture farmers. Innumerable diseases

were caused in fishes due to bacterial pathogens and several of them were

reported from India. Gopalkrishnan (1961) and Kumaraiah (1977) studied

an endemic bacterial disease caused by A. liquifaciens infecting the eyes of

Catla leading complete necrosis and death of the fish. Corneal opacity in

silver carp, (Hypophthalmichthys molitrix Val.) due to Gram-positive

bacterium, Staphylococcus aureus was reported by Shah and Tyagi (1986).

Mycobacterial organisms have been attributed to a condition known as gill

hyperplasia syndrome in common carp (Cyprinus carpio) as reported by

Kumar et al., (1986d). Ulcerative diseases in Calta have been reported to

penetrate the opercular bones and cranium. Gopalkrishnan (1963) and

Karunasagar et al., (1986) have investigated several such outbreaks.

Several workers have reported the occurrence of the diseases in

composite fish culture ponds (Pal and Tripathi, 1978). Recovery of human

enteric pathogenic bacteria indicates the extent of pollution by domestic

sewage (Prabhakar et al., 1985). The presence of virulent strains of

Aeromonas in healthy fish suggests their role as an opportunistic pathogen.

Dropsy is another important fish disease in India were Rohu (Labeo

rohita), Catla (Catla catla) and Mrigal were affected mostly in the late


winter. Kumar et al., (1986a) revealed a mixed infection of A. hydrophila

and myxosporidian parasite in the case of infectious dropsy in Catla catla.

Vibrio species were found to be frequent and apparently

opportunistic pathogens of Pennaeid shrimp (Lightner, 1988). Vibrio

appears to be influenced by the physico chemical features of the

environment (Cheng and Cheng, 1988). It is very important to assess the

presence of pathogens and environmental quality of the medium where

aquaculture is practised. Jhingran (1991) also observed eye diseases in

endemic forms of Channa mauritius and attributed it to the same type of

organisms. Mukherjee et al., (1992) have recorded a mass mortality in

farm reared silver carps and isolated Staphylococcus aureus from the

affected eyes of diseased fish.

Salmonella is an important bacterial pathogen associated with food

borne illness in most of the countries of the world. Nambiar and Iyer (1991)

have reported prevalence of 16 different serotypes of Salmonella in frozen

shrimp and frozen fish samples from Kochi. Nitrogen fixing bacteria

Azotobacter and the obligate anaerobe Clostridium were found abundant in

sediments and in the overlying water. Mukherjee et al., (1991) have

reported the role of A. hydrophila in ulcerative disease of fish and identified

the biochemical differences among the various strains of these organisms.

Nayak and Mukherjee (1994) made a detailed study of the

biochemical properties of A. hydrophila and drawn antibiograms on the

basis of antibiotic sensitivity tests. In a recent study these workers were

elucidated the role of A. hydrophila in dropsy, fin and tail rot and more

elaborately in epizootic ulcerative syndrome. It was also reported the role

32 Chapter 2

of ulcerative disease in necrotizing the muscle tissue and internal organs

like kidney, liver and spleen.

The presence of faecal coliforms and Streptococci in the intestinal

tract and water is an indication of water pollution with faecal material of

man and animals. The agro ecosystems and backwaters of central Kerala

were found to provide habitats for avian fauna in high population density

and they act as the main source of faecal contamination of fresh water

sources (Panicker and Ravindran 1997). Innumerable diseases were caused

in fishes due to bacterial pathogens and several of them were reported from

India. Some of the important bacterial pathogens like Aeromonas

hydrophila, A. salmonicida, Pseudomonas fluorescens, P. putrefaciens,

Vibrio parahaemolotyticus, V. alginolyticus etc. had been identified as most

commonly encountered agents in fish diseases (Mukherjee, 2002).

Coliform bacteria occur in large numbers in faeces and sewage but

are also found in the environment in the absence of human faecal

contamination. Faecal Streptococci were also found occasionally in small

numbers in food and environmental samples. The spores of sulphite

reducing Clostridium perfringens also can survive in the environment.

Pseudomonas aeruginosa also rapidly occur in a wide variety of aquatic

habitat yet it is not always found in human faeces. But it is an important

opportunistic pathogen and a cause of food spoilage as reported by Mackie

and Mc Cartney (2006).

2.5 Nutrient cycling by bacteria in aquatic systems Biochemical transformations of particulate and dissolved detrital

organic matter by bacteria and fungi are fundamental to the structure and

dynamics of nutrient cycling and energy fluxes within aquatic ecosystems.


The decomposition of organic matter by bacteria is governed by many

factors, particularly chemical, biological and physical parameters of the

ecosystem. The regeneration of organic nitrogen by bacteria is carried out

by decomposition and utilization of nitrogenous organic matter in the

aquatic systems (Botan et al., 1960).

Bacteria and fungi assimilate dissolved organic compounds. Some

of which are those they obtained through enzymatic degradation of

particulate organic matter. The decomposition rate of organic substances is

greatly dependent on solubility as reported by Vallentyne (1962). The rate

of decomposition of detrital substrates is a function of their concentration

and of the enzymatic activity of the surfaces of detrital particles (Saunders,

1972b).

Radheshyam (1986) studied the role of microorganisms playing

with organic nutrient cycling in fish ponds and improving the pond

heterotrophic production for maximum yield of fish in integrated farming

systems. Nitrogen transformations include assimilation, mineralization,

nitrification and denitrification in sediments (Rysgaard et al., 1993). Fang

et al., (1994) in the studies of pond water and sediments of polyculture fish

ponds observed the correlation between the load bacteria in fish pond and

the seasonal environmental factors monitored. Bacteria of the genus

Pseudomonas were found commonly occurring in both pond water and

sediment, there were changes or replacement of dominating bacteria along

with the seasons.

Microorganisms occupy the same environment without affecting

each other. Soil microorganisms serve as biogeochemical agents for the

conversion of complex organic compounds into simple inorganic

34 Chapter 2

compound or into their constituent elements (Pelczar, 2001). The metabolic

activity of microorganisms solubilizes phosphate from insoluble calcium,

iron and aluminium phosphates. Phosphates are released from organic

compounds such as nucleic acids by microbial degradation (Pelczar, 2001).

Biofilms of water are important biological structures formed on most

submerged aquatic surfaces. They comprise a unique niche wherein

communities of microorganisms co-exist. The common bacterial genera

comprised Pseudomonas, Vibrio, Aeromonas and Bacillus as reported by

Das et al., (2007). The load of bacteria in the biofilm was similar to that

found in the corresponding water.

2.6 Degradation of organic materials by bacterial enzymes in aquatic system Cellulolytic micro organisms play an important role in the biosphere

by recycling cellulose, the most abundant carbohydrate produced by the

plants. All organisms are known to degrade cellulose efficiently by

producing a number of enzymes with different specificities which may act

together in synergism. Minami et al., (1972) identified chitin decomposers

from the digestive tracts of ayu (Plecoglossus altivelis), carp (Cyprinus

carpio) and rainbow trout (Salmo gairdneri) and found that Aeromonas

species from freshwater fish and mainly Vibrio from marine fish are mainly

chitin decomposers. Microbial breakdown of substances such as cellulose

and chitin, in the gut could make nutrients available for absorption.

Cellulose activity was found to occur in the stomachs of 17 of 62 fish

species examined and was apparently due to the production of this enzyme

by gut microflora (Stickney and Shumway, 1974).


Trust et al., (1979) tested the ability of bacteria from the intestine of

grass carp to break down cellulose and found that Aeromonas hydrophila

was capable of breaking down cellulobiose but not cellulose or carboxy

methyl cellulose. The cellulase activity was derived from gastrointestinal

microorganisms rather than the presence of cellulase in the food

consumed. Cellulose activity in fish is correlated with the ingestion of

invertebrate cellulase or cellulolytic bacteria associated with the food

(Prejs and Blaszcyk, 1977; Lindsay and Harris, 1980), and that

populations of gastro intestinal micro organisms from fish exhibit little

cellulase activity (Trust et al., 1979; Lesel et al., 1986; Anderson 1991).

Cellulolytic bacteria have been known and investigated for many

years (Bisaria and Ghose, 1981). Madden (1983) reported many cellulolytic

bacteria from soil, compost, manure, muncipal soild waste etc. Lesel et al.,

(1986) detected both amylolytic and proteolytic bacteria in the gut of

phytophagous gold fish, C. auratus. Stevens (1988) reported that microbial

fermentation and nutrient synthesis are typically important in organisms

with a diet high in fibre. As vertebrates are incapable of producing cellulase

endogenously, exogenous cellulases play a critical role in the nutrition of

vertebrate herbivores.

Cellulose is an unbranched glucose polymer, composed of anhydro-

D-glucose units linked by 1,4βD glucoside bonds, which can be hydrolysed

by cellulolytic enzymes produced by both bacteria and fungi (Robson and

Chamblis, 1989). Cellulolytic bacteria include aerobic species such as

Pseudomonas and Actinomyces, facultative anaerobes such as Bacillus and

Cellulomonas and strict anaerobes such as Clostridium. Most of the

mesophilic isolates produced amylases and proteases, and 38% of isolates

36 Chapter 2

produced extra cellular enzymes; amylases, proteases, cellulases and

chitinases.

Cellulose fermenting bacteria that fix nitrogen may be widespread

and may play a role in nitrogen cycling as well as in carbon cycling on a

global scale (Leschine and Parola; 1989). Cellulose, the largest renewable

carbon source available, (approximately 150 billion tons of organic

material is photosynthesized annually) is frequently found in close

association with other compounds such as hemi cellulose, lignin and other

polysaccharides which makes its bioconversion more difficult (Person et

al., 1990). Das and Tripathi (1991) reported cellulase producing bacteria as

a part of intestinal flora and were not introduced with food. Gilkes et al.,

(1991) reported that the species of Pseudomonas, Cellulomonas,

Clostridium, Bacteriodes and Streptomyces can produce glycosylated

cellulases. As the diet was mainly composed of carbohydrates resistant to

endogenous digestive enzymes (Annison, 1993), microbial fermentation

and nutrient synthesis are typically important in organisms with a diet high

in fibre.

The report of Luczkovich and Stellwag (1993) was the first

document on the isolation of carboxymethyl cellulose producing micorobes

from the intestinal tract of the omnivorous pinfish, Lagodon rhomboides.

The authors concluded that the gastro intestinal microbiota of pinfish may

contribute to the breakdown of plant material and may be the major source of

cellulose. Subsequently Stellwag et al., (1995) characterised 36 carboxy

methyl cellulose producing obligate anaerobes from the intestinal tract

contents but not from the feeding habitat of the pinfish.


Bacteria constitute principal group of decomposers responsible for

carbon cycling, mostly because of their capacity to produce diverse extra

cellular enzymes that degrade complex compounds and macro molecules

(Hendricks et al., 1995). Ringo et al., (1995) suggested that microorganisms

have a beneficial effect in the digestive processes of fish.

Bairagie et al., (2002) confirmed the presence of a considerable

population of cellulolytic bacteria and their active role in extracellular

enzyme production from the digestive tracts of Indian major carps, Chinese

carps and tilapia and assayed extra cellular protease activity of bacterial

isolates from grass carp. Reports on microbial amylase activity in fish guts

are scarce (Bairagie et al., 2002). Ghosh et al., (2002) reported the

endogenous amylase activity in the gastro intestinal tract of grass carp

which appeared to be the result of its omnivorous feeding habit.

Fishes are unable to produce cellulase endogenously but they

harbour microbial population in their digestive tracts which help in the

digestion of plant materials by Bairagie et al., (2002). Ghosh et al., (2002)

studied bacterial symbionts exhibiting significant cellulolytic activity from the

digestive tract of Chinese grass carp, C. idella, Tilapia and O. mossambica.

The isolated bacteria were identified as Bacillus circulans, B. pumilus and B.

cereus respectively. The observations of Saha and Ray (1998), Ghosh et al.,

(2002), and Bairagie et al., (2002) strengthened the idea that fish harbour

cellulolytic, as well as amylolytic and proteolytic bacteria in their intestinal

tract.

Saha et al., (2006) isolated organisms capable of hydrolyzing

proteins such as caesin and gelatin. Vetriselvi et al., (2007) isolated five

species of bacterial genera namely Pseudomonas, Micrococcus, Bacillus,

38 Chapter 2

Serratia and Proteus from agricultural crop residues along with soil and

their cellulolytic activity has been studied.

2.7 N P K profile of aquaculture farms Nitrogen and phosphorus are the nutrients most likely to induce

environmental impacts like eutrophication in the water column, whereas

organic carbon deposition in addition can contribute to disturbance or

severe impacts of aquatic ecosystems. Carbon is the backbone of all

organic molecules and the primary source for building organic carbon is

inorganic carbon (CO2) dissolved in the oceans. Photosynthesis in aquatic

and terrestrial plants converts CO2 to organic carbon, thus making it

available to the rest of the biosphere.

Nitrogen is an essential element, with high contents in proteins and

nucleic acids. Although 78% of the air is nitrogen in the form of N2 gas,

nitrogen is still often in limited supply for the organism in the biosphere.

Phosphorus in biological systems is always combined with oxygen as

phosphate (PO4). Phosphate may be free as inorganic, or combined with

organic molecules.

Phosphorus in biological systems is always combined with oxygen

as phosphate (PO4). The ultimate source of phosphate is crystalline rocks,

and erosion, weathering and to some extent the action of plant roots and

lichens, which make it available to organisms (Clapham, 1983). Phosphate

is essential in the nucleic acids (DNA and RNA), in adenosine triphosphate

(ATP) which is an important energy storage and transfer molecule in all

organisms, as phospholipids in cell membranes, and in calcium phosphate

forming teeth and bone (Wallace et al., 1991).


Wallace et al., (1991) reported that nitrogen fixing bacteria are the

only organisms able to take up N2 gas and convert it into biomass, whereas

other organisms use dissolved inorganic N (plants and bacteria) or organic

forms of the element (eg, animals). During digestion, proteins are broken

down to amino acids, which can be used to build new proteins in the cells,

or they may be converted to fatty acids or carbohydrate, or respired for

maintenance metabolism. During deamination the amine group (NH2), is

removed from the amino acid as ammonia (NH3). Ammonia is toxic, but

organisms living in water can usually exchange materials easily and thus

get rid of excess ammonia.

All ecosystems are dissipative structures, in the sense that organic

carbon is normally broken down to inorganic carbon by respiration by the

organisms. Approximately 50% of the dry weight of any organism,

including fish and its natural prey, is carbon (Sterner and Elser, 2002).

In order to be taken up in the gastrointestinal tract in fish,

phosphorus compounds must be broken down to inorganic phosphate. If

the plasma concentration of PO4 becomes too high, the fish excretes the

excess in the urine, while undigested phosphorus is expelled from the fish

through faeces (Bureau and Cho, 1999, Roy and Lall, 2004).

2.8. Multiple drug resistance among bacteria of integrated farms Studies have documented the distribution of antibiotic resistant

bacteria in aquatic environment (Koditschek and Guyre 1974, Goyal et al.,

1979). Drug resistance among bacteria depends on the amount and kind of

drugs used in that particular geographical area. Haemagglutination property

of bacteria is believed to be associated with the binding capacity of

bacterial cells to epithelial cell surfaces (Green and Thomas, 1981).

40 Chapter 2

The occurrence of multiple antibiotic resistance (MAR) among the

enteric bacterial species could be a problem associated with transfer of

resistance to other organisms of human/veterinary significance (Toranzos et al.,

1983). Presence of large number of antibiotic resistant E.coli in fish samples

can transfer the resistance to human pathogens through plasmids. E. coli

isolates from various sample sources with MAR value higher than 0.2 may

have originated from high risk source of contamination. Barry (1984) had

been studied the high susceptibility of Gram -ve bacteria to the quinolones

like Ciprofloxacin, Gentamycin etc. Incidence of drug resistant coliform in

Cochin backwaters was reported by Pradeep and Lakshmanaperumalsamy

(1986). The antibiotic resistance has been reported to occur more frequently

in Pseudomonas species and E.coli (Jones et al., 1986 and Alvero, 1987).

Mc Phaearson et al., (1991) and Abraham et al., (1997) studied the

potential hazards of indiscriminate use of chemicals and drugs in

aquaculture systems. Praveen et al., (1997) proposed MAR index for

differentiating the sources of pollution. Williams et al., (1992) reported that

the frequent use of oxytetracycline and nalidixic acid in shrimp aquaculture

farms may enhance the frequency of new oxytetracycline or nalidixic acid

resistant isolates in the system.

The low percentage of resistance to antibiotics by fresh water

bacteria are reported by Shome and Shome, (1999), Magee and Quinn,

(1991) and Dhar et al., (2001). Shome et al., (1998) reported that Gram-ve

bacteria have more resistance power than Gram +ve bacteria. Due to the

widespread use of antibiotics, the resistance profile of the microorganisms

are changing, as evidenced by the increasing resistance among bacterial

population from aquatic and other environments (Campbell et al., 1995,


Ergin and Muthu, 1999 and Shrivastava et al., 2003). Resistance pattern of

different antibiotics for E.coli isolates from various sources can be

compared with isolates from river water, sediment and aquaculture pond

samples (Hatha et al., 1999, Harish et al., 2003). The Gram-negative

bacteria such as Aeromonas and Pseudomonas of the diseased fish were

highly susceptible to many of the broad-spectrum antibiotics, except

nitrofurantoin (Debasis et al., 2004).

The antibiotic sensitivity pattern of shrimp bacterial isolates

indicated that V. harveyi was found to be highly susceptible to

chloramphenicol, ciprofloxacin, nalidixic acid and streptomycin (Selvin et al.,

2005). Kumar and Surendran (2005) isolated Pseudomonas resistant to

nitrofurantoin and sulphamethizol from fish, prawn, brackish water and

fresh water aquaculture farm environments. Chrisolite and Sugumar, (2006)

reported that drug resistance among bacteria depends on the amount and

kind of drugs used in that particular geographical area and he had noticed

the resistant pattern of E.coli and Salmonella from water, beach, sand and

fish collected from the four fish landing centers of Thoothukudi. The E.coli

isolates were found to be resistant to bacitracin, erythromycin and

rifampicin and the Salmonella isolates were resistant to bacitracin,

ampicillin, erythromycin and rifampicin.The MAR index revealed that this

E.coli and Salmonella might have originated from high-risk sources of

contamination such as humans.

2.9 Serological characteristics bacteria from integrated farms Haemolytic activity is considered as one of the pathogenic features

of bacteria. Haemolysis is considered to be one of the virulence factors of

E.coli strains and haemolysin production was related to the release of iron

42 Chapter 2

into the bacterial environment by cytotoxic effects on neutrophils (Cavalieri

and Synder, 1982). Inamura et al., 1984, Chung and Kou, 1985 and

Kodama et al., 1985) reported that haemocytolytic assay is still commonly

used to differentiate among suspected pathogens. Ullah and Arai (1983), Chen

et al., (1995), Lee et al., (1995) and Michael et al., (1988) isolated 12 Vibrio

damsela strains from Pennaeus monodon which were demonstrated as

pathogenic for the tiger prawn and which possessed haemolytic ability for

erythrocytes of sheep.

In addition to haemolysins, bacterial pathogenic factors such as

enterotoxins, proteases and haemagglutinins have also been reported for

aquatic organisms by Inamura et al., (1984). Haemolytic activity is

considered as one of the pathogenic features of bacteria, it may not always be

useful in determining pathogenicity; both haemolytic and non-haemolytic

strains of Streptococcus are important pathogens. Ruangpan and Kitao (1991)

and Chang et al., (1996a) has studied hepatopancreatic necrosis in tiger prawns

and suggested that their haemolytic activity may be correlated with their

pathogenicity. E.coli and other coliforms isolated from drinking water sources

from rural Kerala exhibited low haemagglutination, haemolysin production

properties and antibiotic susceptibility indicated the contamination of these

water bodies with faecal coliforms from avian sources (Panicker and

Raveendran, 1997).

Polluted water environments often contain a variety of harmful

bacteria. Alpha and beta haemolytic bacteria can be infectious to a variety

of hosts, including humans (Atlas and Bartha, 1998). Coliform bacteria

originate from faecal matter and when present in elevated levels are

indicators of pathogens in the water. However, not all haemolytic bacteria


have faecal origin and some can be indigenous to terrestrial or aquatic habitats

(Atlas and Bartha, 1998). Alpha and beta haemolytic bacteria are introduced

into the ecosystem with pollutants. Harmful haemolytic bacteria can initiate

infections by entering small lesions in the skin, mucous membranes or

openings in the host (Madigan et al., 2000).

2.10 Influence of physico chemical parameters on aquatic ecosystem Fish production is enhanced in water of neutrality between pH 7 and 8.

Banerjea (1967) reported that the calcareous waters with alkalinities of more

than 50ppm are most productive, waters with alkalinity less than 10ppm rarely

produce large crops and water intermediates between these groups may

produce useful crops. Nutrient recycling was found crucial to aquaculture

farms and the nitrate-nitrogen may be formed as a result of the

decomposition of organic nitrogen cycle (Sankaranarayanan and Quasim

1969).

Holiday (1971) reported that when salinity increases, the availability

of dissolved oxygen decreases. Reddy and Sankaranarayan, (1972)

observed that in shallow systems, recycling of nutrients is facilitated

through sediments. Pillai et al., (1975) have reported that fishery resources

of any area is mainly dependent on the magnitude of primary and

secondary productivity, which in turn are influenced by various physico-

chemical and biological factors of water. They are of the opinion that high

organic carbon content in the Pokkali rice fields is due to the death and

decay of benthic animals at the end of prawn culture season and the decay

of paddy stumps after cultivation.

Optimum range of pH in body fluids at a given temperature plays

essential role in the homeostatic mechanisms in aquatic animals (Alabaster

44 Chapter 2

and Lloyd, 1984). Vijayan and Varghese (1986) observed that the bottom

dwelling species like C. carpio and C. mrigala are more tolerent to

fluctuations of oxygen concentration. Physico-chemical parameters of

water such as temperature, dissolved oxygen, pH, turbidity and depth has

a direct bearing on the species utilized for culture in rice fields (Ali,

1987a). Upadhaya (1988) stated that nitrate-nitrogen plays significant role

in the primary production, which is evident from the seasonal pattern of

nitrate profile.

Ali (1992) studied the various aspects of water quality parameters

affecting fertility and productivity of rice-fish farming system in Kerian,

North Perak and observed that temperature and dissolved oxygen were

higher in exposed rice fields, than in the sump ponds and observed that

benthic population were higher in the rice fields than in the sump ponds.

Bell and Tranvik (1993) reported that bacterioplankton production has been

observed to be similar under acidic and neutral to slightly alkaline

conditions. Padmakumar et al., (1993) has reported that dissolved oxygen,

salinity and pH are three critical parameters in integrated aquaculture

systems in Kuttanad lowlands. The soil pH in Kuttanad soils are generally

acidic (Padmaja et al., 1994). pH of the water is influenced by soil pH,

concentration of CO2, carbonates and bicarbonates in water. Phytoplankton

and other aquatic vegetation remove CO2 from the water during

photosynthesis and this result in acidic pH.

According to the ranks of total carbon for freshwater pond

sediments, catfish and prawn ponds were medium in pH while carp ponds

were high (Boyd and Pipoppingo, 1994). Studies in USA have revealed that

sediment accumulated organic matter and nutrient concentrations increased


over time in research ponds for sunfish Lepomis species and Channel

catfish Ictalurus puntuatus by Munsiri et al., (1995). Aquaculture pond

sediments seldom contain more than 5% organic carbon (Boyd, 1995).

Inorganic nitrogen is much less frequently limiting to bacterial growth than of

phosphorus reported by Elser et al., (1995a,b) and Jansson et al., (1996).

Major declines in habitat quality of semi permanent wetland of the flood

plains will occur as the difference between flooding and drying events

increase (Poiani et al., 1996).

Jeppesen et al., (1997) reported that bacterioplankton production

commonly decreases under conditions of high pH. A number of studies

have shown that bacterioplanktonic growth is positively correlated with

temperature, particularly at relatively low temperatures by Simon and

Wiinsch (1998). The microbial population in a body of water is to a large

extent, determined by the physical and chemical conditions that prevail in

that habitat. It may vary in both number and kind with the source of water,

composition of the water, microbial nutrients and geographical, biological

and climatic conditions (Pelczar, 2001).

The temperature in lakes, streams and estuaries is influenced by the

seasons and there are corresponding shifts in the microbial flora.

Hydrostatic pressure of the deep sea is an important factor in the

occurrence and growth of marine microorganisms. The depth of the photo

zone varies depending on local conditions as latitude, season and turbidity

of water. In most aquatic habitats primary producers are restricted up to the

zone which light can penetrate. The degree of salinity in natural water

ranges from near zero in fresh water to saturation in salt lakes. Turbidity of

water influences the penetration of light, which in turn affects the

46 Chapter 2

photosynthetic zone. Particulate matter also serves as substrates that are

metabolized. Aquatic micro organisms in general can be grown at a wide

range of pH (6.5 to 8.5). Lakes and rivers may show a wide range of pH

depending upon local conditions. The quantity and type of inorganic and

organic materials present in the aquatic environment are important in

determining the microbial flora (Pelczar, 2001).

pH of water has direct effect on fish growth as well as on the

growth and survival of fish food organisms. Ojah and Mandi (2004) had

observed a diurnal variation in pH in fresh water fish pond culture. More or

less the same results were reported by Mohanty (2003) in rice-fish carp

seed rearing system reported tolerant fluctuations of oxygen concentration.

Thunjai et al., (2004) reported that Tilapia ponds were similar to carp

ponds with respect to total carbon concentration. Tilapia ponds in Thailand

had an average total nitrogen concentration of 0.19% and a carbon nitrogen

concentration ratio of 11%.

Mohan and Omana (2007) reported a linear relationship and

positive correlation between the physico chemical parameters of

Vembanadu backwater which serves as a receptacle for the effluents of

several industries, domestic sewage from Cochin and strip of smaller

townships.


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