Research Article
Anopheline Breeding in Irrigated Rice Land Agro-Ecosystem and
Natural Parasitism of the Fungus Coelomomyces with special
reference to Species Succession in Central Gujarat, India
Rajni Kant Srivastava*
Abstract
Mosquito population studies in rice agro-ecosystem of Kheda district in Central Gujarat
revealed the presence of 14 anopheline species. An. subpictus (69.19%) was predominant
anopheline species in rice agro-ecosystem followed by An. nigerrimus (9.18%), An. annularis
(6.86%), An. culicifacies (5.52%), An. tessellatus (4.52%) and An. barbirostris (2.27%). Profuse
breeding of An. subpictus and An. culcifacies was found in newly transplanted rice fields when
plan height was minimum and distance between plants was maximum, which was later
replaced by more shade loving mosquitoes like An. annularis, An. nigerrimus, An. tessellatus
and An. barbirostris in later stages when there was enough aquatic vegetation in rice plots
with thick growth of plants and canopy development. Breeding of malaria vector An.
culicifacies was found in low proportions in rice nurseries and post harvested rice fields while
rice field channels were the preferred place for its breeding. Besides species replacement,
species groups were also noticed in rice field breeding mosquitoes when species like An.
subpictus and An. culicifacies showed affinity to breed maximum in same kind of conditions of
newly transplanted rice fields while, An. annularis, An. nigerrimus and An. barbirostis
preferred to breed in later stages of the rice crop in an established ecosystem. Better
understanding of the mosquito bionomics in this habitat may prove helpful in devising
appropriate control measures for mosquito control.
Keywords: Rice fields, Anopheles, Species succession, Coelomomyces, Mosquito control.
Introduction
Rice is one of the most important food crops in
developing world in value of production and in
contribution to diet. It is also a primary staple food of
about 60% of mankind and is the main source of
employment and income of the rural population. There
are around 110 rice growing countries and some 140
million hectare of land is devoted to growing rice in the
world, ninety percent of which is both grown and eaten
in Asia. In India, area under rice cultivation increased
from 29.8 m ha in 1950s to about 42 m ha in 1990s and
is expected to be around 45 m ha in recent years.1
Constant standing water for long periods, vast surface
area and diverse ecological niche of irrigated rice land
and associated habitats provide congenial ecological
conditions for mosquitoes to breed and proliferate
abundantly in this complex and diverse ecosystem.2-8
Other micro-organisms including the pathogens and
*
parasites also get an opportunity to flourish in this
ecosystem and sometimes affect mosquito immature
survival. In view of the complex ecological conditions of
the rice agro-ecosystem, present study was attempted
to find out the mosquitoes inhabiting this ecosystem
and factors determining their prevalence and species
succession. Attempts were also made to observe natural
infestation/ parasitism, if any, in immature stages of the
mosquitoes as well as to suggest their suitable control
measures.
Material and Methods
A total of twenty seven rice fields in nine villages of
three talukas of Kheda district in Central Gujarat (now
split in to Kheda and Anand) which have ample canal
irrigation through Mahi-Kadana irrigation project were
selected. In each village, three rice fields which were
Indian Council of Medical Research (ICMR), Ansari Nagar, New Delhi-110029, India.
E-mail Id: [email protected]
© ADR Journals 2015. All Rights Reserved.
J. Commun. Dis. 2015; 47(4)
located adjacent, 0.5 km and 1km away from the
villages were selected and monitored regularly at
weekly intervals for mosquito larval abundance.
Random sampling was also done from the rice fields of
adjoining talukas and associated habitats like rice
nurseries, rice field channels, and post harvested rice
fields. Study was carried out in 4 crop cycles of Rabi
(non-monsoon) and Kharif (monsoon dependent) crop.
Mosquito immatures from the rice fields and associated
habitats were collected with the help of standard
enamel larval dipper, brought to laboratory and reared
up to adult emergence following standard methods as
described earlier.2,3,8 Adults emerged were anesthetized
and identified using the keys of Christophers (1933).9
Record was also maintained with respect to different
biotic and abiotic parameters such as height of the
plants, plant to plant distance, water depth, aquatic
vegetation and presence of predator and parasites, etc
to find out their relationship with mosquito breeding.
Diseased/ infected mosquito larvae if present in any
field were also collected and examined under
microscope for infection. Permanent slides of the
infected larvae were prepared and sent to
Entomologicky Ustav Ceskoslovenske, Czechoslovakia
for identification of the fungus species. Data obtained
was processed and analyzed statistically.
Crop Cycle
Rice is normally cultivated in two seasons, i.e. monsoon
dependent Kharif and the irrigation dependent Rabi
season. For better understanding of mosquito ecology,
their breeding behavior and inter-relationship between
various biotic and abiotic factors, rice agro-ecosystem
can be categorized as follows considering their
agronomic practices and cultivation pattern:
Rice Nurseries
Before transplanting in to field, a bed of rice plants is
made in a corner of a field and is allowed to grow up to
a certain period usually for a month. These nurseries
also remain flooded with water though plants remain
closely embedded in the field. A bunch of around 100200 plants are made while uprooting and transplanting
them in to fallow fields. But these nurseries are also
ideal breeding places of the mosquitoes as they remain
inundated with water throughout the period. Hence
sampling was made from rice nurseries to know the
mosquito species found breeding in this habitat.
5
Srivastava RK
Rice field Channels
These are irrigation channels and criss-cross the rice
plots for irrigation purpose. In a rice growing area, a
large network of rice irrigation channels are noticed as it
carries slow moving water to the rice fields.
These channels support the prolific breeding of vector
mosquitoes due to clean slow moving water and
presence of diatoms, grass on the margins and scanty
aquatic vegetation. Rice field channels were monitored
regularly for mosquito population studies.
Rice field
Rice fields are a major habitat and an important source
of mosquito proliferation due to their vast surface area.
According to the growth of the plants and growing
stages of the entire crop, the rice fields can be divided
as:
Newly Transplanted Rice Fields
Newly transplanted rice fields are the rice plots just
after the rice plants are planted, with full submergence
with turbid water without any aquatic vegetation, with
wider inter-space between rice plants and no canopy
development. Height of the plants is usually below 20
cm.
Vegetative Growing Phase
These rice plots contain a bit older plants with growing
rice plants. Height of the plants reaches to 21-40 cm and
space between plants starts reducing and aquatic
vegetation like algae, hydrilla, lemna starts appearing.
Turbidity of water reduces and fields are almost settled
down with an established ecosystem.
Flowering Stage
This stage of rice crop cycle is an advanced stage of
development as plant height increases to 41-60 cm and
plants starts flowering. The inter-space between plants
reduces further and vegetation also becomes thick with
canopy development.
Mature Ready to Harvest
These rice plots are mature stage of the rice crop with
plants loaded with rice grains and full grown canopy
with minimum space between plants. The height of the
plants varies from 61-80 cm and in some cases goes
beyond 100 cm. The vegetation and other diatoms also
flourish abundantly in this niche.
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Srivastava RK
J. Commun. Dis. 2015; 47(4)
Post Harvested Rice Fields
These rice plots are the fields with left out stumps of
rice plants after the harvesting process is over with
open space and organic content rich water having
different variety of decaying and rotting aquatic
vegetations, which provide ideal breeding conditions for
wide variety of mosquitoes.
Results and Discussion
Mosquito Composition
A total of fourteen anopheline species were
encountered breeding in rice land agro-ecosytem. Out
S. no. Species
Numbers
% Composition
1
An. Aconitus
118
0.54
2
An. annularis
1,479
6.86
3
An. barbirostris 490
2.27
4
An. culicifacies 1,191
5.52
5
An. fluviatilis
6
0.02
6
An. jamesii
6
0.02
7
An. nigerrimus 1,980
9.18
8
An. pallidus
291
1.35
9
An. splendidus
1
0.004
10
An. stephensi
72
0.33
11
An. subpictus
14,912
69.19
12
An. tessellutus 975
4.52
13
An. vagus
20
0.09
14
An. varuna
10
0.04
Total
21,551
100
of 21,551 adults that emerged from the immatures
collected, Anopheles subpictus (69.19%) was
predominant followed by An. nigerrimus (9.18%), An.
annularis (6.86%), An. culicifacies (5.52%), An.
tessellatus (4.52%) and An. barbirostris (2.27%) in order
of abundance.
Other eight species were present in low proportions and
accounted for only 2.46%.
Low vector population was recorded in rice nurseries
and post harvested rice-fields in comparison to that of
field channels and newly transplanted rice fields (Table
1).
Period of Prevalence
-
Preferred Stage of rice cultivation
GRF
NM (Rabi)
NM (Rabi)
M (Kharif)
NM (Rabi)
-
GRF
GRF, MRF
NTRF
GRF
GRF
GRF, MRF
GRF
GRF
GRF
NTRF, GRF
GRF, MRF
NTRF
NTRF, GRF
NM- Non-monsoon, M-Monsoon, GRF- Growing Rice fields, MRF-Mature Rice Fields, NTRF-Newly Transplanted Rice fields
Table 1.Anopheline Composition in Rice Agro-ecosystem
Seasonal Abundance
An. subpictus was prevalent during monsoon (Kharif)
season of rice cultivation, whereas the per cent
composition of An. annularis, An. culicifacies and An.
tessellatus was significantly higher during non-monsoon
(Rabi) period. However, there were no marked
differences in the breeding pattern of other species in
both the season. There were also wide variations within
the season among few anopheline species such as An.
subpictus, An. culicifacies, An. nigerrimus and An.
barbirostris. Extensive breeding of An. subpictus and An.
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culicifacies was found in early months (January to March
and July to August) of both the crops. Their composition
declined gradually in following months. A reverse trend
was seen in the breeding of An. nigerrimus, An.
annularis (except non-monsoon), An. barbirostris and
An. tessellatus. These species were abundant in later
stage (April to June and October to December) of rice
cultivation. No such significant pattern was seen in
other anopheline species (Fig. 1). Prasad et al.4 found
the breeding of An. culicifacies and An. subpictus in
early months (June-Aug) of rice cultivation.
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J. Commun. Dis. 2015; 47(4)
Srivastava RK
Figure 1.Seasonal Prevalence of Prominent Anophelines in Rice fields
Larval Density
Larval density was found inversely proportional to the
height of the plants. It started building up during
vegetative growing and flowering phase of the rice crop
when plant height measured 40-60 cm, thereafter it
declined in mature stages of the rice crop, when plants
attained a height of 100 cm or more.
Mosquito Population Indices in Different
Habitats of Rice Agro-Ecosystem
Rice Nurseries
A total of 13 anopheline species were encountered
breeding in rice nurseries with dominance of An.
subpictus (56.67%) followed by An. nigerrimus (19.92%),
An. annularis (12.06%), and An. tessellatus (5.48%).
Malaria vector An. culicifacies (0.91%) was present in
very low proportions in rice nurseries. Russell and Rao10
also noted the breeding of An. culicifacies in low
proportions in rice nurseries, which might be due to
reduced inter-space between plants creating hindrance
for oviposition.
culicifacies (20.83%) and it was 2nd most predominant
species in this habitat followed by An. nigerrimus
(16.36%) and An. barbirostris (11.18%).
Newly Transplanted Rice fields
They are characterized by: Plant height below 20 cm,
Plant distance 26-30 cm, water quality turbid, without
any established aquatic vegetation and plant space
maximum owing to minimum canopy development.
Breeding of species like An. culicifacies, An. subpictus,
An. annularis was found maximum, while other
anopheline species could not establish during this
phase.
Vegetative Growing Phase
Plant height increased to 21-40. cm, plant space started
reducing (21-25 cm) due to growth of plants and canopy
development, vegetation starts appearing with the
presence of algae and blue green algae. Species like An.
annularis, An. pallidus and An. tessellatus were found
appearing, whereas the population density of An.
subpictus and An. culicifacies started declining.
Rice-field Channels
Flowering Stage
Rice field Channels supported the breeding of total 9
anopheline species. Though An. subpictus (42.09%) was
predominant species but the rice field channels were
found preferred breeding place for malaria vector An.
Paddy plants started maturing due to flowering of
plants, plant height reached to 41-60 cm, distance
between plants reduced further (16-20 cm) due to
growth in plant canopy, aquatic vegetation got thicker
7
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Srivastava RK
J. Commun. Dis. 2015; 47(4)
preventing the movement of few predators such as fish,
etc. Species like An. subpictus and An. culicifacies drops
drastically, while shade loving species such as An.
nigerrimus, An. barbirostris, An. annularis and An.
tessellatus breed prolifically during this stage.
Mature ready to Harvest Rice fields
Rice crop almost ready for harvesting, plant height up to
maximum (60-80 cm and beyond 100 cm in some cases),
distance between plants minimum (11-15 cm and in
advanced stage 5-10 cm), canopy development
maximum.
An established ecosystem with lots of organisms with
full grown vegetation and aquatic flora and fauna is
found. Species like An. subpictus, An. culicifacies, An
stephensi were almost negligible. Stage was found best
suited for the breeding of An. barbirostris, An.
nigerrimus and An. tessellatus. Other species were
almost invisible in this stage of the crop.
Species
An. annularis
An. barbirostris
An. culicifacies
An. nigerrimus
An. subpictus
An. tessellates
Other anophelines
Total Adults emerged
Total species emerged
Nursery
12.06
0.73
0.91
19.92
56.67
5.48
4.23
547
13
RFC
3.77
11.18
20.83
16.36
42.09
2.93
2.84
715
9
Post Harvested Rice Fields
These fields were found most conducive and preferable
place for the breeding of other anopheline species
(15.42%), though their proportion was less than 5% in
other associated habitats of this ecosystem.
Other dominating anopheline species were An.
subpictus (32.65%), An. annularis (24.12%) and An.
nigerrimus (20.55%). Population of An. culicifacies was
found to be 2.51%.
The presence of thick aquatic vegetation enriched with
decaying organic contents supported the prolific
breeding of vegetation loving species like An. annualris
and An. nigerrimus (Table 2).
The different types of aquatic vegetation, diatoms and
other organisms found in rice fields which affect the
breeding and proliferation of anopheline mosquitoes is
shown in Box 1.
Rice fields
5.43
1.86
5.32
7.68
73.53
4.83
1.35
18,776
14
PHRF
24.12
3.7
2.51
20.55
32.65
1.05
15.42
1513
12
Mean
11.34
4.36
7.39
16.12
51.23
3.57
5.96
21,551
14
RFC- Rice Field Channels, PHRF-Post Harvested Rice Fields
Table 2.Percent composition of Major Anophelines in different Habitats of Rice Agro-ecosystem
Breeding of An. fluviatilis was found in nurseries and
rice fields which were very near to canal network. Singh
et al.5 and Sadanandane et al.7 found the breeding of
this species in terraced rice fields with perceptible flow
of water. The profuse breeding of An. annularis, An.
nigerrimus and An. barbirostris in post harvested rice
fields may be due to rich growth of aquatic vegetation.
Species Succession
It was noticed that each species prefer particular stage
of rice cultivation. Heliophilic species such as An.
culicifacies and An. subpictus were more prevalent in
early months of both Rabi and Kharif crops in newly
transplanted rice fields when distance between plants
was maximum and plant height was 40 cm in case of
former and 60 cm in case of latter, and they exhibited
negative co-relation with the plant height. These species
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were subsequently replaced by more shade loving
species such as An. annularis and An. tessellatus and
thereafter by An. nigerrimus and An. barbirostris during
flowering and mature stages of rice cultivation with the
appearance of aquatic vegetation on water surface and
canopy development with the increase in plant height
(Table 3). The dominance of An. culicifacies in early
week of rice cultivation may be due to sparse plantation
and less height of the rice plants. Russell and Rao11
noted that composition of this species decreases when
plant attains a height of 37.5 cm, the subsequent
decline in the composition in later half of the crop was
due to canopy development resulting in mechanical
obstruction in oviposition. Senior White12 also observed
that the prevalence of An. culcifacies ceases after
September.
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J. Commun. Dis. 2015; 47(4)
Srivastava RK
Insects
Coleoptera specially Dytiscidae and Hydrophilidae
Hemiptera particularly Notonectidiae odonata (predators usually have a limited breeding season)
Phytoplankton flora
Cyanobacteria
Unicellular and filamentous algae
Zooflagellates
Other protozoans
Rotifers
Crustaceans
Organic debris
Unspecified inorganic materials
Spores and insect scales
Notonectides
Biotic fauna
Diatoms
Diatoms were present in newly transplanted rice fields and declined with the increase in plant height
Filamentous algae mainly blue green algae and green algae
Observed to form mats and provided protection to mosquito immature from predators.
Blue Green Algae (Anabaena, oscillatoria, Phoromidium, Spirulina, Nostoc)
Green Algae (spirogyra (most abundant among green algae), oedogonium, volvocales)
BGA peak abundance was in 4th week, negligible after 10 weeks
Other Factors
Predators and Parasite
Prawns
Snails
Fungus Coelomomyces
Azolla
Insect Predators and Phytoplankton
Cyclops (mesocyclops), Paramecium, ameba, Daphnia, Vorticella, Cypris, Chironomid larvae, Nauplius larvae,
Nematode, monostyle, Lepadella, Brachinus calciflorus
Box 1.Important Group of Insect Predators found in Rice Fields
Sr.
No.
1.
Mosquito Sp.
2.
Species started
appearing
9
Predominant
Species
Newly Transplanted
Rice fields
An. culicifacies
An. subpictus
---
Vegetative
Growing Phase
An. subpictus
An. culicifacies
Growing
Flowering Stage
An. annularis
An. tessallutus
An. aconitus
An. annularis
An. nigerrimus
An. aconitus
An. barbirostris
An. tessellatus
An. pallidus
Table 3.Species Succession in Rice fields
Mature Rice fields
ready to Harvest
An. nigerrimus
An. barbirostris
---
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J. Commun. Dis. 2015; 47(4)
Other anophelines did not exhibit much variation in
their choice of breeding preference.
Natural Infestation of Fungus Coelomomyces
During the monsoon crop of rice cultivation in some rice
plots rust colored infected/ diseased mosquito larvae
were found. These were collected by dipper and
brought to laboratory for rearing and emergence.
Infected larvae were examined under microscope
thoroughly and infection was found to be of natural
parasitism of the fungus Coelomomyces indicus in
infected/ diseased larvae of An. subpictus which varied
from field to field and was found to be around 20-40 per
cent. Fully developed sporangia were found mainly in
IIIrd and IVth instar larvae giving a yellowish brown
appearance. In the advanced stage of infection, almost
entire coelomic cavity was found filled with orange oval
shaped sporangia. Infection of the fungus was found
maximum in early months of rice cultivation which was
associated with the presence of copepod (Cyclops) and
other aquatic zooplanktons in the fields. All the larvae
died before pupating (Plates 1-3). Maximum infestation
was found in newly transplanted and 20-30 days mature
rice fields, which declined with the growth of the crop.
Application of agro-chemicals like fertilizers and
insecticides had a negative impact on fungus infection.
Daphnia, Cyclops (copepod), Paramecium and other
micro-organisms were found in rice fields in association
with algae and lemna. Cyclops are the intermediate
hosts of the Coelomomyces.
Plates 1-3.Infected larvae of An. subpictus with fungus Coelomomces indicus
Plate 1.Larvae of An. subpictus heavily infected with fungus Coelomomyces indicus
Plate 2.Sporangia of Coelomomyces indicus
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J. Commun. Dis. 2015; 47(4)
Srivastava RK
15
Plate 3.Life cycle of fungus Coelomomyces
Chandrahas and Rajagopalan13 found the larvae of An.
subpictus and An. vagus naturally infected with
Coelomomyces indicus and C. anophelesicus in the
paddy fields in Pondicherry.
Larval abundance in paddy field and associated factors
in respect to impact of biotic and abiotic factors have
been studied in Kenya as well.14
Coelomomyces have a complex life cycle in which sexual
and asexual generations alternate between two
different invertebrate hosts, a mosquito and a copepod
(a tiny, fresh water shrimp).
In the mosquito, the fungus forms sporangia, which
release uniflagellate spores that infect a copepod. In the
copepod, uniflagellate male and female gametes are
produced that fuse, forming a biflagellate zygote that
invades a mosquito larvae (Plate 3).15 The appearance of
orange color is from carotene pigment in the male
gametocyte of the fungus.
Attempts were also made to control mosquito breeding
in rice fields by the application of aquatic fern Azolla,
use of biolarvicde containing powdered formulation of
Bacillus sphaericus and introduction of larvivorous fish
Poecilia reticulata (Guppy) and they have shown
promising results in controlling mosquito population in
rice fields. The results have been reported earlier.16
Mosquito population studies in rice agro-ecosystem will
be helpful in planning proper water management
practices in this habitat and designing appropriate
control measures.
11
Conclusion
Rice agro-ecosystem represents a complex of
interactions between several abiotic and biotic factors
influencing mosquito breeding and prevalence.
Following important observations were made during the
present study:
1. Major anophelines which were found breeding in
this ecosytem were An. subpictus, An. culicifacies,
An. annularis, An. tessellatus, An. nigerrimus and
An. barbirostris.
2. Prolific breeding of malaria vector An. culicifacies
was present in rice field channels and newly
transplanted rice fields. However, it was present in
low proportions in rice nurseries and post
harvested rice fields.
3. There occurs seasonal shift in the breeding of
different mosquito species and species replacement
was also observed to be a significant phenomenon
in this habitat which was inter-related with the
height of the plants, reduced inter-space between
plants with the growing crop, shade and canopy
development.
4. Other cultural and agronomic practices were also
found to affect the mosquito breeding in this
habitat.
5. Natural parasitism of the fungus Coelomomyces
indicus was observed in immature larval stages,
however, more detailed studies on predator and
parasite relationship are needed.
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Srivastava RK
J. Commun. Dis. 2015; 47(4)
A better understanding on mosquito behavior and their
breeding pattern in rice ago-ecosystem will be helpful
for devising their effective control measures.
Acknowledgement
The author extends sincere thanks to Dr V P Sharma,
founder Director, National Institute of Malaria Research
(NIMR), New Delhi for constant encouragement and
support to carry out this study. Sincere thanks are also
extended to Dr D K Gupta, former Scientist, NIMR, New
Delhi for providing help in identifying the fungus species
and to other colleagues at NIMR, Field Station, Nadiad,
Kheda, Gujarat for unstinted support during the course
of investigation.
7.
8.
9.
10.
Conflict of Interest: Nil
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