INTRODUCTION
Malaria is a major public health problem in District Ramgarh of Jharkhand state, India. The malaria ende- micity in this area is primarily due to prevalence of three malaria vector species, viz. Anopheles culicifacies, An.
fluviatilis and An. annularis1. In spite of well-known vec- torial status of these species in the district, no adequate information on ecological factors such as breeding and resting habitats as well as environmental factors such as temperature, humidity and rainfall directly affecting vec- tor population and disease transmission are available. Pre- vious studies suggest the predominant role of ecological and environmental conditions on availability of suitable breeding sites, which play important role in malaria epi- demiology2–4. The land transformation due to deforesta- tion causes vast ecological changes in the area, which directly affect breeding habitats of anophelines, their adult
population structure and density, and finally the dynam- ics of disease transmission5–7. The District Ramgarh has also been facing extensive deforestation due to exces- sive anthropogenic activities such as construction of dams, roads, industry, coal mining and agricultural land development over the years, leading to the formation of new and diversified breeding habitats. As compared to adult anophelines, the immatures are relatively immo- bile and occupy small breeding area8–9, therefore, site- specific vector control strategies could be developed by understanding the vectors’ breeding ecology, their dis- tribution and seasonal prevalence.
The previous studies also suggest that rainfall pro- vides ample breeding sites for anophelines to lay their eggs and the temperature plays important role in larval development and survival which takes about 10 days to metamorphosize from an egg to adult stage at an opti- mum temperature of 28°C10. In view of above, this study
*Authors made equal contribution.
Diversity of breeding habitats of anophelines (Diptera: Culicidae) in Ramgarh district, Jharkhand, India
Siddharth Pandey
1*, M.K. Das
2*& Ramesh C. Dhiman
31National Institute of Malaria Research, GECH Project site-Ranchi; 2National Institute of Malaria Research, Field Unit, Ranchi, Jharkhand;
3National Institute of Malaria Research, New Delhi, India
ABSTRACT
Background & objectives: The Ramgarh district of Jharkhand state, India is highly malarious owing to abundance of different malaria vector species, namely Anopheles culicifacies, An. fluviatilis and An. annularis. In spite of high prevalence of malaria vectors in Ramgarh, their larval ecology and climatic conditions affecting malaria dynamics have never been studied. Therefore, the objective of this study was to identify the diversity of potential breeding habitats and breeding preferences of anopheline vectors in the Ramgarh district.
Methods: Anopheles immature collection was carried out at potential aquatic habitats in Ramgarh and Gola sites using the standard dipper on fortnightly basis from August 2012 to July 2013. The immatures were reared till adult emergence and further identified using standard keys. Temperature of outdoor and water bodies was recorded through temperature data loggers, and rainfall through standard rain gauges installed at each site.
Results: A total of 6495 immature specimens representing 17 Anopheles species including three malaria vectors, viz. An. culicifacies, An. fluviatilis and An. annularis were collected from 11 types of breeding habitats. The highly preferred breeding habitats of vector anophelines were river bed pools, rivulets, wells, ponds, river margins, ditches and irrigation channels. Larval abundance of vector species showed site-specific variation with temperature and rainfall patterns throughout the year. The Shannon-Weiner diversity index ranged from 0.19 to 1.94 at Ramgarh site and 0.16 to 1.76 at Gola site.
Interpretation & conclusion: The study revealed that malaria vector species have been adapted to breed in a wide range of water bodies. The regular monitoring of such specific vector breeding sites under changing ecological and environmental conditions will be useful in guiding larval control operations selectively for effective vector/
malaria control.
Keywords Anophelines; breeding habitats; Jharkhand; larvae; malaria; Ramgarh; temperature
was conducted in District Ramgarh to investigate the diversity of breeding habitats, composition of malaria vector and non-vector species therein and most preferred breeding habitats for vector species. The effect of rainfall and ambient and water body temperature was also studied to know their effect on density of anopheline larvae in different breeding habitats to formulate effective larval control strategy for curbing malaria transmission.
MATERIAL & METHODS Study area
The District Ramgarh (latitude 23°38', longitude 85°34' in Jharkhand, India covers an area of 1360.08 km2, including 487.93 km2 forest area with 949,159 population (Census 2011). The survey of immature anophelines was carried out during August 2012 to July 2013 in two pri- mary health centres (PHCs), viz. Ramgarh and Gola with low and high malaria incidence, respectively. In each PHC, four villages were selected for conducting the study. The geographical coordinates of each village along with its as- sociated aquatic habitats were recorded using global po- sitioning system. The study villages are situated in the for- ested terrain and characterized with both permanent and temporary mosquito breeding habitats such as perennial streams, rivers, rivulets, ponds, wells, large drains etc.
congenial for mosquitoes breeding.
Larval collection, storage and identification
Immature anophelines were sampled from water bod- ies in the vicinity of 1 km of each village in morning hours between 0900 and 1100 hrs using standard dippers (250 ml capacity) on fortnightly basis as per the WHO (1975) manual on practical entomology in malaria11. Col- lection of anopheline larvae and pupae was carried out from different breeding habitats (Fig. 1), i.e. ponds, pools, rivulets, river margins, river bed pools, ditches, pits, wells, irrigation channels, rice-fields and stray fields. About 2–20 dips were taken from each breeding habitat depend- ing upon to its size. The sampled larvae and pupae were transferred to plastic containers (500 ml capacity) using a pipette. All the containers were properly labeled, brought to laboratory, kept at room temperature (25°C) with the help of thermostat for rearing till adult emer- gence and further identified to species using standard keys12–17. Larval densities were calculated as the propor- tion of total number of larvae and pupae per dip for each breeding site.
Larval/pupal density =
Meteorological data collection
To record daily ambient air temperature (since August 2012 to July 2013) at every four hour interval, HOBO data loggers (Australia) were installed in Stevenson screens (H.L. Scientific Industries, Ambala) fixed in open space at each site. The four-hourly tem- perature of aquatic habitat was recorded using water tem- perature data loggers by submerging the device in an iden- tified breeding habitat found positive for mosquito larval breeding site. The four-hourly generated temperature data were computed to daily and monthly maximum, mini- mum, and average temperature using MsExcel 2010. To observe the spatial variation in rainfall, one rain gauge (tipping bucket) was installed at each site. The rainfall was recorded on daily basis.
Statistical analysis
To assess anophelines community structure in each breeding habitat, the Shannon diversity index (H') and species evenness (E) were measured. Shannon diversity is the quantitative measure of species diversity in a com- munity which takes into account the species abundance and evenness of the species present in a habitat. How- ever, evenness is the measure of species closeness in terms of their number in the habitat, which is expressed be- tween 0 and 1 being 0 as complete dominance and 1 as complete evenness of the species.
Relative density (D), Shannon index and evenness of anopheline species were calculated using MsExcel 2010. Relative density of each anopheline species was expressed as its percentage in the whole sample18 as:
Where, D is relative density, I is number of individu-
Fig. 1. Different breeding habitats (from left to right — River, pond, ditch, pond & well, rivulet, and river) of anopheline species at Ramgarh district, Jharkhand.
als of a species, and N is total number of species. Based on values of D, each anopheline species was categorized as satellite (D <1%), subdominant (1 <D <5%) and domi- nant (D >5%) species19. The diversity of anopheline species was calculated as Shannon-Weiner diversity index (H') following Shannon method20 :
Where, s is the number of species in the sample, pi is relative abundance of ith species (ni/N), N is total num- ber of individuals of all kinds, ni is number of individu- als of ith species and ln is natural log. The species even- ness (E)20 swas calculatedas:
Where, H' is Shannon-Weiner diversity index, ln (S) is the natural logarithm of species richness. Species rich- ness is the total number of species present in the area.
RESULTS Anopheline larval surveillance
The anopheline larval abundance varied spatially and temporally at Ramgarh and Gola sites. A total of 6495 immature anophelines were collected from 11 types of breeding habitats during the study period (Table 1). Of total immatures collected, 17 Anopheles species, viz. An.
culicifacies, An. fluviatilis, An. annularis, An. pallidus, An. theobaldi, An. vagus, An. subpictus, An. nigerrimus, An. sergentii, An. splendidus, An. barbirostris, An.
tessellatus, An. jamesii, An. maculatus, An. jeyporiensis, An. crawfordi and An. aconitus were identified (Tables 2 and 3). Among these, An. culicifacies, An. fluviatilis and An. annularis have already been reported as malaria vec- tor species in this region1. The categorization of anopheline species on the basis of relative density [as dominant (>5%), subdominant (<5 and >1%) and satel- lite species (<1%)] revealed that An. culicifacies (32.7%) was most dominant species at Ramgarh site followed by An. fluviatilis (25.1%), An. annularis (12.8%), An.
subpictus (8.4%), An. theobaldi (5.5%), An. splendidus (5.3%), while An. barbirostris, An. crawfordi, An.
pallidus and An. vagus belonged to subdominant species (Table 4). Under satellite category, An. nigerrimus, An.
sergentii, An. tessellatus, An. jamesii, An. maculatus and An. jeyporiensis were identified.
However, at Gola site, An. annularis (26.4%) emerged as most dominant species followed by An.
fluviatilis (19.8%), An. subpictus (15.4%), An.
culicifacies (15%), An. splendidus (7.8%) and An. crawfordi (5.2%) (Table 4). Likewise, An. pallidus, An. barbirostris, An. jeyporiensis and An. vagus were categorized as subdominant species and An. theobaldi, An. jamesii, An. sergentii and An. aconitus as satellite species.
Anopheline larval ecology/Breeding habitats
During the survey, both permanent and temporary breeding habitats were identified in the study area. A to- tal of 11 types of predominant breeding habitats, viz.
ponds, river bed pools, rice-fields, rivulets, river mar- gins, stray fields, borrow pits, ditches, irrigation chan- nels, wells and seepages were recorded from both Ramgarh and Gola sites (Tables 2 and 3). At Ramgarh site, the permanent water bodies, i.e. river bed pools (RBP) (28%), rivulets (22%), ponds (14%) and wells (11%) were main breeding source suggesting that RBPs and rivulets were highly productive for anopheline mos- quitoes. However, temporary breeding habitats, i.e. stray fields (7%) and rice-fields (7%) were also found with anopheline breeding.
Likewise, at Gola, both permanent and temporary
Table 1. Total number of anopheline immatures collected from different breeding habitats and died during rearing from Ramgarh
and Gola sites from August 2012 to July 2013 Breeding habitats No. of larvae and No. of larvae
pupae collected and pupae died Ramgarh
River bed pools 952 537
Rivulets 762 394
Ponds 479 228
Wells 375 166
Stray fields 225 107
Rice-fields 221 148
River margins 142 78
Ditches 133 72
Irrigation channels 76 30
Burrow pits 31 29
Total 3396 1789
Gola
Ponds 1383 645
Ditches 422 245
RBPs 380 182
Stray fields 342 163
Wells 250 136
Rice-fields 203 142
Irrigation channels 64 30
River margins 34 9
Seepages 21 9
Total 3099 1561
Table 2. The emerged anopheline species in different habitats at Ramgarh study site during August 2012 to July 2013 SpeciesRiceStrayBorrowDitchesRBPsWellsRivuletsPondsRiverIrrigationTotal fieldsfieldspitsmarginschannels No. of habitats sampled714181727282556138 An. culicifacies10 (23.8)5 (9.3)04 (11.4)181 (68.3)21 (17.8)95(38.6)1(0.6)6(14.6)2(7.1)325 (32.7) An. fluviatilis2 (4.8)10 (18.5)0033 (12.5)68 (57.6)64 (26)30 (18.3)29 (70.7)14 (50)250 (25.1) An. annularis2 (4.8)6 (11.1)011 (31.4)7 (2.6)9 (7.6)28 (11.4)58 (35.4)3 (7.3)3 (10.7)127 (12.8) An. pallidus02 (3.7)0000013 (7.9)0015 (1.5) An. theobaldi02 (3.7)05 (14.3)30 (11.3)1 (0.8)16 (6.5)01 (2.4)055 (5.5) An. vagus3 (7.1)4 (7.4)02 (5.7)002 (0.8)001 (3.6)12 (1.2) An. subpictus19 (45.2)9 (16.7)2 (100)12 (34.3)3 (1.1)2 (1.7)18 (7.3)16 (9.8)03 (10.7)84 (8.4) An. nigerrimus2 (4.8)0000000002 (0.2) An. sergentii01 (1.9)001 (0.4)01 (0.4)2 (1.2)005 (0.5) An. splendidus015 (27.8)01 (2.9)8 (3)3 (2.5)13 (5.3)13 (7.9)0053 (5.3) An. barbirostris0000010 (8.5)012 (7.3)2 (4.9)024 (2.4) An. tessellatus1 (2.4)00002 (1.7)00003 (0.3) An. jamesii0000000001 (3.6)1 (0.1) An. maculatus00002 (0.8)06 (2.4)0008 (0.8) An. jeyporiensis0000002 (0.8)4 (2.4)01 (3.6)7 (0.7) An. crawfordi3 (7.1)00002 (1.7)1 (0.4)15 (9.1)03 (10.7)24 (2.4) Total42542352651182461644128995 Values in parentheses indicate percent composition. Table 3. The emerged anopheline species in different habitats at Gola study site during August 2012 to July 2013 SpeciesRiceStrayPondsDitchesRBPsWellsIrrigationRiverSeepagesTotal fieldsfieldschannelsmargins No. of habitats sampled71758151322531141 An. culicifacies4 (11.4)6 (5.5)37(8.2)5(4.5)77(67)4(6.6)06 (40)0139(15) An. fluviatilis7 (20)17 (15.5)64 (14.2)33 (29.7)16 (13.9)32 (52.5)7 (38.9)7 (46.7)0183 (19.8) An. annularis015 (13.6)202 (44.9)20 (18)6 (5.2)1 (1.6)000244 (26.4) An. pallidus04 (3.6)32 (7.1)00000036 (3.9) An. theobaldi001 (0.2)04 (3.5)1 (1.6)0006 (0.6) An. vagus4 (11.4)1 (0.9)04 (3.6)1 (0.9)000010 (1.1) An. subpictus20 (57.1)36 (32.7)51 (11.3)31 (27.9)02 (3.3)02 (13.3)0142 (15.4) An. sergentii000001 (1.6)0001 (0.1) An. splendidus025 (22.7)14 (3.1)14 (12.6)9 (7.8)1 (1.6)009 (100)72 (7.8) An. barbirostris0012 (2.7)01 (0.9)10 (16.4)00023 (2.5) An. jamesii01 (0.9)02 (1.8)000003 (0.3) An. jeyporiensis03 (2.7)13 (2.9)00000016 (1.7) An. crawfordi02 (1.8)24 (5.3)1 (0.9)1 (0.9)9 (14.8)11 (61.1)0048 (5.2) An. aconitus0001 (0.9)000001 (0.1) Total351104501111156118159924 Values in parentheses indicate percent composition.
breeding habitats were recorded for anopheline species.
The maximum anopheline producing habitats were ponds (45%) followed by ditches (14%), RBP (12%), stray fields (11%) and wells (8%) (Table 3), indicating pond as ma- jor contributor to anopheline prevalence at this site.
Malaria vectors’ breeding preferences
The results revealed that malaria vector species are adapted to breed in a wide range of water bodies. Based on their emergence, the highly preferred seven breeding habitats of An. culicifacies, An. fluviatilis and An.
annularis were RBPs, rivulets, wells, ponds, river margins, ditches and irrigation channels (Tables 2 and 3). At Ramgarh site, An. culicifacies showed maximum preference for RBPs (68.3%) followed by rivulets (38.6%), rice-fields (23.8%), wells (17.8%) and river margins (14.6%) for its breeding (Table 2), whereas, An.
fluviatilis maximally preferred river margins (70.7%) followed by wells (57.6%) and irrigation channels (50%) as its ideal breeding site. The other breeding habitats, i.e.
rivulets, RBPs, ponds and stray fields were also associated with An. fluviatilis breeding. In contrast, An. annularis showed its highest preference for ponds (35.4%) followed by ditches (31.4%) and other habitats (Table 2).
At Gola site, An. culicifacies preferred mostly two breeding habitats, i.e. RBPs (67%) and river margins
(40%) (Table 3). The other habitats were less preferred.
However, An. fluviatilis mostly preferred wells (52.5%) followed by river margins (46.7%), irrigation channels (38.9%) and ditches (29.7%) (Table 3). Anopheles annularis immatures were more commonly found in ponds (44.9%) than other breeding habitats (Table 3).
The highest H' in stray fields (1.94) at Ramgarh site depicted highest anopheline diversity (Table 5). Com- paratively, other breeding habitats, i.e. ponds (1.89), rivu- lets (1.7), irrigation channels (1.61), and rice-fields (1.6) exhibited less anopheline diversity. The species E in stray fields (0.49), irrigation channels (0.48), rice-fields and ditches (0.43) (Table 5) indicated that the individuals in the community are not distributed more equitably among these habitats. However, E values near 0 for RBP (0.19) and wells (0.29) clearly indicated the dominance of some anopheline species and their unequal proportion in respective habitats. At Gola, the Shannon diversity index (H') was highest in stray fields (1.76), ponds (1.75) and ditches (1.7) (Table 5). The individuals of anopheline species in the community were distributed less equitably among these habitats. There was high dominance of few anophelines over other species in irrigation channels (0.16), RBPs (0.24) and ponds (0.29) (Table 5).
Meteorological data revealed that average daily air and water body temperatures were highly fluctuating at each sites of Ramgarh and Gola.The daily outdoor tem-
Table 5. Species diversity index and evenness at Ramgarh and Gola study sites during August 2012 to July 2013
Rice- Stray Ditches RBPs Wells Ponds Irrigation River Rivulet/
fields fields channels margins Seepages
Ramgarh
Shannon diversity index (H') 1.6 1.94 1.52 1.08 1.37 1.89 1.61 0.96 1.7
Evenness (E) 0.43 0.49 0.43 0.19 0.29 0.37 0.48 0.26 0.31
Gola
Shannon diversity index (H') 1.14 1.76 1.7 1.14 1.48 1.75 0.67 0.99 0+
Evenness (E) 0.32 0.37 0.36 0.24 0.31 0.29 0.16 0.34 0+
Table 4. Anopheline species categorization based on their relative density (%) at Ramgarh and Gola sites during August 2012 to July 2013
Ramgarh
Relative density 32.66 25.13 12.76 1.51 5.53 1.21 8.44 0.20 0.50 5.33 2.41 0.30 0.10 0.80 0.70 2.41 0
Density class D D D SD D SD D S S D SD S S S S SD S
Gola
Relative density 15.04 19.81 26.41 3.90 0.65 1.08 15.37 0 0.11 7.79 2.49 0 0.32 0 1.73 5.19 0.11
Density class D D D SD S SD D S S D SD S S S SD D S
D—Dominant, SD—Sub-dominant, S—Satellite species.
An. culicifacies An. fluviatilis An. annularis An. pallidus An. theobaldi An. vagus An. subpictus An. nigerrimus An. sergentii An. splendidus An. barbirostris An. tessellatus An. jamesii An. maculatus An. jeyporiensis An. crawfordi An. aconitus
Species
perature of Ramgarh site ranged from 11.75–37.07°C and the water body temperature ranged from 14.29–30.7°C during August 2012 to July 2013 (Fig. 2a). The average daily outdoor temperature was lower than average daily water body temperature from October to February months and higher from March to July months. The maximum outdoor temperature was 6.37°C higher and the minimum outdoor temperature was 2.54°C lower than water body temperature. However, at Gola site, the outdoor tempera- ture ranged from 12.87–36.5°C (Fig. 2b). Comparatively, the monthly outdoor temperature of Gola site was re- corded approximately 2°C higher than Ramgarh from October to April months, the trend was reversed after- wards. Likewise, rainfall pattern also varied at each site (Figs 2a and b). There was substantial variation in monthly rainfall in most of months. The maximum monthly rainfall was 470.8 mm at Ramgarh, whereas 385.4 mm at Gola site in the month of August.
DISCUSSION
The survey of immature anopheline breeding habi-
tats at Ramgarh district, Jharkhand revealed that there were ample and conducive sites for anopheline mosqui- toes to breed and survive throughout the year. The river bed pools and rivulets with a constant flow of water were important vector breeding habitats at both Ramgarh and Gola sites. Similar observations have been reported by Kusumawathie et al21 for anopheline breeding. In addition, the role of ponds, wells, rice-fields, ditches, stray fields with stagnant water conditions22–23 can not be ig- nored in anopheline larval productivity as those contrib- uted significantly to anopheline breeding.
During this study, An. culicifacies, An. fluviatilis and An. annularis, the known malaria vectors of District Ramgarh, were identified in wide range of breeding habi- tats. At Ramgarh site, An. culicifacies, the most domi- nant species showed highest breeding preference for RBP and rivulets, which might have served predominant ovi- position sites for this species. Similar findings were also recorded in earlier studies21–23. Besides, irrigation chan- nels, wells, seepages, pits, ditches, rice-fields have also been observed as preferred breeding habitats of An.
culicifacies24–25. Though, An. fluviatilis was earlier con-
Fig.2: Average daily outdoor temperature (°C), aquatic habitat temperature (°C) and rainfall (mm) at Ramgarh (a), and Gola (b) study sites during August 2012 to July 2013.
sidered to breed only in clean and slow flowing water, in the present study it preferred wells and rivulets which indicated its adaptation to changing climatic conditions.
Earlier studies also reported its occurrence in slows flowing streams, river margins, irrigation channels26, wells and thick vegetation27 as observed in the present study. It was observed that An. annularis breed in all type of habitats; however, its major breeding was recorded in ponds, rivulets, and ditches associated with algal growth and grassy margins. Similar findings were re- corded by Yadav et al28 and Sahu et al29. The ability of An. culicifacies, An. fluviatilis and An. annularis to breed excessively in RBPs, wells and ponds, respectively poses a particular problem for this region. Increased breeding of anopheline vectors in such local water bodies may in- fluence malaria transmission in the region. Therefore, critical surveillance and subsequent management of breeding habitats is prerequisite for effective vector con- trol in this area.
Meteorological data of Ramgarh and Gola sites re- vealed temperature variation in the outdoor condition in spite of being located in the same district, which might delay or fasten the development of immature anophelines into adults. Earlier studies also suggested the higher wa- ter body temperature in typical mosquito breeding sites than that of atmospheric air, with a general difference of 4°C30, as observed in present study. Therefore, higher water temperature might shorten the larval development time, and hence increase population growth rate31. In ad- dition, rainfall plays an important role in increasing tem- porary breeding habitats, which provides the medium for development of aquatic stages of anophelines, influenc- ing vector population and malaria prevalence32. Previ- ous studies also suggested that anopheline population dy- namics are not directly influenced by rainfall, but by the level of the stable reservoirs, which offer a constant op- portunity for female anophelines to lay their eggs33.
CONCLUSION
The study revealed that a vast number of productive Anopheles breeding sites in the area of Ramgarh district, Jharkhand state, India are responsible for greater abundance of malaria vectors, which have been adapted to wide range of breeding habitats under changing ecological and meteorological conditions. The river bed pools, river margins, wells and ponds were the major breeding sites for anopheline vector species in this region. Besides ecological conditions, the prevailing outdoor temperature, water body temperature and rain- fall also affected larval density. Therefore, the selective
larval control methods should also be considered in this area.
ACKNOWLEDGEMENTS
The authors acknowledge the Director, National Institute of Malaria Research, New Delhi, for providing opportunity to carry out this study and Indian Council of Medical Research, New Delhi for providing financial support through ‘Global environmental change and health task force project’. The authors also thank field and labo- ratory staff, Messrs Saroj Kumar Das and Chandan Gupta for their assistance during the course of study.
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Correspondence to: Dr R.C. Dhiman, Scientist ‘G’, National Institute of Malaria Research (ICMR), Sector 8, Dwarka, New Delhi–110 077, India.
E-mail: [email protected]
Received: 26 February 2016 Accepted in revised form: 5 September 2016
