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Table of Contents
RESEARCH ARTICLE
Year : 2019  |  Volume : 56  |  Issue : 4  |  Page : 339-344

A study on bionomics of malaria vectors in three different eco-epidemiological settings in Upper Krishna Project catchment area of Karnataka state, India: Implications for malaria vector control


ICMR–National Institute of Malaria Research, Field Unit, Bengaluru, India

Date of Submission16-Jan-2018
Date of Acceptance25-Feb-2020
Date of Web Publication30-Nov-2020

Correspondence Address:
Dr. Susanta Kumar Ghosh
ICMR–National Institute of Malaria Research, Field Unit, Nirmal Bhawan, ICMR Complex, Poojanahalli, Kannanmangla Post, Devanahalli Taluk, Bengaluru–562 110
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.302037

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  Abstract 

Background & objectives: Understanding of malaria vector distribution and influence of climatic environments is essential for devising control strategies. The aim of the study was to study the bionomics of prevalent malaria vectors in three different settings for development of evidence-based sustainable malaria control strategy with special reference to vector control.
Methods: Three villages with different eco-epidemiological settings like riverine-low malarious, riverine-high malarious and non-riverine high malarious villages were selected after baseline studies. Entomological aspects such as man hour density, per structure density, mosquito landing collections, sibling species identification, insecticide susceptibility status, parity rate, etc. were studied in these three villages following standard methods and techniques. The effect of these variables was analysed statistically.
Results: Mosquito collections revealed the presence of three malaria vectors in the study villages, namely Anopheles culicifacies s.l., An. fluviatilis s.l. and An. stephensi (Diptera: Culicidae) with varying proportions and seasonal abundance. Densities of the principal malaria vector, An. culicifacies varied seasonally. Anopheles culicifacies was found resistant to DDT (4%), malathion (5%), lambda-cyhalothrin (0.05%) and alpha-cypermethrin (0.1%). Peak density of An. culicifacies was found during post-monsoon months starting from August-September to December in the high malarious villages.
Interpretation & conclusion: The main vector control interventions should be planned in the post-monsoon months in these villages and suitable insecticide resistance management strategy should be followed as An. culicifacies was found resistant to DDT, malathion, alpha-cypermethrin and lambda-cyhalothrin in the study area.

Keywords: Anopheles culicifacies; An. fluviatilis; An. stephensi: bionomics; insecticide susceptibility; parity rate; vector control


How to cite this article:
Tiwari S, Uragayala S, Ghosh SK. A study on bionomics of malaria vectors in three different eco-epidemiological settings in Upper Krishna Project catchment area of Karnataka state, India: Implications for malaria vector control. J Vector Borne Dis 2019;56:339-44

How to cite this URL:
Tiwari S, Uragayala S, Ghosh SK. A study on bionomics of malaria vectors in three different eco-epidemiological settings in Upper Krishna Project catchment area of Karnataka state, India: Implications for malaria vector control. J Vector Borne Dis [serial online] 2019 [cited 2021 Oct 18];56:339-44. Available from: https://www.jvbd.org/text.asp?2019/56/4/339/302037


  Introduction Top


Malaria is a local and focal disease, and the transmission pattern varies from different topographical features. eco-epidemiological settings and socio-economic conditions. The presence of different malaria parasites and vector species, climatic diversity affecting the growth and proliferation of the parasite and the vector(s), influence malaria transmission in some parts of India. Understanding the spatial distribution of disease vectors, knowledge about the mosquito species and their bionomics, size and peaks of activities, seasonal changes in vector population, etc. are very important aspects in planning effective intervention and prevention strategies[1].

Six major vector species, i.e. Anopheles culicifacies Giles 1901, An. fluviatilis James 1902, An. minimus Theobald 1901, An. dirus Peyton & Harrison 1979, An. sundaicus Rodenwaldt 1925, and An. stephensi Liston 1901 (Diptera: Culicidae) belonging to Anopheles genera are responsible for spreading malaria in India, in addition to few vector species which play a minor role in malaria transmission[2],[3],[4]. Of these, An. culicifacies alone is responsible for the transmission of 60-70% malaria cases reported in India annually[5]. Many of these species belong to sibling species complexes. A species complex is a taxo- nomic group of morphologically identical and closely related species. In addition to differences in the vector status of each species, sibling species also have important differences in their geographical distributions[2],[4],[5],[6].

There are five sibling species of An. culicifacies designated as species A, B, C, D and E that are distinguishable by paracentric inversions in polytene chromosomes and mitotic karyotype Y chromosome polymorphism. They are distinct biologically varying in breeding, feeding and resting habits and also in vectorial potentials[3],[7],[8],[9],[10],[11],[12]. Another major vector of malaria, An. fluviatilis prevalence associated with fore sted and hilly terrain, has four biologically distinct but morphologically identical sibling species designated as S, T, U and V which can be identified by species-specific paracentric inversion in polytene chromosomes[4][13]. Anopheles stephensi is the main urban malaria vector and has three distinct variants known as type form, intermediate form and var. mysorensis that are distinguished by egg morphometry[4],[14]. Proportion and distribution ofthese vectors and their sibling species varies with the forest cover, crops, type of housing, irrigation system, breeding sites, etc. available in the area and variation in minimum and maximum temperature, quantum of rainfall, and rainy days which many times vary within the district[3],[4],[14].

Malaria transmission pattern changes from terrain to terrain and depends on the presence and distribution pattern of the sibling species and variants, feeding behaviour and vectorial capacity of the prevalent species. Malaria is problematic in Upper Krishna Project (UKP) areas of Karnataka state, India due to the presence of congenial atmospheric conditions that aid in breeding and proliferation of vector species. The present study was undertaken to study the bionomics of malaria vectors, their seasonal prevalence, biting and resting behaviour, insecticide susceptibility status, etc. in Almatti Dam catchment area in Karnataka state, which will help in formulating situation-specific vector control measures.


  Methods Top


Study area

Upper Krishna Project is the biggest irrigation project in Karnataka state constructed on the River Krishna and occupies small parts of Vijayapura (erstwhile Bijapur), Bagalkot, Kalaburgi (erstwhile Gulbarga), Raichur and Yadgir districts. There are four antimalaria units, namely Almatti, Narayanpur, Kembhavi and Bheemanarayana Gudi under UKP area. There are 184 villages (Almatti 79, Narayanpur 31, Kembhavi 37 and Bheemanarayana Gudi 37) under the project area. Most of the villages are situated on the bank of the river. In the villages, houses are mostly pucca made up of stones.

River bed pools and streams are the major malaria vector breeding sites in this area. Topographically the area is undulating, broken up mountains and deep ravines. The climate is hot, semi-arid tropical steppe. Canals, river and streams are the major sources of irrigation. Farming is the main source of economy. Paddy, millets, sugarcane, ground nut, maize and jowar are the main crops grown in the area.

Selection of study villages

A total of three villages were selected based on malaria incidence and major anopheline breeding sites. One high malaria incidence village was selected along the river bed (riverine-high malarious village) and another village situated away from the river bed (non-riverine high malarious village). Third village with low malaria incidence was selected along the embankment of the river (riverine- low malarious village). Malaria incidence and major anopheline breeding sources in these villages are shown in [Table 1]. The study was carried out from August 2012 to May 2014. Monthly mosquito landing collections on human and animal baits were done from August 2012 to September 2013.
Table 1: Malaria incidence data of selected villages prior to the study

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dult mosquito collection

Adult mosquitoes were collected from the three selected villages. Monthly indoor resting mosquitoes were collected from human dwellings and cattle sheds in each study village by suction tubing method in the morning between 0600 and 0900 hrs. Collected mosquitoes were brought to the field laboratory, species were identified with the help of standard keys[15],[16], and man hour density was calculated. Pyrethrum space spray was carried out one each in human dwelling and cattle shed in each study village and species-specific per structure density was calculated.

Immature mosquito collection

All the anopheline breeding habitats within and around 1 km of the study villages were checked by dipping method on monthly basis. Anopheline immatures from different breeding habitats were collected, reared in the camp laboratory till adult emergence and anopheline species were identified with the aid of standard keys[15],[16].

Sibling species identification Ovaries of semi-gravid An. culicifacies were preserved in Carnoy’s fixative (Methanol and acetic acid 3:1). Polytene chromosomes were prepared, stained with aceto orcein stain and sibling species were identified as per the method previously described[3],[6],[12]

Parity rate

Field collected unfed/semi-gravid An. culicifacies were dissected in the camp laboratory for parity. In unfed females, ovaries were observed for distended tracheolar skeins and in semi-gravid mosquitoes, ovarian follicles for nodes formed after the egg-laying[17].

Resting feeding habitat preference

All adult malaria vectors, viz. An. culicifacies, An. stephensi and An. fluviatilis collected in the morning hours were processed for abdominal condition, i.e. unfed, full- fed, semi-gravid and gravid to find out the extent ofendophily and/or exophily nature. Outdoor light trap collections were also carried out monthly. Mosquitoes trapped in the whole night were collected and brought to the temporary laboratory for species identification. The abdominal condition, i.e. unfed, full-fed, semi-gravid and gravid ofthe mosquito was also recorded. The number of fed/semi- gravid/gravid mosquitoes indicate the exophily nature.

Biting pattern

Adult mosquitoes landing on human (indoor and outdoor) and on animal baits were collected for whole night from 1800 to 0600 hrs by suction tubing method to study the biting pattern of different mosquito species especially of vector species. Hourly collected mosquitoes were kept separately, brought to the temporary field laboratory and identified to species under microscope using standard keys[15],[16].

Insecticide susceptibility test

During the high-density period adult vectors were exposed to diagnostic dosages of different insecticide impregnated papers as per WHO method to find out the susceptibility status[18].

Statistical analysis

Statistical analysis was carried out following Graph Pad Prism 7.04 (Version 2017).

Ethical statement

The ethical aproval for the study was obtained from the ethical committee of NIMR with No. ECR/NIMR/ EC/2011/113; dated 25 Nov 2011.


  Results Top


Longitudinal surveys in three localities revealed the prevalence of An. culicifacies, An. stephensi, An. fluviatilis, An. subpictus, An. annularis, An. vagus, An. tessellatus, An. jamesi, An. nigerrimus and An. barbirostris. Predominant species were An. culicifacies and An. subpictus with the proportion about 70 and 15%, respectively. The proportion of An. stephensi was around 5% and of An. fluviatilis was 1%. Breeding site surveys revealed that seepages and water pockets in river with stony margins and sandy soil were the major breeding habitats of An. culicifacies in the riverine-high malarious village. In the riverine-low malarious village, muddy pockets, seasonal streams and seepages were the main breeding habitats. In the non-riverine village, wells, irrigation tanks and seasonal streams were the main breeding habitats. During the study period, the mean anopheline III & IV instar larval densities in river with sandy margin, river with muddy margin, seepages, seasonal streams, irrigation tanks, and wells were 0.87, 0.31, 0.56, 0.47, 0.22, and 0.13, respectively. Adult emergence revealed eight anopheline species, namely An. culicifacies, An. stephensi, An. subpictus, An. vagus, An. annularis, An. tessellatus, An. nigerrimus and An. barbirostris from these breeding sites. Malaria vector An. culicifacies contribution was maximum from river with sandy margin (52.7%) followed by seasonal streams (19%), seepages (9.4%), irrigation tank (8.7%), river with muddy margin (5.5%) and wells (4.7%).

Man hour density of An. culicifacies mosquitoes from the three selected villages over the period from August 2012 to May 2014 are summarized in [Figure 1]. The prevalence of An. culicifacies in the riverine-high malarious village was higher than the other two villages. Peak densities could be recorded during November to February in the riverine-high malarious village, whereas peak densities could be recorded during August to September in the both riverine-low malarious village and non-riverine-high malarious village. Interestingly, in non-riverine high malarious village the man hour densities remained very low in comparison to other two settings. ANOVA test revealed significant (p <0.05) difference among mean man hour densities ofmalaria vectorAn. culicifacies in the riverine-high malarious village (mean ± SD; 15.88 ± 13.45), riverine-low malarious village (mean ± SD; 8.22 ± 8.96) and non-riverine-high malarious village (mean ± SD 2.75 ± 5.36)
Figure 1: Man hour density of An. culicifacies mosquitoes collected from study villages from 2012–2014.

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Per structure density (PSD) of An. culicifacies collected through total catch method in the three study villages are presented in [Figure 2]. The PSD of An. culicifacies in the riverine-high malarious village showed its peak during winter (November-December), whereas in the riverine-low malarious and non-riverine-high malarious villages, high PSD was found in September. The results indicate that high densities of An. culicifacies could be observed during post-monsoon months. The average PSD (mean ± SD) in the riverine-high malarious, riverine-low malarious and non-riverine-high malarious villages was 15.38 ± 14.91, 12.47 ± 26.09, and 3.06 ± 5.57, respectively. ANOVA test revealed no significant difference (p >0.05) among these three types of settings.
Figure 2: Per structure density of An. culicifacies in study villages.

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Parity rates of female mosquitoes in the three study villages are depicted in [Figure 3]. The results indicate higher parity rates in the riverine-high malarious village, followed by riverine-low malarious village and non-riverine-high malarious village. The results indicate more longevity of vector mosquitoes in the riverine setting than non-riverine setting.
Figure 3: Parity rate of An. culicifacies in study villages.

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Number of females collected per bait per night in the three villages is shown in [Figure 4]. The results indicate greater biting intensity of An. culicifacies in the riverine- high malarious village followed by riverine-low malarious village. During post-monsoon months, few mosquitoes landed on human bait could only be recorded in the non- riverine-high malarious village.
Figure 4: No. of mosquitoes landed per bait per night on human bait in study villages.

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Sibling species composition of An. culicifacies mosquitoes collected from the three study villages is shown in [Table 2]. The proportion of species A, recognised as vector of malaria was high in both high malarious villages than species B, which is a poor malaria vector, if at all. Whereas in riverine-low malarious village, the proportion of species A and B was almost equal. This once again emphasizes the role of sibling species in malaria transmission.
Table 2: Sibling species composition of An. culicifacies in the study villages

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Insecticide susceptibility status of the An. culicifacies mosquitoes collected from these villages showed resistance to DDT 4%, malathion 5%, alpha-cypermethrin 0.1% and lambda-cyhalothrin 0.05%, indicating development of resistance to all insecticides used in the control of mosquitoes [Table 3].
Table 3: Susceptibility status of malaria vector An. culicifacies against different insecticides in UKP Almatti and Narayanpur areas during 2012–2013

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  Discussion Top


Knowledge of feeding and resting behaviour of mosquito is essential for planning and implementing vector control interventions (endophilic-indoor residual spray and bed nets as personal protection and other control tools), while control of mosquitoes that are exophilic could be targeted using outdoor space spray approaches or larval control[19].

Present study results showed that the peak density of malaria vector An. culicifacies in the riverine-high malaria village was in December during post-monsoon season. The density gradually declined up to April in summer season and a second minor peak was observed in June at onset of the monsoon. In the riverine-low malaria village, the peak density was noticed in September in monsoon season which gradually declined up to April in summer and the second minor peak, lesser than riverine- high malaria village was observed in June. In the non- riverine-high malaria village, the peak density was found only in the month of September in post-monsoon season. The parity rate of An. culicifacies was more in the riverine and non-riverine-high malaria villages than riverine- low malaria village. Anopheles culicifacies was mainly endophilic in resting behaviour and zoophagic in feeding behaviour. Indoor resting of An. culicifacies in new construction sites was more than old structures. The peak landing of An. culicifacies for biting in the riverine and non-riverine high malarious villages was in November and September, respectively in third quarter of night between 0200 and 0300 hrs. However, in the riverine-low malaria village, there was no clear peak and intermittent landing was observed mainly from June to November in second half of the night.

Among major vectors of malaria in India, An. culicifacies sensu lato is the most abundant vector and is highly adaptive species. It is widely distributed in rural and peri-urban areas of India. Anopheles culicifacies has played a major role in perennial malaria transmission in forested areas (e.g. Madhya Pradesh), and this vector species has penetrated deforested areas of northeast states of the country[20],[21],[22],[23].

Rain water flowing in canal and its seepage from canal is likely to facilitate breeding of species such as An. culicifacies in some villages[24],[25],[26]. Joshi et al[26] also reported that in the villages which are just attached to canal or those which are in close vicinity, An. culicifacies has been encountered in two villages, that too during winter season. In the present study also, peak density of An. culicifacies could be observed during post-monsoon months. Anopheles culicifacies populations build up during monsoon and post-monsoon seasons, bring periodical focal outbreaks and epidemics throughout its range of dis- tribution[27],[28].

Five sibling species spread across India have distinct biological characteristics and role in malaria transmission. All the members of An. culicifacies Complex except species E were predominantly zoophilic[3],[4],[27]. Species A has relatively high anthropophilc index (0-4%) compared to species B and D (0-1%), species C has intermediate level of anthropophilic index (0-3%), and species E, has the highest anthropophilic index (80%). All the member species largely rest indoor human dwellings preferentially on roof ceilings after feeding on cattle, but also rests outdoors. All are night biting species with different peak biting activity. The biting activity of A, B and C was observed all through the night except for D for which there was no biting after midnight[4]. The peak biting activity of species A and B occurred between 2200 and 2300 hrs whereas for species C, it was seasonal; in April it occurred between 1800 and 2100 hrs and shifted to second quarter ofthe night in December[14]. In the present study, two sibling species A and B were observed with the proportion of 61.4 and 38.6%, respectively. Sibling species A which is main malaria vector was found more in the high malarious villages than the low malarious village. Both the species were found to rest indoor. The biting was observed throughout the night mainly on cattle.

It is generally believed that irrigation development offers ideal habitats for the proliferation of anophelines, including vectors of malaria. In other studies, it was documented that high mosquitogenic conditions prevail in irrigation project areas and the importance of irrigation water release in maintaining high An. culicifacies adult density during the dry season[24],[25],[27],[29] facilitating extended malaria transmission in these areas. It is concluded that much attention is needed in irrigation project areas for the control of malaria vectors and focussed as well as targeted interventions are needed during monsoon and post-monsoon months for the control of An. culicifacies. In view of development of resistance in An. culicifacies in this area to synthetic pyrethroids, alternative strategies should be implemented for vector control.

Conflict of interest: None


  Acknowledgements Top


The authors acknowledge the support of the Senior Health Officer, Almatti and his staff for their support in the study. The authors extend warm thanks to staff of the NIMR, Field Unit, Bengaluru for their continuous support in field activities. The project was funded by the Indian Council of Medical Research, New Delhi through intramural grant.

 
  References Top

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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]



 

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