Sustainable control of malaria employing Gambusia fishes as biological control in Jalore and Barmer districts of Western Rajasthan
Himmat Singh, Sanjeev Kumar Gupta, Kumar Vikram, Rekha Saxena, Aruna Srivastava, BN Nagpal
ICMR-National Institute of Malaria Research, New Delhi, India
Correspondence Address:
B N Nagpal
ICMR-National Institute of Malaria Research, Sector 8, Dwarka, New Delhi 110077
India
Source of Support: None, Conflict of Interest: None
CheckSardar Sarovar Irrigation Canal system was constructed by Narmada Valley Development Authority (NVDA) to cater to drinking water as well as for irrigation purposes in Jalore and Barmer districts of Western Rajasthan. To cater to the needs of water for the villagers in the command areas, ‘Diggies’ (surface water tanks) with ‘Sumpwells’ (water supply surface tanks) were installed. In a health impact assessment study of the irrigation canals from December 2010 to February 2016, the breeding of two major malaria vectors. An. culicifacies and An. stephensi were observed in diggies and sumpwells. As a biological control, Gambusia affanis fishes were employed for larval control in such stagnated water sites during the intervention phase viz. February 2012 in 251 diggies and 251 sumpwells. A significant reduction of breeding in diggies (99.54%) and sumpwells (97.81%) was observed. The positivity and larval density (dip index) were monitored in the control from up to February 2016 for their sustainability.
Keywords: Biological control, larvivorus fish, Anopheles, malaria, diggies, sumpwells
Malaria is a worldwide problem and is associated with several confounding factors mainly vector ecology, landuse pattern, drug resistance, insecticide resistance, socio-economy, and many other factors. Malaria is said to be a local and focal disease[1] that changes the dynamics according to local settings. However, changes in land use and the introduction of new ecosystems change the dynamics of malaria by enlarge[2],[3],[4],[5],[6],[7],[8].
To cater to increasing population’s food demand, more agricultural production is required as a result of which there is an increase in irrigation canal systems for agriculture as well as for drinking water supply. Irreversible changes in ecosystem in the mega irrigation canal projects in floral and faunal composition[9],[10]. The developmental activities and irrigation canals are proving to be an essential requirement despite having a major contribution to malaria cases. In Rajasthan, India four major irrigation canal systems viz. Indira Gandhi Canal, Chambal Irrigation Canals, Mahibajaj Sagar Irrigation Canals, and Sardar Sarovar Irrigation Canal system have been constructed to cater to drinking water as well as for irrigation purposes.
Incidences of malaria cases have been found to increase during the construction and establishment of dams and irrigation canals during the construction of Sharda Canal, Uttar Pradesh from 1924 to 1928. There was 32 folds increase in malaria cases from 1979 to 1997 when Bargi dam, Madhya Pradesh, India was constructed[11]. A similar happening was observed in several other irrigation projects in Odisha, Almatti Dam, Karnatka, Indira Gandhi Canal, Rajasthan as well[12],[7].
Biological control, with particular reference to larvivorous fishes has proved to be an important strategy for malaria control programmes since the twentieth century in both developed and developing countries[13]. Many studies revealed the role of Gambusia fishes in the control of larval breeding of mosquitoes[14],[15],[16],[17],[18]. Mosquito breeding and its control through Gambusia affinis in paddy fields has shown efficient results whereby over 87% of mosquito larval control has been observed[19].
The present study is a part of a health impact assessment-based intervention study conducted in collaboration with the Department of Health and Narmada Canal Authority, Rajasthan in Jalore and Barmer, districts of Rajasthan. The study envisages sustainable cost-effective control over malarious situations which may arise due to the introduction of these irrigation canals in this unstable malaria zone of southwestern Rajasthan. This research is part of a broader research study that focuses specifically on the aquatic stage of mosquitoes that result in VBDs. The main focus remains centered on how the methods that evolve from this research can be applied by the local communities and reduce the density of vectors and, subsequently disease. Diggies and sumpwells are the main water harbouring reservoir bodies constructed during the Narmada Canal Project (NCP) by the name of Narmada Main Canal (NMC) in Jalore and Barmer districts of Rajasthan to deal with the utmost water deficit prevailing situation. The present study is an attempt to find out whether biological control using Gambushia fishes is effective in the control of larval breeding in the diggies and sumpwells.
Material & MethodsStudy area
Jalore and Barmer districts of Rajasthan are the study area located in the Western parts of the Indian sub-continent, both represent typical desert ecological conditions. The district Barmer is situated between 24.58° to 26.32° N latitudes and 70.05° to 72.52° E longitudes while Jalore at latitude 25.22° N and longitude 72.58° E. [Figure 1]. Barmer district represents a typical desert with rainfall ranging from 200–250 mm per annum and the temperature ranges between 0°C in winters to 50°C in summer. Whereas Jalore is a part of a typical desert but the eastern boundary of Jalore touches the Aravalis mountain range. Rainfall ranges from 250–412 mm per annum, and temperature varies from 4°C to 50°C. Malaria incidences were high in these areas as per 2010 State health department reports.
Figure 1: Location of Jalore and Barmer Districts in Rajasthan state, India.Entomological surveillance
Since the study started with the canal development phases, the study was divided into two different phases viz. study phase (2009–2011) and the intervention phase (2012–2016). As the study was initiated concurrently with the construction of diggies and sumpwells, therefore, initially 152 diggies and 152 sumpwells that were complete and connected with water supply were used for the collection of positivity data. Thereafter, 99 more diggies and sumpwells (a total of 251 diggies and 251 sumpwells) were added in the study.
The positivity was accounted for with the presence of all larval stages except 1st Instar larvae. For calculating the “Dip Index” at least 8 dips were taken from every site (diggies and sumpwells), 4 dips from each corner and 4 dips randomly. The average number of larvae collected from dips were counted as the dip index of the site. During the survey, if the growth of vegetation was observed in the margins of diggies, de-weeding was done accordingly to improve the marginal reach of fishes for larvae feeding.
Entomological surveillance was conducted in the selected villages of the command area during all intervention surveys in Jalore and Barmer. Adult mosquitoes were collected from the surrounding villages for vector species estimation of the area. In addition to this initially, the collection of larvae was also done to assess the species breeding in different sites. The identification of species was carried out using standard taxonomic keys[20],[21].
Intervention
The intervention was done deploying Gambusia affinis procured from the National Vector Borne Disease Control Program (NVBDCP), Government of India. The local hatchery of fishes was made in the escape water of the NMC main canal. The fishes were reared in a local hatchery till February 2012 thereafter, these fishes were used for intervention. Gambusia fishes were released at the rate of 5–10 fishes per linear meter in 3 females to 2 male ratios as per guidelines[22]. The two main intervention sites were diggies and sumpwells. Diggies are square-shaped water ponds of 20ft x20ft with 8ft depth used for storing water for the supply of drinking water to a nearby village and sumpwells with 5ft x10ft with 10ft depth used for collecting water for pumping water.
Data collection and analysis
Larval density was calculated based on the presence of the 2nd stage onward larvae and pupae through the standard dip method. The adult collection was done using the hand catch method using an aspirator. Data on malaria was collected from Health Department on a regular basis. The entomological data were collected through field surveys twice a year and from 2014 onwards thrice a year. Analysis was conducted using Microsoft Excel.
Ethical statement
Since there is no involvement of humans and animals in the study, the study was exempted from ethical clearance. However, we have taken the consent of the house owners for conducting mosquito surveillance.
ResultsSince vector control is an essential part of reducing malaria transmission, the present study was focused on the reduction of larval density to reduce the mosquito density of adults in the Narmada Canal Command area. The diggies and sumpwells are of utmost concern under the proposed work as they harbor water throughout the year. A tremendous reduction was observed in the breeding of larvae (third, fourth stage larvae and pupae) by the intervention of releasing larvivorous fishes (Gambusia).
The average positivity of the diggies was 93.7% (ranging from 88.4% to 96.8%) which was found to be considerably high during the study phase. After the introduction of Gambusia fishes in the intervention phase, a steep reduction (83.1% in six months) was observed, thereafter the reduction was found consistent, and from March 2014 onward, positivity remained <2% in the diggies till the completion of the study. The overall reduction in positivity was 99.5%. The density of larvae in the positive diggies measured through the dip index also showed a reduction of 95.9% within six months of initiation of intervention phase and thereafter after February 2015 onward dip index remained <2 in the diggies up to February 2016 [Table 1]; [Figure 2].
Figure 2: Reduction in larval positivity in diggies and sumpwells after releasing Gambusia fishes from February 2012 onwardsTable 1: Larval density/dips before and after releasing the Gambusia fishes in diggiesSumpwells also showed similar behavior, average positivity was 95.9% (ranging from 92.0% to 98.43%) in the study phase. At the initiation of the intervention phase, a reduction of 72.0% was observed. Thereafter the reduction was consistent and from September 2014 onwards, positivity remained < 4% till the completion of the project. The overall reduction in positivity was 97.8%. The dip index in Sumpwells also showed a reduction of 87.5% within six months and thereafter after February 2015 onward dip index remained <4 [Table 2] & [Figure 2].
Table 2: Larval density/dips before and after releasing the Gambusia fishes in sumpwellThe densities of mosquitoes (Per Man Hour Density, PMHD) and the species were also accounted for through entomological surveillance in the surrounding command villages of the Canal where diggies and sumpwells were installed for irrigation. During the entomological surveillance of command villages, 16 species of mosquitoes (9 Anopheles, 3 Aedes & 4 Culex species) were collected during the study period from 2010 to 2016 [Table 3].
When the average PMH of pre-intervention and post-intervention periods were compared there was a significant reduction observed (χ2 = 28.93; p≥0.01). An. subpictus was found to be the most prevalent followed by Cx. quniquefasciatus and An. culicifacies. However, among the malaria vectors An. culcifacies and An. stephensi were the most common vectors found [Table 2] & [Figure 3]. There was a reduction in major vector species i.e. An, culicifacies, and An. stephensi which breeds commonly in such small water tanks in western Rajasthan. In the absence of other water breeding sites, these species preferably breed in diggies and sumpwells.
Figure 3: Reduction in overall PMH density and density of two major malaria vectors after intervention (village n=12=14)There was strong correlation found between reduction in diggies positivity and Overall PMH density (r=0.805). Similarly a positive correlation was found between dip density and overall PMH density reduction during the study period. This shows that the reduction in positivity and density has a significant effect on the overall density of mosquitoes in the vicinity. However, less association was observed between Diggies positivity and Density of both major vector species, i.e., An. culicifacies and An. stephensi [Table 4].
Table 4: Correlation between diggies positivity and PMH densities of malaria vectorsThe cases of malaria were high during the surveillance from 2010 to 2012. With the introduction of fishes as an intervention the densities of mosquitoes reduced and the cases were also observed to be reduced [Figure 4].
Figure 4: Incidences of malaria in Sanchore tehsil of Jalore district in the command area of NMC DiscussionSouth-Western Rajasthan is one of the water deficit regions in India, and potable and irrigation supply is a need for the inhabitants. The introduction of a canal irrigation system is always required. However, such introductions involve landuse pattern change and bring irreversible changes to the ecosystem, socio-economy, and agriculture, in addition to an increased threat of vector-borne diseases if timely actions of mitigations are not taken23.
In such installations where freshwater introduction is involved, there is a need for an effective, sustainable, and bio-friendly vector control strategy. In larger landmass where IRS and source reduction are not possible, the use of larvivorus fishes was the suitable choice in the ecological system of the southern fringes of Jalore and Barmer. The Narmada irrigation canal has recently changed the landuse pattern due to the introduction of water. It is evident that malaria has been introduced in the Indira Gandhi Canal command area in the north and northwestern part of Rajasthan during its construction in year[7]. Fish intervention in diggies and sumpwells proved to be very effective in controlling larval as there were a significant (99.5%) reduction in the positivity of diggies (from 96.8% to 0.45 %) and 97.8% sumpwells (from 92.0% to 2.0%). The introduction of canals increased malaria in fragile ecosystems i.e., an unstable zone for malaria, the areas where the landuse has majorly changed, and agricultural practices have been introduced than the zones where the landuse pattern has not changed much[24]. Introduction of the Indira Gandhi irrigation canal in 1962 in northwestern Rajashan where there was no water in the large landmass, the water introduction made an irreversible changes in flora and fauna. The water-logging due to seepage increased the density of Anopheles culicifacies, resulting in high incidences and the establishment of malaria in the command area[7]. Narmada canal has similar irrigation diggies associated with sumpwells as they were made in the Indira Gandhi Canal system but the primary purpose was irrigation through drip irrigation. The introduction of fishes in these diggies and sumpwells made a considerable change in the density of mosquito larvae and the cases of malaria post 2012 when the intervention was started.
The entomological surveillance in command villages of adult mosquito density showed a significant reduction after the intervention. Other studies have also shown a similar reduction. Among the major vector species, An. culicifacies and An. stephensi were prevalent in the command area villages during the duration of the study. A major impact of the intervention was on the density reduction of An. culicifacies as it being an outdoor breeding species in the ponds and tanks. It was also evident that domestic containers breeding species like An. stephensi and Ae. aegypti also showed a reduction, which maybe due to change in water storing practice of inhabitants of command area village after continuous water availability through canal water.
Culex species found breeding in diggies and sump-wells also showed a reduction, which may be due to fish intervention although there may be other breeding sites in the villages. Annual data of this region concurrently showed a reduction in the malaria cases, maybe due to a reduction in malaria vector species. Due to landuse change and consistent agricultural practices, there is a reduction in the local migration of inhabitants. As a result of this, the possibility of acquiring parasites from the endemic areas is also reduced. The studies have shown evidence of migrant malaria in western Rajasthan[25],[26].
Our findings are supported by the earlier studies viz. Hyderabad city, India where the study was conducted[27] on wells where the release of the G. a. holbrooki controlled the breeding of An. stephensi in hundreds of wells for about two years. Similarly, another study carried out[28] to assess the feasibility of controlling mosquito breeding in casuarina pits (as An. subpictus is the predominant breeding species) in four coastal villages of Puducherry (then Pondicherry) using G. affinis where drastic reduction in mosquito breeding (~96%) was noted in casuarina pit. In contrast, in the check villages where no fish was noticed, the percentage of pit-breeding mosquitoes ranged up to 91.6%. Similarly, the study conducted by Rajnikant et al.[29] through a series of experiments, showed that G. affinis was the best predator of the larvae of An. stephensi breeding in overhead tanks. Control of mosquito breeding in rice fields through fish seemed to be promising. According to a report[30], when rice fields had been stocked with 250 to 750 G. affinis per hectare, there was a 95% and a 40% reduction in the immature density of An. freeborni and An. pulcherrimus respectively. In similar experimental conditions, Das & Prasad[31] evaluated the mosquito control potential of G. affinis in the rice fields in Shahjahanpur district of Uttar Pradesh, India with the stocking rate of 5 fish/sq.m. Control of mosquito breeding in rice fields through fish seemed to be promising. In a study performed by Prasad et al.[32], it was reported that G. affinis survived well in submerged rice fields and provided 87.8% mosquito larval control in Shahajahanpur district, Uttar Pradesh.
Western Rajasthan was once considered an unstable zone for malaria due to the seasonal appearance of the cases but in recent years, through the change in landuse installation of many energy and irrigation-related projects. there is an increased congregation of people from different parts of India[26],[33]. Malaria has become an annual event and is persistent in many districts of western Rajasthan[34].
Thus the use of Gambusia affinis as a biological intervention for vector control is not only cost-effective compared to the use of larvicides but also eliminates the risk of development of insecticide resistance in the larvae which is now an emerging problem due to excessive use of larvicides and is self-sustaining. Therefore, mega irrigation projects must have an interventional component along with installation during their construction so that some alteration if required can be done to avoid stagnation of water. Also, a plan of intervention due to water-storing can be done simultaneously with cost-effective and eco-friendly methods.
In view of India’s commitment to the 2030 elimination goal for malaria, such a sustainable vector reduction strategy coupled with an effective treatment strategy would be very helpful for achieving the elimination goal in time.
AcknowledgementsThe authors are thankful to the Director of the host Institute for allowing to conduct the study. The authors are also thankful to the Narmada Valley Development Authority NVDA for supporting the project funding and to the ICMR-National Institute of Malaria Research (NIMR) and the project staff involved in the study and interventions.
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