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Chemical Cues for Malaria Vectors Oviposition Site Selection: Challenges and Opportunities  [PDF]
Yousif E. Himeidan,Emmanuel A. Temu,El Amin El Rayah,Stephen Munga,Eliningaya J. Kweka
Journal of Insects , 2013, DOI: 10.1155/2013/685182
Abstract: The attractiveness of oviposition site for malaria vector mosquitoes is dependent upon a number of physical and chemical factors. Many aspects of mosquito behavior, including host location and oviposition, are mediated by volatile semiochemicals. It is anticipated that selection of oviposition site by semio-chemicals in the form of attractants or stimulants can be used in oviposition traps to monitor or possibly in combination with insecticides to control gravid mosquito populations for mass trapping. So far, volatile compounds identified as oviposition attractants for mosquitoes include phenol, 4-methyl phenol, 4-ethyl phenol, indole, skatole, and p-cresol from hay infusions; 3-carene, α-terpinene, α-copaene, α-cedrene, and d-cadinene released by copepods; alcohol and terpenoids including p-cresol from plants; ethyl acetate and hydrocarbon substances, probably released by filamentous algae; 3-methyl-1-butanol identified from bacteria. Research priorities should be directed at identifying more oviposition attractants to determine the properties of these semio-chemicals for possible use in designing control tools. This would aim at luring females to lethal traps or stimulants to increase their exposure to insecticide-impregnated substrates. 1. Background Malaria is one of the most significant and debilitating insect-transmitted human diseases and has infected humans for over thousand years and may have been a human pathogen for the entire history of mankind [1]. Today, malaria causes about 225 million cases of fever and approximately 600,000 deaths annually more specifically in children under age of 5 years [2]. This represents at least one death (child) every 39 seconds and 85–90% of the deaths occur in sub-Saharan Africa [2]. Mosquitoes spend the first part of their lifecycle in aquatic habitats [3]. The choice of an appropriate oviposition sites has significant impact on the fitness of progeny, distribution of larvae, population dynamics, and the overall maternal reproductive fitness and success [4, 5]. Oviposition process requires complex integration of physical and chemical cues by gravid mosquitoes. Long-range cues, probably involving vision, allow mosquitoes to identify different habitats and oviposition site characteristics. As mosquitoes approach an oviposition site other cues such as phenol, 4-methyl phenol, 4-ethyl phenol, indole, skatole, and p-cresol from hay infusions; 3-carene, α-terpinene, α-copaene, α-cedrene, and d-cadinene become important. Once oviposition site is identified, short-range cues become increasingly important. Short-range
Response of Anopheles gambiae s.l. (Diptera: Culicidae) to larval habitat age in western Kenya highlands
Munga Stephen,Vulule John,Kweka Eliningaya J
Parasites & Vectors , 2013, DOI: 10.1186/1756-3305-6-13
Abstract: Background Larval control is of paramount importance in the reduction of vector populations. Previous observations have suggested that, larvae of Anopheles gambiae s.l occur more often in small temporary habitats while other studies showed that long-lasting stable habitats are more productive than unstable habitats. In addition, the physical and biological conditions and stability of larval habitats can change rapidly in natural conditions. Therefore, we examined the effect of larval habitat age on productivity, larval survival and oviposition preference of Anopheles gambiae. Methods We sampled the three different habitat ages (10, 20 and 30 days) on a daily basis for a period of six months to determine mosquito larval abundance. In addition, we tested the effect of age of water (habitat age) on the oviposition choice preference of An. gambiae, larval development time and survivorship, and wing lengths of emerging adults. Additionally, chlorophyll a and abundance of mosquito larval predators in these habitats were monitored. Results Anopheles gambiae s.l. larvae were significantly more abundant (P=0.0002) in habitats that were cleared every 10 days compared to the other habitats. In particular, there were 1.7 times more larvae in this habitat age compared to the ones that were cleared every 30 days. There were significantly (P<0.001) more mosquito larval predators in the ‘30 day’ habitats compared to the other habitats. Oviposition experiments revealed that significantly more eggs (P<0.05) were laid in fresh water and water that was 5 days old compared to water that was 10 and 15 days old. However, pupation rate, development times and wing lengths of male and female An. gambiae in the different habitat ages was statistically insignificant (P>0.05). Conclusion The current study confirmed that age of the habitat significantly influences the productivity of malaria vectors in western Kenya highlands. Given that malaria vectors were found in all habitats with varying ages of water, simple environmental methods of maintaining the drainage ditches in the valley bottoms can help reduce larval abundance of malaria vectors. Such inexpensive methods of controlling mosquito breeding could be promoted to supplement other vector control methods, especially in areas where scarce resources are available for intensive mosquito control.
The Importance of Drains for the Larval Development of Lymphatic Filariasis and Malaria Vectors in Dar es Salaam, United Republic of Tanzania  [PDF]
Marcia C. Castro ,Shogo Kanamori,Khadija Kannady,Sigsbert Mkude,Gerry F. Killeen,Ulrike Fillinger
PLOS Neglected Tropical Diseases , 2010, DOI: 10.1371/journal.pntd.0000693
Abstract: Background Dar es Salaam has an extensive drain network, mostly with inadequate water flow, blocked by waste, causing flooding after rainfall. The presence of Anopheles and Culex larvae is common, which is likely to impact the transmission of lymphatic filariasis and malaria by the resulting adult mosquito populations. However, the importance of drains as larval habitats remains unknown. Methodology Data on mosquito larval habitats routinely collected by the Urban Malaria Control Program (UMCP) and a special drain survey conducted in 2006 were used to obtain a typology of habitats. Focusing on drains, logistic regression was used to evaluate potential factors impacting the presence of mosquito larvae. Spatial variation in the proportion of habitats that contained larvae was assessed through the local Moran's I indicator of spatial association. Principal Findings More than 70% of larval habitats in Dar es Salaam were human-made. Aquatic habitats associated with agriculture had the highest proportion of Anopheles larvae presence and the second highest of Culex larvae presence. However, the majority of aquatic habitats were drains (42%), and therefore, 43% (1,364/3,149) of all culicine and 33% (320/976) of all anopheline positive habitats were drains. Compared with drains where water was flowing at normal velocity, the odds of finding Anopheles and Culex larvae were 8.8 and 6.3 (p<0.001) times larger, respectively, in drains with stagnant water. There was a positive association between vegetation and the presence of mosquito larvae (p<0.001). The proportion of habitats with mosquito larvae was spatially correlated. Conclusion Restoring and maintaining drains in Dar es Salaam has the potential to eliminate more than 40% of all potential mosquito larval habitats that are currently treated with larvicides by the UMCP. The importance of human-made larval habitats for both lymphatic filariasis and malaria vectors underscores the need for a synergy between on-going control efforts of those diseases.
Productivity of Malaria Vectors from Different Habitat Types in the Western Kenya Highlands  [PDF]
Bryson A. Ndenga,Jemimah A. Simbauni,Jenard P. Mbugi,Andrew K. Githeko,Ulrike Fillinger
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0019473
Abstract: Mosquito Larval Source Management (LSM) could be a valuable additional tool for integrated malaria vector control especially in areas with focal transmission like the highlands of western Kenya if it were not for the need to target all potential habitats at frequent intervals. The ability to determine the productivity of malaria vectors from identified habitats might be used to target LSM only at productive ones.
Community-based surveillance of malaria vector larval habitats: a baseline study in urban Dar es Salaam, Tanzania
Michael J Vanek, Bryson Shoo, Deo Mtasiwa, Michael Kiama, Steven W Lindsay, Ulrike Fillinger, Khadija Kannady, Marcel Tanner, Gerry F Killeen
BMC Public Health , 2006, DOI: 10.1186/1471-2458-6-154
Abstract: The Urban Malaria Control Programme of Dar es Salaam recruited and provided preliminary training to teams of Community-Owned Resource Persons (CORPs) who performed weekly surveys of mosquito breeding sites. Two trained mosquito biologists accompanied each of these teams for one week and evaluated the sensitivity of this system for detecting potential Anopheles habitats.Overall, 42.4% of 986 habitats surveyed by an inspection team had previously been identified by CORPs. Agricultural habitats were detected less often than other habitats (30.8% detected, Odds Ratio [95%CI] = 0.46 [0.29–0.73], P = 0.001). Non-agricultural artificial habitats were less suitable than other habitats (29.3% occupancy, OR = 0.69 [0.46–1.03], P = 0.066) but still constituted 45% (169/289) of occupied habitats because of their abundance (51 % of all habitats).The levels of coverage achieved by modestly trained and supported CORPs at the start of the Dar es Salaam UMCP were insufficient to enable effective suppression of malaria transmission through larval control. Further operational research is required to develop surveillance systems that are practical, affordable, effective and acceptable so that community-based integrated vector management can be implemented in cities across Africa.With the prospect of more than half the African population living in urban areas by the year 2030, it is anticipated that the challenge and opportunity for tackling malaria burden in urban areas will also grow [1-3]. Compared to rural settings, malaria in urban Africa is generally characterized by lower intensities and more focal distribution of transmission, resulting in weaker immunity in the afflicted population and distribution of disease burden across older age groups [2,3]. Compared to rural settings, urban areas usually offer more malaria control options because relatively good transport, communication, educational and health infrastructure is available to large populations in small geographic areas. Thr
Field assessments in western Kenya link malaria vectors to environmentally disturbed habitats during the dry season
John C Carlson, Brian D Byrd, Francois X Omlin
BMC Public Health , 2004, DOI: 10.1186/1471-2458-4-33
Abstract: Investigations were conducted in Kisii District during the dry season. Aquatic habitats in were surveyed for presence of malaria vectors. Brick-making pits were further investigated for co-associations of larval densities with emergent vegetation, habitat age, and predator diversity. Indoor spray catches were completed in houses near aquatic habitats. Participatory rural appraisals (PRAs) were conducted with 147 community members.The most abundant habitat type containing Anopheles larvae was brick-making pits. Vegetation and habitat age were positively associated with predator diversity, and negatively associated with mosquito density. Indoor spray catches found that houses close to brick-making sites had malaria vectors, whereas those next to swamps did not. PRAs revealed that brick-making has grown rapidly in highland swamps due to a variety of socioeconomic pressures in the region.Brick-making, an important economic activity, also generates dry season habitats for malaria vectors in western Kenya. Specifically, functional brick making pits contain less that 50% as many predator taxa and greater than 50% more mosquito larvae when compared with nearby abandoned brick making pits. Further evaluations of these disturbed, man-made habitats in the wet season may provide information important for malaria surveillance and control.The World Health Organization estimates that 300 to 500 million people are diagnosed with malaria annually, causing 1.1 to 2.7 million deaths. Approximately 1 million of these deaths are among children in sub-Saharan Africa, where 90% of all malaria cases occur [1]. During the 1950's and 1960's, a coordinated world-wide effort succeeded in eliminating malaria transmission within countries with temperate climates, and dramatically reduced malaria transmission in many other countries. Since the collapse of this campaign, malaria has since resurged, surpassing pre-campaign infection rates in many places, and entering previously unaffected locations
Laboratory tests of oviposition by the African malaria mosquito, Anopheles gambiae, on dark soil as influenced by presence or absence of vegetation
Juan Huang, Edward D Walker, Philip E Otienoburu, Fred Amimo, John Vulule, James R Miller
Malaria Journal , 2006, DOI: 10.1186/1475-2875-5-88
Abstract: To test whether presence and height of grasses influenced oviposition, wild-caught gravid An. gambiae s. l. were offered paired choices between wet, bare soil and wet soil populated with mixed grasses or grasses of differing height. No-choice tests were also conducted by giving females either grassy soil or bare soil.In choice tests, females laid four times more eggs on bare, wet soil than soil populated with grasses. However in no-choice tests, egg output was not significantly different whether grasses were present or not. Females laid significantly more eggs on soil populated with short grass than with medium, or tall grass.This work shows An. gambiae s. l. has the capacity to oviposit into grassy aquatic habitats when typical puddles over bare soil are unavailable. This knowledge will need to be considered in the design and implementation of programmes aimed at reducing malaria transmission by suppression of An. gambiae s. l. immatures.Physical and chemical cues influence acceptance of ovipositional sites by mosquitoes [1-3]. Darkness and wetness are critical positive cues for Anopheles gambiae oviposition, while visual contrast strongly influences finding of prospective ovipositional sites [4,5]. Odours are not required for copious oviposition, however, they may increase egg output in some cases [6] and decrease it in others [7].Physical objects like vegetation can influence oviposition on soil or water substrates [8-10]. Rice plants or glass rods inserted into seepage water reduced Anopheles culicifacies oviposition [8]. However, oviposition by Anopheles hermsi increased in accordance with the density of aquatic macrophytes (Myriophylluym aquaticum) up to 1,000 stems m-2 [10]. In the field, Anopheles funestus breeds mainly in marshes and swamps that contain tall grasses and other plants [11]. An. gambiae is generally thought to utilize puddles over bare soil as its prime larval habitat [12-15] and to avoid standing water populated with vegetation. However, Muir
Anopheline Larval Habitats Seasonality and Species Distribution: A Prerequisite for Effective Targeted Larval Habitats Control Programmes  [PDF]
Eliningaya J. Kweka, Guofa Zhou, Stephen Munga, Ming-Chieh Lee, Harrysone E. Atieli, Mramba Nyindo, Andrew K. Githeko, Guiyun Yan
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0052084
Abstract: Background Larval control is of paramount importance in the reduction of malaria vector abundance and subsequent disease transmission reduction. Understanding larval habitat succession and its ecology in different land use managements and cropping systems can give an insight for effective larval source management practices. This study investigated larval habitat succession and ecological parameters which influence larval abundance in malaria epidemic prone areas of western Kenya. Methods and Findings A total of 51 aquatic habitats positive for anopheline larvae were surveyed and visited once a week for a period of 85 weeks in succession. Habitats were selected and identified. Mosquito larval species, physico-chemical parameters, habitat size, grass cover, crop cycle and distance to nearest house were recorded. Polymerase chain reaction revealed that An. gambiae s.l was the most dominant vector species comprised of An.gambiae s.s (77.60%) and An.arabiensis (18.34%), the remaining 4.06% had no amplification by polymerase chain reaction. Physico-chemical parameters and habitat size significantly influenced abundance of An. gambiae s.s (P = 0.024) and An. arabiensis (P = 0.002) larvae. Further, larval species abundance was influenced by crop cycle (P≤0.001), grass cover (P≤0.001), while distance to nearest houses significantly influenced the abundance of mosquito species larvae (r = 0.920;P≤0.001). The number of predator species influenced mosquito larval abundance in different habitat types. Crop weeding significantly influenced with the abundance of An.gambiae s.l (P≤0.001) when preceded with fertilizer application. Significantly higher anopheline larval abundance was recorded in habitats in pasture compared to farmland (P = 0.002). When habitat stability and habitat types were considered, hoof print were the most productive followed by disused goldmines. Conclusion These findings suggest that implementation of effective larval control programme should be targeted with larval habitats succession information when larval habitats are fewer and manageable. Crop cycles and distance from habitats to household should be considered as effective information in planning larval control.
Diet and density dependent competition affect larval performance and oviposition site selection in the mosquito species Aedes albopictus (Diptera: Culicidae)
Yoshioka Miho,Couret Jannelle,Kim Frances,McMillan Joseph
Parasites & Vectors , 2012, DOI: 10.1186/1756-3305-5-225
Abstract: Background Oviposition-site choice is an essential component of the life history of all mosquito species. According to the oviposition-preference offspring-performance (P-P) hypothesis, if optimizing offspring performance and fitness ensures high overall reproductive fitness for a given species, the female should accurately assess details of the heterogeneous environment and lay her eggs preferentially in sites with conditions more suitable to offspring. Methods We empirically tested the P-P hypothesis using the mosquito species Aedes albopictus by artificially manipulating two habitat conditions: diet (measured as mg of food added to a container) and conspecific density (CD; number of pre-existing larvae of the same species). Immature development (larval mortality, development time to pupation and time to emergence) and fitness (measured as wing length) were monitored from first instar through adult emergence using a factorial experimental design over two ascending gradients of diet (2.0, 3.6, 7.2 and 20 mg food/300 ml water) and CD (0, 20, 40 and 80 larvae/300 ml water). Treatments that exerted the most contrasting values of larval performance were recreated in a second experiment consisting of single-female oviposition site selection assay. Results Development time decreased as food concentration increased, except from 7.2 mg to 20.0 mg (Two-Way CR ANOVA Post-Hoc test, P > 0.1). Development time decreased also as conspecific density increased from zero to 80 larvae (Two-Way CR ANOVA Post-Hoc test, P < 0.5). Combined, these results support the role of density-dependent competition for resources as a limiting factor for mosquito larval performance. Oviposition assays indicated that female mosquitoes select for larval habitats with conspecifics and that larval density was more important than diet in driving selection for oviposition sites. Conclusions This study supports predictions of the P-P hypothesis and provides a mechanistic understanding of the underlying factors driving mosquito oviposition site selection.
Egg hatching, larval movement and larval survival of the malaria vector Anopheles gambiae in desiccating habitats
Constantianus Koenraadt, Krijn P Paaijmans, Andrew K Githeko, Bart GJ Knols, Willem Takken
Malaria Journal , 2003, DOI: 10.1186/1475-2875-2-20
Abstract: The effects of drying conditions were simulated by creating desiccated habitats, which consisted of trays filled with damp soil. Experiments were performed in these trays to (i) test the ability of An. gambiae sensu stricto eggs to hatch on damp soil and for larvae to reach an artificial breeding site at different distances of the site of hatching and (ii) to record survival of the four larval stages of An. gambiae s.s. when placed on damp soil.Eggs of An. gambiae s.s. hatched on damp soil and emerging larvae were capable of covering a distance of up to 10 cm to reach surface water enabling further development. However, proportions of larvae reaching the site decreased rapidly with increasing distance. First, second and third-instar larvae survived on damp soil for an estimated period of 64, 65 and 69 hrs, respectively. Fourth-instar larvae survived significantly longer and we estimated that the maximum survival time was 113 hrs.Short-term survival of aquatic stages of An. gambiae on wet soil may be important and adaptive when considering the transient nature of breeding sites of this species in sub-Saharan Africa. In addition, the results suggest that, for larval vector control methods to be effective, habitats should remain drained for at least 5 days to kill all larvae (e.g. in rice fields) and habitats that recently dried up should be treated as well, if larvicidal agents are applied.Soon after the start of the rains, populations of the malaria vector Anopheles gambiae sensu lato increase explosively in sub-Saharan Africa. The immature stages of this vector can then be found in numerous transient habitats created by the rains, such as hoof prints, car tracks, borrow pits and ditches [1]. The relationship between rainfall on the one hand and mosquito population dynamics and malaria risk on the other is well established and has been modelled accordingly [2-4]. In contrast, the effects of a period of drought on mosquito survival remain less clear.Previous studies h
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