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The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel

The contribution of aestivating mosquitoes to the persistence of Anopheles gambiae in the Sahel
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  RESEARCH Open Access  The contribution of aestivating mosquitoes to thepersistence of   Anopheles gambiae  in the Sahel Abdoulaye Adamou 1 , Adama Dao 1 , Seydou Timbine 1 , Yaya Kassogué 1 , Alpha Seydou Yaro 1 , Moussa Diallo 1 ,Sékou F Traoré 1 , Diana L Huestis 2 and Tovi Lehmann 2* Abstract Background:  Persistence of African anophelines throughout the long dry season (4-8 months) when no surfacewaters are available remains one of the enduring mysteries of medical entomology. Recent studies demonstratedthat aestivation (summer diapause) is one mechanism that allows the African malaria mosquito,  Anopheles gambiae ,to persist in the Sahel. However, migration from distant localities - where reproduction continues year-round -might also be involved. Methods:  To assess the contribution of aestivating adults to the buildup of populations in the subsequent wetseason, two villages subjected to weekly pyrethrum sprays throughout the dry season were compared with twonearby villages, which were only monitored. If aestivating adults are the main source of the subsequentwet-season population, then the subsequent wet-season density in the treated villages will be lower than in thecontrol villages. Moreover, since virtually only M-form  An. gambiae  are found during the dry season, the reductionshould be specific to the M form, whereas no such difference is predicted for S-form  An. gambiae  or  Anophelesarabiensis . On the other hand, if migrants arriving with the first rain are the main source, no differences betweentreated and control villages are expected across all members of the  An. gambiae  complex. Results:  The wet-season density of the M form in treated villages was 30% lower than that in the control (P < 10 -4 ,permutation test), whereas no significant differences were detected in the S form or  An .  arabiensis . Conclusions:  These results support the hypothesis that the M form persist in the arid Sahel primarily byaestivation, whereas the S form and  An. arabiensis  rely on migration from distant locations. Implications for malariacontrol are discussed. Background  Anopheles gambiae , the principal malaria vector is acomplex of species that occupies diverse habitats in sub-Saharan Africa including the dry Sahel [1-4]. The mechanisms that allow these species to survive the longdry season (4-8 months), when no surface waters areavailable, have been debated for over 70 years [5-12]. One explanation that has been proposed is that adultsextend their survival during the dry season by under-going aestivation (i.e. summer diapause) in (unknown)local shelters [13]. The alternative explanation proposesthat migrants from distant locations, where permanentsurface waters are available, colonize areas vacated by previous populations soon after the rains [12]. A recentstudy demonstrated that aestivation (summer diapause)is one mechanism that allows the M form of   An. gam-biae  to persist in the Sahel [7]. Additionally, that study showed that very small numbers of   An. gambiae  adults,mostly fed and gravid females, can be found indoors(~0.035/house) throughout the dry season in the Sahel,presumably representing the larger hidden population of aestivating adults.However, the authors could not rule out additionalmigrants from distant localities (>20 km), where repro-duction continues year-round. While it is possible thatmigrants contribute more than aestivating adults to thepersistence of populations in the Sahel, records of move-ments of   An. gambiae  beyond 2 km in distance are rare[14,15] and no report exceeds 10 km. Knowledge of the source of the early wet season population in arid and * Correspondence: 2 Laboratory of Malaria and Vector Research, NIAID, NIH. Rockville, MD, USAFull list of author information is available at the end of the article Adamou  et al  .  Malaria Journal   2011,  10 :151 © 2011 Abdoulaye et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (, which permits unrestricted use, distribution, andreproduction in any medium, provided the srcinal work is properly cited.  semi-arid habitats represents a critical gap in our under-standing of this vector ’ s ecology. This knowledge may have important implications for vector and malariacontrol.This study was undertaken to assess the relative con-tribution of aestivating adults versus migrants to thebuildup of Sahelian anopheline populations in the subse-quent wet season. Specific predictions of the aestivationand migration hypotheses were tested. Thus, on the onehand, if the primary source of the mosquitoes that seedthe new wet-season populations consists of locally aesti- vating adults, then reducing the population during thedry season by weekly indoor spray with a short-durationinsecticide such as pyrethrum will reduce their survivaland impact the buildup of the wet season population.On the other hand, if migrants from distant locationsplay the key role, then the reduction of the local popula-tion during the dry season will have a negligible effecton the buildup of the wet-season population. Density during the dry season at this Sahelian area remains very low until 3-6 days after the first rain, when numberssurged over ten-fold [7]. If these mosquitoes representmigrants, they arrive just after the first rain and theimpact of the treatment (pyrethrum effect lasts only 1-2 days after application) on them would be minimal.If migrants arrive before the first rain, they should bedetected by our monitoring. Accordingly, it was pre-dicted that under the aestivation hypothesis, the treat-ment should reduce population density in treated villages as opposed to untreated control villages (Densi-ty  T  <Density  C ). Importantly, this prediction appliesexclusively to the M molecular form of   An. gambiae ,but not to the S form or  Anopheles arabiensis  becausethe latter taxa are not found indoors during the dry sea-son [7] and thus cannot be affected by the treatment.On the other hand, if mosquitoes migrate from outsidethe area to establish the new wet-season population,then this treatment will have little effect on the migrantsand therefore (Density  T  = Density  C ) for all members of the  An. gambiae  complex, including the M form. Methods Four villages (Table 1 and Figure 1) were selected for this study based on the following criteria. Each selected village was required to be located in the Sahel, over3 km away from the nearest village to minimize migra-tion from neighbouring villages, and at least 10 km fromany larval site that remained with water after January toensure that no local mosquito reproduction was possibleduring the treatment period (see below). Only villages of small to medium population size were selected, so allhouses (including kitchens, household storage, chickenhouses, etc.) can be sprayed in a single day. Selected vil-lages were divided into pairs based on proximity to eachother and villages in each pair were randomly assignedto either the treatment or control village group. Weekly treatment of pyrethrum spray in all houses of treated villages started after the desiccation of the last larval sitein a radius of 10 km around each village and continueduntil the first rain. The first treatment was applied onDecember 20, 2009 and the last one on May 23, 2010.In the other two villages (controls), only monthly moni-toring was performed. Monitoring consisted of indoorpyrethrum spray in the same 25 houses in each village,performed on the same day in each treatment-control village pair and on consecutive or nearly-consecutivedays on the other pair. Monitoring of population sizeand species composition was conducted monthly ineach village from September 2009 to mid-May 2010 and Table 1 Village information Village a Coordinates Houses b Pair  c  Near Village d  Near Water  e Babobougou(T)13 45N,704W58 1 7 17Boyila (T) 13 47N,720W198 2 9 17Sanafouka (C) 13 33N,710W188 1 3 22Bagadaji (C) 13 51N,706W195 2 7 11 a  Treated villages (T) and control villages (C). b Number of houses in the village. c Pair number. The distance between treated and control village in each pairwas 25 km. d Distance (km) to the nearest village. e Distance (km) to the nearest body of surface water which holds water afterDecember. BanambaKibanSerimana Sarafouka Thierola BoyilaBabobougou NiareToubakoro Bagadaji FlanibougouKonani-BarraqeKoyo   Kondo7 mi = 11.3 km Figure 1  A schematic map showing locations of the four focalvillages (red large dots) . The nearest village (gray dots) andnearest permanent surface waters (blue dots) to each of the focalvillages are shown as well as the site of a previous study (Thierola),to which several citations were made. Roads (unpaved) are shownin gray and the largest town (Banamba) is marked as a gray square.Additional information is provided in Table 1. Adamou  et al  .  Malaria Journal   2011,  10 :151 2 of 9  approximately every ten days from mid-May until theend of October 2010. The effect of monitoring on mos-quito populations of the control villages was small (andconservative) because it consisted of once-a-monthspray of 25 houses of 188 and 195 houses in total(Table 1) rather than once-a-week spray of all houses aswas done in the treated villages during the treatment.This increased frequency of monitoring should enhancethe resolution of the comparison of the buildup of thewet-season populations in the treated and untreated(control) villages. Collected mosquitoes were identified visually to separate  An. gambiae  s.l from other speciesand later subjected to the genetic identification of thesibling species and molecular forms as previously described [16]. Statistical analysis To detect heterogeneity in species and molecular formcomposition between samples, exact tests were per-formed on contingency tables using Proc Freq in SAS9.2 (SAS Institute, Inc., Cary, NC) [17]. Sequential sam-ples from the same village were pooled only if the sam-ple size of one (or both) was small (N<30, as was thecase during parts of the dry season, e.g., February andMarch) and there was no significant heterogeneity inspecies and/or form composition between them. Globaltests were employed to evaluate significance of multipletests. The sequential Bonferroni procedure [18] wasused to test individual departures from the null hypoth-esis, such as non-homogenous (heterogeneous) speciescomposition in one village during a particular samplingperiod. The binomial test (which estimates the probabil-ity of obtaining the observed number of significant testsat the 0.05 level given the total number of tests) wasused to detect weaker departures across multiple tests.To compare densities in treated and control villagesover the series of sampling time periods after the firstrain, the series of the differences (Treated-Control) werecalculated by subtracting the corresponding values of the same sampling period. A permutation test was usedbecause the values of a time series are serially corre-lated, and the series of differences may have retainedthat effect. Accordingly, density values were randomly assigned to either the treated or control village (strati-fied by village pair) prior to calculating the differencebetween the  “ Treated ”  and  “ Control ”  values for eachtime point. The distribution of mean difference derivedfrom each of the 10,000 pseudo-samples provided thebasis to determine if the observed mean of the series of differences is smaller than random expectations for eachspecies and molecular form (see hypotheses, above).Initially, a global test (across villages comparing treatedand control villages) was used for each of the three tax-ons. If the global test was insignificant (P > 0.05), thedecision was reached and no additional tests were used.However, if the global test was significant (P < 0.05), thesame test was applied to compare the treated and con-trol villages in each village pair for the significant taxon. Results A total of 17,430 An. gambiae s.l. (10,602 females and6,828 males) were collected from the four villages over22 sampling periods using pyrethrum knock-down in25 houses/village. Identification to species and molecularform was performed on 4734  An. gambiae  s.l. (3811females and 853 males) of which 73.0% were M-form  An. gambiae , 15.1% were S form and 8.6% were  An. ara-biensis  (3.2% of the mosquitoes could not be identifieddue to poor preservation of DNA and 0.1% (n = 3) wereM/S hybrids).The species and molecular form composition did not vary between males and females because only three of 49 tests indicated heterogeneity (individual tests: 0.0021 <P < 0.05; Binomial multi-sample test: P < 0.44). None of these tests were significant at the multi-test level, usingthe sequential Bonferroni procedure. Therefore, in all sub-sequent analyses males and females collected at the samesampling period were pooled. Variation in species andmolecular form composition was detected among villageswith eight significant tests (individual tests: 10 -5 < P <0.05) of 16 tests (Binomial multi-sample test: P < 0.001).All significant tests (at the multi-test level using theBonferroni procedure) were clustered in the late wet sea-son: September-October 2009 and from the August toOctober 2010. Overall, the seasonal variation in speciesand molecular form composition (Figure 2) followed thepattern previously reported for this region [7].Density in the four villages was monitored starting inthe late wet season (September 2009). During that per-iod, overall density was high (approx. 30/house, range:14-55; Figure 3) and the species and molecular formcomposition changed rapidly (Figure 2) as previously reported for that region [7]. At that time, overall density in the villages selected for treatment was higher orequal to that of the control villages (Figure 3). However, vector composition and density varied among villagesand even between paired villages (Figures 3 and 4) simi- lar to previous reports, e.g. [4].The last larval site dried up in December, almost twomonths after the last rain (October), when the averagedensity dropped to 1.1/house (range 0.7-1.5; Figure 3)and treatment started (in treated villages). Over the nextthree months, the average density of   An. gambiae  s.l.continued to drop reaching 0.05-0.07/house (range:0-0.24) by February and March. This low density lasteduntil May, except during 3-5 days in April, when mos-quito density surged (April 8-10) across the region,which happened to coincide with the monitoring date Adamou  et al  .  Malaria Journal   2011,  10 :151 3 of 9  (Figures 3 and 4). Remarkably, the density returned to its typical low dry-season density from April 11 th (InPreparation). Despite the absence of surface water forlarval sites and regardless of weekly insecticide treat-ments, mosquitoes were present (albeit at low densities)in all villages throughout the dry season. During the dry season (Dec-May), the M form represented >95% of theindividuals (>99% from January-May, Figure 2).The first rain (31 mm) fell on May 29, 2010, fillingempty larval sites with enough water to last over 10 d.The last weekly pyrethrum spray was performed on May 19 (Babobougou) and on May 23 (Boyila). Three daysafter the first rain (before reproduction could increaseadult population sizes), average density increased 12.9fold, from an average of 0.055/house (range: 0-0.12) ear-lier in May to 0.71/house (range: 0.4-1.32). The mos-quito density continued to increase until October,however, the average rate of increase over ~10 d inter- vals during this period was 1.73 (range: 0.8-5.4). DuringMay and June, composition remained dominated by theM form (>97%), although a single  An. arabiensis  wasfound in mid-June and two S-form mosquitoes werefound in mid-May, before the first rain (Figure 2).The overall effect of the treatment was measured asthe difference between treated and control villages overtime, during the entire wet season (June to October2010, see Methods). Population density in treated vil-lages was 30% lower than in control villages (Table 2) aspredicted based on the aestivation hypothesis. A signifi-cant difference was detected exclusively in the M mole-cular form (Table 2, Figures 3 and 4). The effect on the M molecular form was not only detected in the globaltest (across village pairs), but also in each village pairseparately (Table 2). Discussion The contribution of aestivating mosquitoes to the per-sistence of anopheline malaria vectors in Sahelian vil-lages was evaluated in this study. If aestivatingmosquitoes that periodically blood feed (albeit less fre-quently) constitute the main source of the populationafter the 6-7 months long dry season [7,13,19] then 02040608010015SEP09 15NOV0915DEC09 02FEB10 15APR10 25MAY10 15JUN10 10JUL10 05AUG1005SEP10 25SEP10 15OCT1025OCT10BaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSanaBaboBagaBoyiSana          An. arabiensis An. gambiae M An. gambiae S Figure 2  Species and molecular form composition in the four villages over time, based on 4,584 mosquitoes which were successfullygenotyped to species and molecular form (see text for details) . Note that the time intervals are variable. Pooling of adjacent dates wascarried out if samples were small and only if minimal differences in composition were found. Except for the period marked  ‘ 2Feb10 ’  thatcovered samples from January to March, other pooled samples represent periods shorter than three weeks between June and October 2010.Numbers above bars show cases where sample size per village/period were smaller than 20. Significant heterogeneity among villages (P < 0.05,after the sequential Bonferroni procedure) is denoted by stars. Adamou  et al  .  Malaria Journal   2011,  10 :151 4 of 9  051 01 52 02 53 03 54 00 1 S E P 2 0 0 9 3 1 O C T2 0 0 9 3 0 D E C 2 0 0 9 2 8 FE B 2 0 1 0 2 9 AP R 2 0 1 0 2 8 JU N 2 0 1 0 2 7 AU G 2 0 1 0 2 6 O C T2 0 1 0   0481 21 62 02 42 83 20 1 S E P 2 0 0 9 3 1 O C T2 0 0 9 3 0 D E C 2 0 0 9 2 8 FE B 2 0 1 0 2 9 AP R 2 0 1 0 2 8 JU N 2 0 1 0 2 7 AU G 2 0 1 0 2 6 O C T2 0 1 0   02468101201SEP2009 31OCT2009 30DEC2009 28FEB2010 29APR2010 28JUN2010 27AUG2010 26OCT2010   0123456701SEP2009 31OCT2009 30DEC2009 28FEB2010 29APR2010 28JUN 2010 27AUG2010 26OCT2010  A. gambiae s.l.M form A. arabiensis.S form   .l.      D    e    n    s     i    t    y     (    m    o    s    q    u     i    t    o    e    s     /     h    o    u    s    e     ) Figure 3  Overall density (number of mosquitoes/house) in treated (red) and control (black) villages over time, measured bypyrethrum spray collections in 25 houses/village every month until the first rain and every 10 d thereafter . The density of themolecular forms of   An. gambiae  and of   An. arabiensis  was estimated by multiplying the density of   An. gambiae  s.l. (upper panel) by thecorresponding fraction representing the relevant taxon in the corresponding village and time period. The yellow shading denotes the period of treatment in treated villages (from the desiccation of the last larval site 10 km around the village and until the first rain). Adamou  et al  .  Malaria Journal   2011,  10 :151 5 of 9
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