Woodbridge A. Foster

Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector Anopheles gambiae (Diptera: Culicidae).

Abstract Although females of most mosquito species are known to use sugar as a necessary source of energy, female Anopheles gambiae Giles sensu stricto are thought to use it facultatively or not at all. However, field evidence of sugar-free living is inconclusive, and the implications for reproductive fitness and vectorial capacity are unknown. To evaluate the role that sugar may play in the ecology of these mosquitoes, mated female An. gambiae in the laboratory were given access to either no food (water only), 10% sucrose, human blood, or human blood + 10% sucrose, and comparisons of daily mortality, fecundity, and biting frequency were made. The effect of sugar availability on vectorial capacity and the intrinsic rate of increase, a measure of fitness, then were determined. Females (pooled and individual) given blood + sugar lived significantly longer than did those on the other diets. Daily fecundity was higher for females given blood alone than for those fed blood + sugar (13 versus 9 eggs per female daily). However, total fecundity and intrinsic rate of increase were not affected by sugar availability. Biting frequency was significantly higher (0.41 versus 0.26 bites per female per day) for females given blood alone. Despite the reduced survivorship, exclusive blood-feeding led to a theoretically higher vectorial capacity for Plasmodium falciparum at 27°C. These data indicate that female An. gambiae could replace sugar with increased blood feeding without suppressing reproductive fitness. Increased blood feeding could, in turn, increase the rate of malaria transmission and may explain the unusual efficiency of this vector.

Anopheles gambiae feeding and survival on honeydew and extra-floral nectar of peridomestic plants

Abstract.  It is widely believed that the malaria vector Anopheles gambiae Giles (Diptera: Culicidae) rarely or never feeds on sugar in nature. If so, the need for supplemental blood‐feeding may be increased and this would help to explain why it is such an efficient malaria vector. Nonetheless, both sexes of this mosquito species readily imbibe and digest sugar solutions, and sugar is a staple of laboratory colonies. In this study, we investigated whether An. gambiae will feed on the extra‐floral nectar of three common peridomestic plants in Africa, and on honeydew of the mealybug Pseudococcus longispinus (Targioni‐Tozetti) (Hemiptera: Homoptera: Pseudococcidae), and how this affects survivorship.

Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya

Abstract.  The propensity of the malaria vector mosquito Anopheles gambiae Giles (Diptera: Culicidae) to ingest sugars from various plants, and subsequent survival rates, were assessed with laboratory‐reared males and females offered eight species of plants commonly cultivated and/or growing wild in western Kenya. In cages (no‐choice bioassay), mosquitoes given the opportunity to feed on castorbean (Ricinus communis L.) had the longest survival times (mean and median survival time of 6.99 ± 0.23 and 5.67 ± 0.17 days, respectively), comparable to mosquitoes given 6% glucose (mean and median survival time of 8.70 ± 0.23 and 6.67 ± 0.33 days, respectively). Survival rates of An. gambiae were low on the other plants, comparable to mosquitoes given only water. Three plants: sweet potato (Ipomoea batatas L.), wild sage (Lantana camara L.) and castorbean provided levels of sugar ingestion by both sexes of An. gambiae detectable using the cold anthrone method, showing a positive correlation between median survival and sugar consumption (Spearman rank correlation coefficient = 0.905, P < 0.0001). Equal numbers of males and females were released in an enclosed semi‐field screenhouse system containing a range of local plants, but no host for blood, and allowed to feed ad libitum: 6.7 ± 0.5% (11/64) of those recaptured were found to contain detectable fructose (all females). Common plants are clearly a viable source of nutrition for adult female An. gambiae, as well as males, and may constitute and important resource for this important malaria vector.

Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae

BackgroundA previous study showed for Anopheles gambiae s.s. a gradation of feeding preference on common plant species growing in a malaria holoendemic area in western Kenya. The present follow-up study determines whether there is a relationship between the mosquitos preferences and its survival and fecundity.MethodsGroups of mosquitoes were separately given ad libitum opportunity to feed on five of the more preferred plant species (Hamelia patens, Parthenium hysterophorus, Ricinus communis, Senna didymobotrya, and Tecoma stans) and one of the less preferred species (Lantana camara). The mosquitoes were monitored daily for survival. Sugar solution (glucose 6%) and water were used as controls. In addition, the fecundity of mosquitoes on each plant after (i) only one blood meal (number of eggs oviposited), and (ii) after three consecutive blood meals (proportion of females ovipositing, number of eggs oviposited and hatchability of eggs), was determined. The composition and concentration of sugar in the fed-on parts of each plant species were determined using gas chromatography. Using SAS statistical package, tests for significant difference of the fitness values between mosquitoes exposed to different plant species were conducted.Results and ConclusionAnopheles gambiae that had fed on four of the five more preferred plant species (T. stans, S. didymobotrya, R. communis and H. patens, but not P. hysterophorus) lived longer and laid more eggs after one blood meal, when compared with An. gambiae that had fed on the least preferred plant species L. camara. When given three consecutive blood-meals, the percentage of females that oviposited, but not the number of eggs laid, was significantly higher for mosquitoes that had previously fed on the four more preferred plant species. Total sugar concentration in the preferred plant parts was significantly correlated with survival and with the proportion of females that laid eggs. This effect was associated mainly with three sugar types, namely glucose, fructose, and gulose. Except for P. hysterophorus, the results suggest that feeding by mosquitoes on preferred plant species under natural conditions results in higher fitness-related benefits, and that the sugar content in preferred plant parts is largely responsible for these effects.

Diel timing and frequency of sugar feeding in the mosquito Anopheles gambiae, depending on sex, gonotrophic state and resource availability

Abstract Little is known about the sugar‐feeding behaviour of equatorial Africa’s principal vector of malaria, Anopheles gambiae Giles (Diptera: Culicidae). It is suspected to feed on plant sugar infrequently, but possibly the timing depends on environmental circumstances, and males may differ markedly from females. These points of uncertainty were clarified in the laboratory, by monitoring both diel and longterm sugar‐feeding activity in both sexes. Males fed on sugar in a nocturnal diel rhythm closely approximating non‐specific flight activity. Female diel sugar‐feeding patterns resembled published rhythms and cycles of host seeking. Males sugar fed nightly at an average frequency of about twice per night, sustained over 17 days. This was substantially higher than the sugar‐feeding frequency of females that were allowed both blood and oviposition sites every night: they averaged about one sugar feed in every 4 nights. These females fed on sugar between gonotrophic cycles, after eggs were mature but before the next bloodmeal. They did not sugar feed during the 2 days after blood feeding, while blood was being digested and the eggs developed. A slight delay in the availability of either the oviposition site or blood led to an increase in female sugar‐feeding frequency: they averaged more than once per night until the delayed resource was made available. These observations support the conclusion that sugar feeding is a normal part of the biology of both sexes of An. gambiae.

Effect of sugar on male Anopheles gambiae mating performance, as modified by temperature, space, and body size

BackgroundAnopheles gambiae plant-sugar feeding was thought to be rare and physiologically optional. Unlike adult females, males have no alternative source of energy and soon die with only water, yet they might be competent to inseminate all females within their brief lifespan. This study was designed to detect sugars effect, if any, on male performance.MethodsMales with and without 20% sucrose were evaluated at two body sizes and two temperatures, 23° and 27°C. Survival was recorded twice daily, and sexual behaviour was recorded each night after adult emergence. Insemination at a 2:1 male:female ratio was examined in three cage sizes, including walk-in mesocosms.ResultsWithout sugar, males of both sizes lived longer at 23° than 27°C, and large males lived longer at each temperature. Survival of large males at low temperature averaged 3.7 days, small males at high temperature, 1.9 days. With sugar, males in all four treatments suffered minimal mortality. With sugar, in small cages, large males at 27°C matured most rapidly. A few erected fibrillae and inseminated females on night 1. On night 2, maximal proportions erected fibrillae and swarmed, and over one-third of females became inseminated. Small sugar-fed males at 23°C matured most slowly but had achieved nearly maximal levels of swarming by night 3. By night 5, small males had inseminated more than half the females, and large males had inseminated nearly all of them. Without sugar, large males progressed similarly during the first two nights. On night 3, however, the proportion erecting fibrillae and swarming declined precipitously at 27°C, and to a lesser degree at 23°C. Cumulative insemination never reached high levels. Small males never achieved high levels of fibrillar erection or swarming and inseminated few females, even at 23°C. In larger cages and under more semi-natural conditions, regardless of body size, without sugar male insemination capacity was virtually nonexistent.ConclusionUnder some conditions, a limited number of sugar-deprived males can survive long enough to inseminate females. However, in nature males that cannot obtain sugar at frequent intervals will not be competitive with those that can, suggesting that male performance is closely tied to plant communities.

Sugar Deprivation Reduces Insemination of Anopheles gambiae (Diptera: Culicidae), Despite Daily Recruitment of Adults, and Predicts Decline in Model Populations

ABSTRACT Our research tests the hypothesis that the inability to sugar-feed reduces the insemination rate in mosquito populations. To test this, we measured the effects of sugar availability on cumulative insemination performance of male Anopheles gambiae Giles s. s. (Diptera: Culicidae) during 10-d periods of continual emergence of equal numbers of both sexes, and we evaluated the implications at the population level with a matrix population model. On each day of each of four replicates, 20 newly emerged mosquitoes of each sex were recruited into the populations within two mesocosms, large walk-in enclosures with simulated natural conditions. Each mesocosm contained a cage to replicate the experiment on a small scale. Scented sucrose was absent or present (control). A human host was available nightly as a bloodmeal source in both mesocosms. Sugar availability and enclosure size significantly influenced female insemination. In the mesocosms, with sugar 49.7% of the females were inseminated, compared with 10.9% of the females without sugar. In the small cages, the insemination rates were 76.0 and 23.5%, respectively. In the mesocosms, cumulative survival of females after 10 d was 51.6% with sugar and 25.6% without sugar. In the cages, female survival was 95 and 73%, respectively. Sensitivity analysis of the population projection matrix shows that both reduced male survival and reduced mating capability due to a lack of sugar contributed to lower insemination rates in females, and in the absence of sugar the insemination rate was lowered to an extent that led to population decline.

Effects of Plant-Community Composition on the Vectorial Capacity and Fitness of the Malaria Mosquito Anopheles gambiae

Dynamics of Anopheles gambiae abundance and malaria transmission potential rely strongly on environmental conditions. Female and male An. gambiae use sugar and are affected by its absence, but how the presence or absence of nectariferous plants affects An. gambiae abundance and vectorial capacity has not been studied. We report on four replicates of a cohort study performed in mesocosms with sugar-poor and sugar-rich plants, in which we measured mosquito survival, biting rates, and fecundity. Survivorship was greater with access to sugar-rich plant species, and mortality patterns were age-dependent. Sugar-poor populations experienced Weibull mortality patterns, and of four populations in the sugar-rich environment, two female and three male subpopulations were better fitted by Gompertz functions. A tendency toward higher biting rates in sugar-poor mesocosms, particularly for young females, was found. Therefore, vectorial capacity was pulled in opposing directions by nectar availability, resulting in highly variable vectorial capacity values.

Analysis and Optimization of a Synthetic Milkweed Floral Attractant for Mosquitoes

A pentane extract of flowers of common milkweed, Asclepias syriaca (Asclepiadaceae), elicited significant orientation from both male and female Culex pipiens in a dual-port flight olfactometer. Analysis of the extract by gas chromatography–mass spectrometry revealed six major constituents in order of relative abundance: benzaldehyde, (E)-β-ocimene, phenylacetaldehyde, benzyl alcohol, nonanal, and (E)-2-nonenal. Although not all were collected from the headspace profile of live flowers, a synthetic blend of these six compounds, when presented to mosquitoes in the same levels and proportions that occur in the extract, elicited a response comparable to the extract. Subtractive behavioral bioassays demonstrated that a three-component blend consisting of benzaldehyde, phenylacetaldehyde, and (E)-2-nonenal was as attractive as the full blend. These findings suggest the potential use of synthetic floral-odor blends for monitoring or control of both male and female disease-vectoring mosquitoes.

Development and assessment of plant-based synthetic odor baits for surveillance and control of malaria vectors.

Background Recent malaria vector control measures have considerably reduced indoor biting mosquito populations. However, reducing the outdoor biting populations remains a challenge because of the unavailability of appropriate lures to achieve this. This study sought to test the efficacy of plant-based synthetic odor baits in trapping outdoor populations of malaria vectors. Methodology and Principal Finding Three plant-based lures ((E)-linalool oxide [LO], (E)-linalool oxide and (E)-β-ocimene [LO + OC], and a six-component blend comprising (E)-linalool oxide, (E)-β-ocimene, hexanal, β-pinene, limonene, and (E)-β-farnesene [Blend C]), were tested alongside an animal/human-based synthetic lure (comprising heptanal, octanal, nonanal, and decanal [Blend F]) and worn socks in a malaria endemic zone in the western part of Kenya. Mosquito Magnet-X (MM-X) and lightless Centre for Disease Control (CDC) light traps were used. Odor-baited traps were compared with traps baited with either solvent alone or solvent + carbon dioxide (controls) for 18 days in a series of randomized incomplete-block designs of days × sites × treatments. The interactive effect of plant and animal/human odor was also tested by combining LO with either Blend F or worn socks. Our results show that irrespective of trap type, traps baited with synthetic plant odors compared favorably to the same traps baited with synthetic animal odors and worn socks in trapping malaria vectors, relative to the controls. Combining LO and worn socks enhanced trap captures of Anopheles species while LO + Blend F recorded reduced trap capture. Carbon dioxide enhanced total trap capture of both plant- and animal/human-derived odors. However, significantly higher proportions of male and engorged female Anopheles gambiae s.l. were caught when the odor treatments did not include carbon dioxide. Conclusion and Significance The results highlight the potential of plant-based odors and specifically linalool oxide, with or without carbon dioxide, for surveillance and mass trapping of malaria vectors.