Chem. Senses 25: 323-330,
2000
© Oxford University Press 2000
Contribution of Fatty Acids to Olfactory Host Finding of Female Aedes aegypti
Institute for Zoology, University of Regensburg, Regensburg, Germany
Correspondence to be sent to: Oliver J. Bosch, Institut für Zoologie, Universität Regensburg, Universitätsstraße 31, D-93040 Regensburg, Germany. e-mail: oliver.bosch{at}biologie.uni-regensburg.de
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Abstract |
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Single carbon to 18 carbon n-aliphatic carboxylic acids were tested for their attractive effects on female Aedes aegypti in a Y-tube olfactometer. Each acid was tested over a wide range of concentrations together with L-(+)-lactic acid, the indispensable synergist for other attractive components emitted from human hosts. The attractiveness of lactic acid was significantly augmented when combined with fatty acids of chain length C1–C3, C5–C8 and C13–C18, respectively. The addition of the C9 and C11 acids reduced the attractive effect of lactic acid. According to experiments showing a further increase of attractiveness by adding a second fatty acid, we suggest two groups of attractive carboxylic acids: C1–C3 and C5–C8. The addition of a fatty acid from one group to a mixture of lactic acid and an acid from the other group augmented the attraction to the mixture. Together with ammonia, a previously demonstrated attractant for Aedes aegypti, lactic acid plus two fatty acids from the different groups formed the hitherto most attractive, artificially composed blend. Two of the carboxylic acids which were found to be attractive together with lactic acid were also tested alone and in combination with CO2, the major attractant in human breath. In both cases no attractive effect of the carboxylic acids could be observed.
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionErratumReferences |
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For host finding and selection, female mosquitoes use odours of their prey (Bowen, 1991
; Takken, 1991, 1996; Davis and Bowen, 1994; Davis, 1996). One important kairomone is CO2, a major component of breath that has been shown to activate and to attract a number of mosquito species (Gillies, 1980; Takken, 1991; Eiras and Jepson, 1994; Geier et al., 1999a). Another is L-(+)-lactic acid, a component present in human breath as well as on human skin (Acree et al., 1968; Smith et al., 1970; Eiras and Jepson, 1991). This compound is only slightly effective by itself, but acts synergistically with CO2 and other components from human skin, at least for the yellow fever mosquito Aedes aegypti (Geier et al., 1996). Interestingly, the latter components were found to be attractive only in combination with lactic acid. This might be one reason for the not always conclusive and in some case even contradictory data reported earlier on the attractive effects of single odorants [reviewed in (Hocking, 1971; Takken, 1991)]. In contrast to single compounds, odour mixtures such as human sweat, skin residues, breath and even extracts from Limburger cheese were found to be highly attractive to mosquitoes of different species (Hocking, 1971; Takken, 1991; Knols and De Jong, 1996; Knols et al., 1997). This also indicates that an odour blend rather than a single compound represents the attractive principle in the host odour for mosquitoes. Recently, ammonia, which is present on human skin as well as in breath, was identified as an attractant for A. aegypti (Geier et al., 1999b) which also increases the attractive effect of a lactic acid stimulus alone. The combination of the two compounds, however, did not attract as many A. aegypti as did an extract from human skin residues (Geier et al., 1999b). Therefore, additional components of the human body odour must play a role. Promising candidates are the fatty acids which are present in significant amounts on human skin (Stoddart, 1990). Electrophysiological studies have shown that grooved peg sensilla on the antennae of yellow fever mosquitoes house olfactory receptor cells which respond to fatty acids (Lacher, 1967; Pappenberger et al., 1996). Recently, Knols et al. showed that a mixture of 12 aliphatic fatty acids, identified in the head space of Limburger cheese, were attractive for Anopheles gambiae (Knols et al., 1997). Roessler (Roessler, 1961) obtained a weak attraction of A. aegypti to a blend of several aliphatic and amino acids, and Carlson et al. (Carlson et al., 1973) reported C2–C5 carboxylic acids to be attractive for this species when presented together with CO2. But so far, no behavioural tests have been done with single fatty acids in combination with lactic acid as the synergist. Moreover, no attempt has been made to create a synthetic blend of host odours by adding attractive volatiles step by step, in order to understand the role of each single substance. All these findings led us to undertake a broader screening for attractants among fatty acids, keeping in mind the role of lactic acid as an essential synergist. In a modified Y-tube olfactometer we tested first the responses of A. aegypti to C1–C18 aliphatic acids in combination with lactic acid. The effective fatty acids were then tested alone as well as in combination with CO2, ammonia and the other effective fatty acids. |
Materials and methods |
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Animals
Ten- to 40-day-old female A. aegypti from cultures of the Centre for Plant Research (Pflanzenschutzzentrum) at Bayer AG in Monheim (Germany) were used in experiments. The larvae were reared under standard conditions. About 300–500 adults were kept in containers (50 x 40 x 25 cm) at 26–28°C, 60–70% relative humidity and a light–dark regime of 12:12 h. The insects had access to a 10% glucose solution on filter paper.
Olfactometer
The olfactometer consisted of a long Plexiglas® tube with an exchangeable release chamber at the downwind end. The tube was attached to a rectangular box from which two arms of the Y-olfactometer leave the opposite side (Figure 1). Each arm was connected to a PVC® tube (stimulus chamber) at the upwind end into which the stimuli were injected. A constant airstream of 80 l/min from the laboratory’s pressurised air system was purified with activated charcoal, then heated and humidified before being passed through the olfactometer. For more details of this set-up see (Geier, 1995; Geier et al., 1999b). The temperature in the olfactometer was 28 ± 1°C, relative humidity 70 ± 5%, and wind speed 0.2 m/s in both test and control chambers and 0.4 m/s in the long tube. The olfactometer was placed on a white table and covered on both sides with white 20 cm high cardboard shield. Two 40 W light bulbs provided overhead illumination.
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Application of the odour stimuli
Skin odour was produced using an ethanolic extract of human skin residues. After taking 5 µl of the extract into a glass pipette, it was heated to 60°C and the odour was blown out by air at a flow rate of 1600 ml/min [for details see (Geier and Boeckh, 1999; Geier, 1995)]. Pure CO2 (AGA, Hamburg, Germany) at a flow rate of 1600 ml/min was mixed with olfactometer air to a final concentration of 4% CO2 in the test chamber. The other stimuli were delivered as described elsewhere (Ough and Stone, 1961). Therefore, charcoal-filtered compressed air at flow rates between 0.03 and 300 ml/min passed through a 250 ml Erlenmeyer flask over the surface of a solution of the test substance at room temperature. Flow meters (Rota GmbH, Germany, for flow rates of at least 3 ml/min) or a precision tubing pump (Masterflex, Novodirect GmbH, Kehl/Rhein, Germany, for flow rates of <3 ml/min) were used to control the air flow. To cover a wide range of concentrations, two different dilutions (5 and 500 µl in 50 ml of deionized water) of C1–C9 fatty acids were tested at flow rates of 3, 30 and 300 ml/min, respectively. The C10–C18 fatty acids were melted and 2 ml of the pure substance was distributed over the bottom of the Erlenmeyer flask over which air swept at flow rates of 0.03, 0.3, 3, 30 and 300 ml/min. L-(+)-Lactic acid was tested in an amount of 3 µg/min [20 ml of pure lactic acid, flow rate 15 ml/min; see (Geier et al., 1999a)] and ammonia at 5 µg/min [50 ml of 0.13 mol/l ammonia in distilled water, flow rate 3 ml/min; see (Geier et al., 1999b)].
Chemicals were purchased from Merck (Darmstadt, Germany), Sigma-Aldrich (Deisenhofen, Germany), Riedel-de Haën (Seelze, Germany) or Roth (Karlsruhe, Germany). Except for nonanoic acid (97%), tridecanoic acid (98%) and heptadecanoic acid (95%) they were >99% pure. Air purified by a charcoal filter and passed through an Erlenmeyer flask filled with deionized water was used as a control stimulus.
Odour distribution
To check the spatial distribution of odours in the olfactometer, titanium tetrachloride smoke was used to visualize the distribution of odours. In the arms of the olfactometer, smoke was found to be distributed as in the homogeneous plumes reported elsewhere (Geier et al., 1999a). More turbulent odour eddies, i.e. odour clouds and filaments, appeared in the rectangular Plexiglas® chamber into which the two airstreams flew.
Bioassay
Groups of 18–22 female mosquitoes were used for the tests. Using the odour of the experimenter’s hand the animals were lured out of the container into the release chamber, which was then attached to the downwind end of the olfactometer. Before stimulation, the mosquitoes were given 20 min to acclimate. At stimulus onset, the release chamber was opened and the mosquitoes were allowed to enter the olfactometer. After 30 s of stimulation, the screen doors of the release-, control- and test chambers were closed and the distribution of the animals in the olfactometer was measured. After the experiment the mosquitoes were lured back into the release chamber by reversing the airflow in the olfactometer and using the hand as a natural attractant. A given group of animals was tested up to 10 times with an interval of at least 20 min between subsequent tests. In order to avoid possible side effects such as learning or habituation, every stimulus was tested only once in each group of mosquitoes. Furthermore, the test and control chambers alternated in each experiment.
The different concentrations of a given fatty acid were tested within one series of tests. Each stimulus combination and the control stimulus was tested with at least eight different groups of mosquitoes, each exposed to every combination in a random order. Between the tests, a constant flow of fresh air flushed the olfactometer. The experiments ran from 8:00 a.m. to 6:00 p.m.
Evaluation
In each test, three different types of responses were analysed. (i) The percentage of mosquitoes found outside of the release chamber after 30 s was taken as a measure of activation, which included taking off and short upwind progress. (ii) The percentage of mosquitoes trapped in the test chamber was a measure for attraction to the treatment. (iii) The percentage of mosquitoes in the control chamber measured the response to pure air. The values were averaged from at least eight experiments with different groups of individuals. Since the data are percentage values, angular transformation was made for further statistical analysis (Sachs, 1997). The transformed means were analysed independently by a one-way ANOVA using the Duncan test post hoc for comparison of treatments. All calculations and statistics were performed with the statistics program SPSS 8.0 for Windows.
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Results |
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Responses to clean air
Control tests with clean air stimulation were done at random intervals throughout the experiments. All control studies (n = 400 repetitions) were pooled based on the similarity of their evoked responses. The activation of the mosquitoes was 32.1 ± 0.7% (mean ± SE), the attraction to the test chamber was 1.4 ± 0.1% and that to the control chamber was 0.8 ± 0.1%. These low levels of attraction to the pure olfactometer air indicate no contamination effects during the experiments.
Responses to single fatty acids in combination with lactic acid
Different doses of a given fatty acid were tested in combination with lactic acid at a dose of 3 µg/min (Figures 2 and 3). The lactic acid dose was in the range of evaporation rates from human hands (Smith et al., 1970) and was also tested alone as a standard in each series of tests. These tests were performed to see whether the attractive effect of lactic acid could be increased by adding a single fatty acid. In all tests, the attractiveness of lactic acid varied between 15 and 25%, and the attractiveness was significantly increased by addition of certain concentrations of C1–C3, C5–C8 and C13–C18 saturated fatty acids. No increase was observed with butyric acid as well as the C9–C12 fatty acids over a range of various concentrations. In contrast, when nonanoic acid was added to lactic acid from a solution of 1:10 000 and a flow rate of 300 ml/min or from a 1:100 dilution and a flow rate of 30 ml/min a slight decrease of attractiveness was recorded compared with the effect of lactic acid alone. The same was observed for undecanoic acid at a flow rate of 300 ml/min. In general, the attractive effect of the C13–C18 fatty acids increased with higher concentrations, whereas the short chain fatty acids were most effective at low (C1–C3) or medium (C5–C8) concentrations.
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Responses to combinations of fatty acids with lactic acid
To test the possibility of a combinatorial effect of mixtures including short-, medium- and long chain fatty acids, each fatty acid in the C1–C18 series was added to the following mixtures: lactic acid plus C3, lactic acid plus C5, and lactic acid plus the combination of C3 and C5 (Table 1).
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The combination of lactic acid plus propanoic acid became significantly more attractive by adding fatty acids from the C5–C8 series, and no other fatty acid could increase the attractiveness of this base mixture. The attractive effect of the combination of lactic acid plus valeric acid was augmented by adding either short chain fatty acids from the C1–C3 series or stearic acid. The attractiveness of the combination of lactic acid plus propanoic and valeric acid could not be increased by adding other fatty acids, but addition of C11 and C14 caused a significant decrease of attraction for this base combination.
Since a group of mosquitoes was used several times for the experiments, we proved whether possible side effects through habituation or fatigue influence the behavioural responses of the mosquitoes. We thus pooled the data of all experiments with the mixture of lactic acid and propionic acid. When the mixture was tested as the first odour stimulus 31.2 ± 0.7% (mean ± SE) of the mosquitoes were attracted and 73.8 ± 1.2% were activated (n = 22 repetitions). Other mosquito groups which were tested first with two other stimuli and then with the mixture attracted 32.5 ± 1.2% and activated 74.3 ± 0.9% (n = 22 repetitions). Even when the odour mixture was presented as the fifth stimulus in a series (31.7 ± 0.9% attracted, 74.9 ± 1.1% activated; n = 26 repetitions) or the seventh stimulus (29.6 ± 0.9% attracted, 72.4 ± 1.1% activated; n = 25 repetitions), no significant differences were observed (ANOVA, P > 0.1).
Responses to mixtures of two fatty acids, ammonia and lactic acid
To determine whether the efficacy of several attractive compounds add up to higher levels of attractiveness when combined with lactic acid, mixtures of lactic acid, ammonia, propanoic acid and valeric acid were tested (Figure 4). A stepwise increase of attractiveness was observed with successive addition of each component (up to 68.1%). Most attractive was the blend which included all four synthetic components. This blend almost reached the effect of an extract from human skin (77.9%).
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Responses to single fatty acids in combination with CO2
Propanoic and valeric acid, which both increased the attractiveness of lactic acid, were also tested alone at their most effective concentration and in combination with CO2. Neither of the test substances had an effect on the behaviour of the mosquitoes when presented alone (Figure 5A,B): both, activation (ranging from 21 to 33%, Figure 5A) and attraction (maximum 1%, Figure 5B) were in the range of the control groups with clean air (first columns in Figure 5A,B).
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In combination with 4% CO2 none of the fatty acids changed the responses compared with the CO2 stimulus alone (activation 91.5%, attraction 10%; Figure 5A,B). In contrast, lactic acid significantly increased the attractiveness of CO2, corroborating the synergistic effect of the CO2 plus lactic acid mixture (Figure 5B).
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Discussion |
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Our experiments demonstrate that the attractive effects of fatty acids in host finding of A. aegypti depend on two factors: their chain length and their specific combination in the blend. A possible role for fatty acids as attractants for mosquitoes has already been proposed by several authors as many of these substances are present on human skin (Roessler, 1961
; Carlson et al., 1973; Knols et al., 1997). This has been confirmed in our present study and, moreover, since we have tested the fatty acids in more detail, we can now precisely state the effectiveness of these compounds. The mosquitoes are able to discriminate between fatty acids of distinct chain length when combined with lactic acid. The attractiveness of mixtures of fatty acids varies greatly with the specific composition of the blend. With regard to the interpretation of our findings, it is essential that we can exclude possible effects like habituation or fatigue on the behavioural responses of the insects, since we used every group of mosquitoes several times in a series of tests. Our data show clearly that preceding stimuli have no effect on subsequent ones. These results are also in agreement with earlier findings (Geier and Boeckh, 1999).
The attractive effect of the fatty acids was only apparent when lactic acid was present. Carbon dioxide could not replace lactic acid as the synergist, confirming the crucial role of lactic acid in host finding by the yellow fever mosquito. Lactic acid acts as a synergist with CO2 in breath (Acree et al., 1968) and with components from human skin (Geier et al., 1996) in attracting mosquitoes. Ammonia, present in both host odour sources, is only attractive in combination with lactic acid (Geier et al., 1999b). In accordance with the data of Geier et al. (Geier et al., 1999b), our results demonstrate that the attractive host odour for mosquitoes consists not of a single substance but rather of a blend of odorants which are not or only slightly attractive by themselves. The idea of a complex blend as the attractive olfactory signal in host finding of mosquitoes has already been mentioned (Galun, 1977; Takken, 1991).
Our data indicate that the following compounds contribute to the attractive blend emitted from human hosts: a short chain fatty acid, a medium-length fatty acid and ammonia, with lactic acid as the indispensable synergist. Whether fatty acids with a longer carbon chain (C13–C18) also play a role in host finding is not yet clear. When tested as pure compounds, these fatty acids significantly increase the attraction to lactic acid, but their addition to mixtures of lactic-, propanoic- and valeric acid did not cause any further increase in attractiveness. Interestingly, both the fatty acid C14, which is the most abundant in human sweat (Cork and Park, 1996), and C11 even reduced the attractiveness of any combination of lactic acid with another fatty acid. These findings point in a direction similar to those reported by Skinner et al. (Skinner et al., 1965, 1967), who found a repellent effect of skin-surface lipids. The authors suggested that the attraction to a given host depends upon a balance between naturally occurring attractants and repellents. It still remains open whether some long chain fatty acids of human skin odour play a role in the mosquito’s preference for certain persons [reviewed in (Khan, 1977)]. Since only a single concentration per stimulus has been tested so far in our experiments with odour mixtures, we cannot exclude effects at other concentrations.
Lactic acid and ammonia are attractive in doses which are supposed to evaporate from a human host (Smith et al., 1970; Geier et al., 1999b). In the case of fatty acids, however, we know neither their evaporation rate from human skin nor the absolute concentrations in our olfactometer. In order to confirm the attractive role of fatty acids, both the behavioural thresholds and the emitted doses from the host have to be determined. Although the artificial blend, composed of only four components, was almost as attractive as the whole skin extract, the slight difference in attractiveness might indicate that some other attractants have still to be identified. It is, however, also conceivable that the concentrations and proportions of the synthetic compounds tested so far were not optimal.
The behavioural effects of fatty acids in A. aegypti are also supported by electrophysiological studies (Pappenberger et al., 1996). These authors found receptor cells in antennal A3 sensilla that responded to fatty acids. These receptor cells differed with regard to their maximum sensitivity to fatty acids of different chain length, but revealed overlapping response spectra. Such receptors could enable the mosquitoes to detect both the combinations as well as the relative proportions of these fatty acids in host odour.
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Erratum |
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In the paper ‘Ammonia as an attractive component of host odour for the yellow fever mosquito, Aedes aegypti’ (Chem. Senses 24: 647–653, 1999) the information about the concentration of ammonia, 0.13 mmol/l NH3, is wrong. 0.13 mol/l is correct.
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Acknowledgments |
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We thank the Bayer AG (Leverkusen, Germany) for supply of the mosquito eggs.
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References |
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Accepted December 20, 1999
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