Particle and Fibre Toxicology | |
Behavioural response of the malaria vector Anopheles gambiae to host plant volatiles and synthetic blends | |
Baldwyn Torto3  James H Tumlinson1  Wolfgang R Mukabana2  Peter EA Teal4  Vincent O Nyasembe2  | |
[1] Center for Chemical Ecology, Department of Entomology, Pennsylvania State University, University Park, Pennsylvania, PA, 16802, USA;School of Biological Sciences, University of Nairobi, P. O. Box 30197, GPO, Nairobi, Kenya;International Centre of Insect Physiology and Ecology, Box 30772, GPO, Nairobi, Kenya;Center for Medical, Agricultural, and Veterinary Entomology, U.S. Department of Agriculture, Agricultural Research Service, 1700 Southwest 23 Drive, Gainesville, FL, 32604, USA | |
关键词: Terpenoids; Attractant; Malaria vector; An. gambiae s.s; Host plants; Sugar feeding; | |
Others : 1229072 DOI : 10.1186/1756-3305-5-234 |
|
received in 2012-08-22, accepted in 2012-10-08, 发布年份 2012 | |
【 摘 要 】
Background
Sugar feeding is critical for survival of malaria vectors and, although discriminative plant feeding previously has been shown to occur in Anopheles gambiae s.s., little is known about the cues mediating attraction to these plants. In this study, we investigated the role of olfaction in An. gambiae discriminative feeding behaviour.
Methods
Dual choice olfactometer assays were used to study odour discrimination by An. gambiae to three suspected host plants: Parthenium hysterophorus (Asteraceae), Bidens pilosa (Asteraceae) and Ricinus communis (Euphorbiaceae). Sugar content of the three plant species was determined by analysis of their trimethylsilyl derivatives by coupled gas chromatography–mass spectrometry (GC-MS) and confirmed with authentic standards. Volatiles from intact plants of the three species were collected on Super Q and analyzed by coupled GC-electroantennographic detection (GC-EAD) and GC-MS to identify electrophysiologically-active components whose identities were also confirmed with authentic standards. Active compounds and blends were formulated using dose–response olfactory bioassays. Responses of females were converted into preference indices and analyzed by chi-square tests. The amounts of common behaviourally-active components released by the three host plants were compared with one-way ANOVA.
Results
Overall, the sugar contents were similar in the two Asteraceae plants, P. hysterophorus and B. pilosa, but richer in R. communis. Odours released by P. hysterophorus were the most attractive, with those from B. pilosa being the least attractive to females in the olfactometer assays. Six EAD-active components identified were consistently detected by the antennae of adult females. The amounts of common antennally-active components released varied with the host plant, with the highest amounts released by P. hysterophorus. In dose–response assays, single compounds and blends of these components were attractive to females but to varying levels, with one of the blends recording a significantly attractive response from females when compared to volatiles released by either the most preferred plant, P. hysterophorus (χ2 = 5.23, df = 1, P < 0.05) or as a synthetic blend mimicking that released by P. hysterophorus.
Conclusions
Our results demonstrate that (a) a specific group of plant odours attract female An. gambiae (b) females use both qualitative and quantitative differences in volatile composition to associate and discriminate between different host plants, and (c) altering concentrations of individual EAD-active components in a blend provides a practical direction for developing effective plant-based lures for malaria vector management.
【 授权许可】
2012 Nyasembe et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20151022082528363.pdf | 1371KB | download | |
Figure 6. | 53KB | Image | download |
Figure 5. | 82KB | Image | download |
Figure 4. | 66KB | Image | download |
Figure 3. | 95KB | Image | download |
Figure 2. | 61KB | Image | download |
Figure 1. | 68KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
【 参考文献 】
- [1]Van Handel E: Metabolism of nutrients in the adult mosquito. J Am Mosq Control Assoc 1984, 44:573-579.
- [2]Foster WA: Mosquito sugar feeding and reproductive energetics. Annu Rev Entomol 1995, 40:443-474.
- [3]Foster WA: Phytochemicals as population sampling lures. J Am Mosq Control Assoc 2008, 24:138-146.
- [4]Reisen WK, Meyer RP, Milby MM: Patterns of fructose feeding by Culex tarsalis (Diptera: Culicidae). J Med Entomol 1986, 23:366-373.
- [5]Gary RE, Cannon JW, Foster WA: Effect of sugar on male Anopheles gambiae mating performance. As modified bytemperature, space and body size. Parasites and vectors 2009, 2:19. BioMed Central Full Text
- [6]Nayar JK, Sauerman DM: Physiological effects of carbohydrates on survival, metabolism and flight potential of female Aedes taeniorhynchus. J Insect Physiol 1971, 17:2221-2233.
- [7]Nayar JK, Sauerman DM: The effect of diet on life-span fecundity and flight potential of female Aedes taeniorhynchus adults. J Med Entomol 1971, 8:506-513.
- [8]Nayar JK, Sauerman DM: The effects of nutrition on survival and fecundity in Florida mosquitoes. Part 1. Utilization of sugar for survival. J Med Entomol 1975, 12:92-98.
- [9]Magnarelli LA: Nectar-feeding by female mosquitoes and its relation to follicular development and parity. J Med Entomol 1978, 14:527-530.
- [10]Impoinvil DE, Kongere JO, Foster WA, Njiru BN, Githure JI, Beier JC, Hassanali A, Knols BGJ: Feeding and survival of the malaria vector Anopheles gambiae on plants growing in Kenya. Med Vet Entomol 2004, 18:108-115.
- [11]Manda H, Gougna LC, Nyandat E, Kabiru EW, Jackson RR, Foster WA, Githure JI, Beier JC, Hassanali A: Discriminative feeding behaviour of Anopheles gambiae s.s. on endemic plants in western Kenya. Med Vet Entomol 2007, 21:103-111.
- [12]Sandholm HA, Price RD: Field observations on the nectar feeding habits of some Minesota mosquitoes. Mosq News 1962, 22:346-349.
- [13]Grimstad PR, DeFoliart GR: Nectar sources of Wisconsin mosquitoes. J Med Entomol 1974, 11:331-341.
- [14]Yuval B: The other habit: sugar feeding by mosquitoes. Bull Soc Vector Ecol 1993, 17:150-156.
- [15]Gary RE, Foster WA: Effects of available sugar on the reproductive fitness and vectorial capacity of the malaria vector Anopheles gambiae (Diptera: Culicidae). J Med Entomol 2001, 38:22-28.
- [16]Gu W, Müller G, Schlein Y, Novak RJ, Beier JC: Natural plant sugar sources of Anopheles mosquitoes strongly impact malaria transmission potential. PLoS One 2011, 6(1):e15996.
- [17]Beier JC: Frequent blood-feeding and restrictive sugar-feeding behavior enhance the malaria vector potential of Anopheles gambiae s.l. and An. funestus (Diptera: Culicidae) in western Kenya. J Med Entomol 1996, 33:613-688.
- [18]Manda H, Gougna LC, Foster WA, Jackson RR, Beier JC, Githure JA, Hassanali A: Effect of discriminative plant-sugar feeding on the survival and fecundity of Anopheles gambiae. Malaria J 2007, 6:113. BioMed Central Full Text
- [19]Müller GC, Beier JC, Traore SF, Toure MB, Traore MM, Doumbia SBS, Schlein Y: Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malaria J 2010, 9:262. BioMed Central Full Text
- [20]Gary RE, Foster WA: Anopheles gambiae feeding and survival on honeydew and extra-floral nectar of peridomestic plants. Med Vet Entomol 2004, 18:102-107.
- [21]Jepson PC, Healy TP: The location of floral nectar sources by mosquitoes: an advanced bioassay for volatile plant odours and initial studies with Aedes aegypti (L.) (Diptera: Culicidae). Bull Entomol Res 1988, 78:641-650.
- [22]Bowen MF: The sensory physiology of host-seeking behavior in mosquitoes. Annu Rev Entomol 1991, 36:139-158.
- [23]Foster WA, Hancock RG: Nectar-related olfactory and visual attractants for mosquitoes. J Am Mosq Control Assoc 1994, 10:288-296.
- [24]Mauer DJ, Rowley WA: Attraction of Culex pipiens pipiens (Diptera: Culicidae) to flower volatiles. J Med Entomol 1999, 36:503-507.
- [25]Foster WA, Takken W: Nectar-related vs. human-related volatiles: behavioural response and choice by female and male Anopheles gambiae (Diptera: Culicidae) between emergence and first feeding. Bull Entomol Res 2004, 94:145-157.
- [26]Torto B, Fombong AT, Mutyambai D, Muli E, Arbogast RT, Teal PEA: Aethina tumida (Coleoptera: Nitidulidae) and Oplostomus haroldi (Coleoptera: Scarabaeidae): Occurrence in Kenya, distribution within honey bee colonies, and responses to host odours. Ann Entomol Soc Am 2010, 102(3):389-396.
- [27]Kugel M: The time course of the electroretinogram of compound eyes in insects and its dependence on special recording conditions. J Exp Biol 1977, 71:1-6.
- [28]Carsson MA, Anderson P, Hartlieb E, Hansson BS: Experience-dependent modification of orientational response to olfactory cues in larvae of Spodoptera littoralis. J Chem Ecol 1999, 25(11):2445-2454.
- [29]R Development Core Team: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; ISBN 3-900051-07-0, URL http://www.R-project.org webcite
- [30]Thorsteinson AJ, Brust RA: The influence of flower scents on aggregations of caged adult Aedes aegypti. Mosq News 1962, 22:349-351.
- [31]Healy TP, Jepson PC: The location of flower nectar sources by mosquitoes: the long-range responses of Anopheles arabiensisPatton (Diptera: Culicidae) to Achillea millefolium flowers and isolated floral odor. Bull Entomol Res 1988, 78:651-657.
- [32]Kline DL, Takken W, Wood JR, Carlson DA: Field studies on the potential of butanone, carbon dioxide, honey extract, 1-octen-3-ol, L-lactic acid and phenols as attractants for mosquitoes. Med Vet Entomol 1990, 4:383-391.
- [33]Bowen MF: Terpene-sensitive receptors in female Culex pipiens mosquitoes: Electrophysiology and behaviour. J Insect Physiol 1992, 38:759-764.
- [34]Hancock RG, Foster WA: Effect of preblood-meal sugar on sugar seeking and upwind flight by gravid and parous Aedes aegypti (Diptera: Culicidae). J Med Entomol 1993, 30:353-359.
- [35]Otienoburu PE, Ebrahimi B, Phelan PL, Foster WA: Analysis and optimization of a synthetic milkweed floral attractant for mosquitoes. J Chem Ecol 2012.
- [36]Stoutamire WP: Mosquito pollination of Habenaria obtusata (Orchidaceae). Mich Bot 1968, 7:203-212.
- [37]McCrae AWR, Ssenkubuge Y, Manuma P, Mawejje C, Kitama A: Mosquito and tabanid activity at plant sugar sources. E Afr Virus Res Inst Rep 1968, 18:96-102.
- [38]Thien LB: Mosquito pollination of Habenaria obtusata (Orchidaceae). Am J Bot 1969, 56:232-237.
- [39]Grimstad PR, Defoliart GR: Nectar sources of Wisconsin mosquitoes. J Med Entomol 1974, 11:3313-41.
- [40]Jhumur US, Dötterl S, Jürgens A: Floral odors of Silene otites: Their variability and attractiveness to mosquitoes. J Chem Ecol 2008, 34:14-25.
- [41]Carey AF, Wang G, Su C, Zwiebel LJ, Carlson JR: Odorant reception in the malaria mosquito Anopheles gambiae. Nature 2010, 464:66-71.
- [42]Dekker T, Ignell R, Glinwood R, Hopkins R: Identification of repellent odours from Ocimum forkolei. Parasites and vectors 2011, 4:183. BioMed Central Full Text
- [43]Allan SA, Bernier UR, Kline DL: Laboratory evaluation of avian odors for mosquito (Diptera: Culicidae) attraction. J Med Entomol 2006, 43:225-231.
- [44]Cha DH, Nojima S, Hesler SP, Zhang A, Linn CE Jr, Roelofs WL, Loeb GM: Identification and field evaluation of grape shoot volatiles attractive to female grape berry moth (Paralobesia viteana). J Chem Ecol 2008, 34(9):1180-1189.
- [45]Tasin M, Bäckman AC, Bengtsson M, Loriatti C, Witzgall P: Essential host plant cues in the grapevine moth. Naturwissenschaften 2006, 93:141-144.
- [46]Riffell JA, Lei H, Christensen TA, Hildebrand JG: Characterization and coding of behaviorally significant odor mixtures. Cur Bio 2009, 19:335-340.
- [47]Schoonhoven LM, van Loon JJA, Dicke M: Insect-plant biology. Oxford: Oxford Univ Press; 2005:412.
- [48]Visser JH: Host odour perception in phytophagous insects. Annu Rev Entomol 1986, 31:121-144.
- [49]Schlein Y, Müller G: An approach to mosquito control: Using the dominant attraction of flowering Tamarix jordanis trees against Culex pipiens. J Med Entomol 2008, 45:384-390.
- [50]Müller GC, Kravchenko VD, Schlein Y: Decline of Anopheles sergentii and Aedes caspius populations following presentation of attractive, toxic (Spinosad), sugar bait stations in an oasis. J Am Mosq Control Assoc 2010, 24:147-149.