Journal of the American Mosquito Control Association, 10(2):309-315, 1994 Copyright @ 1994 by the American Mosquito Control Association, Inc.
SENSORY BASES OF ATTRACTANCY: MORPHOLOGY OF MOSQUITO OLFACTORY SENSILLA_A REVIEW
JAMES F. SUTCLIFFE
Department of Biology, Trent University, Peterborough, Ontario KgJ 788 Canada
ABSTRACT. The internal and external ultrastructure of virtually all of the olfactory sensilla of the mosquitoes Aedes aegypti and Anopheles stephensi have been described. Many other mosquitoes have had their olfactory complements partially described. This review summarizes ultrastructural features and suspectedbiological roles ofthe small sensillacoeloconica, large sensilla coeloconica, sensilla ampullaceae, grooved pegsand sensilla trichodea of mosquito antennae,and the capitate pegsof mosquito palps. In addition to a generalreview of the topic, severalnew points are raised: l) the lamellate dendrite is the COr-sensitiveelement in the capitate pegsof mosquitoesand in equivalent pegsof certain other insects; 2) the presenceof the purported COr-sensitive lamellate dendrite in many male mosquitoes and other biting flies arguesfor more widespreadoccurrence ofmales seekingout hosts for mating purposes;3) the grooved pegs,considered to have a single apical pore are olfactory sensillaof the multiporous grooved type bearing many pores along their side grooves; and 4) the large sensillacoeloconica are mgltiporous grooved sensillaand may have structural and functional equivalenceswith grooved peg sensilla.
INTRODUCTION Insect odor-sensitive sensilla may have from one (Schmidt The life of the female mosquito is governed, and Gnatzy 1972)to more than 50 (Barlin and Vinson l98l) sensory in largepart, by its orientation responsesto stim- cellsalthough 2-6 is more common (Zacharuk uli from important resourcessuch as resting sites, 1985). Den- drites from sensory cells usually oviposition sites,nectar sources, mates, and blood extend, either branched or unbranched, into hosts. Odors emanating from these (with the the hollow seta processwhere they come into probable exception of a mate) are known to be contact or close proximity with pores or pore-tubules important orienting stimuli for the female mos- extending from the pores. Odorant molecules quito. The purposeofthis contributionis to brief- apparently diftrse into pores ly review our current knowledge of the mor- the eventually coming into contact with, or phology ofthe cuticular sensoryreceptors used affecting in some indirect man- ner, the (1985) by mosquitoesto detect and orient to odor-type dendrites.Z,ac}lraruk reviewed in- stimuli (including heat and humidity). Orienta- sect sensillar structure and classified olfactory sensillaon the tion to these resourcesalso involves visual and, basisofpore distribution and wall in the caseof mate-finding by the male mosquito, thickness.He distinguishedbetween smooth-sid- ed "multiporous pitted" "MPP" auditory stimuli. The morphological bases for or sensilla,which may be "thin-walled" "thick-walled", these sensesin mosquitoes are summarized by or and sculpted"multiporous grooved" "MPG" Mclver (1982);Allenet al. (1987)reviewed the or sen- silla. role of vision in biting fly (including mosquito) "aporous" ecology. Zac}raruk (1985) also included an category into which fall sensilla generally con- sidered to be hygro-/thermoreceptive. In such NATURE OF INSECT sensilla,convection or conduction heat and wa- vapor CUTICULAR SENSORY ter affect the dendrites either by passing RECEPTORS through the overlying cuticle or by altering the microconformation of the cuticle thus affecting Mosquito cuticular sensoryreceptors (: sen- the dendrites indirectly. Insect hygro-/thermo- silla) are typical of those of insects in general. sensillaare reviewedby Altner and Loftus (1985). They consist ofan external cuticular processin the form of a seta or modified seta (depending MOSQUTTO on specific function). The seta is underlain by a OLFACTORY small group of modified epithelial cells including SENSILLA a bipolar sensorycell(s) and various sheathcells. Since Mclver's major review in 1982, no new Each sensorycell(s) extends a dendrite that as- information has been published on the mor- sociateswith the setain a sensorymodality-spe- phology of mosquito olfactory sensilla. The ex- cific manner.Each sensory cell also sendsan axon ception to this is a study of palpal pegs of the to the central nervous system.The axon goesto non-host-seeking mosquito, Toxorhynchites the central nervous systemwithout synapsingor brevipalpis Theobald by Mclver and Siemicki fusing with others. ( I 984). Mclver ( I 982) reviewed literature dating 309 310 Jour.rver, or rne Arr,rnnrcer Mosqurro Corqrnor AssocrenoN VoL. 10, No. 2 frorn the early 1950sand provided detailed sum- within a behaviorally significantrange (additions maries of sensillar distribution, numbers on dif- of 0.0 l0loto ambient CO, concentration)for cap- fererrtspecies and eachsex, and of the ultrastruc- itate pegsof Ae. aegypti was confirmed electro- ture ofall the sensillartypes discussedherein. In physiologicallyby Kellogg (1970). He also found all, Mclver's review provides information on as- that capitatepegs in this speciesrespond to odors pectsof the sensillarcomplement of mosquitoes ofn-heptane, acetone,and amyl acetate(the lat- from 1l genera.The mostthoroughlyknown spe- ter induces inhibition). cies are Anopheles stephensiListon, Culex pi- It is not possible with this information alone piens Linn., and Aedes aegypti (Linn.). Indeed, to determine which dendritesin the capitatepegs the claim is justifiably made that virtually all of respond to specific stimuli. However, morpho- the sensilla of Ae. aegypti have been mapped, logical evidence can be used to build a strong counted,and describedultrastructurally (Mclver circumstantial case for which dendrite is the 198'). probable CO, detector. Capitate peg equivalents Basedon a combination of detailed ultrastruc- occur on other nematoceranbiting flies such as tural information and careful counts of sensillar simuliids (Mercer and Mclver 1973) and cera- types on the antennae of Ae. aegypti and An. topogonids (Rowley and Cornford 1972) where stephensi,Mclver ( 1982)calculated that93o/o and they are found in a deep pit on the 3rd segment 850/0,respectively, ofthe neurons in the flagellar of the maxillary palp. In the black fly, Simulium nerves of these species carry information on arcticum Malloch, these pegsare innervated by odors. This speaks to the importance of odor a single neuron producing a lamellar dendrite information to the mosquito and its speaksto (Sutcliffe et al. 1987), whereasin the ceratopo- the great variety of odor information available gonid Culicoides furens (Poey), they are inner- in the mosquito's environment. vated by 2 neurons, one producing a digitiform Ar:cordingto Mclver (1982),in Ae. aegypti,5 dendrite, the other a lamellate dendrite (Chu- types ofolfactory sensillaoccur on the antennae wang et al. 1975). (largeand small sensillacoeloconica, sensilla am- Sutcliffe et al. (1987) argued that, becauseall pullaceae,grooved pegs,sensilla trichodea) and 3 biting groups (Simuliidae, Ceratopogonidae, one occurson the palps (capitatepegs). The same and Culicidae) respond to COt and becausethe sensillar types appear to occur (with some vari- lamellate dendrite is the only dendrite common ations-see below) on An. stephensiand other to the capitate pegsof all 3 groups,the lamellate species.In addition, large sensillacoelconica oc- dendrite is the probable COr detector. cur only on anopheline mosquitoes. The mor- In fact, many insects, not just bloodfeeders, phology of these sensillar types is summarized are known to respondto CO2.For instance,Bog- in the following sections. In addition, the pos- ner et al. (1986)and ke et al. (1985)described sible sensitivities and biological roles of these palpal sensilla possessinga lamellate dendrite sensillain mosquitoes,and in other insectswhere (only) in the moth Rhodogastria sp. (Arctiidae) equivalent types occur, is discussed. and in the butterfly Pieris rapae (Pieridae), re- Capitatepegs.' These sensillaoccur on palpal spectively. Furthermore, Bogner et al. (1986) segments24 in female anophelines,on palpal demonstrated electrophysiologically that these segment 4 in male anophelines (Mclver and palpal sensilla(and therefore the lamellate den- Siemicki 1975), and on segment4 only in male drite within) are CO, sensitive. This provides and female culicines studied (Mclver and Charl- further circumstantial support for the lamellate ton 1970,Mclver 197l). Numberspresent range dendrite of mosquitoesand other biting flies be- from lessthan 20 per palp in female Uranotaenia ing the COr-sensitive unit. It would be very in- sp. l:Omerand Gillies l97l) to more than 200 terestingto know what it is about CO, detection in various Culex species(see for exampleMclver that necessitatessuch an elaborate dendritic 1970).Males generallyhave fewer than females. structure. Capitate pegshave been studied ultrastructurally Morphological evidence also points out a in a number of mosquitoesincluding ,4e. aegypti seemingincongruity with respectto the sex-spe- (Mclver 1972) and An. stephensi(Mclver and cific occurrenceofthe capitate pegs;that is, al- Siemicki 1975). They are thin-walled MPP sen- though femalesalways have more such pegs,ne- silla possessing,in these species,3 neurons; 2 of matoceran males, which have no apparent need these produce a branching, digitiform dendrite to locatethe host, generallyhave some.What use each; the 3rd produces a highly lamellate den- could males make of this information? Sutcliffe drite. et al. (1987) pointed out that some male black Palpal ablation studies(Bassler 1958, Omer flies (Simulium arcticum, Boophthora erythro- and Gillies l97l) suggesta Co2-detectionrole cephalaDe Geer, Odagmia ornata (Meigen)) in- for these sensillain Ae. aegypti and Culex quin- tercept females at or near the host and may, quefasciatus Say.Carbon dioxide responsiveness therefore. orient to host odors including COz. Mosqurro Orrecrony SrNsule 3ll
Although males of a few mosquito species(e.g., monia, acetone,and water (by excitation) and of Ae. aegypti) are also known to seek mates at or aceticacid and anisole(by inhibition). Davis and near hosts, this is not thought to occur widely. Sokolove(1976) could only partiallyconfirm this In a study involving animal-baited trapping in responsespectrum but were able to show that Sweden,males of the mosquito, Aedesdiantaeus the grooved pegsof Ae. aegypti respond to lactic Howard, Dyar and Knab made up more than acid, a known mosquito attractant (Acree et al. 500/ooftrap catchesand were apparently attract- 1968). The lactic acid responsecomes from 2 ed by odors becausethe bait animals werehidden cells; one is inhibited by increasing lactic acic behind a screen (Jaenson 1985). Perhaps male concentration whereasthe other is excited by it. mosquitoes, black flies, etc., orient to hosts to The grooved pegsof Ae. aegypti also respond to locate mates more than generallyrealized. Their organic vapors including those of certain fatty absencefrom many trap collections may be due acids (possibly skin associated)and essentialoils to differences in near-host response that nor- (possibly flower/nectar-sourceassociated) (Da- mally keepthem at a distance.Alternatively, per- vis 1977).In addition, both lactic acid-sensitive haps males of some speciesonly seek mates at cells in the grooved pegsof Ae. aegypti are deet- hosts under certain special conditions. inhibited (Davis and Sokolove 1976). Although still not definitive, further evidence The grooved pegs as described by Mclver in support of mate seeking as a role for CO2- (1974) are very unusual as insect olfactory sen- detection by male nematoceranbiting flies come silla in that they have but a single apical pore from the finding that male Tx. brevipalplslack instead of the usual (for olfactory sensilla) nu- capitate pegs altogether. This mosquito species merous pores in the side walls. According to does not bloodfeed. If the females do not mass Zacharuk (1985), MPG sensilla, which the around hosts, perhaps there is no point in the grooved pegsresemble strongly, have very small males possessingsensory equipment to detect pores that open in the bottoms of the groovesin COr. the peg shaft. Theseconnect by meansof"spoke Groovedpegs.' Males and females of all mos- canals" to the lumen of the peg. Electron-dense quito speciesexamined to date possessthe short, material from the dendritic chamber often fills deeply grooved sensillacalled ,A,3sensilla in le. thesespoke canals and flows out to coat the bot- aegyptiby Stewardand Atwood ( I 963). Grooved toms of the grooves. Odorant molecules are pegs occur on all flagellar segmentsin females thought to dissolve in this material and even- varying from l0 per antenna in female (Jrano- tually diffuse to pores and into the peg lumen taenia lateraft'sLudlow to 350 per antenna in through the canals.Although Mclver (1974,Fi9. female Culex restuansTheobald (Mclver 1970). 7) observed "electron-dense strands" that look Male Ae. aegypti and,An. stephensihave fewer Iike spoke canals, this possibility was rejected grooved pegsthan conspecific females (36 in male becauseso few were seen.Spoke canals are easily Ae. aegypti vs. more than 100 in females) and missed,however, because they are not numerous they are restricted to antennal segmentsl2 and (asfew as 200 per sensillum)and may be as small l3 (Mclver 1970). as 5 nm in diameter (Zacharuk 1985). The Mclver (1974) described the grooved pegsin grooved pegs also have electron-densematerial Ae. aegypti as thick-walled and having 3-5 (usu- in their grooves. It is possible that the multi- ally 3) unbranched dendrites that make contact porous nature of these sensilla has been misin- with the outside by a single apical pore. In An. terpreted and that the single apical pore is ac- stephensithe grooved pegs are categorizedinto tually a molting pore such as occurs at the tips Al and A2 subtypesbut have the same number of many sensilla (Z,acharuk1985). In my view, of dendrites and similar ultrastructure as in Ae. there is enoughmorphological evidenceto justify aegypti (Boo and Mclver 1976, Boo 1980). leaving the possibility that the antennal grooved Groovedpeg sensilla in Cx. pipiensalsoresemble pegsof mosquitoes are conventional MPG sen- those ofle. aegypti but possessonly 2 dendrites silla open pending further examination of their (Elizarovand Chaika 1972). ultrastructure. Despite what appearsto be a contact chemo- Large sensilla coeloconica: Called "sunken sensillarmorphology (singleapical pore), Mclver pegs" by Boo and Mclver (1976) and simply "sensilla (1974) concludedthat the grooved pegsmust op- coeloconica"by Ismail ( I 962), the large erateas olfactory sensillabecause their shortness sensilla coeloconica occur only in anopheline and the fact that they are located among much mosquitoes.Female anophelines,which usually longer setaewould make contact with a substrate have a few such sensilla on each of the 7 basal virtually impossible for them. Kellogg (1970) flagellomeres,have more than conspecificmales, confirmed an olfactory function for the grooved which have between 8 and 14 mainly on the pegswith physiological evidence that the grooved subterminal flagellomere(Mclver 1982). pegs of Ae. aegypti respond to vapors of am- Large sensillacoeloconica consist ofshort pegs 3t2 Jourxnr. on rne Arr.renrclN Moseurro Corsrnor- AssocrerroN Vou 10.No. 2
"cold" (5 pm in lengthinAn. stephensi[Boo and Mclver creasingtemperature(i.e., a cell). The fact 19751)in the floor of a pit the sides of which that air temperature and relative humidity co- close partly over the peg tip. Four or 5 neurons vary often posesproblems in properly interpret- extend branched dendrites into the peg lumen. ing the responsesofthese sensilla. The dendrites appear to have contact with the Morphological evidence can suggest,but not exterior by means of up to 16 grooves that run establishdefinitively, which of the triad units are from just above the peg base to just below its humidity sensitive and which is thermorecep- tip. These grooves contain electron-densema- tive. Altner and Loftus (1985) point out that the terial along their bottoms that appearsto come microtubule-filled dendrites of the aporous peg from the peg lumen. Although no spoke canals respond mechanically to moisture-induced dis- are observed in the micrographs, these sensilla tortions of the peg cuticle. Although morpholog- fit the description of Zacharuk's (1985) MPG ically similar to mechanosensitivetubular bodies sensilla and, in my opinion, may have closer (Mclver 1975, 1985),these units may be func- affiliations with the grooved pegsthat I also sug- tional moisture detectors.The lamellate dendrite gestare MPG-type sensilla(see previous section). may be the temperature sensor; the extent of The large sensillacoeloconica are probably ol- development of the lamellae has been suggested faclory in function although no electrophysio- to relate to the temperaturerange the dendrite is logical evidence exists to support this, let alone designedto operate in-the more lamellae, the to determine specific sensitivities. However, if lower the operating temperature range may be the large sensilla coeloconica are another form (Altner and Loftus 1985). ofgrooved pegs,they may alsohave grooved peg- Early ablation experiments (Roth and Willis type sensitivitiesto skin-associatedvolatiles, deet, 1952) suggestedthat sensillaat the antennal tip and/or lactic acid. of Ae. aegypli are thermosensitive. Davis and Small sensillacoeloconica: Two or 3 so-called Sokolove (l 975) made physiological recordings "small sensilla coeloconica" occur at the tip of from the small sensillacoeloconica in the tip of both antennaeofboth sexesofall culicine. an- the antennaeof Ae. aegypti and showedthat these opheline, and toxorhynchitine speciesthat have sensillapossess 2 thermosensitive cells (one ex- been examined (Mclver 1973, Boo and Mclver cited by increasing temperature, one inhibited 1975,Mclver 1982).Each small sensillumcoe- by it). No evidencewas found for the detection loconicum consists of an aporous peg approxi- of water vapor, COr, or infrared radiation by mately 2-3 pm long set into the bottom of a thesesensilla. Considering the extent ofevidence shallow pit. Eachpeg is innervated by 2 neurons, showing such sensilla in other insectsto be hu- "packed" the dendrites of which are closely into midity sensitive,it may be premature, basedon the peglumen. The dendrite of a 3rd cell extends this one report, to dismiss the possibility of hy- toward the pegbase but stopswell short of it and groreceptionfor such sensillain all mosquitoes. takes on a lamellate form. It is tempting to ascribea role in host-seeking These morphological features are consistent behavior to the small sensillacoeloconica. Those with the "no pore, inflexible socket" hygro-/ther- of Ae. aegypti are capable of responding to the mosensilla of insectsas reviewed by Altner and small temperature changes that might occur Loftus (1985). Such sensilla are widespread in within a meter or so of the warm-blooded host insects (e.9., found in certain beetles [Arbogast (Davis and Sokolove 1975).A role for the la- etal.1972,Haug 19851;crickets Utoh et al. 19841; mellate dendrite in host seekingis also suggested moths [Haug 1985];and in the bloodfeedingbug, by morphological evidence that this dendrite is Rt\odniusprolixus Stahl [Mclver and Siemicki much reducedin sizein the antennaeof the non- 19851).Typically, these sensilla occur in very host seeker,Tx. brevipalpls(Mclver and Siemic- small numbers usually at the antennal tips and ki 1978). at the ends of the antennal segmentsand, typt- Among mosquitoes examined, the lamellate "triad" cally, they are innervated by a ofcells as dendrite is most elaborate in male Deinocerites in mosquitoes. cancerTheobald,which spendmuch oftheir lives These sensilla have been studied physiologi- in dark crab holes where they attend female pu- cally in many insects (e.g., stick insects [Tichy pae and mate with the female adults as they 19t871;locusts [Ameismeier and Loftus 1988]; emerge.Mclver and Siemicki (1976) suggested certain lepidopteran caterpillars [Schoonhoven that the elaboratelamellate dendrite of male De. 1967, Dethier and Schoonhoven 19681).Al- cancer is an infrared radiation receptor used to though much variation in response has been identify the older (arguably warmer) female pu- found, such sensilla often have 2 cells that re- pae.The highly developedlamellate dendrites of spond to changes in humidity (one cell being cavebeetles, which also spendtheir lives in dark- inhibited, the other excited by moisture increase) ness,were also suggestedas infrared detectorsby and a 3rd cell that responds positively to de- Corbidre-Tichan6(1971). No subsequentsup- JuNs 1994 Moseuro Olrecrony SeNsrr-le 3r3 port for infrared detection by these sensilla has sory function (although it is not necessarilycor- beenforthcoming. On the other hand, Altner and rect to concludethat sensillaof a given morpho- Loftus (1985)suggested that the more highly de- logical type all sharethe same sensoryfunction). veloped the lamellate dendrite, the more sensi- Given their variety in mosquitoes then, it is tive it may be to small temperature changes probable that the sensillatrichodea serve many through conduction or convection. This may ex- specific sensory functions. A number of physi- plain the elaboratelamellate dendrite in the crab- ological studies have been done on the response hole mosquito because,if about-to-emergepu- spectra of sensilla trichodea of Ae. aegypti and pae are warmer than younger ones, as Mclver other mosquito species;many of these are sum- and Siemicki (1976) argued,temperature differ- marizedin detail by Mclver (1982).Briefly, sen- encesmust be slight. silla trichodea types and subtypes have been Although presumed thermo-/hygrosensillaon found that respond to oviposition site-related biting insects may be involved in host seeking compounds(Davis 1976, Bentley et al. 1982), or, in specializedcases, mate seeking,such sen- essential oils (often associatedwith nectar silla occur in virtually all insectswhere they have sources-Lacher 1967,Davis 1977),fatty acids been looked for. The function of these sensilla and oils associatedwith skin, and to certain re- in insects,including mosquitoes,may be a gen- pellents(Lacher 1971,Davis and Rebert 1972). eral one because,as Altner and Loftus (1985: Interestingly,none ofthe sensilla "For trichodea have 273) wrote, animals as small as insects, been found to be sensitive to lactic acid. sunlit biotopes may be quite unmanageableif not quickly lethal in the absenceofinstant cluesabout their temperature and humidity." CONCLUSION Sensilla ampullaceae (pegsin deep pits) also Through the application of morphological occur in small numbers along the antennae of techniques,a thorough understandingofthe sen- male and female An. stephensiand Ae. aegypti. sillar complement (including olfactory sensilla) Their morphological similarity to small sensilla of 2 speciesof mosquitoes,Ae. aegypti and,An. coeloconica s rggeststhat the sensilla ampulla- stephensi,is now available. Less "no comprehensive, ceaeare pore, inflexible socket"-type sensilla but nonethelessuseful, information is available (Boo and Mclver 1975, Mclver and Siemicki on sensillar morphology for many other mos- 1979) sensitive to thermal and moisture stimuli quito species.IJnfortunately, very little new in- but no physiological investigations have been formation on mosquito sensorymorphology has done to confrrm their sensitivities. been forthcoming in the last l0 years. Sensilla ftichodea: These are the most nu- As the rangeof mosquito speciesof interest in merous and varied sensillaon the mosquito an- the context of attractants researchcontinues to tenna. Antennae of Tx. brevipalplsfemales bear grow, the information baseon mosquito sensory more than 1,200such sensilla (Omer and Gillies complement becomes more and more inade- l97l), whereasthose of femalesof smallerspe- quate. The foregoing summary shows that con- cies bear fewer (ca. 650 in Ae. aegypti [Steward siderable variation in sensillar types, numbers, and Atwood 19631, 550 in Anophelesspp. [Omer distribution, and ultrastructure occurs between and Gillies l97ll). Numbersofsensilla trichodea species.Although across-the-boardcataloging of on males are significantly lower than on conspe- the sensory complements of various mosquito cific females. Sensilla trichodea occur generally speciesis no longer desirable,it is still important distributed over the antennal segments,are much that proper morphological descriptions of spe- longer than the grooved pegs(though shorter than cific sensillar types continue to be made to sup- the mechanoreceptive sensilla chaetica at the port electrophysiologicaland behavioral studies basesof most antennal segments),and occur in ofattractants. For the electrophysiologistto ac- a number of variants basedon length and wheth- quire and interpret recordingsfrom mosquito at- er sharp or blunt at the tip (seeMclver [1982] tractant receptorsit is important to know things for a detailed discussionofvariants). Irrespective suchas how many of the particular sensillartypes of the variant, Mclver (1982)noted that all sen- occur on the antenna and where they are, how silla trichodea of the mosquito antennaeare in- many neurons innervate the sensillum, whether nervated by 2 sensorycells and that eachsensory this number varies from one sensillum to anoth- cell produces an unbranched dendrite that ex- er, how the dendrites associatewith the peg or tends the length of the inside of the seta.These seta,etc. Morphological information such as the conform to the thick-walled MPP-type of olfac- presence(or absence)and abundanceofsensillar tory sensillum(Zacharuk 1985)that occurswide- types of known function may also correlate with ly in insects. behavior. For instance, nonbloodfeeding mos- It is generallytrue that identifiable differences quito speciesand males often possessfewer sen- in morphology correspondto differencesin sen- silla for which functions in host attractant de- 3t4 Jounner or run Alrpmcex Moseurro CoNrtol Assocre^non Vol. 10, No. 2 tection are known or suspected than do females the surface and sunken grooved pegs on the antenna of host-seeking species. of female Anophelesstephensi (Diptera: Culicidae). Future morphological work on mosquito sen- Can. J. Zool. 54:235-244. sory structures will need to be closely linked to Chu-Wang,J-Wu, R. C. Axtell and D. R. Kline. 1975. Antennal and palpal sensilla of the sand fly Culi- behavioral and physiological studies of attrac- coidesfurens (Poey)(Diptera: Ceratopogonidae).Int. tants and other directing influences in the mos- J. InsectMorphol. Embryol. 4:l3l-149. quito's life. This means that morphologists, Corbidre-Tichan6,G. I 97 l. Structurenerveuse 6nig- phyrsiologists, and behavioral researchers will matique dans I'antennede la larve de Speophyeslu- nee
Mclver, S. B. 1970. Comparative study of antennal of pegs on the maxillary palps of adult Toxorhyn- senseorgans offemale culicine mosquitoes.Can. En- chitesbrevipalpli Theobald (Diptera: Culicidae).Int. tomol. 102:1258-1267. J. InsectMorphol. Embryol. 13:l l-20. Mclver, S. B. 1971. Comparative studieson the sense Mclver, S. B. and R. Siemicki. 1985. Fine structure organsand maxillary palps of selectedculicine mos- of antennal putative thermo-/hygrosensillaof adult quitoes. Can. J. Zool. 49:235-239. Rhodniusprolixzs Stahl (Hemiptera: Reduviidae).J. Mclver, S. B. 1972. Fine structure ofthe pegson the Morphol. 183:15J7. palps of female culicine mosquitoes. Can. J. Zool. Mercer, K. L. and S. B. Mclver. 1973. Sensilla on 50:,571-576. the palps of selectedblackflies (Diptera: Simuliidae). Mclver, S.B. 1973. Fine structureofantennal sensilla J. Med. Entomol. lO:236-239. coeloconica of culicine mosquitoes. Tissue & Cell Omer,S. M. andM. T. Gillies. 1971. Lossofresponse 5:105-l12. to carbon dioxide in palpectomizedfemale mosqui- Mclver, S. B. 1974. Fine structureofantennal grooved toes. Entomol. Exp. Appl. 14:251-252. pegsofthe mosqttito, Aedesaegyprl. Cell TissueRes. Roth, L. M. and E. R. Willis. 1952. Possiblehygro- 153:327-337. receptors in Aedes aegypti (L.) and Blatella german- Mclver, S. B. 1975. Structure of cuticular mecha- ica (L.). J. Morphol. 9 I : l-14. noreceptorsofarthropods. Annu. Rev. Entomol. 20: Rowley, W. A. and M. Cornford. 1972. Scanning 381-397. electronmicroscopy ofthe maxillary palp of selected Mclver, S. B. 1982. Sensillaof mosquitoes(Diptera: speciesof Czllcoides.Can. J. Zool. 50:1207-1210. Culicidae).J. Med. Entomol. 19:489-535. Schmidt, K. and W. Gnatzy. 1972. Dre Feinstruktur Mclver, S. B. 1985. Mechanoreception,pp. 7l-132. der Sinneshaareaufden Cerci von Gryllus bimacu- In: G. A. Kerkut and L. I. Gilbert (eds.).Compre- /4tt$ (Saltatoria, Gryllidae). III. Die kurzen Bor- hensive insect physiology, biochemistry, and phar- stenhaare.Z. Z,ellfor*,h. Mikrosk., Anat. 126:,206- macology, Volume 6. PergamonPress, Oxford. 222. Mclver, S. B. and C. C. Charlton. 1970. Studieson Schoonhoven,L. M. 1967. Some cold receptors in the senseorgans on the palps of selectedculicine larvae ofthree lepidoptera species.J. Insect Physiol. mosquitoes.Can. J. Zool. 48:293-295. l3;82t-826. Mclver, S. B. and R. Siemicki. 1975. Palpalsensilla Steward,C. C. and C. E. Atwood. 1963. The sensory ofselected anopheline mosquitoes.J. Parasitol. 6l: organs of the mosquito antenna. Can. J. ZaoL 4l: 535-538. 577-594. Mclver, S. B. and R. Siemicki. 1976. Fine structure Sutcliffe, J. F., J. L. Shipp and E. G. Kokko. 1987. ofthe antennal tip ofthe crabhole mosquito, Deino- ultrastructure of the palpal bulb sensilla of the black cerites cancer Theobald (Diptera: Culicidae). Int. J. fly Simulium arcticum (Dipteft: Simuliidae).J. Med. Insect Morphol. Embryol. 5:3 19-334. Entomol. 24:324-331. Mclver, S. B. and R. Siemicki. 1978. Fine stnrcture Tichy, H. 1987. Hygroreceptoridentiflcation and re- of antennal sensillacoeloconica of adult Toxorhvn- sponsecharacteristics in the stick insect Carausiw chites brevipalprs(Diptera: Culicidae). J. Med. Ln- morosus.J. Comp. Physiol.A 160:43-53. tomol. 14:673-676. Zachantk, R. Y. 1985. Antennae and sensilla,pp. l- Mclver, S. B. and R. Siemicki. 1979. Fine structure 69. In: G. A. Kerkut and L. I. Gilbert (eds.).Com- of the antennal sensilla of male Aedes aegypti (L.). prehensive insect physiology, biochemistry and J. Insect. Physiol. 25:21-28. pharmacology,Volume 6. PergamonPress, Oxford. Mclver, S. B. and R. Siemicki. 1984. Fine structure