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,largesensillacoeloconica,sensillaampullaceae,
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 widespreadoccurrenceofmales seekingout hosts for mating purposes;3) the
grooved pegs,consideredto have a single apical pore are olfactory sensillaof the multiporous grooved
type bearing many pores along their side grooves; and 4) the large sensillacoeloconicaare mgltiporous
grooved sensillaand may have structural and functional equivalenceswith grooved peg sensilla.
INTRODUCTION
Insect odor-sensitive sensilla may have from
(Schmidt and Gnatzy 1972)to more than 50
one
The life of the female mosquito is governed,
(Barlin and Vinson l98l) sensorycellsalthough
in largepart, by its orientation responsesto stim(Zacharuk 1985). Denuli from important resourcessuchasrestingsites, 2-6 is more common
oviposition sites,nectarsources,mates,and blood drites from sensory cells usually extend, either
hosts. Odors emanating from these (with the branched or unbranched, into the hollow seta
probable exception of a mate) are known to be processwhere they come into contact or close
proximity with pores or pore-tubules extending
important orienting stimuli for the female mosquito. The purposeofthis contributionis to brief- from the pores. Odorant molecules apparently
ly review our current knowledge of the mor- diftrse into the pores eventually coming into
phology ofthe cuticular sensoryreceptors used contact with, or affecting in some indirect man(1985) reviewed inby mosquitoesto detect and orient to odor-type ner, the dendrites.Z,ac}lraruk
stimuli (including heat and humidity). Orienta- sect sensillar structure and classified olfactory
tion to these resourcesalso involves visual and, sensillaon the basisofpore distribution and wall
He distinguishedbetweensmooth-sidin the caseof mate-finding by the male mosquito, thickness.
"multiporous pitted" or "MPP" sensilla,which
ed
auditory stimuli. The morphological bases for
"thin-walled"
"thick-walled", and
these sensesin mosquitoes are summarized by may be "multiporous or
grooved" or "MPG" senMclver (1982);Allenet al. (1987)reviewedthe sculpted
silla.
role of vision in biting fly (including mosquito)
Zac}raruk (1985) also included an "aporous"
ecology.
category into which fall sensilla generally considered to be hygro-/thermoreceptive. In such
sensilla,convection or conduction heat and waNATURE OF INSECT
ter vapor affect the dendrites either by passing
CUTICULAR SENSORY
through the overlying cuticle or by altering the
RECEPTORS
microconformation of the cuticle thus affecting
Mosquito cuticular sensoryreceptors (: sen- the dendrites indirectly. Insect hygro-/thermosilla) 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 OLFACTORY
on specific function). The seta is underlain by a
SENSILLA
small group of modified epithelial cellsincluding
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 morsociateswith the setain a sensorymodality-spe- phology of mosquito olfactory sensilla. The excific manner.Eachsensorycell 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 capfererrtspeciesand eachsex,and of the ultrastruc- itate pegsof Ae. aegypti was confirmed electroture ofall the sensillartypes discussedherein. In physiologicallyby Kellogg (1970). He also found
all, Mclver's review provides information on as- that capitatepegsin this speciesrespondto odors
pectsof the sensillarcomplement of mosquitoes ofn-heptane, acetone,and amyl acetate(the latfrom 1l genera.The mostthoroughlyknown spe- ter induces inhibition).
It is not possible with this information alone
cies are Anopheles stephensiListon, Culex pipiens 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, morphothe 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
probable CO, detector. Capitate peg equivalents
198').
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 ceratypes on the antennae of Ae. aegypti and An. topogonids (Rowley and Cornford 1972) where
stephensi,Mclver ( 1982)calculatedthat93o/oand 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 ceratopothe great variety of odor information available gonid Culicoides furens (Poey), they are innervated by 2 neurons, one producing a digitiform
in the mosquito's environment.
Ar:cordingto Mclver (1982),in Ae. aegypti,5 dendrite, the other a lamellate dendrite (Chutypes ofolfactory sensillaoccur on the antennae wang et al. 1975).
Sutcliffe et al. (1987) argued that, becauseall
(largeand small sensillacoeloconica,sensillaampullaceae,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 sensillacoelconicaoc- dendrite is the probable COr detector.
In fact, many insects, not just bloodfeeders,
cur only on anopheline mosquitoes. The morphology of these sensillar types is summarized are known to respondto CO2.For instance,Bogin 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)
and in the butterfly Pieris rapae (Pieridae), reequivalent types occur, is discussed.
palpal
spectively. Furthermore, Bogner et al. (1986)
pegs.'
These
sensilla
occur
on
Capitate
segments24 in female anophelines,on palpal demonstrated electrophysiologically that these
segment 4 in male anophelines (Mclver and palpal sensilla(and therefore the lamellate denSiemicki 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). Numberspresentrange dendrite of mosquitoesand other biting flies befrom lessthan 20 per palp in female Uranotaenia ing the COr-sensitive unit. It would be very insp. l:Omerand Gillies l97l) to more than 200 terestingto know what it is about CO, detection
in various Culex species(seefor exampleMclver that necessitatessuch an elaborate dendritic
1970).Males generallyhave fewer than females. structure.
Morphological evidence also points out a
Capitate pegshave been studied ultrastructurally
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, alSiemicki 1975). They are thin-walled MPP sen- though femalesalways have more such pegs,nesilla 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
et al. (1987) pointed out that some male black
drite.
Palpal ablation studies (Bassler1958, Omer flies (Simulium arcticum, Boophthora erythroand Gillies l97l) suggesta Co2-detectionrole cephalaDe Geer, Odagmia ornata (Meigen)) infor 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
Although males of a few mosquito species(e.g.,
Ae. aegypti) are also known to seek mates at or
near hosts, this is not thought to occur widely.
In a study involving animal-baited trapping in
Sweden,males of the mosquito, Aedesdiantaeus
Howard, Dyar and Knab made up more than
500/ooftrap catchesand were apparently attracted by odors becausethe bait animals werehidden
behind a screen (Jaenson 1985). Perhaps male
mosquitoes, black flies, etc., orient to hosts to
locate mates more than generallyrealized. Their
absencefrom many trap collections may be due
to differences in near-host response that normally keepthem at a distance.Alternatively, perhaps males of some speciesonly seek mates at
hosts under certain special conditions.
Although still not definitive, further evidence
in support of mate seeking as a role for CO2detection by male nematoceranbiting flies come
from the finding that male Tx. brevipalplslack
capitate pegs altogether. This mosquito species
does not bloodfeed. If the females do not mass
around hosts, perhaps there is no point in the
males possessingsensory equipment to detect
COr.
Groovedpegs.' Males and females of all mosquito speciesexamined to date possessthe short,
deeply grooved sensillacalled ,A,3sensillain le.
aegyptiby Stewardand Atwood ( I 963). Grooved
pegs occur on all flagellar segmentsin females
varying from l0 per antenna in female (Jranotaenia lateraft'sLudlow to 350 per antenna in
female Culex restuansTheobald (Mclver 1970).
Male Ae. aegypti and,An. stephensihave fewer
grooved pegsthan conspecificfemales(36 in male
Ae. aegypti vs. more than 100 in females) and
they are restricted to antennal segmentsl2 and
l3 (Mclver 1970).
Mclver (1974) described the grooved pegsin
Ae. aegyptias thick-walled and having 3-5 (usually 3) unbranched dendrites that make contact
with the outside by a single apical pore. In An.
stephensithe grooved pegs are categorizedinto
Al and A2 subtypesbut have the same number
of dendrites and similar ultrastructure as in Ae.
aegypti (Boo and Mclver 1976, Boo 1980).
Groovedpegsensillain Cx. pipiensalsoresemble
those ofle. aegyptibut possessonly 2 dendrites
(Elizarov and Chaika 1972).
Despite what appearsto be a contact chemosensillarmorphology (singleapical pore),Mclver
(1974) concludedthat the grooved pegsmust operateas olfactory sensillabecausetheir shortness
and the fact that they are located among much
longer setaewould make contact with a substrate
virtually impossible for them. Kellogg (1970)
confirmed an olfactory function for the grooved
pegswith physiological evidence that the grooved
pegs of Ae. aegypti respond to vapors of am-
SrNsule
3ll
monia, acetone,and water (by excitation) and of
aceticacid and anisole(by inhibition). Davis and
Sokolove(1976)could only partiallyconfirm this
responsespectrum but were able to show that
the grooved pegsof Ae. aegypti respond to lactic
acid, a known mosquito attractant (Acree et al.
1968). The lactic acid responsecomes from 2
cells; one is inhibited by increasing lactic acic
concentration whereasthe other is excited by it.
The grooved pegsof Ae. aegypti also respond to
organic vapors including those of certain fatty
acids (possiblyskin associated)and essentialoils
(possibly flower/nectar-sourceassociated)(Davis 1977).In addition, both lactic acid-sensitive
cells in the grooved pegsof Ae. aegypti are deetinhibited (Davis and Sokolove 1976).
The grooved pegs as described by Mclver
(1974) are very unusual as insect olfactory sensilla in that they have but a single apical pore
instead of the usual (for olfactory sensilla) numerous pores in the side walls. According to
Zacharuk (1985), MPG sensilla, which the
grooved pegsresemblestrongly, have very small
pores that open in the bottoms of the groovesin
the peg shaft. Theseconnectby meansof"spoke
canals" to the lumen of the peg. Electron-dense
material from the dendritic chamber often fills
thesespokecanalsand flows out to coat the bottoms of the grooves. Odorant molecules are
thought to dissolve in this material and eventually diffuse to pores and into the peg lumen
through the canals.Although Mclver (1974,Fi9.
7) observed "electron-dense strands" that look
Iike spoke canals, this possibility was rejected
becauseso few were seen.Spokecanalsare easily
missed,however,becausethey are not numerous
(asfew as 200 per sensillum)and may be as small
as 5 nm in diameter (Zacharuk 1985). The
grooved pegs also have electron-densematerial
in their grooves. It is possible that the multiporous nature of these sensilla has been misinterpreted and that the single apical pore is actually a molting pore such as occurs at the tips
of many sensilla (Z,acharuk1985). In my view,
there is enoughmorphological evidenceto justify
leaving the possibility that the antennal grooved
pegsof mosquitoes are conventional MPG sensilla open pending further examination of their
ultrastructure.
Large sensilla coeloconica: Called "sunken
pegs" by Boo and Mclver (1976) and simply
"sensilla coeloconica"
by Ismail ( I 962), the large
sensilla coeloconica occur only in anopheline
mosquitoes.Female anophelines,which usually
have a few such sensilla on each of the 7 basal
flagellomeres,have more than conspecificmales,
which have between 8 and 14 mainly on the
subterminal flagellomere(Mclver 1982).
Largesensillacoeloconicaconsistofshort pegs
3t2
Jourxnr. on rne Arr.renrclN Moseurro Corsrnor- AssocrerroN
Vou 10. No. 2
(5 pm in lengthinAn. stephensi[Boo and Mclver
creasingtemperature(i.e., a "cold" cell). The fact
19751)in the floor of a pit the sides of which that air temperature and relative humidity coclose partly over the peg tip. Four or 5 neurons vary often posesproblems in properly interpretextend branched dendrites into the peg lumen. ing the responsesofthese sensilla.
Morphological evidence can suggest,but not
The dendrites appear to have contact with the
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 thermoreceptip. 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 disare observed in the micrographs, these sensilla tortions of the peg cuticle. Although morphologfit the description of Zacharuk's (1985) MPG ically similar to mechanosensitivetubular bodies
sensilla and, in my opinion, may have closer (Mclver 1975, 1985),theseunits may be funcaffiliations with the grooved pegsthat I also sug- tional moisture detectors.The lamellate dendrite
gestare MPG-type sensilla(seeprevious section). may be the temperature sensor; the extent of
The large sensillacoeloconicaare probably ol- development of the lamellae has been suggested
faclory in function although no electrophysio- to relate to the temperaturerangethe 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).
Early ablation experiments (Roth and Willis
ofgrooved pegs,they may alsohave grooved pegvolatiles,deet, 1952) suggestedthat sensillaat the antennal tip
type sensitivitiesto skin-associated
of Ae. aegypli are thermosensitive. Davis and
and/or lactic acid.
Small sensillacoeloconica: Two or 3 so-called Sokolove (l 975) made physiological recordings
"small sensilla coeloconica" occur at the tip of from the small sensillacoeloconicain the tip of
both antennaeofboth sexesofall culicine. an- the antennaeof Ae. aegyptiand showedthat these
opheline, and toxorhynchitine speciesthat have sensillapossess2 thermosensitive cells (one excited by increasing temperature, one inhibited
been examined (Mclver 1973, Boo and Mclver
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.Consideringthe extent ofevidence
shallow pit. Eachpegis innervated by 2 neurons, showing such sensilla in other insectsto be hu"packed" into midity sensitive,it may be premature, basedon
the dendrites of which are closely
peg
The
lumen.
dendrite of a 3rd cell extends this one report, to dismiss the possibility of hythe
toward the pegbasebut stopswell short of it and groreceptionfor such sensillain all mosquitoes.
It is tempting to ascribea role in host-seeking
takes on a lamellate form.
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 laetal.1972,Haug 19851;cricketsUtoh 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 non19851).Typically, these sensilla occur in very host seeker,Tx. brevipalpls(Mclver and Siemicsmall numbers usually at the antennal tips and ki 1978).
Among mosquitoes examined, the lamellate
at the ends of the antennal segmentsand, typt"triad" ofcells as dendrite is most elaborate in male Deinocerites
cally, they are innervated by a
cancerTheobald,which spendmuch oftheir lives
in mosquitoes.
These sensilla have been studied physiologi- in dark crab holes where they attend female pucally 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 pufound, 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 darkinhibited, 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
port for infrared detection by these sensilla has
beenforthcoming. On the other hand, Altner and
Loftus (1985)suggested
that the more highly developed the lamellate dendrite, the more sensitive it may be to small temperature changes
through conduction or convection. This may explain the elaboratelamellatedendrite in the crabhole mosquito because,if about-to-emergepupae are warmer than younger ones, as Mclver
and Siemicki (1976) argued,temperature differencesmust be slight.
Although presumed thermo-/hygrosensillaon
biting insects may be involved in host seeking
or, in specializedcases,mate seeking,such sensilla occur in virtually all insectswherethey have
been looked for. The function of these sensilla
in insects,including mosquitoes,may be a general one because,as Altner and Loftus (1985:
273) wrote, "For animals as small as insects,
sunlit biotopes may be quite unmanageableif not
quickly lethal in the absenceofinstant cluesabout
their temperature and humidity."
Sensilla ampullaceae (pegsin deep pits) also
occur in small numbers along the antennae of
male and female An. stephensiand Ae. aegypti.
Their morphological similarity to small sensilla
coeloconica s rggeststhat the sensilla ampullaceaeare "no pore, inflexible socket"-type sensilla
(Boo and Mclver 1975, Mclver and Siemicki
1979) sensitive to thermal and moisture stimuli
but no physiological investigations have been
done to confrrm their sensitivities.
Sensilla ftichodea: These are the most numerous and varied sensillaon the mosquito antenna. Antennae of Tx. brevipalplsfemalesbear
more than 1,200suchsensilla(Omer and Gillies
l97l), whereasthose of femalesof smaller species bear fewer (ca. 650 in Ae. aegypti [Steward
and Atwood 19631,550 in Anophelesspp.[Omer
and Gillies l97ll). Numbersofsensillatrichodea
on males are significantly lower than on conspecific females. Sensilla trichodea occur generally
distributed over the antennal segments,are much
longer than the grooved pegs(though shorter than
the mechanoreceptive sensilla chaetica at the
basesof most antennal segments),and occur in
a number of variants basedon length and whether sharp or blunt at the tip (seeMclver [1982]
for a detailed discussionofvariants). Irrespective
of the variant, Mclver (1982)noted that all sensilla trichodea of the mosquito antennaeare innervatedby 2 sensorycellsand that eachsensory
cell produces an unbranched dendrite that extends the length of the inside of the seta.These
conform to the thick-walled MPP-type of olfactory sensillum(Zacharuk 1985)that occurswidely in insects.
It is generallytrue that identifiable differences
in morphology correspondto differencesin sen-
3r3
SeNsrr-le
sory function (although it is not necessarilycorrect to concludethat sensillaof a given morphological type all sharethe same sensoryfunction).
Given their variety in mosquitoes then, it is
probable that the sensillatrichodea serve many
specific sensory functions. A number of physiological studies have been done on the response
spectra of sensilla trichodea of Ae. aegypti and
other mosquito species;many of these are summarizedin detail by Mclver (1982).Briefly, sensilla trichodea types and subtypes have been
found that respond to oviposition site-related
compounds(Davis 1976, Bentley et al. 1982),
essential oils (often associatedwith nectar
sources-Lacher 1967,Davis 1977),fatty acids
and oils associatedwith skin, and to certain repellents(Lacher 1971,Davis and Rebert 1972).
Interestingly,none ofthe sensillatrichodea have
been found to be sensitive to lactic acid.
CONCLUSION
Through the application of morphological
techniques,a thorough understandingofthe sensillar complement (including olfactory sensilla)
of 2 speciesof mosquitoes,Ae. aegypti and,An.
stephensi,is now available. Lesscomprehensive,
but nonethelessuseful, information is available
on sensillar morphology for many other mosquito species.IJnfortunately, very little new information on mosquito sensorymorphology has
been forthcoming in the last l0 years.
As the rangeof mosquito speciesof interest in
the context of attractants researchcontinues to
grow, the information baseon mosquito sensory
complement becomes more and more inadequate. The foregoing summary shows that considerable variation in sensillar types, numbers,
distribution, and ultrastructure occurs between
species.Although across-the-boardcatalogingof
the sensory complements of various mosquito
speciesis no longer desirable,it is still important
that proper morphological descriptions of specific sensillar types continue to be made to support electrophysiologicaland behavioral studies
ofattractants. For the electrophysiologistto acquire and interpret recordingsfrom mosquito attractant receptorsit is important to know things
suchashow many of the particular sensillartypes
occur on the antenna and where they are, how
many neurons innervate the sensillum, whether
this number varies from one sensillum to another, how the dendrites associatewith the peg or
seta,etc. Morphological information such as the
presence(or absence)and abundanceofsensillar
types of known function may also correlatewith
behavior. For instance, nonbloodfeeding mosquito speciesand males often possessfewer sensilla for which functions in host attractant de-
3t4
Jounner or run Alrpmcex Moseurro CoNrtol
tection are known or suspected than do females
of host-seeking species.
Future morphological work on mosquito sensory structures will need to be closely linked to
behavioral and physiological studies of attractants and other directing influences in the mosquito's life. This means that morphologists,
phyrsiologists, and behavioral researchers will
nee<lto work more closely than ever. Indeed, the
combination of these approaches will be essential
to the complete understanding of the mosquito's
olfactory responses because no one approach
provides all the pieces ofthe puzzle.
ACKNOWLEDGMENTS
I am grateful to Ed Davis and Susan Mclver
for discussions that helped shape this review.
REFERENCES CITED
Acree, F., Jr., R. B. Turner, H. K. Gouck, M. Beroza
anldN. Smith. 1968. t-lactic acid; a mosquito attractant isolatedfrom humans. Science161:13461347.
Allen,S. A., J. F. Dayand J. D. Edman. 1987. Visual
ecologyofbiting flies. Annu. Rev. Entomol. 32:297316.
Altner, H. and R. Loftus. 1985. Ultrastructure and
function of insectthermo- and hygroreceptors.Annu.
Rev. Entomol. 30:273-29 5.
Ameismeier, J. and R. Loftus. 1988. Responsecharacteristics of cold cell on the antenna of Locusta
migratoriaL. J. Comp. Physiol.A 163:507-516.
Arbogast,R. T., R. M. Roppeland M. Carthon. 1972'
Hygroreceptors of adult sawtoothed grain beetles,
Oryzaephilussuranamensis(L.) (Coleoptera:Cucujirlae). Can. J. Zool. 50:l 147-1153.
Barlin, M. R. and S. B. Vinson. 1981. Multiporous
plate sensilla in the antennae of Chalcidoidea (Hymenoptera).Int. J. Insect Morphol. Embryol. l0:2942.
Bassler, U. 1958. Versuche zur Orientierung der
Stechmuchen:die Schwarmbildung und die Bedeutung des JohnstonschenOrgans.Z. Vgl. Physiol. 4 I :
300-330.
Bentley,M. D., I. N. McDaniel and E. E. Davis. I 982.
Studiesof 4-methylcyclohexanol:art AedestriseriatnJ (Diptera: Culicidae) oviposition attractant. J. Med.
Entomol.l9:589-592.
Bogner, F., M. Boppre, K.-D. Ernst and J. Boeckh.
I 986. CO, sensitive receptors on labial palps of
Rhodogastriamoths (Lepidoptera:Arctiidae): physiology, fine structure and central projection. J' Comp.
Physiol.A 158;74l-7 49.
Boo, K. S. 1980. Antennal sensoryreceptors ofthe
male mosquito, Anophelesstephensi.Z. Parasitenkd.
6l;249-264.
Boo, K. S. and S. B. Mclver. 1975. Fine structure of
sunken thick-walled pegs (sensilla ampullacea and
coeloconica)on the antennaeofmosquitoes. Can. J.
7noL 53:262-266.
Boo, K. S. and S. B. Mclver. 1976. Fine structure of
Assocre^non
Vol. 10, No. 2
the surface and sunken grooved pegson the antenna
of female Anophelesstephensi(Diptera: Culicidae).
Can. J. Zool. 54:235-244.
Chu-Wang,J-Wu, R. C. Axtell and D. R. Kline. 1975.
Antennal and palpal sensilla of the sand fly Culicoidesfurens (Poey)(Diptera: Ceratopogonidae).Int.
J. InsectMorphol. Embryol. 4:l3l-149.
Corbidre-Tichan6,G. I 97 l. Structurenerveuse6nigmatique dans I'antennede la larve de Speophyeslucidulus Delat. (Col6optdre cavernicole de la sousfamilledesBathysciinae).
J. Microsc.(Paris)l0:191202.
Davis, E. E. 1976. A receptorsensitiveto oviposition
site attractantson the antennaofthe mosquito,ledes
aegypti.J. InsectPhysiol.22:1371-1376.
Davis, E. E. 1977. Responseto the antennalreceptors
of themaleAedesaegyptimosquito.J. InsectPhysiol.
2}.613417.
Davis, E. E. and C. S. Rebert. 1972. Elements of
olfactory receptor coding in the yellow fever mosquito.J. Econ.Entomol.65:1058-1061.
Davis, E. E. and P. G. Sokolove. 1975. Temperature
responsesof antennal receptorsof mosquito, ledes
aegypti.J. Comp. Physiol. 496:223-236.
Davis, E. E. and P. G. Sokolove. 1976. Lactic acid
sensitivereceptorson the antennaeofmosquito ledesaegypti.J. Comp. Physiol.A 105:43-54.
Dethier,V. G. and L. M. Schoonhoven. 1968. Evaluation ofevaporation by cold and humidity receptors in caterpillars.J. InsectPhysiol. l4:1049-1054.
Elizarov, Y. and S. Y. Chaika. 1972. Ultrastructure
ofthe olfactory sensillaeon antennaeand palps of
the mosquito Culex pipiens molestus (Diptera: Culicidae). Zool. Zh. 5 I : I 665- I 675. [In Russian.]
Haug, T. 1985. Ultrastructure of the dendritic outer
segmentsof sensorycells in poreless(no-pore) sensilla of insects.A cryofixation study. Cell TissueRes.
242:313-322.
Ismail, I. A. H. 1962. Senseorgans in the antennae
of Anophelesmaculipennisatroparvzs(V. Thiel), and
their possible function in relation to the attraction
of femalemosquitoto man. Acta Trop. 19:1-58.
Itoh, T., F. Yokohori and Y. Tominaga. 1984. Two
types of antennal hygro- and thermoreceptive sensilla of the cricket, Gryllus bimaculalas (De Geer).
Zool. Sci. 1:533-543.
Jaenson,T. G. T. 1985. Attraction to mammals of
male mosquitoes with special reference to Aedes
diantaeusin Sweden.J. Am. Mosq. Control Assoc.
1:195-198.
Kellogg, F. E. 1970. Water vapour and carbon dioxide receptorsin Aedesaegypti(L.\. J. Insect Physiol. 16:99-108.
Lacher, V. 1967. Elektrophysiologische Untersuchungen an Einzelnen Geruchsrezeptorenauf den
Antennen Weiblicher Moskitos (,4edesaegptiL.) J.
InsectPhysiol. 13:1461-1470.
Lacher,V. 1971. Arbeitsbereichevon Geruchsrezeptoren auf der Moskitoantenne (Aedesaegypti).J. Ir.rsect.Physiol. 17:507-517.
Lee, J. K., R. SelzerandH. Altner. 1985. Lamellated
outer dendritic segmentsof a chemoreceptor within
a wall-pore sensillain the labial palp-pit organ ofthe
butterfly, Pieris rapae L. (Insecta:Lepidoptera).Cell
Tissue Res. 24O:333-342.
JuNe 1994
Mosetrrro Orncrony
Mclver, S. B. 1970. Comparative study of antennal
senseorgansoffemale culicine mosquitoes.Can. Entomol. 102:1258-1267.
Mclver, S. B. 1971. Comparative studieson the sense
organsand maxillary palps of selectedculicine mosquitoes. Can. J. Zool. 49:235-239.
Mclver, S. B. 1972. Fine structure ofthe pegson the
palps of female culicine mosquitoes. Can. J. Zool.
50:,571-576.
Mclver, S.B. 1973. Fine structureofantennal sensilla
coeloconica of culicine mosquitoes. Tissue & Cell
5 : 1 0 5 - 1l 2 .
Mclver, S. B. 1974. Fine structureofantennal grooved
pegsofthe mosqttito, Aedesaegyprl.Cell TissueRes.
153:327-337.
Mclver, S. B. 1975. Structure of cuticular mechanoreceptorsofarthropods. Annu. Rev. Entomol. 20:
381-397.
Mclver, S. B. 1982. Sensillaof mosquitoes(Diptera:
Culicidae).J. Med. Entomol. 19:489-535.
Mclver, S. B. 1985. Mechanoreception,pp. 7l-132.
In: G. A. Kerkut and L. I. Gilbert (eds.).Comprehensive insect physiology, biochemistry, and pharmacology, Volume 6. PergamonPress,Oxford.
Mclver, S. B. and C. C. Charlton. 1970. Studieson
the senseorgans on the palps of selectedculicine
mosquitoes.Can. J. Zool. 48:293-295.
Mclver, S. B. and R. Siemicki. 1975. Palpalsensilla
ofselected anopheline mosquitoes.J. Parasitol. 6l:
535-538.
Mclver, S. B. and R. Siemicki. 1976. Fine structure
ofthe antennal tip ofthe crabhole mosquito, Deinocerites cancer Theobald (Diptera: Culicidae). Int. J.
Insect Morphol. Embryol. 5:3 19-334.
Mclver, S. B. and R. Siemicki. 1978. Fine stnrcture
of antennal sensillacoeloconicaof adult Toxorhvnchites brevipalprs(Diptera: Culicidae). J. Med. Lntomol. 14:673-676.
Mclver, S. B. and R. Siemicki. 1979. Fine structure
of the antennal sensilla of male Aedes aegypti (L.).
J. Insect. Physiol. 25:21-28.
Mclver, S. B. and R. Siemicki. 1984. Fine structure
SeNsu-r-l
315
of pegs on the maxillary palps of adult Toxorhynchitesbrevipalpli Theobald (Diptera: Culicidae).Int.
J. InsectMorphol. Embryol. 13:l l-20.
Mclver, S. B. and R. Siemicki. 1985. Fine structure
of antennal putative thermo-/hygrosensillaof adult
Rhodniusprolixzs Stahl (Hemiptera: Reduviidae).J.
Morphol. 183:15J7.
Mercer, K. L. and S. B. Mclver. 1973. Sensilla on
the palps of selectedblackflies(Diptera: Simuliidae).
J. Med. Entomol. lO:236-239.
Omer,S.M. andM. T. Gillies. 1971. Lossofresponse
to carbon dioxide in palpectomizedfemale mosquitoes. Entomol. Exp. Appl. 14:251-252.
Roth, L. M. and E. R. Willis. 1952. Possiblehygroreceptors in Aedesaegypti (L.) and Blatella germanica (L.). J. Morphol. 9 I : l-14.
Rowley, W. A. and M. Cornford. 1972. Scanning
electronmicroscopyofthe maxillary palp of selected
speciesof Czllcoides.Can. J. Zool. 50:1207-1210.
Schmidt, K. and W. Gnatzy. 1972. Dre Feinstruktur
der Sinneshaareaufden Cerci von Gryllus bimacu/4tt$ (Saltatoria, Gryllidae). III. Die kurzen Borstenhaare.Z. Z,ellfor*,h. Mikrosk., Anat. 126:,206222.
Schoonhoven,L. M. 1967. Some cold receptors in
larvae ofthree lepidoptera species.J. Insect Physiol.
l3;82t-826.
Steward,C. C. and C. E. Atwood. 1963. The sensory
organs of the mosquito antenna. Can. J. ZaoL 4l:
577-594.
Sutcliffe, J. F., J. L. Shipp and E. G. Kokko. 1987.
ultrastructure of the palpal bulb sensilla of the black
fly Simulium arcticum (Dipteft: Simuliidae).J. Med.
Entomol. 24:324-331.
Tichy, H. 1987. Hygroreceptoridentiflcation and responsecharacteristicsin the stick insect Carausiw
morosus.J. Comp. Physiol.A 160:43-53.
Zachantk, R. Y. 1985. Antennae and sensilla,pp. l69. In: G. A. Kerkut and L. I. Gilbert (eds.).Comprehensive insect physiology, biochemistry and
pharmacology,Volume 6. PergamonPress,Oxford.