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Gustation Across the Class Insecta: Body Locations

Article in Annals of the Entomological Society of America · February 2023

DOI: 10.1093/aesa/saac027

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https://doi.org/10.1093/aesa/saac027
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Gustation Across the Class Insecta: Body Locations

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Bethia H. King1, and Panchalie B. Gunathunga
Department of Biological Sciences, Northern Illinois University, DeKalb, IL 60115, USA and 1Corresponding author,
e-mail: bking@niu.edu

Subject Editor: Vonnie Shields

Received 5 July 2022; Editorial decision 28 November 2022

Abstract
This review summarizes which body parts have taste function in which insect taxa. Evidence of taste by mouth-
parts, antennae, and tarsi is widespread. Mouthparts that commonly have taste function are the labium,
including the labella and labial palps, the maxillae, including the galeae and maxillary palps, the inner surface
of the labrum or clypeolabrum of chewers, and inside the precibarium/cibarium of hemipterans, which have
piercing-sucking mouthparts. Tasting with mandibles has not been found, and tasting with the hypopharynx
is seldom reported. Use of the antennae appears uncommon among fly species, but common among species
of lepidopterans, hymenopterans, beetles, and bugs. Although tasting with legs, especially tarsi, is reported
mostly for fly and lepidopteran species, there is also evidence of it for multiple species of beetles, grasshop-
pers, and hemipterans, and one species of a roach, an ant, and a bee. Ovipositor taste function has been sup-
ported for some species of flies, lepidopterans, hymenopterans, orthopterans, and odonates. Taste by wings
has been much less studied, but has been documented in a few fly species. Taste remains unstudied for any
species or any body parts of Archaeognatha, Dermaptera, Mantodea, Mecoptera, Phasmatodea, Megaloptera,
Neuroptera, Phthiraptera, Psocoptera, Siphonaptera, as well as Raphidioptera, Strepsiptera, Embioptera,
Notoptera, and Zoraptera. Across holometabolous insects, larvae have not often been examined, the excep-
tion being some species of lepidopterans, flies, and beetles. Taste studies of antenna and legs are uncommon
for even lepidopteran and beetle larvae.

Key words: antennae, gustatory, mouthpart, ovipositor, tarsi

In humans, gustation versus olfaction is defined not only by the re-
sponse being to nonvolatile versus volatile compounds, but also by
the body part that detects the chemical, tongue versus nose. However,
some animals taste with parts of their body other than just their
mouthparts (Caprio et al. 1993). For example, some insects taste
with their tarsi as they walk on their food source prior to feeding
(Yarmolinsky et al. 2009). This may allow insects to more quickly
locate appetitive compounds and avoid aversive compounds (Scott
2018). In insects, the rough equivalent of human taste buds are taste
sensilla, which are often hair shaped. We tend to associate human
eyes, nose, mouth, and ear each with a different sensory function. In
insects, a given body part may have more than one of these sensory
functions. Insect maxillary palps and antennae are often referred to
as olfactory organs (Li et al. 2018, Oh et al. 2021), but their func-
tion varies among insect species. In larvae of the beetle Melolontha
melolontha L. (Coleoptera: Scarabaeidae), there appear to be not
only olfactory sensilla but also taste sensilla on the antennae, maxil-
lary palps, and labial palps (Eilers et al. 2012). Electrophysiological
tests show that the antennae of the beetle Chrysomela populi L.
(Coleoptera: Chrysomelidae) have taste function (Pentzold et al.
2019). The labium of the mosquito Anopheles gambiae (Diptera:
Culicidae) has both gustatory (Supp Table 1 [online only]) and ol-
factory function (Kwon et al. 2006). To date, olfactory receptor
proteins appear to be restricted to olfactory function, yet they are ex-
pressed not just on the antennae, but also on the nectar-sucking pro-
boscis and the legs of adults of the butterfly Heliconius melpomene
L. (Lepidoptera: Nymphalidae) (Briscoe et al. 2013).
Most recent reviews of insect taste focus primarily, or even ex-
clusively, on taste in one species, the common fruit fly, Drosophila
melanogaster Meigen (Diptera: Drosophilidae) (e.g., Scott 2018,
Toshima and Schleyer 2019, Chen and Dahanukar 2020, Montell
2021, Puri and Lee 2021, Komarov and Sprecher 2022). This is not
surprising because this species is by far the best studied. However,
there are more than a million species of insects, from about 23 other
orders, not just Diptera, and some are economically important.
Understanding insect taste is relevant to control of pest insects, e.g.,

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2 Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
when the control involves the insect eating the pesticide. Thus, nar-
ratives about insect taste need to incorporate what has been learned
about other insect species in the last 20+ years. For example, there
is information about which body parts D. melanogaster tastes with;
but what about other species? At least some flies and lepidopterans
taste with their feet, but is it all, and is it just these taxa? This review
compiles what body parts are used to taste by which insects. Thus, it
addresses questions such as: which parts of the mouth and digestive
tract are used? Do all insects use their antennae and legs? Are wings
commonly used? Do abdominal structures such as ovipositors and
male external genitalia ever have taste function? Do internal organs
other than the digestive tract taste?
This review also identifies areas that need further research. With
the recent emphasis on course-based undergraduate research experi-
ences (CURES) (Dolan 2016), it is worth noting that many taste
experiments are fun and feasible for undergraduates to do with ac-
curacy after fairly minimal training, e.g., projects on specific body
parts or specific taste hairs with a variety of tastants, e.g., different
sweeteners and bitter compounds like caffeine and quinine. Many
taste experiments are also cheap and safe, and they lend themselves
to getting undergraduates to really focus on and understand the
most important aspects of experimental design, e.g., controls and
testing blind (i.e., without knowledge of which test subject got which
treatment, to avoid inadvertently biasing the results).
Methods
References on insect taste were located by searching with Google
Scholar and the databases Web of Science and Scopus, until we were
no longer finding additional articles, by which point we had found
hundreds of articles. For each body part, we report which species
appear to have taste function, as well as the type of evidence: mor-
phological and neuroanatomical, behavioral, electrophysiological,
or molecular. Although some studies suggesting the absence of taste
in a body part have been included, it remains possible that taste func-
tion may later be demonstrated for those species. For example, elec-
trophysiological taste tests with the ovipositor of migratory locusts
were initially unsuccessful (Woodrow 1965) but have since been suc-
cessful (Gaaboub and Tousson 2010). Also, a body part may respond
to tastants that were not tested, or techniques of recording neural
responses may improve. There are also likely experiments in which
evidence of taste was not found, and the result was not published
because the authors were aware of biases against negative results
(Csada et al. 1996, Chouvenc et al. 2011).
For behavioral and electrophysiological evidence we required
that another sense, e.g., strictly tactile or olfactory, had been ruled
out as an alternative explanation. For example, imagine that a body
part is touched to different tastants or concentrations, and they elicit
different responses. All involve touch, so the difference in response is
likely not just mechanosensory. Differences in viscosity among solu-
tions are assumed to be inconsequential. If the chemical being tested
is not volatile that indicates gustation rather than olfaction.
For morphological evidence, some authors suggest gustatory
function based on a sensillum having a single terminal (apical or
subapical) pore (e.g., Zacharuk and Shields 1991, He et al. 2019,
Taszakowski et al. 2019). However, we required more evidence, be-
cause a single terminal pore might be strictly a molting (ecdysial)
pore, rather than the entry for tastants (Zacharuk et al. 1977), and
recognizing whether or not a pore is strictly used in molting is not
straightforward (Zacharuk et al. 1977; Faucheux 2012, 2017).
Also, some sensilla with a single terminal pore appear to have a
nongustatory function. Some appear to be mechanosensory, based
on the presence of only a single dendrite and that dendrite having
a tubular body (Chu-Wang and Axtell 1972, Singh and Singh 1984,
Rist and Thum 2017). Some seem to have hygro and/or thermal func-
tion, based on features such as location in a pit or the presence of
lamellated dendrites (Altner et al. 1978, Steinbrecht 1984, Schneider
et al. 2018). Thus, we suggest that gustatory function should not be
concluded until more evidence than a terminal pore is available, e.g.,
transmission electron microscope (TEM) images that show internal
features of the sensilla, behavioral tests, or electrophysiological tests.
Many gustatory sensilla have both taste and touch func-
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tion (Shanbhag et al. 2001, Sparks and Dickens 2017). However,
they are nevertheless called gustatory or taste sensilla or con-
tact chemosensilla or contact chemoreceptors (Isidoro et al. 1998,
Komendant 2011, Rebora et al. 2019). The published literature that
we read is consistent in assigning gustatory function when there is
a tubular body on one dendrite, which is indicative of that neuron
being mechanosensory (tactile), and at least one other neuron
without a tubular body. When that was not the case, we looked for
the sensilla being uniporous and no evidence that the function was
thermo- or hydro-sensory, olfactory, or strictly mechanosensory.
Evidence of temperature or humidity function includes being set in
a depression, lamellated dendrites, and/or the space at the tip of the
sensillum sometimes so filled with dendrites that no lymph is seen
(Steinbrecht 1984, Tichy and Kallina 2010, Schneider et al. 2018).
Olfactory function is usually concluded when the sensillum wall is
multiporous (Stocker 1994, Schoonhoven et al. 2005, Rebora et al.
2019, Sevarika et al. 2021, but see Ruschioni et al. 2012); there is
also often, but not always, extensive branching of dendrites (Sutcliffe
1994, Shanbhag et al. 1999). Evidence of strictly mechanosensory
function is one, rarely two, dendrites, each with a tubular body
(Dumpert 1972, Keil 1997).
Pharyngeal chemosensilla were assumed not to be olfactory based
on their location within the body where very little air movement is
expected. Pharyngeal chemosensilla were also assumed not to re-
spond to changes in humidity or temperature, because such function
seems like it would be more useful on the outside of an insect. Thus,
the presence of a single terminal pore, sometimes with evidence that
cobalt solution will pass through it, was considered sufficient to sug-
gest a taste function in pharyngeal chemosensilla (Zacharuk 1980).
Further evidence justifying these assumptions is needed.
Results and Discussion
Best-Studied Larvae
Generally, taste has been less well-studied for larvae than for adults
(Supp Tables 1–10 [online only]). However, taste has been very well-
studied in certain mouthparts of Lepidoptera larvae. Among cater-
pillars, evidence of taste function of the maxillary galeae’s sensilla,
i.e., of the lateral and medial styloconica, has been reported for
many species and from more than a dozen families (Supp Table 2
[online only], Schoonhoven and van Loon 2002, Shields and Martin
2012). These sensilla are especially well-studied because electro-
physiological recordings from them are relatively easy (Schoonhoven
and van Loon 2002). Some caterpillars also seem to taste with their
maxillary palps and their epipharynx (the underside of the labrum)
(Supp Table 2 and 4 [online only]).
Taste has also been studied in fly larvae, although not as ex-
tensively as in caterpillars. The head region of the larvae of D.
melanogaster, house flies, and some other flies, contains three pairs
of external chemosensory structures: the dorsal organ (DO), which
may be derived from the antenna segment; the terminal organ (TO),
which is also called the maxillary palp complex; and the ventral
Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
organ (VO), which may be derived from the mandibular segment
(Fig. 1 in Apostolopoulou et al. 2015, Hartenstein et al. 2018).
In some flies these organs are known to have gustatory neurons
(along with other types of sensory neurons) (Supp Tables 2, 3, and
5 [online only]). However, taste remains unexplored in most flies
with these three pairs of organs, e.g., Piophila casei (Linnaeus)
(Diptera: Piophilidae) (Sukontason et al. 2005), Parasarcophaga
dux (Thomson) (Diptera: Sarcophagidae), Chrysomya albiceps
Wiedemann (Diptera: Calliphoridae), and Cochliomyia macellaria
(Fabricius) (Diptera: Calliphoridae) (Mendonca et al. 2010, 2014).
Mouthparts and Digestive Tract
For an insect with chewing mouthparts, the labrum is positioned
like an upper lip, and its inner side is called the epipharynx Figure.
The labium is positioned like a lower lip or chin. Laterally are a
pair of mandibles (jaws) and then ventral to them is a pair of max-
illae. A hypopharynx is in the center, and is sometimes described as
tongue-like. There are two pairs of palps, the maxillary palps, and
the labial palps. In some insects, mouthparts have evolved from the
ancestral chewing parts into new forms, such as sucking, as in mos-
quitoes and hemipterans; sponging, as in house flies; and siphoning,
as in lepidopterans Figure. Given current evidence, it would be very
surprising if any insects are found to lack taste function in at least
some mouthparts in life stages that feed. The mouthparts for which
evidence of tasting has been reported most often are the labium,
including the labellum or labial palps, and the maxillae, including
the maxillary galeae and palps (Supp Tables 1 and 2 [online only]).
Taste function in labial parts has been found broadly taxonom-
ically (Supp Table 1 [online only]). Labial palps with taste func-
tion have been documented in species of: a mayfly naiad, a locust,
two roaches, two beetle larvae and an adult, a honey bee, an ant,
three moths, and three caddisflies. Taste function in other parts of
the labium, including the labellum, has been documented in even
more species: a roach, five true bugs/hemipterans, a thrips, a honey
bee, and almost 28 flies from 11 different families. In adult D.
melanogaster, the labellum is the only external mouthpart with taste
function, although there are taste sensilla within the proboscis (Chen
and Dahanukar 2017).
Tasting with parts of the maxillae also seems to be widespread
among insects (Supp Table 2 [online only]). In adult Lepidoptera
that feed, the maxillary galeae form their most obvious mouthpart,
the sucking, often coiled, proboscis. There is evidence of taste func-
tion of this proboscis in at least seven lepidopteran species from five
families. Taste sensilla can be found on the inside and outside of
this proboscis (Inoue et al. 2009, Faucheux 2013). As noted above,
evidence of taste function on the maxillary galeae has been demon-
strated in many species of caterpillars, with the caterpillars coming
from more than a dozen different families (Supp Table 2 [online
only], Schoonhoven and van Loon 2002, Shields and Martin 2012).
Evidence of taste function of the maxillary galeae has also been
documented for five species of beetles from three different families
and in five bee species from Apidae.
Evidence of taste function in the maxillary palps has been seen
in six caterpillar species from five different families, as well as in
species of: two damselfly naiads; three grasshoppers; one termite;
two roaches; two adult and two larval beetles; a honey bee; three
caddisflies from three different families; and some flies (Supp Table
2 [online only]). In D. melanogaster, taste appears to be absent in
adult maxillary palps (Singh and Nayak 1985), but present in the
larva’s terminal organs, which appear to develop from the maxillary
segment. Across all of the studies with Diptera, taste with the adult
maxillary palps is absent in four species and present in one; and taste
3
by the larva’s terminal organs is present in all four of the species that
have been examined. Taste function also appears to be absent in the
maxillary lacinias of adult green head horse flies and in the maxillary
stylets of the one hemipteran in which taste function of the maxillae
has been examined (Peregrine 1972).
A taste function is infrequently discussed for mandibles, but
appears to be absent in three species of hemipterans, a caterpillar
species, and adult mosquitoes (Supp Table 3 [online only]). We hy-
pothesize that taste sensilla are rare on mandibles because such
sensilla would have difficulty withstanding the considerable mech-
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anical force that mandibles are subject to. Mandibles of insets with
chewing mouthparts are sometimes subject to considerable stress
(Weihmann et al. 2015, Rühr and Blanke 2022). The mandibles of
hemipterans are modified into long thin stylets and also may experi-
ence more force than more interior mouthparts. In kissing bugs, the
mandibular stylets are exposed to force as they pierce through the
host’s outer surface, whereas the maxillary stylets enter a blood vessel
(Escandón-Vargas et al. 2017). Likewise, cotton strainers pierce the
seed coat with their mandibular stylets (Wang and Dai 2017). Larvae
of certain fly species have sensory organs called the ventral organs,
which have been hypothesized to develop from the mandibular seg-
ment (Hartenstein 1988, Cobb et al. 2009). A taste function has been
seen in the ventral organs of two of four fly species that have been
examined, in D. melanogaster and house fly larvae, but not in two
species of root fly maggots (Supp Table 3 [online only]).
Evidence of taste with other parts of the digestive tract also
exists. In sap sucking insects like aphids and other homopterans,
the hypopharynx and epipharynx join to make a precibarium and/
or cibarial pump, which are located in the base of the proboscis
and are described as being part of the pharynx or just anterior to
the pharynx (Ruschioni et al. 2019). Similarly, in flies with spon-
ging mouthparts, just anterior to the pharynx are the cibarial sense
organs and labral sense organs (Fig. 1 in Stocker and Schorderet
1981). Evidence of taste function in the precibarium or cibarium has
been shown in four families of Hemiptera; in two families of Diptera
(tsetse flies and a mosquito); and in a thrips species (Supp Table 4
[online only]). Whether the cibarial cavity of adult lepidopterans has
a taste function appears to be unexplored (Inoue et al. 2009, Krenn
2010), although, as noted, the maxillae that form a siphoning tube,
a proboscis, have taste function (Figure, Supp Table 2 [online only]).
Gustatory sensilla on the hypopharynx appear absent in mosquitoes
and in a horse fly species, both of which take liquid meals. However,
gustatory sensilla have been reported for a species of roach, which
has chewing mouthparts. Tasting with the labrum, epipharynx (the
internal surface of the labrum), or inner surface of the clypeolabrum
has been reported for a variety of insect species: two locusts, a ter-
mite, a roach, the cotton stainer bug, the larval stage of a beetle,
adults of four mosquitoes, and some, but not all, caterpillars (Supp
Table 4 [online only]).
Pharyngeal taste sensilla have been well-documented in adult D.
melanogaster (Chen et al. 2021). These sensilla lack a cuticular ex-
tension such as a hair; instead, there is just a pore in the cuticle (Fig.
1h in Chen and Dahanukar 2020). These sensilla respond to sweet,
bitter, acid, salt, and amino acids (Chen et al. 2019, 2021). Pharyngeal
taste sensilla also occur in the larval stage of D. melanogaster, where
they have been shown to respond to caffeine (Apostolopoulou et al.
2016).
Pharyngeal taste input in D. melanogaster helps them avoid
many aversive compounds (Chen et al. 2019). In D. melanogaster
adults, pharyngeal taste neurons respond to sucrose by inhibiting
feeding (Joseph et al. 2017), and nutritive-sugar sensors in the brain
also help limit overconsumption (Dus et al. 2015). Another benefit
4 Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
to taste receptors on body parts that are not initially exposed to food
sources is that not all aversive compounds are present in food before
ingestion. Some are breakdown products of digestion and bind to
receptor(s) on deterrent gustatory receptor neurons only after diges-
tion has begun (Wada-Katsumata and Schal 2021)..
Antennae, Legs, Wings, and Abdominal Structures
Apart from mouth parts, the body parts in which taste has been
most often documented are the antennae and tarsi (Supp Table 5
and 6 [online only]). Insect antennae are perhaps best known for
functioning in olfaction and touch. However, antennae also are used
to taste in a wide range of insect taxa, including naiads in three fam-
ilies of Ephemeroptera, three families of Blattodea, eleven families of
Hemiptera, eleven of Coleoptera (adults in eleven and larvae in one),
eight of Hymenoptera, and eight of Lepidoptera, as well as in one
family each of Zygentoma, Orthoptera, Thysanoptera, Plecoptera,
and Isoptera (Supp Table 5 [online only]).
Bernays and Chapman (1994) note that taste sensilla have not
been reported for caterpillars on body parts other than the mouth-
parts. However, since then; taste function has been demonstrated for
larval antennae of the maize stalk borer, Busseola fusca (Lepidoptera:
Noctuidae) (Juma et al. 2008). In Diptera, some larvae have clearly
identifiable antennae that are slender protrusions, and some have less
obtrusive paired structures called dorsal organs (DOs), which seem
to develop from the same segment of the body as typical antennae
do. Among larval flies, there is evidence of taste function of antennae
or DOs for 17 families (Supp Table 5 [online only]), but there is
evidence for a lack of taste function on the DOs in D. melanogaster
(Oppliger et al. 2000). Among fly adults, taste sensilla seem to be
absent in the antennae of most species that have been examined, in
yellow fever mosquitoes, a biting midge species, a tephritid species,
house flies, and one of two Tabanus (Diptera: Tabanidae) horse fly
species, as well as in at least parts of the antennae of D. melanogaster
(Supp Table 5 [online only]). However, taste sensilla have been docu-
mented in the antennae of some adult flies: a horse fly species in
Tabanus and two species of biting midges in Culicoides (Diptera:
Culicides). An absence of taste sensilla in antennae has been reported
not only for these flies, but also for a true bug nymph and for adult
males of a scale insect species (Supp Table 5 [online only]).
Tasting with the legs, especially the tarsi (Supp Table 6 [online
only]), is best known in Diptera, where it has been demonstrated in
ten families. Evidence for leg taste function has also been reported
in eight families of Lepidoptera, three families of Hemiptera, two
of Hymenoptera, and one of Orthoptera, Blattodea, and Coleoptera
(Supp Table 6 [online only]). In D. melanogaster adults, the tarsi
have more taste sensilla than do the better-studied mouthparts
(Vosshall and Stocker 2007, Ling et al. 2014). Male D. melanogaster
have more taste sensilla on their forelegs than do females. In
D. melanogaster (Joseph and Carlson 2015) and the butterfly
Heliconius erato (Linnaeus, 1758) (Lepidoptera: Nymphalidae)
(Silva et al. 2017), the three different pairs of insect legs do not re-
spond to the same tastants. An apparent lack of tarsal taste has been
reported for the harlequin bug and for a species of ladybird beetle
(Supp Table 6 [online only]). In the case of the ladybird beetle, the
tarsal sensilla appear to lack dendrites, and tarsal contact with su-
crose does not elicit a behavioral response, despite sucrose doing so
upon mouthpart contact (Yosano et al. 2020). We found no evidence
for or against the presence of taste function on legs of caterpillars.
Whether there are any entire insect orders without taste function in
the legs remains to be seen.
Tasting with wings has been reported for only three species of
insects (Supp Table 7 [online only]), each of which is in a different
fly family. Technical challenges in making electrophysiological re-
cordings from wing sensilla at least partly explain why taste func-
tion in wings has not been well-studied (Agnel et al. 2017). In D.
melanogaster; the anterior wing margins respond to sweet and bitter
molecules (Raad et al. 2016), bits of dead E. coli (Yanagawa et al.
2014), salts, and lipopolysaccharides (Yanagawa et al. 2019). The
desert locust, Schistocerca gregaria Forskål (Orthoptera: Acrididae),
may have chemoreceptors in its wings (Page and Matheson 2004),
but whether the responses to sucrose solution and to salt solution
were to the chemical per se versus to the contact that presentation of
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the solutions entails is difficult to distinguish.
Some evidence of taste has been reported for ovipositors in
six families of flies, five of Lepidoptera, five of Hymenoptera, two
of Odonata, and one of Orthoptera (Supp Table 8 [online only]).
Evidence of taste by the ovipositor is not strong for D. melanogaster
(Stocker 1994, Dweck et al. 2021), but has been documented with
electrophysiological and behavioral tests for D. suzukii (Matsumura)
(Biolchini 2016).
Taste by the male intromittent (copulatory) organ has been pro-
posed, but support is limited. An apparent single pore is seen in scan-
ning electron microscope (SEM) images of the ground beetle Carabus
fiduciarius Csiki (Coleoptera: Carabidae) (Kim and Yamasaki 1996)
and of the southern sickle bush cricket, Phaneroptera nana Fieber
(Orthoptera: Tettigoniidae), although uniporous sensilla appear
to be absent on the male intromittent organ of some other orth-
opterans (Faucheux 2012). Internal vaginal sensilla have been seen
in some damselflies, but are reported as mechanosensory (Córdoba-
Aguilar 2003, Cordero-Rivera 2017), with no vaginal taste sensilla
yet reported.
The cerci of a cricket species has taste function (Supp Table 8
[online only]), as do the cerci (anal/lateral leaflets/lobes) that are part
of at least some fly species’ ovipositors (Hooper et al. 1972, Rice
1976). Taste function has been documented on the upper surface of
the head of migratory locusts (Supp Table 9 [online only]), and mo-
lecular evidence suggests that it may occur on the thoracic surface of
D. melanogaster larvae (Cobb et al. 2009).
Well-Studied Species
For most orders for which there is some information on the location
of taste, only one or two body parts have been examined, although
there are about fourteen species with evidence of taste in four or
more body parts (Supp Table 10 [online only]). These well-studied
species are mostly lepidopterans and flies, but also two species of
orthopterans, a beetle, and adult honey bees. Drosophila seems to
be the most-studied insect with regards to which body parts have
taste function. For adult Drosophila there is evidence of taste func-
tion for the labellum, labrum, pharynx, tarsi, wings, and ovipositors,
and evidence of a lack of taste function for the maxillary palps and
antennae. For Drosophila larvae there is evidence of taste function
for the terminal organ (TO), ventral organ (VO), epipharynx, and
abdomen.
Conclusions
Tasting with feet is not restricted to species of flies and lepidop-
terans, but has also been reported for species of orthopterans, some
hemipterans, some adult beetles, a roach, a bee, and an ant. Most
insect species that have been tested appear to taste with their feet,
the exception being some, but not all, tsetse flies. Antennae have a
taste function in most species examined, the exception being some
flies. Taste function of wings is understudied but has been demon-
strated in a few flies. For each mouthpart except adult mandibles,
there is evidence of taste function in at least one insect species, but
Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
taste function has most consistently been reported for the labia, e.g.,
labellum and labial palps, and for maxillae. There is evidence of taste
function for the ovipositor in insects from several orders, although
surprisingly little such evidence for D. melanogaster. Similarly, evi-
dence of a taste function of male external genitalia is weak, and evi-
dence of a vaginal taste function is nonexistent.
Supplementary Data
Supplementary data are available at Annals of the Entomological Society of America
online.
Acknowledgments
Thank you to M. Abrahams, M. Muyizere, and E. Taylor for helpful com-
ments on an early draft, and to A. Nwawueze for assistance with reference
formatting. This research was supported by Northern Illinois University.
References Cited
Agnel, S., M. da Rocha, and A. Robichon. 2017. Transcriptome profiling of
neurosensory perception genes in wing tissue of two evolutionary dis-
tant insect orders: Diptera (Drosophila melanogaster) and Hemiptera
(Acyrthosiphon pisum). J. Mol. Evol. 85: 234–245. doi: 10.1007/
s00239-017-9814-8
Altner, H., H. Tichy, and I. Altner. 1978. Lamellated outer dendritic segments
of a sensory cell within a poreless thermo- and hygroreceptive sensillum
of the insect Carausius morosus. Cell Tissue Res. 191: 287–304. doi:
10.1007/BF00222425
Apostolopoulou, A. A., S. Kohn, B. Stehle, M. Lutz, A. Wust, L. Mazija, A. Rist,
C. G. Galizia, A. Ludke, and A. S. Thum. 2016. Caffeine taste signaling
in Drosophila larvae. Front. Cell. Neurosci. 10: 193. doi: 10.3389/
fncel.2016.00193
Apostolopoulou, A. A., A. Rist, and A. S. Thum. 2015. Taste processing
in Drosophila larvae. Front. Integr. Neurosci. 9: 50. doi: 10.3389/
fnint.2015.00050
Bernays, E. A., and R. F. Chapman. 1994. Chpt. 3. Sensory systems, pp. 61–94. In
Host-plant selection by phytophagous insects. Chapman and Hall, New York.
Biolchini, M. 2016. Role of labellar and ovipositor taste sensilla of Drosophila
suzukii in host recognition: a morpho-functional and behavioural ap-
proach. PhD, University of Cagliari, Italy.
Briscoe, A. D., A. Macias-Munoz, K. M. Kozak, J. R. Walters, F. Yuan, G. A.
Jamie, S. H. Martin, K. K. Dasmahapatra, L. C. Ferguson, J. Mallet, et
al. 2013. Female behaviour drives expression and evolution of gustatory
receptors in butterflies. PLoS Genet. 9: e1003620. doi: 10.1371/journal.
pgen.1003620
Caprio, J., J. G. Brand, J. H. Teeter, T. Valentincic, D. L. Kalinoski, J. Kohbara,
T. Kumazawa, and S. Wegert. 1993. The taste system of the channel cat-
fish: from biophysics to behavior. Trends Neurosci. 16: 192–197. doi:
10.1016/0166-2236(93)90152-c
Chen, Y. D., and A. Dahanukar. 2017. Molecular and cellular organization of
taste neurons in adult Drosophila pharynx. Cell Rep. 21: 2978–2991. doi:
10.1016/j.celrep.2017.11.041
Chen, Y. C. D., and A. Dahanukar. 2020. Recent advances in the genetic basis
of taste detection in Drosophila. Cell. Mol. Life Sci. 77: 1087–1101.
Chen, Y. D., V. Menon, R. M. Joseph, and A. A. Dahanukar. 2021. Control of
sugar and amino acid feeding via pharyngeal taste neurons. J. Neurosci.
41: 5791–5808. doi: 10.1523/JNEUROSCI.1794-20.2021
Chen, Y. D., S. J. Park, R. M. Joseph, W. W. Ja, and A. A. Dahanukar. 2019.
Combinatorial pharyngeal taste coding for feeding avoidance in adult
Drosophila. Cell Rep. 29: 961–973.e4. doi: 10.1016/j.celrep.2019.09.036
Chouvenc, T., N. -Y. Su, and J. K. Grace. 2011. Fifty years of attempted bio-
logical control of termites – analysis of a failure. Biol. Control 59: 69–82.
Chu-Wang, I. W., and R. C. Axtell. 1972. Fine structure of the terminal organ
of the house fly larva, Musca domestica L. Z. Zellforsch. Mikrosk. Anat.
127: 287–305. doi: 10.1007/BF00306874
5
Cobb, M., K. Scott, and M. Pankratz. 2009. Gustation in Drosophila
melanogaster, pp. 1–38. In P. L. Newland, M. Cobb and F. Marion-Poll
(eds.), Insect taste. SEB Experimental Biology Series, vol. 63, 2009/01/30
ed. Taylor & Francis, New York, NY.
Córdoba-Aguilar, A. 2003. A description of male and female genitalia and
a reconstruction of copulatory and fertilisation events in Calopteryx
haemorrhoidalis (Vander Linden) (Odonata: Calopterygidae).
Odonatologica. 32: 205–214.
Cordero-Rivera, A. 2017. Sexual conflict and the evolution of genitalia: male
damselflies remove more sperm when mating with a heterospecific female.
Sci. Rep. 7: 7844.
Downloaded from https://academic.oup.com/aesa/advance-article/doi/10.1093/aesa/saac027/7023662 by guest on 19 February 2023
Csada, R. D., P. C. James, and H. M. E. Richard. 1996. The ‘file drawer
problem’ of non-significant results: does it apply to biological research?.
Oikos 76: 591–593.
Dolan, E. L. 2016. Course-based undergraduate research experiences: current
knowledge and future directions, pp. 1–34. National Research Council
Commissioned Paper, Washington, DC.
Dumpert, K. 1972. Structure and distribution of sensilla on antennal flagellum
of Lasius fuliginosus (Latr.) (Hymenoptera: Formicidae). Z. Morphol.
Tiere. 73: 95.
Dus, M., J. S. Lai, K. M. Gunapala, S. Min, T. D. Tayler, A. C. Hergarden,
E. Geraud, C. M. Joseph, and G. S. B. Suh. 2015. Nutrient sensor in the
brain directs the action of the brain-gut axis in Drosophila. Neuron. 87:
139–151.
Dweck, H. K. M., G. J. S. Talross, W. Y. Wang, and J. R. Carlson. 2021.
Evolutionary shifts in taste coding in the fruit pest Drosophila suzukii.
eLife. 10: e64317.
Eilers, E. J., G. Talarico, B. S. Hansson, M. Hilker, and A. Reinecke. 2012.
Sensing the underground--ultrastructure and function of sensory organs
in root-feeding Melolontha melolontha (Coleoptera: Scarabaeinae) larvae.
PLoS One. 7: e41357. doi: 10.1371/journal.pone.0041357
Escandón-Vargas, K., C. A. Muñoz-Zuluaga, and L. Salazar. 2017. Blood-
feeding of Rhodnius prolixus. Biomédica. 37: 299–302. Doi: 10.7705/
iomedical.v37i3.3304
Faucheux, M. J. 2012. The structure of the male postabdomen and associated
sensilla of Phaneroptera nana Fieber 1853, and remarks on uniporous sen-
silla of genitalia (Orthoptera: Tettigoniidae: Phaneropterinae). Bull. Inst.
Sci. Sect. Sci. Terre. 34: 107–114.
Faucheux, M. J. 2013. Sensillum types on the proboscis of the Lepidoptera: a
review. Ann. Soc. Entomol. Fr. 49: 73–90.
Faucheux, M. J. 2017. Antennal sensilla of the armoured ground cricket,
Eugaster powysi Kirby, 1891 (Orthoptera, Tettigoniidae, Hetrodinae).
Bulletin de l’Institut Scientifique, Rabat. 39: 1–17.
Gaaboub, I., and E. Tousson. 2010. Electrophysiological responses of
the chemosensory sensilla on the ventral ovipositor valve of Locusta
migratoria to some electrolytes and non-electrolytes. In Proc. 6th Int. Con.
Biol. Sci. (Zool). 6: 477–483.
Hartenstein, V. 1988. Development of Drosophila larval sensory organs:
spatiotemporal pattern of sensory neurones, peripheral axonal pathways
and sensilla differentiation. Development. 102: 869–886. doi: 10.1242/
dev.102.4.869
Hartenstein, V., J. J. Omoto, K. T. Ngo, D. Wong, P. A. Kuert, H. Reichert, J. K.
Lovick, and A. Younossi-Hartenstein. 2018. Structure and development of
the subesophageal zone of the Drosophila brain. I. Segmental architecture,
compartmentalization, and lineage anatomy. J. Comp. Neurol. 526: 6–32.
doi: 10.1002/cne.24287
He, Z., Y. Luo, X. Shang, J. S. Sun, and J. R. Carlson. 2019. Chemosensory
sensilla of the Drosophila wing express a candidate ionotropic pheromone
receptor. PLoS Biol. 17: e2006619. doi: 10.1371/journal.pbio.2006619
Hooper, R. L., C. W. Pitts, and J. A. Westfall. 1972. Sense organs on the ovi-
positor of the face fly, Musca autumnalis. Ann. Entomol. Soc. Am. 65:
577–586. doi: 10.1093/aesa/65.3.577
Inoue, T. A., K. Asaoka, K. Seta, D. Imaeda, and M. Ozaki. 2009. Sugar re-
ceptor response of the food-canal taste sensilla in a nectar-feeding swal-
lowtail butterfly, Papilio xuthus. Naturwissenschaften. 96: 355–363. doi:
10.1007/s00114-008-0483-8
Isidoro, N., E. Bartlet, J. Ziesmann, and I. H. Williams. 1998. Antennal
contact chemosensilla in Psylliodes chrysocephala responding to
6 Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
cruciferous allelochemicals. Physiol. Entomol. 23: 131–138. doi:
10.1046/j.1365-3032.1998.232066.x
Joseph, R. M., and J. R. Carlson. 2015. Drosophila chemoreceptors: a mo-
lecular interface between the chemical world and the brain. Trends Genet.
31: 683–695. doi: 10.1016/j.tig.2015.09.005
Joseph, R. M., J. S. Sun, E. Tam, and J. R. Carlson. 2017. A receptor and neuron
that activate a circuit limiting sucrose consumption. eLife. 6: e24992.
Juma, G., M. Chimtawi, P. O. Ahuya, P. G. N. Njagi, B. Le Rü, G. Magoma, J. -F.
Silvain, and P. -A. Calatayud. 2008. Distribution of chemo- and mechano-
receptors on the antennae and maxillae of Busseola fusca larvae. Entomol.
Exp. Appl. 128: 93–98. doi: 10.1111/j.1570-7458.2008.00673.x
Keil, T. A. 1997. Functional morphology of insect mechano-
receptors. Microsc. Res. Tech. 39: 506–531. doi: 10.1002/
(SICI)1097-0029(19971215)39:6<506::AID-JEMT5>3.0.CO;2-B
Kim, J. L., and T. Yamasaki. 1996. Sensilla of Carabus (Isiocarabus) fiduciarius
saishutoicus Csiki (Coleoptera: Carabidae). Int. J. Insect Morphol.
Embryol. 25: 153–172. doi: 10.1016/0020-7322(95)00015-1
Komarov, N., and S. G. Sprecher. 2022. The chemosensory system of the
Drosophila larva: an overview of current understanding. Fly (Austin). 16:
1–12. doi: 10.1080/19336934.2021.1953364
Komendant, M. 2011. Antennal contact chemoreception in ground beetles
(Coleoptera: Carabidae). PhD, Estonian University of Life Sciences, Tartu,
Estonia.
Krenn, H. W. 2010. Feeding mechanisms of adult Lepidoptera: structure, func-
tion, and evolution of the mouthparts. Annu. Rev. Entomol. 55: 307–327.
doi: 10.1146/annurev-ento-112408-085338
Kwon, H. -W., T. Lu, M. Rutzler, and L. J. Zwiebel. 2006. Olfactory re-
sponses in a gustatory organ of the malaria vector mosquito Anopheles
gambiae. Proc. Natl. Acad. Sci. U. S. A. 103: 13526–13531. doi: 10.1073/
pnas.0601107103
Li, H., P. Wang, L. Zhang, X. Xu, Z. Cao, and L. Zhang. 2018. Expressions of
olfactory proteins in locust olfactory organs and a palp odorant receptor
involved in plant aldehydes detection. Front. Physiol. 9: 663. doi: 10.3389/
fphys.2018.00663
Ling, F., A. Dahanukar, L. A. Weiss, J. Y. Kwon, and J. R. Carlson. 2014. The
molecular and cellular basis of taste coding in the legs of Drosophila. J.
Neurosci. 34: 7148–7164. doi: 10.1523/JNEUROSCI.0649-14.2014
Mendonca, P. M., R. R. Barbosa, L. B. Cortinhas, J. R. dos Santos-Mallet,
and M. M. de Carvalho Queiroz. 2014. Ultrastructure of immature stages
of Cochliomyia macellaria (Diptera: Calliphoridae), a fly of medical and
veterinary importance. Parasitol. Res. 113: 3675–3683. doi: 10.1007/
s00436-014-4032-4
Mendonca, P. M., J. R. Dos Santos-Mallet, and M. M. Queiroz. 2010.
Ultramorphological characteristics of immature stages of Chrysomya
albiceps (Wiedemann 1819) (Diptera: Calliphoridae), a fly specie of fo-
rensic importance. Microsc. Res. Tech. 73: 779–784. doi: 10.1002/
jemt.20819
Montell, C. 2021. Drosophila sensory receptors—a set of molecular Swiss
Army Knives. Genetics. 217: 1–34. doi: 10.1093/genetics/iyaa011
Oh, S. M., K. Jeong, J. T. Seo, and S. J. Moon. 2021. Multisensory interactions
regulate feeding behavior in Drosophila. Proc. Natl. Acad. Sci. U. S. A.
118: e2004523118. doi: 10.1073/pnas.2004523118
Oppliger, F. Y., G. P. M, and M. Vlimant. 2000. Neurophysiological and be-
havioural evidence for an olfactory function for the dorsal organ and a
gustatory one for the terminal organ in Drosophila melanogaster larvae. J.
Insect Physiol. 46: 135–144.
Page, K. L., and T. Matheson. 2004. Wing hair sensilla underlying aimed
hindleg scratching of the locust. J. Exp. Biol. 207: 2691–2703. doi:
10.1242/jeb.01096
Pentzold, S., F. Marion-Poll, V. Grabe, and A. Burse. 2019. Autofluorescence-
based identification and functional validation of antennal gustatory
sensilla in a specialist leaf beetle. Front. Physiol. 10: 343. doi: 10.3389/
fphys.2019.00343
Peregrine, D. J. 1972. Some evidence of gustatory discrimination in the cotton
stainer Dysdercus fasciatus Sign. (Hem., Pyrrhocoridae). Bull. Entomol.
Res. 62: 211–214. doi: 10.1017/s0007485300047660
Puri, S., and Y. Lee. 2021. Salt sensation and regulation. Metabolites. 11: 175.
doi: 10.3390/metabo11030175
Raad, H., J. F. Ferveur, N. Ledger, M. Capovilla, and A. Robichon. 2016.
Functional gustatory role of chemoreceptors in Drosophila wings. Cell
Rep. 15: 1442–1454. doi: 10.1016/j.celrep.2016.04.040
Rebora, M., G. Salerno, and S. Piersanti. 2019. Aquatic insect sensilla: morph-
ology and function, pp. 139–166. In K. Del-Claro and R. Guillermo (eds.),
Aquatic insects: behavior and ecology. Springer International Publishing,
Cham, Switzerland.
Rice, M. 1976. Contact chemoreceptors on the ovipositor of Lucilia cuprina
(Wied.), the Australian sheep blowfly. Aust. J. Zool. 24: 353–360. doi:
10.1071/zo9760353
Rist, A., and A. S. Thum. 2017. A map of sensilla and neurons in the taste
Downloaded from https://academic.oup.com/aesa/advance-article/doi/10.1093/aesa/saac027/7023662 by guest on 19 February 2023
system of Drosophila larvae. J. Comp. Neurol. 525: 3865–3889. doi:
10.1002/cne.24308
Rühr, P. T., and A. Blanke. 2022. ForceX and forceR: a mobile setup and r
package to measure and analyse a wide range of animal closing forces.
Methods Ecol. Evol. 13: 1938–1948. doi: 10.1111/2041-210x.13909
Ruschioni, S., E. Ranieri, P. Riolo, R. Romani, R. P. P. Almeida, and N. Isidoro.
2019. Functional anatomy of the precibarial valve in Philaenus spumarius
(L.). PLoS One. 14: e0213318. doi: 10.1371/journal.pone.0213318
Ruschioni, S., R. Romani, P. Riolo, and N. Isidoro. 2012. Morphology and
distribution of antennal multiporous gustatory sensilla related to host rec-
ognition in some Trichogramma spp. Bull. Insectol. 65: 171–176.
Schneider, E. S., C. J. Kleineidam, G. Leitinger, and H. Romer. 2018.
Ultrastructure and electrophysiology of thermosensitive sensilla
coeloconica in a tropical katydid of the genus Mecopoda (Orthoptera,
Tettigoniidae). Arthropod Struct. Dev. 47: 482–497. doi: 10.1016/j.
asd.2018.08.002
Schoonhoven, L. M., and J. J. A. van Loon. 2002. An inventory of taste in cater-
pillars: each species its own key. Acta Zool. Acad. Sci. Hung. 48: 215–263.
Schoonhoven, L. M., J. J. A. van Loon, and M. Dicke. 2005. Insect-plant
biology, 2nd ed. Oxford University Press, Oxford.
Scott, K. 2018. Gustatory processing in Drosophila melanogaster. Annu. Rev.
Entomol. 63: 15–30. doi: 10.1146/annurev-ento-020117-043331
Sevarika, M., M. V. R. Stacconi, and R. Romani. 2021. Fine morphology of
antennal and ovipositor sensory structures of the gall chestnut wasp,
Dryocosmus kuriphilus. Insects. 12: 231.
Shanbhag, S., B. Müller, and R. Steinbrecht. 1999. Atlas of olfactory organs
of Drosophila melanogaster: 1. Types, external organization, innervation
and distribution of olfactory sensilla. Int. J. Insect Morphol. Embryol. 28:
377–397. doi: 10.1016/s0020-7322(99)00039-2
Shanbhag, S. R., S. K. Park, C. W. Pikielny, and R. A. Steinbrecht. 2001.
Gustatory organs of Drosophila melanogaster: fine structure and expres-
sion of the putative odorant-binding protein PBPRP2. Cell Tissue Res.
304: 423–437. doi: 10.1007/s004410100388
Shields, V. D., and T. L. Martin. 2012. The structure and function of taste or-
gans in caterpillars, pp. 147–166. In E. J. Lynch and A. P. Petrov (eds.), The
sense of taste. Nova Science Publishers, Inc., New York.
Silva, D. S., E. A. Barp, L. C. R. Kucharski, and G. R. P. Moreira. 2017. Sensing
the plant surface prior to feeding and oviposition: differences in external
ultrastructure and function among tarsi of Heliconius erato. Neotrop.
Entomol. 47: 85–95. doi: 10.1007/s13744-017-0508-0
Singh, R. N., and S. V. Nayak. 1985. Fine structure and primary sensory projec-
tions of sensilla on the maxillary palp of Drosophila melanogaster Meigen
(Diptera: Drosophilidae). Int. J. Insect Morphol. Embryol. 14: 291–306.
Singh, R. N., and K. Singh. 1984. Fine structure of the sensory organs of
Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int. J.
Insect Morphol. Embryol. 13: 255–273.
Sparks, J. T., and J. C. Dickens. 2017. Mini review: gustatory reception of
chemicals affecting host feeding in aedine mosquitoes. Pestic. Biochem.
Physiol. 142: 15–20. doi: 10.1016/j.pestbp.2016.12.009
Steinbrecht, R. A. 1984. Chemo-, hygro-, and thermoreceptors, pp. 523–553.
In J. Bereiter-Hahn, A. G. Matoltsy and S. K. Richards (eds.), Biology of
the integument. Springer, Berlin.
Stocker, R. F. 1994. The organization of the chemosensory system in Drosophila
melanogaster: a review. Cell Tissue Res. 275: 3–26. doi: 10.1007/BF00305372
Stocker, R. F., and M. Schorderet. 1981. Cobalt filling of sensory projections
from internal and external mouthparts in Drosophila. Cell Tissue Res.
216: 513–523. doi: 10.1007/BF00238648
 Annals of the Entomological Society of America, 2023, Vol. XX, No. XX
Sukontason, K., T. Chaiwong, F. Tayutivutikul, P. Somboon, W. Choochote, S.
Piangjai, and K. L. Sukontason. 2005. Susceptibility of Musca domestica
and Chrysomya megacephala to permethrin and deltamethrin in Thailand.
J. Med. Entomol. 42: 812–814.
Sutcliffe, J. F. 1994. Sensory bases of attractancy - morphology of mosquito
olfactory sensilla – a review. J. Am. Mosq. Control Assoc. 10: 309–315.
Taszakowski, A., A. Nowińska, and J. Brożek. 2019. Morphological study of
the labial sensilla in Nabidae (Hemiptera: Heteroptera: Cimicomorpha).
Zoomorphology. 138: 483–492. doi: 10.1007/s00435-019-00455-3
Tichy, H., and W. Kallina. 2010. Insect hygroreceptor responses to continuous
changes in humidity and air pressure. J. Neurophysiol. 103: 3274–3286.
doi: 10.1152/jn.01043.2009
Toshima, N., and M. Schleyer. 2019. Neuronal processing of amino acids in
Drosophila: from taste sensing to behavioural regulation. Curr. Opin.
Insect. 36: 39–44.
Vosshall, L. B., and R. F. Stocker. 2007. Molecular architecture of smell and
taste in Drosophila. Annu. Rev. Neurosci. 30: 505–533. doi: 10.1146/
annurev.neuro.30.051606.094306
Wada-Katsumata, A., and C. Schal. 2021. Salivary digestion extends the
range of sugar-aversions in the German Cockroach. Insects. 12: 263. doi:
10.3390/insects12030263
Wang, Y., and W. Dai. 2017. Fine structure of mouthparts and feeding per-
formance of Pyrrhocoris sibiricus Kuschakevich with remarks on the
specialization of sensilla and stylets for seed feeding. PLoS One. 12:
e0177209–e0177209. doi: 10.1371/journal.pone.0177209
Weihmann, T., L. Reinhardt, K. Weißing, T. Siebert, and B. Wipfler. 2015.
Fast and powerful: biomechanics and bite forces of the mandibles in the
View publication stats
7
American cockroach Periplaneta americana. PLoS One. 10: e0141226.
doi: 10.1371/journal.pone.0141226
Woodrow, D. F. 1965. The responses of the African migratory locust
Locusta migratoria migratorioides R. & F. to the chemical com-
position of the soil at oviposition. Anim. Behav. 13: 348–356. doi:
10.1016/0003-3472(65)90056-4
Yanagawa, A., A. Couto, J. C. Sandoz, T. Hata, A. Mitra, M. A. Agha, and
F. Marion-Poll. 2019. LPS perception through taste-induced reflex in
Drosophila melanogaster. J. Insect Physiol. 112: 39–47.
Yanagawa, A., A. M. Guigue, and F. Marion-Poll. 2014. Hygienic grooming is
induced by contact chemicals in Drosophila melanogaster. Front. Behav.
Downloaded from https://academic.oup.com/aesa/advance-article/doi/10.1093/aesa/saac027/7023662 by guest on 19 February 2023
Neurosci. 8: 254. doi: 10.3389/fnbeh.2014.00254
Yarmolinsky, D. A., C. S. Zuker, and N. J. Ryba. 2009. Common sense about
taste: from mammals to insects. Cell. 139: 234–244. doi: 10.1016/j.
cell.2009.10.001
Yosano, S., Y. Kutsuwada, M. Akatsu, S. Masuta, R. Kakazu, N. Masuoka,
K. Matsuda, and M. Hori. 2020. Taste recognition through tarsal
gustatory sensilla potentially important for host selection in leaf bee-
tles (Coleoptera: Chrysomelidae). Sci. Rep. 10: 4931. doi: 10.1038/
s41598-020-61935-x
Zacharuk, R. Y. 1980. Ultrastructure and function of insect chemosensilla. Annu.
Rev. Entomol. 25: 27–47. doi: 10.1146/annurev.en.25.010180.000331
Zacharuk, R. Y., P. J. Albert, and F. W. Bellamy. 1977. Ultrastructure and
function of digitiform sensilla on the labial palp of a larval elaterid
(Coleoptera). Can. J. Zool. 55: 569–578. doi: 10.1139/z77-072
Zacharuk, R. Y., and V. D. Shields. 1991. Sensilla of immature insects. Annu.
Rev. Entomol. 36: 331–354. doi: 10.1146/annurev.en.36.010191.001555