Tasting with legs

By Dr. Stefan Pentzold

Imagine you could taste the ground as you are walking on. This would be quite unpleasant for most of us, such as in dirty walkways, muddy meadows or sweaty shoes. However, many insects rely on their legs, not only to move, but also to taste! Such a “tongue” on the legs enables insects to assess their food mainly by identifying substances that aren’t in the air and can therefore not be smelled the ‘normal’ way. Using their taste sensors on the legs, just walking over food tells hungry insects whether their next meal is safe or toxic.

 

Taste is important for insects and insects are important for humans

 

There are at least one million insect species on earth constituting more than half of all known living organisms. Most insects are plant-feeding and consume parts like leaves, fruits, roots, plant sap, pollen, seeds or wood. Such insect herbivores can be agricultural pests and vectors for human diseases, but many are also highly beneficial for humans due to pollination of many crop plants. Similar to humans and other animals, taste is of key importance for insect herbivores to identify and evaluate any potential food source. In addition, insects can also taste and evaluate mating partners and egg deposition sites. Thus, taste plays an essential role in the insect’s daily life for survival and reproduction. Surprisingly, relatively little is known about taste in insects, especially in comparison to smell. In the last years characterisation of taste or gustatory receptors (GR), as central unit for initial taste processing, has revealed remarkable insights that go beyond the identification of nonvolatile (not airborne) substances, e.g. detection of heat, light and carbon dioxide. Given that only a limited number of insect herbivore GRs has been characterized so far and some insects may harbor over different 100 GR genes, there is a huge potential for basic and applied research to unravel and exploit how GRs contribute to the survival of insect herbivores.

 

Making contact – with more than one tongue

 

In addition to the legs, also the antennae and the mouthparts of insects contribute to decoding food sources, i.e. they are covered with taste hairs (Figure 1). Taste hairs contain neurons that have GRs integrated into their cell membrane. Similar to legs, antennae and mouthparts need to get in contact with the food source in order to taste it. Therefore, taste is also called “contact chemosensation”, in contrast to smell a.k.a. distant chemosensation. This is due to the nature of the tastant substance that is usually nonvolatile, in contrast to smell defined by airborne substances. For us humans it means we have to bite into an apple to taste it, essentially with our tongue, the only organ for gustation among mammals.

 

Before feeding on a plant, insects explore its surface mainly by bringing taste hairs on legs, antennae or mouthparts into brief contacts. Insects may also take test bites or compress leaves to express small amounts of leaf sap. In all cases, the tastant substance diffuses into taste hairs (through the terminal pore) and reaches the GR in the interior. If it is the “correct” substance, binding with the GR generates a signal that is transmitted via nerve cells to the insect brain’s primary taste center, the subesophageal zone. Thus, the final check for the suitability of a plant as meal takes place in the brain that tells the muscles of the mouthpart “eat me!”. This story is getting even more interesting, when taking into account that GRs may also occur in internal body tissues such as the gut, brain or gonads where they probably act as nutrient sensor telling the insect “I’m hungry” or “I’m full”. Whether there is communication between internal and external GRs remains to be investigated.

 

Figure 1. (A) Taste hairs on the (fore)legs of the poplar leaf beetle, Chrysomela populi. (B) Adult beetles and (C) larvae specifically choose to feed on leaves of poplar (Populus spp.) that contain bitter-tasting salicin. Whereas salicin is a putative feeding stimulant for specialist C. populi, salicin deters many other insects from feeding on poplar. [© S. Pentzold, MPI Chem. Ecol.]

A Swiss army knife

 

Insects encounter a geographical and temporal mosaic of plant species. Consequently, they are exposed to many different substances with different chemical structures and characteristics. In order to recognize them, insects “tuned” their GRs accordingly, i.e. some GRs have a narrow spectrum of tastants they can recognize, while other GRs have broad a spectrum. Different tastants activate different GRs finally resulting in a unique neural pattern which is send to the brain. This scenario is similar to a Swiss army knife having a different number of tools for different tasks. Such an equipment of GRs is necessary because some tastants like sugars and amino acids are nutritious and beneficial, while other tastants are harmful. This is true for generalist insects (feeding on many different plant species) when consuming toxic plant substances. However, for specialists that feed on few plant species and are often adapted to these plant substances, the same tastants often stimulate feeding. Examples are the poplar leaf beetle eating salicin-rich poplar leaves (Figure 1) and the burnet caterpillars preferring plants rich in cyanogenic glucosides (Figure 2).

Single substances may also indicate a plant as suitable egg deposition site that needs to be recognized by females. One illustrative example in this respect is the butterfly Papilio xuthus. Females lay their eggs on citrus when they detect specific chemicals through their foreleg taste hairs while drumming on the leaf surface. Ozaki and colleagues found that female P. xuthus use a single GR that is specific for synephrine to distinguish citrus from other plants. They silenced the according taste gene PxutGr1, which strongly reduced taste sensitivity to synephrine and egg laying behaviour in response to synephrine.

 

 

Figure 2. The specialist caterpillar Zygaena filipendulae feeding on leaves of Lotus corniculatus that contain toxic and bitter-tasting cyanogenic glucosides. These larvae have overcome host toxicity and prefer feeding on Lotus plants with high levels of cyanogenic glucosides. [©S. Pentzold, MPI Chem. Ecol.]

A foretaste on the future of insect taste research

 

Studies on insect GRs gives us some idea of the abilities, remarkable complexity and importance of the insect taste system. However, only the tip of the iceberg is known so far. Surprisingly, it was found that honeybees, famous for their olfactory learning abilities, are not able to taste insecticides such as imidacloprid and are this not deterred by these nonvolatile toxins. Therefore bees cannot control imidacloprid exposure and intake during flower visit. In contrast, fruit flies are able to taste the insect repellent diethyltoluamide (DEET) by the action of three GRs resulting in the flies’ distaste towards DEET.

A better understanding why some tastant substances lead to feeding responses in some insect herbivores, but not in others, will largely benefit from characterizing GRs. Therefore, current advances of ultra-fast DNA sequencing techniques will lay the groundwork to identify more GRs, whereas elucidation of their actual function will likely benefit from combining molecular, chemical and ecological assays.

 

References:

Agnihotri, A., Roy, A. & Joshi, R. (2016). Gustatory receptors in Lepidoptera: chemosensation and beyond. Insect Molecular Biology 25, 519–529.

Bargmann, C. I. (2006). Comparative chemosensation from receptors to ecology. Nature 444, 295-301.

Benton, R. (2017). The neurobiology of gustation in insect disease vectors: progress and potential. Current Opinion in Insect Science 20, 19-27.

Chapman, R. (2003). Contact chemoreception in feeding by phytophagous insects. Annual Review of Entomology 48, 455-484.

Chapman, R. & Bernays, E. (1989). Insect behavior at the leaf surface and learning as aspects of host plant selection. Experientia 45, 215-222.

Kessler, S. C., Tiedeken, E. J., Simcock, K. L., Derveau, S., Mitchell, J., Softley, S., Stout, J. C. & Wright, G. A. (2015). Bees prefer foods containing neonicotinoid pesticides. Nature 521, 74-76.

Lee, Y., Kim, S. H. & Montell, C. (2010). Avoiding DEET through insect gustatory receptors. Neuron 67, 555-561.

Montell, C. (2013). Gustatory receptors: not just for good taste. Current Biology 23, R929-R932.

Orians, C. M., Huang, C. H., Wild, A., Dorfman, K. A., Zee, P., Dao, M. T. T. & Fritz, R. S. (1997). Willow hybridization differentially affects preference and performance of herbivorous beetles. Entomologia experimentalis et applicata 83, 285-294.

Ozaki, K., Ryuda, M., Yamada, A., Utoguchi, A., Ishimoto, H., Calas, D., Marion-Poll, F., Tanimura, T. & Yoshikawa, H. (2011). A gustatory receptor involved in host plant recognition for oviposition of a swallowtail butterfly. Nature Communications 2, 542.

Pentzold, S., Burse, A. & Boland, W. (2017). Contact chemosensation of phytochemicals by insect herbivores. Natural Product Reports 34, 478-483.

Reiter, S., Rodriguez, C. C., Sun, K. & Stopfer, M. (2015). Spatiotemporal coding of individual chemicals by the gustatory system. Journal of Neuroscience 35, 12309-12321.

Zhang, B., Zhang, W., Nie, R. E., Li, W. Z., Segraves, K. A., Yang, X. K. & Xue, H. J. (2016). Comparative transcriptome analysis of chemosensory genes in two sister leaf beetles provides insights into chemosensory speciation. Insect Biochemistry and Molecular Biology 79, 108-118.

Leave a Reply