R. W. Glaser.
Evidence in Support of the Olfactory Function of the Antennæ of Insects.
Psyche 34:209-215, 1927.

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19271 Olfactory Function of the Antennae of Insects 209 EVIDENCE IN SUPPORT OF THE OLFACTORY
, FUNCTION OF THE ANTENNA OF INSECTS.=
1.
The Present Status of the Problem.
Investigators agree that chemotropism or the reaction of an .
animal to chemical stimuli plays a very important role in the biology of insects. Richardson (1) recently reviewed the ex- tensive literature on odor as a factor in the selection of places for oviposition and in the choice of food. Odor likewise assists insects in gathering material for their nests, in detecting mem- bers of their own or "alien" species, and in bringing the sexes together.
The assignment of the sense of smell to particular organs has been beset with great difficulties. Most histologists assign the olfactory sense chiefly to the antennae. On these organs sensillae are found in the form of pits, cones or plate organs which are morphologically of such a nature that a chemoreceptor function has been attributed to them. Similar sensillae may occur in other places, as on the maxillary and labial palpi, on the cerci and perhaps elsewhere, but they seem generally to be numericaJly greatest on the antenna Correlations between the number of antennal sensillse and the habits of certain insects have disclosed a number of facts. The antennae of Diptera that oviposit on putrid meat or feces harbor many olfactory pits whereas phyto- phagous forms possess few. Bloodsucking flies have many, as do those forms whose larvae are parasitic, such as Oestrids, Bomby- liids and Tachinids. The Hymenoptera possess enormous numbers of antennal sense organs. In male honey bees the number of plate organs has been computed at 30,000. In Odo- nata, large-eyed forms that prey on other swiftly moving insects, the number of antennal olfactory sense organs is small. Among those species where sexual dimorphism of the antennae exists, these organs are generally more fully developed in the males than in the females. This seems to be associated with the more 1From the Department of Animal Pathology of the Rockefeller for Medical Research, Princeton, N. J.




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210 Psyche [December
aggressive nature of the males and assists them to find the op- posite sex even at great distances.
Contributions on the habits of certain moths by Fore1 (2) and Riley (3) and the extremely interesting deductions made from careful observations on the life of ants by Fore1 (2), Wheeler (4), Lubbock (5)) Bethe (6)) Wasmann (7), Fielde (8), and others seem to demonstrate that the antennae serve as tactile and olfactory organs. The results of these investigators may be briefly summer up. They chiefly considered the behavior of insects when subject to various stimuli, such as the exploratory movements of the antennae when the creatures are searching for food or for proper places to lay their eggs; the antenna1 move- ments and subsequent behavior of insects when encountering members of their own or "alien" species; the part the antennae play when the animals are attempting to find their way to their nests and back to the forage supply; the trilling of the antennae .by males in the presence of females, etc. Experiments to prove the above contentions are not lacking. Fore1 showed that certain insects which appear to find their mates by smell are unable to do so when the antennae are am- putated. Kellogg (9) showed that when one antenna is removed from silkworm moths, they always turn towards the source of odor stimulation in the direction of the remaining antenna. Barrows (10) demonstrated that Drosophila is unable to respond to odors when the last segment of the antennae is removed. Von
Frisch (11) trained bees to come to an odorous food supply. When the antennae were amputated the bees could no longer find the food. In order to prove that this failure was not due to any general constitutional effects of the operation, he trained other bees to associate the food with a particular color. When the antennae of such bees were removed they promptly found the food. Minnich (12) in some experiments on the cabbage butter- fly found that the antennae were olfactory organs but not the only ones. Most of the experimenters referred to agree that some insects will still respond, but much more slowly, to odors after the antennae have been removed or coated with substances impermeable to volatile materials. This seems to show that ol- factory organs are also located in other regions of the body.



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19271 Olfactory Function of the Antennas of Insects 211 McIndoo (13) entirely discards the view that the antennae function as olfactory organs. This investigator has done much work on this subject and has experimented chiefly with beetles, bees and ants.
McIndoo considers the abnormal behavior of insects towards odor when the antennae are amputated, but thinks this is due to the fact that such insects are abnormal in their whole behavior. This is, of course, contrary to von Frisch's careful experiments and, if true, would apply equally to McIn- doo's own work.
Any animal that has been deprived of a sense organ will react abnormally with respect to a stimulation that affects this particular organ. McIndoo finds that olfactory pores exist in other regions of the body, especially at the bases of the wings and legs. When these pores are varnished over the insects respond much more slowly to odors than do those whose antennae are amputated. Kennedy (14) recently carefully weighed the evidence for and against the antennal sense of smell and thinks that while olfactory receptors undoubtedly do occur on other parts of the body, the experimental evidence against the older theory of an antennal sense of smell is insufficient. Judging from the literature, it seems that much substantial evidence exists in favor of the older theory. However, since roaches are exceedingly favorable material for a study of this question and furnish another rather lucid illustration in support of the older view, the writer feels prompted to report some observations. 2.
Observations and Experiments on Periplaneta americana. Periplaneta americana, the large American roach, carries two extremely long antennae on which occur the so-called olfactory cones. The maxillary and labial palpi of this species also bear sense organs which were, likewise, considered by Graber to function in the detection of odors. It was noticed by us that the antennae of starved roaches moved continuously when some odorous food was tendered but held at a distance to prevent contact. This then led to the performance of some further ex- periments which would demonstrate whether the antennae har- bored chemoreceptors. Full grown male and female roaches were placed in an atmosphere containing a slight amount of ether vapor. After a minute or two the insects began to behave



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in a curious manner. First one antenna was pushed down with the fore legs, caught near the base and rapidly passed through the mouth parts clear to the tip when it was released and the procedure repeated with the other antenna. This apparent cleaning of the antennae continued indefinitely, or until the animals became completely anaesthetized. The maxillary and labial palps were also frequently drawn through the mouth. The same reactions occured when carbon tetrachloride vapor or bro- mine was used. Two inert esters, ethyl acetate and amyl acetate (banana oil) produced identical reactions. The animals simply responded to these volatilized substances with their antennae and palpi. No other reactions occurred until the anaesthetic effect through the spiracles became noticeable. These experi- ments, it seems to us, signify that chemoreceptors are located on the
antennae and on the maxillary and labial palps. This, however, does not necessarily mean that these chemoreceptors are those of smell. The reactions obtained might very easliy represent merely the effect of violent chemical irritations such as the reaction of the human eye to onion oil or the reactions of the mucous membrane of the human mucosa to pollen particles. It seems unlikely, however, that two such inert substances as amyl and ethyl acetate could produce much irritation aside from ex- citing perhaps an obnoxious odor sensation in the insects. Never-
theless, insect sense organs are constructed differently from those of higher animals. Their surfaces, as pointed out by Kennedy, are often external and on long processes. They are also dry and
consequently the direct contact with a chemical stimulus, not first dissolved in mucous secretions, may explain the differences in behavior and the reason for the great sensitivity to such sti- muli. To meet the objection of simple chemical irritation and to prove that olfactory sensations are received through the antennae some additional experiments were performed. Two roaches with perfect antennae were segregated in an oblong cage having a glass top and a corked hole on each of two eri'ds. These holes were ordinarily used for the introduction of food and water. Another pair of roaches with their antennae amputated at the base was placed in a similar cage. Each cage was completely divided in half by a double layer of a fine mesh



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19271 Olfactory Function of the Antennas of Insects 213 copper screen, producing two compartments, one for the roaches the other empty. The roaches were then held for two days to permit the operated ones to recover from the effects of the am- putation. During this time they were given nothing but water in order to create an intense hunger. On the second day the insects seemed perfectly normal and a small piece of Roquefort cheese, for which these animals manifest a great fondness, was placed in the empty compartment one inch from the copper screen. In a few seconds the normal insects, which were huddled in a far dark corner, began to move their antennae and within two or three minutes one began to move over towards that part of the screen from which the cheese odor emanated. This one waved his antennae about near the cheese, but not being able to touch it soon returned to the corner. A little later the other roach followed the same maneuver. Both insects repeated this behavior three to four times. During the entire length of these operations, the roaches with amputated antennae gave no res- ponse and when they moved they progressed along the side op- posite the cheese which happened to be the darker side. During these tests both cages were held in the same position and at the same distance from the source of light. The cheese and the roaches were then removed and the cages washed thoroughly to remove all odors.
In a few days the roaches were again placed in their res- pective cages, and after the animals had been starved again for two days some Roquefort cheese was smeared on each cork plugging the hole of the compartment containing the insects. Within one to two minutes the normal roaches ran over to the soiled cork and ate off the cheese. The roaches with amputated antennae did not respond. After more than two hours they finally came across the cheese, waved their palpi and ate. It seems that the antennae receive smell impressions at considerable distances and that the maxillary and labial palps can only per- ceive an odor when the insects are in close proximity to the volatile substance. The antennae, maxillary and labial palpi were removed from another group of roaches. After recovery from the operation, and after the customary starvation, they had even greater difficulty in finding the cheese than those



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214 Psyche [December
roaches with simply the antennae amputated. They did not
perceive the cheese until it was placed under their mouth parts, when they carefully tasted it before eating. Another experiment appears significant. If the end of a stick is smeared with cheese and held at a distance of about one inch from the head of roaches with amputated antennae nothing occurs. When the same stick is held at the same distance from the head of the normal roaches the antennae follow the move- ments of the stick until they touch it, much like the pursuit of a magnet by a piece of iron. If one antenna is removed and the other left intact and the contaminated stick is held alternately on the right and left side of the head, the response occurs in about half the time on the unoperated side than on the other. Naturally cheese is not the only substance that produces the above reactions. Dog biscuit will cause an identical response in starved roaches, but more tardily due to the much slighter odor emanating from this food.
Roaches are gregarious animals and are often found huddled together in enormous numbers. These insects emit a strong species odor rather disagreeable to humans. This odor is probably responsible for their gregarious habit. During the course of our experiments, it was noticed that those insects with the antennae removed did not huddle as readily as was the case with the un- operated ones. After huddling the roaches with antennae were separated by disturbing them with a prod. In approximately one-half minute they were usually found together again. Those with amputated antennae remained separated until they accident- ally ran into one another.
All of the roaches operated upon are alive up to tlhe present (six weeks after the experiments). They behave perfectly nor- mally in so far as their appetite is concerned and the females have deposited several egg capsules. That they are abnormal with respect to the function of smell is a foregone conclusion, but it would certainly require a stretch of the imagination to assert that they were abnormal in all their behavior. 3. Conclusions.
Chemoreceptors are located on the antenrise, maxillary and labial palps of Periplaneta arnericana. The antennae are the most



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19271 Olfactory Function of the Antennae of Insects 215 efficient organs in detecting odor stimuli, especially from a dis- tance. This does not imply that olfactory organs do not exist elsewhere on the body.
4. Bibliography.
Richardson, C. H., The oviposition response of insects, U. S. Dept. Agric. Bull., No. 1324, 1925, 1. Forel, A., Sur les sensations des insectes, Rec. zool. Suisse, 1888, iv, No. 2.
.
Riley, C. V., The senses of insects, Nature, 1895, lii, 209. Wheeler, W. M., Ants, their structure, development, and behavior, New York, 1910.
Lubbock, J., Ants, bees and wasps, New York, 1883. Bethe, A., Durfen wir den Ameisen u. Bienen psychische Qualitaten zuschreiben? Pfluger's Arch., 1898, lxx, 15. Wasmann, E., Die psychischen Fghigkeiten der Ameisen. Zoologica, 1899, Heft 26.
Fielde, A. M., Further study of an ant. Proc. Philadelphia Acad. Nat. Sci., 1901, liii, 521.
Kellogg, V. L., Some silkworm moth reflexes, Biol. Bull., 1907, xii, 152.
Barrows, W. M., The reactions of the pomace fly, Dro- sophila arnpelophila Loew, to odorous substances, J. Exp. Zool., 1907, iv, 515.
Frisch, K. v., Ueber den Geruchsinn der Bienen, Zool. Jahrb., Abth. f. 2001. u. Physiol., 1919, xxxvii, 1. Minnich, D. E., The olfactory sense of the cabbage butter- fly, Pieris rape Leim, Journ. Exp. Zool., 1924, xxxix, 339.
McIndoo, N. E., The olfactory sense of the honey bee, Journ. Exp. Zool., 1914, xvi, 265; The olfactory sense of hymenoptera, Proc. Acad. Nat. Sci., Philadelphia, April, 1914; The olfactory sense of insects, Smith- sonian Misc. Coll., 1914, lxiii, 1; The olfactory sense of coleoptera, Bid Bull., 1915, xxviii, 407. Kennedy, C. H., Some non-nervous factors that condition the sensitivity of insects to moisture, temperature, light and odors, Annals Ent. Soc. America, 1927, xx 87.



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