Chemoreception In Insects is the process of transmitting and perceiving information from the environment through chemical stimuli or signals; it is considered the most ancient way of intraspecific communication. Starting with the simplest reactions of unicellular organisms to attracting and repelling substances, in the process of evolution, complex chemical bonds have been developed that to a large extent ensure the appropriate behavior of animals in various situations. A huge variety of chemical compounds, their great importance as signals and means of communication between animals make chemoreception one of the most important factors in orienting an animal and in developing adaptations to changing environmental conditions.
In vertebrates, visual and auditory analyzers have gained the greatest importance in the process of evolution (although, for example, many mammals have a strong sense of smell). The system of communication in insects in the process of evolution developed along the path of improving chemoreception. As a result of the evolutionary process, which lasted for tens of millions of years, representatives of the insect class formed a special pheromone analyzer and pheromone communication system as a genetically fixed system for the chemoregulation of relationships between individuals of a species or individual populations. The functioning of the pheromone analyzer is closely connected with the central nervous system as a whole and is involved in the formation and manifestation of complex genetically fixed chains of behavioral acts – instincts (unconditionally reflex activity).
Thus, pheromone communication is one of the oldest ways of intraspecific communication; it is carried out by means of allocation into the external environment of biologically active substances – pheromones. Isolated pheromone is a kind of signal in which information is encoded using chemicals. Pheromone communication of insects is associated with the implementation of such vital tasks as meeting the opposite sex for mating, finding a place for egg laying, regulating nesting activity, stimulating egg laying, signaling about danger, marking the path to a discovered source of food, attracting to a suitable shelter, regulating the physiological state organism, etc.
The sender of the message and its recipient can be insects of both sexes. In the transmitter, by a certain selection of characters in accordance with the content of the transmitted message, it is encoded and a signal is sent that is convenient for transmission through a given communication channel, for example, by air. Pheromone glands and the corresponding behavior of the sender serve for this purpose.
In a pheromone signal, information is encoded using signs that can serve as the chemical structure of substances, various qualitative and quantitative combinations of these substances, their spatial and temporal placement in the environment. The signal is sent to the receiver via a communication channel; the channel may be the air where the insect is or is flying, or the substrate along which the insect moves. The communication channel may contain artificial or natural disturbances, such as structurally similar pheromones of other insect species, artificial chemicals, strong winds, rain, etc. a certain sequence. Chemoreceptors are most often located on antennas and in the area of the oral apparatus (external chemoreceptors) and inside the body of an insect (interchemoreceptors). The receiver decodes the signal and then processes it at the level of the central nervous system of the insect.
A separate sensilla is a morphologically isolated receptor organ consisting of different types of cells. An integral part of the chemoreceptor cuticle is its cuticular section, which closes the opening in the cuticle, where the processes of sensitive cells are suitable. Distinguish contact chemoreceptor sensilla, having one or two pores at the apex, and distant, with up to several thousand and even tens of thousands of pores. The different number of pores and their localization are due to different working conditions of the receptors. Contact sensilla is in contact with a source of pheromone whose molecules are located on some substrate, for example, on the leaves, body of the queen bee or queen of termites. Distant chemoreceptor sensilla traps pheromone molecules from the air, where their concentration is much lower than on the substrate.
All elements of sensilla are formed from hypodermal cells during embryonic development. The chemoreceptor sensilla is located mainly on the flagellum flagellum, playing a major role in the perception of odors, although they can also be located on the oral appendages, legs and other parts of the insect’s body.
The trichoid (thin, slightly curved hairs with a rounded apex), basonic (thin-walled hairs with a rounded apex), whole-conic (thin-walled cone located in the fossa and surrounded by cuticular spines), bell-shaped, styloconic (small cones, cylindrical process on the antenna), chetoid (powerful, strongly chitinized long hairs with a thin articulated membrane at the base), placoid (in the form of tubercles) and some other types of sen sill (Fig. 15). The most common are trichoid, basonic, placoid and coelonic sensilla.
The number of sensilla on insect antennae varies widely, and, as a rule, several types of sensilla are present on the antennae of the insect. Antheraea polyphemus Cramer males of the North American saturnia Antheraea polyphemus Cramer have about 66,000 sensilla on the flagellum , over 73,000 sensilla on the American cockroach Periplaneta americana L., and about 170,000 sensilla on males of the coddler Manduca sexta L.
In the peacock-eye butterflies of Artemis, six types of sensilla are located on the antennas, trichoid and basonic ones prevailing among them. At the same time, on the male’s antenna, there are about 12,000 trichoid thin-walled sensilla, which are absent on the antennae of the female. Six types of sensilla were also found on the antennas of butterflies of unpaired silkworms: two types of trichoid, basiconical, hetoid, coelonic and styloconic. The male of an unpaired silkworm has the number of trichoid sensilla on the antenna reaches 15,000, while the female has no more than 590. The antenna of the male silkworm has 19,000 trichoid sensilla and the female has 11,000. The male apple moth on the antenna has 5200 sensilla and the female has 3200. The number of placoid sensilla on the antenna of the working individual of the honey bee is 2260, while in the drone their number reaches 18 600.
The number of sensilla in insects with incomplete transformation changes when passing from one larval age to the next and then when molting into the adult. So, in the blood-sucking bug Rhodnius prolixus Stal. on the antenna of the larva of the first age there are 262 sensilla of six types, on the antenna of the larva of the fifth age – 848 sensilla, and on the antenna of the imago there are already 1668.
The distribution of sensilla on the antenna is uneven. So, at the base and at the top of the antenna of the male peacock-eye of Artemis, the density of arrangement of trichoid sensilla is 100 sensilla / 1 mm, in the middle sections – 120 sensilla / 1 mm, and they are absent in the last five or seven segments of the flagellum. In honey bees, sensilla are located on the last eight segments of the flagella of antennas; their number ranges from 260 to 300 sensilla per flagellum. The accumulation of sensilla of one type forms the so-called receptive field.
The composition of chemoreceptor sensilla includes from one to several tens of sensitive cells – neurons, and several specialized auxiliary cells.
A bipolar receptor cell (neuron) consists of three parts: the cell body and the peripheral and central processes. The central process, or axon, enters the central nervous system of the insect. Axons departing from the sensilla, without merging, form the nerve trunk. This forms the common nerve of the appendage: antennas, proboscis, etc. The peripheral process, or dendrite, enters the cuticular section of the sensilla. The body of the receptor cell is distinguished by the presence of a large nucleus surrounded by a relatively narrow layer of cytoplasm rich in organoids: mitochondria and Golgi apparatus evenly distributed throughout the body, granular endoplasmic reticulum, lysosomes, etc.
The peripheral process of the receptor cell and its body are surrounded by specialized auxiliary cells – wrapping and Schwann cells (see Fig. 16).
Trichogenic, inhibitory, and tecogenic cells belong to wrapping, but together they cannot always be identified. The inhibitory cell has an oval nucleus. Its cytoplasm contains a large number of mitochondria, elements of a smooth and especially granular endoplasmic reticulum, Golgi apparatus complexes, multivesicular and dense bodies. The surface of the trichogenic cell, bordering the vacuole, is covered with numerous microvilli, under which and in which there are many bubbles. The trichogenic cell secretes the liquid contents of the vacuole and maintains the constancy of its salt composition. The surface of the inhibitory cell also borders on the vacuole and is covered with numerous microvilli.
The Schwann cell has an elongated nucleus. Its cytoplasm contains mitochondria, membranes of smooth and granular endoplasmic reticulum, granules of different densities, numerous granules of glycogen. Both the nucleus and cytoplasm of the Schwann cell are characterized by high electron density.
The peripheral process of the receptor cell is enclosed in a dense cuticular sheath, called the scolopoid membrane (dendrite case). The shell consists of a homogeneous electron-dense material and forms the cuticular part of the sensilla.
The receptor cell of the insect chemoreceptor sensilla is primarily sensitive, i.e., it perceives the stimulus and generates a volley of impulses.
Its peripheral process has a ciliary structure, its proximal part is enlarged, and the distal one is narrowed and has the structure of the cilium, consisting of nine pairs of peripheral and sometimes one pair of central fibrils. The latter are then replaced by microtubules, which are diffusely distributed over the entire width of the peripheral process; between them clusters of small bubbles are sometimes found. At the base of the cilia in the cytoplasm of the peripheral process is clearly visible basal body, from which cross-striated roots depart.
Depending on the type of sensilla, the plasma membrane of the distal part of the peripheral process is directly adjacent to the pore ducts of the cuticular region or to filiform formations (filaments, cords) in its wall. However, if pore tubes or filamentary formations are absent, then the membrane is at some distance from the pore.
When pheromone molecules enter the chemoreceptor sensilla and pass through the pore membrane, they reach the dendrite in two ways: through the pore tubes of the distant receptors or through the receptor fluid surrounding the dendrite, both in distant and contact chemoreceptors (Fig. 17).
Since pheromone molecules (like other signaling substances) are hydrophobic (lipophilic) compounds, they must be put into a soluble state in order to reach receptors. This role is played by special proteins that are produced by inhibitory and trichogenic cells and then enter the cavity of the cuticular part of the sensilla filled with receptor fluid. The receptor fluid surrounding the dendrite contains ferromone-binding proteins, as well as proteins that bind other compounds. Most likely, these proteins can perform several functions at once: they are carriers of odor substances, perform the function of selective filters, and purify the receptor fluid by deactivating molecules of odor substances after signal transmission.
Binding proteins characterized by high specificity form soluble ligands (complex compounds of the protein and pheromone) with pheromone molecules, which diffuse from the receptor fluid into the membrane of the neuron dendrite.
Primary periodic factors, such as light and temperature, affect the perception of pheromones in the first place. Male bears Holomelina aurantiaca Htibner in nature are attracted by synthetic pheromone from 10 to 22 hours. Illumination and ambient temperature are the main factors that control, as described above, the perception of the sex pheromone of the queen bee uterus by working bees: in summer at maximum air temperature and the longest daylight hours the sensitivity of working bees to uterine pheromone is significantly higher than in autumn: the threshold dose of pheromone needed for arousal is two orders of magnitude lower.
The age of the insect also affects the ability to perceive pheromone. For newly emerged from the cells of hatching working bees, the uterus is not of interest and does not attract them. Starting on the 3rd day of life, their interest in the uterus increases. This may be due to the growth of sensillary distant chemoreceptors, that is, to the completion of their formation after the pupa is transformed into an imago, as well as the development of deutero-cerebrum neurons.
Male scoops of sulfur metallidid (Trichoplusia ni Hiibner) begin to respond to the female pheromone only on the 3rd day of life, and Icelandic scoops (Eichoa ochrogaster Guenee) on the 5th – 9th day after exiting the pupa. In males of unpaired silkworms, the maximum sensitivity to pheromone is observed on the 2nd-4th day of life.
Probably, common to many types of insects is that in a newly developed adult individual (imago) the pheromone analyzer is not fully developed and a certain time is needed for its final formation.
The change in the sensitivity of an insect to pheromones is also interconnected with its physiological state. For example, in the family of honey bees, working individuals on the 12-18th day of their life cease to be nurse bees and become flying collector bees. They cease to produce milk, and their sensitivity to uterine pheromone decreases.
Thus, two groups of factors can be distinguished that regulate the ability of pheromone perception to adult insects. The first group is the lighting modes (photoperiods) and ambient temperature rhythmically changing during the day or year; under their influence, the internal rhythms of pheromone perception are synchronized with environmental rhythms. The second group of factors is the age of the insect and its physiological state; under their influence, a pheromone analyzer develops, as a result, the insect acquires the ability to perceive a pheromone signal, or this ability decreases.
The regulation of perception of pheromone in insects is carried out in two stages. The first stage is the preparation for perception of pheromone of the corresponding body structures, the second stage is the launch of perception of pheromone.
The principles of regulation of pheromone excretion and its perception are the same, therefore both the sender of the pheromone signal and its recipient synchronously function in time.
The process of perception of a pheromone signal covers a number of behavioral acts. Initially, under its influence, the insect enters a state of excitation, after which it begins to move in the zone of the signal. If the signal is transmitted through air, then the insect flies, if the pheromone is applied to any surface, then the insect moves along it, passing through all the chemical constituent layers of the pheromone cloud – the “signs” of the signal. Having reached the sender of the signal, the insect stops. If the sequence of signs of the pheromone signal has been exhausted, the insect switches to the perception of signals of a different physical nature, if not, then it continues tracking until it is necessary.
In the behavior of the insect during the perception of the pheromone signal, three stages can be distinguished: excitation, movement in the direction of the pheromone signal and the delay at its sender.
Before considering each of the stages, attention should be paid to some features of the perception of the pheromone signal. A signal of any nature consists of signs, but the nature of the signs is different. For example, an audio signal propagates in space at a certain speed, and the entire sequence of characters reaches the recipient, regardless of whether it is stationary or mobile at the moment. Unlike a sound signal, a pheromone signal is not able to perceive a stationary insect. So, a motionless pheromone cloud, consisting of several substances, is for some time in still air or on a substrate. If the insect is at rest, then it can perceive only the sign of the pheromone signal, which can lead it to a state of excitement. For complete perception with the help of chemoreceptors of the whole signal, it is necessary to approach each of the signs of the signal, that is, movement is necessary. Thus, the behavior of the insect during the perception of the pheromone signal is associated with the simultaneous solution of two problems: “reading” the signal and searching for its sender. Moreover, the “reading” of the signal leads the recipient to the sender, which once again confirms the need for movement of the insect – the receiver of the signal. So, if a working bee, ready to perceive the pheromone of the uterus, moves along the honeycombs and meets the uterus, then in its behavior there are signs of arousal. Thus, the working bee becomes excited regardless of whether it entered the pheromone signal zone itself or fell under the influence of one of its elements in a stationary state. that is, movement is necessary. Thus, the behavior of the insect during the perception of the pheromone signal is associated with the simultaneous solution of two problems: “reading” the signal and searching for its sender. Moreover, the “reading” of the signal leads the recipient to the sender, which once again confirms the need for movement of the insect – the receiver of the signal. So, if a working bee, ready to perceive the pheromone of the uterus, moves along the honeycombs and meets the uterus, then in its behavior there are signs of arousal. Thus, the working bee becomes excited regardless of whether it entered the pheromone signal zone itself or fell under the influence of one of its elements in a stationary state. that is, movement is necessary. Thus, the behavior of the insect during the perception of the pheromone signal is associated with the simultaneous solution of two problems: “reading” the signal and searching for its sender. Moreover, the “reading” of the signal leads the recipient to the sender, which once again confirms the need for movement of the insect – the receiver of the signal. So, if a working bee, ready to perceive uterine pheromone, moves along the honeycombs and meets the uterus, then in its behavior signs of arousal are observed. Thus, a working bee becomes excited regardless of whether it entered the zone of the pheromone signal itself or fell under the influence of one of its elements in a stationary state. In this case, the “reading” of the signal leads the recipient to the sender, which once again confirms the need for movement of the insect – the recipient of the signal. So, if a working bee, ready to perceive uterine pheromone, moves along the honeycombs and meets the uterus, then in its behavior signs of arousal are observed.
Thus, a working bee becomes excited regardless of whether it entered the zone of the pheromone signal itself or fell under the influence of one of its elements in a stationary state. In this case, the “reading” of the signal leads the recipient to the sender, which once again confirms the need for movement of the insect – the recipient of the signal. So, if a working bee, ready to perceive the pheromone of the uterus, moves along the honeycombs and meets the uterus, then in its behavior there are signs of arousal. Thus, the working bee becomes excited regardless of whether it entered the pheromone signal zone itself or fell under the influence of one of its elements in a stationary state.
Similar reactions are observed in other insects. For example, if a male male silkworm (Anthereaea pernyi Guer.) Is released beyond the limits of the pheromone cloud, then it first performs a search flight. The behavior of a pheromone cloud that has flown in dramatically changes: from a chaotic flight, it goes on to a zigzag shape. Individuals in an active state pass into a dormant state faster than individuals in a dormant state. The males of many Lepidoptera exhibit similar behavioral reactions: raising antennas, fluttering wings, curving abdomen.
Females of many Lepidoptera emit an oblong pheromone cloud into the air. On such a cloud, males fly in a zigzag fashion. The pheromone traces left by the ants on their way to the source of food are long and narrow; the ants also move in zigzag patterns along them.
The working bee, which entered the zone of action of the pheromone signal of the uterus, immediately departs from it by more than 1 cm, that is, it leaves the radius of the signal, and then returns again, closer to the uterus. She makes several such inputs and outputs, gradually approaching the uterus. Schematically, this resembles the damped oscillations of a pendulum or a strongly squeezed sinusoid. If the uterus is removed from the bee family, then after some time the sensitivity of the working bee to the pheromone will increase and, accordingly, the radius of action of its pheromone signal will increase when the uterus returns to the family. And in this case, the working bee moves in a zigzag fashion, with the zigzags resembling a damped sinusoid.
The distance of action of the pheromone signal determines the shape of the zigzag motion of the insect. If the distance is small and measured in millimeters, then the effect of oscillations of the damping pendulum is manifested, if it is large, then the effect of the damped sinusoid is manifested. The oval-shaped pheromone signal is secreted not only by the queen bee, but also by some other insects. So, the radius of action of a pheromone of a female American cockroach is 30 cm, and at this distance you can observe the zigzag movement of the male or the effect of a damped sinusoid.
Chemoreceptors are known to have high sensitivity, that is, a low threshold of excitability. They can only perceive stimuli adequate in strength of their sensitivity.
The insect entering the pheromone cloud initially moves along the increasing concentration gradient of the outer layer of the cloud. But then, as the concentration of the substance increases, the receptors become unable to perceive it, otherwise a breakdown will occur, and therefore the insect seeks to leave the zone of the signal or this component of the pheromone signal.
At this moment, the receptors switch to the perception of another component of the pheromone signal, which has a low concentration in this place. The insect makes a turn and moves again along the increasing concentration gradient of the second component of the pheromone to a certain limit and again tends to leave its action zone when the concentration of the substance becomes suprathreshold and the insect is not able to perceive it. Then the second switching occurs, that is, the switching of receptors to the perception of the third component of pheromone, etc. Such a switching, which seems to occur in deutero-cerebrum, was called the principle of high-quality switching. Here again, the meaning of the complex composition of the pheromone signal and generally all pheromones should be emphasized: they always consist of several chemicals. Apparently, when an insect moves along a pheromone signal, each sign or group of signs that it meets prepares the receptor system for the perception of the next sign or group of signs. Thus, the individual components of the pheromone, by means of high-quality switching, transfer the receptor system to a new and new range of adequate and higher concentrations of stimuli and thereby ensure directed flight of the insect along the concentration gradient to the source of the pheromone signal. As a result of this, the insect instinctively performs a number of stereotypical movements, but in general, flexible execution of the program under certain conditions and achievement of the final goal is provided. Thus, the individual components of the pheromone, by means of high-quality switching, transfer the receptor system to a new and new range of adequate and higher concentrations of stimuli and thereby ensure directed flight of the insect along the concentration gradient to the source of the pheromone signal. As a result of this, the insect instinctively performs a number of stereotypical movements, but in general, flexible execution of the program under certain conditions and achievement of the final goal is provided. Thus, the individual components of the pheromone, by means of high-quality switching, transfer the receptor system to a new and new range of adequate and higher concentrations of stimuli and thereby ensure directed flight of the insect along the concentration gradient to the source of the pheromone signal. As a result of this, the insect instinctively performs a number of stereotypical movements, but in general, flexible execution of the program under certain conditions and achievement of the final goal is provided.
By the delay at the sender of the pheromone signal is meant the behavior of the insect in which the pheromone continues to act on the recipient when it has already reached the sender. During the delay at the source of the pheromone, the insect feels it with antennas, the bees can proceed to lick the pheromone with the tongue or eat it. In honey bees, working individuals feel the uterus with antennas, and then some of them begin to lick the pheromone from the surface of its body. The absorption of pheromone usually regulates a particular physiological process in the body of an individual detained at the source. In the family of honey bees, the uterine pheromone inhibits the development of egg tubes in the ovaries of working individuals. Experiments have shown that palpation can be direct (with touch) and indirect when the bee only brings the antenna closer to the uterus, but does not touch it. In this case, the bee changes the distance of the antennas to the body of the uterus with a variable frequency. Active at the moment are distant chemoreceptors. Indirect feeling becomes direct and vice versa. With direct palpation, contact antenna chemoreceptors are involved. Pheromone licking is usually called the process when a working bee, as it were, wipes the source of the pheromone proboscis. Upon a more detailed examination of this process, it was found that some bee suites actively secrete saliva, dilute the pheromone with it and absorb this mixture, therefore, practically no traces of its pheromone are found on the combs along which the uterus moves. Bee suites are young bees aged 3 to 9-12 days. In experiments it was found that all bees in the suite feel the uterus, and some of them also lick it.
In the body of a working bee, a pheromone licked from the body of the uterus undergoes a series of chemical transformations, and the products of these reactions presumably affect intestinal tract choheraceptors and are also absorbed through its walls and enter the hemolymph.
Uterine pheromone, getting into the hemolymph of the working bee, reduces the sensitivity of distant chemoreceptors to the queen bee pheromone and affects the endocrine and reproductive systems of the working bee, inhibiting the function of neurosecretory cells of the adjacent bodies, which entails the suppression of the development of egg tubes in the ovaries of the working bee.
As mentioned earlier, worker bees are immature females, but in the absence of a uterus, egg tubes capable of producing eggs begin to develop. Since working bees cannot mate with drones, since they do not have a copulative apparatus, they begin to lay unfertilized eggs – they turn into bee-minders. In order for the family of honey bees to function as a whole, continuous suppression of the activity of the adjacent bodies of the brain of working bees is necessary, which is achieved by licking the uterine pheromone. Licking the uterine substance, working bees receive much more pheromone than when feeling the uterus with antennas, that is, different doses of pheromone cause different behavioral reactions. Getting into the zone of action of the uterine pheromone, the bee initially receives a small dose of it, which causes an act of indirect feeling, then direct feeling, when the dose of the received pheromone increases, and finally, when the bee comes close to the uterus, a behavioral act of licking occurs during which it receives the largest dose of pheromone. Therefore, the dose of pheromone plays a significant role in organizing the behavior of the insect at the source of the pheromone. An increase in the dose of pheromone causes the connection in a strictly defined sequence of various chemoreceptors, which is accompanied by appropriate motor reactions and behavioral acts. Excitation of distant chemoreceptors of antennas causes the movement of the antennas and then the entire insect to the source of the pheromone; excitation of contact chemoreceptors of antennas with direct palpation entails the movement of the proboscis; excitation of the proboscis chemoreceptors causes it to stretch, followed by a behavioral act of licking; lysed pheromone or its metabolites cause excitation of interchemoreceptors and, in addition, affect the endocrine system of the insect in a humoral way, which affects its behavior and physiological state.
The pheromone analyzer is distinguished by a variety of sensing elements and multi-input. Inputs are connected according to a given program, in which the concentration gradient of pheromone components plays a large role. In order for the analyzer inputs to work in a wide range of concentrations, peculiar switches developed in the process of evolution. Their main functions are to switch the analyzer inputs to a new operating mode or to connect new inputs. Two types of switches are supposed to exist: qualitative and quantitative. Usually, at the beginning, when moving along a pheromone signal, high-quality switches are triggered, and when their capabilities are exhausted, quantitative ones are connected. Thus, due to multi-input and switching principle,