BIOLOGY OF REPRODUCFION 4, 309-326 (1971)

Semiochemicals-Structure and Function

F. E. REGNIER

Department of Biochemistry, Purdue University, Lafayette, Indiana Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 Received September 9, 1970

To appreciate the influence of the environ- they relate directly and indirectly to repro- ment on reproduction we must first consider duction. the nature of the environment and an ani- There are two major types of semiochemic mal’s response to it. The biotic community communication in nature; (1) between mem- is a dynamic system of interacting plant and bers of the same species (intraspecific com- populations. Few species are free munication), and (2) between different spe- from some sort of pressure from another cies (interspecific communication). Those species, whether it be in the form of preda- compounds that carry signals between mem- tion, competition for the same resources, or bers of the same species have been called parasitism. To maintain its place in an eco- “” (Karlson and Butenandt, system an organism must be able to com- 1959). Pheromones (Fig. I) are of two types, municate with its environment; i.e., it must releasers and primers. These two types of be able to sense physical and chemical stimuli pheromones are easily differentiated on the from the environment and respond to them. basis of the behavior of the receiver. When a In some cases this response consists of send- releaser is detected by an animal ing messages of its own to other organisms. an immediate behavior response occurs; or In the case of a prey, it must be able to sense behavior is said to be released. An example its predator and in some species defend it- would be a sex attractant produced by a self against the predator by the emission of a female which upon reception by a noxious odorant that “tells” it to desist. mature male immediately releases sexual In recent years, it has been found that behavior. The response of an animal upon organic compounds may be used to carry reception of a primer pheromone is delayed: messages between in nature. This is a Primer pheromones often induce physio- type of chemical communication for which I logical changes in an organism which ulti- propose the term “semiochemic communi- mately manifest themselves in a behavioral cation.” The word semiochemic is derived response sometime after initial pheromone from the Greek semeion (sign or signal) and reception. Blockage of ova implantation in chemeceia (aichemic). At the present time a female mice by the odor of an alien male is wide array of these signal-carrying com- an example of the action of a primer phero- pounds have been isolated, chemically char- mone. acterized, and synthesized. In addition, I Interspecific semiochemic communication propose the name “” for those is of two types: (1) that which adaptively chemical signal vehicles that carry informa- favors the emitter, and (2) that which is tion between organisms. are adaptively favorable to the receiver. Brown, clearly different from hormones and nucleic Eisner, and Wittaker (1970) have designated acids, since the latter two are used for chemi- those semiochemicals that evoke behavioral cal communication within an organism. It is or physiological changes in a receiving or- the purpose of this review to discuss the ganism that adaptively favor the emitter structure and function of semiochemicals as “allomones”. It is obvious that the noxious

309 310 REGNIER

Semiochemicois

Introspecies Interspecies Pherdmones Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 ReIesers Pri’mers AIIoriones Kairdmones

FIG. 1. Classification of types of chemical signal vehicles used to carry signals between animals in nature.

odor of the skunk is adaptively favorable to will be chosen for discussion because they the transmitter. On the other hand, the in- are unusual or illustrate a particular point I advertent release of specific compounds by wish to emphasize. As a consequence, ex- an animal that reveals it to a predator favors clusion of many excellent pieces of work will the receiver. Brown el a!. (1970) has desig- be necessary and by no means intentional. nated these semiochemicals that favor the I. FOOD AND HOST SELECTION receiver “kairomones”. It is apparent in nature that ecology and It is well known that organisms show reproduction of a species are intimately as- feeding preferences for different types of food sociated. The survival of a species is depend- (Schoonhoven, 1968). There is often little or ent on the development of sexually mature no relationship between the nutritional value adults that are capable of reproducing at a of food and its probability of being con- rate that will maintain or increase the popu- sumed. In many cases, this specific food lation. If we divide the life cycle of an or- selection has a chemosensory basis. An or- ganism into presexual and sexual phases, it ganism is able to orient spatially to its favor- is easier to isolate the effects of the environ- ite food by diffusible compounds that ema- ment and the different kinds of semiochemic nate from it. The type of signal vehicles in- communication used by organisms. During volved range from simple amino acids and the presexual or nonsexual stage of life, the sugars in the bacteria to more specific com- primary preoccupation of the organism is pounds such as those used in host selection survival. Animals must find food and shelter, in higher animals. avoid predators, defend themselves, and in Motile bacteria are chemotactic to a num- the case of animal societies maintain colonial ber of amino acids, sugars, and TCA cycle organization. The importance of the chemo- acids (Weibull, 1960). It has been shown by sensory channel to survival through food and Adler (1969) in a series of papers that this host selection, recruitment to food sources, chemotaxis is initiated by chemoreceptors alarm signaling, defense, and aggregation on the surface of the bacteria that are not will make up the first section of this paper. triggered by metabolism of compounds to The second section of the paper will deal which the bacteria show chemotaxis. Since specifically with sex pheromones, i.e., terri- many of the attractants are not metabolized, torial marking substances and sex attract- it is clear that chemotaxis is not dependent ants. on energy produced by the metabolism of the The amount of work done on semiochemic attractant. The general basis for chemore- communication in nature is indeed vast. I ception and chemotaxis has been established will therefore not attempt a complete dis- by the isolation of a series of E. coil chemo- cussion of the subject in this limited treat- tactic mutants. These mutants showed ment of chemical communication. Examples altered chemotaxis toward serine, aspartate, SEMIOCHEMICAL STRUCTURE AND FUNCTION 311 and galactose, but normal metabolism of new prey. Observations of Hydra feeding in the compounds. This supports the idea that this situation indicate that this does not there are specific chemoreceptors that trigger happen. Under these conditions a chemically chemotaxis upon reception of a specific controlled modification in the feeding be- attractant molecule. The isolation by Arm. havior occurs. The gastrovascular cavity con- strong (1969) of 40 motile mutants that are stricts locally just below the tentacles to seal not chemotactic to any of the normal attract- off the gut from the outside medium during Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 ants suggests that the mutants are defective mouth opening. As soon as the new prey is at some stage beyond chemoreception. ingested and the mouth closes, the constric- It is also possible that microorganisms use tion disappears and the food is dropped into chemotaxis for more than the selection of the gut (Fig. 2). Blanquet and Lenhoff (1968) simple nutrients. Recent studies have indi- have found that this modified feeding re- cated that microorganisms may be predatory sponse is controlled by the interaction of an and parasitic on other species of microor- ectodermal receptor for glutathione and an ganisms and that this predation and para- endodermal receptor system for tyrosine. In sitism is an important factor in maintaining the situation where the Hydra is fasted when the balance of microflora in nature (Mitchell, it encounters prey, the concentration of tyro- 1970). Prey and host selection in many cases sine at the endodermal receptors will be low appears to occur by techniques other than by while the concentration of reduced gluta- chance encounter between organisms. It is thione at the ectodermal receptors will be not unlikely that cases will be found where selection is on the basis of the emanation of kairomone(s) from a prey or host. External chemical stimuli are also impor- tant in the feeding behavior of Hydra. When prey brush against the tentacles of the Hydra, spearlike nematocysts are discharged into the body of the prey. Loomis (1955) discovered that nematocyst discharge into a suitable prey is followed by a coordinated feeding reaction in which the mouth is opened and the tentacles move to the mouth with the A B prey. It was found that this feeding reaction is controlled by reduced glutathione that is released from the body of the prey when its skin is punctured. Since Hydra only feed on C prey that release glutathione after nemato- cyst puncture, its feeding is confined to Nemathelminihes and higher phyla. Cani- balism does not occur in Hydra because they do not produce reduced glutathione. Because feeding in Hydra is discontinuous, new prey are often captured before previ- ously captured prey are digested. Since the gastrovascular cavity is a tubular sack with H a mouth at one end, undigested food should FIG. 2. Modified feeding response of Hydra leak out when the mouth is opened to receive (Blanquet and LenhoiF, 1968). 312 REGNIER

above lO_6 M. Thus a fasted Hydra will been shown where hematophagous exhibit a feeding response without neck con- are either attracted to CO2 (Garcia, 1962; striction. As digestion proceeds, the concen- Fallis and Smith, 1964; Nelson, 1965; tration of tyrosine at the endodermal recep- Thomspon, 1967; DeFoliert and Morris, tors steadily increases. In the event that new 1967; Gouck and Bowman, 1959; Gouck prey is encountered, the Hydra will undergo and Gilbert, 1962) or it acts synergistically

the modified feeding response. This occurs with other compounds. Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 anytime that both the endo- and ectodermal II. FOOD GATHERING receptors are bing stimulated simultaneously. Numerous examples of food and host For social insects it is very important that selection may also be found in insects. The newly discovered food sources be exploited beetle Atemeles publicollis has been shown to as quickly as possible before competing live as a guest in ant colonies during its life species find the food (Lindauer, 1967). The cycle. Soon after hatching in the nest of evolution of efficient recruiting systems as- Formica polyctena the beetle migrates to the sures that this will be the case. Probably the nest of its second host, Myrmica Iaevinodis, most familiar example of recruitment to a where it hibernates. Since the Myrmica nest source of food in insects is that of the bee. may be some distance from that of the Von Frisch (1950) and Lindauer (1967) have Formica nest, the question of how the beetle over the course of many years demonstrated finds the second host arises. In laboratory the intricacies of this system. The returning experiments, Holldobler (1969) has found forager, who has found a good food source, that the beetle orients in air currents that can communicate to her fellow workers the carry the odor of the Myrmica host. Adop- quality of the food, its distance, and direc- tion behavior in Myrmica is released by tion from the hive by means of a dance on compounds that are secreted by dorsally the interior of the hive. Even though the food located integumental gland cells in the ab- source may be hundreds of meters from the dominal segments of Atemeles. After hiber- hive, workers are directed to within a few nation, Atemeles leaves the Myrmica nest meters of the food find. If the vegetation at and returns to the Formica nest by the use of the food source is dense, it is still difficult to chemical clues, and thus the life cycle starts find the food. Fine navigational corrections over. of this type are achieved with the Nasanoff The orientation of blood-feeding insects to gland. The forager usually marks the source their host also appears to be a case of chemo- with the odorous contents of this gland. sensory orientation. In studies on human Boch and Shearer (1964) and Shearer and attractiveness to mosquitoes (Khan, Mai- Boch (1966) have found the contents of this bach, Strauss, and Fischer 1969), it was gland to be geraniol, neral, geranial, and found that physical exercise made individuals geranoic acid (Table 1). more attractive to mosquitoes. Acree, Tur- The more primitive stingless bees of the ner, Gouck, Beroza, and Smith (1968) have subfamily Meliponini on the other hand do identified L-lactic acid as the major attractive not recruit workers with the dance. Alternate component from human sweat that is at- techniques are used. Trigona droryana scouts, tractive to female yellow fever mosquitoes, for example, establish scent posts on the Aedes aegypli. However, the presence of CO2 vegetation every few yards that lead novices is essential for attraction. The response of to a feeding station (Lindauer, 1967). It is mosquitoes to both compounds together is apparently the secretion of the well-devel- 65 times greater than the sum of their in- oped mandibular gland that is used by this dividual activities. A number of cases have species for recruitment. SEMIOCHEMICAL STRUCTURE AND FUNCTION 313

It appears that terrestrial social insects TABLE 1 also rely heavily on chemical clues to recruit RECRUITING PHEROMONES other members of the society to a food Compound Insect Reference source. Wilson (1962) has shown that the imported fire ant (Solenopsis saevissima) lays Geraniol Honeybee Boch and a trail between its nest and a food source by Apis inellifera Shearer

extruding its sting and depositing the mate- (1964) Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 Geraniol rial from the Dufour’s gland on the trail. Honeybee Shearer and Apis mellifera Boch (1966) Hangartner (1969) later showed that the Neral Honeybee Shearer and closely related species Solenopsis geminata is Apis mellifera Boch (1966) able to communicate food quality by the Geranoic acid Honeybee Boch and type of trail a forager lays when it is return- Apis mellifera Shearer ing to the nest from a food source. This is (1964) Nerolic acid Honey bee Boch and done by controlling the sting pressure on the Apis mellifera Shearer ground and presumably the amount of trail (1964) pheromone deposited. Hexanoic acid Termite Hummel and The mechanism for laying trails and the Zootermopsis Kar Ison glandular origin of trail marking chemicals ize vadensjs (1968) cis, cis, trans,- Termite Matsumura, varies considerably among terrestrial or- 3,6,8-Dode- Ret iculitermes Coppel, ganisms. The above example was one of catrien-i -ol” flavipes and Tai sting trail laying using the contents of (1968) Dufour’s gland. The ant Acanthomyops “This compound was isolated from fungus- interjectus lays odor trails that consist of infested wood and not demonstrated unequivo- small droplets of hind gut contents that are cally to be the natural pheromone of the termite. released by intermittently pressing the tip of the abdomen against the substrate (Hangart- and synthesis of a trail pheromone for ner, 1969). Crematogaster ashmeadi on the Reticulitermes flavipes. They were aided in other hand releases its trail substance from a these studies by the discovery that wood gland in its leg that exudes trail substance as decayed by the fungus Lenzites trabea pro- the ant stretches its leg out behind it (Leut- duces a substance that is attractive to these hold, 1968). At the present time none of termites (Esenther, Allen, Casidic, and Shen- these compounds has been identified. feldt, 1961). Analytical data obtained from Termites appear to be equally adept at the fungal pheromone and the natural ter- odor trail recruitment (Luscher and Muller, mite pheromone led them to conclude that 1960; Stuart, 1963, 1964). The first isolation the two compounds were very similar, if not of a termite trail pheromone was achieved by structurally identical. In the three cases of Moore (1966) using Nasutitermes exitiosus. termite trail laying discussed above, the trail The pheromone was characterized as an pheromone was secreted by sternal glands in unsaturated diterpenoid hydrocarbon, C20H32, the abdomen of the termite (Stuart, 1963, with one ring and four isolated double bonds. 1964). Hummel and Karlson (1968) later estab- III. ALARM COMMUNICATION lished the structure of the principle trail sub- stance of Zootermopsis nevadensis as hexa- Alarm pheromones have been observed in noic acid and by so doing achieved the first a wide distribution of organisms. However, identification of a trail pheromone. Within the greatest number of cases is to be found in several months Matsumura, Coppel, and the social insects. The reason for this is prob- Tai (1968) reported the structure (Table 1) ably that the social insects live at high enough 314 REGNIER

population densities to make chemical com- citronellal. Chadha, Eisner, Monro, and munication of alarm efficient. A large num- Meinwald (1962) have shown that the man- ber of compounds has been found to function dibular glands of this insect produce citro- as alarm substances in insects as will be seen nellal, neral, and geranial. This insect pro- in Table 2. Rather than try to consider all of duces as much as 0.2% of its body weight of these alarm pheromones I will choose what these compounds. Ghent (1961) showed that

I consider to be a few characteristic systems. these terpenoid compounds function as both Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 When the ant Acanthomyops c!aviger is alarm and defense substances. Citronellal alarmed, one smells the characteristic odor of serves as a repellent and also enhances the

TABLE 2 ALARM PHEROMONES

Compound Insect family Reference

Undecane Formicinae Regnier and Wilson (1968) Tridecane Formicinae Regnier and Wilson (1968) Pentadecane Formicinae Regnier and Wilson (1968) Heptan-2-one Hymenoptera, Dolichoderinae Morse, Shearer, Bach, and Benton (1967), Shearer and Boch (1965), Blum, Monroe and Chidester (1963). Blum, Warter, and Trayn- ham (1966) Blum (1969) Nonan-2-one Hymenoptera BIum (1969) Tridecan-2-one Formicinae Regnier and Wilson (1968) 2-trans-Hexen-l -al Myrmicinae Bevan, Birch, and Caswell (1961) Isoamyl acetate Hymenoptera Morse, Shearer, Boch, and Benton (1967), Bach, Shearer, and Stone (1962) 4-Methylhexan-2-one Dolichoderinae Cavill and Hinterberger (1962), Blum (1969) 2-Methy-2-hepten-6-one Dolichoderinae Cavill and Hinterberger (1960), Cavill, Ford and Locksley (1956), Cavill and Ford (1953), Casnati, Pavan, and Ricca (1964), Trave and Pavan (1956) 2.Methylheptan-4-one Dolichoderinae Trave and Pavan (1956) 4-Methylheptan-3-cne Myrmici nae Blum, Padovani and Amante (1968), Moser, Brownlee and Silverstein (1968), McGurk, Frost, Eisenbraun, Vick, Drew and Young (1966) Octan-3-one Myrmicinae Crewe, Brand, Fletcher and Eggers (1970) 2, 6-Dimethyl-5-hepten-1 -al Formicinae Regnier and Wilson (1968) 2, 6-Dimethyl-5-hepten-1 -01 Formicinae Regnier and Wilson (1968) Citronellal Formicinae Regnier and Wilson (1968), Ghent (1961) Citral Formicinae, Hymenoptera Regnier and Wilson (1968), Blum (1966), Moore (1964) a-Pinene Isoptera Moore (1964) Terpinolene ISoptera Moore (1968) Limonene Isoptera, Myrmicinae Moore (1968), Quilico, Grunanger, and Pavan (1960) SEMIOCHEMICAL STRUCTURE AND FUNCTION 315

penetration of the formic acid defense secre - many cases mixed with the insects’ venom. tion of this species. There appears to be some correlation be- The Dufour’s gland of this species also tween molecular shape and alarm pher- serves in an alarm-defense capacity (Regnier omone specificity, although it is much less and Wilson, 1968). When this species stings rigid than sex pheromones. For a synthetic another insect it discharges the contents of compound to be active as an alarm pher-

its venom gland (formic acid) and Dufour’s omone it must have approximately the same Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 gland (a mixture of hydrocarbons) simul- volatility as the natural pheromone, have a taneously through a common duct. By so molecular weight of 100-200 (Bossert and doing an emulsion is formed that spreads Wilson, 1963) and have the same general over a large surface area. As the undecane molecular shape (Blum, 1969). An interest- evaporates into the air it alarms other mem- ing example of the importance of molecular bers of the species in the vicinity. It has been shape may be found in the report by Blum determined that the alarm threshold con- (1969) on the response of Iridomyrmex centration in A. claviger for citronella! and pruinosis to analogs of its alarm pheromone, undecane is approximately 1012 and 1012 2-heptanone. n-Butyl acetate has higher molecules/cm3 of air, respectively. alarm pheromone activity than the chemical The formicine ant Lasius alien us, on the homolog 2-octanone in this insect apparently other hand, produces essentially the same because the molecular shape of the ester is compounds with the same glandular dtstri- more nearly like that of 2-heptanone. bution except that the terpene concentration When the earthworm Lumbricus lerresiris in the mandibular glands is much lower, and is touched or handled roughly, it secretes a its alarm threshold concentration for un- large quantity of mucus material over the decane is essentially 100 times lower (Regn- full length of the body. Electrical shock and ier and Wilson, 1969). Alarm communica- strong chemicals also induce this response. tion in L. alienus differs from A. ciaviger in Ressler, Cialdini, Ghoca, and Kleist (1968) two respects: (1) alinus workers run more have reported that this secretion in fact rapidly and orient less to the odor source, contains an alarm substance. Worms that and (2) they have lower response thresholds were given a 0.15-mA shock of a I-sec to undecane. These differences result in duration every 5 sec for 3 mm left a viscous alienus workers receiving the alarm signal deposit of mucus that turned white on sooner and dispersing more rapidly from an drying and would alarm other earthworms area of disturbance. It is possible that the as long as 3 months after deposition. It is slower aggressive reaction of claviger con- interesting to note that after the material centrates this species with its superior de- dried it was not readily soluble in water and fense organs at the area of disturbance and is the authors felt that the secretion was more advantageous in overcoming an enemy, while effective in communicating alarm when dry alienus depends on early warning and flight as its principle method of survival. than wet. In general, alarm substances of the social The ability to communicate alarm chemi- hymenoptera (wasps, bees, and ants) are cally may even be found in mammals. always associated with the tools of glands Valenta and Rigby (1968) have clearly es- of defense such as the mandibular glands, tablished that rats can distinguish between the Dufour’s gland, and the anal gland. As air samples taken from stressed and un- Maschwitz (1964) has shown, alarm pher- stressed rats. The possibility that animals omones may be released separately or in may be able to leave chemical signals in a 316 REGNIER

test apparatus is of major significance to triggers cyanogenesis is stored in another behavioral scientists. (Eisner, Eisner, Hurst, Karatos, and Mein- wald, 1963). Mixing the components of IV. DEFENSE these two compartments at the instant of While discussing alarm communication I discharge results in cyanogenesis external to touched briefly on defense mechanisms. One the insect. It has been shown that the Un-

of the first defense chemicals identified was dissociated cyanogenic precursor is man- Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 formic acid produced by ants (Wray, 1670). delonitrile and that the discharged secretion The work of Stumper (1952) indicates that of this millipede contains benzaldehyde and most Formicinae produce formic acid which hydrogen cyanide but no free sugar. Centi- is released in fine droplets from the venom pedes (Schildknecht, Maschwitz, and Wink- gland when these ants are molested. The ler, 1968) also produce hydrogen cyanide in fact that undecane is discharged with formic large unicellular glands in quantities up to acid and used as a spreading agent impli- 2.2 jig/insect. The hydrogen cyanide pro- cates it as a defense substance in a secondary duced by this insect is used strictly in self- sense (Regnier and Wilson, 1968). The defense and may be used to repulse as many amount of work done on defense chemicals as 15 attackers before the glandular reservoir in nature is substantial. Not only are the is exhausted. The hydrogen cyanide is proba- defense chemicals themselves unusual but bly also formed from mandelonitrile by the delivery systems are equally unusual. enzymatic decomposition. Probably the most unusual chemical defense Benzaldehyde itself may also be used as system in terms of chemistry, physiology, a defensive substance. In the harvester ant, and mode of delivery of defense chemical is Beromessor pergandei, benzaldehyde is pro- that of the bombardier beetle (Brachinus). duced in the mandibular glands and is used When this beetle is disturbed it ejects a primarily as a defensive substance. A minor defensive spray of quinones and water vapor constituent produced in this gland also at 100C (Aneshansley, Eisner, Widom, and functions as an alarm pheromone (Blum, Widom, 1969). This remarkable feat is 1969). achieved by mixing hydroquinones and hy- The tenebroid beetle, Zophobas rubipes, drogen peroxide with a mixture of catalases has a pair of prothoracic glands secreting and peroxidases (Schildknecht and Holou- phenols, and a pair of abdominal defensive bek, 1961) in a thick walled gland. The glands secreting quinones. The phenols iso- ensuing decomposition of hydrogen perox- lated from the prothoracic glands were m- ide and oxidation of hydroquinones occurs cresol, rn-ethyl phenol, and phenol (Tsckin- explosively due to the rapid generation of kel, 1969). The quinone-producing abdomi- oxygen and liberation of heat. The defense nal glands are a pair of reversible sacs spray pops out of the jet at the tip of the located on the fifth and sixth sternites. These abdomen and is directed toward an enemy glands produce benzoquinone, toluquinone, by rotation of the abdominal tip. The dura- and ethylquinone. tion of the discharge is about 30 msec. The production of quinones as defensive Probably the most unusual defense chemi- secretions is widespread in the cal is the hydrogen cyanide produced by (Eisner and Meinwald, 1966). At least 34 polydesmoid millipedes and centipedes. In genera in 7 different insect orders have been the polydesmoid millipede Apheloria corru- found to use these compounds defensively. gala, undissociated cyanogenic precursors Happ (1968) has shown that in the tenebroid are stored in one compartment of the de- beetles Eleodes longicolis and Tribolium cas- fensive glands while the chemical factor that tafleum quinones are generally formed from SEMIOCHEMICAL STRUCTURE AND FUNCTION 317

TABLE 3

SOME COMMON DEFENSE CHEMICALS

Compound Insect Reference

Formic acid Ant Stumper (1952) (Formicinae) Undecane Ant Regnier and Wilson (1968) (Acamhomyops c/a viger) Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 Citronellal Ant Chadha, Eisner, Monro, and Meinwald (1962) (Acant/zomyops c/a viger) Water vapor Bombadier beetle Aneshansley, Eisner, Widom, and Widom (1969) (Branc/zinus) Hydrocyanic acid Millepede Eisner, Eisner, Hurst, Karates, and Meinwald (Apheloria corrugata) (1963) Centipede Schildknecht, Maschwitz, and Winkler (1968) Benzaldehyde Millipede Eisner, Eisner, Hurst, Karatos, and Meinwald (Aphe/oria corrugata) (1963) Centipede Schildknecht, Maschwitz, and Winkler (1968) Harvester ant Blum (1969) (Beromesser pergandei) p-Benzoquinone Bombadier bettle Aneshansley, Eisner, Widom, and Widom (1969) (Brac/zinus) Toluquinone Bombadier beetle Aneshansley, Eisner, Widom, and Widom (1969) (Brac/zinus) Phenol Tenebroid beetle Tschinkel (1969) (Zophobas rubipes) m-Cresol Tenebroid beetle Tschinkel (1969) (Zop/zobas i-ubipes) phenol glucosides by hydrolysis and subse- remove all doubt about the possibility of quent oxidation. one species being able to “tell” another to The occurrence of repellents among marine cease and desist. Some common defense organisms is also widespread. The boxfish, chemicals are found in Table 3. Ostracion lentiginosus, secretes a substance V. AGGREGATING SUBSTANCES that acts as both a repellent and toxicant to other fish. Boylan and Schever (1967) have The devastating infestation of pine and successfully isolated and characterized the spruce forests by the beetle genera Dendroc- compound responsible and found it to be tonus and Ips illustrates the impact that the choline chloride ester of 3-acetoxyhexa- animals using highly efficient chemical com- decanoic acid for which they proposed the munication systems can have on the environ- name pahutoxin. Synthetic pahutoxin was ment. A list of compounds that have been toxic in laboratory tests to adult brackish- implicated will be found in Table 4. In the water mollies (Moilienesia lallipinna) and southern pine- beetle Dendroctonus fron tails, hemolyzed red blood cells of bigeye tuna in a female will find a suitable host and begin vitro. The adaptive advantage of the produc- to release an attractant pheromone (Vite, tion of this allomone is obvious in this slow Care, and Von Scheller, 1964), frontalin, moving unprotected species. while penetrating the bark. Penetration of Most of us are familiar, either from first- the bark releases host volatiles that further hand experience or by reputation, with the enhance the attractiveness of frontalin. In defensive secretion of the skunk. Experi- the case of D. fron tails the a-pinene of the ences with this defensive chemical should host is the most active enhancing agent. 318 REGNIER

TABLE 4 AGGREGATING PHEROMONES

Compound Organism Reference

Methyl oleate Beetle Ikan, Bergmann, Yinon, and Shulov (Trogoderma granarium) (1969) Ethyl oleate Beetle Ikan, Bergmann, Yinon, and Shulov Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 (Trogoderma granarium) (1969) Ethyl palmitate Beetle Ikan, Bergmann, Yinon, and Shulov (Trogoderma granarium) (1969) Ethyl stearate Beetle Ikan, Bergmann, Yinon, and Shulov (Trogoderma granarium) (1969) Ethayl linoleate Beetle Ikan, Bergmann, Yinon, and Shulov (Trogoderma granarium) (1969) 2-Methyl-6-methylene- Bark beetle Silverstein, Rodin, and Wood (1966) 7-octen-4-ol (Ips confusus) 2-Methyl-6-methylene- Bark beetle Silverstein, Rodin, and Wood (1966) 2,7-Octadien-4-ol (Ips confusus) Verbenol Bark beetle Silverstein, Rodin, and Wood (1966) (ips con fusus) Verbenone Bark beetle Renwick (1967) (De,zdroctonus) Brevicomin Bark beetle Silverstein, Brownlee, Bellas, Wood, and (Dendrocionus brevicomis) Browne (1968) Frontalin Bark beetle Kinzer (1969) (Dendroctoizus fro,Ita/is) Cyclic AMP Slime mold Barkley (1969) (Dictyosie/ium discoideum)

The mixture of frontalin and a-pinene at- gregation (Rudinsky, 1969). The release of tracts males and females of the same species masking substance is triggered by stridula- in the ratio 3 males to 1 female. The rapidly tion of males near the attractive female prior increasing numbers of males begin to release to mating. verbenone (Renwick, 1967) which initially Dendroctonus brevicomis appears to use a reduces the response of males and eventually different mixture of compounds than D. reaches concentrations that inhibit further frontalis for host selection and aggregation. aggregation of both sexes. The function of The attraction of both sexes of D. brevicomis verbenone here is to block the reception of by the female producing aggregating sub- frontalin. Renwick and Vite (1969) have stances, brevicomin and frontalin, is en- proposed the attack mechanism for D. hanced by the host terpene myrcene (Bedard, frontalis outlined in Fig. 3. It is also known Wilden, Wood, Silverstein, Brownlee, and that females produce the pheromone trans- Rodin, 1969). It is probable that host- verbenol, but these workers do not feel it is specific synergists will vary from species to an essential component. species in Dendroctonus. The attack mechanism of Dendroctonus The beetle Trogoderma granarium spends pseudotsugae on Douglas-fir trees is ap- its life in the dark recesses of granaries where parently different. In this species the female it lives on stored grain products. Both sexes still finds the host and releases the aggregat- of this species secrete material that acts as a ing pheromone, but she also releases the repellant for the flour beetle, Tribolium masking substance that inhibits further ag- castatewn, and an assembling scent for mem- SEMIOCHEMICAL STRUCTURE AND FUNCTION 319 bers of its own species. This secretion has been shown to be a mixture of the fatty acid esters, methyl oleate, ethyl palmitate, ethyl 9 fc(d’ FRONTALIN stearate, ethyl oleate, and ethyl linoleate A d-PINENE 9 (Ikan, Bergmann, Yinon and Shulov, 1969). Synthetic mixtures in the natural concentra- tion ratios were found to have the same Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 biological activity as Trogoderma extracts.

VI. TERRITORIAL MARKING

An essential part of the behavior of many VERBENONE I d’ 6 species of animals is the possession and B 9 FRONTALIN -, 9 2 defense of a definite territory, the boundaries -PINENE t of which are often marked by excretions from scent glands. The actual reason for the establishment of territories is not often ap- parent. Some animals express territoriality during the mating period and only the males of the species establish territories. C VERBENONE {: Males of the Mongolian gerbil (Meriones unguicalatus) mark objects in their environ- ment with the secretion of a midventral sebaceous gland (Thiessen, Friend, and Lindzey, 1968). Both gland size and marking FIG. 3. Mechanism of colonization by De,z- behavior are under androgen control. Cas- drocto,zusfronta/is (Renwick and Vite, 1969). tration drastically reduces gland integrity and marking behavior while treatment with other hand, have found the principle volatile testosterone propionate restores both activi- of male B. terrestris to be 2, 3-dihydrofarne- ties. Replacement therapy with large doses sol. of testosterone propionate resulted in “su- A major component of head extracts of permarking” activity. B. agrorium males was 7-hexadecen-l-ol. Detailed chemical studies on territorial The compound could not be found in ex- marking are few and not completely con- tracts of workers or queen heads. The major vincing on the basis of behavioral assays component of B. lapidarius was 9-hexadecen- with synthetic compounds. Behavioral in- l-ol (palmitoleyl alcohol) along with hexa- vestigation by Haas (1952) and Kullenberg decanol and n-tricosane. Extracts of heads (1956) have made it clear the male bumble- of male B. lucorum yielded ethyl-9-tetra- bees of the genus Bombus produce odor- decenoate as the major constituent in addi- iferous compounds in their mandibular tion to ethyl esters of lauric, myristic, and C16 glands that are placed on different objects in and C,8 unsaturated acids. The exact bio- their flying territories. logical function of all of these compounds Calam (1969) has shown that the heads of awaits the development of suitable bio- male B. agrorurn, B. lap/darius, and B. assays. lucorum contain a series of aliphatic alcohols VII. SEX ATTRACTION and esters as the principle volatile com- ponents. Bergstrom, Kullenberg, Stallberg- When an organism has reached sexual Stenhagen, and Stenhagen (1968), on the maturity and is ready for mating, it is con- 320 REGNIER

TABLE S SEX PHEROMONES

Compound Organism Reference

cis-7-Dodecenyl acetate Cabbage looper Berger (1968) (Tric/zoplusia iii) irans-7-Dodecenyl acetate False codling moth Read, Warren, and Hewitt Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 (Argyroplace leucotreza) (1968) cis-8-Dodecenyl acetate Oriental fruit moth Roelofs, Commcau, and Selle (Grapholitha moleata) (1969) cis-9-Tetradecen-1-ol Fall army worm Sekul and Sparks (1967) (Laphygma frugiperda) c/s-11-Tetradecenyl acetate European corn borer KIun and Brindley (1969) (Oat rinia nubilalis) tra,zs-3-cis-5-Tetradecadienoic Black carpet beetle Silverstein, Rodin, Burkholder, acid (AHagenus megatoma) and Gorman (1967) ira,zs-1O-cis-12-Hexadecadien- Silkworm moth Butenandt, Beckmann, Stamm, 1-01 (Bombyx mori) and Hecker (1959)

(- ) -14-Methyl-c-/s-8-hexadecen - Grain beetle Rodin, Silverstein, Burkholder, 1-ol (Trogoderma inc/usum) and Gorman (1969) (- ) -14-Methyl-cis-8-hexadece- Grain beetle Rodin, Silverstein, Burkholder, noic acid (Trogoderma inclusum) and Gorman (1969) fronted with the problem of finding a suitable million virgin female moths and character- mate. Even if an organism has been totally ized it as trans-lO-cis-12-hexadecadien-l-ol solitary and never communicated with (Butenandt, Beckmann, Stamm, and Hecker, another member of its species, it must do so 1959). The name bombykol was proposed now. It must locate a member of the oppo- for this first sex pheromone. Shortly after site sex, identify it as a member of its species, the identification of bombykol, Jacobson, and determine if it is ready for mating. This Beroza, and Jones (1960) isolated and identi- may of course be a complicated process and fied the sex attractant of female gypsy moths require the use of multiple sensory channels. in an equally impressive feat of persistence It has been found in recent years, particularly and dexterity with organic microanalysis. in insects, that this vital information is often With the advent of combination gas chro- conveyed with chemical signals. matograph-mass spectrometry, high resolu- In many insects all of the information tion nuclear magnetic resonance spectrome- necessary for mating is carried by a single try, high sensitivity infrared spectroscopy, organic compound that the female releases and reaction gas chromatography, the char- when she is ready for mating. Still other acterization of small quantities of an organic species rely heavily on male-produced phero- compound is much simpler. mone, while a third category relies on stimuli Female insects usually produce their sex from both sexes. pheromones in a specialized gland. In the A number of female insect sex attractants , these glands are located in the have been isolated as will be seen in Table 5. intersegmental membrane between the eighth In 1939 Butenandt and his colleagues under- and ninth abdominal segments (Jacobson, took the isolation and characterization of 1965). Gland structure is of five general the sex attractant from the silk worm moth, types and the method of releasing pheromone Bombyx mon. They reported in 1959 that varies between different insects. In Bombyx they had isolated a few milligrams of a inori, the female everts the scent gland and derivative of the compound from half a airs the contents to increase the rate of SEMIOCHEMICAL STRUCTURE AND FUNCTION 321 evaporation of the pheromone. Enlarge- and the distance from the source is a few ment of the gland duct or actual eversion of yards or less, he may orient osmotactically. the gland at the time of pheromone trans- At these short distances the pheromone mission to increase evaporation rate is concentration gradient is steep enough per probably common. unit distance that an insect may easily seek The amount of pheromone that is actually out the point of highest concentration. How- present at any one time has been very low in ever, at distances of a few hundred yards, Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 the few studies done. Shorey and Gaston the concentration gradient is so small that (1965) found that the gland from the female osmotaxis is impossible. Orientation in long cabbage looper contained 1-2 jig of phero- range communication systems is usually by mone while that of the silkworm moth positive anemotaxis (Jacobson, 1965). When (Steinbrecht, 1964) contains approximately the male is stimulated by pheromone recep- 1.5 jig. Gas chromatographic analysis of tion he simply turns and flies into the wind extracts of abdomens of the female grass since the wind is carrying the compound to grub beetle, Costelytra zealandica, indicated him. The insect may be thought of as moving that each beetle contains 0.5-1.0 jig of sex through an odor corridor (Wilson and pheromone (Henzell and Lowe, 1970). The Bossert, 1963) toward the pheromone source. total amount of material that may be isolated As he comes into close proximity with the from a gland at any time, of course, has no source, anemotactic orientation will give way relationship to the rate of release of the to osmotactic. pheromone. At the present time this has not Sex pheromone reception in insects is been determined in any species. generally very specific. Other than to state Since the sex pheromone must travel in air that reception occurs in antennal sensilla, I between two organisms at a significant will not discuss the nature of olfaction. I will enough rate to make an impact on the instead discuss the chemoselectivity and sensory system of the receiver, the com- sensitivity of insect sex pheromone chemore- pounds must have some inherent volatility. ception. The efficiency and selectivity of The limiting value on the molecular weight this process is demonstrated in Table 6. thus becomes about 300 (Wilson and Bossert, Synthetic bombykol is l0-trans-12-cis-hex- 1963). Few cases of compounds larger than adecadien-l-ol and is attractive to males at a this have been found to function in com- concentration of 10-12 jig/mi according to munication through air at distances of a few the standard assay technique. Changing the meters. Communication in aqueous sys- tems, however, is another matter. Here TABLE 6 volatility has nothing to do with transmis- COMPARATIVE ATTRACTANCY OF sion. BOMBYKOL ISOMERS Transmission of airborne pheromones may Attractanc-” Compound be by simple diffusion in the case of short (tag,’ ml) range communication or by transport in air streams. Simple diffusion of an odorant is 1O-tra,zs-1 2-tra,zs-Hexadecadien-l -ol I lO-tra,zs-l2-cis-Hexadecadien-l -ol l012 important in sex attraction, but the primary lO-cis-12-trans-Hexadecadien -1 -01 lO means of transport in long range sexual 10-c is-12-cis-Hexadecadien-1-ol 10 attraction is by the wind. Bombykol (natural) 1010 When the male receives a sex attractant Attractancy of bombykol is expressed as the and is stimulated to seek out the source he concentration of pheromone in pentane on a glass must orient his locomotory activity towards rod that will attract 50’ of the B. mon males the source. If the pheromone is very volatile tested. 322 REGNIER

stereochemistry of the molecule drastically sesquiterpenoid (Machlis, Nutting, and reduces the attractancy of a compound Rapoport, 1968). (Butenandt and Hecker, 1961). l0-trans-12- Ryan (1966) has also found that the crab, trans-Hexadecadien-l-ol is 1012 times less Port un us sanguinolenius, uses sex phero- active than synthetic bombykol while l0-cis- mones in mating. His experiments indicate 1 2-c/s-hexadecadien -1 -ol shows a lO”-fold that the premolt female releases a sex at-

decrease in activity. In the case of the tractant in urine that attracts males. The Downloaded from https://academic.oup.com/biolreprod/article/4/3/309/2768582 by guest on 23 September 2021 gypsy moth only the cis isomers of synthetic exact origin of this compound, its chemical compounds have activity comparable to structure, and the way that the males detect that of natural gyptol. A single change in the compound still remain to be elucidated. molecular geometry (c/s isomer to mans) can Male sex pheromones are seldom used in decrease the activity lO’5-fold. The d- and communication systems where the distance /-isomers of the compound are equally exceeds a few meters. such as active however. Temporary blockage of the Danaus gilippus beren ice, Lycorea ceres antennal sensory system may occur when an ceres, and Danaus piexippus are species in unnatural geometric isomer of a pheromone which the male pheromone must be brought is presented to an insect. As little as 15 % of into close proximity with the female’s anten- 10-propyl-cis-5 , 9-tridecadienyl acetate com- nae before it influences the behavior of the pletely blocks the reception of the natural female. Brower, Brower, and Cranston trans isomer (Jacobson, 1969). This is also (1965) showed that mating did not occur in true with the trans isomer of the sex attract- the Queen , Dancus gil/pp us berenice, ant for the gypsy moth, 12-acetoxy-cis-9- until the male wafted a pheromone-contain- octadecen-l-ol. In the case of the cabbage ing brushlike organ in front of the female looper whose natural pheromone is cis-7- while either in aerial pursuit or after the dodecenyl acetate, reception is blocked by female had alighted on vegetation. In a more the corresponding trans isomer (Jacobson, recent study (Myers and Brower, 1969), it 1969). It is interesting to note that in two has been shown that courtship is sub- closely related species of Gelechiidae one stantially reduced either by the removal of form which Roelofs and Commeau (1969) the brushlike organ or by blocking the refer to as (Bl) is always attracted to the sex chemoreceptors on the female antennae. lure c/s-9-tetradecenyl acetate and the other It is clear that the most challenging species (B2) is attracted to trans-9-tetra- problems in the future for the “phero- decenyl acetate. Mixtures of the two isomers monologist” are to be found in higher were not attractive to either species. These animal systems. Not a single compound has workers feel that such a system could be been identified as a pheromone in a higher important as a natural species isolating animal at the present time. It is easily mechanism. anticipated that the studies described here Chemotactic orientation between mating should be valuable models for these studies. pairs has also been demonstrated in fungi. To those who would enter the field, there is Unopened female gametes of the water one criterion for a pheromone that I am mold, Allomyces, produce a compound that sure all of those people who have worked attracts the motile male gametes. The at- with insect systems would relate. A com- tracted male gametes cluster around the pound is a pheromone only when it has been female gametes as they are released from the isolated from an organism, chemically char- gametangia. This sex pheromone, sirenin, acterized, synthesized, and the synthetic has been isolated and shown to be a bicyclic compound shown to elicit a behavioral re- SEMIOCHEMICAL STRUCTURE AND FUNCTION 323 sponse at a concentration level approxi- (1966). Chemical releasers of social behavior. VI. The relation of structure to activity of ketones as mating the natural situation. releasers of alarm for Inidomynmex pruinosus (Roger). U. Insect Physio/. 12, 419-427. REFERENCES Bocj-i, R., AND SHEARER, D. A. (1964). Identification ACREE, F., TURNER, J. B., GOUCK, H. K., BEROZA, M., of geraniol as the active component in the Nassanoff AND SMITH, N. (1968). L-lactic acid: A mosquito pheromone of the honey bee. Nature Lozzdon 194, 704-706.

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