The Cockroach Connection—Ancient, Seemingly Indestructible Pest

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Current Comments@ EUGENE GARFIELD INSTITUTE FOR SCIENTIFIC INFORMATION(9 3W1 MARKET ST PHILADELFI+A PA 19104 The Cockroach Connection—Ancient, Seemingly Indestructible Pest. Part 2. Population Control, or: “Dr. Djerassi, How Do You (let Them to Take the Pill’?”

Number 46 November 12, 1990 In Part 1, we examined the edcroach’s morphology and behavior and the link to allergic reactions in humans. In Part 2, we examine how scientists are attacking the problem of cockroach infestations via pesticides and artificial analogs of the insect’s hormones and pheromones. Four Cirdon Cfassics@J relating to research on cockroach development and gnnwh are discussed, and lSI@ research-front data highlight activity in cdcmach control.

Declaring War on Roaches down less easily. Many of the pyrethroids are much more active than the natural pyre- The cockroach is one of the most vilified thrins (some 1,000 times more) and, unlike insects known to mart. In the US more than the natural pyrethrins, are stable in sunlight. $1.5 billion was spent in 1989 on consumer In contrast, because of their instability in pesticide products to get rid of cdroaches, sunlight, the natural pyrethrins cannot be the single largest expenditure for a pest in used on field crops. Permethrin was the the country. 1 Let’s take a look at what this first sunlight-stable commercial pyrethroid.3 money is spent on and at the eradica- Many insects have developed a resistance tion/control efforts of insect researchers in to pyrethrins and pyrethroids (synthetic de- the laboratory. rivatives of pyrethrins). According to Clive Scientists are attacking the problem of A. Henrick, Sandoz Crop Protection Re- cockroach infestations in three ways: by search Division, Palo Alto, California, gen- using chemicals that attack the roach’s cen- eral insect resistance is becoming wide- tral nervous system, by using those that spread,3 with the cockroach fast becoming mimic the insect’s itormone/endocrine sys- one of the insects that is resistant.4 Consid- tem (causing disruptions in the life cycle), ering that each generation of roaches fol- and by using artificially synthesized phero- lows itself in quick succession (survivors monai attractants to draw cockroaches to passing on their resistance to offspring), this sex-bait traps where they get stuck in a .giue comes as no surprise. and die. The organophosphates constitute another category of insecticides used on roaches. Chemical Pesticides These include chemicals called cftior- pyriphox, malathion, diazinon, and dichior- One of the oldest insecticides known to vos (also known as DDVP). These chemi- man is pyrethrum. Pyrethrin insecticides cals work by inhibiting the enzyme are derived from pyrethrum flowers. such as choiinesterase. This causes nerves to stimu- chrysanthemums. The aromatic flower late muscles continuously. Some organo- heads are powdered or extracted with sol- phosphates are fairly toxic to mammals, vents, and the resultant substances are con- while others, including malathion, are of tact poisons and nerwe toxins for inseets.2 iow toxicity and break down rapidfy.5 Because natural pyrethrins are unstable and The carbamates, inciuding hendioearh and expensive, chemists have produced syn- propoxur, encompass another category of thetic pyrethroids that mimic the natural py- roach insecticide. Carbamates are used rethrins. These are more stable and break most frequently in over-the-counter sprays

413 ~lgure 1: Historiographs of research fronts on chemical inwticktes. Numben at the bottomof ewh box indicate numbersof cordciting papers.

m /l pyrethroids ~,2~

10172

and professional applications because they secticide applications “do not significantly act within minutes=ne of the quickest act- affect German cockroach population dis- ing contact poisons. These have the same persal or movement patterns within apart- mode of action as the organophosphates. ments.’~ Another chemical group is composed of Another recent study looked at the perfor- inorganic dusts. These include silica gel mance of consumer roach bait products. It and boric acid. These are cafled “mechani- found that, of all those avaiIable, hydra- cal” insecticides because they kill the methybron (the active ingredient in Combat roaches by dehydration. Boric acid also roach traps) “has the greatest potential for works as a stomach ~ison, but is toxic to field effectiveness. Only hydramethylnon pets and humans.s The inorganic dusts lose significantly reduced German cockroach their effectiveness in humid weather. But populations,’6 Hydramethyhron is a chemi- when combined with pyrethrins, they are cal that affects the cell’s ability to convert used as an agent to flush cockroaches from food into energy. The net result is that the their hiding places. insect eats the chemical, slowly runs out of The number of chemicals, however, that energy, falls asleep, and dies.’ cockroaches are becoming resistant to is growing. In one recently published study of insecticides and their effects on the German Repellents: Shoo, Roach, Don’t cockroach, S.J. Barcay and colleagues, Bother Me! Purdue University, West Lafayette, Indiana, found that pyrethrins, diazinon, permethrin, I don’t think that anyone would argue that and propoxur in lethal quantities “did not we ‘d prefer cockroaches to stay outdoors. induce any significant changes in cockroach As for ways of making these insects leave distribution.” With sublethal doses, the (instead of exterminating them), there have roaches “settled to their original distribution been numerous suggestions, ranging from 24 hours after treatment.” Results from old home remedies, such as cucumbers and both experiments indicate that thorough in- bay leaves, 8 to highly touted high-tech

414 -, .- I 1 1 1 ~ activitystudies of I pyrethroids I 3/30

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t , ware, such as ultrasound. The high-pitched Gainesville scientists hope to determine noise, according to proponents, drives away what conditions the insects need to thrive— all sorts of insect pests, including cock- whether in the attic, among the insulation, roaches. Unfortunately, studies show that or in the walls. From these data, it may German cockroaches enter “ultrasound- become possible through new home con- treated rooms as readily as they [do] un- struction techniques to repel cockroaches. treated rooms.”9 To date, scientists have found that roaches On the biochemical front, scientists report thrive in areas of stagnant air and high hu- that synthetic and nahmdiy occurring chem- midity, and that they avoid dry, ventilated icals both have repdent properties, accord- environments. ing to controlled studies on the German and the American cockroach. The synthetic Cockroach Biochemistry and Ci&ation chemicals include amides, sulfonamides, Classic@’ : Putting Roaches on the Pill carboxamides, and cyanoacetic acids. Natu- rally occ urnng chemicals include plant oils In addition to synthetic and naturally oc- from the Japanese mint and Scotch spear- curring pesticides, scientists seek to control mint. 10 Usua]lY, these repellents are used in cockroaches through the insect’s own bio- concert with insecticides to achieve the chemical reactions. Studying these reac- greatest deterrent effect. tions helps insect researchers understand There may be a better. nonchemical sokl- how cockroaches mature from egg to tion to the cockroach infestation problem, nymph to adult. The studies also provide however—build better houses! At the US hints as to where artiticiai mimics of the Department of AL@xritore laboratory in hormone regulators of these reactions might Gainesville, Florida, entomologists are be used to disrupt the cockroach’s develop- monitoring cockroach activity in a specially mental and behavioral processes. built attic in an effort to understand what The road to manipulating the cockroach’s factors control cockroach movement. 11 In biological processes actually began nearly this building 100 sensors and probes set at 40 years ago, when entomologists discov- various locations measure humidity, temper- ered that a series of proteins which affect atures inside insulation and wood, airflow egg yolk production in vertebrates also ap- patterns, as well as roach distribution and peared in insects. 12 In the following de- activity (via proximity sensors and video). cades, studies on how these proteins affect

415 Figure 2: Htstoriograph of research fmnfs on coctuwach sex pheromones. Numbersat the fmuomof each tw. indicatenumks of corelcitmgpapers

86-5308 Wtttig rearrangement and synthesis of American r cockroach sex pheromone 5/45

— egg production and insect nymph growth In his 1979 commentary 17 on the 1951 l;~ t; efforts to identify and rnanipurate in- vitellogenin discovery and resulting review sect hormones. Many of the discoveries papr,lz W.H. Telfer, University of Pennsyl- dealing with these insect hormones took vania, Philadelphia, noted that vitellogene- place in the late 1960s and 1970s.13-’5 sis studies came into their own during the mid- 1960s with the discovery of the organ- The Discovery of Insect Vitellogenins elle for vitellogenin transport, as well as when the endocrinological community con- We have four Cifation Classics that fol- centrated their efforts on this field. low the development of this interesting branch of entomology. 12-’5 Although they The VitellogenintEcdysone Hormone are not specifically on cmkroaches, the Connection commentmies are generally applicable. They begin in 1951 with the discovery of While vitellogenesis was discovered in the egg yolk proteins called vitellogenins, the early 1950s, it wasn’t until the 1970s then move to establishing the connection of that vitellogenesis in other insects was hormones in regulating these proteins, and linked to steroid hormones generated by the finally to the branching out of studies in the gonads. In his Cfassic commentssyl 8 on the regulation of the hormones that affect insect landmark paper*3 that was the first to report molting and metamorphosis through the that ecdysone (a molting hormone) stimu- varying stages from egg to nymph to adult. lated vitellogenin synthesis in the fat body These hormones include brain hormones of the mosquito, Henry H. Hagedom, Uni- (called pptides), molting hormones (called versity of Arizona, Tucson, comments that ecdysones), and juvenile hormones, which “by 1975 very Iittfe was known about the modify the outcome of the molt. hormonaf control of egg development, ex- Vhellogenin is the generic name for a cept for the common observation that re- group of proteins synthesized outside the moval of the source of juvenile hormone [s] ovaries that become the major egg yolk vi- somehow interfered with the process .... tellin. This protein is manufactured in both Since, for the most part, insects chosen for vertebrates and insects. Vitellogenesis in physiological work are large, it is notewor- many insects, the cockroach included, de- thy that work on the tiny mosquito opened pends on the secretion of juvenile hormones new doors in this field.” Ecdysone was fwst from the corpus allatum, a part of the roach identified in 1956 in Germany by biochem- endocrine system that regulates juvenile ist Peter Karlson, University of Munich, and characteristics in the larva and is responsi- colleagues who started with 1,00U pounds ble for oocyte (egg case) development and of silkworm pupae to extract the small secondary sexuaf organ secretion in the amounts of the chemical that were harbored adult roach. 16 However, the main function by each insect. 19 of insect juvenile hormones is to control the Another Classic paper also concerns the outcome of each molt (it maintains the im- hormone ecdysme and its effect on molting mature character of the developing insect) of the embryo in the locust. 14 According to while their secondary functions are involved their Classic commentary, M. Lagueux, with yolk formation.3 M. Him. and J. A. Hoffmann. Louis Pasteur

416 87-5389 88-208 89-2268 Synthesizing vinblastine Diurnal rhythm of Wittig rearrangement, derivatives and W~ig B/ate//agemrarrica L. allylic ethers, and rearrangement and American cockroach American cockroach 3134 6/39 8/62

University, Strasbourg, France, found seren- In his Classic commentary on the devel- dipitously that ecdysone not only stimulated opment of juvenile hormone mimics at molting and metamorphosis in adult insects, Zoecon Corporation, Henrick gives a but afso regulated molts of the developing thumbnail sketch of methoprene: embryo. They were originally trying to prove that ecciysone was oniy a molting hor- Methoprene became our first commercial product, and it has been used worldwide mone and believed that adult female Ioeusts as the standard fiuvenile hormone mimic] would prove this since they would no longer since its discovery .... Methoprene was the undergo further growth. Each molt of the first “biorational” insecticide, a term embryo was preceded by or coincident with coined...in 1974D to describe our ap- a concentration peak of the ecdysone hor- proach to developing new envirmrnen- mone. Their observations “probably repre- tally safe pesticides. Methoprene is re- sent the best documented example of a markably nontoxic to mammals. ... It is in transfer of steroid hormones of maternal ori- a sense also nontoxic to young insects in gin to the embryo in egg-laying animals.”z” that it has no effect on early larval [stages] and only affects the last larval stages by interfering with metamorphosis. . The commercial success of methoprene and Early Work on Juvenile Hormones subsequently hydroprene (for ccckroach control) has fully justified the initiaf en- While vitellogenesis and hormone regula- thusiasm and marked the beginning of the tion were not linked until the 1970s, the first use of biorational insecticides.23 paper on the identification of an insect juvenile hormone was published in 1967.21 Hydroprene has been shown in field-test Prior to this, the chemical structures of natu- situations to reduce cockroach populations ral juvenile hormones were unknown (af- by 95 percent within six months after an though the presence of juveniie hormones application of the compottnd.5 Speaking of was established in the 1930s3). hormone regulators for cockroaches, Carl The potential to selectively control insect Djerassi, Stanford University, Cafifomia, pests by using analogs of their natural juve- has been (over the years) involved in this nile hormones was realized in late 1970 at a quest. Back in the mid- 1980s, when he also start-up compatty named Zoecon Corpora- served as chief executive officer of Z&eon tion, Palo Alto. The compound, called Corporation (a company specializing in the hydroprene, was the fist juvenile hormone development of insect biochemicrd regula- mimic synthesized that evenrttally became a tors), Carl publicized a cockroach sterilizer commercial product fit W.s acrually the called GENCOR, which contains lydroprene as the active ingredient. In a 394th mimic synthesized>), with a second appearing in 1971 called methoprene. Forthcoming autobiography, Carl recalls his These chemical compounds, based on ethyl ~dvertising experiences: and isopropyl esters, are potent hormone I premiered on the cockroach circuit in mimics that cause some insect species that Orlando, Honda, where newspapers were come into contact wirh them to be irrever- at the time full of stories of sightings of sibly sterilized. A paper describing these tbe Asian cdwoach . ... I did TV inter- compounds and their effects was published views on the same day in four local sta- subsequently in 1973.*5 tions: the mother of Zcecon’s newest

417 Figure 3: Historingraph of research fronts on insect jut enile hormones. Numbers N the bottom of each tmx indicatenumbersof cwelciturg papers.

85-0480 — Juvenile hormones, cockroaches, locusts, and mosquitoes 18/111 86-0066 Anti-juvenile hormone agents 84-5831 15/122 Vhellogenesis and 85-3041 ovarian activity in Juvenile hormone biosynthesis, insects vitellogenin, and cockroaches 4/46 12f98

president, John Dlekmacr, was astonished insects, the cockroach included, use various to see her son’s fomrer professor pontifi- pheromones to mark territorial boundaries, cating abouf cockroaches on her favorite pathways to food sources (one of the rea- Orlando channel one aftemcnm, then sons Roach Motel traps work), and, of again on the new charnel she switched to, course, to attract members of the opposite then again on the evening news of a third gender. channel ! My professorial spiel started The sex pheromones released by females with my early work in fhe 1950s on ste- biologically communicate to males of their roid orat contraceptives, then noted the species that they are in a sexually receptive conceptual similarity between Zoecon’s condition. Some insects, like moths, can research and the development of the Pill, detect from miles away the pheromone and ended by calling GENCOR a funda- given off by a receptive femafe. It should mentally new prophylactic approach to cockroaches. My references to “cmk- be stressed, however, that many natural pheromones are short-lived and need to be roach birth control” may have been tm clever for our own good or perhaps I was continuously produced to be useful over catering too much to the anthropomor- long periods of time,z~,ab In cockroaches phism of my TV hostesses, because in- there are a number of pheromones (such as variably I would hear some version of wing-raising sex pheromones, “arrestant” “Buf doctor. how do you gel a cockroach male pheromones for keeping the female 10 take ~he pill’?” My explanation that one quiescent during mating, and aggregation had only fo spray mom comem. base- pheromones to bring other roaches to a spe- boards, and other likely paths seemed to cific area), but for the most part these are disappoint them.~~ effective over very short distances, such as three inches or less.z’ Juvenile hormones are only one type of The first successful synthesizing of the insect biochemical that entomologists. or- sex pheromone of a cockroach species hap- ganic biochemists. and endocrinologists are pened in 1974. C.J. Persoons, F.J. Ritter, researching. Another family of these bio- and W.J. Lichtendonk, TNO, Delft, The chemical are the pheromones. Netherlands, identified four biologically active components of the sex pheromone of Pheromonal Lures: The Cockroach the American cockrodch.28 The Dutch sci- Honey Trap entists isolated two of these chemicals, which were cafled periplartone-A and peri - In an effort to have a mechanism to con- pkmone-B. This group was elementiil in trol infestations, insect researchers have identifying the structure of periplanone-B been active for more than 25 years in trying and the subsequent artificial synthesis of to isolate, characterize, and synthesize the this chemical in 1979.29 H. Hauptrnarrn, female cockroach sex pheromone. Many G. Miihlbauer, and H. Sass, Regensberg

418 87-1566 Juvenile hormone biosynthesis in vitroand larval brain factor in the cockroach Dip/optera punctata ==entz27L 361204 i

University, Germany, were the f~st in 1986 Pesticides to successfully synthesize a version of peri- Figure 1 represents two distinct series of planone-A.30 linked research. Both highlight studies of Entomologists have learned that the use of cockroach central nervous system functions pheromones can affect the cockroach’s diur- with the effects of nerve toxins. The upper nal rhythm (the habit of avoiding light and series of research specialties focus nearly concentrating activity-such as foraging exclusively on pyrethroid insecticides. Two and sexual behavior—in the dark and at of the fronts, #87-3817, “Pyrethroid insecti- night) and that mrde roaches will follow the cides,” and #88-37 10, “Molecular targets of pheromone scent almost anywhere.31 This pyrethroid insecticides,” indicate a signifi- latter finding forms the basis of some of the cant upturn in this field of research. The popular roach traps, in which a peripkmone- number of core papers increased fourfold B/glue mixture awaits amorous male (from 5 in 1987 to 20 in 1988), and the roaches that get stuck in the glue and either number of citing articles increased nearly die of starvation or of contact poisons lacing sevenfold (from 42 to more than 290). the glue. However, it should be noted that The lower series of fronts emphasize re- penplanone-B is mostly an excitant chemi- search in identifying neural transmission cal for males and not an attractant. Accord- mechanisms and of a chemical found in ing to Henrick, “h only works on the Ameri- cockroaches called octopamine. Octopam- can cockroach (10 percent of the US ine is a neurotransmitter found in the problem) and not on the German cockroach hemolymph (body fluid or blood) of the in- (about 80 percent of the problem).”3 sect. Hemolymph circulates through the fat body, the main organ of intermediary me- ISI@ Research Fronts Highlight Activity tabolism that also stores protein during on Insecticide, Pheromone, and Juvenile metamorphosis. 32 If octopmine release is Hormone Investigations inhibited or interrupted, the cockroach’s Figures 1, 2, and 3 illustrate, via historio- ability to eat, grow, and reproduce is se- graphs, research on cockroaches during the verely affected, if not stopped outright. The years 1984 through 1989. A research front research-front titles indicate that octopam- is formed by the connections made by sci- ine research is closely linked to hemolymph entists in their referencing patterns. Using a cell studies and central nervous system ex- method called co-citation clustering, it is periments. Octopamine agonists (chemical possible to order automatically the scientific substances that combine with a nerve recep- literature into bibliographically distinct and tor and initiate a reaction) are aimed at af- intellectually coherent units. Articles that fecting insect behavior by exciting the cen- are frequently cited together by current pa- tral nervous system.3 pers constitute the “core”””’of the specialty. The research front, in parr, is composed of Sex Pheromone Studies citing articles and is named from phrases co-occurring in these citing titles. If core Figure 2 emphasizes work on synthesiz- papers are co-cited during a number of con- ing cockroach pheromones. Two of the re- secut ive years, the research fronts are search fronts, #84-793 1, “Pheromone syn- linked, thesis” and #85-0150, “Insect behavior and

419 sex pheromone components of Per-iplarwta of nerve toxins, hormone and biochemical Americana,” indicate a research explosion regulators, and pheromonal lures, in the end in this field of entomological biochemistry. the roaches may yet become inheritors of The number of core papers during the two the planet. A glimpse of this ~ssibility can years increased nearly 30-fold, and the be found in the field of radiobiology, where numtm of citing works jumped 36-fold, scientists are interested in measuring the from 13 to 476. ability of living organisms to tolerate varying levels of radiation, based on a unit Juvenile Hormone Research called a roentgen (measure of energy equaf to 100 ergs per gram of irradiated material), Figure 3 is a series of research specialties also known as a “rad” or “rem.” A “rem” that emphasize the synthesis and the role of stands for roentgen equivalent n-ram--the hormones on the growth and development dosage that will cause a specifically mea- of insects, including cockroaches. The data sured amount of injury to human tissue.w A indicate that sustained high levels of re- “rad” is used for equivalent exposures for search and published work on cockroach ju- nonhuman living tissue. venile hormones, as well as efforts in creat- Radiobiologists have found that humans ing man-made anafogs of these, took place can safely wiihstand a one-time exposure of from 1985 through 1987. According to the 5 reins or less (most people are exposed to historiograph, more recent specialties con- only 16 reins in their lifetime), while a le- centrate on this trend, especially on the arti- thal dose is 800 reins or more. 34 In experi- ficial hormonal analog precmene. Pre- ments conducted during the 1950s on cocene is an anti-juvenile hormone found in gamma-radiation effects, insect researchers plants that induces irrevemible precocious found—in contrast—that the cockroach’s metamorphosis and sterilization in insects lethal dosage was horrifically higher—for (such as grasshoppers and locusts) by sup- the Americasr cockroach, 67,500 rads; for pressing the function of the corpora allata the German cockroach, between 90,000 and gland, which plays a major role in 105,00U rads.35 The amount of radiation vitellogenin synthesis.33 However, pre- roaches can withstand is equivalent to that cocene has very limited effects on cock- of a thermonuclear explosion! 36 h is hum- roaches—in the nymphal stage, the insects bling to think that such a lowly creature are not sensitive to precocene when exposed may survive the human race in the event of to practical doses of the chemicals a nuclear holocaust.

Conclusion: Will Cockroaches Have ● *.** the Last Laugh? My thanks to CJ. Fiscus, Peter While scientists are endeavoring to con- Pesavento, and Judith Schaeffer for their trol cockroach populations with an arsenal help in the preparation of this essay ~,w, ,~,

REFERENCES

1. Garfield E. The cockroach connection—ancient,seemingly indestmctible pest. Pat 1. Morphology, behavior, and the relauonship to disease, Current Contents (45):5- 10, 5 November 19%3. 2. Pyethrum. The MW en{yclopuedia Britmvm-a Chicago, IL Encyclopedia Britannica, 1985. Vol. 9. p. 825, 3, Henrick C A. PersonaJ communication. 25 September 1990. 4. Barcay S J, Schneider B M & Bennett G W. Influence of insecticide rrearmen[ on German cockroach (Dictyoptera: Blatellidae ) movement and dispersat within apartments. J. Econ Err/omcd. X3(l): 142-7, Febmary 1990. 5. Gnldman J. What’s bugging you. NW York 18(21):52-6 58-9; 62-7, 27 May 1985. 6. Appel A G. Laboratory and field p’fommnce of consumer bait products for German cnckrnach (D1ctyoprera: Blattelidae) control. J. .Econ. .Enfomo/, 83(I): 153-9, February 1990. 7. Rafofl J. Rnaches: the battle continues. Sci, New-$ 129:378-9, 1986. 8. Tired of roaches? Try cucumbers. Na[, Wildlife 21( I):35, Decemlxr/January 1983,

420 9, Knehler P G, Patterson R S & Webb J C. Efficacy of ultrasound for German cockroach (Orthoptera: Blatellidae) and oriental rat flea (Siphonoptera: Pulicidae) control. J. Econ. En/omo/. 79:1027-31, 1986. 10. Hagenbuch B E, Kuehier P G, McGovern T P, Patterxun R S & Brenner R J. Two chemical repellents for control of Gernran (Gthuptera Blatellidae) and American cockroaches (Orthoptera: Blattidae). J. Econ. Emomol. 80:10224, 1987. 11. Kinzel B, Cockroaches in the attic, Agr, Res. 37(9):4-7, Septemker 1989, 12. Telfer W H. ?he mechanism and conrrol of yolk formation. Anrru. Rev. Entomo/. 10:161-84, I%S, 13, Hagedom H H, O’Connor J D, Fuchs M S, Sage B, Schlaeger D A & Bohm M K. The ovary as a source of a-ecdysone in an adult mosquito. Proc. NaI. Acad. Sri. USA 72:3255-9, 1975. 14. Lagueux M, Hkn M & Hoffmann J A. Ecdysone during ovarian development in Locusfa migraforia. J. insect Phwiol. 23:109-19, 1977, 15. Henrick C A, Sfaal G B & Sidrbdl J B. Alkyl 3, 7, 11-trimethyl-2,4-dodecadienoates, a new class of pment insect gowtb regulators with juvenile hormoue activity. J. Agr. Food Chem. 21:354-9, 1973, 16. Gurney A B, Onbopteran (cockroaches, mantids, stick and leaf insects, grasshoppcm, crickets). The new encyc/opaedia Britannica. Chicago, fL: Encyclopedia Britannic% 1985. Vol. 21. p. 604-12 17. Teffer W H. Citaticm Classic. Comment~ on Annu. Reu .Ermmo/. 10:161-84, 1965. (Barrett J T, comp.) Coruemporary classics in plant, animal, and environmental sciences. Philadelphia 1S1Press, 1986. p. 264, 18. Hagedom H H. Ekdysone production by insect ovaries. Citation Classic. Commentary on Proc. Nal. Acad. Sci. USA 72:3255-9, 1975. Current Conrenfs/Agricu/ture, Bio/ogy & Em)irorvnental Sciences 20(13): 14, 27 March 1989, 19, Karlsmr P, Hoffmeister H, Hoppe W & Huber R. Zur chemie des ecdysrms (Tfre chemistry of ecdyxones). Liebigs Ann. Chem. 662:1-20, 1963. 20. Lagrreux M, Him M & Hoffmann J A. Steroid borrrmres and ovadan+mb~onic &velopment of inxccts.. Citation Classic. Commentary on J. /n.secI Physiol. 23: 10!- 19, 1977. Currtwf Contents/Agriculture, ffio/ogy & J@ir@vrrerua/ Sciences 21(11): 14, 12 March 1990, 21. Roller H, Dabm K H, Sweely C C & ‘fYnstB M. The structureof juvenile hormone, Angew. Chem. /ru, Ed. 6179-80, 1967, 22. Djerassi C, Sbib-Coleman C & Diekman J. Insect control of the future: operational and pulicy axpects. Science 186:596-fKt7, 1974. 23. Henrick C A. Methoprene and hydmprene: putent juvenile hormone mimics. Citation Classic. Commentary on J. ARr. Food Chem. 21:354-9, 1973. Current ContenrslAgricu/tu re, Biology & Environmental Sciences 21(3) 14, 15 January 1990. 24. Djeraasi C. “How do you get a ccckroach to take the pill?” The pi//. pygmy chimp.!, and Degask horse: on autobiography. New York: Macmillan, 1991. (In press. ) 25. Behavior, animal. The new ertcy@aedia Briranniccr. Chicago, IL: Encyclopedia Britannica, 1985. Vol. 14. p. 691. 26. Life. VIP nrw encyclopedia Brifarmica Chicago, IL: Encyclopedia Britannica, 1985. Vol. 22. p. 991. 27, Henrick C A. Ccckroach pheromones. Memorandum to Tom Graves. 1 Novemtxr 1978. 28. Persumrs C J, Ritter F J & Lkbtendonk W J. Sex pheromnne. of tbe American cockroach, Periplaneta americana. Isolation und partial identification oft wo excimnts. Proc. K. Ned. Akad. Weferwchap. C 77:2014, 1974. 29. Persuons C J, Ritter F J, Verwiel P E J, Hauptmann H & Mori K. Nomenclature of American cockroach sex pberontmres. Fitrahedron L.ert, 31(12): 1747-50, 1990, 30. Hauphnann H, Miihlbmter G & Ssss H. Identifiziemng turd symhese von Periplanon A (Identification and synthesis of periplanone A). Tefrahedrcm J!.#f. 27:6189-92, 1986. 31. Guthrie D M & Tindall A R. The bio/ogy o~fhe cockroach. London: Edward Arnold, 1968. p. 82-3; 221. 32. Wlgglesworth V B. fnscct.s:the class insects. The new encyc/qxredia Britannica. Chicago, IL: EnzyclopaediaBritannica, 1985. Vol. 21. p. 593. 33, Bowers W S, Obta T, Cleere J S & Marsella P A. Diszove~ of insect anti-juvenile hormones in plaats. Science 193:542-7, 1976. 34. Bowman J S. The Chernobyl curriculum. The Furls on Fik’ scientific yeorfwok 1987. New York Facts on File, 1987, p, 80-5. 3S. Cole M M, LaBrecque G C & Burden G S. Effects of gamma radiation on some insects afTecting man. J. Econ. Entorrwl. 52:448-50, 1959. 36, Marley F. A durable bazwd. Sci. News 92:304-5, 1967.

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