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Circadian rhythms of insect pheromone titer, calling, emission, and response: a review

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Abstract

Many insect species have circadian rhythms of pheromone production/titer, calling, emission, and response that are involved in intraspecific communication and impact pest management practices. Rhythms of pheromone biosynthesis, most studied in moths affecting forestry and agriculture, contribute to a periodicity of pheromone concentration or titer within glands or hemolymph. Calling rhythms by the pheromone-emitting sex are physical movements (pumping, vibrating wings) that aid in release and dispersion of the volatile pheromone components attractive to the opposite conspecific sex or both sexes. Circadian rhythms of emission of pheromone also occur as a result of an interaction between calling and the titer of pheromone available for release. Responding individuals usually show a coincidental rhythm of dispersal flight while seeking pheromone plumes in which, by orienting upwind, the insects find mates or food resources. However, some species begin searching an hour or more before the emitting sex initiates calling and emission, which benefits mass trapping control programs because the baited traps do not compete initially with natural pheromone sources. In our review, data of daily rhythms of moths and other insects were extracted from the literature by screen capture software to calculate mean time of activity and standard deviation and fit to normal curves. These methods are illustrated for various insects and as a basis for discussion of interactions of pheromonal circadian rhythms of the well-studied gypsy moth Lymantria dispar, spruce budworm moth Choristoneura fumiferana, turnip moth Agrotis segetum, and cabbage looper moth Trichoplusia ni. The various circadian rhythms are discussed in relation to application of species-specific sex and aggregation pheromones for benign biological control and management of pest insects.

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References

  • Alford AR, Hammond AM Jr (1982) Temperature modification of female sex pheromone release in Trichoplusia ni (Hubner) and Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae). Environ Entomol 11:889–892

    Article  Google Scholar 

  • Aschoff J (1969) Phasenlage der Tagesperiodik in Abhängigkeit von Jahreszeit und Breitengrad. Oecologia 3:125–165

    Article  PubMed  Google Scholar 

  • Babilis NA, Mazomenos BE (1992) Pheromone production in Sesamia nonagrioides: diel periodicity and effect of age and mating. J Insect Physiol 38:561–564

    Article  CAS  Google Scholar 

  • Baker TC, Cardé RT (1979) Endogenous and exogenous factors affecting periodicities of female calling and male sex pheromone response in Grapholitha molesta (Busck). J Insect Physiol 25:943–950

    Article  Google Scholar 

  • Bashir T, Birkinshaw LA, Farman D, Hall DR, Hodges RJ (2003) Pheromone release by Rhyzopertha dominica (F.) (Coleoptera: Bostrichidae) in the laboratory: daily rhythm, inter-male variation and association with body weight and/or boring activity. J Stored Prod Res 39:159–169

    Article  Google Scholar 

  • Bento JMS, Parra JRP, Vilela EF, Walder JM, Leal WS (2001) Sexual behavior and diel activity of citrus fruit borer Ecdytolopha aurantiana. J Chem Ecol 27:2053–2065

    Article  CAS  PubMed  Google Scholar 

  • Bestmann HJ, Erler J, Vostrowsky O (1988) Determination of diel periodicity of sex pheromone release in three species of Lepidoptera by “closed-loop-stripping.” Experientia 44:797–799

    Article  CAS  Google Scholar 

  • Bjostad LB, Linn CE, Du JW, Roelofs WL (1984) Identification of new sex pheromone components in Trichoplusia ni, predicted from biosynthetic precursors. J Chem Ecol 10:1309–1323

    Article  CAS  PubMed  Google Scholar 

  • Bollinger JF, Shorey HH, Gaston LK (1977) Effect of several temperatures on the development and timing of responsiveness of males of Trichoplusia ni to the female sex pheromone. Environ Entomol 6:311–314

    Article  CAS  Google Scholar 

  • Borges M, Millar JG, Laumann RA, Moraes CB (2007) A male produced sex pheromone from the neotropical redbanded stink bug, Piezodorus guildinii (W.). J Chem Ecol 33:1235–1248

    Article  CAS  PubMed  Google Scholar 

  • Brady J (1979) Biological clocks. The Institute of Biology’s studies in biology no. 104. Edward Arnold Ltd., London

  • Brézot P, Malosse C, Mori K, Renou M (1994) Bisabolene epoxides in sex pheromone in Nezara viridula (L.) (Heteroptera: Pentatomidae) role of cis isomer and relation to specificity of pheromone. J Chem Ecol 20:3133–3147

    Article  PubMed  Google Scholar 

  • Byers JA (1981) Effect of mating on terminating aggregation during host colonization in the bark beetle, Ips paraconfusus. J Chem Ecol 7:1135–1147

    Article  CAS  PubMed  Google Scholar 

  • Byers JA (1983) Electronic fraction collector used for insect sampling in the photoperiod-induced diel emergence of bark beetles. Physiol Entomol 8:133–138

    Article  Google Scholar 

  • Byers JA (1987) Novel fraction collector for studying the oviposition rhythm in the turnip moth. Chronobiol Internat 4:189–194

    Article  CAS  Google Scholar 

  • Byers JA (2011) Analysis of vertical distributions and effective flight layers of insects: three-dimensional simulation of flying insects and catch at trap heights. Environ Entomol 40:1210–1222

    Article  PubMed  Google Scholar 

  • Byers JA (2012) Modelling female mating success during mass trapping and natural competitive attraction of searching males or females. Entomol Exp Appl 145:228–237

    Article  Google Scholar 

  • Byers JA (2013) Modeling and regression analysis of semiochemical dose-response curves of insect antennal reception and behavior. J Chem Ecol 39:1081–1089

    Article  CAS  PubMed  Google Scholar 

  • Byers JA, Löfqvist J (1989) Flight initiation and survival in the bark beetle Ips typographus (Coleoptera: Scolytidae) during the spring dispersal. Holarctic Ecol 12:432–440

    Google Scholar 

  • Byers JA, Fefer D, Levi-Zada A (2013) Sex pheromone component ratios and mating isolation among three Lygus plant bug species of North America. Naturwissenschaften 100:1115–1123

    Article  CAS  PubMed  Google Scholar 

  • Bäckman AC, Bengtsson M, Witzgall P (1997) Pheromone release by individual females of codling moth, Cydia pomonella. J Chem Ecol 23:807–815

    Article  Google Scholar 

  • Calvert I, Corbet SA (1973) Reproductive maturation and pheromone release in the flour moth Anagasta kuehniella (Zeller). J Entomol 47:201–209

    Google Scholar 

  • Cameron JH, Isman MB, Upadhyaya MK (2007) Trichoplusia ni growth and preference on brococoli and eight common agricultural weeds. Can J Plant Sci 87:413–421

    Article  Google Scholar 

  • Cameron EA, Knipling EF, Beroza M, Schwalbe CP (1974) Disruption of gypsy moth mating with microencapsulated disparlure. Science 183:972–973

    Article  CAS  PubMed  Google Scholar 

  • Cardé RT (1974) Diel periodicities of female calling and male pheromone attraction in Holomelina aurantiaca (Lepidoptera: Arctiidae). Can Entomol 106:933–944

    Article  Google Scholar 

  • Cardé RT, Willis MA (2008) Navigational strategies used by flying insects to find distant, wind-borne sources of odor. J Chem Ecol 34:854–866

    Article  PubMed  CAS  Google Scholar 

  • Cardé RT, Doane CC, Roelofs WL (1974) Diel periodicity of male sex pheromone response and female attractiveness in the gypsy moth (Lepidoptera: Lymantriidae). Can Entomol 106:479–484

    Article  Google Scholar 

  • Cardé RT, Charlton RE, Wallner WE, Baranchikov YN (1996) Pheromone-mediated diel activity rhythms of male Asian gypsy moths (Lepidoptera: Lymantriidae) in relation to female eclosion and temperature. Ann Entomol Soc Am 89:745–753

    Article  Google Scholar 

  • Castrejón-Gómez VR (2010) Evidence of a sex pheromone and daily calling pattern of females of Zamagiria dixolophella (Lepidoptera: Pyralidae). Fla Entomol 93:147–152

    Article  Google Scholar 

  • Castrovillo PJ, Cardé RT (1979) Environmental regulation of female calling and male pheromone response periodicities in the codling moth (Laspeyresia pomonella). J Insect Physiol 25:659–667

    Article  Google Scholar 

  • Charlton RE, Cardé RT (1982) Rate and diel periodicity of pheromone emission from female gypsy moths, (Lymantria dispar) determined with a glass-adsorption collection system. J Insect Physiol 28:423–430

    Article  Google Scholar 

  • Choi MY, Tatsuki S, Boo KS (1998) Regulation of sex pheromone biosynthesis in the oriental tobacco budworm, Helicoverpa assulta (Lepidoptera: Noctuidae). J Insect Physiol 44:653–658

    Article  CAS  Google Scholar 

  • Chon TS, Liang D, Schal C (1990) Effects of mating and grouping on oocyte development and pheromone release activities in Supella longipalpa (Dictyoptera: Blattellidae). Environ Entomol 19:1716–1721

    Article  Google Scholar 

  • Chuman T, Landolt PJ, Heath RR, Tumlinson JH (1987) Isolation, identification, and synthesis of male-produced sex pheromone of papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: Tephritidae). J Chem Ecol 13:1979–1992

    Article  CAS  PubMed  Google Scholar 

  • Cibrian-Tovari J, Mitchell ER (1991) Courtship behavior of Heliothis subflexa (gn.)(Lepidoptera: Noctuidae) and associated backcross insects obtained from hybridization with H. virescens (F.). Environ Entomol 20:419–426

    Article  Google Scholar 

  • Cloudsley-Thompson JL (1980) Biological Clocks. Camelot Press Limited, London

    Google Scholar 

  • Coffelt JA, Sower LL, Vick KW (1978) Quantitative analysis of identified compounds in pheromone gland rinses of Plodia interpunctella and Ephestia cautella at different times of day. Environ Entomol 7:502–505

    Article  CAS  Google Scholar 

  • Cooperband MF, Böröczky K, Hartness A, Jones TH, Zylstra KE, Tumlinson JH, Mastro VC (2012) Male-produced pheromone in the European woodwasp, Sirex noctilio. J Chem Ecol 38:52–62

    Article  CAS  PubMed  Google Scholar 

  • Cross JH, Byler RC, Silverstein RM, Greenblatt RE, Gorman JE, Burkholder WE (1977) Sex pheromone components and calling behavior of the female dermestid beetle, Trogoderma variabile Ballion (Coleoptera: Dermestidae). J Chem Ecol 3:115–125

    Article  CAS  Google Scholar 

  • David CT, Kennedy JS, Ludlow AR, Perry JN, Wall C (1982) A reappraisal of insect flight towards a distant point source of wind-borne odor. J Chem Ecol 8:1207–1215

    Article  CAS  PubMed  Google Scholar 

  • Delisle J, McNeil JN (1987) Calling behaviour and pheromone titre of the true armyworm Pseudaletia unipuncta (Haw.) (Lepidoptera: Noctuidae) under different temperature and photoperiodic conditions. J Insect Physiol 33:315–324

    Article  CAS  Google Scholar 

  • Delisle J, Royer L (1994) Changes in pheromone titer of oblique banded leafroller, Choristoneura rosaceana, virgin females as a function of time of day, age, and temperature. J Chem Ecol 20:45–66

    Article  CAS  PubMed  Google Scholar 

  • Delisle J, Picimbon JF, Simard J (1999) Physiological control of pheromone production in Choristoneura fumiferana and C. rosaceana. Arch Insect Biochem Physiol 42:253–265

    Article  CAS  PubMed  Google Scholar 

  • Dobson ID, Teal PEA (1986) Field studies of the temporal response patterns of male Diabrotica virgifera virgifera_LeConte an D. barberi Smith and Lawrence to 8R-methyl-2R-decyl propanoate. Physiol Entomol 11:405–410

    Article  Google Scholar 

  • Dong SL, Du JW (2001) Diel rhythms of calling behavior and sex pheromone production of beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae). Entomol Sinica 8:89–96

    Google Scholar 

  • Dunkelblum E, Kehat M, Harel M, Gordon D (1987) Sexual behaviour and pheromone titre of the Spodoptera littoralis female moth. Entomol Exp Appl 44:241–247

    Article  CAS  Google Scholar 

  • Eisenbach J, Mittler TE (1980) An aphid circadian rhythm: factors affecting the release of sex pheromone by oviparae of the greenbug, Schizaphis graminum. J Insect Physiol 26:511–515

    Article  Google Scholar 

  • Elkinton JS, Liebhold AM (1990) Population dynamics of gypsy moth in North America. Annu Rev Entomol 35:571–596

    Article  Google Scholar 

  • El-Sayed AM, Suckling DM, Wearing CH, Byers JA (2006) Potential of mass trapping for long-term pest management and eradication of invasive species. J Econ Entomol 99:1550–1564

    Article  CAS  PubMed  Google Scholar 

  • Epsky ND, Heath RR (1993) Pheromone production by male Anastrepha suspensa (Diptera: Tephritidae) under natural light cycles in greenhouse studies. Environ Entomol 22:464–469

    Article  CAS  Google Scholar 

  • Erasmus A, Van Rensburg JBJ, Van Den Berg J (2010) Effects of Bt Maize on Agrotis segetum (Lepidoptera: Noctuidae): A pest of maize seedlings. Environ Entomol 39:702–706

    Article  CAS  PubMed  Google Scholar 

  • Esbjerg P, Sigsgaard L (2014) Phenology and pest status of Agrotis segetum in a changing climate. Crop Prot 62:64–71

    Article  Google Scholar 

  • Eveleigh ES, McCann KS, McCarthy PC, Pollock SJ, Lucarotti CJ, Morin B, McDougall GA, Strongman DB, Huber JT, Umbanhowar J, Faria LDB (2007) Fluctuations in density of an outbreak species drive diversity cascades in food webs. Proc Nat Acad Sci Wash 104:16976–16981

    Article  CAS  Google Scholar 

  • Farine JP, Le Quere JL, Duffy J, Everaerts C, Brossut R (1994) Male sex pheromone of cockroach Eurycotis floridana (Walker) (Blattidae, Polyzosteriinae): role and composition of tergites 2 and 8 secretions. J Chem Ecol 20:2291–2306

    Article  CAS  PubMed  Google Scholar 

  • Farine JP, Sirugue D, Abed-Vieillard D, Everaerts C, Le Quéré JL, Bonnard O, Brossut R (2007) The male abdominal glands of Leucophaea maderae: chemical identification of the volatile secretion and sex pheromone function. J Chem Ecol 33:405–415

    Article  CAS  PubMed  Google Scholar 

  • Fatzinger CW (1973) Circadian rhythmicity of sex pheromone release by Dioryctria abietella (Lepidoptera: Pyralidae (Phycitinae) and the effect of a diel light cycle on its precopulatory behavior. Ann Entomol Soc Am 66:1147–1153

    Article  Google Scholar 

  • Faustini DL, Giese WL, Phillips JK, Burkholder WE (1982) Aggregation pheromone of the male granary weevil, Sitophilus granarius (L.). J Chem Ecol 8:679–686

    Article  CAS  PubMed  Google Scholar 

  • Field SA, Kaspi R, Yuval B (2002) Why do calling medflies (Diptera: Tephritidae) cluster? Assessing the empirical evidence for models of medfly lek evolution. Fla Entomol 85:63–72

    Article  Google Scholar 

  • Fleissner G, Fleissner G (2002) Perception of natural zeitgeber signals. In: Kumar V (ed) Biological Rhythms. Springer, Heidelberg, pp 83–93

    Chapter  Google Scholar 

  • Fonseca MG, Vidal DM, Zarbin PHG (2010) Male-produced sex pheromone of the cerambycid beetle Hedypathes betulinus: chemical identification and biological activity. J Chem Ecol 36:1132–1139

    Article  CAS  PubMed  Google Scholar 

  • Foster SP (2000) Periodicity of sex pheromone biosynthesis, release and degradation in the lightbrown apple moth, Epiphyas postvittana (Walker). Arch Insect Biochem Physiol 43:125–136

    Article  CAS  PubMed  Google Scholar 

  • Foster SP, Roelofs WL (1994) Regulation of pheromone production in virgin and mated females of two tortricid moths. Arch Insect Biochem Physiol 25:271–285

    Article  CAS  Google Scholar 

  • Foster SP, Anderson KG, Casas J (2020) Calling behavior and sex pheromone release and storage in the moth Chloridea virescens. J Chem Ecol 46:10–20

    Article  CAS  PubMed  Google Scholar 

  • Garcia J, Escaneula M, Bhat S, Lampert E (2020) The Trichoplusia ni gut microbiome and its derivation from the phylloshpere of its food plants. Georgia Journal of Science 78, No. 2, Article 9.

  • Geiselhardt S, Jakobschy D, Ockenfels P, Peschke K (2008) A sex pheromone in the desert tenebrionid beetle Parastizopus armaticeps. J Chem Ecol 34:1065–1071

    Article  CAS  PubMed  Google Scholar 

  • Gerber GH, Howlader MA (1987) The effects of photoperiod and temperature on calling behaviour and egg development of the bertha armyworm, Mamestra configurata (Lepidoptera: Noctuidae). J Insect Physiol 33:429–436

    Article  Google Scholar 

  • Giebultowicz JM, Webb RE, Raina AK, Ridgway RL (1992) Effects of temperature and age on daily changes in pheromone titer in laboratory-reared and wild gypsy moth (Lepidoptera: Lymantriidae). Environ Entomol 21:822–826

    Article  Google Scholar 

  • Goodbody TRH, Coops NC, Hermosilla T, Tompalski P, McCartney G, MacLean DA (2018) Digital aerial photogrammetry for assessing cumulative spruce budworm defoliation and enhancing forest inventories at a landscape-level. ISPRS J Photogramm Remote Sens 142:1–11

    Article  Google Scholar 

  • Gorsuch CS, Karandinos MG, Koval CF (1975) Daily rhythm of Synanthedon pictipes (Lepidoptera: Aegeriidae) female calling behavior in Wisconsin: temperature effects. Entomol Exp Appl 18:367–376

    Article  Google Scholar 

  • Gray DR (2008) The relationship between climate outbreak characteristics of the spruce budworm in eastern Canada. Clim Change 87:361–383

    Article  CAS  Google Scholar 

  • Groot AT (2014) Circadian rhythms of sexual activities in moths: a review. Frontiers in Ecology and Evolution 2:article 43, 1–21

  • Gueldner RC, Wiygul G (1978) Rhythms in pheromone production of the male boll weevil. Science 199:984–986

    Article  CAS  PubMed  Google Scholar 

  • Guldemond JA, Tigges WT, De Vrijer PWF (1994) Circadian rhythm of sex pheromone production and male activity of coexisting sibling species of Cryptomyzus aphids (Homoptera: Aphididae). Eur J Entomol 91:85–89

    CAS  Google Scholar 

  • Hall DR, Cork A, Phythian SJ, Chittamuru S, Jayarama BK, Venkatesha MG, Sreedharan K, Vinod Kumar PK, Seetharama HG, Naidu R (2006) Identification of components of male-produced pheromone of coffee white stemborer, Xylotrechus quadripes. J Chem Ecol 32:195–219

    Article  CAS  PubMed  Google Scholar 

  • Halstead DGH (1973) Preliminary biological studies on the pheromone produced by male Acanthoscelides obtectus (Say) (Coleoptera: Bruchidae). J Stored Prod Res 9:109–117

    Article  CAS  Google Scholar 

  • Hamilton JGC, Dawson GW, Pickett JA (1996) 3-Methyl-α-himachalene: proposed structure for novel homosesquiterpene sex pheromone of Lutzomyia longipalpis (Diptera: Psychodidae) from Jacobina, Brazil. J Chem Ecol 22:2331–2340

    Article  CAS  PubMed  Google Scholar 

  • Hammack L, Bukkholder WE (1976) Circadian rhythm of sex pheromone-releasing behaviour in females of the dermestid beetle, Trogoderma glabrum: regulation by photoperiod. J Insect Physiol 22:385–388

    Article  CAS  Google Scholar 

  • Haynes KF, Baker TC (1988) Potential for evolution of resistance to pheromones: worldwide and local variation in chemical communication system of pink bollworm moth. Pectinophora Gossypiella J Chem Ecol 14:1547

    Article  CAS  PubMed  Google Scholar 

  • Haynes KF, Birch MC (1984) The periodicity of pheromone release and male responsiveness in the artichoke plume moth, Platyptilia carduidactyla. Physiol Entomol 9:287–295

    Article  Google Scholar 

  • Haynes KF, Gaston LK, Mistrot Pope M, Baker TC (1983) Rate and periodicity of pheromone release from individual female artichoke plume moths, Platyptilia carduidactyla (Lepidoptera: Pterophoridae). Environ Entomol 12:1597–1600

    Article  CAS  Google Scholar 

  • Heath RR, Landolt PJ, Dueben BD, Murphy RE, Schneider RE (1992) Identification of male cabbage looper sex pheromone attractive to females. J Chem Ecol 18:441–453

    Article  CAS  PubMed  Google Scholar 

  • Heath RR, McLaughlin JR, Proshold F, Teal PEA (1991) Periodicity of female sex pheromone titer and release in Heliothis subflexa and H. virescens (Lepidoptera: Noctuidae). Ann Entomol Soc Am 84:182–189

    Article  CAS  Google Scholar 

  • Heath RR, Manukian A, Epsky ND, Sivinski J, Calkins CO, Landolt PJ (1993) A bioassay system for collecting volatiles while simultaneously attracting tephritid fruit flies. J Chem Ecol 19:2395–2410

    Article  CAS  PubMed  Google Scholar 

  • Hendrichs J, Hendrichs MA (1990) Mediterranean fruit fly (Diptera: Tephritidae) in nature: location and diel pattern of feeding and other activities on fruiting and nonfruiting hosts and nonhosts. Ann Entomol Soc Am 83:632–641

    Article  Google Scholar 

  • Hendricks DE (1985) Portable electronic detector system used with inverted-cone sex pheromone traps to determine periodicity and moth captures. Environ Entomol 14:199–204

    Article  Google Scholar 

  • Hoglund U, Alatalo RV (1995) Leks. Princeton University Press, Princeton, NJ, USA

    Book  Google Scholar 

  • Hoo CRS, Coudriet DL, Vail PV (1984) Trichoplusia ni (Lepidoptera: Noctuidae) larval development on wild and cultivated plants. Environ Entomol 13:843–846

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46:10–18

    Article  Google Scholar 

  • Hunt RE, Haynes KF (1990) Periodicity in the quantity and blend ratios of pheromone components in glands and volatile emissions of mutant and normal cabbage looper moths, Trichoplusia ni. J Insect Physiol 36:769–774

    Article  CAS  Google Scholar 

  • Ichikawa T (1998) Activity patterns of neurosecretory cells releasing pheromonotropic neuropeptides in the moth Bombyx mori. Proc Nat Acad Sci Wash 95:4055–4060

    Article  CAS  Google Scholar 

  • Itagaki H, Conner WE (1988) Calling behavior of Manduca sexta (L.) (Lepidoptera: Sphingidae) with notes on the morphology of the female sex pheromone gland. Ann Entomol Soc Am 81:798–807

    Article  Google Scholar 

  • Jacobson M, Ohinata K, Chambers DL, Jones WA, Fujimoto MS (1973) Insect sex attractants. 13. Isolation, identification, and synthesis of sex pheromones of the male Mediterranean fruit fly. J Med Chem 16:248–251

    Article  CAS  PubMed  Google Scholar 

  • Jarvis EK, Rutledge LC (1992) Laboratory observations on mating and leklike aggregations in Lutzomyia longipalpis (Diptera: Psychodidae). J Med Entomol 29:171–177

    Article  CAS  PubMed  Google Scholar 

  • Jones MDR, Gubbins SJ (1979) Modification of female circadian flight-activity by a male accessory gland pheromone in the mosquito, Culex pipiens quinquefasciatus. Physiol Entomol 4:345–351

    Article  Google Scholar 

  • Kamimura M, Tatsuki S (1993) Diel rhythms of calling behavior and pheromone production of oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J Chem Ecol 19:2953–2963

    Article  CAS  PubMed  Google Scholar 

  • Kamimura M, Tatsuki S (1994) Effects of photoperiodic changes on calling behavior and pheromone production in the oriental tobacco budworm moth, Helicoverpa assulta (Lepidoptera: Noctuidae). J Insect Physiol 40:731–734

    Article  Google Scholar 

  • Kaneko J (1986) Effect of temperature on the timing of calling of the yellow peach moth Congethes punctiferalis (Guenée) (Lepidoptera: Pyralidae). Jpn J Appl Entomol Z 30:239–246

    Article  Google Scholar 

  • Kaster LV, Showers WB, Mulder PG (1989) Seasonality in the hourly reproductive behavior of adult Agrotis ipsilon (Lepidoptera: Noctuidae) in Iowa. Environ Entomol 18:674–677

    Article  Google Scholar 

  • Kawasaki K (1986) Activity rhythms and behavior of adult Spodoptera litura F. (Lepidoptera: Noctuidae) at night: factors determining male attraction time by females. Appl Entomol Zool 21:493–499

    Article  Google Scholar 

  • Kawasaki K, Tamaki Y, Nakamura K (1983) Seasonal difference in diel periodicity of male attraction of the smaller tea tortrix moth Adoxophyes-sp (Lepidoptera: Tortricidae) to synthetic sex pheromones and virgin females. Jpn J Appl Entomol Z 27:106–111

    Article  Google Scholar 

  • Khoo CCH, Yuen KH, Tan KH (2000) Attraction of female Bactrocera papayae to sex pheromone components with two different release devices. J Chem Ecol 26:2487–2496

    Article  CAS  Google Scholar 

  • Kipp LR, Lonergan GC, Bell WJ (1995) Male periodicity and the timing of mating in the spruce budworm (Lepidoptera: Tortricidae): influences of population density and temperature. Environ Entomol 24:1150–1159

    Article  Google Scholar 

  • Kochansky JP, Cardé RT, Taschenberg EF, Roelofs WL (1977) Rhythms of male Antheraea polyphemus attraction and female attractiveness, and an improved pheromone synthesis. J Chem Ecol 3:419–427

    Article  CAS  Google Scholar 

  • Konno Y (1986) Time-lag between sex pheromone content and the calling behavior in the yellow peach moth, Conogethes punctiferalis (Guenee) (Lepidoptera: Pyralidae). Appl Entomol Zool 21:622–624

    Article  CAS  Google Scholar 

  • Konstantopoulou MA, Pratsinis H, Kletsas D, Mazomenos BE (2006) Pheromone-binding protein and general odorant binding protein of Sesamia nonagrioides: sex- and diel-dependent expression. Entomol Exp Appl 119:129–136

    Article  CAS  Google Scholar 

  • Kou R, Chow YS (1987) Calling behavior of the cotton bollworm, Heliothis armigera (Lepidoptera: Noctuidae). Ann Entomol Soc Am 80:490–493

    Article  Google Scholar 

  • Krupke CH, Jones VP, Brunner JF (2006) Diel periodicity of Euschistus conspersus (Heteroptera: Pentatomidae) aggregation, mating, and feeding. Ann Entomol Soc Am 99:169–174

    Article  Google Scholar 

  • Kumara ADNT, Chandrashekharaiah M, Subaharan K, Chakravarthy AK (2015) Periodicity of adult emergence and sexual behaviour of coconut black headed caterpillar, Opisina arenosella Walker (Lepidoptera: Oecophoridae). Phytoparasitica 43:701–712

    Article  Google Scholar 

  • Landolt PJ, Heath RR (1988) Effects of age, mating, and time of day on behavioral responses of female papaya fruit fly, Toxotrypana curvicauda Gerstaecker (Diptera: Tephritidae), to synthetic sex pheromone. Environ Entomol 17:47–51

    Article  CAS  Google Scholar 

  • Leal WS, Sawada M, Matsuyama S, Kuwahara Y, Hasegawa M (1993) Unusual periodicity of sex pheromone production in the large black chafer Holotrichia parallela. J Chem Ecol 19:1381–1391

    Article  CAS  PubMed  Google Scholar 

  • Leal WS, Hasegawa M, Sawada M, Ono M, Tada S (1996) Scarab beetle Anomala albopilosa albopilosa utilizes a more complex sex pheromone system than a similar species A. cuprea. J Chem Ecol 22:2001–2010

    Article  CAS  Google Scholar 

  • Levi-Zada A, Nestel D, Fefer D, Nemni-Lavy E, Deloya-Kahane I, David M (2012) Analyzing diurnal and age–related pheromone emission of the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae) by sequential SPME–GCMS analysis. J Chem Ecol 38:1036–1041

    Article  CAS  PubMed  Google Scholar 

  • Levi-Zada A, Sadowsky A, Dobrinin S, David M, Ticuchinski T, Fefer D, Greenberg A, Blumberg D (2013) Reevaluation of the sex pheromone of the lesser date moth, Batrachedra amydraula, using autosampling SPME-GC/MS and field bioassays. Chemoecology 23:13–20

    Article  CAS  Google Scholar 

  • Levi-Zada A, David M, Fefer D, Seplyarsky V, Sadowsky A, Dobrinin S, Ticuchinski T, Harari D, Blumberg D, Dunkelblum E (2014) Circadian release of male-specific components of the greater date moth, Aphomia (Arenipses) sabella, using sequential SPME/GC/MS analysis. J Chem Ecol 40:236–243

    Article  CAS  PubMed  Google Scholar 

  • Levi-Zada A, Fefer D, David M, Eliyahu M, Franco JC, Protasov A, Dunkelblum E, Mendel Z (2014) Diel periodicity of pheromone release by females of Planococcus citri and Planococcus ficus and the temporal flight activity of their conspecific males. Naturwissenschaften 101:671–678

    Article  CAS  PubMed  Google Scholar 

  • Levi-Zada A, Sadowsky A, Dobrinin S, Ticuchinski T, David M, Fefer D, Dunkelblum E, Byers JA (2018) Monitoring and mass-trapping methodologies using pheromones: the lesser date moth Batrachedra amydraula. Bull Entomol Res 108:58–68

    Article  CAS  PubMed  Google Scholar 

  • Levi-Zada A, Steiner S, Fefer D, Kaspi R (2019) Identification of the sex pheromone of the spherical mealybug Nipaecoccus viridis. J Chem Ecol 45:455–463

    Article  CAS  PubMed  Google Scholar 

  • Levi-Zada A, Fefer D, Madar R, Steiner S, Kaspi R (2020) Evaluation of pheromone of false codling moth Thaumatotibia leucotreta in Israel by sequential SPME/GCMS analysis and field trials. J Pest Sci 93:519–529

    Article  Google Scholar 

  • Levi-Zada A, Levy A, Rempoulakis P, Fefer D, Steiner S, Gazit Y, Nestel D, Yuval B, Byers JA (2020b) Diel rhythm of volatile emissions of males and females of the peach fruit fly Bactrocera zonata. J Insect Physiol 120: in press

  • Liang D, Schal C (1990) Circadian rhythmicity and development of the behavioural response to sex pheromone in male brown-banded cockroaches, Supella longipalpa. Physiol Entomol 15:355–361

    Article  CAS  Google Scholar 

  • Liang D, Schal C (1993) Calling behavior of the female German cockroach, Blattella germanica (Dictyoptera: Blattellidae). J Insect Behav 6:603–614

    Article  Google Scholar 

  • Linn CE Jr, Roelofs WL (1992) Role of photoperiod cues in regulating the modulatory action of octopamine on pheromone-response thresholds in the cabbage looper moth. Arch Insect Biochem Physiol 20:285–302

    Article  CAS  Google Scholar 

  • Linn CE, Campbell MG, Poole KR, Wu WQ, Roelofs WL (1996) Effects of photoperiod on the circadian timing of pheromone response in male Trichoplusia ni: relationship to the modulatory action of octopamine. J Insect Physiol 42:881–891

    Article  CAS  Google Scholar 

  • Liu H, Zhao W, Yang M, Liu J, Zhang J (2013) Diel rhythms of sexual behavior and pheromone titers in Isoceras sibirica Alpheraky (Lepidoptera, Cossidae). Arch Insect Biochem Physiol 84:15–26

    Article  CAS  PubMed  Google Scholar 

  • Lu Q, Huang LY, Liu FT, Wang XF, Chen P, Xu J, Deng JY, Ye H (2017) Sex pheromone titre in the glands of Spodoptera litura females: circadian rhythm and the effects of age and mating. Physiol Entomol 42:156–162

    Article  CAS  Google Scholar 

  • Löfstedt C, Van Der Pers JNC, Löfqvist J, Lanne BS, Appelgren M, Bergström G, Thelin B (1982) Sex pheromone components of the turnip moth, Agrotis segetum: chemical identification, electrophysiological evaluation and behavioral activity. J Chem Ecol 8:1305–1321

    Article  PubMed  Google Scholar 

  • Ma M, Burkholder WE (1978) Sex pheromone releasing behavior of Anthrenus flavipes (furniture carpet beetles) females (Coleoptera: Dermestidae). Ann Entomol Soc Am 71:129–133

    Article  Google Scholar 

  • Margaritopoulos JT, Malarky G, Tsitsipis JA, Blackman RL (2007) Microsatellite DNA and behavioural studies provide evidence of host-mediated speciation in Myzus persicae (Hemiptera: Aphididae). Biol J Linn Soc 91:687–702

    Article  Google Scholar 

  • Del Mazo-Cancino A, Malo EA, Cruz-López L, Rojas JC (2004) Diel periodicity and influence of age and mating on female sex pheromone titre in Estigmene acrea (Lep., Arctiidae). J Appl Entomol 128:459–463

    Article  Google Scholar 

  • Mazor M, Dunkelblum E (2005) Circadian rhythms of sexual behavior and pheromone titers of two closely related moth species Autographa gamma and Cornutiplusia circumflexa. J Chem Ecol 31:2153–2168

    Article  CAS  PubMed  Google Scholar 

  • Mbata GN, Ramaswamy SB (1990) Rhythmicity of sex pheromone content in female Heliothis virescens: impact of mating. Physiol Entomol 15:423–432

    Article  CAS  Google Scholar 

  • McBrien HL, Millar JG, Gottlieb L, Chen X, Rice RE (2001) Male-produced sex attractant pheromone of the green stink bug, Acrosternum hilare (Say). J Chem Ecol 27:1821–1839

    Article  CAS  PubMed  Google Scholar 

  • McBrien HL, Millar JG, Rice RE, McElfresh JS, Cullen E, Zalom FG (2002) Sex attractant pheromone of the red-shouldered stink bug Thyanta pallidovirens: a pheromone blend with multiple redundant components. J Chem Ecol 28:1797–1817

    Article  CAS  PubMed  Google Scholar 

  • McGhee PS, Miller JR, Thompson DR, Gut LJ (2016) Optimizing aerosol dispensers for mating disruption of codling moth, Cydia pomonella L. J Chem Ecol 42:612–616

    Article  CAS  PubMed  Google Scholar 

  • McLaughlin JR, Heath RR, Ashley TR (1990) Periodicity of pheromone release from female white peach scale. Physiol Entomol 15:193–197

    Article  Google Scholar 

  • McNeil JN, Brodeur J (1995) Pheromone-mediated mating in the aphid parasitoid, Aphidius nigripes (Hymenoptera: Aphididae). J Chem Ecol 21:959–971

    Article  CAS  PubMed  Google Scholar 

  • Merlin C, Lucas P, Rochat D, François MC, Maïbèche-Coisne M, Jacquin-Joly E (2007) An antennal circadian clock and circadian rhythms in peripheral pheromone reception in the moth Spodoptera littoralis. J Biol Rhythms 22:502–514

    Article  CAS  PubMed  Google Scholar 

  • Ming QL, Yan YH, Wang CZ (2007) Mechanisms of premating isolation between Helicoverpa armigera (Hübner) and Helicoverpa assulta (Guenée) (Lepidoptera: Noctuidae). J Insect Physiol 53:170–178

    Article  CAS  PubMed  Google Scholar 

  • Monti L, Lalanne-Cassou B, Lucas P, Malosse C, Silvain JF (1995) Differences in sex pheromone communication systems of closely related species: Spodoptera latifascia (Walker) and S. descoinsi Lalanne-Cassou & Silvain (Lepidoptera: Noctuidae). J Chem Ecol 21:641–660

    Article  CAS  PubMed  Google Scholar 

  • Morse D, Szittnerg R, Grant GG, Meighen EA (1982) Rate of pheromone release by individual spruce budworm moths. J Insect Physiol 28:863–866

    Article  CAS  Google Scholar 

  • Mozuraitis R, Buda V, Borg-Karlson AK, Ivinskis P (1997) Chemocommunication in Phyllonorycter ulmifoliella (Hbn.) (Lepidoptera: Gracillariidae): periodicity, sex pheromone, and inhibitors. J Chem Ecol 23:175–189

    Article  CAS  Google Scholar 

  • Nagari M, Szyszka P, Galizia G, Bloch G (2017) Task-related phasing of circadian rhythms in antennal responsiveness to odorants and pheromones in honeybees. J Biol Rhythms 32:593–608

    Article  CAS  PubMed  Google Scholar 

  • Nation JL (1990) Biology of pheromone release by male Caribbean fruit flies, Anastrepha suspensa (Diptera: Tephritidae). J Chem Ecol 16:553–571

    Article  CAS  PubMed  Google Scholar 

  • Nealis VG, Turnquist R, Morin B, Graham RI, Lucarotti CJ (2015) Baculoviruses in populations of western spruce budworm. J Invertebr Pathol 127:76–80

    Article  CAS  PubMed  Google Scholar 

  • Nojima S, Classen A, Groot AT, Schal C (2018) Qualitative and quantitative analysis of chemicals emitted from the pheromone gland of individual Heliothis subflexa females. Plos One 13:e0202035

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Odell TM (1978) Periodicity of eclosion and pre-mating behavior of gypsy moth. Ann Entomol Soc Am 71:748–751

    Article  Google Scholar 

  • Ono T, Charlton RE, Cardé RT (1990) Variability in pheromone composition and periodicity of pheromone titer in potato tuberworm moth, Phthorimaea operculella (Lepidoptera: Gelechiidae). J Chem Ecol 16:531–542

    Article  CAS  PubMed  Google Scholar 

  • Pain J, Roger B (1978) Circadian rhythm of 9-ketodec-2-enoic acid, queen pheromone, and 10-hydroxydec-2-enoic acid of worker bees, Apis mellifica ligustica S. Apidologie 9:263–272

    Article  CAS  Google Scholar 

  • Pashley DP, Hammond AM, Hardy TN (1992) Reproductive isolating mechanisms in fall armyworm host strains (Lepidoptera: Noctuidae). Ann Entomol Soc Am 85:400–405

    Article  Google Scholar 

  • Pope MM, Gaston LK, Baker TC (1982) Composition, quantification, and periodicity of sex pheromone gland volatiles from individual Heliothis virescens females. J Chem Ecol 8:1043–1055

    Article  CAS  PubMed  Google Scholar 

  • Pope MM, Gaston LK, Baker TC (1984) Composition, quantification, and periodicity of sex pheromone volatiles from individual Heliothis zea females. J Insect Physiol 30:943–945

    Article  CAS  Google Scholar 

  • Quartey GK, Coaker TH (1996) Periodicity of activity and sexual response of adult Ephestia cautella (Walk.) (Lep., Phycitidae). J Appl Entomol 120:335–339

    Article  Google Scholar 

  • Quilici S, Franck A, Peppuy A, Dos Reis CE, Mouniama C, Blard F (2002) Comparative studies of courtship behavior of Ceratitis spp. (Diptera: Tephritidae) in reunion island. Fla Entomol 85:138–142

    Article  Google Scholar 

  • Rafaeli A, Klein Z (1994) Regulation of pheromone production by female pink bollworm moths Pectinophora gossypiella (Sanders) (Lepidoptera: Gelechiidae). Physiol Entomol 19:159–164

    Article  CAS  Google Scholar 

  • Raina AK, Klun JA, Stadelbacher EA (1986) Diel periodicity and effect of age and mating on female sex pheromone titer in Heliothis zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 79:128–131

    Article  CAS  Google Scholar 

  • Raina AK, Davis JC, Stadelbacher EA (1991) Sex pheromone production and calling in Helicoverpa zea (Lepidoptera: Noctuidae): effect of temperature and light. Environ Entomol 20:1451–1456

    Article  Google Scholar 

  • Ramaswamy SB, Ma PWK, Pitre HN (1988) Calling rhythm and pheromone titers in Spodoptera frugiperda (JE Smith) (Lep., Noctuidae) from Mississippi and Honduras. J Appl Entomol 106:90–96

    Article  Google Scholar 

  • Rechav Y (1978) Lack of daily rhythm in the release of assembly pheromones by the tick Amblyomma hebraeum (Koch). Experientia 34:478–479

    Article  CAS  Google Scholar 

  • Robacker DC (1988) Behavioral responses of female Mexican fruit flies, Anastrepha ludens, to components of male-produced sex pheromone. J Chem Ecol 14:1715–1726

    Article  CAS  PubMed  Google Scholar 

  • Robacker DC, Aluja M, Cossé AA, Sacchetti P (2009) Sex pheromone investigation of Anastrepha serpentina (Diptera: Tephritidae). Ann Entomol Soc Am 102:560–566

    Article  CAS  Google Scholar 

  • Rosén W (2002) Endogenous control of circadian rhythms of pheromone production in the turnip moth, Agrotis segetum. Arch Insect Biochem Physiol 50:21–30

    Article  PubMed  CAS  Google Scholar 

  • Rosén WQ, Han GB, Löfstedt C (2003) The circadian rhythm of the sex-pheromone-mediated behavioral response in the turnip moth, Agrotis segetum, is not controlled at the peripheral level. J Biol Rhythms 18:402–408

    Article  PubMed  CAS  Google Scholar 

  • Royama T (1984) Population Dynamics of the Spruce Budworm Choristoneura fumiferana. Ecol Monogr 54:429–462

    Article  Google Scholar 

  • Royer L, McNeil JN (1991) Changes in calling behaviour and mating success in the European corn borer (Ostrinia nubilalis), caused by relative humidity. Entomol Exper Appl 61:131–138

    Article  Google Scholar 

  • Rymer J, Bauernfeind AL, Brown S, Page TL (2007) Circadian rhythms in the mating behavior of the cockroach, Leucophaea maderae. J Biol Rhythms 22:43–57

    Article  PubMed  Google Scholar 

  • Régnière J, Nealis VG (2007) Ecological mechanisms of population change during outbreaks of the spruce budworm. Ecol Entomol 32:461–477

    Article  Google Scholar 

  • Saario CA, Shorey HH, Gaston LK (1970) Sex pheromones of noctuid moths. XIX. Effect of environmental and seasonal factors on captures of males of Trichoplusia ni in pheromone-baited traps. Ann Entomol Soc Am 63:667–672

    Article  Google Scholar 

  • Sadek MM, Von WG, Löfstedt C, Rosén WQ, Anderson P (2012) Modulation of the temporal pattern of calling behavior of female Spodoptera littoralis by exposure to sex pheromone. J Insect Physiol 58:61–66

    Article  CAS  PubMed  Google Scholar 

  • Sasaerila Y, Gries G, Gries R, Boo TC (2000) Specificity of communication channels in four limacodid moths: Darna bradleyi, Darna trima, Setothosea asigna, and Setora nitens (Lepidoptera: Limacodidae). Chemoecol 10:193–199

    Article  CAS  Google Scholar 

  • Schal C, Charlton RE, Cardé RT (1987) Temporal patterns of sex pheromone titers and release rates in Holomelina lamae (Lepidoptera: Arctiidae). J Chem Ecol 13:1115–1129

    Article  CAS  PubMed  Google Scholar 

  • Schlamp KK, Brown K, Gries R, Hart M, Gries G, Judd GGR (2006) Diel periodicity of sexual communication in Anarsia lineatella (Lepidoptera: Gelechiidae). Can Entomol 138:384–389

    Article  Google Scholar 

  • Schuckel J, Siwicki KK, Stengl M (2007) Putative circadian pacemaker cells in the antenna of the hawkmoth Manduca sexta. Cell Tissue Res 330:271–278

    Article  PubMed  Google Scholar 

  • Segura D, Petit-Marty N, Sciurano R, Vera T, Calcagno G, Allinghi A, Cendra PG, Cladera J, Vilardi J (2007) Lekking behavior of Anastrepha fraterculus (Diptera: Tephritidae). Fla Entomol 90:154–162

    Article  Google Scholar 

  • Shelly TE (2001) Lek size and female visitation in two species of tephritid fruit flies. Anim Behav 62:33–40

    Article  Google Scholar 

  • Silvegren G, Löfstedt C, Rosén WQ (2005) Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis. J Insect Physiol 51:277–286

    Article  CAS  PubMed  Google Scholar 

  • Skabeikis DD, Teale SA, Fierke MK (2016) Diel rhythms in Monochamus (Coleoptera: Cerambycidae): production of and response to a male-produced aggregation pheromone. Environ Entomol 45:1017–1021

    Article  CAS  PubMed  Google Scholar 

  • Smith AF, Schal C (1991) Circadian calling behavior of the adult female brown-banded cockroach, Supella longipalpa (F.) (Dictyoptera: Blattellidae). J Insect Behav 4:1–14

    Article  Google Scholar 

  • Sollai G, Solari P, Crnjar R (2018) Olfactory sensitivity to major, intermediate and trace components of sex pheromone in Ceratitis capitata is related to mating and circadian rhythm. J Insect Physiol 110:23–33

    Article  CAS  PubMed  Google Scholar 

  • Sower LL, Shorey HH, Gaston LK (1971a) Sex pheromones of noctuid moths. XXV. Effects of temperature and photoperiod on circadian rhythms of sex pheromone release by females of Trichoplusia ni. Ann Entomol Soc Am 64:488–492

    Article  Google Scholar 

  • Sower LL, Shorey HH, Gaston LK (1971b) Sex pheromones of noctuid moths. XXVI. female release rate, male response threshold, and communication distance for Trichoplusia ni. Ann Entomol Soc Am 64:1448–1456

    Article  Google Scholar 

  • Sreng L (1990) Seducin, male sex pheromone of the cockroach Nauphoeta cinerea: isolation, identification, and bioassay. J Chem Ecol 16:2899–2912

    Article  CAS  PubMed  Google Scholar 

  • Stevenson DE, Harris MK (2009) Determining circadian response of adult male Acrobasis nuxvorella (Lepidoptera: Pyralidae) to synthetic sex attractant pheromone through time-segregated trapping with a new clockwork timing trap. Environ Entomol 38:1690–1696

    Article  PubMed  Google Scholar 

  • Stewart-Jones A, Dewhirst SY, Durrant L, Fitzgerald JD, Hardie J, Hooper AM, Pickett JA, Poppy GM (2007) Structure, ratios and patterns of release in the sex pheromone of an aphid, Dysaphis plantaginea. J Exp Biol 210:4335–4344

    Article  CAS  PubMed  Google Scholar 

  • Svensson GP, Valeur PG, Reynolds DR, Smith AD, Riley JR, Baker TC, Poppy GM, Löfstedt C (2001) Mating disruption in Agrotis segetum monitoried by hamonic radar. Entomol Exp Appl 101:111–121

    Article  CAS  Google Scholar 

  • Tang JD, Charlton RE, Cardé RT, Yin CM (1992) Diel periodicity and influence of age and mating on sex pheromone titer in gypsy moth, Lymantria dispar (L.). J Chem Ecol 18:749–760

    Article  CAS  PubMed  Google Scholar 

  • Teal PEA (1985) The effect of hybridization on the periodicity of sex pheromone release of Euxoa species (Lepidoptera: Noctuidae). Physiol Entomol 10:463–466

    Article  Google Scholar 

  • Thieme T, Dixon AEG (1996) Mate recognition in the Aphis fabae complex: daily rhythm of release and specificity of sex pheromones. Entomol Exp Appl 79:85–89

    Article  CAS  Google Scholar 

  • Tobin PC, Klein KT, Leonard DS (2009) Gypsy moth (Lepidoptera: Lymantriidae) flight behavior and phenology based on field-deployed automated pheromone-baited traps. Environ Entomol 38:1555–1562

    Article  PubMed  Google Scholar 

  • Todd JL, Baker TC (1999) Function of peripheral olfactory organs. In: Hansson BS (ed) Insect Olfaction. Springer, Berlin, pp 67–96

    Chapter  Google Scholar 

  • Valles SM, Heath RR, Capinera JL (1992) Production and release of sex pheromone by Diaphania nitidalis (Lepidoptera: Pyralidae): periodicity, age, and density effects. Ann Entomol Soc Am 85:731–735

    Article  CAS  Google Scholar 

  • Wang Q, Zeng W, Chen L, Li J, Yin X (2002) Circadian reproductive rhythms, pair-bonding, and evidence for sex-specific pheromones in Nadezhdiella cantori (Coleoptera: Cerambycidae). J Insect Behav 15:527–539

    Article  Google Scholar 

  • Wang P, Chen GF, Zhang JS, Xue Q, Zhang JH, Chen C, Zhang QH (2017) Pheromone-trapping the nun moth, Lymantria monacha (Lepidoptera: Lymantriidae) in inner Mongolia, China. Insect Sci 24:631–639

    Article  CAS  PubMed  Google Scholar 

  • Webster RP, Cardé RT (1982) Influence of relative humidity on calling behaviour of the female European corn borer moth (Ostrinia nubilalis). Entomol Exp Appl 32:181–185

    Article  Google Scholar 

  • Webster RP, Cardé RT (1982) Relationships among pheromone titre, calling and age in the omnivorous leafroller moth (Platynota stultana). J Insect Physiol 28:925–933

    Article  CAS  Google Scholar 

  • Webster RP, Cardé RT (1984) The effects of mating, exogenous juvenile hormone and a juvenile hormone analogue on pheromone titre, calling and oviposition in the omnivorous leafroller moth (Platynota stultana). J Insect Physiol 30:113–118

    Article  CAS  Google Scholar 

  • Wicker-Thomas C (2007) Pheromonal communication involved in courtship behavior in Diptera. J Insect Physiol 53:1089–1100

    Article  CAS  PubMed  Google Scholar 

  • Witzgall P, Frérot B (1989) Pheromone emission by individual females of carnation tortrix, Cacoecimorpha pronubana. J Chem Ecol 15:707–717

    Article  CAS  PubMed  Google Scholar 

  • Worster AS, Seabrook WD (1989) Electrophysiological investigation of diel variations in the antennal sensitivity of the male spruce budworm moth Choristoneura fumiferana (Lepidoptera: Tortricidae). J Insect Physiol 35:1–5

    Article  Google Scholar 

  • Xiang YY, Yang MF, Li ZZ (2010) Calling behavior and rhythms of sex pheromone production in the black cutworm moth in China. J Insect Behav 23:35–44

    Article  Google Scholar 

  • Zhang QH, Paiva MR (1998) Female calling behaviour and male response to the sex pheromone in Thaumefopoea pityocampa (Den. & Schiff.) (Lep., Thaumetopoeidae). J Appl Entomol 122:353–360

    Article  Google Scholar 

  • Zhang QH, Schlyter F, Chu D, Ma XY, Ninomiya Y (1996) Female calling behaviour and response of males to synthetic pheromone and virgin females in spring and summer generations of Hyphantria cunea (Lep., Arctiidae) (Drury) in Northeastern China. J Appl Entomol 120:467–476

    Article  Google Scholar 

  • Zarbin PHG, Lorini LM, Ambrogi BG, Vidal DM, Lima ER (2007) Sex pheromone of Lonomia obliqua: daily rhythm of production, identification, and synthesis. J Chem Ecol 33:555–565

    Article  CAS  PubMed  Google Scholar 

  • Závodska R, Von WG, Löfstedt C, Rosén W, Sauman I (2009) The release of a pheromonotropic neuropeptide, PBAN, in the turnip moth Agrotis segetum, exhibits a circadian rhythm. J Insect Physiol 55:435–440

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

We thank the anonymous reviewers for suggestions that improved the manuscript.

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Authors and Affiliations

  1. Department of Entomology, Institute of Plant Protection, Agricultural Research Organization, Volcani Institute, 7505101, Rishon LeZion, Israel

    Anat Levi-Zada

  2. Semiochemical Solutions, 7030476, Beer Yaakov, Israel

    John A. Byers

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ALZ conceived the review, ALZ and JAB wrote the manuscript, and JAB programmed Java software to extract and analyze data from figures in the literature.

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Correspondence to Anat Levi-Zada.

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Key messages

• Pheromone production/titer, calling, emission, and response exhibit circadian rhythms affecting insect communication.

• Graphical data on insect circadian rhythms were analyzed by computer giving mean ± SD for fitting normal curves and quantitative evaluation.

• Knowledge of rhythms of pheromone emission and response are important for understanding insect mating systems and effective pest management.

• Pests where response begins before emission are most favorable for mass trapping control.

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Levi-Zada, A., Byers, J.A. Circadian rhythms of insect pheromone titer, calling, emission, and response: a review. Sci Nat 108, 35 (2021). https://doi.org/10.1007/s00114-021-01746-w

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