Abstract
To date, all known or suspected pheromones of click beetles (Coleoptera: Elateridae) have been identified solely from species native to Europe and Asia; reports of identifications from North American species dating from the 1970s have since proven to be incorrect. While conducting bioassays of pheromones of a longhorned beetle (Coleoptera: Cerambycidae), we serendipitously discovered that males of Cardiophorus tenebrosus L. and Cardiophorus edwardsi Horn were specifically attracted to the cerambycid pheromone fuscumol acetate, (E)-6,10-dimethylundeca-5,9-dien-2-yl acetate, suggesting that this compound might also be a sex pheromone for the two Cardiophorus species. Further field bioassays and electrophysiological assays with the enantiomers of fuscumol acetate determined that males were specifically attracted by the (R)-enantiomer. However, subsequent analyses of extracts of volatiles from female C. tenebrosus and C. edwardsi showed that the females actually produced a different compound, which was identified as (3R,6E)-3,7,11-trimethyl-6,10-dodecadienoic acid methyl ester (methyl (3R,6E)-2,3-dihydrofarnesoate). In field trials, both the racemate and the (R)-enantiomer of the pheromone attracted similar numbers of male beetles, suggesting that the (S)-enantiomer was not interfering with responses to the insect-produced (R)-enantiomer. This report constitutes the first conclusive identification of sex pheromones for any North American click beetle species. Possible reasons for the strong and specific attraction of males to fuscumol acetate, which is markedly different in structure to the actual pheromone, are discussed.
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Arakaki N, Nagayama A, Kobayashi A, Hokama Y, Sadoyama Y, Mogi N, Kishita M, Adaniya K, Ueda K, Higa M, Shinzato T, Kawamitsu H, Nakama S, Wakamura S, Yamamura K (2008a) Mating disruption for control of Melanotus okinawensis (Coleoptera: Elateridae) with synthetic sex pheromone. J Econ Entomol 101:1568–1574
Arakaki N, Nagayama A, Kobayashi A, Kishita M, Sadoyama Y, Mougi N, Kawamura F, Wakamura S, Yamamura K (2008b) Control of the sugarcane click beetle Melanotus okinawensis Ohira (Coleoptera: Elateridae) by mass trapping using synthetic sex pheromone on Ikei Island, Okinawa, Japan. Appl Entomol Zool 43:37–47
Arakaki N, Nagayama A, Kobayashi A, Tarora K, Kishita M, Sadoyama Y, Mougi N, Kijima K, Suzuki Y, Akino T, Yasui H, Fukaya M, Yasuda T, Wakamura S, Yamamura K (2008c) Estimation of abundance and dispersal distance of the sugarcane click beetle Melanotus sakishimensis Ohira (Coleoptera: Elateridae) on Kurima Island, Okinawa, by mark-recapture experiments. Appl Entomol Zool 43:409–419
Barsics F, Haubruge E, Verheggen J (2013) Wireworms’ management: an overview of the existing methods, with particular regards to Agriotes spp. (Coleoptera: Elateridae). Insects 4:117–152
Blanchard F (1889) Revision of the species of Cardiophorus Esch. of America north of Mexico. Trans Am Entomol Soc 16:1–27
Butler LI, McDonough LM, Onsager JA, Landis BJ (1975) Sex pheromones of the Pacific coast wireworm, Limonius canus (Coleoptera: Elateridae). Environ Entomol 4:229–230
Chapman JA (1964) Evidence for a sex attractant in the elaterid beetle, Hemicrepidius morio (LeConte). Can Entomol 96:909–910
Collignon RM, Swift IP, Zou F, McElfresh JS, Hanks LM, Millar JG (2016) The influence of host plant volatiles on the attraction of longhorn beetles to pheromones. J Chem Ecol 42:215–229
Crozier S, Tanaka A, Vernon RS (2003) Flight activity of Agriotes lineatus L. and A. obscurus L. (Coleoptera: Elateridae) in the field. J Entomol Soc British Columbia 100:91–92
Dajoz R (2000) Insects and forests. The role and diversity of insects in the forest environment. Intercept Ltd., Paris
Doane JF (1961) Movement on the soil surface of adult Ctenicera aeripennis destructor (Brown) and Hypolithus bicolor Esch. (Coleoptera: Elateridae), as indicated by funnel pitfall traps, with notes on captures of other arthropods. Can Entomol 93:636–644
Douglas H (2011) Phylogenetic relationships of Elateridae inferred from adult morphology, with special reference to the position of Cardiophorinae. Zootaxa 2900:1–45
Douglas HB (2017) World reclassification of the Cardiophorinae (Coleoptera, Elateridae), based on phylogenetic analyses of morphological characters. Zookeys 655:1–130
Dunn OJ (1964) Multiple comparisons using rank sums. Technometrics 6:241–252
Edwards EE, Evans JR (1950) Observations on the biology of Corymbites cupreus F. (Coleoptera: Elateridae). Ann Appl Biol 37:249–259
Evans AV, Hogue JN (2006) Field guide to beetles of California. University of California Press, Berkeley
Furlan L (1996) The biology of Agriotes ustulatus Schaller (Col., Elateridae). I. Adults and oviposition. J Appl Entomol 120:269–274
Furlan L (2005) An IPM approach targeted against wireworms: what has been done and what still has to be done. IOBC/wprs Bull 28:91–100
Furlan L, Tóth M, Parker WE, Ivezic M, Pancic S, Brmez M, Dobrincic R, Barcic JI, Muresan F, Subchev M, Toshova T, Molnar Z, Ditsch B, Voigt D (2001) The efficacy of the new Agriotes sex pheromone traps in detecting wireworm population levels in different European countries. Proc. XXI IWGO Conference, Venice, Oct. 27–Nov. 3, 2001, 293–303
Hanks LM, Millar JG (2016) Sex and aggregation pheromones of cerambycid beetles: basic science and practical applications. J Chem Ecol 42:631–654
Hayes JT, Wheeler AG (1968) Evidence for a sex attractant in Hemicrepidius decoloratus (Coleoptera: Elateridae). Can Entomol 100:207–208
Ho H-Y, Millar JG (2001a) Identification and synthesis of a male-produced sex pheromone from the stink bug Chlorochroa sayi. J Chem Ecol 27:1177–1201
Ho H-Y, Millar JG (2001b) Identification and synthesis of male-produced sex pheromone components of the stink bugs Chlorochroa ligata and Chlorochroa uhleri. J Chem Ecol 27:2067–2095
Hughes GP, Zou Y, Millar JG, Ginzel MD (2013) (S)-Fuscumol and (S)-fuscumol acetate produced by a male Astyleiopus variegatus (Coleoptera: Cerambycidae). Can Entomol 145:1–6
Ivashchenko II, Adamenko EA (1980) Place of pheromone formation in females of Selatosomus latus (Coleoptera: Elateridae). Zool Z 59:225–228
Iwanaga S, Kawamura F (2000) Trapping efficacy of funnel-vane and water pan traps baited with synthetic sex pheromone of the sugarcane wireworms Melanotus sakishimensis Ohira and Melanotus okinawensis Ohira (Coleoptera: Elateridae). Appl Entomol Zool 35:283–285
Jacobson M, Lilly CE, Harding C (1968) Sex attractant of sugar beet wireworm: identification and biological activity. Science 159:208–210
Johnson PJ (2002) Elateridae. In: Arnett RH, Thomas MC, Skelley PE, Frank JH (eds) American beetles, vol 2. CRC Press, Boca Raton, pp 160–173
Kabalak M, Sert O (2011) Faunistic composition, ecological properties and zoogeographical composition of the family Elateridae (Coleoptera) of the central Anatolian region of Turkey. J Insect Sci 11(57):1–36
Kishita M, Arakaki N, Kawamura F, Sadoyama Y, Yamamura K (2003) Estimation of population density and dispersal parameters of the adult sugarcane wireworm, Melanotus okinawensis Ohira (Coleoptera: Elateridae), on Ikei Island, Okinawa, by mark-recapture experiments. Appl Entomol Zool 38:233–240
König C, Szallies A, Steidle JLM, Tolasch T (2015) Sex pheromone of the rare click beetle Betarmon bisbimaculatus. J Chem Ecol 42:55–59
Lilly CE (1959) Response of males of Limonius californicus (Mann.) (Coleoptera: Elateridae) to a sex attractant separable by paper chromatography. Can Entomol 91:145–146
Lilly CE, McGinnis AJ (1965) Reactions of male click beetles in the laboratory to olfactory pheromones. Can Entomol 97:317–321
Lilly CE, McGinnis AJ (1968) Quantitative responses of males of Limonius californicus (Coleoptera: Elateridae) to female sex pheromone. Can Entomol 100:1071–1078
Marske KA, Ivie MA (2003) Beetle fauna of the United States and Canada. Coleopt Bull 57:495–503
Merivee E, Erm A (1993) Studies on sex pheromone gland morphology and pheromone components in female elaterid beetles Agriotes obscurus L. and Agriotes lineatus L. (Coleoptera: Elateridae). Proc Estonian Acad Sci Biol Ecol 42:108–117
Morris RF (1951) The larval Elateridae of eastern spruce forests and their role in the natural control of Gilpinia hercyniae Htg. Can Entomol 83:133–147
Nagamine M, Kinjo M (1990) Report on the establishment of the control technique for the sugarcane wireworm Melanotus okinawensis. Okinawa-ken Togyo Sinkou Kyokai, Naha (in Japanese)
Ogle DH (2016) FSA: fisheries stock analysis. R package version 0.8.8
Onsager JA, McDonough LM, George DA (1968) A sex pheromone in the Pacific coast wireworm. J Econ Entomol 61:691–693
Parker WE, Howard JJ (2001) The biology and management of wireworms (Agriotes spp.) on potato with particular reference to the UK. Agric For Entomol 3:85–98
R-Development-Core-Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
RStudio-Team (2016) RStudio: integrated development for R. RStudio, Inc., Boston
Schallhart N, Wallinger C, Juen A, Traugott M (2009) Dispersal abilities of adult click beetles in arable land revealed by analysis of carbon stable isotopes. Agric For Entomol 11:333–339
Shirck FH (1942) The flight of sugar-beet wireworm adults in southwestern Idaho. J Econ Entomol 35:423–427
Stone MW (1941) Life history of the sugar-beet wireworm in southern California. US Dep Agric Tech Bull 744:1–88
Stone MW (1957) Notes on the biology of three elaterids injurious to vegetable crops (Coleoptera). Pan-Pac Entomol 33:79–85
Svensson GP, Liedtke C, Hedenström E, Breistein P, Bång J, Larsson MC (2012) Chemical ecology and insect conservation: optimizing pheromone-based monitoring of the threatened saproxylic click beetle Elater ferrugineus. J Insect Conserv 16:549–555
Tamaki Y, Sugie M, Nagamine M, Kinjo M (1986) Female sex pheromone of the sugarcane wireworm Melanotus okinawensis Ohira (Coleoptera: Elateridae). Jpn Kokai Tokkyo Koho JP 61–12601 (in Japanese)
Tamaki Y, Sugie M, Nagamine M, Kinjo M (1990) 9,11-Dodecadienyl butyrate and 9,11-dodecadienyl hexanoate, female sex pheromone of the sugarcane wireworm Melanotus sakishimensis Ohira (Coleoptera: Elateridae). Jpn Kokai Tokkyo Koho JP 2–53753 (in Japanese)
Tolasch T, von Fragstein M, Steidle JLM (2007) Sex pheromone of Elater ferrugineus L. (Coleoptera: Elateridae). J Chem Ecol 33:2156–2166
Tolasch T, König C, von Fragstein M, Steidle JLM (2013) Identification of the sex pheromone of Idolus picipennis (Bach, 1852) revealed the presence of a cryptic sibling species. J Chem Ecol 39:1433–1440
Tóth M (2013) Pheromones and attractants of click beetles: an overview. J Pest Sci 86:3–17
Tóth M, Furlan L, Vuts J, Szarukán I, Ujváry I, Yatsynin VG, Tolasch T, Francke W (2015) Geranyl hexanoate, the female-produced pheromone of Agriotes sordidus Illiger (Coleoptera: Elateridae) and its activity on both sexes. Chemoecology 25:1–10
Traugott M, Schallhart N, Kaufmann R, Juen A (2008) The feeding ecology of elaterid larvae in central European arable land: new perspectives based on naturally occurring stable isotopes. Soil Biol Biochem 40:342–349
Traugott M, Benefer CM, Blackshaw RP, van Herk WG, Vernon RS (2015) Biology, ecology, and control of elaterid beetles in agricultural land. Annu Rev Entomol 60:313–334
Turnock WJ (1969) Predation by larval Elateridae of pupae of the pine looper Bupalus piniarius (L.) Neth J Zool 19:393–416
van Herk WG, Vernon RS (2014) Click beetles and wireworms (Coleoptera: Elateridae) of Alberta, Saskatchewan, and Manitoba. Arthropods Can Grasslands 4:87–117
Vernon RS, van Herk WG (2013) Wireworms as pests of potato. In: Giordanengo P, Vincent C, Alyokhin A (eds) Insect pests of potato: global perspectives on biology and management. Academic Press, Elsevier, Amsterdam, pp 103–164
Vernon RS, van Herk WG, Tolman J (2005) European wireworms (Agriotes spp.) in North America: distribution, damage, monitoring, and alternative integrated pest management strategies. IOBC/WPRS Bull 28:73–79
Vernon RS, van Herk WG, Clodius M, Harding C (2009) Wireworm management I: stand protection versus wireworm mortality with wheat seed treatments. J Econ Entomol 102:2126–2136
Yatsynin VG, Oleschenko IN, Rubanova EV, Ismailov VY (1980) Identification of active components of the sex pheromones of click beetles Agriotes gurgistanus, A. litigiosus, and A. lineatus. Khim Sel’sk Khoz Edition Moskova, Khimiya, pp 33–35 (in Russian)
Yatsynin VG, Rubanova EV, Okhrimenko NV (1996) Identification of female-produced sex pheromones and their geographical differences in pheromone gland extract composition from click beetles (Col. Elateridae). J Appl Entomol 120:463–466
Yen YP, Chen PH (1998) Simple and stereoselective synthesis of attractant of the sugarcane wireworm Melanotus tamsuyensis. Synth Commun 28:4561–4569
Zauli A, Chiari S, Hedenstrom E, Svensson GP, Carpaneto GM (2014) Using odour traps for population monitoring and dispersal analysis of the threatened saproxylic beetles Osmoderma eremita and Elater ferrugineus in central Italy. J Insect Conserv 18:801–813
Zhang YN, Yang ZQ, Huang HH, Fan JX (2008) Cryptalaus berus (Coleoptera: Elateridae): an important predator of Monochamus alternatus (Coleoptera: Cerambycidae), the vector of pine wilt disease in China. Chin J Biol Control 24:215–219
Acknowledgements
We thank Stacy Hishinuma and Tom Coleman for providing access to field sites, and Sean Halloran and J. Steven McElfresh for assistance with laboratory and field work. We also thank Rochelle Hoey-Chamberlain and Eric Gordon for assistance with specimen imaging. This work was funded in part by financial support from the Robert van den Bosch Scholarship to JMS, and a UC Academic Senate research grant to JGM.
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Serrano, J.M., Collignon, R.M., Zou, Y. et al. Identification of Sex Pheromones and Sex Pheromone Mimics for Two North American Click Beetle Species (Coleoptera: Elateridae) in the Genus Cardiophorus Esch.. J Chem Ecol 44, 327–338 (2018). https://doi.org/10.1007/s10886-018-0940-6
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DOI: https://doi.org/10.1007/s10886-018-0940-6