Skip to main content
SpringerLink
Log in

Carabidae Semiochemistry: Current and Future Directions

  • Review Article
  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Ground beetles (Carabidae) are recognized for their diverse, chemically-mediated defensive behaviors. Produced using a pair of pygidial glands, over 250 chemical constituents have been characterized across the family thus far, many of which are considered allomones. Over the past century, our knowledge of Carabidae exocrine chemistry has increased substantially, yet the role of these defensive compounds in mediating behavior other than repelling predators is largely unknown. It is also unclear whether non-defensive compounds produced by ground beetles mediate conspecific and heterospecific interactions, such as sex-aggregation pheromones or kairomones, respectively. Here we review the current state of non-exocrine Carabidae semiochemistry and behavioral research, discuss the importance of semiochemical research including but not limited to allomones, and describe next-generation methods for elucidating the underlying genetics and evolution of chemically-mediated behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alatalo RV, Mappes J (1996) Tracking the evolution of warning signals. Nature 382(6593):708–710

    CAS  Google Scholar 

  • Albre J, Liénard MA, Sirey TM, Schmidt S, Tooman LK, Carraher C, Greenwood DR, Löfstedt C, Newcomb RD (2012) Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of Leafroller moths. PLoS Genet 8(1):e1002489

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allan RA, Capon RJ, Brown V, Elgar MA (2002) Mimicry of host Cuticular hydrocarbons by Salticid spider Cosmophasis bitaeniata that preys on larvae of tree ants Oecophylla smaragdina. J Chem Ecol 28(4):835–848

    CAS  PubMed  Google Scholar 

  • Althoff DM (2003) Does parasitoid attack strategy influence host specificity? A test with New World braconids. Ecol Entomol 28(4):500–502

    Google Scholar 

  • Andersen J, Skorping A (1990) Parasites of carabid beetles: prevalence depends on habitat selection of the host. Can J Zool 69(5):1216–1220

    Google Scholar 

  • Aneshansley DJ, Eisner T, Widom JM, Widom B (1969) Biochemistry at 100 °C: explosive secretory discharge of Bombardier beetles (Brachinus). Science 165(3888):61–63

    CAS  PubMed  Google Scholar 

  • Aneshansley DJ, Jones TH, Alsop D, Meinwald J, Eisner T (1983) Thermal concomitants and biochemistry of the explosive discharge mechanism of some little known bombardier beetles. Experientia 39(4):366–368

    CAS  Google Scholar 

  • Arndt E, Beutel RG, and Will K. (2005). Carabidae Latreille, 1802. In: Beutel RG, Leschen RAB (Eds.) Handbook of Zoology. Vol. IV Arthropoda: Insecta, Part 38. Coleoptera, Beetles. Vol 1: Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim). (pp. 119–144). Walter de Gruyter, Berlin

  • Arndt EM, Moore W, Lee WK, Ortiz C (2015) Mechanistic origins of the bombardier beetle (Brachinini) explosive pulsed chemical defense. Science 348(6234):563–567

    CAS  PubMed  Google Scholar 

  • Ashworth AC, Erwin TL (2016) Antarctotrechus balli sp. n. (Carabidae, Trechini): the first ground beetle from Antarctica. ZooKeys 635:109–122

    Google Scholar 

  • Attygalle AB, Meinwald J, Liebherr JK, Eisner T (1991a) Sexual dimorphism in the defensive secretion of a carabid beetle. Experientia 47(3):296–299

    CAS  PubMed  Google Scholar 

  • Attygalle AB, Meinwald J, Eisner T (1991b) Biosynthesis of methacrylic acid and isobutyric acids in a carabid beetle, Scarites subterraneus. Tetrahedron Lett 32(37):4849–4852

    CAS  Google Scholar 

  • Attygalle AB, Meinwald J, Eisner T (1992) Defensive secretion of a carabid beetle, Helluomorphoides clairvillei. J Chem Ecol 18(3):489–498

    CAS  PubMed  Google Scholar 

  • Attygalle AB, Wu X, Will KW (2006) Biosynthesis of Tiglic, Ethacrylic, and 2-Methylbutyric acids in a carabid beetle, Pterostichus (Hypherpes) californicus. Jo Chem Ecol 33(5):963–970

    Google Scholar 

  • Attygalle AB, Wu X, Maddison DR, Will KW (2009) Orange/lemon-scented beetles: opposite enantiomers of limonene as major constituents in the defensive secretion of related carabids. Naturwissenschaften 96(12):1443–1449

    CAS  PubMed  Google Scholar 

  • Baker TC (1998) Species specificity of pheromone responses. Biochemist 20:26–29

    CAS  Google Scholar 

  • Baker TC (2002) Mechanism for saltational shifts in pheromone communication systems. Proc Natl Acad Aci USA 99(21):13368–13370

    CAS  Google Scholar 

  • Bakke A (1981) Inhibition of the response in Ips typographus to the aggregation pheromone; field evaluation of verbenone and ipsenol. J Appl Entomol 92(1–5):172–177

    Google Scholar 

  • Balestrazzi E, Dazzini MLV, De Bernardi M, Vidari G, Vita-Finzi P, Mellerio G (1985) Morphological and chemical studies on the pygidial defence glands of some Carabidae (Coleoptera). Naturwissenschaften 72(9):482–484

    Google Scholar 

  • Bando T (1991) Visual perception of texture in aggressive behavior of Betta splendens. J Comp Physiol A 169(1):51–58

    CAS  PubMed  Google Scholar 

  • Beutel RG, Haas A (1996) Phylogenetic analysis of larval and adult characters of Adephaga (Coleoptera) using cladistics computer programs. Insect Syst Evol 27(2):197–205

    Google Scholar 

  • Bjostad LB, Roelofs WL (1983) Sex pheromone biosynthesis is Trichoplusia ni: key steps involve delta-11 desaturation and chain-shortening. Science 220(4604):1387–1389

    CAS  PubMed  Google Scholar 

  • Blum MS (1969) Alarm pheromones. Annu Rev Entomol 14:57–80

    CAS  Google Scholar 

  • Blum MS (1996) Semiochemical parsimony in the Arthropoda. Annu Rev Entomol 41:353–374

    CAS  PubMed  Google Scholar 

  • Blum MS, Jones TH, House GJ, Tschinkel WR (1981) Defensive secretions of tiger beetles: Cyanogenetic basis. Comp Biochem Physiol 69(4):903–904

    Google Scholar 

  • Bolnick DI, Fitzpatrick BM (2007) Sympatric speciation: models and empirical evidence. Annu Rev Eco, Evol System 38:459–487

    Google Scholar 

  • Bonacci T, Brandmayr P, Dalpozzo R, De Nino A, Massolo A, Tagarelli A, Brandmayr TZ (2008) Odour and colour similarity in two species of gregarious carabid beetles (Coleoptera) from the Crati Valley, southern Italy: a case of Müllerian mimicry? Entom News 119(4):325–337

    Google Scholar 

  • Bonacci T, Brandmayr P, Zetto T, Perrotta ID, Guarino S, Peri E, Colazza S (2011) Volatile compounds released by disturbed and undisturbed adults of Anchomenus dorsalis (Coleoptera, Carabidae, Platynini) and structure of the pygidial gland. ZooKeys 81:13–25

    Google Scholar 

  • Borden JH, Ryker LC, Chong LJ, Pierce HD, Johnston BD, Oehlschlager AC (1987) Response of the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), to five semiochemicals in British Columbia lodgepole pine forests. Can J For Res 17(2):118–128

    CAS  Google Scholar 

  • Brandmayr TZ, Bonacci T, Massolo A, Brandmayr P (2006) What is going on between aposematic carabid beetles? The case of Anchomenus dorsalis (Pontoppidan 1763) and Brachinus sclopeta (Fabricius 1792) (Coleoptera Carabidae). Ethol Ecol Evol 18(4):335–348

    Google Scholar 

  • Brodeur J (2000) Host specificity and trophic relationships of Hyperparasitoids. In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton, pp 163–183

    Google Scholar 

  • Brown WL, Eisner T, Whittaker RH (1970) Allomones and kairomones: Transpecific chemical messengers. Bioscience 20(1):21–22

    CAS  Google Scholar 

  • Buček A, Matouškova P, Vogel H, Šebesta P, Jahn U, Weißflog J, Svatoš A, Pichová I (2015) Evolution of moth sex pheromone composition by a single amino acid substitution in a fatty acid desaturase. Proc Natl Acad Sci U S A 112(41):12586–12591

    PubMed  PubMed Central  Google Scholar 

  • Buček A, Brabcová J, Vogel H, Prchalová D, Kindl J, Valterová I, Pichová I (2016) Exploring complex pheromone biosynthetic processes in the bumblebee male labial gland by RNA sequencing. Insect Mol Biol 25(3):295–314

    PubMed  Google Scholar 

  • Butenandt VA, Beckmann R, Stamm D, Hecker E (1959) Über den Sexual-Lockstoff des Seidenspinners Bombyx mori – Reindarstellung und Konstitution. Z Naturforsch 14:283–284

    Google Scholar 

  • Cardé RT (2014) Defining attraction and aggregation pheromones: teleological versus functional perspectives. J Chem Ecol 40(6):519–520

    PubMed  Google Scholar 

  • Cardé RT and Baker TC. (1984). Sexual communication with pheromones. In: Bell WJ, Cardé RT (Eds.) Chemical ecology of insects. Springer, Boston

    Google Scholar 

  • Cheng Y, Wen P, Dong S, Tan K, Nieh JC (2017) Poison and alarm: the Asian hornet Vespa velutina uses sting venom volatiles as an alarm pheromone. J Exp Biol 220:645–651

    PubMed  Google Scholar 

  • Conesa A, Madrigal P, Tarazona S, Gomez-Cabrero D, Cervera A, McPherson A, Szcześniak MW, Gaffney DJ, Elo LL, Zhang X, Mortazavi A (2016) A survey of best practices for RNA-Seq data analysis. Genome Biol 17(13)

  • Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819–823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Costa-Leonardo AM, Haifig I (2010) Pheromones and exocrine glands in Isoptera. Vitam Horm 83:521–549

    CAS  PubMed  Google Scholar 

  • Darwin C (1846) Letter no. 1009, To Leonard Jenyns. Darwin Correspondence Project. http://www.darwinproject.ac.uk/DCP-LETT-1009. Accessed 10 Sept 2017

  • Dean J, Aneshansley DJ, Edgerton HE, Eisner T (1990) Defensive spray of the bombardier beetle: a biological pulse jet. Science 248(4960):1219–1221

    CAS  PubMed  Google Scholar 

  • Dempster JP, Pollard E (1981) Fluctuations in resource availability and insect populations. Oecologia 50(3):412–416

    CAS  PubMed  Google Scholar 

  • Dettner K (1985) Ecological and phylogenetic significance of defensive compounds from pygidial glands of Hydradephaga (Coleoptera). Proc Academy Nat Sci Philadelphia 137(1):156–171

    Google Scholar 

  • Dettner K (1987) Chemosystematics and evolution of beetle chemical defenses. Annu Rev Entomol 32:17–48

    CAS  Google Scholar 

  • Di Giglio A, Brandmayr P, Dalpozzo R, Sindona G, Tagarelli A, Talarico F, Brandmayr TZ, a d Ferrero EA (2009) The defensive secretion of Carabus lefebvrei Dejean 1826 Pupa (Coleoptera, Carabidae): gland ultrastructure and chemical identification. Microsc Res Tech 72(5):351–361

    CAS  PubMed  Google Scholar 

  • Di Giglio A, Brandmayr P, Talarico F, Brandmayr TZ (2011) Current knowledge on exocrine glands in carabid beetles: structure, function, and chemical compounds. ZooKeys 100:193–201

    Google Scholar 

  • Di Giulio A, Fattorini S, Moore W, Robertson J, Maurizi E (2014) Form, function and evolutionary significance of stridulatory organs in ant nest beetles (Coleoptera: Carabidae: Paussini). Eur J Entomol 111(5):692–702

    Google Scholar 

  • Di Giulio A, Muzzi M, Romani R (2015) Functional anatomy of the explosive defensive system of bombardier beetles (Coleoptera, Carabidae, Brachininae). Arthropod Struct Develop 44(5):468–490

    Google Scholar 

  • Di Mauro G, Perez M, Lorenzi MC, Guerrieri FJ, Millar JG, d’Ettorre P (2015) Ants discriminate between different hydrocarbon concentrations. Front Ecol Evol 3:133

    Google Scholar 

  • Eisner T (1958) The protective role of the spray mechanism of the bombardier beetle, Brachynus ballistarius Lec. J Insect Physiol 2(3):215–220

    Google Scholar 

  • Eisner T, Aneshansley DJ (1999) Spray aiming in the bombardier beetle: photographic evidence. Proc Natl Acad Sci U S A 96(17):9705–9709

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisner T, Dean J (1976) Ploy and counterploy in predator-prey interactions: orb-weaving spiders versus bombardier beetles. Proc Natl Acad Sci U S A 73(4):1365–1367

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisner T, Swithenbank C, Meinwald J (1963) Defense mechanisms of arthropods. VIII. Secretion of Salicylaldehyde by a carabid beetle. Ann Entomol Soc Am 56(1):37–41

    CAS  Google Scholar 

  • Eisner T, Kriston I, Aneshansley DJ (1976) Defensive behavior of a termite (Nasutitermes exitiosus). Behav Ecol Sociobiol 1(1):83–125

    Google Scholar 

  • Eisner T, Jones TH, Aneshansley DJ, Tschinkel WR, Silberglied RE, Meinwald J (1977) Chemistry of defensive secretions of Bombardier beetles (Brachinini, Metriini, Oxaenini, Paussini). J Insect Physiol 23(11–12):1383–1386

    CAS  Google Scholar 

  • Eisner T, Ball GE, Roach B, Aneshansley DJ, Eisner M, Blankespoor C, Meinwald J (1989) Chemical defense of an Ozaenine Bombardier beetle from New Guinea. Psyche 96(3–4):153–160

    Google Scholar 

  • Eisner T, Aneshansley DJ, Eisner M, Attygalle AB, Alsop DW, Meinwald J (2000) Spray mechanism of the most primitive bombardier beetle (Metrius contractus). J Exp Biol 203:1265–1275

    CAS  PubMed  Google Scholar 

  • Eisner T, Aneshansley DJ, Yack J, Attygalle AB, Eisner M (2001) Spray mechanism of crepidogastrine bombardier beetles (Carabidae; Crepidogastrini). Chemoecology 11(4):209–219

    CAS  Google Scholar 

  • Eisner T, Aneshansley D, del Campo ML, Eisner M, Frank JH, Deyrup M (2006) Effect of bombardier beetle spray on a wolf spider: repellency and leg autotomy. Chemoecology 16(4):185–189

    Google Scholar 

  • Elgar MA, Allan RA (2004) Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91(3):143–147

    CAS  PubMed  Google Scholar 

  • El-Sayed AM. (2018). The Pherobase: Database of Pheromones and Semiochemicals. http://www.pherobase.com

  • Emery VJ, Tsutsui ND (2013) Recognition in a social Symbiosis: chemical phenotypes and Nestmate recognition behaviors of Neotropical Parabiotic ants. PLoS One 8(2):e56492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Erwin TL (1967) Bombardier beetles (Coleoptera: Carabidae) of North America: part II. Biology and behavior of Brachinus pallidus Erwin in California. Coleopt Bull 21:41–55

    Google Scholar 

  • Erwin TL (1979) A review of the natural history and evolution of Ectoparasitoid relationships in carabid beetles. In: Erwin TL, Ball GE, Whitehead DR, Halpern AL (eds) Carabid Beetles. Springer, Dordrecht

    Google Scholar 

  • Erwin TL, Aschero V (2004) Cicindis horni Bruch (Coleoptera: Carabidae, Cicindini): the fairy shrimp hunting beetle, its way of life on the Salinas Grandes of Argentina. Zootaxa 553(1):16

    Google Scholar 

  • Espelie KE, Hermann HR (1988) Congruent cuticular hydrocarbons: biochemical convergence of a social wasp, an ant and a host plant. Bioch System Ecol 16(5):505–508

    CAS  Google Scholar 

  • Fain A, Noti MI, Dufrêne M (2009) Observations on the mites (Acari) associated with Carabidae (Coleoptera) in Belgium. I Annotated list of the species. Internat J Acarol 21(2):107–122

    Google Scholar 

  • Farine JP, Semon E, Everaerts C, Abed D, Grandcolas P, Brossut R (2002) Defensive secretion of Therea petiveriana: chemical identification and evidence of an alarm function. J Chem Ecol 28(8):1629–1640

    CAS  PubMed  Google Scholar 

  • Ferveur JF (2005) Cuticular hydrocarbons: their evolution and roles in Drosophila pheromonal communication. Behav Genet 35(3):279–295

    PubMed  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas S, Driver SE, Mello CC (1998) Potent and specific genetic interference by a double-stranded RNA in Caenorhabditis elegans. Nature 391(6669):806–811

    CAS  PubMed  Google Scholar 

  • Forsyth DJ (1968) The structure of the defence glands in the Dytiscidae, Noteridae, Haliplidae and Gyrinidae (Coleoptera). Trans Ro Entomol Soc London 120(6):159–181

    Google Scholar 

  • Forsyth DJ (1970) The structure of the defence glands of the Cicindelidae, Amphizoidae, and Hygrobiidae (Insecta: Coleoptera). J Zool 160(1):51–69

    Google Scholar 

  • Forsyth DJ (1972) The structure of the pygidial defence glands of Carabidae (Coleoptera). Trans Zool Soc London 32:249–309

    Google Scholar 

  • Francke W and Dettner K. (2005). Chemical Signalling in beetles. In: Schulz S. (eds.) The Chemistry of Pheromones and Other Semiochemicals II. Topics in Current Chemistry. Vol. 240. (pp. 85-166). Springer, Berlin, Heidelberg

  • Fuller E, Elderd BD, Dwyer G (2012) Pathogen persistence in the environment and insect-Baculovirus interactions: disease-density thresholds, epidemic burnout and insect outbreaks. Am Nat 179(3):E70–E96

    PubMed  Google Scholar 

  • Gamberale G, Tullberg BS (1998) Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence. Proc R Soc B Biol Sci 265(1399):889–894

    Google Scholar 

  • Garry CE (1993) Ground beetles (Coleoptera: Carabidae) of Paleoenvironmental significance of the Forest-tundra and open woodland of northern Manitoba, Canada. Coleopt Bull 47(1):89–106

    Google Scholar 

  • Geiselhardt SF, Geiselhardt S, Peschke K (2006) Chemical mimicry of cuticular hydrocarbons – how does Eremostibes opacus gain access to breeding burrows of its host Parastizopus armaticeps (Coleoptera, Tenebrionidae)? Chemoecology 16(1):59–68

    CAS  Google Scholar 

  • Geiselhardt SF, Peschke K, Nagel P (2007) A review of myrmecophily in ant nest beetles (Coleoptera: Carabidae: Paussinae): linking early observations with recent findings. Naturwissenschaften 94(11):871–894

    CAS  PubMed  Google Scholar 

  • Geiselhardt S, Jakobschy D, Ockenfels P, Peschke K (2008) A sex pheromone in the desert tenebrionid beetle Parastizopus armaticeps. J Chem Ecol 34(8):1065–1071

    CAS  PubMed  Google Scholar 

  • Gunawardena NE, Bandumathie MK (1993) Defensive secretion of rice bug, Leptocorisa oratorius fabricus, (Hemiptera: Coreidae): a unique chemical combination and its toxic, repellent, and alarm properties. J Chem Ecol 19(4):851–861

    CAS  PubMed  Google Scholar 

  • Hallem EA, Dahanukar A, Carlson JR (2006) Insect odor and taste receptors. Annu Rev Entomol 51:113–135

    CAS  PubMed  Google Scholar 

  • Hamilton WD. (1964a). The genetical evolution of social behavior. I J Theor Biol 7(1): 1–16

  • Hamilton WD. (1964b). The genetical evolution of social behavior. II J Theor Biol 7(1): 17–52

  • Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31(2):295–311

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomena, mainly in social insects. Annu Rev Ecol Syst 3:193–232

    Google Scholar 

  • Hansson BS, Stensmyr MC (2011) Evolution of insect olfaction. Neuron 72(5):698–711

    CAS  PubMed  Google Scholar 

  • Holliday AE, Holliday NJ, Mattignly TM, Naccarato KM (2012) Defensive secretions of the carabid beetle Chlaenius cordicollis: chemical components and their geographic patterns of variation. J Chem Ecol 38(3):278–286

    CAS  PubMed  Google Scholar 

  • Holliday AE, Mattingly TM, Holliday NJ (2015) Defensive secretions of larvae of a carabid beetle. Physiol Entomol 40(2):131–137

    CAS  Google Scholar 

  • Ioannou CC, Morell LJ, Ruxton GD, Krause J (2009) The effect of prey density on predators: conspicuousness and attack success are sensitive to spatial scale. Am Nat 173(4):499–506

    PubMed  Google Scholar 

  • James A, Morison K, Todd S (2012) A mathematical model of the defence mechanism of a bombardier beetle. J Royal Soc Interface 10(79):20120801

    Google Scholar 

  • Jennings JH, Mazzi D, Ritchie MG, Hoikkala A (2011) Sexual and postmating reproductive isolation between allopatric Drosophila montana populations suggest speciation potential. BMC Evol Biol 11(68)

  • Jennings JH, Snook RR, Hoikkala A (2014) Reproductive isolation among allopatric Drosophila montana populations. Evolution 68(11):3095–3108

    PubMed  Google Scholar 

  • Johnson CA, Vander Meer RK, Lavine B (2001) Changes in the Cuticular hydrocarbon profile of the slave-maker ant queen, Polyergus breviceps Emery, after killing a Formica host queen (Hymenoptera: Formicidae). J Chem Ecol 27(9):1787–1804

    CAS  PubMed  Google Scholar 

  • Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21(3):149–156

    PubMed  Google Scholar 

  • Juliano SA (1984) Multiple feeding and aggression among larvae of Brachinus lateralis Dejean (Coleoptera: Carabidae). Coleopt Bull 38(4):358–360

    Google Scholar 

  • Kanehisa K, Kawazu K (1985) Differences in neutral components of the defensive secretion in formic acid-secreting carabid beetles. Appl Entomol Zool 20(3):299–304

    CAS  Google Scholar 

  • Kanehisa K, Murase M (1977) Comparative study of the Pygidial defensive Systems of Carabid Beetles. Appl Entomol Zool 12(3):225–235

    CAS  Google Scholar 

  • Kárpáti Z, Tasin M, Cardé RT, Dekker T (2013) Early quality assessment lessens pheromone specificity in a moth. Proc Natl Acad Sci U S A 110(18):7377–7382

    PubMed  PubMed Central  Google Scholar 

  • Kasting R, McGinnis AJ (1958) Use of glucose labelled with Carbon-14 to determine the amino-acids essential for an insect. Nature 182:1380–1381

    CAS  PubMed  Google Scholar 

  • Kelley KC, Schilling AB (1998) Quantitative variation in chemical defense within and among subgenera of Cicindela. J Chem Ecol 24(3):451–472

    CAS  Google Scholar 

  • Kistler KE, Vosshall LB, Matthews BJ (2015) Genome engineering with CRISPR-Cas9 in the mosquito Aedes aegypti. Cell Rep 11(1):51–60

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kleeberg I, Menzel F, Foitzik S (2017) The influence of slavemaking lifestyle, caste and sex on chemical profiles in Temnothorax ants: insights into the evolution of cuticular hydrocarbons. Proc R Soc B Biol Sci 284:20162249

    Google Scholar 

  • Klun JA, Chapman DL, Mattes KC, Wojtkowski PW, Beroza M, Sonnet PE (1973) Insect sex pheromones: minor amount of opposite geometrical isomer critical to attraction. Science 181(4100):661–663

    CAS  PubMed  Google Scholar 

  • Klun JA et al (1975) Insect sex pheromones: intraspecific Pheromonal variability of Ostrinia nubilalii in North America and Europe. Environ Entomol 4(6):891–894

    CAS  Google Scholar 

  • Kocbansky J, Carde RT, Liebberr J, Roelofs WL (1975) Sex pheromones of the European corn borer, Ostrinia nubialis (Lepidoptera: Pyralidae), in New York. J Chem Ecol 1(2):225–231

    Google Scholar 

  • Landolt PJ (1997) Sex attractant and aggregation pheromones of male phytophagous insects. Am Entomol 43(1):12–22

    Google Scholar 

  • Lečić S, Ćurčić S, Vujisić L, Ćurčić B, Ćurčić N, Nikolić Z, Anđelković B, Milosavljević S, Tešević V, Makarov S (2014) Defensive secretions in three ground-beetle species (Insecta: Coleoptera: Carabidae). Ann Zool Fenn 51(3):285–300

    Google Scholar 

  • Li J, Lehmann S, Weißbecker B, Naharros IO, Schütz S, Joop G, Wimmer EA (2013) Odoriferous defensive stink gland transcriptome to identify novel genes necessary for Quinone synthesis in the red flour beetle, Tribolium castaneum. PLoS Genet 9(7):e1003596

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lockwood JA, Story RN (1987) Defensive secretion of the southern green stink bug (Hemiptera: Pentatomidae) as an alarm pheromone. Ann Entomol Soc Am 80(5):686–691

    Google Scholar 

  • Löfqvist J (1976) Formic acid and saturated hydrocarbons as alarm pheromones for the ant Formica rufa. J Insect Physiol 22(10):1331–1346

    Google Scholar 

  • Machado G, Bonato V, Oliveria PS (2002) Alarm communication: a new function for the scent-gland secretion in harvestmen (Arachnida: Opiliones). Naturwissenschaften 89(8):357–360

    CAS  PubMed  Google Scholar 

  • Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc B Biol Sci 275(1640):1271–1278

    CAS  Google Scholar 

  • Mast JD, De Moraes CM, Alborn HT, Lavis LD, Stern DL (2014) Evolved differences in larval social behavior mediated by novel pheromones. elife 3:e04205

    PubMed  PubMed Central  Google Scholar 

  • McCullough BT (1966) Quantitative determination of salicylaldehyde in the scent fluid of Calosoma macrum, C. alternans sayi, C. affine, and C. parvicollis (Coleoptera: Carabidae). Ann Entomol Soc Am 59(5):1018

    CAS  Google Scholar 

  • McDonald DB (1989) Correlates of male mating success in a lekking bird with male-male cooperation. Anim Behav 37(6):1007–1022

    Google Scholar 

  • Miller DR, Borden JH, Lindgren SB (1995) Verbenone: dose-dependent interruption of pheromone-based attraction of three sympatric species of pine bark beetles (Coleoptera: Scolytidae). Environ Entomol 24(3):692–696

    CAS  Google Scholar 

  • Miller DR, Lindgren SB, Borden JH (2005) Dose-dependent pheromone responses of mountain pine beetle in stands of lodgepole pine. Environ Entomol 34(5):1019–1027

    CAS  Google Scholar 

  • Moore BP, Brown WV (1979) Chemical composition of the defensive secretion in Dyschitius Bonelli (Coleoptera: Carabidae: Scaritinae) and its taxonomic significance. J Austr Entomolog Soc 18(2):123–125

    CAS  Google Scholar 

  • Moore BP, Wallbank BE (1968) Chemical composition of the defensive secretion in carabid beetles and its importance as a taxonomic character. Syst Entomol 37(5–6):62–72

    Google Scholar 

  • Moore W, Song XB, Di Giulio A (2011) The larva of Eustra (Coleoptera: Paussinae, Ozaenini): a facultative associate of ants. ZooKeys 90:63–82

    Google Scholar 

  • Mori A, Grasso DA, Visicchio R, Le Moli F (2000a) Colony founding in Polyergus rufescens: the role of the Dufour’s gland. Insect Soc 47(1):7–10

    Google Scholar 

  • Mori A, Visicchio R, Sledge MF, Grasso DA, Le Moli F, Turillazzi S, Spencer S, Jones GR (2000b) Behavioural assays testing the appeasement allomone of Polyergus rufescens queens during host-colony usurpation. Ethol Ecol Evol 12(3):315–322

    Google Scholar 

  • Nadeau JA, Petereit J, Tillett RL, Jung K, Fotoohi M, MacLean M, Young S, Schlauch K, Blomquist GJ, Tittiger C (2017) Comparative transcriptomics of mountain pine beetle pheromone-biosynthetic tissues and functional analysis of CYP6DE3. BMC Genomics 18:331

    Google Scholar 

  • Nanda P, Singh BN (2012) Behavioural reproductive isolation and speciation in Drosophila. J Biosci 37(2):359–374

    PubMed  Google Scholar 

  • Ohlen M, Herfurth AM, Kerbstadt H, Wittstock U (2016) Cyanide detoxification in an insect herbivore: Molecular identification of β-cyanoalanine synthases from Pieris rapae. Insect Biochem Mol Biol 70:99–110

    CAS  PubMed  Google Scholar 

  • Okumura E, Yoshiga T (2014) Host orientation using volatiles in the phoretic nematode Caenorhabditis japonica. J Exp Biol 217:3197–3199

    PubMed  Google Scholar 

  • Pearson DL, Blum MS, Jones TH, Fales HM, Gonda E, White BR (1988) Historical perspective and the interpretation of ecological patterns: defensive compounds of tiger beetles (Coleoptera: Cicindelidae). Am Nat 132(3):404–416

    Google Scholar 

  • Philip BA, Burgess EPJ (2012) Observations on the ecology and behaviour of Ctenognathus novaezelandiae (Fairmaire) (Coleoptera: Carabidae). New Zealand Entomol 31(1):35–39

    Google Scholar 

  • Raffa KF (2011) Mixed messages across multiple trophic levels: the ecology of bark beetle chemical communication systems. Chemoecology 11:49–65

    Google Scholar 

  • Roach B, Dodge KR, Aneshansley DJ, Wiemer D, Meinwald J, Eisner T (1979) Chemistry of defensive secretions of Ozaenine and Paussine bombardier beetles (Coleoptera: Carabidae). Coleopt Bull 33(1):17–19

    Google Scholar 

  • Robertson JA, Moore W (2016) Phylogeny of Paussus L. (Carabidae: Paussinae): unravelling morphological convergence associated with myrmecophilous life histories. Syst Entomol 42(1):134–170

    Google Scholar 

  • Rock GC, King KW (1966) Amino acid composition in hydrolysates of the red-banded leaf roller, Argyrotaenia velutinana (Lepidoptera: Tortricidae) during development. Ann Entomol Soc Am 59(2):273–277

    CAS  Google Scholar 

  • Roelofs WL, Bjostad L (1984) Biosynthesis of lepidopteran pheromones. Bioorg Chem 12(4):279–298

    CAS  Google Scholar 

  • Roelofs WL, Rooney AP (2003) Molecular genetics and evolution of pheromone biosynthesis in Lepidoptera. Proc Natl Acad Sci U S A 100(16):9179–9184

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roelofs WL, Du JW, Tang XH, Robbins PS, Eckenrode CJ (1985) Three European corn borer populations in New York based on sex pheromones and voltinism. J Chem Ecol 11(7):829–836

    CAS  PubMed  Google Scholar 

  • Roelofs WL, Liu WT, Hao GX, Jiao HM, Rooney AP, Linn CE (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci U S A 99(21):13621–13616

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruther J, Reinecke A, Tolasch T, Hilker M (2001) Make love not war: a common arthropod defence compound as sex pheromone in the forest cockchafer Melolontha hippocastani. Oecologia 128(1):44–47

    PubMed  Google Scholar 

  • Salt G (1928) Notes on the life history of Pelecium sulcatum Guerin. Psyche 35:131–134

    Google Scholar 

  • Sasahara K, Cody ML, Cohen D, Taylor CE (2012) Structural design principles of complex bird songs: a network-based approach. PLoS One 7(9):e44436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sasakawa K, Ikeda H, Sutou M, Dobata S, Ito M (2011) Parasitism of adult Poecilus versicolor (Coleoptera: Carabidae) by hymenopteran larvae. Can Entomol 143(3):211–223

    Google Scholar 

  • Saska P, Honek A (2004) Development of the beetle parasitoids, Brachinus explodens and B. crepitans (Coleoptera: Carabidae). J Zool 262(1):29–36

    Google Scholar 

  • Schildknecht H (1970) The defensive chemistry of land and water beetles. Angew Chem Int Ed 9(1):1–9

    CAS  Google Scholar 

  • Schildknecht H, Holoubek K, Weis KH, Krämer H (1964) Defensive substances of the arthropods, their isolation and identification. Angew Chem Int Ed Eng 3(2):73–82

    Google Scholar 

  • Schildknecht H, Maschwitz U, Winkler H (1968a) Über Arthropoden-Abwehrstoffe XXXII. Zur Evolution der Carabiden-Wehrdrüsensekrete. Naturwissenschaften 55:112–117

    CAS  PubMed  Google Scholar 

  • Schildknecht H, Winkler H, and Maschwitz U. (1968b). Über Arthropoden-Abwehrstoffe XXXI. Vergleichend chemische Untersuchungen der Inhaltsstoffe der Pygidialwehrblasen von Carabiden Zeitschrift für Naturforschung B 23: 637–644

    CAS  Google Scholar 

  • Schultz TD, Puchalski J (2001) Chemical defenses in the Tiger beetle Pseudoxycheila tarsalis bates (Carabidae: Cicindelinae). Coleopt Bull 55(2):164–166

    Google Scholar 

  • Steiner AM, Busching C, Vogel H, Wittstock U (2018) Molecular identification and characterization of rhodaneses from the insect herbivore Pieris rapae. Sci Rep 8:10819

    PubMed  PubMed Central  Google Scholar 

  • Stelicht M (1973) Parasitic wasps attracted by the sex pheromone of the coccid host. Entomophaga 18(4):339–342

    Google Scholar 

  • Strand MR, Obrycki JJ (1996) Host specificity of insect parasitoids and predators. BioScience 46(6):422–429

    Google Scholar 

  • Sturgis SJ, Gordon DM (2012) Nestmate recognition in ants (Hymenoptera: Formicidae): a review. Myrmecolog News 16:101–110

    Google Scholar 

  • Symonds MRE, Elgar MA (2003) The mode of pheromone evolution: evidence from bark beetles. Proc R Soc B Biol Sci 271(1541):839–846

    Google Scholar 

  • Symonds MRE, Elgar MA (2007) The evolution of pheromone diversity. Trends Ecol Evol 23(4):220–228

    Google Scholar 

  • Talarico F, Bonacci T, Brandmayr P, Dalpozza R, De Nino A, Giglio A, Tagarelli A, Brandmayr TZ (2009) Avoiding ant detection in Siagona europaea Dejean 1826 (Coleoptera Carabidae): an evolutionary step towards true myrmecophily. Ethol Ecol Evol 21(1):45–61

    Google Scholar 

  • Teal PE, Tumlinson JH (1986) Terminal steps in pheromone biosynthesis by Heliothis virescens and H. zea. J Chem Ecol 12(2):353–366

    CAS  PubMed  Google Scholar 

  • Teal PE, Tumlinson JH (1988) Properties of cuticular oxidases used for sex pheromone biosynthesis by Heliothis zea. J Chem Ecol 14(11):2131–2145

    CAS  PubMed  Google Scholar 

  • Thomas CFG, Parkinson L, Griffiths GJK, Fernandez-Garcia A, Marshall EJP (2001) Aggregation and temporal stability of carabid beetle distributions in field and hedgerow habitats. J Appl Ecol 38(1):100–116

    Google Scholar 

  • Tillman JA, Seybold SJ, Jurenka RA, Blomquist GJ (1999) Insect pheromones—an overview of biosynthesis and endocrine regulation. Insect Biochem Mol Biol 29(6):481–514

    CAS  PubMed  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and the evolution of the social insect. Science 191(4224):249–263

    CAS  PubMed  Google Scholar 

  • Vander Meer RK, Wojcik DP (1982) Chemical mimicry in the Myrmecophilous beetle Myrmecaphodius excavaticollis. Science 218(4574):806–808

    CAS  Google Scholar 

  • Visicchio R, Sledge MF, Mori A, Grasso DA, Le Moli F, Turillazzi S, Moneti G, Spencer S, Jones GR (1999) Dufour’s gland contents of queens of the slave-making ant Polyergus rufescens and its host species Formica cunicularia. Ethol Ecol Evol 12(1):67–73

    Google Scholar 

  • Vogel H, Heidel AJ, Heckel DG, Groot AT (2010) Transcriptome analysis of the sex pheromone gland of the noctuid moth Heliothis virescens. BMC Genomics 11:29

    PubMed  PubMed Central  Google Scholar 

  • Walgenbach CA, Phillips JK, Faustini DL, Burkholder WE (1982) Male-produced aggregation pheromone of the maize weevil, Sitophilus zeamais, and interspecific attraction between three Sitophilus species. J Chem Ecol 9(7):831–841

    Google Scholar 

  • Weber I (1973) Tactile communication among free-range langurs. Amer J Phys Anthropol 32(2):481–486

    Google Scholar 

  • Weber DC, Saska P, and Chaboo CS. (2008). Carabid Beetles (Coleoptera: Carabidae) as Parasitoids. In: Capinera JL (ed.) Encyclopedia of entomology, Springer, Netherlands. 719–721

  • Weiss I, Rössler T, Hofferberth J, Brummer M, Ruther J, Stökl J (2013) A nonspecific defensive compound evolves into a competition avoidance cue and a female sex pheromone. Nat Commun 4:2767

    PubMed  PubMed Central  Google Scholar 

  • Wertheim B, van Baalen EJA, Dicke M, Vet LEM (2005) Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu Rev Entomol 50:321–346

    CAS  PubMed  Google Scholar 

  • Wicker-Thomas C (2009) Evolution of insect pheromones and their role in reproductive isolation and speciation. Annales de la Société entomologique de France 47(1–2):55–62

    Google Scholar 

  • Will KW, Attygalle AB, Herath K (2000) New defensive chemical data for ground beetles (Coleoptera: Carabidae): interpretations in a phylogenetic framework. Biol J Linn Soc 71(3):459–481

    Google Scholar 

  • Wilson EO, Regnier FE (1971) The evolution of the alarm-defense system in the Formicine ants. Am Nat 105(943):279–289

    Google Scholar 

  • Wölfling M, Rostás M (2009) Parasitoids use chemical footprints to track down caterpillars. Commun Integr Biol 2(4):353–355

    PubMed  PubMed Central  Google Scholar 

  • Xu T, Yasui H, Teale SA, Fujiwara-Tsujii N, Wickham JD, Fukaya M, Hansen L, Kiriyama S, Hao D, Nakano A, Zhang L, Watanabe T, Tokoro M, Millar JG (2017) Identification of a male-produced sex-aggregation pheromone for a highly invasive cerambycid beetle, Aromia bungii. Sci Rep 7:7330

    PubMed  PubMed Central  Google Scholar 

  • Yew JY, Chung H (2015) Insect pheromones: an overview of function, form, and discovery. Prog Lipid Res 59:88–105

    CAS  PubMed  Google Scholar 

  • Young S, Watt PJ, Grover JP, Thomas D (1994) The unselfish swarm? J Anim Ecol 63(3):611–618

    Google Scholar 

  • Zhang G, Chen J, Yu H, Tian X, Wu J (2018) Molecular and functional characterization of pheromone binding protein 1 from the oriental fruit moth, Grapholita molesta (Busck). Sci Rep 8:2276

    PubMed  PubMed Central  Google Scholar 

  • Ziegenhain C, Vieth B, Parekh S, Reinius B, Guillaumet-Adkins A, Smets M, Leonhardt H, Heyn H, Hellmann I, Enard W (2017) Comparative analysis of single-cell RNA sequencing methods. Mol Cell 65(4):631–643

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Science Foundation (DEB 1556931/1762760 to Tanya Renner). The authors thank Wendy Moore for comments on an earlier version of the manuscript, as well as Kipling Will and Athula Attygalle for thoughtful discussion and advice.

Author information

Authors and Affiliations

  1. Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, State College, PA, 16802, USA

    Adam M. Rork & Tanya Renner

Authors
  1. Adam M. Rork
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tanya Renner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam M. Rork.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rork, A.M., Renner, T. Carabidae Semiochemistry: Current and Future Directions. J Chem Ecol 44, 1069–1083 (2018). https://doi.org/10.1007/s10886-018-1011-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-018-1011-8

Keywords

Search

Navigation