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Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses

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Abstract

Chemical composition of volatiles emitted from fresh mouse carcasses (laboratory mice, Mus musculus) was studied using solid sample injection technique (solid-phase micro-extraction), two-dimensional gas chromatography with time of flight mass spectrometric detection and gas chromatography with electroantennographic detection. Electroantennography (EAG) and laboratory olfactometric behavioural observations were used to study the antennal sensitivity to identified infochemicals and their attractiveness for burying beetles Nicrophorus vespillo and Nicrophorus vespilloides (Silphidae: Nicrophorinae). Chemical analysis showed that immediately after death, emitted volatiles did not differ from those emitted by a living organism. However, in the course of time, sulphur-containing chemicals, specifically methanethiol, methyl thiolacetate, dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide appear. EAG measurements revealed antennal sensitivity to these compounds. Behavioural tests in laboratory olfactometer showed that dimethyl sulphide, dimethyl disulphide and dimethyl trisulphide are highly attractive to both studied species. The data suggest that sulphur-containing chemicals are involved in mediating the fresh carcass attractiveness for N. vespillo and N. vespilloides.

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References

  • Abbot CE (1927) Experimental data on the olfactory sense of Coleoptera, with special reverence to the Necrophori. Ann Entomol Soc Am 20:207–215

    Google Scholar 

  • Al Rouz H, Thibout E (1988) Analyse en olfactomètre de l’attraction des larves d’Acrolepiopsis assectella par des substances allelochimiques. Entomol Exp Appl 47:231–237. doi:10.1007/BF00352209

    Article  CAS  Google Scholar 

  • Anderson RS (1982) Resource partitioning in the carrion beetle (Coleoptera: Silphidae) fauna of southern Ontario: ecological and evolutionary considerations. Can J Zool 60:1314–1325. doi:10.1139/z82-178

    Article  Google Scholar 

  • Anderson RS, Peck SB (1984) Bionomics of Nearctic species of Aclypea Reitter: phytophagous “carrion” beetles (Coleoptera: Silphidae). Pan-Pac Entomol 60:248–255

    Google Scholar 

  • Anderson RS, Peck SB (1985) The insects and arachnids of Canada, part 13. The Carrion beetles of Canada and Alaska (Coleoptera: Silphidae and Agyrtidae). Research Branch, Agriculture Canada, Ottawa

    Google Scholar 

  • Anderson RS, Peck SB (1986) Geographic patterns of colour variation in North American burying beetles (Coleoptera; Silphidae). J Nat Hist 20:283–297. doi:10.1080/00222938600770241

    Article  Google Scholar 

  • Auger J, Lecomte C, Paris J, Thibout E (1989a) Identification of leek-moth and diamondback-moth frass volatiles that simulate parasitoid, Diadromus pulchellus. J Chem Ecol 15:1391–1398. doi:10.1007/BF01014838

    Article  CAS  Google Scholar 

  • Auger J, Lecomte C, Thibout E (1989b) Leek odor analysis by gas chromatography and identification of the most active substance for the leek moth, Acrolepiopsis assectella. J Chem Ecol 15:1847–1854. doi:10.1007/BF01012271

    Article  CAS  Google Scholar 

  • Barlett J (1987) Evidence for a sex attractant in burying beetles. Ecol Entomol 12:471–472. doi:10.1111/j.1365-2311.1987.tb01028.x

    Article  Google Scholar 

  • Baxter D, Hughes PS (2001) Beer: quality, safety and nutritional aspects. RSC Paperback, Royal Society of Chemistry, London

    Google Scholar 

  • Boeckh J (1962) Elektrophysiologische Untersuchungen an einzelnen Geruchsrezeptoren auf den Antennen des Totengräbers (Necrophorus, Coleoptera). Z Vgl Physiol Berl 46:212–248. doi:10.1007/BF00341551

    Article  Google Scholar 

  • Borg-Karlson AK, Englund FO, Unelius CR (1994) Dimethyl oligosulfides, major volatiles released from Sauromatum guttatum and Phallus impudicus. Phytochemistry 35:321–323. doi:10.1016/S0031-9422(00)94756-3

    Article  CAS  Google Scholar 

  • Cuer A, Dauphin G, Kergomard A, Dumont JP, Adda J (1979) Production of S-methylthioacetate by Brevibacterium linens. Appl Environ Microbiol 38:332–334

    PubMed  CAS  Google Scholar 

  • Dethier VG (1947) The role of the antennae in the orientation of carrion beetles to odors. J NY Entomol Soc 55:285–293

    Google Scholar 

  • DeVault TL, Brisbin IL Jr, Rhodes OE Jr (2004) Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers. Can J Zool 82:502–509. doi:10.1139/z04-022

    Article  Google Scholar 

  • Eggert AK (1992) Alternative male mate-finding tactics in burying beetles. Behav Ecol 3:243–254. doi:10.1093/beheco/3.3.243

    Article  Google Scholar 

  • Eggert AK, Müller JK (1989a) Mating success of pheromone-emitting Necrophorus males: do attracted females discriminate against resource owners? Behaviour 110:248–257. doi:10.1163/156853989X00493

    Article  Google Scholar 

  • Eggert AK, Müller JK (1989b) Pheromone-mediated attraction in burying beetles. Ecol Entomol 14:235–237. doi:10.1111/j.1365-2311.1989.tb00774.x

    Article  Google Scholar 

  • Eggert AK, Müller JK (1997) Biparental care and social evolution in burying beetles: Lessons from the larder. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, New York, pp 216–236

    Google Scholar 

  • Ernst KD (1972) Sensillum coelosphaericum, die Feinstruktur eines neuen olfaktorischen Sensillentyps. Z Zellforsch Mikrosk Anat 132:95–106. doi:10.1007/BF00310299

    Article  PubMed  CAS  Google Scholar 

  • Grassberger M, Frank C (2004) Initial study of arthropod succession on pig carrion in a central European urban habitat. J Med Entomol 41:511–523

    Article  PubMed  CAS  Google Scholar 

  • Haberer W, Schmitt T, Peschke K, Schreier P, Müller JK (2008) Ethyl 4-methyl heptanoate: a male-produced pheromone of Nicrophorus vespilloides. J Chem Ecol 34:94–98. doi:10.1007/s10886-007-9406-y

    Article  PubMed  CAS  Google Scholar 

  • Halffter G, Anduaga S, Huerta C (1983) Nidification des Nicrophorus (Col. Silphidae). Bull Soc Entomol Fr 88:648–666

    Google Scholar 

  • Hoskovec M, Kalinová B, Konečný K, Koutek B, Vrkoč J (1993) Structure-activity correlations among analogs of the currant clearwing moth pheromone. J Chem Ecol 19:737–750. doi:10.1007/BF00985005

    Article  Google Scholar 

  • Hoskovec M, Grygarová D, Cvačka J, Streinz L, Zima J, Verevkin SP, Koutek B (2005) Determining the vapour pressures of plant volatiles from gas chromatographic retention data. J Chrom A 1083:161–172. doi:10.1016/j.chroma.2005.06.006

    Article  CAS  Google Scholar 

  • Janzen DH (1977) Why fruits rot, seeds mold, and meat spoils. Am Nat 111:691–713. doi:10.1086/283200

    Article  CAS  Google Scholar 

  • Jojola-Elverum SM, Shivik JA, Clark L (2001) Importance of bacterial decomposition, and carrion substrate to foraging, brown treesnakes. J Chem Ecol 27:1315–1331. doi:10.1023/A:1010357024140

    Article  PubMed  CAS  Google Scholar 

  • Jürgens A, Dötterl S, Meve U (2006) The chemical nature of fetid floral odours in stapeliads (Apocynaceae-Asclepiadoideae-Ceropegieae). New Phytol 172:452–468. doi:10.1111/j.1469-8137.2006.01845.x

    Article  PubMed  CAS  Google Scholar 

  • Kadota H, Ishida Y (1972) Production of volatile sulfur compounds by microorganisms. Annu Rev Microbiol 26:127–138. doi:10.1146/annurev.mi.26.100172.001015

    Article  PubMed  CAS  Google Scholar 

  • Kite GC, Hetterschieid WLA (1997) Inflorescence odours of Amorphophallus and Pseudodracontium (Araceae). Phytochemistry 46:71–75. doi:10.1016/S0031-9422(97)00221-5

    Article  CAS  Google Scholar 

  • Kočárek P (1997) The occurrence of Silphidae and Leiodidae: Cholevinae (Coleoptera) in the Litovelské Pomoraví Protected Lanscape Area. Zprávy Vlastivěd Muz v Olomouci 275:17–29 (in Czech, English abstract)

    Google Scholar 

  • Kočárek P (2000) A pitfall trap for carrion ecology studies. Biologia (Bratisl) 55:575–577

    Google Scholar 

  • López del Castillo-Lozano M, Mansour S, Tâche R, Bonnarme P, Landaud S (2008) The effect of cysteine on production of volatile sulfur compounds by cheese-ripening bacteria. Int J Food Microbiol 122:321–327

    PubMed  Google Scholar 

  • Milne LJ, Milne M (1976) The social behavior of burying beetles. Sci Am 235:84–89

    Article  Google Scholar 

  • Müller JK, Eggert AK, Furlkröger E (1990) Clutch size regulation in the burying beetle Necrophorus vespilloides Herbst (Coleoptera: Silphidae). J Insect Behav 3:265–270. doi:10.1007/BF01417917

    Article  Google Scholar 

  • Nagano M, Suzuki S (2007) Effect of carcass size and male presence on clutch size in Nicrophorus quadripunctatus (Coleoptera: Silphidae). Entomol Sci 10:245–248. doi:10.1111/j.1479-8298.2007.00220.x

    Article  Google Scholar 

  • Ollerton J, Raguso RA (2006) The sweet stench of decay. New Phytol 172:379–381. doi:10.1111/j.1469-8137.2006.01903.x

    Article  Google Scholar 

  • Parliment TH, Kolor MG, Rizzo DJ (1982) Volatile components of limburger cheese. J Agric Food Chem 30:1006–1008. doi:10.1021/jf00114a001

    Article  CAS  Google Scholar 

  • Peck SB (1990) Insecta: Coleoptera Silphidae and the associated families Agyrtidae and Leiodidae. In: Dindal DL (ed) Soil biology guide. Wiley, New York, pp 1113–1136

    Google Scholar 

  • Peck SB, Kaulbars MM (1987) A synopsis of the distribution and bionomics of the carrion beetles (Coleoptera: Silphidae) of the conterminous United States. Proc Entomol Soc Ont 118:47–81

    Google Scholar 

  • Petruška F (1975) The effect of predominating winds on the flight of some species of beetles from the group of Silphidae into pitfall traps (Col. Silphidae). Acta Universitatis Palackianae Olomucensis. Facultas Rerum Natur 51:155–175

    Google Scholar 

  • Pfrommer A, Krell FT (2004) Who steals the eggs? Coprophanaeus telamon (Erichson) buries decomposing eggs in western Amazonian Rain Forest (Coleoptera: Scarabaeidae). Coleopt Bull 58:21–27. doi:10.1649/585

    Article  Google Scholar 

  • Pukowski E (1933) Ökologische Untersuchungen an Necrophorus F. Z Morphol Oekol Tiere 27:518–586. doi:10.1007/BF00403155

    Article  Google Scholar 

  • Pukowski E (1934) Die Brutpflege des Totengräbers. Entomol Blatt 30:109–112

    Google Scholar 

  • Raguso RA (2004) Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Curr Opin Plant Biol 7:434–440. doi:10.1016/j.pbi.2004.05.010

    Article  PubMed  Google Scholar 

  • Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Evol Syst 39:549–569. doi:10.1146/annurev.ecolsys.38.091206.095601

    Article  Google Scholar 

  • Ratcliffe BC (1996) The carrion beetles (Coleoptera: Silphidae) of Nebraska. Bull Univ Nebr State Mus 13:1–100

    Google Scholar 

  • Roelofs WL (1984) Electroantennogram assays: rapid and convenient screening procedures for pheromones. In: Hummel HE, Miller TA (eds) Techniques in pheromone research. Springer, New York, pp 131–159

    Google Scholar 

  • Růžička J (2007) Fauna Europaea: Silphidae. In: Alonso-Zarazaga MA, Audisio P (eds) Fauna Europaea: Coleoptera, Beetles. Fauna Europaea version 1.3. http://www.faunaeur.org

  • Růžička J, Schneider J (2004) Family Silphidae Latreille, 1807. In: Löbl I, Smetana A (eds) Catalogue of Palaearctic Coleoptera, vol. 2: Hydrophiloidea–Histeroidea—Staphylinoidea. Apollo Books, Steensrup, pp 229–237

    Google Scholar 

  • Scott MP (1998) The ecology and behavior of burying beetles. Annu Rev Entomol 43:595–618. doi:10.1146/annurev.ento.43.1.595

    Article  PubMed  CAS  Google Scholar 

  • Segal W, Starkey RL (1969) Microbial decomposition of methionine and identity of the resulting sulfur products. J Bacteriol 98:908–913

    PubMed  CAS  Google Scholar 

  • Sikes DS (2005) Silphidae Latreille, 1807. In: Beutel RG, Leschen RAB (eds) Handbook of zoology, volume IV: Arthropoda: Insecta, Part 38: Coleoptera, Beetles. Volume 1: morphology and systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim). Walter de Gruyer, Berlin, pp 288–296

    Google Scholar 

  • Smisetf PT, Moore AJ (2002) Does resource availability affect offspring begging and parental provisioning in a partially begging species? Anim Behav 63:577–585. doi:10.1006/anbe.2001.1944

    Article  Google Scholar 

  • Smith RJ, Heese B (1995) Carcass selection in a high altitude population of the burying beetle, Nicrophorus investigator (Silphidae). Southwest Nat 40:50–55

    Google Scholar 

  • Stensmyr MC, Urru I, Collu I, Celander M, Hansson BS, Angioy AM (2002) Pollination: rotting smell of dead-horse arum florets. Nature 420:625–626. doi:10.1038/420625a

    Article  PubMed  CAS  Google Scholar 

  • Steullet P, Guerin PM (1992) Perception of breath components by the tropical bont tick, Amblyomma variegatum Fabricius (Ixodidae). J Comp Physiol [A] 170:677–685. doi:10.1007/BF00198977

    Article  CAS  Google Scholar 

  • Stránský K, Valterová I (1999) Release of volatiles during the flowering period of Hydrosme rivieri (Araceae). Phytochemistry 52:1387–1390. doi:10.1016/S0031-9422(99)00247-2

    Article  Google Scholar 

  • Šustek Z (1981) Key to identification of insects: Carrion beetles of Czechoslovakia (Coleoptera, Silphidae). Zprávy Československé Společnosti Entomologické při ČSAV, Klíče k určování hmyzu 2:1–47 (in Czech)

    Google Scholar 

  • Thomas CJ, McMeekin TS (1981) Production of off odours by isolates from poultry skin with particular reference to volatile sulphides. J Appl Bacteriol 198:529–534

    Google Scholar 

  • Trumbo ST (1994) Interspecific competition, brood parasitism, and the evolution of biparental cooperation in burying beetles. Oikos 69:241–249. doi:10.2307/3546144

    Article  Google Scholar 

  • Trumbo ST, Fernandez AG (1995) Regulation of brood size and cues employed to assess resource size by burying beetles. Ethol Ecol Evol 7:313–322

    Google Scholar 

  • Waldow U (1973) Elektrophysiologie eines neuen Aasgeruchrezeptors und seine Bedeutung für das Verhaltern des Totengräbers (Necrophorus). J Comp Physiol 83:415–424. doi:10.1007/BF00696356

    Article  Google Scholar 

  • Wasserman SL, Itagaki H (2003) The olfactory responses of the antenna and maxillary palp of the fleshfly, Neobellieria bullata (Diptera: Sarcophagidae) and their sensitivity to blockage of nitric oxide synthase. J Insect Physiol 49:271–280. doi:10.1016/S0022-1910(02)00288-3

    Article  PubMed  CAS  Google Scholar 

  • Watson EJ, Carlton CE (2004) Insect succession and decomposition of wildlife carcasses during Fall and Winter. J Med Entomol 42:193–203. doi:10.1603/0022-2585(2005)042[0193:ISADOW]2.0.CO;2

    Google Scholar 

  • Wawrzkiewicz K, Ziókowska G, Wawrzkiewiczyna J (1997) In vitro biodegradation of hair from different animal species by Microsporum canis. Int Biodeter Biodegr 39:15–25. doi:10.1016/S0964-8305(96)00040-6

    Article  Google Scholar 

  • Wilson DS, Knollenberg WG (1984) Food discrimination and ovarian development in burying beetles (Coleoptera: Silphidae: Nicrophorus). Ann Entomol Soc Am 77:165–170

    Google Scholar 

  • Woodard CBS (2006) Odor masking of a vertebrate carcass by a burying beetle (Nicrophorus marginatus). Master’s thesis, Texas Tech University, Lubbock, TX

  • Xu H, Suzuki N (2001) Effects of carcass size and parental feeding on reproductive success of the burying beetle Nicrophorus quadripunctatus (Coleoptera Silphidae). Entomol Sci 4:217–222

    Google Scholar 

  • Zoecklein B (2005) The good volatile sulfur compounds. Enology Notes 101. http://www.fst.vt.edu/extension/enology/EN/101.html

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Acknowledgement

We are highly indebted to Jarmila Titzenthalerová and to Ondřej Blažek (in memoriam) for their skilful technical assistance in insect handling and electrophysiological experiments. We also thank to Miroslav Šálek (Faculty of Environmental Sciences, Czech University of Life Sciences, Prague) for help in statistical calculations. Special thanks are addressed to Yvonne Kavanagh (Dublin and IOCB Prague) for the language check of this paper. We very much thank the anonymous referees for constructive criticism of the manuscript. This work was supported by research project Z4-055-905 (Institute of Organic Chemistry ASCR, v.v.i.) and by grant CULS-IGA 200741110031 (Faculty of Environmental Sciences, Czech University of Life Sciences, Prague).

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Kalinová, B., Podskalská, H., Růžička, J. et al. Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96, 889–899 (2009). https://doi.org/10.1007/s00114-009-0545-6

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