Abstract
In the necrophagous burying beetle Nicrophorus vespilloides (Coleoptera: Silphidae), cadaver preference appears to depend on cadaver size and on the maturity of the beetle. We previously showed that newly emerged females with immature ovaries prefer later stages of decomposition of large cadavers. Our present aim is the determination of specific chemical compounds involved in the discrimination of cadaveric odor bouquets and the recognition of specific stages of decomposition. We used headspace samples of maggot-infested piglet cadavers at various decomposition stages and performed gas chromatography coupled with electroantennography (GC-EAD) to record 45 EAD-active compounds. Using GC coupled with mass spectrometry, we identified 13 of the EAD-active compounds. The headspace of the fresh decomposition stage was characterized mainly by high relative amounts of trimethylpyrazine. High relative amounts of dimethyl trisulfide were characteristic of bloated, post-bloating, and advanced decay stages. The advanced decay and dry remains stages were dominated by high relative amounts of phenol. Statistically, this compound had the highest impact on discrimination between the fresh decomposition stage, which is important for mature burying beetles for reproduction, and the advanced decay stage, which is nutritionally more attractive for newly emerged beetles. Phenol might, therefore, function as a key substance for newly emerged female burying beetles, so that they can locate suitable cadavers for feeding to maturation.
Similar content being viewed by others
References
Anderson GS, Vanlaerhoven SL (1996) Initial studies on insect succession on carrion in south western British Columbia. J Forensic Sci 41:617–625
Anton E, Niederegger S, Beutel RG (2011) Beetles and flies collected on pig carrion in an experimental setting in Thuringia and their forensic implications. Med Vet Entomol 25:353–364
Barro N, Aly S, Tidiane OCA, Sababénédjo TA (2006) Carriage of bacteria by proboscises, legs, and feces of two species of flies in street food vending sites in Ouagadougou, Burkina Faso. J Food Prot 69:2007–2010
Benbow ME, Tomberlin JK, Tarone AM (2016) Carrion ecology, evolution, and their applications. CRC Press, Boca Raton
Boeckh J (1962) Elektrophysiologische Untersuchungen an einzelnen Geruchsrezeptoren auf den Antennen des Totengräbers (Necrophorus, Coleoptera). Z Vgl Physiol 46:212–248
Böhm H, Wendler G (1988) Die Windorientierung von Aaskäfern. Mitt Dtsch Ges Allg Angew Entomol 6:91–94
Brodie B, Gries R, Martins A, VanLaerhoven S, Gries G (2014) Bimodal cue complex signifies suitable oviposition sites to gravid females of the common green bottle fly. Entomol Exp Appl 153:114–127
Brodie BS, Babcock T, Gries R, Benn A, Gries G (2015) Acquired smell? Mature females of the common green bottle fly shift semiochemical preferences from feces feeding sites to carrion oviposition sites. J Chem Ecol 42:40–50
Centeno N, Maldonado M, Oliva A (2002) Seasonal patterns of arthropods occurring on sheltered and unsheltered pig carcasses in Buenos Aires Province (Argentina). Forensic Sci Int 126:63–70
Clarke KR, Gorley RN (2006) Primer v6. user manual/tutorial. Primer-E Ltd., Plymouth
Cossé AA, Baker TC (1996) House flies and pig manure volatiles: wind tunnel behavioral studies and electrophysiological evaluations. J Agric Entomol 13:301–317
Davis TS, Crippen TL, Hofstetter RW, Tomberlin JK (2013) Microbial volatile emissions as insect semiochemicals. J Chem Ecol 39:840–859
DeGreeff LE, Furton KG (2011) Collection and identification of human remains volatiles by non-contact, dynamic airflow sampling and SPME-GC/MS using various sorbent materials. Anal Bioanal Chem 401:1295–1307
Dekeirsschieter J, Verheggen FJ, Gohy M, Hubrecht F, Bourguignon L, Lognay G, Haubruge E (2009) Cadaveric volatile organic compounds released by decaying pig carcasses (Sus domesticus L.) in different biotopes. Forensic Sci Int 189:46–53
Dekeirsschieter J, Stefanuto PH, Brasseur C, Haubruge E, Focant JF (2012) Enhanced characterization of the smell of death by comprehensive two-dimensional gas chromatography-time-of-flight mass spectrometry (GCxGC-TOFMS). PLoS One 7:e39005
Dekeirsschieter J, Frederickx C, Lognay G, Brostaux Y, Verheggen FJ, Haubruge E (2013) Electrophysiological and behavioral responses of Thanatophilus sinuatus Fabricius (Coleoptera: Silphidae) to selected cadaveric volatile organic compounds. J Forensic Sci 58:917–923
Eggert AK, Müller JK (1997) Biparental care and social evolution in burying beetles: lessons from the larder. In: Choe JC, Crespi BJ (eds) Social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp. 216–236
Fauvergue X, Lo Genco A, Lo Pinto M (2008) Virgins in the wild: mating status affects the behavior of a parasitoid foraging in the field. Oecologia 156:913–920
Forbes SL, Perrault KA, Stefanuto P-H, Nizio KD, Focant J-F (2014) Comparison of the decomposition VOC profile during winter and summer in a moist, mid-latitude (Cfb) climate. PLoS One 9:e113681
Frederickx C, Dekeirsschieter J, Verheggen FJ, Haubruge E (2012) Responses of Lucilia sericata Meigen (Diptera: Calliphoridae) to cadaveric volatile organic compounds. J Forensic Sci 57:386–390
Goff M (2009) Early post-mortem changes and stages of decomposition in exposed cadavers. Exp Appl Acarol 49:21–36
Groer MW, Luciano AA, Dishaw LJ, Ashmeade TL, Miller E, Gilbert JA (2014) Development of the preterm infant gut microbiome: a research priority. Microbiome 2:38
Heinzel HG, Böhm H (1989) The wind-orientation of walking carrion beetles. J Comp Physiol A 164:775–786
Hoffman EM, Curran AM, Dulgerian N, Stockham RA, Eckenrode BA (2009) Characterization of the volatile organic compounds present in the headspace of decomposing human remains. Forensic Sci Int 186:6–13
Kalinová B, Podskalská H, Růžička J, Hoskovec M (2009) Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses. Naturwissenschaften 96:889–899
Kasper J, Mumm R, Ruther J (2012) The composition of carcass volatile profiles in relation to storage time and climate conditions. Forensic Sci Int 223:64–71
Kasper J, Hartley S, Schatkowski S, Hoch H (2015) The influence of the physiological stage of Lucilia caesar (L.) (Diptera: Calliphoridae) females on the attraction of carrion odor. J Insect Behav 28:183–201
Kentner E, Streit B (1990) Temporal distribution and habitat preference of congeneric insect species found at rat carrion. Pedobiologia 34:347–359
Kočárek P (2003) Decomposition and Coleoptera succession on exposed carrion of small mammal in Opava, the Czech Republic. Eur J Soil Biol 39:31–45
Kreuter K, Bunk E, Lückemeyer A, Twele R, Francke W, Ayasse M (2012) How the social parasitic bumblebee Bombus bohemicus sneaks into power of reproduction. Behav Ecol Sociobiol 66:475–486
Matuszewski S, Bajerlein D, Konwerski S, Szpila K (2008) An initial study of insect succession and carrion decomposition in various forest habitats of Central Europe. Forensic Sci Int 180:61–69
Matuszewski S, Bajerlein D, Konwerski S, Szpila K (2010) Insect succession and carrion decomposition in selected forests of Central Europe. Part 2: composition and residency patterns of carrion fauna. Forensic Sci Int 195:42–51
Matuszewski S, Konwerski S, Fratczak K, Szafalowicz M (2014) Effect of body mass and clothing on decomposition of pig carcasses. Int J Legal Med 128:1039–1048
Matuszewski S, Fratczak K, Konwerski S, Bajerlein D, Szpila K, Jarmusz M, Szafalowicz M, Grzywacz A, Madra A (2015) Effect of body mass and clothing on carrion entomofauna. Int J Legal Med 130:221–232
Müller JK, Eggert AK, Dressel J (1990) Intraspecific brood parasitism in the burying beetle, Necrophorus vespilloides (Coleoptera: Silphidae). Anim Behav 40:491–499
Paczkowski S, Schütz S (2011) Post-mortem volatiles of vertebrate tissue. Appl Microbiol Biotechnol 91:917–935
Paczkowski S, Maibaum F, Paczkowska M, Schütz S (2012) Decaying mouse volatiles perceived by Calliphora vicina Rob.-Desv. J Forensic Sci 57:1497–1506
Paczkowski S, Nicke S, Ziegenhagen H, Schütz S (2015) Volatile emission of decomposing pig carcasses (Sus scrofa domesticus L.) as an indicator for the postmortem interval. J Forensic Sci 60:130–137
Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:e177
Pechal JL, Crippen TL, Tarone AM, Lewis AJ, Tomberlin JK, Benbow ME (2013) Microbial community functional change during vertebrate carrion decomposition. PLoS One 8:e79035
Pechal JL, Crippen TL, Benbow ME, Tarone AM, Dowd S, Tomberlin JK (2014) The potential use of bacterial community succession in forensics as described by high throughput metagenomic sequencing. Int J Legal Med 128:193–205
Peschke K, Krapf D, Fuldner D (1987) Ecological separation, functional relationships, and limiting resources in a carrion insect community. Zool Jahrbücher (Syst) 114:241–265
Powers RH (2005) The decomposition of human remains. In: Rich J, Dean DE, Powers RH (eds) Forensic medicine of the lower extremity: Human identification and trauma analysis of the thigh, leg, and foot, Chapter 1. The Humana Press Inc, Totowa, pp. 3–15
Pukowski E (1933) Ökologische Untersuchungen an Necrophorus f. Z Morphol Ökol 27:518–586
Stadler S, Stefanuto PH, Brokl M, Forbes SL, Focant JF (2013) Characterization of volatile organic compounds from human analogue decomposition using thermal desorption coupled to comprehensive two-dimensional gas chromatography–time-of-flight mass spectrometry. Anal Chem 85:998–1005
Stadler S, Desaulniers J-P, Forbes SL (2015) Inter-year repeatability study of volatile organic compounds from surface decomposition of human analogues. Int J Legal Med 129:641–650
Statheropoulos M, Agapiou A, Spiliopoulou C, Pallis GC, Sianos E (2007) Environmental aspects of VOCs evolved in the early stages of human decomposition. Sci Total Environ 385:221–227
Stefanuto P-H, Perrault KA, Lloyd RM, Stuart B, Rai T, Forbes SL, Focant J-F (2015) Exploring new dimensions in cadaveric decomposition odour analysis. Anal Methods 7:2287–2294
Tomberlin J, Mohr R, Benbow M, Tarone A, VanLaerhoven S (2011) A roadmap for bridging basic and applied research in forensic entomology. Annu Rev Entomol 56:401–421
Trumbo ST, Fiore AJ (1994) Interspecific competition and the evolution of communal breeding in burying beetles. Am Midl Nat 131:169–174
Urbański A, Baraniak E (2015) Differences in early seasonal activity of three burying beetle species (Coleoptera: Silphidae: Nicrophorus F.) in Poland. Coleopt Bull 69:1–10
Vass AA, Bass WM, Wolt JD, Foss JE, Ammons JT (1992) Time since death determinations of human cadavers using soil solution. J Forensic Sci 37:1236–1253
Vass AA, Smith RR, Thompson CV, Burnett MN, Wolf DA, Synstelien JA, Dulgerian N, Eckenrode BA (2004) Decompositional odor analysis database. J Forensic Sci 49:760–769
von Hoermann C, Ruther J, Reibe S, Madea B, Ayasse M (2011) The importance of carcass volatiles as attractants for the hide beetle Dermestes maculatus (de Geer). Forensic Sci Int 212:173–179
von Hoermann C, Ruther J, Ayasse M (2012) The attraction of virgin female hide beetles (Dermestes maculatus) to cadavers by a combination of decomposition odour and male sex pheromones. Front Zool 9:18
von Hoermann C, Steiger S, Müller JK, Ayasse M (2013) Too fresh is unattractive! The attraction of newly emerged Nicrophorus vespilloides females to odour bouquets of large cadavers at various stages of decomposition. PLoS One 8:e58524
Waldow U (1973) Elektrophysiologie eines neuen Aasgeruchrezeptors und seine Bedeutung für das Verhalten des Totengräbers (Necrophorus). J Comp Physiol 83:415–424
Wilson DS, Knollenberg WG (1984) Food discrimination and ovarian development in burying beetles (Coleoptera: Silphidae: Nicrophorus). Ann Entomol Soc Am 77:165–170
Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, Magris M, Hidalgo G, Baldassano RN, Anokhin AP, Heath AC, Warner B, Reeder J, Kyczynski J, Caporaso JG, Lozupone CA, Lauber C, Clemente JC, Knights D, Knight R, Gordon JI (2012) Human gut microbiome viewed across age and geography. Nature 486:222–227
Zito P, Sajeva M, Raspi A, Dötterl S (2014) Dimethyl disulfide and dimethyl trisulfide: so similar yet so different in evoking biological responses in saprophilous flies. Chemoecology 24:261–267
Acknowledgments
We thank the Evangelisches Studienwerk Villigst (Protestant Academic Foundation) for financial support of our study. We are grateful to Gerhard Birling for assistance with fieldwork. We thank Gabriele Wiest-Danner for supporting us with chemical analyses. We cordially thank Ann-Marie Rottler-Hoermann for assistance in statistical analysis and manuscript writing. Finally, we are grateful to Theresa Jones for linguistic advice.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All necessary permits were obtained for the described field studies. No animals were killed for this study. Experiments were conducted with stillborn piglets obtained from a local pig farm (Josef Möst, Jedesheim, Germany).
Conflict of Interest
The authors declare that they have no conflicts of interest.
Rights and permissions
About this article
Cite this article
von Hoermann, C., Ruther, J. & Ayasse, M. Volatile Organic Compounds of Decaying Piglet Cadavers Perceived by Nicrophorus vespilloides . J Chem Ecol 42, 756–767 (2016). https://doi.org/10.1007/s10886-016-0719-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-016-0719-6