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Volatile compounds reveal age: a study of volatile organic compounds released by Chrysomya rufifacies immatures

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Abstract

Age determination of insects collected from vertebrate remains is an essential step in estimating time since colonization as related to the post-mortem interval. Long-established methods for making such estimates rely on determining age related to stage of development at the time of collection in relation to conditions experienced. However, such estimates are based on the completion of a stage of development. Methods allowing for more precise estimates of age (i.e., within a stage of development) are sorely needed. This study examined the potential of volatile organic compounds emitted by blow fly, Ch. rufifacies (Macquart), immatures to determine stage of development, which could potentially be used to estimate the age. Volatile organic compounds (VOCs) from the larval and pupal stages of Ch. rufifacies were collected by headspace solid-phase micro-extraction followed by gas chromatography-mass spectrometry (GC-MS). Analyses indicated 37 compounds shift quantitatively, as well as qualitatively, as the larvae and pupae age. Furthermore, compounds, such as 2-ethyl-1-hexanol, phenol, butanoic acid, hexadecanoic acid, octadecanoic acid, 2-methyl propanamide, and 2-methyl butanoic acid, serve as indicator compounds of specific stages within Ch. rufifacies development. This information could be important to determine if these compounds can be used in the field to predict the presence of certain developmental stages, in order to determine the potential of using volatile markers to estimate time of colonization.

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References

  1. Tarone AM, Sanford MR (2017) Is PMI the hypothesis or the null hypothesis? J Med Entomol 54(5):1109–1115

    PubMed  Google Scholar 

  2. Greenberg B (1991) Flies as forensic indicators. J Med Entomol 28:565–577

    CAS  PubMed  Google Scholar 

  3. Anderson GS (2000) Minimum and maximum development rates of some forensically important Calliphoridae (Diptera). J Forensic Sci 45:824–832

    CAS  PubMed  Google Scholar 

  4. Dadour IR, Cook DF, Wirth N (2001) Rate of development of Hydrotaea rostrata under summer and winter (cyclic and constant) temperature regimes. Med Vet Entomol 15:177–182

    CAS  PubMed  Google Scholar 

  5. Grassberger M, Reiter C (2001) Effect of temperature on Lucilia sericata (Diptera: Calliphoridae) development with special reference to the isomegalen- and isomorphen-diagram. Forensic Sci Int 120:32–36

    CAS  PubMed  Google Scholar 

  6. Wells JD, King J (2001) Incidence of precocious egg development in flies of forensic importance (Calliphoridae). Pan-Pac Entomol 77:235–239

    Google Scholar 

  7. Anderson GS (2004) Determining time of death using blow fly eggs in the early postmortem interval. Int J Legal Med 118:240–241

    CAS  PubMed  Google Scholar 

  8. Kaneshrajah G, Turner B (2004) Calliphora vicina larvae grow at different rates on different body tissues. Int J Legal Med 118:242–244

    PubMed  Google Scholar 

  9. Sharma R, Garg RK (2015) Various methods for the estimation of the postmortem interval from Calliphoridae: a review. Egypt J Forensic Sci 5(1):1–12

    CAS  Google Scholar 

  10. Bala M, Sharma A (2016) Review of some recent techniques of age determination of blow flies having forensic implications. Egypt J Forensic Sci 6(3):203–208

    Google Scholar 

  11. Moore HE, Adam CD (2013) Drijfhout FP (2013) potential use of hydrocarbons for aging Lucilia sericata blowfly larvae to establish the postmortem interval. J Forensic Sci 58:404–412

    CAS  PubMed  Google Scholar 

  12. Moore HE, Adam CD, Drijfhout FP (2014) Identifying 1st instar larvae for three forensically important blowfly species using “fingerprint” cuticular hydrocarbon analysis. Forensic Sci Int 240:48–53

    CAS  PubMed  Google Scholar 

  13. Braga MV, Pinto ZT, Queiroz MMC, Matsumoto N, Blomquist GJ (2013) Cuticular hydrocarbons as a tool for the identification of insect species: Puparial cases from Sarcophagidae. Acta Trop 128(3):479–485

    CAS  PubMed  Google Scholar 

  14. Ye G, Li K, Zhu j, Zhu G, Hu C (2007) Cuticular hydrocarbon composition in pupal exuviae for taxonomic differentiation of six necrophagous flies. J Med Entomol 44: 450–456

  15. Roux O, Gers C, Legal L (2008) Ontogenetic study of three Calliphoridae of forensic importance through cuticular hydrocarbon analysis. Med Vet Entomol 22:309–317

    CAS  PubMed  Google Scholar 

  16. Sharma A, Drijfhout FP, Tomberlin JK, Bala M (2020) Cuticular hydrocarbons as a tool for determining the age of Chrysomya rufifacies (Diptera: Calliphoridae) larvae. J Forensic Sci:1–10

  17. Statheropoulos M, Agapiou A, Spiliopouiou C, Pallis GC, Sianos E (2007) Environmental aspects of VOCs evolved in the early stages of human decomposition. Sci Total Environ 385:221–227

    CAS  PubMed  Google Scholar 

  18. Frederickx C, Dekeirsschieter J, Brostaux Y, Wathelet JP, Verheggen FJ, Haubruge E (2012) Volatile organic compounds released by blowfly larvae and pupae: new perspectives in forensic entomology. Forensic Sci Int 219:215–220

    CAS  PubMed  Google Scholar 

  19. Smith KGV (1986) A manual of forensic entomology, British museum (natural history). UK and Cornell University Press, Ithaca, New York, London

    Google Scholar 

  20. Wall R, Warnes ML (1994) Responses of the sheep blowfly Lucilia sericata to carrion odour and carbon dioxide. Entomol Exp Appl 73:239–246

    Google Scholar 

  21. Fisher P, Wall R, Ashworth JR (1998) Attraction of the sheep blowfly, Lucilia sericata (Diptera: Calliphoridae) to carrion bait in the field. Bull Entomol Res 88:611–616

    Google Scholar 

  22. Anderson GS (2001) Succession on carrion and its relationship to determining time of death. In: Castner JL (ed) Byrd JH. CRC Press, Boca Raton, Forensic Entomology. The Utility of Arthropods in Legal Investigations, pp 143–175

    Google Scholar 

  23. Amendt J, Krettek R, Zehner R (2004) Forensic entomology. Naturwissenschaften 91:51–65

    CAS  PubMed  Google Scholar 

  24. Ody H, Bulling MT, Barnes KM (2017) Effects of environmental temperature on oviposition behavior in three blow fly species of forensic importance. Forensic Sci Int 275:138–143

    PubMed  Google Scholar 

  25. Barton Browne L, Bartell RJ, Shorey HH (1969) Pheromone-mediated behaviour leading to group oviposition in the blowfly Lucilia cuprina. J Insect Physiol 15:1003–1014

    Google Scholar 

  26. Tomberlin JK, Crippen TL, Tarone AM, Singh B, Adams K, Rezenom YH, Benbow ME, Flores M, Longnecker M, Pechal JL, Russell DH, Beier RC, Wood TK (2012) Interkingdom responses of flies to bacteria mediated by fly physiology and bacterial quorum sensing. Anim Behav 84(6):1149–1456

    Google Scholar 

  27. 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

    CAS  PubMed  Google Scholar 

  28. 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(2):386–390

    PubMed  Google Scholar 

  29. Gill-King H (1997) Chemical and ultrastructural aspects of decomposition. In: Haglung WD, Sorg MH (eds) Forensic taphonomy: the postmortem fate of human remains. CRC Press, Boca Raton, FL, pp 93–108

    Google Scholar 

  30. Vass AA, Barshick SA, Sega G, Caton J, Skeen JT, Love JC, Synstelien JA (2002) Decomposition chemistry of human remains: a new methodology for determining the postmortem interval. J Forensic Sci 47:542–553

    CAS  PubMed  Google Scholar 

  31. Easton C, Feir D (1991) Factors affecting the oviposition of Phaenicia sericata (meigen) (diptera, calliphoridae). J Kansas Entomol Soc 64:287–294

    Google Scholar 

  32. Tenorio FM, Olson JK, Coates CJ (2003) Decomposition studies, with a catalog and descriptions of forensically important blow flies (Diptera:Calliphoridae) in Central Texas. Southwes Entomol 28:37–45

    Google Scholar 

  33. Jirón L (1979) On the calliphorid flies of Costa Rica (Diptera: Cyclorrhapha). Brenesia 16:65–68

    Google Scholar 

  34. Greenberg B, Povolny D (1971) Bionomics of flies. Flies and disease, Greenberg B (Ed.), Vol. 1, Princeton University press, Princeton, pp 57-83

  35. Wells JD, Greenberg B (1992) Laboratory interaction between introduced Chrysomya rufifacies and native Cochliomyia macellaria (Diptera: Calliphoridae). Environ Entomol 21:641–645

    Google Scholar 

  36. Chitnis PS (1965) Some studies of cannibalism in the larvae of the blow fly Chrysomya rufifacies, Macq. (Diptera). J Univ Poona 42:27–36

    Google Scholar 

  37. Baumgartner DL (1993) Review of Chrysomya rufifacies (Diptera: Calliphoridae). J Med Entomol 30:338–352

    CAS  PubMed  Google Scholar 

  38. Drijfhout FP (2010) Cuticular hydrocarbons a new tool in forensic entomology. In: Amendt J, Carlo P, Campobasso M, Goff L, Grassberger M (eds) Current concepts in forensic entomology. Springer, The Netherlands, pp 179–203

    Google Scholar 

  39. Leroy PD, Sabri A, Verheggen FJ, Francis F, Thonart P, Haubruge E (2011) The semiochemically mediated interactions between bacteria and insects. Chemoecology 21:113–122

    CAS  Google Scholar 

  40. 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(2):998–1005

    CAS  PubMed  Google Scholar 

  41. Kepchia D, Xu P, Terryn R, Castro A, Schürer SC, Leal WS, Luetje CW (2019) Use of machine learning to identify novel, behaviorally active antagonists of the insect odorant receptor co-receptor (Orco) subunit. Sci Rep 9(1):4055

    PubMed  PubMed Central  Google Scholar 

  42. Sheoran N, Valiya Nadakkakath A, Munjal V, Kundu A, Subaharan K, Venugopal V, Rajamma S, Eapen SJ, Kumar A (2015) Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res 173:66–78

    CAS  PubMed  Google Scholar 

  43. Xie S, Zang H, Wu H, Uddin Rajer F, Gao X (2018) Antibacterial effects of volatiles produced by Bacillus strain D13 against Xanthomonas oryzae pv. Oryzae. Mol Plant Pathol 19(1):49–58

    CAS  PubMed  Google Scholar 

  44. Leroy PD, Sabri A, Heuskin S, Thonart P, Lognay G, Verheggen FJ, Francis F, Brostaux Y, Felton GW, Haubruge E (2011) Microorganisms from aphid honeydew attract and enhance the efficacy of natural enemies. Nat Commun 2(1):348

    PubMed  PubMed Central  Google Scholar 

  45. Metcalf RL (1990) Chemical ecology of dacine fruit flies (Diptera: Tephritidae). Ann Entomol Soc Am 83:1017–1030

    CAS  Google Scholar 

  46. Fletcher BS (1969) The structure and function of the sex pheromone glands of the male Queensland fruit fly, Dacus tryoni. J Insect Physiol 15(8):1309–1322

    Google Scholar 

  47. Kobayashi RM, Ohinata K, Chambers DL, Fujimoto MS (1978) Sex pheromones of the oriental fruit fly and the melon fly: mating behavior, bioassay method, and attraction of females by live males and by suspected pheromone glands of males. Environ Entomol 7:107–112

    Google Scholar 

  48. 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 28:1629–1640

    CAS  PubMed  Google Scholar 

  49. Tomberlin JK, Crippen TL, Wu G, Griffin AS, Wood TK, Kilner RM (2017) Indole: an evolutionary conserved influencer of behavior across kingdoms. BioEssays 39(2):1600203

    Google Scholar 

  50. Ma Q, Fonseca A, Liu W, Fields AT, Pimsler ML, Spindola AF, Tarone AM, Crippen TL, Tomberlin JK, Wood TK (2012) Proteus mirabilis interkingdom swarming signals attract blow flies. ISME J 6(7):1356–1366

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Fedina TY, Kuo TH, Dreisewerd K, Dierick HA, Yew JY, Pletcher SD (2012) Dietary effects on cuticular hydrocarbons and sexual attractiveness in Drosophila. PLoS One 7(12):e49799

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Authors are grateful to United States-India Educational Foundation to provide funding support to complete this study. Authors are also thankful to Dr. Travis Rusch from FLIES Facility, Texas A&M, for providing C. rufifacies adults to start a colony and members of the F.L.I.E.S Facility for the assistance during experimental work. Authors extend thanks to the Geochemical and Environmental Research Group (GERG), Texas A&M, for providing GC-MS facility. We thank Dr. Vivek Polshettiwar an associate professor from Tata Institute of Fundamental research, Mumbai, India, for providing access to his laboratory to use Chemstation software to complete the GC-MS analysis.

Funding

This study was funded by Institute of International Education, New York, USA (Grant number: 2221/DR/2017-2018).

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Authors and Affiliations

  1. Department of Zoology and Environmental Sciences, Punjabi University, Patiala, 147002, India

    Anika Sharma & Madhu Bala

  2. Department of Entomology, Texas A&M University, College Station, TX, USA

    Jeffery K. Tomberlin

  3. Department of Biology & Biochemistry, University of Houston, Houston, TX, USA

    Pablo Delclos

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  1. Anika Sharma
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  4. Madhu Bala
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Correspondence to Anika Sharma.

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Sharma, A., Tomberlin, J.K., Delclos, P. et al. Volatile compounds reveal age: a study of volatile organic compounds released by Chrysomya rufifacies immatures. Int J Legal Med 135, 967–977 (2021). https://doi.org/10.1007/s00414-020-02471-1

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