Advertisement

International Journal of Legal Medicine

, Volume 133, Issue 4, pp 1267–1278 | Cite as

Environmental factors influencing flight activity of forensically important female blow flies in Central Europe

  • Lena LutzEmail author
  • Marcel A. Verhoff
  • Jens Amendt
Original Article

Abstract

In forensic entomology, evaluation of a possible delay between a person’s death and insect colonization is crucial. We monitored the seasonal flight activities of the most abundant blow flies in an urban habitat in Frankfurt/Germany based on 152 sampling days between April and October 2017. Thirty-six thousand female specimens of 12 necrophagous taxa were sampled as a possible groundwork for establishing a prediction tool for the activity of certain forensically relevant taxa. The most abundant taxon was Lucilia sericata (n = 19,544), followed by Lucilia caesar (n = 8025), Calliphora vicina (n = 5224), and Lucilia ampullacea (n = 1834). Up to six environmental parameters were statistically significant predictors of fly presence, leading to unique patterns of seasonal and daily activity for all four species. In detail, our analysis proved that L. sericata is a sun-loving, high-summer species that dominates the warmer months and is mostly influenced by mean day temperature. In contrast, L. caesar seems to be a shade-loving species that dominates in autumn resp. late-season and is mainly influenced by mean day temperature and wind speed. The activity of L. ampullacea was highly related to mean day temperature and relative humidity. In contrast to all other species, C. vicina behaved differently, particularly due to its occurrence throughout the entire sampling interval and the higher tolerance limits for the measured abiotic parameters, especially temperature. The present study is groundwork for establishing a prediction tool for the flight and oviposition activity of forensically relevant taxa.

Keywords

Female blowflies Forensic entomology Abiotic parameters Monitoring 

Notes

Acknowledgements

The authors would like to thank D. Ricciardi and V. Bernhardt for their assistance during fieldwork, an anonymous colleague for helping with the statistical analysis, and the two anonymous reviewers for their careful reading and commenting of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

414_2018_1967_Fig6_ESM.png (13.4 mb)
Supplementary Figure 1

(PNG 13673 kb)

414_2018_1967_MOESM1_ESM.tif (2.7 mb)
High Resolution (TIF 2809 kb)
414_2018_1967_Fig7_ESM.png (69.4 mb)
Supplementary Figure 2

(PNG 71032 kb)

414_2018_1967_MOESM2_ESM.tif (16 mb)
High Resolution (TIF 16373 kb)

References

  1. 1.
    Villet MH, Richards CS, Midgley JM (2010) Contemporary precision, bias and accuracy of minimum post-mortem intervals estimated using development of carrion-feeding insects. In: Campobasso G (ed) Amendt J, Goff M. Current Concepts in Forensic Entomology. Springer, Dordrecht, pp 109–137Google Scholar
  2. 2.
    Pietro CC, Di Vella G, Introna F (2001) Factors affecting decomposition and Diptera colonization. Forensic Sci Int 120:18–27.  https://doi.org/10.1016/S0379-0738(01)00411-X CrossRefGoogle Scholar
  3. 3.
    Reibe S, Madea B (2010) How promptly do blowflies colonise fresh carcasses? A study comparing indoor with outdoor locations. Forensic Sci Int 195:52–57.  https://doi.org/10.1016/j.forsciint.2009.11.009 CrossRefGoogle Scholar
  4. 4.
    Hofer IMJ, Hart AJ, Martín-Vega D, Hall MJR (2017) Optimising crime scene temperature collection for forensic entomology casework. Forensic Sci Int 270:129–138.  https://doi.org/10.1016/j.forsciint.2016.11.019 CrossRefGoogle Scholar
  5. 5.
    Smith KGV (1986) A manual of forensic entomology. British Museum, LondonGoogle Scholar
  6. 6.
    Amendt J, Krettek R, Zehner R (2004) Forensic entomology. Naturwissenschaften 91:51–65.  https://doi.org/10.1007/s00114-003-0493-5 CrossRefGoogle Scholar
  7. 7.
    George KA, Archer MS, Toop T (2013) Abiotic environmental factors influencing blowfly colonisation patterns in the field. Forensic Sci Int 229:100–107.  https://doi.org/10.1016/j.forsciint.2013.03.033 CrossRefGoogle Scholar
  8. 8.
    Tomberlin JK, Mohr R, Benbow ME, Tarone AM, VanLaerhoven S (2011) A roadmap for bridging basic and applied research in forensic entomology. Annu Rev Entomol 56:401–421.  https://doi.org/10.1146/annurev-ento-051710-103143 CrossRefGoogle Scholar
  9. 9.
    Matuszewski S, Szafałowicz M, Grzywacz A et al (2014) Temperature-dependent appearance of forensically useful flies on carcasses. Int J Legal Med 128:1013–1020.  https://doi.org/10.1007/s00414-013-0921-9 CrossRefGoogle Scholar
  10. 10.
    Ahmad A, Ahmad AH, Dieng H, Satho T, Ahmad H, Aziz AT, Boots M (2011) Cadaver wrapping and arrival performance of adult flies in an oil palm plantation in northern Peninsular Malaysia. J Med Entomol 48:1236–1246.  https://doi.org/10.1603/MI10247 CrossRefGoogle Scholar
  11. 11.
    Bhadra P, Hart AJ, Hall MJR (2014) Factors affecting accessibility to blowflies of bodies disposed in suitcases. Forensic Sci Int 239:62–72.  https://doi.org/10.1016/j.forsciint.2014.03.020 CrossRefGoogle Scholar
  12. 12.
    Comstock JL, Desaulniers J-P, LeBlanc HN, Forbes SL (2015) New decomposition stages to describe scenarios involving the partial and complete exclusion of insects. Can Soc Forensic Sci J 48:1–19.  https://doi.org/10.1080/00085030.2014.929850 CrossRefGoogle Scholar
  13. 13.
    Mohr RM, Tomberlin JK (2014) Environmental factors affecting early carcass attendance by four species of blow flies (Diptera: Calliphoridae) in Texas. J Med Entomol 51:702–708.  https://doi.org/10.1603/ME13149 CrossRefGoogle Scholar
  14. 14.
    Searle KRR, Blackwell A, Falconer D et al (2012) Identifying environmental drivers of insect phenology across space and time: Culicoides in Scotland as a case study. Bull Entomol Res 103:1–16.  https://doi.org/10.1017/S0007485312000466 Google Scholar
  15. 15.
    Berg MC, Benbow ME (2013) Environmental factors associated with Phormia regina ( Diptera : Calliphoridae ) oviposition. J Med Entomol 50:451–457.  https://doi.org/10.1603/ME12188 CrossRefGoogle Scholar
  16. 16.
    Lecheta MC, Corrêa RC, Moura MO (2017) Climate shapes the geographic distribution of the blowfly sarconesia chlorogaster (Diptera: Calliphoridae): an environmental niche modeling approach. Environ Entomol 46:1051–1059.  https://doi.org/10.1093/ee/nvx124 CrossRefGoogle Scholar
  17. 17.
    Rose H, Wall R (2011) Modelling the impact of climate change on spatial patterns of disease risk: sheep blowfly strike by Lucilia sericata in Great Britain. Int J Parasitol 41:739–746.  https://doi.org/10.1016/j.ijpara.2011.01.012 CrossRefGoogle Scholar
  18. 18.
    Nicholson AJ (1934) The influence of temperature on the activity of sheep-blowflies. Bull Entomol Res 25:85.  https://doi.org/10.1017/S0007485300012529 CrossRefGoogle Scholar
  19. 19.
    Taylor LR (1963) Analysis of the effect of temperature on insects in flight. J Animal Ecol 32:99–117.  https://doi.org/10.2307/2520 CrossRefGoogle Scholar
  20. 20.
    Ngoen-Klan R, Moophayak K, Klong-Klaew T et al (2011) Do climatic and physical factors affect populations of the blow fly Chrysomya megacephala and house fly Musca domestica? Parasitol Res 109:1279–1292.  https://doi.org/10.1007/s00436-011-2372-x CrossRefGoogle Scholar
  21. 21.
    Azevedo RR, Krüger RF (2013) The influence of temperature and humidity on abundance and richness of Calliphoridae (Diptera). Iheringia Série Zool 103:145–152.  https://doi.org/10.1590/S0073-47212013000200010 CrossRefGoogle Scholar
  22. 22.
    Crespo J, Castelo MK (2012) Barometric pressure influences host-orientation behavior in the larva of a dipteran ectoparasitoid. J Insect Physiol 58:1562–1567.  https://doi.org/10.1016/j.jinsphys.2012.09.010 CrossRefGoogle Scholar
  23. 23.
    Mahat NA, Zafarina Z, Jayaprakash PT (2009) Influence of rain and malathion on the oviposition and development of blowflies (Diptera: Calliphoridae) infesting rabbit carcasses in Kelantan, Malaysia. Forensic Sci Int 192:19–28.  https://doi.org/10.1016/j.forsciint.2009.07.008 CrossRefGoogle Scholar
  24. 24.
    Parman DC (1916) Observations of the effect of storm phenoma on insect activity. J Econom Entomol 13:339–343CrossRefGoogle Scholar
  25. 25.
    Mann RW, Bass WM, Meadows L (1990) Time since death and decomposition of the human body: variables and observations in case and experimental field studies. J Forensic Sci 35:103–111.  https://doi.org/10.1520/JFS12806J Google Scholar
  26. 26.
    MacLeod J, Donnelly J (1962) Microgeographic aggregations in blowfly populations. J Anim Ecol 31:525–543CrossRefGoogle Scholar
  27. 27.
    Pitts KM, Wall R (2004) Adult mortality and oviposition rates in field and captive populations of the blowfly Lucilia sericata. Ecol Entomol 29:727–734.  https://doi.org/10.1111/j.0307-6946.2004.00653.x CrossRefGoogle Scholar
  28. 28.
    Wellington WG (1946) Some reactions of Muscoid Diptera to changes in atmospheric pressure. Can J Research 24:105–117CrossRefGoogle Scholar
  29. 29.
    McAlpine D (2011) Observations on antennal morphology in Diptera, with particular reference to the articular surfaces between segments 2 and 3 in the Cyclorrhapha. Rec Aust Museum 63:113–166.  https://doi.org/10.3853/j.0067-1975.63.2011.1585 CrossRefGoogle Scholar
  30. 30.
    Edwards DK (1961) Activity of two species of Calliphora (Diptera) during barometric pressure changes of natural magnitude. Can J Zool 39:623–635.  https://doi.org/10.1139/z61-067 CrossRefGoogle Scholar
  31. 31.
    Digby PSB (1958) Flight activity in the blowfly, Calliphora erythrocephala, in relation to wind speed, with special reference to adaptation. J Exp Biol 35:776–795Google Scholar
  32. 32.
    Wooldridge J, Scrase L, Wall R (2007) Flight activity of the blowflies, Calliphora vomitoria and Lucilia sericata, in the dark. Forensic Sci Int 172:94–97.  https://doi.org/10.1016/j.forsciint.2006.12.011 CrossRefGoogle Scholar
  33. 33.
    Amendt J, Zehner R, Reckel F (2008) The nocturnal oviposition behaviour of blowflies (Diptera: Calliphoridae) in Central Europe and its forensic implications. Forensic Sci Int 175:61–64.  https://doi.org/10.1016/j.forsciint.2007.05.010 CrossRefGoogle Scholar
  34. 34.
    Moophayak K, Sukontason KL, Ruankham W, Tomberlin JK, Bunchu N (2017) Variation in the time of colonization of broiler carcasses by carrion flies in Nakhonsawan Province, Thailand. J Med Entomol 54:1157–1166.  https://doi.org/10.1093/jme/tjx082 CrossRefGoogle Scholar
  35. 35.
    Smith JL, Palermo NA, Theobald JC, Wells JD (2016) The forensically important blow fly, Chrysomya megacephala (Diptera: Calliphoridae), is more likely to walk than fly to carrion at low light levels. Forensic Sci Int 266:245–249.  https://doi.org/10.1016/j.forsciint.2016.06.004 CrossRefGoogle Scholar
  36. 36.
    Erzinçlioğlu Z (1996) Blowflies. Richmond Publishing, SloughGoogle Scholar
  37. 37.
    Vogt WG, Woodburn TL, Morton R, Ellem BA (1983) The analysis and standardisation of trap catches of Lucilia cuprina (Wiedemann) (Diptera: Calliphoridae). Bull Entomol Res 73:609–617.  https://doi.org/10.1017/S0007485300009214 CrossRefGoogle Scholar
  38. 38.
    Baldridge RS, Wallace SG, Kirkpatrick R (2006) Investigation of nocturnal oviposition by necrophilous flies in Central Texas. J Forensic Sci 51:125–126.  https://doi.org/10.1111/j.1556-4029.2005.00022.x CrossRefGoogle Scholar
  39. 39.
    Wall R, French NP, Morgan KL (1993) Predicting the abundance of the blowfly Lucilia sericata (Diptera: Calliphoridae). Bull Entomol Res 83:431–436.  https://doi.org/10.1017/S0007485300029345 CrossRefGoogle Scholar
  40. 40.
    Rognes K (1991) Blowflies (Diptera, Calliphoridae) of Fennoscandia and Denmark. Scandinavian Science Press, LeidenGoogle Scholar
  41. 41.
    Szpila K (2012) Key for identification of European and Mediterranean blowflies (Diptera, Calliphoridae) of medical and veterinary importance - adult flies. In: Gennard (ed) Forensic entomology: an introduction, 2nd edn. Wiley-Blackwell, Hoboken, pp 77–81Google Scholar
  42. 42.
    Oksanen J, Blanchet FG, Kindt R et al (2018) Vegan: community ecology package. R Packag Version 2:4–6.  https://doi.org/10.1093/molbev/msv334 Google Scholar
  43. 43.
    R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL http://www.R-project.org/ Google Scholar
  44. 44.
    Martín-Vega D, Baz A (2013) Sex-biased captures of sarcosaprophagous Diptera in carrion-baited traps. J Insect Sci 13(14):1–12.  https://doi.org/10.1673/031.013.1401 CrossRefGoogle Scholar
  45. 45.
    Hwang C, Turner BD (2005) Spatial and temporal variability of necrophagous Diptera from urban to rural areas. Med Vet Entomol 19:379–391.  https://doi.org/10.1111/j.1365-2915.2005.00583.x CrossRefGoogle Scholar
  46. 46.
    Pohjoismäki JLO, Karhunen PJ, Goebeler S, Saukko P, Sääksjärvi IE (2010) Indoors forensic entomology: colonization of human remains in closed environments by specific species of sarcosaprophagous flies. Forensic Sci Int 199:38–42.  https://doi.org/10.1016/j.forsciint.2010.02.033 CrossRefGoogle Scholar
  47. 47.
    Holdaway FG (1933) Differential behaviour of Lucilia sericta Meig. and Lucilia caesar L. in natural envirnonments. J Anim Ecol 2:263–265CrossRefGoogle Scholar
  48. 48.
    Bernhardt V, Bálint M, Verhoff MA, Amendt J (2018) Species diversity and tissue specific dispersal of necrophagous Diptera on human bodies. Forensic Sci Med Pathol 14:76–84.  https://doi.org/10.1007/s12024-018-9947-0 CrossRefGoogle Scholar
  49. 49.
    Greenberg B (1991) Flies as forensic indicators. J Med Entomol 28:565–577.  https://doi.org/10.1093/jmedent/28.5.565 CrossRefGoogle Scholar
  50. 50.
    Barry RG, Chorely RJ (2003) Atmosphere, weather and climate. Routledge, LondonGoogle Scholar
  51. 51.
    Wellington WG (1946) The effects of variations in atmospheric pressure upon insects. Can J Res 24:51–70CrossRefGoogle Scholar
  52. 52.
    Barton Browne L (1962) The relationship between oviposition in the blowfly Lucilia cuprina and the presence of water. J Insect Physiol 8:383–390.  https://doi.org/10.1016/0022-1910(62)90072-0 CrossRefGoogle Scholar
  53. 53.
    Cragg JB, Ramage GR (1945) Chemotropic studies on the blow-flies Lucilia sericata (Mg.) and Lucilia caesar (L.). Parasitology 36:168–175.  https://doi.org/10.1017/S0031182000012142 CrossRefGoogle Scholar
  54. 54.
    Dabbs GR (2015) How should forensic anthropologists correct National Weather Service Temperature Data for use in estimating the postmortem interval? J Forensic Sci 60:581–587.  https://doi.org/10.1111/1556-4029.12724 CrossRefGoogle Scholar
  55. 55.
    Johnson AP, Wallman JF, Archer MS (2012) Experimental and casework validation of ambient temperature corrections in forensic entomology. J Forensic Sci 57:215–221.  https://doi.org/10.1111/j.1556-4029.2011.01900.x CrossRefGoogle Scholar
  56. 56.
    Michalski M, Nadolski J (2018) Thermal conditions in selected urban and semi-natural habitats, important for the forensic entomology. Forensic Sci Int 287:153–162.  https://doi.org/10.1016/j.forsciint.2018.03.042 CrossRefGoogle Scholar
  57. 57.
    Matuszewski S, Szafalowicz M, Jarmusz M (2013) Insects colonising carcasses in open and forest habitats of Central Europe: search for indicators of corpse relocation. Forensic Sci Int 231:234–239.  https://doi.org/10.1016/j.forsciint.2013.05.018 CrossRefGoogle Scholar
  58. 58.
    Smith KE, Wall R (1997) The use of carrion as breeding sites by the blowfly Lucilia sericata and other Calliphoridae. Med Vet Entomol 11:38–44.  https://doi.org/10.1111/j.1365-2915.1997.tb00287.x CrossRefGoogle Scholar
  59. 59.
    Díaz-Aranda LM, Martín-Vega D, Gómez-Gómez A, Cifrián B, Baz A (2018) Annual variation in decomposition and insect succession at a periurban area of central Iberian Peninsula. J Forensic Legal Med 56:21–31.  https://doi.org/10.1016/j.jflm.2018.03.005 CrossRefGoogle Scholar
  60. 60.
    Lane RP (1975) An investigation into blowfly (Diptera:Calliphoridae) succession on corpses. J Nat Hist 9:581–588.  https://doi.org/10.1080/00222937500770461 CrossRefGoogle Scholar
  61. 61.
    Cragg JB, Hobart J (1955) A study of a field population of the blowflies Lucilia caesar (L.) and L. sericata (Mg.). Ann Appl Biol 43:645–663CrossRefGoogle Scholar
  62. 62.
    Kuusela S, Hanski I (1982) The structure of carrion fly communities: the size and the type of carrion. Ecogr 5:337–348.  https://doi.org/10.1111/j.1600-0587.1982.tb01048.x CrossRefGoogle Scholar
  63. 63.
    Aak A, Knudsen GK, Soleng A (2010) Wind tunnel behavioural response and field trapping of the blowfly Calliphora vicina. Med Vet Entomol 24:250–257.  https://doi.org/10.1111/j.1365-2915.2010.00872.x Google Scholar
  64. 64.
    Fremdt H, Amendt J (2014) Species composition of forensically important blow flies (Diptera: Calliphoridae) and flesh flies (Diptera: Sarcophagidae) through space and time. Forensic Sci Int 236:1–9.  https://doi.org/10.1016/j.forsciint.2013.12.010 CrossRefGoogle Scholar
  65. 65.
    Vanin S, Tasinato P, Ducolin G, Terranova C, Zancaner S, Montisci M, Ferrara SD, Turchetto M (2008) Use of Lucilia species for forensic investigations in Southern Europe. Forensic Sci Int 177:37–41.  https://doi.org/10.1016/j.forsciint.2007.10.006 CrossRefGoogle Scholar
  66. 66.
    Gennard D (2012) Forensic entomology: an introduction. Wiley-Blackwell, HobokenGoogle Scholar
  67. 67.
    Deonier CC (1940) Carcass temperatures and their relation to winter blowfly populations and activity in the Southwest. J Econ Entomol 33:166–170CrossRefGoogle Scholar
  68. 68.
    Faucherre J, Cherix D, Wyss C (1999) Behaviour of Calliphora vicina (Diptera,Calliphoridae) under extreme conditions. J Insect Behav 12:687–690CrossRefGoogle Scholar
  69. 69.
    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.  https://doi.org/10.1016/j.forsciint.2017.03.001 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Institute of Legal Medicine, University Hospital Frankfurt am MainGoethe-UniversityFrankfurt am MainGermany

Personalised recommendations