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Low Temperature Episodes in Development of Blowflies: Implications for Postmortem Interval Estimation

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Low Temperature Episodes in Development of Blowflies: Implications for Postmortem Interval Estimation Medical and Veterinary Entomology (2003) 17, 178–186 Low temperature episodes in development of blowflies: implications for postmortem interval estimation C. AMES andB. TURNER Department of Life Sciences, King’s College London, U.K. Abstract. Traditionallythe calculation of accumulated degree daysor hours (ADD or ADH) involves the concept of a minimum threshold temperature below which development ceases. Hence in fluctuating conditions, where tempera- tures drop below this threshold, there maybe periods of time when development is taken to be zero. This has important implications when the calculation of post- mortem interval (PMI) is based on the ADD or ADH of larval dipterans. Normal development of larvae of the blowflies Calliphora vicina Robineau-Desvoidyand C. vomitoria L. (Diptera: Calliphoridae) at 20C was interrupted bycold episodes. The expectation was that total development time would increase bythe period at low (therefore no development) temperature but the total ADD or ADH should be the same as non-cold treated cohorts. The results, however, showed that total ADH for both species decreased linearlywith increasing temperature with no evidence of anyminimum threshold temperature effect. The increased ADH at low temperatures maybe due to either continued but reduced development or a delayin development restarting after the cold episode. Use of ADH in PMI estimations has shortcomings particularlyduring the winter period where low temperatures are involved or where there are sudden summer cold spells during the development period. As blowflydevelopment progresses from egg to pupa such errors will be compounded. Key words. Calliphora vicina, Calliphora vomitoria, development threshold tem- perature, forensic entomology, postmortem interval. Introduction Northern Europe. In favourable conditions these species lay their eggs around natural orifices or wounds on the fresh In forensic science, insect evidence is most commonlyused corpse within a short time after death. These hatch to to estimate the time of death of a corpse (the postmortem larvae, which grow through three stages. During the interval, PMI). Some of the first insects to invade a corpse latter part of the third stage, larvae stop feeding, migrate in the U.K. are Calliphoridae (Diptera), including species of from the corpse and burrow down into the soil to pupate. Calliphora, Protophormia and Lucilia (Lane, 1975). In many The pupal stage has the largest duration before adults temperate regions Calliphora species are considered emerge. the most important, with Calliphora vicina (Robineau- Being poikilothermic, the rate of development in insects is Desvoidy) (¼ C. erythrocephala Meigen) and Calliphora governed byambient temperature; the higher the tempera- vomitoria (Linnaeus) being widelydistributed throughout ture the faster development occurs. Thus byknowing the ambient temperature and the progress of blowflydevelop- ment, an estimation of time since the eggs were laid can be made. Correspondence: Dr B. D. Turner, Department of Life Sciences, Two methods to estimate PMI using blowflydevelop- King’s College London, Franklin Wilkins Building, 150 Stamford St., ment are available. Larval size, usuallylength, can be London SE1 9NN, U.K. E-mail: [email protected] compared with data on larval size related to temperature 178 # 2003 The Royal Entomological Society Low temperature and blowfly development 179 and time in an isomegalendiagram (Grassberger & Reiter, room temperature (20–22C). Flies were supplied with 2001). There are a number of difficulties with this approach, granulated sugar and water ad libitum. New flies were including the actual size, the limited number of published added to these populations as the experiment progressed. isomegalendiagrams and the restriction of this method to Each cage onlycontained approximately100 flies to avoid the larval stages only. The other approach is to measure the overcrowding (Saunders, 1997). accumulated degree days or hours (ADD or ADH) needed A few days before eggs were required, liquid liver exudate to reach a particular stage of development. Accumulated was provided as a protein source for the flies. Fresh pigs’ degree days or hours are the product of temperature above liver was then introduced as an oviposition and larval food a species’ (and possiblygeographical population) minimum source. Females massed upon the liver and oviposition developmental threshold and the time spent at that would normallybegin 30 min to 1 h later. The time of temperature. Prediction of insect development focuses on oviposition was noted and the liver and eggs were removed the range where the relationship between development rate from the adult cage. Eggs were then separated onto new and temperature is constant and is based on the work of liver in a disposable weighing boat. To prevent anylarval Abrami (1972), Allen (1976), Arnold (1960), and Baskerville & mass effects which might cause a localized temperature Emin (1969) (see also Wagner et al., 1984). One difficulty elevation (Vinogradova & Marchenko, 1984 cited in Catts & with this linear day/hour degree model is that it only truly Goff, 1992; Turner & Howard, 1992), eggs were separated applies to the thermal range where temperature is directly into small clumps of about two to five and spread over the proportional to development. The calculated ADD/ADH liver. The liver, which had been kept refrigerated, was required for development will be too low at temperatures allowed to warm up to room temperature before the eggs near the lower threshold and too high near the optimum were placed on it. Approximately30–40 eggs were used in temperature (Wagner et al., 1984). Additionally, although it each experimental replicate. is accepted that development ceases at low temperatures The weighing boats, containing liver and eggs, were (Laudien, 1973 cited in Lamb et al., 1984), the lower placed on a 2-cm layer of soil-less compost in individual threshold temperature is often verydifficult to determine plastic containers (7 Â 8 Â 11 cm) with a plastic lid. The accuratelybecause insects survive for long periods with near compost provided a medium in which the post-feeding zero development. The Development Threshold Tempera- larvae could pupate. The liver was changed regularlyso ture (DTT) is most commonlyestimated bymeasuring that food for the larvae was always in excess, to avoid developmental rates at a range of temperatures and fitting competition. The containers were then kept at 20C (Cooled a regression line to the results. This can then be extrapolated Incubator, LMS, Sevenoaks, Kent, U.K.) and a second to the x-axis where development is zero. incubator (Cooled Incubator, Sanyo-Gallenkamp, U.K.) According to Higley& Haskell (2001) who reworked was used when needed for the alternative temperature. Kamal’s data (Kamal, 1958), the DTT for C. vicina and The laboratorywas air-conditioned at 20 C Æ 1Cso C. vomitoria is 6C, yet recent studies suggest this varies that the removal of larvae from the 20C incubator for with locality(Saunders & Hayward,1998). The majorityof measurement did not varytheir temperature regime. The past research on the effects of temperature on development second incubator (monitored using a TinyTag, Gemini data on species in the Calliphoridae has been done at tempera- loggers, Chichester, U.K.) returned to the set temperature tures close to the optimum, mainlyover 20 C (Dallwitz, within 10 min of opening and closing the door to put in the 1984; Greenberg & Tantawi, 1993; Anderson, 2000). experimental larvae and was then left unopened until the Vinogradova & Marchenko (1984), however, did include end of the exposure period. Larvae were kept in continuous lower temperatures. In Britain and Northern Europe, dark. Statistical analyses were carried out using the SAS temperatures for the greater part of the year are relatively package STATVIEW v. 5.01. low. Calliphora vicina and C. vomitoria are able to develop at The effects of low temperature episodes were explored in these low temperatures and C. vicina is active through the year. two series of experiments on both blowflyspecies. Specific This studyreports on a series of laboratoryexperiments criteria for each series were influenced byprevious experi- that explore the effects of short periods of low temperature mental experience. Development was followed from the egg on the development of two locallycommon blowflyspecies stage through to adult eclosion. with particular reference to ADD/ADH estimation. A recent study(Myskowiak & Doums, 2002), considering the impact of the practice of refrigeration of insect evidential material Series 1 – Low temperature period at different development (using Protophormia terraenovae Robineau-Desvoidy) to stages temporarilyhalt development until passed to a forensic entomologist, is complementaryto this present study. Egg development took place at 20C. Individual cohorts of larvae were then subjected to cold episodes, of 5C for 5 days, at one of the following developmental stages – larval Materials and methods stages one, two or three (feeding) or the pupal stage. Following the cold episode the blowflies were returned to Wild populations of C. vicina and C. vomitoria were raised 20C for the remainder of their development. Controls and maintained in gauze covered cages (22 Â 38 Â 27 cm) at remained at 20C for the entire developmental duration. # 2003 The Royal Entomological Society, Medical and Veterinary Entomology, 17, 178–186 180 C. Ames and B. Turner Series 2 – Differing low temperatures
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