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Larval Growth Rates of the Blowfly, Calliphora Vicina, Over a Range of Temperatures

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Larval Growth Rates of the Blowfly, Calliphora Vicina, Over a Range of Temperatures Medical and Veterinary Entomology (2006) 20, 106–114 doi: 10.1111/j.1365-2915.2006.00600.x Larval growth rates of the blowfly, Calliphora vicina, over a range of temperatures S. E. DONOVAN1 ,M.J.R.HALL1 ,B.D.TURNER2 and C . B . MO NC R I E F F 1 1The Natural History Museum, London, 2Department of Life Sciences and Forensic Science Unit, Kings College, University of London, U.K. Abstract. Blowfly larvae (Diptera: Calliphoridae) fulfil an important ecological function in the decomposition of animal remains. They are also used extensively in forensic entomology, predominantly to establish a minimum time since death, or a minimum post-mortem interval, using the larval length as a ‘biological clock’. This study examined the larval growth rate of a forensically important fly species, Calliphora vicina Robineau-Desvoidy (Diptera: Calliphoridae) at tem- peratures of between 4Cand30C, under controlled laboratory conditions. The laboratory flies had been trapped initially in London, U.K. The minimum devel- opmental temperature was estimated to be 1C and 4700 accumulated degree hours (ADH) were required for development from egg hatch to the point of pupariation. Lines fitted to the laboratory larval growth data were found to adequately explain the growth of larvae in the field. The nature of variation in growth rates from geographically isolated populations is discussed. Key words. Calliphora vicina, Calliphoridae, forensic entomology, larval growth, temperature, U.K. Introduction Many species of blowfly are attracted to dead bodies of Forensic entomology involves the interpretation of insect animals and humans (Greenberg & Kunich, 2002). If evidence in legal investigations. It has many applications allowed access to a body, the adults will feed on any secre- (Byrd & Castner, 2001), but the most important and sig- tions, including blood, and gravid females will rapidly lay their eggs on the corpse. In the case of Calliphora vicina nificant is in investigations involving human corpses. Insects recovered from a body, predominantly fly larvae (Robineau-Desvoidy), at temperatures above 15 C the eggs and beetles, can provide information on the conditions hatch after about 24 h, whereupon the larvae begin to feed experienced by the body following death, and sometimes, on the body tissues. Once fully grown, the post-feeding in cases of neglect, prior to death. Most commonly though, larvae usually migrate away from the body to pupariate, fly larvae are used to estimate the minimum time since although some species will pupariate on or in the immediate death, that is the minimum post-mortem interval (PMI). vicinity of the body (Greenberg, 1991). At any of these This can be inferred from the species composition of insects stages the police, or forensic entomologists, can remove found on the body, as the types of insects found on and in a insect specimens, some of which will be killed and the rest body follow a fairly predictable succession, first reported by reared to the adult stage to facilitate species identification. Me´ gnin (1894). However, when the first generation of off- The size of a larva, usually represented by its length, is spring from the first flies to locate the corpse are still on or related to its age as a function of time and temperature, around it, a more precise figure can be obtained by estimat- and so should be able to provide a minimum age for the ing the age of the largest, and therefore oldest, larvae on the oldest (longest) larvae and therefore a minimum PMI. body. Their greatest ages indicate the time when flies first Different species of blowfly grow at different rates, and laid their eggs on the corpse. considerable effort has gone into generating developmental Correspondence: Dr Sarah Donovan, School of Biological Sciences, University of Plymouth, Drakes Circus, Plymouth, Devon PL4 8AA, UK. Tel.: þ 44 (0)1626 325880; fax: þ 44 (0)1626 325616; e-mail: [email protected] 106 # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society Larval growth in Calliphora vicina 107 data for a number of species of forensic importance: Calliphora growth with those of larvae from field populations and also alpina Zett. (Davies & Ratcliffe, 1994); Calliphora vicina to compare the results with published data for this species, (Kamal, 1958; Reiter, 1984; Greenberg, 1991; Davies & to consider the potential importance of geographical varia- Ratcliffe, 1994); Calliphora vomitoria (Linnaeus) (Kamal, tion on development rate. 1958; Greenberg & Tantawi, 1993; Davies & Ratcliffe, 1994); Chrysomya megacephala (Fabricius) (Wells & Kurahashi, 1994); Chrysomya albiceps (Wiedemann) (Grassberger et al., Methods 2003); Chrysomya rufifacies (Macquart) (Greenberg, 1991; Byrd & Butler, 1997); Cochliomyia macellaria (Fabricius) Source of larvae (Greenberg, 1991; Wells & LaMotte, 1995; Byrd & Butler, 1996); Lucilia sericata Meigen (Kamal, 1958; Ash & Colonies of C. vicina were used for the studies. These had Greenberg, 1975; Greenberg, 1991; Wall et al., 1992; Davies been collected initially from two locations in London, & Ratcliffe, 1994; Grassberger & Reiter, 2001); Phormia regina U.K.: the wildlife gardens of the Natural History (Meigen) (Kamal, 1958; Greenberg, 1991; Byrd & Allen, 2001); Museum (NHM), South Kensington and from the roof of Protophormia terraenovae (Robineau-Desvoidy) (Kamal, South Bank University (SBU), near Waterloo Station. 1958; Greenberg, 1991; Greenberg & Tantawi, 1993; Davies Adults were kept at 18Æ 4C and LD 12 : 12 h. Newly & Ratcliffe, 1994; Grassberger & Reiter, 2002b). Similar infor- emerged adults were provided with protein (fresh lamb liver mation has recently been published on two species of fleshfly of exudate) to allow egg maturation. Flies had access to water forensic importance (Diptera: Sarcophagidae) (Byrd & Butler, and granulated sugar cubes at all times. Lamb liver was 1998; Grassberger & Reiter, 2002a). added to the cages about a week after adult emergence, to Development is usually quantified as accumulated degree allow oviposition. After about 12 h the eggs were removed, hours (ADH) or days (ADD) above some minimum tem- rinsed in distilled water and then placed on damp filter perature below which development ceases (Sharpe & paper in Petri dishes. First-stage larvae were used within DeMichele, 1977). However, for C. vicina this minimum is 3 h of hatching (90% within 2 h). not universally agreed and published values range from 6C (Haskell et al., 2000) down to 2C (Vinogradova & Marchenko, 1984; Greenberg, 1991). Davies and Ratcliffe Measurement of growth rates observed eggs of C. vicina to hatch at 3.5C and therefore concluded that the minimum threshold must be below Using a fine, dampened paintbrush, groups of 20 first- 3.5C (Davies & Ratcliffe, 1994). Ames and Turner studied stage larvae were transferred into 20 mL polystyrene cups, development of C. vicina at temperatures down to 1C, but each containing 20 g of roughly chopped lamb liver, which concluded that there was no clear cut minimum develop- was dampened periodically to prevent desiccation. Each ment threshold (Ames & Turner, 2003). cup was covered with a fine, nylon mesh, held in place An alternative approach to estimating the age of larvae is with an elastic band. Six cups were placed in a larger plastic the use of isomegalen diagrams (Reiter, 1984; Grassberger & box (25 Â 15 Â 10 cm deep) with a loose lid. The box Reiter, 2001). From these diagrams it is possible to estimate contained a layer of water to maintain a sufficiently high a larva’s age from its length, assuming that it has developed humidity around the larvae; the average relative humidity throughout at a constant temperature. In reality, tempera- was above 40% in all cases. Groups of eight plastic boxes at tures will have varied, and dealing with fluctuating tempera- a time were placed in total darkness in incubators set at a tures can be problematic because an average temperature has specified constant temperature. to be calculated for the entire period of development. This Incubator temperatures encompassed the range likely to problem can be overcome to some extent by using accumu- be experienced by larvae in the U.K.: 4, 10, 14, 19, 23, 26 and lated degree days or degree hours, despite the potential 30C (each Æ 1.5C). In a pilot study, all larvae reared at uncertainty if meteorological data is of poor quality. 35C had died before pupariation. The boxes were venti- A further problem in the use of knowledge of develop- lated daily, and moved within the incubators to minimize ment rates to estimate larval age is that populations of the the effect of any systematic temperature gradients. A data- same species can differ physiologically depending on their logger [Tinytag Plus, Gemini Data Loggers Ltd (Chichester, geographical origin. For example, populations of C. vicina U.K.)] was placed in each incubator to record temperature from the south of England and those from Finland differ and relative humidity at 10-min intervals. significantly in their diapause response to photoperiod and To validate the laboratory results, field trials were run in temperature. There is strong evidence that the differences August, October and November 2001. For these, individual are genetic (McWatters & Saunders, 1996, 1998). There cups of larvae were prepared as described above. These appears to be considerable variation in the accumulated were placed in a wire cage under shrubs in the grounds of degree hours required for development by geographically the Wildlife Garden at The Natural History Museum. The different populations of forensically important fly species cage provided protection from vertebrate scavengers, and (Higley & Haskell, 2000). The aim of this study, therefore, was also covered with nylon mesh to prevent local wild was to describe larval growth of laboratory populations of blowflies from laying eggs on the liver. As before, a data- C. vicina derived from London, to compare these rates of logger recorded temperature and relative humidity. # 2006 The Authors Journal compilation # 2006 The Royal Entomological Society, Medical and Veterinary Entomology, 20, 106–114 108 S.
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