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1 April 2013 The Community of Hymenoptera Parasitizing Necrophagous Diptera in an Urban Biotope
Christine Frederickx, Jessica Dekeirsschieter, François J. Verheggen, Eric Haubruge
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Most reports published in the field of forensic entomology are focused on Diptera and neglect the Hymenoptera community. However, Hymenoptera are part of the entomofaunal colonization of a dead body. The use of Hymenoptera parasitoids in forensic entomology can be relevant to evaluate the time of death. Hymenoptera parasitoids of the larvae and pupae of flies may play an important role in the estimation of the post-mortem period because their time of attack is often restricted to a small, well-defined window of time in the development of the host insect. However, these parasitoids can interfere with the developmental times of colonizing Diptera, and therefore a better understanding of their ecology is needed. The work reported here monitored the presence of adult Hymenoptera parasitoids on decaying pig carcasses in an urban biotope during the summer season (from May to September). Six families and six species of parasitoids were recorded in the field: Aspilota fuscicornis Haliday (Braconidae), Alysia manducator Panzer, Nasonia vitripennis Walker (Pteromalidae), Tachinaephagus zealandicus Ashmead (Encyrtidae), Trichopria sp. (Diapriidae), and Figites sp. (Figitidae). In the laboratory, five species emerged from pupae collected in the field: Trichopria sp., Figites sp., A. manducator, N. vitripennis, and T. zealandicus. These five species colonize a broad spectrum of Diptera hosts, including those species associated with decomposing carcasses, namely those from the families Calliphoridae, Muscidae, Fanniidae, and Sarcophagidae.


As soon as an animal dies, the carcass becomes a food source for many organisms (Grassberger and Frank 2004; Carter et al. 2007). In temperate natural biotopes, the most specialized organisms inhabiting the “cadaver-ecosystem” are insects (Amendt et al. 2004). Necrophagous insects, mainly Diptera and Coleoptera, are attracted to the cadaver, which is then colonized in a relatively predictable sequence called the entomofaunal succession or insect succession (Megnin 1894; Putman 1983; Schoenly and Reid 1987; Marchenko 1988, 2001; Benecke 2004). Study of these insects in a medico-legal context is a component of forensic entomology (Hall 1990; Amendt et al. 2004). Many forensic entomological studies have been conducted using pig carcasses as surrogate human models due to physiological, ethical, legal, and economic reasons (Rodriguez and Bass 1983; Catts and Goff 1992; Anderson and VanLaerhoven 1996; Hart and Whitaker 2005), but few of the studies conducted on pig carcasses have taken place in Europe (Garcia-Rojo 2004; Grassberger and Frank 2004; Wyss and Cherix 2006; Matuszewski et al. 2008; Dekeirsschieter et al. 2011; Matuszewski et al. 2011).

Many published reports are focused on the Diptera community, but very few look at the parasite community (Davies 1999; Amendt et al. 2000; Campobasso et al. 2001; Grassberger and Frank 2003; Schroeder et al. 2003; Amendt et al. 2004; Wang et al. 2008). Predators and parasites are generally considered to be the second most significant group of carrion-frequenting taxa (Goff 2010, 2011). Among these, a special group of parasites, called parasitoids, attack several necrophagous taxa. A parasitoid larvae or pupae feed exclusively on other arthropods, mainly insects, resulting in the death of the host (Eggleton and Gaston 1990; Amendt et al. 2010). They represent an extremely diverse group, though mainly belonging to Hymenoptera. In Europe, 83 parasitoids species, which attack the larval and pupal stages of synanthropic Diptera, are listed (Fabritius and Klunker 1991). The use of Hymenoptera parasitoids in forensic entomology can be useful to evaluate the time of death (Amendt et al. 2000; Grassberger and Frank 2003; Amendt et al. 2010). The pupal parasitoids of blowflies may play an important role in the estimation of the post-mortem period, because their time of attack is often restricted to a small, welldefined window of time in the development of the host insect (Anderson and Cervenka 2002). This specialized group might also lead to significant problems for forensic entomologists. For example, changes in developmental times for Lucilia sericata L. have been observed after attack by the parasitoid Alysia manducator Panzer, the result being premature pupation (Holdaway and Evans 1930). Families of Hymenoptera parasitoids of forensic importance include Braconidae, Pteromalidae, and Ichneumonidae (Amendt et al. 2000; Disney and Munk 2004; Turchetto and Vanin 2004). Among them, Nasonia vitripennis Walker (Pteromalidae) and Alysia manducator Panzer (Braconidae) are the most common parasitoids found on cadavers (Grassberger and Frank 2003; Grassberger and Frank 2004; Turchetto and Vanin 2004).

So far, little information is available on the Hymenoptera post-mortem community in temperate biogeoclimatic countries (Woodcock et al. 2002; Wyss and Cherix 2006; Lefebvre and Gaudry 2009). This paper identifies the Hymenoptera parasitoid community that was identified on large carcasses in a temperate urban biotope during summer.

Materials and Methods

Field site and study periods

This study was conducted during summer 2010 (4 May – 30 September) in an abandoned garden at an urban site located in Belgium. The garden consisted of hazel trees (Corylus avellana L.), spruce (Picea spp.), and ash trees (Fraxinus excelsior L.). The shrub layer was absent. The soil vegetation was scattered, and the herb layer was mainly constituted of nettles (Urtica dioica L.) and ivies (Hedera helix L.). Regarding the moss layer, there were some sparse areas of Polytrichum sp.

The ambient air temperature and humidity were automatically measured once an hour using a data logger (HOBO RH/Temp 8K©; Onset Computer Corporation, placed on the lateral side of each cage at a height of 75 cm. The daily mean temperature was calculated on the basis of ambient air temperature recorded at time intervals of 24 hr.

Animal model

Each month, two male piglets, Sus domesticus L. (Artiodactyla: Suidae) (5 kg), were killed by penetrative captive bolt (fractured skull) and placed at the experimental sites within two hours. Piglets were provided by the experimental farm of the Veterinary Medicine Faculty of the University of Liege, Belgium (ethical authorization number: FUSAGx-08-07). Immediately after euthanasia, the pig carcasses were packed in double plastic bags to avoid any insect colonization, before being placed at the experimental site.

Figure 1.

Position of yellow traps around each pig carcass. High quality figures are available online.


Each pig carcass was placed 30 m from each other in a plastic box (50 cm × 95 cm × 50 cm) filled with 30 cm of soil from the site in order to facilitate the collection of pupae samples. This box was placed in a metal mesh cage (180 cm × 90 cm × 90 cm) to avoid scavenging by vertebrate carnivores. Dates of exposure of the piglets were 4 May, 2 June; 30 June; 11 August, and 13 September.

Insect collection and identification

In order to quantify insect colonization on pig carcasses, four yellow traps (plastic containers of 9 cm height and 27 cm diameter) filled with soapy water were placed around each carcass. The distribution of the yellow traps on the ground was as follows: one near the head, one near the dorsal face, one near the anus, and one near the ventral face (Figure 1). The insect traps were removed every week and the collected specimens were conserved in 80% norvanol D (ethanol denatured with ether). Only adult stages were included in the counting of collected insects during this study.

Figure 2.

Average monthly ambient temperatures (lines) and average monthly relative humidity (bars). High quality figures are available online.


At the end of each month, pupae present in the soil under the pig carcasses were collected before being transported to the laboratory for rearing. Rearing was conducted under environmentally controlled conditions of 23 ± 1° C with a daylight regime of 16:8 L: D and 70% RH. Pupae were stored together in plastic containers until either an adult fly or parasitoids emerged. Emerged specimens were killed in 80% norvanol D. Pupae from which no adult flies or parasitoids had emerged after eight weeks were dissected for evidence.

Emerged Diptera were identified by their species. However, parasitoid hosts were not identified. Typically, the puparium were very similar in general appearance, being coarctate and light-brown to dark-brown in color, which made identification difficult (Sukontason et al. 2007). Moreover, only one pupal identification key exists. This key identified seven fly species of forensic importance in Thailand, such as Chrysomya spp. (Sukontason et al. 2007). Hymenoptera were identified by family, or to genera when it was possible. Moreover, the subfamilies of Alysiinae, Pteromalinae, Encyrtinae, Figitinae, and Diapriinae were mounted on insect pins and identified by species. Hymenoptera specimens were determining using different identification keys (Fischer 1971, 1972; Nixon 1980; Fergusson 1986; Delvare and Aberlenc 1989; Goulet and Huber 1993).


Environmental parameters

The mean atmospheric temperatures measured during the decompositional process were 11.0° C for May, 16.6 °C for June, 19.9° C for July, 16.2° C for August, and 12.9° C for September (Figure 2). The mean relative humidity was 75.1% for May, 73.2% for June, 71.3% for July, 85.6% for August, and 88.3 % for September (Figure 2).

Hymenoptera specimens collected in the field

The Hymenoptera superfamilies identified on pig carcasses were Ichneumonidea (one family), Chalcidoidea (two families), Cynipoidea (two families), and Proctotrupoidea (one family) (Table 1). Six families were identified: were identified: Braconidae, Pteromalidae, Encyrtidae, Figitidae, Eucoilidae, and Diapriidae. The richness of variety in seasonal families was shown to be three families in May, five families in June, six families in July, and five families both in August and September.

Table 1.

List of Hymenoptera collected in yellow traps.


Six species of Hymenoptera were identified during the sampling period, and subfamilies of Alysiinae included species of Alysia manducator Panzer (803 specimens) and Aspilota fuscicornis Haliday (Braconidae) (six specimens). N. vitripennis (11 specimens), Tachinaephagus zealandicus Ashmead (Encyrtidae) (53 specimens), Trichopria sp. (Diapriidae) (20 specimens), and Figites sp. (Figitidae) (85 specimens) were also identified. Figites sp., Trichopria sp., and A. manducator were collected all through the summer season. T. zealandicus was collected from June to September, however, A. fuscicornis was collected only during July.

Of the total individuals (Table 1), 10.15% were collected in May, 37.27% in June, 13.95% in July, 19.41% in August, and 19.22% in September. A. manducator was the most abundant species overall (78.34%), followed by Figites sp. (8.29%) and T. zealandicus (5.17%). The remaining families consisted of fewer than 30 collected individuals. In May, Figites sp. and N. vitripennis were the most abundant species. During June, the predominant species was Figites sp., followed by N. vitripennis. The most predominant species in July was T. zealandicus, followed by Figites sp. and A. fuscicornis. In August and September, Figites sp. was most abundant, followed by T. zealandicus and Trichopria sp.

Hymenoptera reared from fly pupae

In total, 13,310 Diptera pupae were collected from the soil under carcasses throughout the study (Table 2). Of these, 47.96% were parasitized by Hymenoptera parasitoids, which yielded 6,833 successfully emerged parasitoid specimens. The percentage of parasitism during the summer season was 3.48% in May, 8.99% in June, 8.88% in July, 49.79% in August, and 90.10% in September.

Table 2.

Number of pupae collected, emerged, parasitized, and not emerged in laboratory.


Table 3.

List of Hymenoptera reared from fly pupae.


Table 4.

Diptera species emerged in laboratory.


Five parasitoid species emerged from pupal samples collected in the field (Table 3). The number of A. manducator collected increased dramatically in September. N. vitripennis and Trichopria sp. were collected only in May and July. T. zealandicus and Figites sp. were collected from June to September. A. manducator was the predominant species (84.30%), followed by T. zealandicus (10.16%) and Figites sp. (5.12%). Comparatively, parasitism of fly pupae by N. vitripennis and Trichopria sp. was rare, with both species contributing less than 0.3% of the total parasitism recorded.

Of the Diptera specimens that emerged in the laboratory, two families were identified in association with carcasses: Calliphoridae with five species, and Muscidae with one species (Table 4). All of these species have previously been reported as carrion breeding flies in Europe (Wyss and Cherix 2006; Lefebvre and Gaudry 2009).


The objective of this study was to document Hymenoptera, and more precisely Hymenoptera parasitoids of necrophagous Diptera, in an urban site. At this site, the Hymenoptera community was represented by six families and was found to change over time. The make-up of the Hymenoptera community differed between months. The Hymenoptera diversity was highest in July, followed by June, August, September, and finally May. However, the lowest abundance of Hymenoptera occurred in May, with approximately three times fewer specimens trapped than in June. June had the highest level of caught insects, followed by August, September, and July. Our breeding in the laboratory showed the highest rate of parasitism was observed in September. All previous reports from Europe have been anecdotal, limited to family level or carrion fauna lists (Woodcock et al. 2002; Wyss and Cherix 2006; Lefebvre and Gaudry 2009).

This study identified five species of parasitoids that visited decomposing remains in search of host carrion flies: A. manducator, N. vitripennis, Figites sp., Trichopria sp., and T. zealandicus. These five species colonized a broad spectrum of Diptera hosts associated with decomposing carcasses, including Calliphoridae, Muscidae, Fanniidae, and Sarcophagidae (Laing 1937; Whiting 1967; Rueda and Axtell 1985; Blanchot 1992; Goulet and Huber 1993; Ferreira De Almeida et al. 2002; Voss et al. 2010).

In the field and laboratory, the most abundant parasitoid species, approximately 78% of the species caught and 84% of the species that emerged, was A. manducator. 5,760 pupae were parasitized by A. manducator in the field. These females are attracted to decomposing meat (Laing 1937; Blanchot 1992; Reznik et al. 1992). On the carrion, an A. manducator female walks over the surface, stabbing frequently with her ovipositor until a host larva is encountered (Laing 1937; Reznik et al. 1992). Hosts are discovered by contact, and female parasites prefer larger size larvae (Graham-Smith 1919; Blanchot 1992). A. manducator is an endoparasitoid, and it lays one egg per host (Reznik et al. 1992; Goulet and Huber 1993). This species is present worldwide, but much more prevalent in temperate regions (Goulet and Huber 1993), and has been collected in an urban site in central Europe in May (Grassberger and Frank 2004). In the British Isles, A. manducator is the most common of the parasitic Hymenoptera likely to be seen in carrion (Smith 1986). The seasonal activity of A. manducator reported in the present study is in agreement with previous observations in the Paris region, where it was active from May to October (Blanchot 1992). In the present study, the peak of it is presence in yellow traps was observed during June (337 specimens).

Three subfamilies are recognized in Figitidae: Anacharitinae, Aspiceratinae, and Figitinae (Goulet and Huber 1993). Aspiceratinae and Figitinae are solitary endoparasitoids of Diptera pupae and early stage larvae, respectively, but the parasitoid emerges from the puparium (Fergusson 1986; Goulet and Huber 1993). Payne and Mason (1971) identified two genera of Figitinae, Figites and Neralsia, which were collected from pig carcasses. Exposed larvae were generally parasitized; however, Figites would also enter the carcass in search of prey. Neralsia were only observed parasitizing exposed larvae (Payne and Mason 1971). Six percent of the total caught specimens belonged to the Figitinae subfamily. In the laboratory, 350 pupae were parasitized by one single species of Figites sp. These small parasitoids were attracted to carrion where Lucilia spp. and Sarcophaga spp. larvae were the prevalent species (Payne and Mason 1971). The parasitism of Figites sp. in the field corresponded to the time period when Lucilia spp. was predominant (June to September) (Payne and Mason 1971).

Encyrtidae is one of the most important chalcidoid families for biological control (Goulet and Huber 1993; Voss et al. 2010). Species are gregarious endoparasitoids of eggs, third instar larvae, and postfeeding or prepupae of several forensically important Diptera (Fanniidae, Muscidae, Calliphoridae) (Goulet and Huber 1993; Ferreira De Almeida et al. 2002; Voss et al. 2010). In 2003, the presence of T. zealandicus was detected in northern Italy during September (Turchetto et al. 2003; Turchetto and Vanin 2004). This species, probably native to Australia and New Zealand, has been introduced into various parts of the world in attempts to control pest species of synanthropic Diptera, but no records are available for Europe or the northern regions (Turchetto and Vanin 2010). Following Italy, this is the second recording of T. zealandicus in the Palearctic Region (Turchetto et al. 2003).

The family of Diapriidae includes four subfamilies: Belytinae, Ismarinae, Ambositrinae, and Diapriinae (Goulet and Huber 1993). Only Diapriinae contains parasitoid species of necrophagous Diptera (Goulet and Huber 1993). In the field, Trichopria sp. made-up approximately 2% of the total specimens caught. In the laboratory, one species of Trichopria sp. parasitized only five pupae in July. Moreover, only three specimens were collected in July. These small black insects are endoparasitoids of the immature stages of Diptera (Payne and Mason 1971; Goulet and Huber 1993). In the United Kingdom, three genera of Diapriinae were recorded in the Graham-Smith study on carrion. Aneurhynchus and Psilus were found in insect-open carrion, and Trichopria in buried carrion (Graham-Smith 1919; Payne and Mason 1971). In France, Trichopria inermis Kieffer, a gregarious parasitoid of L. sericata, was been observed (Blanchot 1995).

The last species identified in the laboratory was N. vitripennis, a gregarious ectoparasitoid of the pupae of several fly species of forensic importance, including blowflies, flesh flies, and houseflies (Whiting 1967; Rueda and Axtell 1985; Blanchot 1992). The attraction of females of this species toward the host can be caused, in natura, by decomposing meat (Laing 1937; Blanchot 1992; Frederickx et al. In Press). These wasps are regularly found on carcasses (Blanchot 1995; VanLaerhoven and Anderson 1999; Amendt et al. 2000; Grassberger and Frank 2004; Pohjoismaki et al. 2010) or in bird nests (Whiting 1967; King and Ellison 2005). This species has been recorded worldwide (Braack 1987). N. vitripennis was identified in Belgium in 1920 (Mitroiu 2001; Vago 2006), is a cosmopolitan species (Darling and Werren 1990; Yoder et al. 1994), and has been widely investigated in the subjects of genetic, ecological, evolutionary, and developmental research over the last 50 years (Darling and Werren 1990; Grassberger and Frank 2003; Steiner et al. 2006; Gadau et al. 2008). These wasps are commercially supplied and widely used as biological control agents of blowflies in Australia and in the United States (Mandeville et al. 1990; Morgan et al. 1991; Floate et al. 1999; Grassberger and Frank 2003). Only one pupa was parasitized by female N. vitripennis. N. vitripennis is not considered to be adapted for burrowing, and buried pupae are typically beyond the reach of parasitizing females (Altston 1920; Wylie 1958; Beard 1964; Whiting 1967; Vinson 1976; Voss et al. 2009). In 1950, a higher incidence of parasitism by this species in pupae located on or near the surface of a carcass, rather than on those buried in the soil was reported (Ullyett 1950). In the present study, no Diptera specimens were collected on the ground.

Forensic interest

Forensic entomology is the application of the study of insect biology to criminal matters and is frequently used to estimate the time that has elapsed since death, or the post-mortem interval (Gennard 2007; Ricciuti 2007; Eberhardt and Elliot 2008). Forensic practitioners have previously postulated the use of parasitoids as a tool in criminal investigations, although the presence of parasitoids at crime scenes has largely been ignored due to their small size and the paucity of biological information available (Grassberger and Frank 2003; Amendt et al. 2007; Voss et al. 2009). Females of Hymenoptera parasitoids usually prefer to parasitize particular instars of their hosts (Reznik et al. 1992). In many cases, the most preferable stages are also the most suitable, creating optimal synchronization (Laing 1937; Vinson 1976; Reznik et al. 1992). A. manducator prefer larvae of Calliphora vicina that have already finished their feeding but have not yet left the food substrate (Reznik et al. 1992). N. vitripennis usually lay eggs in their host one day after the pupation, when the skin of the larva has separated from the inner pupal cuticle (Gunn 2006; Gaudry 2010). However, it has been reported that two dayold pupae were parasitized at a significantly lower rate than pupae exposed for four days (Kaufman et al. 2001).

Considering the abundance of A. manducator, T. zealandicus, and Figites sp., the use of these species as a reliable forensic indicator for estimating post-mortem interval is promising. In order to estimate post-mortem interval using these species, the calculated developmental time of the parasitoid simply has to be added to the time of development of the host, therefore providing an extended post-mortem interval timeframe in cases where traditional forensic indicators have completed their development (Grassberger and Frank 2003; Amendt et al. 2010). However, when considering the potential influence, especially of larval parasitoids, it is important to take into account that they can also create significant problems, as seen in the change of developmental times for L. sericata after attack of A. manducator, which results in a premature pupation (Holdaway and Evans 1930). This problem clearly illustrates the need for further research in this field.


Christine Frederickx and Jessica Dekeirsschieter are financially supported by a PhD grant from the Fonds pour la formation à la Recherche dans l'Industrie et l'Agriculture. The voucher Hymenoptera specimens are stored at the entomological conservatory of the Department of Functional and Evolutionary Entomology (Gembloux Agro-Bio Tech, University of Liege, Belgium).



A. Altston 1920. The life-history and habits of two parasites of blowflies. Proceedings of the Zoological Society of London 3: 195–243. Google Scholar


J Amendt , R Krettek , C Mess , R Zehner , H. Bratzke 2000. Forensic entomology in Germany. Forensic Science International 113 : 309–314. Google Scholar


J Amendt , R Krettek , R. Zehner 2004. Forensic entomology. Naturwissenschaften 91: 51–65. Google Scholar


J Amendt , CP Campobasso , E Gaudry , C Reiter , HN LeBlanc , MJR. Hall 2007. Best practice in forensic entomology – standards and guidelines. International Journal of Legal Medicine 121: 90–104. Google Scholar


J Amendt , R Zehner , DG Johnson , J. Wells 2010. Future trends in forensic entomology. In: J Amendt , CP Campobasso , ML Goff , M Grassberger , Editors. Current concepts in Forensic Entomology , pp. 353–368. Springer. Google Scholar


GS Anderson , SL. VanLaerhoven 1996. Initial studies on insect succession on carrion in southwestern British Columbia. Journal of Forensic Sciences 41: 617–625. Google Scholar


GS Anderson , VJ. Cervenka 2002. Insects associated with the body: their use and analyses. In: WD Haglund , MH Sorg , Editors. Advances in forensic taphonomy: method, theory and archaeological perspectives , pp. 173–200. CRC Press. Google Scholar


R. Beard 1964. Parasites of Muscoid Flies. Bulletin of the World Health Organization 31: 491–493. Google Scholar


M. Benecke 2004. Forensic entomology: Arthropods and Corpses. In: M Tsokos , Editor . Forensic Pathology Reviews , pp. 207– 240. Humana Press. Google Scholar


P. Blanchot 1992. Nouveau répertoire bibliographique et nouvelles données biologiques sur les parasites de Musca domestica L. (Dipt. Muscidae). EPHE, Biologie et Evolution des Insectes 5: 1–54. Google Scholar


P. Blanchot 1995. Inventaire des parasitoïdes de mouches synanthropes recensés en France. Biolologie et Evolution des Insectes 7–8: 111–119. Google Scholar


LEO. Braack 1987. Community dynamics of carrion-attendant arthropods in tropical african woodland. Oecologia 72: 402–409. Google Scholar


C Campobasso , G Di Vella , F. Introna 2001. Factors affecting decomposition and Diptera colonization. Forensic Science International 120: 18–27. Google Scholar


DO Carter , D Yellowlees , M. Tibbett 2007. Cadaver decomposition in terrestrial ecosystems. Naturwissenschaften 94: 12–24. Google Scholar


EP Catts , ML. Goff 1992. Forensic Entomolgy in Criminal Investigations. Annual Review of Entomology 37: 253–272. Google Scholar


C Darling , JH. Werren 1990. Biosystematics of Nasonia (Hymenoptera: Pteromalidae): Two New Species Reared from Birds' Nests in North America. Annals of the Entomological Society of America 83: 352– 370. Google Scholar


L. Davies 1999. Seasonal and spatial changes in blowfly production from small and large carcasses at Durham in lowland northeast England. Medical and Veterinary Entomology 13: 245–251. Google Scholar


J Dekeirsschieter , FJ Verheggen , E Haubruge , Y. Brostaux 2011. Carrion beetles visiting pig carcasses during early spring in urban, forest and agricultural biotopes of Western Europe. Journal of Insect Science 11:173. Available online:  Google Scholar


G Delvare , H-P. Aberlenc 1989. Les insectes d'afrique et d'amérique tropicale- Clés pour la reconnaissance des familles. CIRAD Departement GERDAT. Google Scholar


R Disney , T. Munk 2004. Potential use of Braconidae (Hymenoptera) in forensic cases. Medical and Veterinary Entomology 18: 442– 444. Google Scholar


TL Eberhardt , DA. Elliot 2008. A preliminary investigation of insect colonisation and succession on remains in New Zealand. Forensic Science International 176: 217–223. Google Scholar


P Eggleton , KJ. Gaston 1990. Parasitoid species and assemblages – convenient definitions or misleading compromises. Oikos 59: 417–421. Google Scholar


K Fabritius , R. Klunker 1991. Die Larvenund Puparienparasitoide von synanthropen Fliegen in Europa. Angewandte Parasitologic 32: 1–24. Google Scholar


NDM. Fergusson 1986. Charipidae, Ibaliidae & Figitidae: Hymenoptera: Cynipoidea. Royal Entomological Society of London. Google Scholar


MA Ferreira De Almeida , A Pires Do Prado , CJ. Geden 2002. Influence of temperature on development time and longevity of Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), and effects of nutrition and emergence order on longevity. Biological Control 31:375–380. Google Scholar


M. Fischer 1971. Untersuchungen über die europäischen Alysiini mit besonderer Berücksichtigung der Fauna Niederösterreichs (Hymenoptera, Braconidae). Polskie Pismo Entomologiezne 41: 19–160. Google Scholar


M. Fischer 1972. Erste gliederung des paläarktischen Aspilota-Arten (Hymenoptera, -Braconidae, Alysiinae). Polskie Pismo Entomologiezne 42: 323–459. Google Scholar


K Floate , B Khan , G. Gibson 1999. Hymenopterous parasitoids of filth fly (Diptera : Muscidae) pupae in cattle feedlots. Canadian Entomologist 131: 347–362. Google Scholar


C Frederickx , J Dekeirsschieter , FJ Verheggen , E. Haubruge In Press. Host-habitat location by the parasitoid, Nasonia vitripennis Walker (Hymenoptera: Pteromalidae). Journal of Forensic SciencesGoogle Scholar


J Gadau , O Niehuis , A Peire , J Werren , E Baudry , L. beukeboom 2008. The Jewel Wasp-Nasonia. In: W Hunter , CS Kole , Editors. Genome mapping and genomics in animals , pp. 27–41. Springer. Google Scholar


AM. Garcia-Rojo 2004. A study of the insect succession in carcasses in Alcala de Henares (Madrid administrative region, Spain) using pigs as animal models. Boletin de la Sociedad Entomologica Aragonesa 34: 263–269. Google Scholar


E. Gaudry 2010. The Insects Colonisation of Buried Remains. In: J Amendt , CP Campobasso , ML Goff , M Grassberger , Editors. Current Concepts in Forensic Entomology. pp. 273–311. Springer. Google Scholar


DE. Gennard 2007. Forensic Entomology: an Introduction. John Wiley & Sons, Ltd. Google Scholar


ML. Goff 2010. Early Postmortem Changes and Stages of Decomposition. In: J Amendt , ML Goff , CP Campobasso , M Grassberger , Editors. Current Concepts in Forensic Entomology , pp. 1–24. Springer. Google Scholar


ML. Goff 2011. Forensic entomology. In: A Mozayani , C Noziglia , Editors. The Forensic Laboratory Handbook: Procedures and Practice , pp. 447–478. Springer. Google Scholar


H Goulet , JT. Huber 1993. Hymenoptera of the world: an identification guide to families. Agriculture Canada Publication 1894/E. Google Scholar


GS. Graham-Smith 1919. Further observations on the habits and parasites of common flies. Parasitology International 11 : 347–384. Google Scholar


M Grassberger , C. Frank 2003. Temperaturerelated development of the parasitoid wasp Nasonia vitripennis as forensic indicator. Medical and Veterinary Entomology 17: 257– 262. Google Scholar


M Grassberger , C. Frank 2004. Initial study of arthropod succession on pig carrion in a central European urban habitat. Journal of Medical Entomology 41: 511–523. Google Scholar


A. Gunn 2006. Essential Forensic Biology. John Wiley & Sons, Ltd. Google Scholar


RD. Hall 1990. Medicocriminal entomology. In: EP Catts , NH Haskell , Editors. Entomology and Death, a Procedural Guide. pp. 1–8. Forensic Entomology Associates. Google Scholar


AJ Hart , AP. Whitaker 2005. Forensic Entomology. Antennae 30: 159–164. Google Scholar


FG Holdaway , AC. Evans 1930. Parasitism a stimulus to pupation: Alysia manducator in relation to the host Lucilia sericata. Nature 125: 598–599. Google Scholar


PE Kaufman , SJ Long , DA. Rutz 2001. Impact of exposure length and pupal source on Muscidifurax raptorellus and Nasonia vitripennis (Hymenoptera : Pteromalidae) parasitism in a New York poultry facility. Journal of Economic Entomology 94: 998– 1003. Google Scholar


B King , J. Ellison 2005. Resource quality affects restlessness in the parasitoid wasp Nasonia vitripennis. Entomologia Experimentalis et Applicata 118: 71–76. Google Scholar


J. Laing 1937. Host-finding by insect parasites. 1. Observations on the finding of hosts by Alysia manducator, Mormoniella vitripennis and Trichogramma evanescens. Journal of Animal Ecology 6: 298–317. Google Scholar


F Lefebvre , E. Gaudry 2009. Forensic entomology: a new hypothesis for the chronological succession pattern of necrophagous insect on human corpses. Annales de la Societe Entomologique de France 45: 377–392. Google Scholar


JD Mandeville , BA Mullens , DS. Yu 1990. Impact of selected pesticides on field population-dynamics of parasitic Hymenoptera (Pteromalidae) in caged-layer poultry manure in Southern California, USA. Medical and Veterinary Entomology 4: 261– 268. Google Scholar


M. Marchenko 1988. Medico-legal relevance of cadaver entomofauna for the determination of the time of death. Acta Medicinae Legalis et Socialis 38: 257–302. Google Scholar


M. Marchenko 2001. Medicolegal relevance of cadaver entomofauna for the determination of the time of death. Forensic Science International 120: 89–109. Google Scholar


S Matuszewski , D Bajerlein , S Konwerski , K. Szpila 2008. An initial study of insect succession and carrion decomposition in various forest habitats of Central Europe. Forensic Science International 180: 61–69. Google Scholar


S Matuszewski , D Bajerlein , S Konwerski , K. Szpila 2011. Insect succession and carrion decomposition in selected forests of Central Europe. Part 3 : Succession of carrion fauna. Forensic Science International 207: 150–163. Google Scholar


JP. Megnin 1894. La Faune des Cadavres, Application de l'Entomologie à la Médecine Légale. Encyclopédie Science, Aide mémoire. Google Scholar


M. Mitroiu 2001. Révision des collections de Chalcidoidea Pteromaldidae (Hymenoptera) de l'Institut royal des Sciences naturelles de Belgique, et la découverte de 31 espèces nouvelles pour la Belgique. Bulletin & Annales de la Societe Royale Belge d'Entomologie 137: 91–97. Google Scholar


PB Morgan , E Berti , VA. Costa 1991. Lifehistory of Spalangia gemina Boucek (Hymenoptera, Pteromalidae), a fast-breeding microhymenopteran pupal parasitoid of Muscoid flies. Medical and Veterinary Entomology 5: 277–281. Google Scholar


GEJ. Nixon 1980. Diapriidae (Diapriinae): Hymenoptera, Proctotrupoidea. Royal Entomological Society of London. Google Scholar


JA Payne , WRM. Mason 1971. Hymenoptera associated with pig carrion. Proceedings of the Entomological Society of Washington 73 : 132–141. Google Scholar


JLO Pohjoismaki , PJ Karhunen , S Goebeler , P Saukko , IE. Saaksjarvi 2010. Indoors forensic entomology: Colonization of human remains in closed environments by specific species of sarcosaprophagous flies. Forensic Science International 199: 38–42. Google Scholar


RJ. Putman 1983. Carrion and Dung: the Decomposition of Animal Wastes. Hodder. Google Scholar


SY Reznik , DG Chernoguz , KB. Zinovjeva 1992. Host searching, oviposition preferences and optimal synchronization in Alysia manducator (Hymenoptera, Braconidae), a parasitoid of the blowfly, Calliphora vicina. Oikos 65: 81–88. Google Scholar


E. Ricciuti 2007. Science 101: Forensics. HarperCollins. Google Scholar


WC Rodriguez , WM. Bass 1983. Insect activity and its relationship to decay rates of human cadavers in East Tennessee. Journal of Forensic Sciences 28: 423–432. Google Scholar


LM Rueda , RC. Axtell 1985. Comparison of hymenopterous parasites of house fly, Musca domestica (Diptera: Muscidae), pupae in different livestock and poultry production systems. Environmental Entomology 14: 217– 222. Google Scholar


K Schoenly , W. Reid 1987. Dynamics of heterotrophic succession in carrion arthropod assemblages- Discrete seres or a continuum of change. Oecologia 73: 192–202. Google Scholar


H Schroeder , H Klotzbach , K. Püschel 2003. Insects' colonization of human corpses in warm and cold season. Legal Medicine 5: S372–S374. Google Scholar


KGV. Smith 1986. A manual of forensic entomology. British Museum (Natural History). Google Scholar


S Steiner , N Hermann , J. Ruther 2006. Characterization of a female-produced courtship pheromone in the parasitoid Nasonia vitripennis. Journal of Chemical Ecology 32: 1687–1702. Google Scholar


KL Sukontason , R Ngern-Klun , D Sripakdee , K. Sukontason 2007. Identifying fly puparia by clearing technique: application to forensic entomology. Parasitology Research 101: 1407–1416. Google Scholar


M Turchetto , C Villemant , S. Vanin 2003. Two fly parasitoids collected during an entomo-forensic: the widespread Nasonia vitripennis (Hymenoptera Pteromalidae) and the newly recorded Tachinaephagus zealandicus (Hymenoptera Encyrtidae). Bollettino della Societa Entomologica Italiana 135: 109–115. Google Scholar


M Turchetto , S. Vanin 2004. Forensic evaluations on a crime case with monospecific necrophagous fly population infected by two parasitoid species. Aggrawal's Internet Journal of Forensic Medicine and Toxicology 5: 12–18. Google Scholar


M Turchetto , S. Vanin 2010. Climate change and forensic entomology. In: J Amendt , CP Campobasso , ML Goff , M Grassberger , Editors. Current Concepts in Forensic Entomology , pp. 327–351. Springer. Google Scholar


GC. Ullyett 1950. Competition for food and allied phenomena in sheep-blowfly populations. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 234: 77–174. Google Scholar


J-L. Vago 2006. Révision des collections de Chalcidoidea Pteromalidae (Hymenoptera) de l'Institut royal des Sciences naturelles de Belgique et de la Faculté univeristaire des Sciences agronomiques de Gembloux, et la découverte de 145 espèces nouvelles pour la Belgique. Bulletin & Annales de la Societe Royale Belge d'Entomologie 142: 73–99. Google Scholar


SL VanLaerhoven , GS. Anderson 1999. Insect succession on buried carrion in two biogeoclimatic zones of British Columbia. Journal of Forensic Sciences 44: 32–43. Google Scholar


SB. Vinson 1976. Host selection by insect parasitoids. Annual Review of Entomology 21: 109–133. Google Scholar


SC Voss , H Spafford , IR. Dadour 2009. Hymenopteran Parasitoids of Forensic Importance: Host Associations, Seasonality, and Prevalence of Parasitoids of Carrion Flies in Western Australia. Journal of Medical Entomology 46: 1210–1219. Google Scholar


SC Voss , H Spafford , IR. Dadour 2010. Temperature-dependent development of the parasitoid Tachinaephagus zealandicus on five forensically important carrion fly species. Medical and Veterinary Entomology 24: 189–198. Google Scholar


JF Wang , ZG Li , YC Chen , QS Chen , XH. Yin 2008. The succession and development of insects on pig carcasses and their significances in estimating PMI in south China. Forensic Science International 179: 11–18. Google Scholar


AR. Whiting 1967. The biology of the parasitic wasp Mormoniella vitripennis (= Nasonia brevicornis (Walker). The Quarterly Review of Biology 42: 333–406. Google Scholar


BA Woodcock , AD Watt , SR. Leather 2002. Aggregation, habitat quality and coexistence: a case study on carrion fly communities in slug cadavers. Journal of Animal Ecology 71 : 131–140. Google Scholar


HG. Wylie 1958. Factors that affect host finding by Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). The Canadian Entomologist 90: 597–608. Google Scholar


C Wyss , D. Cherix 2006. Traité d'Entomologie Forensique: Les insectes sur la scène de crime. Presses Polytechniques et Universitaires romandes. Google Scholar


J Yoder , D Rivers , D. Denlinger 1994. Water relationships in the ectoparasitoid Nasonia vitripennis during larval diapause. Physiological Entomology 19: 373–378. Google Scholar
Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed.
Christine Frederickx, Jessica Dekeirsschieter, François J. Verheggen, and Eric Haubruge "The Community of Hymenoptera Parasitizing Necrophagous Diptera in an Urban Biotope," Journal of Insect Science 13(32), 1-14, (1 April 2013).
Received: 12 December 2011; Accepted: 1 May 2012; Published: 1 April 2013
Alysia manducator
carrion ecology
forensic entomology
Nasonia vitripennis
Tachinaephagus zealandicus
temperate area
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