ABSTRACT
Forensic entomology could provide valuable data for the minimum postmortem interval (PMImin) estimation and other relevant information, such as causes and circumstances of death. Some representatives of flesh flies are one of the dominant necrophagous insects during early stages of decomposition, demonstrating unique biological characteristics compared with other necrophagous flies. Moreover, they lead to global health concerns as carriers of various pathogenic micro-organisms, and dominantly result in the traumatic myiasis. Thus, sarcophagid flies are considered important in decomposition processes for PMImin estimation. However, the utility of sarcophagid flies has been seriously hampered by limited ecological, biological and taxonomic knowledge of them. The aim of this paper is to provide a brief review on the species, distribution and biological habit of forensically important sarcophagid flies. In addition, the relation between traumatic myiasis and flesh flies, molecular identification methods and developmental pattern of flesh flies are summarized.
KEYWORDS: Forensic science, forensic entomology, sarcophagid flies, decomposition, biology, distribution
Introduction
The correct sampling, measuring and subsequent interpretation of the insects found on decomposed remains would provide valuable information in forensic science, such as the minimum postmortem interval (PMImin), the causes and circumstances of the death, toxication and human DNA from the gut of the larvae [1,2]. By determining the developmental stage of necrophagous insects colonized on decomposed remains and the initial colonization timeframes, the PMImin estimation for decomposed corpses is relatively accurate [3]. The common necrophagous insects are Diptera order, mainly including Sarcophagidae, Calliphoridae and Muscidae family, which are critically important in forensic investigations [4–6].
Sarcophagid flies (known as flesh flies) visiting a corpse mostly belong to the synanthropic dement of subtropical or even tropical origin, which constitute a part of the insect faunal succession representing actually the first and very important destruction stage responsible for the essential decomposition [7–9]. Nevertheless, compared with other fly species, sarcophagids have unique characteristics facilitating the estimation of PMImin. First, many flesh flies are well known for adopting the reproductive strategy of ovoviviparity (or ovolarviparity); they deposit maggots directly on a corpse instead of eggs [4,9,10]. Second, they are more observable than others because of the larger size [5,7,11]. Third, sarcophagid flies are more active in various decay stages of corpses [6,8,12]. Moreover, they may play important role in decomposition of buried carrion since they are more efficient colonizers for these types of substrates than blowflies [13,14].
As mentioned above, sarcophagid flies should be widely applied to estimate the PMI, whereas in forensic investigations, it is severely limited by the insufficiency of systematic studies on the taxonomic features and inadequate documentation of their thermobiological histories. Establishment of detailed database on the flesh flies is vitally important. Hence, the aim of this review is to provide a comprehensive review on the species and distribution of sarcophagid species in forensic investigations, especially in indoor cases. Besides, reports of traumatic myiasis caused by sarcophagid species, the effect of drugs on the growth rates of flesh flies, species identification and the developmental pattern of flesh flies are summarized.
Species diversity and distribution of flesh flies
Sarcophagid flies distribute worldwide, and consist of more than 100 genera and 2600 species, among which approximately 800 species belong to the genus Sarcophaga [5,7,8,11,15,16]. Since the dominant species vary significantly with geographic region and climate [10], insect faunal succession on decaying carcasses concerning flesh flies were currently performed, e.g. in Finland, Switzerland, Portugal, Germany, Poland, Spain, Italy, Brazil, United States, India, Australia, Malaysia, Thailand, Japan, Egypt and China.
The geographic region or biogeoclimatic zone has a major impact on the species of insects existed on a corpse. For instance, Sarcophaga africa (Wiedemann), Sarcophaga argyrostoma (Robineau-Desvoidy), Sarcophaga caerulescens Zetterstedt, Sarcophaga dux Thomson, Sarcophaga melanura Meigen and Sarcophaga similis Meade are dominant species in Europe (e.g. Finland, Switzerland, Germany, Spain and Poland) [10,17–20]. The species of Sarcophaga peregrina (Robineau-Desvoidy), Sarcophaga ruficornis (Fabricius) and Sarcophaga taenionota Wiedemann are widely distributed in China and Malaysia [12,21–26]. Sarcophaga albiceps Meigen is extensively found in Asia (e.g. China, India and Malaysia) [9,12,22,26], and Europe (e.g. Germany and Poland) [10,17]. Sarcophaga crassipalpis Macquart is widespread in Spain, Australia and China. Wohlfahrtia nuba (Wiedemann) is frequently recorded in the Middle East (e.g. Egypt and Kuwai) [27,28]. Moreover, a new record of Sarcophaga cultellata Pandelle was identified at preimaginal stages collected in autopsies performed in Spain, which is reported for the first time in human corpses [29]. The detailed summary is shown in Table 1.
Table 1.
The common species and distribution of forensically important flesh flies.
No | Species | Location | Animal model | Habitat | Date of collection | References |
---|---|---|---|---|---|---|
1 |
Boettcherisca highlandica Kurahashi & Tan |
Malaysia (Pahang) | Rabbits | Highland | Unstated | [12] |
2 | Blaesoxipha plinthopyga (Wiedemann) | USA (Idaho) | Human | Mountain | August 2002 | [30] |
3 | Liosarcophaga babiyari (Lehrer) | Saudi Arabia (Al-Baha) | Rabbits | Mountain | Unstated | [31] |
4 | Oxysarcodexia intona (Curran & Walley) | Brazil (Maranhão) | Baited traps | Outdoor | 2009–2012 | [32] |
Brazil (Recife) | Pigs | Rainforest | Unstated | [33] | ||
5 | Oxysarcodexia riograndensis Lopes | Brazil (Pernambuco) | Human | Rural | 2008 | [34] |
Brazil (Recife) | Pigs | Rainforest | Unstated | [33] | ||
6 | Oxysarcodexia thornax (Walker) | Brazil (Maranhão) | Baited traps | Outdoor | 2009–2012 | [32] |
Brazil (São Paulo) | Baited traps | Rural, urban, forest | September 2009–August 2010 | [35] | ||
7 | Peckia chrysostoma* (Wiedemann) | Brazil (Pernambuco) | Male cadaver | Indoor | July 2012 | [36] |
Brazil (Maranhão) | Baited traps | Outdoor | 2009–2012 | [32] | ||
8 | Peckia (Squamatodes) ingens (Walker) | Brazil | Baited traps | Outdoor | 2009–2012 | [32] |
Baited traps | Outdoor | Unstated | [34] | |||
Pig | Rainforest | Unstated | [33] | |||
9 | Peckia (Sarcodexia) lambens (Wiedemann) | Brazil | Baited traps | Outdoor | 2009–2012 | [32] |
Baited traps | Outdoor | Unstated | [34] | |||
Baited traps | Rural, urban, forest | September 2009–August 2010 | [35] | |||
10 | Ravinia belforti (Prado & Fonseca) | Brazil (Pernambuco) | Human corpse | Rural | 2008 | [34] |
11 | Ravinia pernix (Harris) | Saudi Arabia (Riyadh) | Rabbits | Agricultural/desert/urban area | June 2014 | [37] |
12 | Sarcophaga aegyptiaca*Salem | Egypt (El-Qalyubiya) | Rabbit | House | August–September 2008 | [27] |
13 | Sarcophaga albiceps Meigen | China (Zhongshan) | Pigs | Outdoor | December 2003–October 2004 | [22] |
China (Guizhou) | Pigs | Outdoor | April 1998–April 1999 | [26] | ||
India (Punjab) | Mutton | Wooden platform | September 2005 | [9] | ||
Germany (Frankfurt) | Baited traps | Rural | September 2008–May 2011 | [17] | ||
Malaysia (Pahang) | Rabbits | Highland | 2011–2012 | [12] | ||
Poland | Pig | Forest and grassland | Unstated | [10] | ||
India (Punjab) | Rabbits | Campus area | March 1997–December 1999 | [38] | ||
14 | Sarcophaga africa*(Wiedemann) | Switzerland (canton de Vaud) | Human | Indoor | Unstated | [19] |
Spain (Alcala´ de Henares) | Carrion-baited traps | Urban | October 2005–September 2006 | [20] | ||
Poland | Pig | Forest and grassland | Unstated | [10] | ||
Kuwait | Rabbits | Outdoor | 2009 | [28] | ||
15 | Sarcophaga argyrostoma* (Robineau-Desvoidy) | Switzerland (canton de Vaud) | Human | Indoor | Unstated | [19] |
Poland | Pig | Forest and grassland | Unstated | [10] | ||
Spain (Alcala´ de Henares) | Carrion-baited traps | Urban | Unstated | [20] | ||
Central Europe | Woman | Indoor | April 1993 | [14] | ||
16 | Sarcophaga caerulescens* Zetterstedt | Southern Finland (Turku) | Human | Indoor | Unstated | [39] |
Switzerland (canton de Vaud) | Unstated | [19] | ||||
Germany (Frankfurt) | Baited traps | Rural | September 2008–May 2011 | [17] | ||
Poland (Biedrusko) | Pigs | Grassland | 2012–2014 | [18] | ||
Poland | Unstated | [10] | ||||
17 | Sarcophaga carnaria (Linnaeus) | Germany (Frankfurt) | Baited traps | Rural | September 2008–May 2011 | [17] |
18 | Sarcophaga crassipalpis* Macquart | Spain (Alcala´ de Henares) | Carrion-baited traps | Indoor | October 2005–September 2006 | [20] |
Australia (Queensland) | Human | Indoor | December 2011–January 2014 | [24] | ||
China (Shenzhen) | Man, pig and rabbit | Forest | August 2013 | [21] | ||
Japan (Saitama) | Human | Unstated | July–September/Unstated | [40] | ||
Moravia (Brno) | Woman | Indoor | August 1992 | [8] | ||
19 | Sarcophaga cultellata Pandelle | Spain | Human corpse | Unstated | Unstated | [29] |
20 | Sarcophaga dux Thomson | Japan (Saitama) | Human | Unstated | July–September/Unstated | [40] |
Switzerland (canton de Vaud) | Human | Outdoor | Unstated | [19] | ||
northern Thailand (Chiang Mai) | Baited traps | Outdoor | July 2002–February 2003 | [41] | ||
21 | Sarcophaga hirtipes Wiedemann | India (Punjab) | Mutton | Wooden platform | September 2005 | [9] |
India (Punjab) | Rabbits | Campus area | March 1997–December 1999 | [38] | ||
Saudi Arabia (Riyadh) | Rabbits | Agricultural/desert/urban area | June 2014 | [37] | ||
22 | Sarcophaga impatiens*Walker | Australia (Queensland) | Human | Indoor | December 2011–January 2014 | [24] |
23 | Sarcophaga melanura Meigen | Poland | Pig | Forest and grassland | Unstated | [10] |
Spain (Alcala´ de Henares) | Carrion-baited traps | Periurban | October 2005–September 2006 | [20] | ||
24 | Sarcophaga peregrina*(Robineau-Desvoidy) | China | Pigs | Indoor | April 1998–April 1999 | [26] |
Human | River | July 2010 | [23] | |||
Man, pig and rabbit | Forest | August 2013 | [21] | |||
Malaysia (Terengganu) | Rabbits | Rural | 2011–2012 | [12] | ||
Japan (Saitama) | Human | Unstated | July–September/Unstated | [40] | ||
Northern Thailand (Chiang Mai) | Baited traps | Outdoor | July 2002–February 2003 | [41] | ||
25 | Sarcophaga praedatrix Walker | Australia (Queensland) | Human | Grassland | 2011–2012 | [24] |
26 | Sarcophaga princeps Wiedemann | Malaysia | Human, Rabbits | Outdoor | July 2007–July 2010 | [25] |
Unstated | [11] | |||||
India (Punjab) | Rabbits | Campus area | March 1997–December 1999 | [38] | ||
27 | Sarcophaga ruficornis*(Fabricius) | Australia (Queensland) | Human | Indoor | December 2011–January 2014 | [24] |
Malaysia (Penang) | July 2007–July 2010 | [25] | ||||
China (Zhongshan) | Pigs | Outdoor | December 2003–October 2004 | [22] | ||
Kuwait | Rabbits | Outdoor | 2009 | [28] | ||
northern Thailand (Chiang Mai) | Baited traps | Outdoor | July 2002–February 2003 | [41] | ||
28 | Sarcophaga similis*Meade | Switzerland (canton de Vaud) | Human | Indoor | Unstated | [19] |
Poland (Biedrusko) | Pigs | Grassland | Unstated | [34] | ||
Poland | Pigs | Forest and grassland | Unstated | [10] | ||
Germany (Frankfurt) | Baited traps | Urban | September 2008–May 2011 | [17] | ||
29 | Sarcophaga subvicina Baranov | Germany (Frankfurt) | Baited traps | Rural | September 2008–May 2011 | [17] |
30 | Sarcophaga taenionota Wiedemann | China (Zhongshan) | Pigs | Outdoor | December 2003–October 2004 | [22] |
Malaysia (Pahang) | Rabbits | Rural/highland | Unstated | [12] | ||
31 | Sarcophaga tibialis*Macquart | Spain (Alcala´ de Henares) | Carrion-baited traps | Indoor | October 2005–September 2006 | [20] |
32 | Sarcophagavariegata (Scopoli) | Germany (Frankfurt) | Baited traps | Rural | September 2008–May 2011 | [17] |
33 | Sarcophaga spp. | Malaysia | Human | Indoor | 2004 | [42] |
Indoor | July 2007–July 2010 | [25] | ||||
Indoor (high-rise buildings) | 2015 | [43] | ||||
Indoor | January 2010–December 2013 | [44] | ||||
Italy (Tuscany) | Indoor | 2009–2010 | [45] | |||
34 | Tricharaea occidua (Fabricius) | Brazil (Maranhão) | Baited traps | Outdoor | 2009–2012 | [32] |
35 | Wohlfahrtia nuba (Wiedemann) | Kuwait | Rabbits | Outdoor | 2009 | [28] |
*The common species and distribution of flesh flies with indoor activity habits.
The diversity and abundance of biases towards flesh flies may be explained by habitat preferences, as they are strongly synanthropic [10,17]. Fremdt and Amendt [17] demonstrated that Sarcophaga subvicina Baranov, and Sarcophaga variegata (Scopoli) could serve as indicators of urban habitats during summer and S. albiceps as indicator of rural habitats in Frankfurt, Germany. A significant association of S. caerulescens with rural habitats as well as S. similis with urban habitats was observed [17]. Geographical region has obvious influence on arrival time of different species of insects, suggesting that data generated in one region or biogeoclimatic zone cannot be used as a direct reference to estimate the PMI in a different region. It is recommended that databases should be developed for every biogeoclimatic zone in which insects are used to estimate the time of colonization.
Effect of indoor environment on flesh flies
Flesh flies were widely reported to colonize on indoor corpses, which may be due to the special biological features [30,46–48]. In recent years, flesh flies were frequently found to invade corpses in indoor cases, which were mainly reported in Japan, Southern Finland, Switzerland, Spain, Australia, Brazil, United States, Malaysia, Italy, Poland and China. In Switzerland, S. caerulescens, S. similis and S. africa have been reported to be the dominant species colonizing on the corpses in indoor cases, and S. argyrostoma was commonly found indoors during summer [19]. Meanwhile, the involvement of S. argyrostoma in indoor cases has also been reported in Poland [49]. In Italy, S. africa was also recorded in indoor cases [45]. However, it should be treated with caution when estimating the PMImin according to the developmental data of the larvae of S. africa on human corpses, as it is well known that this fly prefers to larviposit of faeces [50]. Moreover, S. caerulescens was dominant species found in indoor corpses in Finland [39]. In conclusion, S. peregrina, S. ruficornis and S. (Liosarcophaga) tibialis Macquart were often reported in China, Spain and Australia, respectively [20,24,26]. Sarcophaga crassipalpis and Sarcophaga impatiens Walker were also found to colonize on the corpses at the earliest stage of decomposition in Australia [24].
Additionally, Syamsa et al. [43] reported the occurrence of flesh flies at higher altitudes. Unfortunately, the authors failed to identify them to the species level because of insufficient taxonomical studies regarding the larvae of this taxon. In summary, more than 10 common species of flesh flies typically colonize on indoor cadavers, including S. africa, S. argyrostoma, S. caerulescens, S. crassipalpis, S. peregrina, S. ruficornis, S. similis, etc. (Table 1). Even so, the insufficient taxonomic and developmental data of flesh flies severely limit their application in the PMI estimation compared with blowflies.
Influence of drugs on flesh flies
Certain cases of drug-related deaths occurred in concealed places, particularly for solitary victims. The cadavers are usually found at the later stages of decomposition. Although it is difficult to estimate the PMI according to the postmortem phenomena, forensic entomology has unique advantages in such cases [51–59], whereas, if the effects of drugs on the developmental pattern of flies are not taken into account, misestimate of PMI might occur. Therefore, knowledge of various drugs on the development of immature carrion-breeding insects could be potentially valuable in redefining the PMI estimation, which involves deducing minimum and maximum PMI [60].
Drugs can affect the developmental pattern of flesh flies, potentially leading to the misestimation of PMI. As early as 1989–1991, Goff et al. [55,56] reported that cocaine and heroin residues and metabolites accelerated the development of the larvae of S. peregrina. Later, Goff et al. [57,61] reported again that higher concentrations of methamphetamine (‘ice’) accelerated the development of S. ruficornis, and lower concentrations of 3, 4-methylenedioxymethamphetamine (MDMA) delayed the larval development of the same species. Whereas, puparial durations of S. ruficornis were significantly longer for the colonizers fed on tissues from the rabbits receiving the high concentrations of amitriptyline and phencyclidine [58,59]. These effects could potentially lengthen the PMI estimation up to 70 h [58]. In South Africa, Musvasva et al. [53] demonstrated that the larvae of S. tibialis exposed to the hydrocortisone and sodium methohexital took significantly longer time to reach pupation compared with those in the control while the larvae exposed to sodium methohexital passed through pupation significantly faster than those in the control. Yet, no systematic relationship was found between drug concentration and developmental time of larvae or pupae. The total developmental period from hatching to eclosion did not differ after drug treatments, implying that estimation of the PMI based on the emergence of adult flies will not be affected by the involvement of these drugs in a case. On the other hand, anomalous pupation spans might indicate the presence of barbiturates. Recently in China, Zhang et al. [62] explored that the larvae of S. crassipalpis grew faster with the increased concentration of morphine hydrochloride. Moreover, Goff et al. [55,56,58] also emphasized the need for studies on the effects of more drugs on the development of various species of necrophagous flies. Thus, further analyses involving different fly species, drug types, concentrations and means of administration should be undertaken to establish a systematic database in support of criminal investigations.
Besides, sarcophagids and their remains could be used for entomological toxicology (entomotoxicology) analyses. Entomotoxicology is the science studies the potential use of insects for detecting drugs or other toxic substances that may not be measurable in decomposing tissues. Necrophagous insects, feeding on the decomposing remains, accumulate toxins present in their food substrates. These insects, in some cases, provide a more reliable and sensitive result than traditional analytical methods dealing with decomposed tissues [52].
Relation between traumatic myiasis and flesh flies
Myiasis is the invasion of tissues and organs both in humans and animals by dint of the larvae of sarcosaprophagous flies. Those larvae feed on the host tissues, body fluids, or ingested food as parasites in the skin, subcutaneous tissues, mouth, stomach, eyes, nose, ears, intestines, urinogenital system, and other soft tissues of humans and warm-blooded vertebrate animals [63]. Relevant cases were mainly reported in Europe and Asia at present. In humans and animals, sarcophagid species have been reported to cause myiasis in ophthalmic, nasal, urinogenital, aural, cutaneous, oral and gastrointestinal cases [64–89]. Accordingly, it is crucial to exclude traumatic myiasis in the PMI estimation based on the development of sarcosaphagous flies [63]. Investigations illustrated that the most common species causing traumatic myiasis is Wohlfahrtia magnifica Schiner, Wohlfahrt's wound myiasis fly, the third of the most important obligatory traumatic myiasis agents [63,90]. Besides, the common sarcophagid species causing myiasis also includes S. africa, S. argyrostoma, S. crassipalpis and S. ruficornis.
Traumatic myiasis caused by sarcophagid species is extensively reported as the consequence of ignorance and can be used as an indicator of wound care neglect, either by oneself or by the nurses [63]. Obviously, criminal investigations require more researches involving various fly species and means of administration to establish a systematic database.
Species identification of flesh flies
Although the species of sarcophagids can be identified by their morphological characteristics of male terminalia, they present as being very numerous and diverse [10,91,92]. Thus, species identification based on morphological methods requires specialized taxonomic knowledge, only a few specialists are able to identify larvae of forensically relevant insects to species level [13,93]. To implement the use of sarcophagids for PMI estimation, a method for easy and accurate species-level identification at any life stage is required. DNA-based method is an alternative method proposed to identify species credibly and rapidly with lower requirement of sample preservation. DNA sequence data would serve as standards for further analysis [94]. Phylogenies also improve the understanding of the taxonomy and systematics of flesh flies [95–99].
At present, the partial genes of mitochondrial genome have been broadly applied to the species-level identification, mainly including the different fragments of Cytochrome c oxidase subunit I (COI) gene [94,95,100–115], in addition to the Cytochrome c oxidase subunit II (COII) gene [108–113], 16S ribosomal RNA (16S rRNA) [108–119], 12S ribosomal RNA (12S rRNA) [119], the nicotinamide adenine dinucleotide (NADH) dehydrogenase subunit 5 [108,109], the ribosomal internal transcribed spacer regions [119,120] and the nuclear period and 28S rRNA genes [111,112] (Table 2). Although these markers could be potentially served as discriminatory tools in identification of forensically important flesh flies, available gene sequences are deficient in the species-level identification of Sarcophagidae on GenBank databases, such as a flaw of insufficient discrimination power in utility of short gene fragments. The use of complete gene remains time-consuming and has a higher requirement for the preservation quality of specimens [104]. Until recently, a set of 4-SNP marker system has been developed for the identification of forensically important sarcophagid flies using the Pyrosequencing (PSQ) method, which showed high discriminating power, specificity of PCR amplification and particular advantages for degraded insect samples [121].
Table 2.
DNA-based identification of forensically important Sarcophagid flies.
No | DNA region | Amplified fragment length (bp) | Primer ID and sequences | Collection location | References |
---|---|---|---|---|---|
1 | COI | 783 | Unstated | USA | [94] |
2 | COI | 278 | C1-J-2495: 5′-CAGCTACTTTATGAGCTTTAGG-3′ C1-N-2800: 5′-CATTTCAAGCTGTGTAAGCATC-3′ |
Australia | [95] |
3 | COI | 304 | 5′-CTGCTACTTTATGAGCTTTAGG-3′ 5′-GATGCTTACACAACTTGAAATG-3′ |
Japan | [108] |
4 | COI | 658 | 5′-GGTCWACWAATCATAAAGATATTGG-3′ 5′-RAAACTTCWGGRTGWCCAAARAATCA-3′ |
Australia | [101] |
[102] | |||||
5 | COI | 304 | 5′-CAGCTACTTTATGAGCTTTAGG-3′ 5′-CATTTCAAGCTGTGTAAGCATC-3′ |
China and Egypt | [103] |
6 | COI | 127/658 | TY-J-1460: TACAATTTATCGCCTAAACTTCAGCC C1-N-2191: CCCGGTAAAATTAAAATATAAACTTC C1-J-2183: CAACATTTATTTTGATTTTTTGG TL2-N-3014: TCCAATGCACTAATCTGCCATATTA 5′-AAAATTATAATAAARGCRTGRGC-3′ 5′-TCYACTAATCATAAAGATATTGGYAC-3′ |
West Europe | [104] |
7 | COI | 272/1 173 | 272- COI: 5′-CAGATCGAAATTTAAATACTTC-3′ 5′-GTATCAACATCTATTCCTAC-3′ 1173- COI: 5′-TACAATTTATCGCCTAAACTTCAGCC-3′ 5′-CAGCTACTTTATGAGCTTTAGG-3′ |
Egypt and China | [105] |
8 | COI | 465 | 5′-CAGCTACTTTATGATCTTTAGG-3′ 5′-CATTTCAAGCTGTGTAAGCATC-3′ |
India | [106] |
9 | COI | 400 | Unstated | Brazil | [107] |
10 | COI + ND5 | 296 + 386 | COI: 5′-CAGCTACTTTATGATCTTTAGG-3′ COI: 5′-CATTTCAAGCTGTGTAAGCATC-3′ ND5: 5′-CCAAAATATTCTGATCATCCTTG-3′ ND5: 5′-GGATTAACTGTTTGTTATACTTTTCG-3′ |
Germany | [108] |
India | [109] | ||||
11 | COI + 16SrDNA | 278 + 289 | C1-J-2495: 5′-CAGCTACTTTATGAGCTTTAGG-3′ C1-N-2800: 5′-CATTTCAAGCTGTGTAAGCATC-3′ 5′-CGCTGTTATCCCTAAGGTAA-3′ 5′-CTGGTATGAAAGGTTTGACG-3′ |
China | [110] |
12 | COI + period | 700 + 678 | COI: 5′-CTTTACCTGTACTTGCTGGAG-3′ COI: 5′-AACTTGTCGTTGTGATGCT-3′ Period: 5′-CGCTGTTATCCCTAAGGTAA-3′ Period: 5′-CTGGTATGAAAGGTTTGACG-3′ |
China | [111] |
13 | COI + 28SrDNA | Unstated | Unstated | Thailand (Chiang Mai) | [112] |
14 | COII | 189 | 5′-ATTAGATGTTGATAATCG-3′ 5′-ACAAATTTC-TGAACATTG-3′ |
China | [116] |
15 | COII | 635 | 5′-AGAGCCTCTCCTTTAATAGAACA-3′ 5′-GAGACCATTACTTGCTTTCAGTCATC-3′ |
Egypt and China | [117] |
16 | COII + 16S rDNA | 637 + 555 | C2-J-3138: 5′-AGAGCCTCTCCTTTAATAGAACA-3′ TK-N-3775: 5′-GAGACCATTACTTGCTTTCAGTCATC-3′ LR-J-12 887: 5′-CCGGTCTGAACTCAGATCACGT-3′ LR-N-13 398: 5′-CGCCTGTTTAACAAAAACAT-3′ |
China | [118] |
17 | COI + COII | 2 300 | TY-J-1460: 5′-TACAATTTATCGCCTAAACTTCAGCC-3′ C1-N-2800: 5′-CATTTCAAGCTGTGTAAGCATC-3′ C1-J-2495: 5′-CAGCTACTTTATGAGCTTTAGG-3′ TK-N-3775: 5′-GAGACCATTACTTGCTTTCAGTCATCT-3′ |
Malaysia | [111] |
China | [114] | ||||
18 | COI + COII | 1 300 | 5′-CAGCTACTTTATGAGCTTTAGG-3′ 5′-GAGACCATTACTTGCTTTCAGTCATCT-3′ |
Egypt and China | [115] |
19 | 12S and 16SrDNA + ITS | 1 172 + 1 500 | mtD-33F: 5′-ATGTTTTTGTTAAACAGGCG-3′ mtD-12SR: 5′-AAACTAGGATTAGATACCCTATTAT-3′ 18SF-1975F: 5′-TAACAAGGTTTCCGTAGGTG-3′ 28SR-52R: 5′-GTTAGTTTCTTTTCCTCCCCT-3′ |
Malaysia | [119] |
20 | ITS2 | Unstated | ITS2_F: 5′-TGCTTGGACTACATATGGTTG A-3′ ITS2_R: 5′-GTAGTCCCATATGAGTTGAGGTT-3′ |
China | [120] |
21 | MtSNP markers | <150 | Unstated | China | [121] |
Due to the recent burst of development in forensic sciences, new court criteria require the evaluation of scientific evidence prior to its submission to the court [122]. Limitation of individual gene for species identification has been illustrated by recent studies [111,123]. Combined use of multiple genes is more valuable for evolutionary analysis and closely related species. To raise the identification efficiency of certain genes, the molecular markers still require further screening and optimization. Meanwhile, it is necessary to explore accurate, rapid and reliable species determination methods that are relatively insensitive to sample preservation so as to improve the application of flesh flies in forensic investigations.
Developmental pattern of flesh flies
Generally, the developmental pattern of flesh flies is in a predictable manner under controlled temperature [93]. To ensure accurate PMImin estimation, it is particularly important to collect precise basic data on the developmental pattern of flesh flies [124]. In 1994, Amoudi et al. [125] explored that the developmental time of S. ruficornis at constant temperatures varying from 13 °C to 37 °C, indicating that the optimal temperature in terms of rapid development, low mortality and greatest weight was from 22 °C to 28 °C. In 1998, Byrd and Butler [126] reported that the developmental durations from first instar to adult for the larva and pupa of S. haemorrhoidalis (Fallen) ranged from 252 h to 802 h under cyclic temperatures with means of 15.6 °C, 21.1 °C, 26.7 °C and 35 °C, and a constant temperature of 25 °C. In 2002, Grassberger and Reiter [127] studied the total developmental time of S. argyrostoma from larviposition to adult emergence was from (54.9 ± 1.45) to (14.9 ± 0.4) days reared at six constant temperature regimes (8 °C–35 °C), respectively. Moreover, the minimum development threshold for total immature development is 7.4 °C. In 2014, Mariana et al. [128] explored the rates of development, viability and survival of immature S. ruficornis and Microcerella halli (Engel) that were reared at different temperatures, demonstrating that the range of optimum temperature for S. ruficornis was between 20 °C and 35 °C, and that for M. halli was between 20 °C and 25 °C. Furthermore, for both species, the longest time of developmental duration was at the lowest temperature, and the survival rate was lower at extreme temperatures (10 °C and 35 °C). In 2017, Wang et al. [129] reported that the developmental durations of S. peregrina at seven constant temperatures (16 °C–34 °C) ranged from (1 064.7 ± 34.8) to (258.0 ± 3.5) h. Moreover, the developmental threshold temperature of S. peregrina was (10.87 ± 0.49) °C, and the thermal summation constant was (5 809.7 ± 291.4) degree days. In the same year, Yang et al. [130] investigated the development patterns of S. similis which was reared at nine constant temperatures ranging from 15 °C to 35 °C (Table 3).
Table 3.
The developmental pattern of forensically important flesh flies
No | Species | Temperature (°C) | First-instar (h) | Second-instar (h) | Third-instar (h) | Pupa (h) | Total duration (h) | References |
---|---|---|---|---|---|---|---|---|
1 | Microcerella halli (Engel) | 10 | 12 ± 2 | 103 ± 12 | 576 ± 12 | Unstated | Unstated | [130] |
15 | 12 ± 2 | 44 ± 2 | 288 ± 12 | 720 ± 24 | 1 074 ± 40 | |||
20 | 12 ± 2 | 31 ± 1 | 216 ± 12 | 528 ± 24 | 787 ± 39 | |||
25 | 10 ± 2 | 22 ± 2 | 156 ± 12 | 336 ± 24 | 524 ± 40 | |||
30 | 8 ±1 | 12 ± 1 | 144 ± 12 | 288 ± 24 | 425 ± 38 | |||
35 | 8 ± 1 | 12 ± 1 | 144 ± 12 | Unstated | Unstated | |||
2 | Sarcophaga argyrostoma (Robineau-Desvoidy) | 8 | 102* | 215* | Unstated | Unstated | Unstated | [129] |
15 | 41* | 43* | 355* | 879* | 1 318* | |||
20 | 24* | 26* | 245* | 456* | 751* | |||
25 | 14* | 16* | 164* | 339* | 533* | |||
30 | 12* | 14* | 125* | 240* | 391* | |||
35 | 12* | 12* | 106* | 228* | 358* | |||
3 | Sarcophaga crassipalpis Macquart | 18 | 28.08* | 42* | 144* | 501.12* | 715.2* | [16] |
21 | 19.92* | 34.08* | 102* | 312* | 468* | |||
24 | 18* | 27.12* | 108* | 270.48* | 423.6* | |||
27 | 17.04* | 18.96* | 83.04* | 216* | 335.04* | |||
30 | 14.4* | 17.04* | 75.6* | 192* | 299.04* | |||
33 | 11.04* | 12.48* | 72* | 168* | 263.52* | |||
4 | Sarcophaga haemorrhoidalis (Fallen) | 15.6 | 14* | 72* | 186* | 540* | 812* | [128] |
21.1 | 12* | 34* | 114* | 344* | 504* | |||
25.0 | 12* | 32* | 112* | 300* | 456* | |||
26.7 | 6* | 18* | 86* | 142* | 252* | |||
32.2 | 6* | 18* | 72* | 264* | 360* | |||
5 | Sarcophaga peregrina (Robineau-Desvoidy) | 16 | 56.0 ± 2.8 | 53.6 ± 2.2 | 170.0 ± 4.4 | 713.3 ± 30.0 | 1 064.7 ± 34.8 | [131] |
19 | 40.5 ± 5.3 | 43.0 ± 2.0 | 121.3 ± 4.7 | 490.0 ± 16.2 | 756.0 ± 19.0 | |||
22 | 29.0 ± 1.0 | 28.6 ± 3.0 | 95.2 ± 1.8 | 366.8 ± 2.7 | 559.6 ± 5.5 | |||
25 | 20.3 ± 0.5 | 19.5 ± 1.0 | 70.0 ± 1.6 | 270.0 ± 5.2 | 414.3 ± 3.9 | |||
28 | 16.8 ± 1.8 | 15.6 ± 0.9 | 59.6 ± 2.2 | 200.6 ± 0.9 | 315.0 ± 2.0 | |||
31 | 14.5 ± 1.7 | 13.6 ± 2.2 | 53.5 ± 2.3 | 177.0 ± 1.7 | 278.0 ± 4.0 | |||
34 | 12.4 ± 0.9 | 12.2 ± 0.4 | 48.4 ± 3.0 | 170.0 ± 3.8 | 258.0 ± 3.5 | |||
6 | Sarcophaga ruficornis (Fabricius) | 10 | 12 ± 2 | 120 ± 12 | 528 ± 12 | Unstated | Unstated | [130] |
15 | 12 ± 2 | 24 ± 2 | 288 ± 12 | 768 ± 24 | 1 092 ± 40 | |||
20 | 12 ± 2 | 24 ± 2 | 156 ± 12 | 504 ± 48 | 696 ± 64 | |||
25 | 10 ± 2 | 12 ± 2 | 110 ± 12 | 288 ± 24 | 420 ± 40 | |||
30 | 4 ± 2 | 8 ± 2 | 108 ± 12 | 240 ± 24 | 360 ± 40 | |||
35 | 4 ± 2 | 8 ± 2 | 108 ± 12 | 240 ± 24 | 360 ± 40 | |||
16 | Unstated | Unstated | Unstated | 748.8 ± 26.6 | 1 166.4 ± 40 | [127] | ||
19 | Unstated | Unstated | Unstated | 499.2 ± 18.2 | 751.2 ± 34.6 | |||
22 | Unstated | Unstated | Unstated | 434.4 ± 21.4 | 664.8 ± 28.6 | |||
25 | Unstated | Unstated | Unstated | 386.4 ± 15.6 | 592.8 ± 26 | |||
28 | Unstated | Unstated | Unstated | 273.6 ± 13.7 | 436.8 ± 15.4 | |||
31 | Unstated | Unstated | Unstated | 232.8 ± 14.2 | 381.6 ± 17.7 | |||
34 | Unstated | Unstated | Unstated | 225.6 ± 11.8 | 362.4 ± 15.8 | |||
7 | Sarcophaga similis Meade | 15 | 52.0 ± 5.8 | 56.8 ± 7.5 | 161.2 ± 15.2 | 759.0 ± 16.8 | 1 029.0 ± 26.6 | [132] |
17.5 | 33.3 ± 5.5 | 30.8 ± 5.6 | 136.0 ± 13.7 | 521.0 ± 12.6 | 731.0 ± 20.4 | |||
20 | 23.0 ± 3.7 | 26.0 ± 5.2 | 111.0 ± 16.1 | 408.5 ± 15.0 | 568.5 ± 20.8 | |||
22.5 | 19.3 ± 2.8 | 20.0 ± 4.8 | 94.0 ± 9.8 | 324.5 ± 9.0 | 457.8 ± 19.8 | |||
25 | 16.3 ± 2.5 | 14.0 ± 3.0 | 78.0 ± 7.0 | 239.3 ± 9.2 | 347.7 ± 14.6 | |||
27.5 | 16.0 ± 1.3 | 14.8 ± 3.5 | 64.0 ± 5.7 | 209.5 ± 7.4 | 304.5 ± 10.4 | |||
30 | 10.0 ± 1.0 | 9.7 ± 1.7 | 60.7 ± 5.0 | 186.7 ± 6.1 | 267.0 ± 9.2 | |||
32.5 | 11.3 ± 1.3 | 10.0 ± 1.4 | 55.0 ± 4.4 | 173.8 ± 6.0 | 250.0 ± 7.3 | |||
35 | 10.3 ± 1.5 | 8.0 ± 1.7 | 53.0 ± 6.2 | 166.0 ± 9.2 | 237.3 ± 7.7 |
*Average stage duration.
In conclusion, the developmental duration of S. ruficornis from Central Arabian Peninsula is longer than that from south-eastern Brazil even at the same temperature [125,128]. At the constant temperature of 25 °C, the developmental duration of S. ruficornis is distinctly longer than that of S. similis [125,130]. Accordingly, the developmental durations of flesh flies should be related to the diversity of geography and climate in addition to the temperature and species. Therefore, further analysis of the developmental pattern of flesh flies at various temperatures in different geographic locations could improve the value of flesh flies in forensic investigations.
Funding Statement
This study is supported by the National Natural Science Foundation of China [grant numbers 81302615 and 81772026]; the National Natural Science Foundation of Hunan Province [grant number 2017JJ3512].
Acknowledgments
We are grateful to two anonymous reviewers for providing invaluable comments and suggestions.
Compliance with Ethical Standards
This article does not contain any studies with human participants or animals performed by any of the authors.
Disclosure statement
No potential conflict of interest was reported by the authors.
References
- [1].Manhoff DT, Hood I, Caputo F, et al. Cocaine in decomposed human remains. J Forensic Sci. 1991;36:1732–1735. [PubMed] [Google Scholar]
- [2].Wells JD, Introna FJ, Di Vella G, et al. Human and insect mitochondrial DNA analysis from maggots. J Forensic Sci. 2001;46:685–687. [PubMed] [Google Scholar]
- [3].Amendt J. Forensic entomology. Forensic Sci Res. 2017.. DOI: 10.1080/20961790.2017.1403081 [DOI] [PMC free article] [PubMed] [Google Scholar]
- [4].Byrd JH, Castner JL. Forensic entomology – the utility of arthropods in legal investigation. 2nd ed Boca Raton: (FL): CRC Press; 2010. [Google Scholar]
- [5].Cai JF. Forensic entomology. Beijing: People's Medical Publishing House; 2015. [Google Scholar]
- [6].Anderson G, VanLaerhoven SL. Initial studies on insect succession on carrion in Southwestern British Columbia. J Forensic Sci. 1996;41:617–625. [PubMed] [Google Scholar]
- [7].Pape T. Catalogue of the Sarcophagidae of the world (Insecta: Diptera). Florida, Gainesville: Associated Publishers. Mem Entomol Inter; 1996;8:1–558. [Google Scholar]
- [8].Povolny D, Verves YG. The flesh-flies of central Europe (Insecta, Diptera, Sarcophagidae). Spixiana Suppl. 1997;24:1–260. [Google Scholar]
- [9].Singh D, Bharti M. Some notes on the nocturnal larviposition by two species of Sarcophaga (Diptera: Sarcophagidae). Forensic Sci Int. 2008;177:19–20. [DOI] [PubMed] [Google Scholar]
- [10].Szpila K, Mądra A, Jarmusz M, et al. Flesh flies (Diptera: Sarcophagidae) colonising large carcasses in central Europe. Parasitol Res. 2015;114:2341–2348. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [11].Tomberlin JK, Benbow ME. Forensic entomology international dimensions and frontiers. Boca Raton (FL): CRC Press; 2015. [Google Scholar]
- [12].Silahuddin SA, Latif B, Kurahashi H, et al. The Importance of habitat in the ecology of decomposition on rabbit carcasses in Malaysia: implications in forensic entomology. J Med Entomol. 2015;52:9–23. [DOI] [PubMed] [Google Scholar]
- [13].Szpila K, Voss JG, Pape T. A new dipteran forensic indicator in buried bodies. Med Vet Entomol. 2010;24:278–283. [DOI] [PubMed] [Google Scholar]
- [14].Pastula EC, Merritt RW. Insect arrival pattern and succession on buried carrion in Michigan. J Med Entomol. 2013;50:432–439. [DOI] [PubMed] [Google Scholar]
- [15].Hu C. Forensic entomology. Chongqing: Chongqing Publishing House; 2000. [Google Scholar]
- [16].Chen LS. The necrophagous flies of China (Insecta, Diptera). Vol. 9, Guizhou, Guiyang: Guizhou Publishing Group; 2013. [Google Scholar]
- [17].Fremdt H, Amendt J. Species composition of forensically important blow flies (Diptera: Calliphoridae) and flesh flies (Diptera: Sarcophagidae) through space and time. Forensic Sci Int. 2014;236:1–9. [DOI] [PubMed] [Google Scholar]
- [18].Matuszewski S, Frątczak K, Konwerski S, et al. Effect of body mass and clothing on carrion entomofauna. Int J Legal Med. 2016;130:221–232. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [19].Cherix D, Wyss C, Pape T. Occurrences of flesh flies (Diptera: Sarcophagidae) on human cadavers in Switzerland, and their importance as forensic indicators. Forensic Sci Int. 2012;220:1–3. [DOI] [PubMed] [Google Scholar]
- [20].Baz A, Botías C, Martínvega D, et al. Preliminary data on carrion insects in urban (indoor and outdoor) and periurban environments in central Spain. Forensic Sci Int. 2014;248:41–47. [DOI] [PubMed] [Google Scholar]
- [21].Wang Y, Ma MY, Jiang XY, et al. Insect succession on remains of human and animals in Shenzhen, China Forensic Sci Int. 2017;271:75–86. [DOI] [PubMed] [Google Scholar]
- [22].Wang J, Li Z, Chen Y, et al. The succession and development of insects on pig carcasses and their significances in estimating PMI in south China. Forensic Sci Int. 2008;179:11–18. [DOI] [PubMed] [Google Scholar]
- [23].Liu Y, Chen Y, Guo Y, et al. Estimation of post-mortem interval for a drowning case by using flies (Diptera) in Central-South China: implications for forensic entomology. Rom J Leg Med. 2013;21:293–298. [Google Scholar]
- [24].Farrell JF, Whittington AE, Zalucki MP. A review of necrophagous insects colonising human and animal cadavers in south-east Queensland, Australia. Forensic Sci Int. 2015;257:149–154. [DOI] [PubMed] [Google Scholar]
- [25].Kumara TK, Disney RH, Abu HA, et al. Occurrence of oriental flies associated with indoor and outdoor human remains in the tropical climate of north Malaysia. J Vector Ecol. 2012;37:62–68. [DOI] [PubMed] [Google Scholar]
- [26].Chen LS. Experimental study on postmortem interval with the invasion of sarcosaphagous insects on cadavers in different environments. Chin J Forensic Med. 2000;15:157–160. [Google Scholar]
- [27].Abd El-bar MM, Sawaby RF. A preliminary investigation of insect colonization and succession on remains of rabbits treated with an organophosphate insecticide in El-Qalyubiya Governorate of Egypt. Forensic Sci Int. 2011;208:26–30. [DOI] [PubMed] [Google Scholar]
- [28].Al-Mesbah H, Moffatt C, El-Azazy OM, et al. The decomposition of rabbit carcasses and associated necrophagous Diptera in Kuwait. Forensic Sci Int. 2012;217:27–31. [DOI] [PubMed] [Google Scholar]
- [29].Velásquez Y, Magaña C, Martínez-Sánchez A, et al. Diptera of forensic importance in the Iberian Peninsula: larval identification key. Med Vet Entomol. 2010;24:293–308. [DOI] [PubMed] [Google Scholar]
- [30].Wells JD, Smith JL. First report of Blaesoxipha plinthopyga (Diptera: Sarcophagidae) from a human corpse in the U.S.A. and a new state geographic record based on specimen genotype. J Forensic Sci. 2013;58:1378–1380. [DOI] [PubMed] [Google Scholar]
- [31].Abouzied EM. Insect colonization and succession on rabbit carcasses in southwestern mountains of the kingdom of Saudi Arabia. J Med Entomol. 2014;51:1168–1174. [DOI] [PubMed] [Google Scholar]
- [32].de Sousa JR Carvalho-Filho Fda S, Esposito MC. Distribution and abundance of necrophagous flies (Diptera: Calliphoridae and Sarcophagidae) in Maranhão Northeastern Brazil J Insect Sci. 2015;15:15. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [33].Vasconcelos SD, Cruz TM, Salgado RL, et al. Dipterans associated with a decomposing animal carcass in a rainforest fragment in Brazil: notes on the early arrival and colonization by necrophagous species. J Insect Sci. 2013;13:145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [34].Oliveira TC, Vasconcelos SD. Insects (Diptera) associated with cadavers at the Institute of Legal Medicine in Pernambuco, Brazil: implications for forensic entomology. Forensic Sci Int. 2010;198:97–102. [DOI] [PubMed] [Google Scholar]
- [35].de Souza CR, Von Zuben CJ. Synanthropy of Sarcophagidae (Diptera) in southeastern Brazil. Neotrop Entomol. 2016;45:637–641. [DOI] [PubMed] [Google Scholar]
- [36].Vasconcelos SD, Soares TF, Costa DL. Multiple colonization of a cadaver by insects in an indoor environment: first record of Fannia trimaculata (Diptera: Fanniidae) and Peckia (Peckia) chrysostoma (Sarcophagidae) as colonizers of a human corpse. Int J Legal Med. 2014;128:229–233. [DOI] [PubMed] [Google Scholar]
- [37].Mashaly AM. Entomofaunal succession patterns on burnt and unburnt rabbit carrion. J Med Entomol. 2016;53:296–303. [DOI] [PubMed] [Google Scholar]
- [38].Bharti M, Singh D. Insect faunal succession on decaying rabbit carcasses in Punjab. India J Forensic Sci. 2003;48:1133–1143. [PubMed] [Google Scholar]
- [39].Pohjoismäki JL, Karhunen PJ, Goebeler S, et al. Indoors forensic entomology: colonization of human remains in closed environments by specific species of sarcosaprophagous flies. Forensic Sci Int. 2010;199:38–42. [DOI] [PubMed] [Google Scholar]
- [40].Toukairin Y, Arai T, Hoshi T, et al. The geographical distribution of fly larvae on corpses in Saitama Prefecture in Japan during the summer season. Leg Med (Tokyo). 2017;24:75–77. [DOI] [PubMed] [Google Scholar]
- [41].Sukontason K, Bunchu N, Chaiwong T, et al. Forensically important flesh fly species in Thailand: morphology and developmental rate. Parasitol Res. 2010;106:1055–1064. [DOI] [PubMed] [Google Scholar]
- [42].Syamsa RA, Ahmad FM, Marwi MA, et al. An analysis of forensic entomological specimens by Universiti Kebangsaan Malaysia. Med J Malaysia. 2010;65:192–195. [PubMed] [Google Scholar]
- [43].Syamsa RA, Omar B, Zuha RM, et al. Forensic entomology of high-rise buildings in Malaysia: three case reports. Trop Biomed. 2015;32:291. [PubMed] [Google Scholar]
- [44].Syamsa RA, Omar B, Ahmad FM, et al. Comparative fly species composition on indoor and outdoor forensic cases in Malaysia. J Forensic Leg Med. 2017;45:41–46. [DOI] [PubMed] [Google Scholar]
- [45].Bugelli V, Forni D, Bassi LA, et al. Forensic entomology and the estimation of the minimum time since death in indoor cases. J Forensic Sci. 2015;60:525–531. [DOI] [PubMed] [Google Scholar]
- [46].Goff ML. Comparison of insect species associated with decomposing remains recovered inside dwellings and outdoors on the island of Oahu, Hawaii. J Forensic Sci. 1991;36:748–753. [PubMed] [Google Scholar]
- [47].Ren LP, Deng HX, Dong SZ, et al. Survey of indoor sarcosaphagous insects. Trop Biomed. 2017;34:284–294. [PubMed] [Google Scholar]
- [48].Frost CL, Braig HR, Amendt J, et al. Indoor arthropods of forensic importance: insects associated with indoor decomposition and mites as indoor markers. In: Amendt J, Goff ML, Campobasso CP, Grassberger M, Current concepts in forensic entomology. Dordrecht: Springer; 2010. p. 93–108. [Google Scholar]
- [49].Draber-Monko A, Malewski T, Pomorski J, et al. On the morphology mitochondrial DNA barcoding of the flesh fly Sarcophaga (Liopygia) argyrostoma (Robineau-Desvoidy, 1830) (Diptera: Sarcophagidae) an important species in forensic entomology. Ann Zool. 2009;59:465–493. [Google Scholar]
- [50].Banzinger H, Pape T. Flowers, faeces and cadavers: natural feeding and laying habits of flesh flies in Thailand (Diptera: Sarcophagidae, Sarcophaga spp.). J Nat Hist. 2004;38:1677–1694. [Google Scholar]
- [51].Beyer JC, Enos WF, Stajic M. Drug identification through analyses of maggots. J Forensic Sci. 1980;25:411–412. [PubMed] [Google Scholar]
- [52].Magni PA, Pacini T, Pazzi M, et al. Development of a GC-MS method for methamphetamine detection in Calliphora vomitoria L. (Diptera: Calliphoridae). Forensic Sci Int. 2014;241:96–101. [DOI] [PubMed] [Google Scholar]
- [53].Musvasva E, Williams KA, Muller WJ, et al. Preliminary observations on the effects of hydrocortisone and sodium methohexital on development of Sarcophaga (Curranea) tibialis Macquart (Diptera: Sarcophagidae), and implications for estimating post mortem interval. Forensic Sci Int. 2001;120:37–41. [DOI] [PubMed] [Google Scholar]
- [54].Wilson Z, Hubbard S, Pounder DJ. Drug analysis in fly larvae Am. J Foren Med Pathol. 1993;14:118–120. [DOI] [PubMed] [Google Scholar]
- [55].Goff ML, Omori AI, Goodbrod JR. Effects of cocaine in tissues on the development rate of Boettcherisca peregrina (Diptera: Sarcophagidae). J Med Entomol. 1989;26:91–93. [DOI] [PubMed] [Google Scholar]
- [56].Goff ML, Brown WA, Hewadikaram KA, et al. Effects of heroin in decomposing tissues on the developmental rate of Boettcherisca peregrina (Diptera, Sarcophagidae) and implications of this effect on estimation of post mortem intervals using arthropod developmental patterns. J Forensic Sci. 1991;36:537–542. [PubMed] [Google Scholar]
- [57].Goff ML, Brown WA, Omori AI. Preliminary observations of the effect of methamphetamine in decomposing tissues on the development rate of Parasarcophagaruficornis (Diptera: Sarcophagidae) and implications of this effect on the estimations of postmortem intervals. J Forensic Sci. 1992;37:867–872. [PubMed] [Google Scholar]
- [58].Goff ML, Brown WA, Omori AI, et al. Preliminary observations of the effects of amitriptyline in decomposing tissues on the development of Parasarcophaga ruficornis (Diptera: Sarcophagidae) and implications of this effect to estimation of post mortem interval. J Forensic Sci. 1993;38:316–322. [PubMed] [Google Scholar]
- [59].Goff ML, Brown WA, Omori AI, et al. Preliminary observations of the effects of phencyclidine in decomposing tissues on the development of Parasarcophaga ruficornis (Diptera: Sarcophagidae). J Forensic Sci. 1994;39:123–128. [PubMed] [Google Scholar]
- [60].Catts EP. Problems in estimating the post mortem interval in death investigations. J Agric Entomol. 1992;9:245–255. [Google Scholar]
- [61].Goff ML, Miller ML, Paulson JD, et al. Effects of 3,4-methylenedioxymethamphetamine in decomposing tissues on the development of Parasarcophaga ruficornis (Diptera: Sarcophagidae) and detection of the drug in post mortem blood, liver tissue, larvae and puparia. J Forensic Sci. 1997;42:276–280. [PubMed] [Google Scholar]
- [62].Zhang N, Niu XL, Liang J, et al. Effect of morphine hydrochloride on grow accumulated degree hour and cephalopharyngeal skeleton of the larvae of Sarcophaga crassipalpis under natural condition. Acad J Second Mil Med Univ. 2015;36:1202–1206. [Google Scholar]
- [63].Hall MJ, Wall RL, Stevens JR. Traumatic myiasis: a neglected disease in a changing world. Annu Rev Entomol. 2016;61:159–176. [DOI] [PubMed] [Google Scholar]
- [64].Pezzi M, Whitmore D, Chicca M, et al. Traumatic myiasis caused by an association of Sarcophaga tibialis (Diptera: Sarcophagidae) and Lucilia sericata (Diptera: Calliphoridae) in a domestic cat in Italy. Korean J Parasitol. 2015;53:471–475. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [65].Severini F, Nocita E, Tosini F. Myiasis of the Tracheostomy wound caused by Sarcophaga (Liopygia) argyrostoma (Diptera: Sarcophagidae): molecular identification based on the mitochondrial cytochrome c oxidase I gene. J Med Entomol. 2015;52:123–130. [DOI] [PubMed] [Google Scholar]
- [66].Graffi S, Peretz A, Wilamowski A, et al. External Ophthalmomyiasis caused by a rare infesting larva, Sarcophaga argyrostoma. Case Rep Ophthalmol Med. 2013;3:850–865. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [67].Burgess I, Spraggs PD. Myiasis due to Parasarcophaga argyrostoma–first recorded case in Britain. Clin Exp Dermatol. 1992;17:261–263. [DOI] [PubMed] [Google Scholar]
- [68].Gaglio G, Brianti E, Abbene S, et al. Genital myiasis by Wohlfahrtia magnifica (Diptera, Sarcophagidae) in Sicily (Italy). Parasitol Res. 2011;109:1471–1471. [DOI] [PubMed] [Google Scholar]
- [69].Rafinejad J, Akbarzadeh K, Rassi Y, et al. Traumatic myiasis agents in Iran with introducing of new dominant species, Wohlfahrtia magnifica (Diptera: Sarcophagidae). Asian Pac J Trop Biomed. 2014;4:451–455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [70].Alizadeh M. A review of myiasis in Iran and a new nosocomial case from Tehran, Iran. 2014;8:124–131. [PMC free article] [PubMed] [Google Scholar]
- [71].Giangaspero A, Traversa D, Trentini R, et al. Traumatic myiasis by wohlfahrtia magnifica in italy. Vet Parasitol. 2011;175:109–112. [DOI] [PubMed] [Google Scholar]
- [72].Derraik JG, Heath AC, Rademaker M. Human myiasis in New Zealand: imported and indigenously-acquired cases: the species of concern and clinical aspects. N Z Med J. 2010;123:21–38. [PubMed] [Google Scholar]
- [73].Farkas R, Hall MJ, Bouzagou AK, et al. Traumatic myiasis in dogs caused by Wohlfahrtia magnifica and its importance in the epidemiology of wohlfahrtiosis of livestock. Med Vet Entomol. 2009;1:80–85. [DOI] [PubMed] [Google Scholar]
- [74].Boscarelli A, Levi Sandri GB. Periungual myiasis caused by Wohlfahrtia magnifica mimicking an ingrown toenail. Transl Pediatrics. 2016;5:95–96. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [75].Tligui H, Bouazzaoui A, Agoumi A. Human auricular myiasis caused by Wohlfahrtia magnifica (Diptera: Sarcophagidae): about three observations in Morocco. Bull Soc Pathol Exot. 2007;100:61–64. [PubMed] [Google Scholar]
- [76].Ferraz AC, Proença B, Gadelha BQ, et al. First record of human myiasis caused by association of the species Chrysomya megacephala (Diptera: Calliplioridae), Sarcophaga (Liopygia) ruficornis (Diptera: Sarcophagidae), and Musca domestica (Diptera: Muscidae). J Med Entomol. 2010;47:487–490. [DOI] [PubMed] [Google Scholar]
- [77].Nazni WA, Jeffery J, Lee HL, et al. Nosocomial nasal myiasis in an intensive care unit. Malays J Pathol. 2011;33:53–56. [PubMed] [Google Scholar]
- [78].Chaiwong T, Temeiam N, Limpavithayakul M, et al. Aural myiasis caused by Parasarcophaga (Liosarcophaga) dux (Thomson) in Thailand. Trop Biomed. 2014;31:496–498. [PubMed] [Google Scholar]
- [79].Maleki RN, Shayeghi M, Najibi B, et al. Infantile nosocomial myiasis in Iran. J Arthropod Borne Dis. 2012;6:156–163. [PMC free article] [PubMed] [Google Scholar]
- [80].Braverman I, Dano I, Saah D, et al. Aural myiasis caused by flesh fly larva, Sarcophaga haemorrhoidalis. Am J Otolaryng. 1994;23:204–205. [PubMed] [Google Scholar]
- [81].Abdel-Hafeez EH, Mohamed RM, Belal US, et al. Human wound myiasis caused by Phormia regina and Sarcophaga haemorrhoidalis in Minia Governorate, Egypt. Parasitol Res. 2015;114:3703–3709. [DOI] [PubMed] [Google Scholar]
- [82].Dutto M, Bertero M. Traumatic myiasis from Sarcophaga (Bercaea) cruentata Meigen, 1826 (Diptera, Sarcophagidae) in a hospital environment: reporting of a clinical case following polytrauma. J Prev Med Hyg. 2010;51:50–52. [PubMed] [Google Scholar]
- [83].Uni S, Shinonaga S, Nishio Y, et al. Ophthalmomyiasis caused by Sarcophaga crassipalpis (Diptera: Sarcophagidae) in a hospital patient. J Med Entomol. 1999;36:906–908. [DOI] [PubMed] [Google Scholar]
- [84].Hiraoka H, Ozawa T, Sowa-Osako J, et al. Repeated myiasis in a female vulvar squamous cell carcinoma caused by Lucilia sericata and Sarcophaga crassipalpis. J Dermatol. 2015;42:840–841. [DOI] [PubMed] [Google Scholar]
- [85].Chigusa Y, Tanaka K, Yokoi H, et al. Two cases of otomyiasis caused by Sarcophaga peregrina and S. similis (Diptera: Sarcophagidae). Med Entomol Zool. 1994;45:153–157. [Google Scholar]
- [86].Türk M, Afşar I, Ozbel Y, et al. A case of nasomyiasis whose agent was Sarcophaga sp. Turkiye Parazitol Derg. 2006;30:330–332. [PubMed] [Google Scholar]
- [87].Aldemir OS, Şimşek E. The first case of otomyiasis caused by Sarcophaga spp. (Diptera; Sarcophagidae) larvae in a goose in the world. Turkiye Parazitol Derg. 2014;38:211–213. [DOI] [PubMed] [Google Scholar]
- [88].Ahmad AK, Abdel-Hafeez EH, Madiha M, et al. Gastrointestinal myiasis by larvae of Sarcophaga sp. and Oestrus sp. in Egypt: report of cases, and endoscopical and morphological studies. Korean J Parasitol. 2011;49:51–57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [89].Dutto M, Bertero M. Cutaneous superficial myiasis: report of a rare nosocomial parasitic disease caused by Sarcophaga spp. (Diptera, Sarcophagidae). Cent Eur J Public Health. 2011;19:232–234. [DOI] [PubMed] [Google Scholar]
- [90].Szpila K, Hall MJ, Wardhana AH, et al. Morphology of the first instar larva of obligatory traumatic myiasis agents (Diptera: Calliphoridae, Sarcophagidae). Parasitol Res. 2014;113:1629–1640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [91].Ubero-Pascal N, Á Paños, García MD, et al. Micromorphology of immature stages of Sarcophaga (Liopygia) cultellata Pandellé, 1896 (Diptera: Sarcophagidae), a forensically important fly. Microsc Res Tech. 2015;78:148–172. [DOI] [PubMed] [Google Scholar]
- [92].Szpila K, Richet R, Pape T. Third instar larvae of flesh flies (Diptera: Sarcophagidae) of forensic importance–critical review of characters and key for European species. Parasitol Res. 2015;114:2279–2289. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [93].Amendt J, Richards CS, Campobasso CP, et al. Forensic entomology: applications and limitations. Forensic Sci Med Pathol. 2011;7:379–392. [DOI] [PubMed] [Google Scholar]
- [94].Wells JD, Pape T, Sperling FA. DNA-based identification and molecular systematics of forensically important Sarcophagidae (Diptera). J Forensic Sci. 2001;46:1098–1102. [PubMed] [Google Scholar]
- [95].Harvey ML, Dadour IR, Gaudieri S. Mitochondrial DNA cytochrome oxidase I gene: potential for distinction between immature stages of some forensically important fly species (Diptera) in western Australia. Forensic Sci Int. 2001;131:134–139. [DOI] [PubMed] [Google Scholar]
- [96].Piwczy´nski M, Szpila K, Grzywacz A, et al. A large-scale molecular phylogeny of flesh flies (Diptera: Sarcophagidae). Syst Entomol. 2014;39:783–799. [Google Scholar]
- [97].Buenaventura E, Whitmore D, Pape T. Molecular phylogeny of the hyperdiverse genus Sarcophaga (Diptera: Sarcophagidae), and comparison between algorithms for identification of rogue taxa. Cladistics. 2016;2:1–25. [DOI] [PubMed] [Google Scholar]
- [98].Piwczyński M, Pape T, Deja-Sikora E, et al. Molecular phylogeny of miltogramminae (Diptera: Sarcophagidae): implications for classification, systematics and evolution of larval feeding strategies. Mol Phylogenet Evol. 2017;116:49–60. [DOI] [PubMed] [Google Scholar]
- [99].Buenaventura E, Pape T. Multilocus and multiregional phylogeny reconstruction of the genus Sarcophaga (Diptera, Sarcophagidae). Mol Phylogenet Evol. 2017;107:619–629. [DOI] [PubMed] [Google Scholar]
- [100].Saigusa K, Takamiya M, Aoki Y. Species identification of the forensically important flies in Iwate prefecture, Japan based on mitochondrial cytochrome oxidase gene subunit I (COI) sequences. Leg Med (Tokyo). 2005;7:175–178. [DOI] [PubMed] [Google Scholar]
- [101].Meiklejohn KA, Wallman JF, Dowton M. DNA-based identification of forensically important Australian Sarcophagidae (Diptera). Int J Legal Med. 2011;125:27–32. [DOI] [PubMed] [Google Scholar]
- [102].Meiklejohn KA, Wallman JF, Dowton M. DNA barcoding identifies all immature life stages of a forensically important flesh fly (Diptera: Sarcophagidae). J Forensic Sci. 2013;58:184–187. [DOI] [PubMed] [Google Scholar]
- [103].Aly SM, Wen J. Applicability of partial characterization of cytochrome oxidase I in identification of forensically important flies (Diptera) from China and Egypt. Parasitol Res. 2013;112:2667–2674. [DOI] [PubMed] [Google Scholar]
- [104].Jordaens K, Sonet G, Richet R, et al. Identification of forensically important Sarcophaga species (Diptera: Sarcophagidae) using the mitochondrial COI gene. Int J Legal Med. 2013;127:491–504. [DOI] [PubMed] [Google Scholar]
- [105].Aly SM. Reliability of long vs short coi markers in identification of forensically important flies. Croat Med J. 2014;55:19–26. [DOI] [PMC free article] [PubMed] [Google Scholar]
- [106].Sharma M, Singh D, Sharma AK. Mitochondrial DNA based identification of forensically important Indian flesh flies (Diptera: Sarcophagidae). Forensic Sci Int. 2015;247:1–6. [DOI] [PubMed] [Google Scholar]
- [107].Napoleão KS, Mello-Patiu CA, Oliveira-Costa J, et al. DNA-based identification of forensically important species of Sarcophagidae (Insecta: Diptera) from Rio de Janeiro, Brazil. Genet Mol Res. 2016;15:1–7. DOI: 10.4238/gmr.15027705 [DOI] [PubMed] [Google Scholar]
- [108].Zehner R, Amendt J, Schütt S, et al. Genetic identification of forensically important flesh flies (Diptera: Sarcophagidae). Int J Legal Med. 2004;118:245–247. [DOI] [PubMed] [Google Scholar]
- [109].Bajpai N, Tewari RR. Mitochondrial DNA sequence-based phylogenetic relationship among flesh flies of the genus Sarcophaga (Sarcophagidae: Diptera). J Genet. 2010;89:51–54. [DOI] [PubMed] [Google Scholar]
- [110].Guo Y, Cai J, Chang Y, et al. Identification of forensically important sarcophagid flies (Diptera: Sarcophagidae) in China, based on COI and 16S rDNA gene sequences. J Forensic Sci. 2011;56:1534–1540. [DOI] [PubMed] [Google Scholar]
- [111].Guo Y, Zha L, Yan W, et al. Identification of forensically important sarcophagid flies (Diptera: Sarcophagidae) in China based on COI and period gene. Int J Legal Med. 2014;128:221–228. [DOI] [PubMed] [Google Scholar]
- [112].Zajac BK, Sontigun N, Wannasan A, et al. Application of DNA barcoding for identifying forensically relevant Diptera from northern Thailand. Parasitol Res. 2016;115:2307–2320. [DOI] [PubMed] [Google Scholar]
- [113].Tan SH, Rizmanidi M, Mohdaris E, et al. DNA-based characterisation and classification of forensically important flesh flies (Diptera: Sarcophagidae) in Malaysia. Forensic Sci Int. 2010;199:43–49. [DOI] [PubMed] [Google Scholar]
- [114].Zhang C, Fu X, Xie K, et al. MtDNA analysis for genetic identification of forensically important Sarcophagid flies (Diptera: Sarcophagidae) in China. J Med Entomol. 2015;52:1225–1233. [DOI] [PubMed] [Google Scholar]
- [115].Aly SM, Wen J, Wang X. Identification of forensically important Sarcophagidae (Diptera) based on partial mitochondrial cytochrome oxidase I and II genes. Am J Forensic Med Pathol. 2013;34:159–163. [DOI] [PubMed] [Google Scholar]
- [116].Guo YD, Cai JF, Li X, et al. Identification of the forensically important sarcophagid flies Boerttcherisca peregrina, Parasarcophaga albiceps and Parasarcophaga dux (Diptera: Sarcophagidae) based on COII gene in China. Trop Biomed. 2010;27:451–460. [PubMed] [Google Scholar]
- [117].Aly SM, Mahmoud SM. COII “long fragment” reliability in characterisation and classification of forensically important flies. Arch Med Sadowej Kryminol. 2016;66:95–105. [DOI] [PubMed] [Google Scholar]
- [118].Guo YD, Cai JF, Xiong F, et al. The utility of mitochondrial DNA fragments for genetic identification of forensically important sarcophagid flies (Diptera: Sarcophagidae) in China. Trop Biomed. 2012;29:51–60. [PubMed] [Google Scholar]
- [119].Roziah A, Tan SH, Lee HL, et al. Mitochondrial and nuclear DNA for identification of forensically important flesh flies (Sarcophagidae: Boettcherisca Spp). Entomol Ornithol Herpetol. 2015;4:163. [Google Scholar]
- [120].Song Z, Wang X, Liang G. Species identification of some common necrophagous flies in Guangdong province, southern China based on the rDNA internal transcribed spacer 2 (ITS2). Forensic Sci Int. 2008;175:17–22. [DOI] [PubMed] [Google Scholar]
- [121].Zhang CQ, Fu XL, Yang X, et al. Application of mtsnp marker for genetic identification of forensically important Sarcophagid flies (Diptera: Sarcophagidae) in China. Forensic Sci Int-Gen Suppl. 2015;5:240–242. [Google Scholar]
- [122].Baqué M, Amendt J. Strengthen forensic entomology in court—the need for data exploration and the validation of a generalized additive mixed model. Int J Legal Med. 2013;127:213–223. [DOI] [PubMed] [Google Scholar]
- [123].Roe AD, Sperling FAH. Patterns of evolution of mitochondrial cytochrome c oxidase I and II DNA and implications for DNA barcoding. Mol Phylogenet Evol. 2007;44:325–345. [DOI] [PubMed] [Google Scholar]
- [124].Brown K, Thorne A, Harvey M. Calliphora vicina (Diptera: Calliphoridae) pupae: a timeline of external morphological development and a new age and PMI estimation tool. Int J Legal Med. 2015;129:835–850. [DOI] [PubMed] [Google Scholar]
- [125].Amoudi MA, Diab FM, Abou-Fannah SS. Development rate and mortality of immature Parasarcophaga (Liopygia) ruficornis (Diptera: Sarcophagidae) at constant laboratory temperatures. J Med Entomol. 1994;31:168–170. [DOI] [PubMed] [Google Scholar]
- [126].Byrd JH, Butler JF. Effects of temperature on Sarcophaga haemorrhoidalis (Diptera: Sarcophagidae) development. J Med Entomol. 1998;35:694–698. [DOI] [PubMed] [Google Scholar]
- [127].Grassberger M, Reiter C. Effect of temperature on development of Liopygia ( = Sarcophaga) argyrostoma (Robineau-Desvoidy) (Diptera: Sarcophagidae) and its forensic implications. J Forensic Sci. 2002;47:1332–1336. [PubMed] [Google Scholar]
- [128].Nassu MP, Thyssen PJ, Linhares AX. Developmental rate of immatures of two fly species of forensic importance: Sarcophaga (Liopygia) ruficornis and Microcerella halli (Diptera: Sarcophagidae). Parasitol Res. 2014;113:217–222. [DOI] [PubMed] [Google Scholar]
- [129].Wang Y, Wang JF, Zhang YN, et al. Forensically important Boettcherisca peregrina (Diptera: Sarcophagidae) in China: development pattern and significance for estimating postmortem interval. J Med Entomol. 2017;54:1491–1497. [DOI] [PubMed] [Google Scholar]
- [130].Yang L, Wang Y, Li L, et al. Temperature-dependent development of Parasarcophaga similis (Meade 1876) and its significance in estimating postmortem interval. J Forensic Sci. 2017;62:1234–1243. [DOI] [PubMed] [Google Scholar]
- [131].Mulieri PR, Mariluis JC, Aballay FH. Two species of Microcerella (Diptera: Sarcophagidae) found in highland arid landscapes of Argentina, during forensic studies. J Med Entomol. 2012;49:183–191. [DOI] [PubMed] [Google Scholar]
- [132].Bonacci T, Silvia G, Berardo C, et al. The flesh fly Sarcophaga (Liopygia) crassipalpis Macquart 1839 as an invader of a corpse in Calabria (southern Italy). J Forensic Sci Criminol. 1987;1:1–5. [Google Scholar]