Tropical Biomedicine 34(2): 284–294 (2017)

Survey of indoor sarcosaphagous

Ren, L.P.1, Deng, H.X.1, Dong, S.Z.1, Li, J.B.2, Hu, X.H.2, Cai, J.F.1 and Guo, Y.D.1* 1Department of Forensic Science, School of Basic Medical Sciences, Central South University, Changsha 410013, Hunan, China 2The Changsha Public Security Bureau in Hunan, Changsha 410008, Hunan, China *Corresponding author e-mail: [email protected] Received 5 August 2016; received in revised form 14 February 2017; accepted 16 February 2017

Abstract. Entomological evidence provides valuable information for estimating postmortem interval and location of death in criminal or legal investigations. The colonization of sarcosaphagous insects are commonly discovered in the decomposed corpses in most indoor cases. Therefore, by analyzing the growth patterns and behavioral rhythms of these insects, the application of indoor sarcosaphagous insects in actual cases can be investigated. This study classifies the common of indoor sarcosaphagous insects and analyzes the characteristics of these insects (such as foraging, oviposition, and growth). It further discusses the effect of micro-environment on their behavior. In addition, the research status of the application of indoor sarcosaphagous insects in forensic investigations is summarized.

INTRODUCTION emphasized that PMI based on succession data determined the period of The recovery of entomological fauna from insect activity rather than PMI and did not human cadavers is one of the important cover the time of corpse exposition to the first features of forensic investigations. Through wave of colonizing and ovipositing insects. identifying the insect specimens collected This process can be called pre-colonization from cadavers and determining insect interval (Pre-CI) estimation. species and developmental stages, the Studies on the various influencing factors estimation of postmortem interval (PMI) of the application of sarcosaphagous insects can be conducted in combination with in forensic investigations have focused on the entomological succession of ecological growth status and community succession communities on the cadavers. Forensic pattern of these insects in the indoor micro- entomology possesses a distinct advantage environment (Goff, 1991; Reibe & Madea, in estimating PMI in cases of decomposed 2010a; Anderson, 2011; Nazni et al., 2011; corpses (Wang et al., 2008; Johnson et al., Mahat & Jayaprakash, 2013; Farrell, 2015). 2012; Zhang et al., 2015a). The estimation However, the present systematic investi- of location of death, cause of death, and gations on species, distributions, and other forensic medical issues can also be morphological characteristics of indoor solved on the basis of the regional and sarcosaphagous insects hinder the behavioral characteristics of these insects application in the estimation of PMI. Such (Catts & Haskell, 1990). Amend et al. (2011) insufficiency is explained mainly by that, indicated that the insect community data on species and behavior of sarco- succession was affected by many factors, saphagous insects are still mainly derived which led to inaccurate estimation of the PMI. from the collection and analysis of fragments Therefore, the practicality of this approach of information, rather than from systematic is still restricted. Tomberlin et al. (2011) and dynamic research. Moreover, the present

284 data collection on succession pattern and Until now, C. vicina was also reported to be growth status of indoor sarcosaphagous a typical synantropic species in colder insects depends mainly on wild seasons, particularly in spring and autumn experiments (Reibe & Madea, 2010a; in Europe (Bugelli et al., 2015). Meanwhile, Anderson, 2011). This paper reviews the L. sericata and Chrysomya albiceps were pertinent literatures relating to the collected in almost 50% of the indoor cases application of indoor sarcosaphagous in Italy (Bugelli et al., 2015). In addition, insects in forensic investigations, especially Cynomya cadaverina was also discovered in the estimation of PMI. indoors at early spring (Hall, 1948). Afterwards, Wang et al. (2014) showed the Common species of indoor sarco- existence of adult Chrysomya chain on the saphagous insects fourth day indoor after exposure in China. Reviews on sarcosaphagous insects in Basically, the stable indoor environment indoor micro-environment suggest that is conducive to the activities of insects, but Calliphoridae, Sarcophagidae, , the process of outdoors is and Phortdae of Diptera, and a few species of generally faster than that observed indoors. Coleoptera are the dominant sarcosaphagous Bugelliet et al. (2015) investigated that the insects collected in indoor cases. However, delayed arrival of L. sericata and C. albiceps the distribution of these species markedly in the indoor corpses uncertainty of 1 to 2 varies with regional differences, diversity, days in the estimation of PMI. Additionally, and complexity of the indoor micro- drugs also affected larval development, and environment. The current study summarizes brought about difference between real the common species of indoor sarco- and estimated mean instar (Carvahlo, 2009; saphagous insects identified by the Syamsa et al., 2010). Wang et al. (2012) morphological method. The specific species reported the utilization of C. megacephala are presented in Table 1. for the estimation of PMI in an indoor case in Guangdong. The estimated 5 days was Indoor blow (Diptera: Calli- 2 days longer than the real PMI concluded ) by forensic investigation because larval Blow flies, which are commonly found in development was delayed by the excessive human settlements, can distinctly detect amount of clozapine taken by the decedent. carcasses inside buildings and enter Moreover, Reibe and Madea (2010a) dwellings to oviposit . Study on blow flies in observed that L. sericata presented at human corpses of indoor cases has been places with strong light, while C. vicina was mainly reported in Europe, America, West usually observed in shady environments and and Southeast Asia. (Goff, 1991; Greenberg urban habitats (Schumann, 1971; Goff, 1991; & Kunich, 2002; Pohjoismäki et al., 2010; Battan et al., 2007). Whether L. sericata and Anderson, 2011). Reaserches showed that C. vicina are related to this phenomenon Chrysomya megacephala and Chrysomya remains to be verified. rufifacies were commonly discovered in indoor cases in Malaysia, Thailand and China Indoor flesh flies (Diptera: Sarco- (Sukontason et al., 2005; Syamsa et al., 2010; phagidae) Bunchu et al., 2012; Kumara et al., 2012; Flesh flies have special activity behavior Kavitha et al., 2012; Kumara et al., 2013; indoors or in relatively concealed Wang et al., 2014; Syamsa et al., 2015). While environments (Pohjoismäki et al., 2010; Calliphora vicina was frequently found in Anderson, 2011; Kumara et al., 2012; Guo indoor corpses in Columbia and New Zealand et al., 2014; Bugelli et al., 2015), and are (Smeeton et al., 1984; Anderson, 1995). Later, frequently found to infest corpses in indoor in Germany, C. vicina and Lucilia sericata cases (Byrd & Castner, 2009; Bonacci et al., were the only two species of blow flies found 2011; Syamsa et al., 2012). In indoor corpses, indoors, oviposition occurred with a 24h argyrostoma and Sarcophaga delay after exposure (Reibe et al., 2010a). crassipalpis were considered as the

285 Table 1. Common species of indoor sarcosaphagous insects

Order Subfamily Species

Diptera Calliphoridae Calliphorinae Calliphora Calliphora vomitoria Calliphora vicina Lucilia Lucilia sericata Lucilia cuprina Lucilia illustris Cynomya Cynomya cadaverina Chrysomyinae Chrysomya Chrysomya chain Chrysomya albiceps Chrysomya megacephala Chrysomya chain Protophormia Protophormia terraenovae Phormia Phormia regina Sarcophagidae Parasarcophaga Parasarcophaga crassipalpis Parasarcophaga albiceps Parasarcophaga ruficornis Parasarcophaga similis Parasarcophaga argyrostoma Sarcophaga impatiens Sarcophaga tibialis Sarcophaga caerulescens Bercaea Bercaea cruentata Helicophagella Helicophagella melanura Boettcherisca Boettcherisca peregrina

Muscidae Reinwardtiinae Azeliinae Hydrotaea Hydrotaea spinigera Phortdae – Megaselia scalaris Megaselia spiracularis Megaselia curtineura – Puliciphora Puliciphora borinquenensis Puliciphora obtecta Puliciphora beckeri – Diplonevra Diplonevra peregrina Fanniidae Fanniinae Fannia Fannia canicularis Fannia trimaculata Coleoptera Cleridae – Necrobia Necrobia rufipes Staphylinidae – Creophilus Creophilus maxillosus Histeridae – Saprinus Saprinus splendens Dermstidae – Dermestes Dermestes maculatu Dermestes undulatu Dermestes peruvianus Dermestes lardarius Dermestes haemorrhoidalis Dermestes ater Drmestes tessellatocollis

286 dominant population (Kumara et al., 2012; Syamsa et al. (2015) currently analyzed three Cherix et al., 2012; Bonacci et al., 2014; Baz indoor cases in high-rise buildings and et al., 2015). And in Italy and Switzerland, indicated that a large number of flesh flies Bercaea cruentata was frequently found in colonized the corpses. Unfortunately, the indoor cases (Leccese, 2004; Cherix et al., authors failed to identify the species level 2012). Recently, in Switzerland, Sarcophaga because of insufficient taxonomical studies caerulescens and Parasarcophaga similis concerning the larvae of this taxon. have been reported to be the dominant species In summary, more than 10 common colonizing corpses in indoor cases, S. species of flesh flies exhibit indoor behavior. argyrostoma was commonly found indoors The specific details are attached in Figure 1. during summer (Cherix et al., 2012). Flesh flies are obviously dominant population Interestingly, the involvement of S. in indoor cadavers and have significant argyrostoma in indoor cases has also been potential in forensic application (Guo et reported in Poland (Draber-Monko et al., al., 2016; Fu et al., 2016). However, the 2009). Moreover, S. caerulescens was insufficient taxonomical, growth, and dominant species found in indoor corpses development data of flesh flies poses various in Finland and Spain (Pohjoismäki et al., obstacles to forensic experts in applying 2010; Baz et al., 2015). In comparision, these flies to the estimation of PMI (Battan Parasarcophaga albiceps, Boettcherisca et al., 2007; Zhang et al., 2015b). peregrina, Parasarcophaga ruficornis and Sarcophaga tibialis were discovered in Indoor scuttle flies (Diptera: Phoridae) indoor cases in China, Thailand and Spain PMI is estimated mostly on the basis of the (Chen, 2000; Chen, 2010; Yin et al., 2014; identification of larval instar of blow and flesh Sukontason et al., 2007; Baz et al., 2015). flies. However, the arrival of these flies at the Sarcophaga impatiens and S. crassipalpis corpse may be delayed in relatively sealed were also found to colonize corpses at the indoor (Reibe & Madea, 2010b; Farrell, 2015). earliest stage in Australia (Reibe & Madea, Scuttle flies reach the body earlier than other 2010a; Farrell et al., 2015). insects due to their unique biological At present, we also summarize the behavior and presence in nearly closed decedent’s personal details from the indoor environments (such as sealed plastic bags, cases discovered in Hunan, mainly including indoors, and graves) and low temperature the species of indoor flesh flies. The specific spaces where activities of other flies are details are presented in Table 2. Furthermore, limited. Therefore, scuttle flies are

Table 2. We summarize the decedent’s personal details from the indoor cases in Hunan, mainly involving the species of sarcosaprophagous flies indoors. Sex, age, cause of death, stage of decay are also specified in the table

PMI Age No Gender Manner of death Decomp Species (days) (years)

14 ♀ 25 alcoholism early P. crassipalpis; P. similis 215 ♂ 37 drug overdose advanced P. albiceps 35 ♂ 32 suicide-CO poisoning early B. peregrina 428 ♂ 68 illness advanced B. cruentata 537 ♂ 70 illness advanced H. melanura 614 ♀ 44 homicide moderate B. peregrina 778 ♀ 50 undetermined advanced H. melanura; B. cruentata 817 ♂ 18 sexual Asphyxia advanced B. peregrina 910 ♂ 45 drug overdose moderate P. crassipalpis 10 7 ♀ 37 homicide early P. albiceps; P. similis

287 Figure 1. The species and distribution of indoor flesh flies (Diptera: Sarcophagidae). In the figure, I: Bercaea cruentata, II: Parasarcophaga argyrostoma, III: Sarcophaga caerulescens, IV: Parasarcophaga similis, V: Parasarcophaga crassipalpis, VI: Sarcophaga tibialis, VII: Sarcophaga impatiens, VIII: Parasarcophaga ruficornis, IX: Parasarcophaga albiceps, X: Boettcherisca peregrina, XI: Helicophagella melanura. The name of every country is abbreviated. ESP: Spain, ITA: Italy, CH: Switzerland, PL: Poland, FI: Finland, CHN: China, THA: Thailand, MAS: Malaysia, AU: Australia. It shows that the species and distribution of indoor flesh flies are obviously different in each country. considered to be the first colonizers to reach study sites were 16.0±0.5°C, 88.0±3.0%. Four the corpses in indoor cases occurred at hours later, Diplonevra peregrina (Diptera: ground level or high altitudes (Manlove & phoridae) was commonly found on the legs Disney, 2008; Reibe & Madea, 2010b; Kumara of the carcass. The specific description is et al., 2010; Zuha et al., 2012; Syamsa et al., presented in Figure 2. 2015). However, M. scalaris on humans The species of scuttle flies commonly and has been reported and found in indoor cases mainly included summarized by several authors, and can lead Megaselia scalaris (Kumara et al., 2010; Anderson, 2011; Bugelli et al., 2015). Reibe & Madea (2010b) indicated that blow flies were delayed to reach indoor corpses, while M. scalaris could infest corpses and oviposit within a short time after exposure. In an indoor case of Pisa, M. Scalaris, C. vicina and C. albiceps were mainly collected, using the available data of C. vicina and C. albiceps, PMI of 13–27 days was estimated, while using those of M. scalaris indicated PMI of 21 (18–23) days (Bugelli et al., 2015). Thus, M. scalaris was considered to be accurate in the estimation of PMI in indoor cases. Moreover, Megaselia curtineura, Megaselia spiracularis, Puliciphora borinquenensis, Puliciphora obtecta and Puliciphora beckeri have also been first reported in indoor cases in Malaysia (Kumara Figure 2. The species of scuttle flies (Diptera: et al., 2010; Zuha et al., 2014). Phoridae) commonly discovered in concealed In June 2015, we put a pig carcass in the environment. basement with all windows closed, the means A pig corpse was in a basement with all windows closed, four hours later, Diplonevra peregrina and standard deviations of the ambient (Diptera: phoridae) was commonly found on the temperatures and relative humidities in legs of the carcass.

288 to inaccuracy in PMI estimation (Syamsa et that S. nudiseta has colonized a corpse in al., 2012). Bugelli et al. (2015) reported an a high-rise building in Malaysia. However, Italian indoor case in which Sarcophaga whether the presence of S. nudiseta in a high- larvae and M. scalaris pupae were present rise building was due to the unique behavior in the corpse. The developmental stage of of this species or accidental factors still Sarcophaga larvae indicated a minimum requires further investigation by forensic colonization time of 1–2 days, whereas the entomologists. presence of M. scalaris pupae suggested a Omar et al. (1994) investigated the colonization time of approximately 1 week developmental cycle of S. nudiseta. Their (6–8 days). In fact, the decedent has been experiment confirmed that the first alive for 2 days prior to the discovery of the oviposition of S. nudiseta occurred 4 days body. These data were in agreement with the after exposure in indoor cases. In 2009, estimated PMI based on the developmental Kumara et al. (2009b) reported the growth stage of Sarcophaga larvae, while data the larve of S. nudiseta in the indoor concerning M. scalaris pupae were fluctuating temperatures of Malaysia. The consistent with a myiasis occurring several total developmental time was 13.4 ± 0.8 days (nearly 5 days) before death. Moreover, days. Later, Abu Hassan et al. (2015) studied M. scalaris is also an omnivorous species the immature life cycle of S. nudiseta from because they can consume a wide spectra of the egg stage until adult emergence was food, including decomposing organic matter 14.0 ±1.0 days under fluctuating temperature and artificial media (Disney, 2008). of indoor environments. Recently, Syamsa In indoor cases, sealed environment may et al. (2015) indicated that the time of the result in the delay in insect arrival. However, first oviposition of this species was messy and dirty houses may create a certain inconsistent with that reported by Omar et micro-environment that is conducive to the al. (1994). The reasons for this divergence breeding of sarcosaphagous insects prior to may be that the oviposition process can be the occurrence of death. Therefore, lighting, affected by many biotic (such as inter- temperature, humidity, hygienic condition, specific and intraspecific competition and possible passage of insects, and activity ecological habits) and abiotic factors (such and predation of other insects must be as weather condition, temperature, humidity, comprehensively considered to correctly degree of decay, and accessibility to insects), apply the entomological approach in indoor which may ultimately change the ecology of cases. Notably, the myiasis and medication carrion flies (George et al., 2013; Tomberlin history receive inadequent concern. et al., 2011).

Indoor house flies (Diptera: Muscidae) Indoor Coleoptera insects House flies were the common species to Coleoptera (beetles) usually appears during infest and colonize corpses in indoor cases the middle and later stages of decomposition mainly in Malaysia and Thailand (Schumann, of corpse. Data of the species, quantity, 1971; Nazni et al., 2007; Sukontason et al., occurrence time, and succession pattern of 2007; Syamsa et al., 2012; Syamsa et al., beetles in the corpses are important in the 2015), while Synthesiomyia nudiseta was estimation of PMI for dry human skeletal a rare species in Malaysia found only on remains (Wang et al., 2008). indoor cadavers (Lee et al., 2004; Nazni et As early as 1965, Dermestes lardarius al., 2007; Kavitha et al., 2013b). In 2012, a and Dermestes haemorrhoidalis were decomposing body of an adult female was applied to estimate the PMI as 1–2 years in found on the top floor of a 13-story building the case of a skeletonized body discovered in Kuala Lumpur, Malaysia. The body was in a Copenhagen flat. This case was one of colonized by the larvae of S. nudiseta for the earliest reports on PMI estimation using the first time. The PMI was estimated at beetles. Later, Dermestes maculatus was approximately 5 days to 9 days (Syamsa et the only species found indoors and then al., 2012). Syamsa et al. (2015) also reported the PMI was estimated as no longer than 5

289 months in Germany. (Schroeder et al., 2002). particularities and limitations. For example, Additiontally, in Malaysia, Dermestes ater relatively closed indoor micro-environment was reported to estimate the PMI as 14 days can slow down the decomposition rate of in an indoor case. Meanwhile, the authors cadavers and hinder the spread of putrid emphasized that the unusually rapid arrival odor. These phenomena can contribute to of dermestids was most likely attributed to the delay in the arrival and oviposition of the warm climate indoors (Kumara et al. sarcosaphagous insects. In addition, bodies 2009a). Nazni et al. (2011) also experi- of socially isolated persons are usually mentally confirmed that the order Coleoptera difficult to be discovered indoors. Further- was more diverse with 6 families recovered more, a few sarcosaphagous insects may in indoor condition: Lampyridae, Lycidae, invade into indoor cadavers in advance under Scarabaeidae, Sliphidae, Staphylinidae and the temptation of certain baits (such as putrid Tenebrionidae, unfortunately, they were not food and waste). Moreover, a large number identified as a specific species. Recently, of maggots oviposited by sarcosaphagous Charabidze et al. (2014) analyzed 81 cases insects can accelerate the decomposition involving the invasion of beetles in France rate of cadavers and produce considerable and confirmed Dermestes peruvianus were metabolic heat energy. Such change in mainly distributed in indoor cases. In China, temperature may remarkably change the Chen (2000) experimentally found that D. micro-environment and influence the growth frischii and Drmestes tessellatocollis were rate of maggots on cadavers. dominant beetles in indoor environments in Indoor micro-environments where Guizhou. Furthermore, the time of invasion corpses are usually found at the middle and of carcasses was approximately 40 days later stages of decomposition are complex after exposure. Wang et al. (2014) experi- and have certain particularities (Archer mentally confirmed in Shenzhen that et al., 2005; Long et al., 2015), thus, the beetles distributed in indoor mainly including application of entomological evidence is D. maculatus, Creophilus maxillosus, advantageous in the estimation of PMI in Saprinus splendens, and Necrobia rufipes. indoor cases (Wang et al., 2008; Johnson et Adult of C. maxillosus, S. splendens and al., 2012). However, various factors may D. maculatus mainly appeared in 6-17 days, influence the species and distribution of 7-10 days, and after 13 days, respectively. D. sarcosaphagous insects, such as the position maculatus and N. rufipes were discovered of cadavers in the building, the height of the more frequently indoors than outdoors. building, the direction and seal of the interior As a dominant population during the windows and the lighting, ventilation and middle and later stages of decomposition of temperature of the house. carcasses, sarcosaphagous beetles play a pivotal role in estimating the PMI of dry Expectation human skeletal remains. In addition, posture The rapid development of molecular biology changes of carcasses and the specific damage technology in recent years has facilitated of a part of the carcass are closely related to the application of molecular markers of the decomposition and depend on the unique sarcosaphagous insects as a supplementary necrophagous characteristics of the beetles. measure of morphological identification. However, forensic entomologists still remain Integrating gene expression data with a challenge in speculating the succession traditional morphological data is an pattern of beetles using various factors and important direction in the research on correctly distinguishing antemortem events sarcosaphagous insects. Estimation of the from the influence of beetles after death. time covering the entire maturity of sarcosaphagous insects can significantly Limitations improve the accuracy in the estimation of In criminal cases, the incidence rate of indoor PMI. The following directions can be cases is generally higher than that of considered in future studies: the identification outdoor cases. Indoor cases have their own efficiency of different gene fragments,

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