Tropical Biomedicine 37(4): 1146–1151 (2020)

Short Communication

Preliminary observation on the lepidopteran colonization on rat and rabbit carcasses in Malaysia

Singh, S.1, Yong, S.K.2,3, Jalaludin, N.H.3, Brau, E.3, Shamsudin, N.N.3, Keawbaingam, N.4 and Heo, C.C.1,5* 1Department of Medical Microbiology and Parasitology, Faculty of Medicine, Universiti Teknologi MARA, Sungai Buloh Campus, 47000 Selangor, Malaysia 2Faculty of Applied Sciences, Universiti Teknologi MARA, 40450 Shah Alam, Selangor, Malaysia 3Soil Assessment and Remediation (SAR) Research Group, Faculty of Applied Sciences, Universiti Teknologi MARA, 40450 Shah Alam, Selangor, Malaysia 4Department of Environmental Science, School of Energy and Environment, University of Phayao, Phayao 56000, Thailand 5Institute of Pathology, Laboratory & Forensic Medicine (I-PPerForM), Universiti Teknologi MARA, 47000 Sungai Buloh, Selangor, Malaysia *Corresponding author e-mail: [email protected] Received 20 July 2020; received in revised form 14 September 2020; accepted 14 September 2020

Abstract. The immature stages of necrophagous such as Diptera and Coleoptera play a vital ecological role in carrion decomposition. These invertebrates reduce the necromass significantly through consumption and recycle nutrients into organic forms which are readily being used by autotrophs or served as an abiotic storage in the soil ecosystem. Fly and beetle larvae are frequently encountered decomposers on ephemeral resource patches; however, lepidopterans associated with carrion decomposition is seldom reported. Here, we report colonization of Monopis sp. (Tineidae) and an unknown of Psychidae on a rat carcass, and a Lithosiini caterpillar (Arctiidae) on a rabbit carcass in Peninsular Malaysia for the first time. The feeding behaviour and their potential forensic implications are discussed.

Animal decomposition is an ecological Diptera, beetles, for instance, Dermestidae, process involving breakdown of complex are also involved in the process of molecules into simpler forms and to be re- succession on carrion, albeit they are late absorbed by the producer (Swift et al., 1979; colonizers compared to carrion flies (Kumara Parmenter & MacMahon, 2009). In Malaysia, et al., 2009). Due to its predictive sequence the primary carrion colonizers are usually in insect arrival on carrion, this natural blow flies (family Calliphoridae), especially phenomenon has prompted the use of the genus Chrysomya (Lee et al., 2004; insect succession on carrion in the appli- Silahuddin et al., 2015; Syamsa et al., 2017). cation of forensic entomology (Anderson & The first colonizers will be succeeded by Vanlaerhoven, 1996; Michaud & Moreau, secondary colonizers such as flesh flies 2009; Perez et al., 2014). (Boettcherisca, Parasarcophaga), and Lepidopterans collected from decom- subsequent carrion consumers of the families posing remains have been scarcely recorded. Muscidae, Fanniidae, Piophilidae, and Thus far, no specific literature emphasizes Stratiomyiidae (Nazni et al., 2008; Heo et al., on forensically important lepidopterans 2015; Silahuddin et al., 2015). Other than other than Payne & King (1969) who

1146 documented nine families and 21 species ethanol. In September 2017, another two of collected from pig carrion rat carcasses (R. norvegicus) were placed during summer months (1962, 1963, and on the ground surface which was partially 1966) at Clemson, South Carolina, USA. These shaded by trees. The average temperature lepidopteran families include Papilionidae, of the site ranged from 24°C – 33°C. During Satyridae, , Hesperiidae, the dry/remains stage, two caterpillars were Sphingidae, Noctuidae, Geometridae, collected from one of the rat carcasses. The Pyralidae and Tineidae. These lepidopterans specimens were then brought back to the were attracted to the pig carrion due to laboratory and microscopic observation and several factors, primarily: (1) attracted to identification were conducted under a stereo the odours of carcass decomposition; and microscope (Olympus SZ61, Japan) at the (2) feed on the carrion fluid, dried tissue, Institute for Medical Molecular Biotech- skin and hairs/furs (Payne & King, 1969). nology (IMMB), Faculty of Medicine, Adults of many lepidopteran species Universiti Teknologi MARA (UiTM). Among frequently visit moist ground, perspiration, four caterpillars, two belonged to Psychidae tears, excrements, or carcasses to (cases were made from grass segments) suck water and dissolved nutrients. (Figure 1a) and the other two were identified Arnaldos et al. (2004) presented a as Monopis sp. (Tineidae, Lepidoptera) forensic case in Spain where two live (cases were made from fur) (Figures 1b &1c). caterpillars of Tineidae were collected On another occasion, a forensic soil during the autopsy of a male corpse in the chemistry study was conducted in August skeletal stage. The presence of Tineidae 2019 where a total of three rabbit carcasses was an indicator for a long post-mortem [Oryctolagus cuniculus (L.)] were placed interval (PMI) since the tineids are commonly on the surface of peat soil and sand soil found in exposed and desiccated cadavers. sites in Paya Indah Wetlands, Dengkil, In Malaysia, five species of adult nymphalid Selangor (2.86°N 101.62°E, 266 m above sea were recorded visiting pig level (a.s.l)). The sand site was surrounded carcasses placed in an oil palm plantation by fresh water lakes and the distance from in Selangor (Heo et al., 2010). These adult the carcasses to the lakes was approximately butterflies were attracted to the pig carcasses 5 m from the east and 9 m from the west. at different stages of decomposition, and The sandy site was dominated by tropical there was no immature of Lepidoptera carpet grass [Axonopus compressus found on the carcass remains. Hence, their (Swartz)] and coconut trees [Cocos nucifera roles in forensic investigations remain L.] where as the peat soil site was dominated unclear. by bamboos trees [Fargesia sp.]. We As there is no precedent record of carrion observed an adult dejone (Erichson) colonization by lepidopteran larvae in (Nymphalidae, Lepidoptera) (Figure 2a) and Malaysia, here in we report the colonization a Lithosiini caterpillar (, Eribidae, of rat and rabbit carcasses by Lepidoptera Lepidoptera) (Figure 2b) on the rabbit in Malaysia for the first time. carcasses along the course of decomposition. In August 2017, two rat carcasses visited the bloating carcass [Rattus norvegicus] were placed on the (Day 2) which was placed on the peat soil ground surface within the campus of whereas the Arctiinae caterpillar was found Faculty of Medicine, UiTM (3°13’17.92" N on the dried carcass (Day 10) on the sandy 101°35’38.65" E, 60 m a.s.l.) for a carrion soil (Table 1). decomposition study. The study site was The bagworms (Psychidae, Lepidoptera), covered by grass [Imperata cylindrica (L.) or case moths, are known from all zoogeo- and some Mimosa pudica L.] and was near logical regions except Antarctica and they to a garbage dumping ground (~ 10 m). During include approximately 1,000 species, all of the dry/remains stage of rat carcasses, two which complete its larval development caterpillars were collected from one of the within a self-enclosing bag, and the larvae carcasses using forceps and preserved in 70% are omnivorous scavengers or polyphagous

1147 Figure 1. A. Dorsal view of a psychid case with a larva inside (Psychidae, Lepidotera). B. Monopis sp. (Tineidae, Lepidoptera) cases and larvae associated with a rat carcass at the advanced- decay stage of decomposition. C. Monopis cases (black arrow) and larvae (white arrow) placed on a leaf surface after being removed from the rat carcass.

Figure 2. A. Dorsal view of adult Vindula dejone (Nymphalidae, Lepidoptera) collected from the rabbit carcass placed on peat soil site. B. Dorsal view of Lithosiini caterpillar (Arctiinae, ) collected from the rabbit carcass placed on sand soil site. Both study sites were located in Paya Indah Wetlands, Dengkil, Selangor, Malaysia.

Table 1. Caterpillar infestation and adult attraction of Lepidopteraon animal carcasses in Selangor, Malaysia in 2017 and 2019

Stages of Post- Lepidoptera Stages of Number of Month / Carcass carrion mortem collected specimen specimen Year species decomposition (day) (family) collected identified

August Rat (Rattus Unidentified sp. Dry / remains Larva 2 2017 norvegicus)9 (Psychidae)

September Rat (Rattus Monopis sp. Dry / remains 15 Larva 2 2017 norvegicus) (Tineidae)

August Rabbit Vindula dejone Bloated 2 Adult 1 2019 (Oryctolagus (Nymphalidae) cuniculus) Unidentified sp., Dry / remains 10 Larva 1 Arctiinae (Erebidae)

1148 defoliators with a broad range of hosts On the other hand, family Erebidae (Rhainds et al., 2009; Sobczyk, 2011). In (Arctiinae) are a large and diverse subfamily Malaysia, bagworms are commonly found of moths. The larvae of Lithosiini mostly feed in many orchard, landscape and ornamental on mosses and lichens instead of carcasses trees (Ahmad & Ho, 1980). In this study, the (Wagner, 2009). There are also a few reports cases of Psychidae were found around a of the caterpillars feeding on mushrooms rat carcass (~ 5 cm from the carcass). It is (Moskowitz & Haramaty, 2012). To date, there possible that these bagworms fed on lichens is no report on Arctiidae larvae feeding on and mosses, as well as on small insects and carcasses. In our findings, the presence of organic debris of carrion origin (Rhainds et arctiid larva indicates an advanced decay al., 2009). Thus far, no Psychidae larvae have stage of decomposition (it was collected on been reported from decomposing animal day 10 post-mortem). remains. Their role in carrion ecology and From our recent observations, it is forensic entomology remains unclear and evident that some species of Lepidoptera should be further explored. are attracted towards animal carcasses. Many species of the subfamily Tineinae, Caterpillar colonization on carrion should such as Tinea, Niditinea, and Monopis, be documented more frequently as they have been reported in bird nests, faeces, and might be useful in forensic entomology wool products (Lee et al., 2016; Lee et al., particularly in the determination of minimum 2020). The larvae of these moths are known postmortem interval (mPMI) or serve as to feed on keratin and chitin sources, such locality indicators. We recommend more as feathers, fur, pellets, remains, taxonomical and ecological studies to guano, and wool (Robinson, 1988; Robinson understand the role of caterpillars in carrion & Nielsen, 1993). The genus currently decomposition processes. comprises approximately 100 species, which are widespread and diverse throughout Acknowledgements. The author would like the Old World (Robinson & Nielsen, 1993) to acknowledge James E. Hayden (Division but there are approximately 36 species of Plant Industry, Entomology Section, have been recorded in the Palaearctic and Florida Department of Agriculture and Oriental regions (Xiao & Li, 2006). Recently, Consumer Services), John Heppner and two species of tineid moths, Monopis Jacqueline Miller (McGuire Center for longella (Walker) and Monopis congestella Lepidoptera and Biodiversity, Florida (Walker) have been collected using artificial Museum of Natural History, University of feather traps in South Korea (Lee et al., 2016). Florida) for their help in the identification of There was a case in Italy where the bodies larval specimens in this study. Also, we are of two missing children were infested with grateful to Mohd Sofian Azirun (University of Tineidae in an enclosed underground Malaya), Thary Gazi (University Malaya) and environment (Introna et al., 2011). Tineidae Sofwan Badr (Imperial College London) for usually colonize bodies in the late stages of their help in the identification of the adult decomposition when the body is in dry stage, and the caterpillar from rabbit feeding on natural fibres such as hairs and carcasses. We also thank the Institute for also on clothing that contain human sweat or Medical Molecular Biotechnology (IMMB), putrefactive fluids (Introna et al., 2011). This Faculty of Medicine, Universiti Teknologi family represents a useful biological indicator MARA for the laboratory facility provided. for an extended period of postmortem interval (PMI). In the present observations, Conflict of Interests the larvae of Monopis sp. could be feeding The authors declare that they have no on the rat’s fur during the dry and remains conflict of interests. stage (they were collected on day 15 post- mortem).

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