Determination of Coleoptera fauna on carcasses in Ankara province, Turkey

Article Outline

• Abstract
• 1. Introduction
• 2. Material and methods
• 3. Results and discussion
• 4. Conclusions
• Acknowledgements
• References
• Biography
• Copyright

Abstract 

In this study, 40 species from Staphylinidae, Histeridae, Dermestidae, Silphidae, Nitidulidae and Cleridae families of Coleoptera which were found in 12 pig (Sus scrofa L.) carcasses were identified and recorded during a one-year period at the Hacettepe University Beytepe Campus located in Ankara, Turkey. According to the duration of their presence on the carcasses, 22 of these species were accepted to be important in decomposition. Their distribution over the months and the duration of their presence in the various decomposition stages over the seasons were determined.

Keywords: Forensic entomology, Coleoptera, Carcass, Decomposition, Succession, Turkey

Back to Article Outline

1. Introduction 

Decomposition is a natural and necessary process responsible for the return of organic material to the ecosystem [1]. A corpse, whether human or animal, is a large food source for a great many creatures and supports a large and rapidly changing fauna as it decomposes [2]. Insects are generally the first organisms which come to carcasses and they colonize in a predictable sequence. This sequence is dependent on nutritional changes in the body and variables like geographical region, habitat, season, and climatological and microclimatic conditions, but this sequence is predictable within these parameters [2]. In forensic cases, the longest time passed after death can be predicted by the composition of invertebrate species on a decomposing human body [3]. Decomposition is a continuous process and separating it into certain stages is unreasonable [4] in some respects but can be of practical value. Although the simple sequence of decomposition is predictable, the duration of every stage and species that are present vary by study site and season of the year [5]. The process is divided into five stages: fresh, bloated, active decomposition (decay), advanced decomposition (postdecay) and dry (skeletal).

In decomposition studies, regardless of differences in the study site, there is a certain sequence most of the time. Although the species are different from one site to another, the same general groups are involved [4]. Insect fauna on a carcass is separated into four ecological groups: necrophages, saprophages, predator/parasites and accidental species, which are characterized by interactions of insects with the carcass, food diversity and biology of species [1].

Back to Article Outline

2. Material and methods 

The study was conducted at two different wooded sites of Hacettepe University's Beytepe Campus in Ankara, Turkey (39°52′17″N; 32°44′8″E) between March 2006 and March 2007. Vegetation of both sites was the same and Pinus nigra L. was the dominant species. Pig carcasses were partially in shade depending on the time of the day and, except the first one, which was fully exposed to sun, all were deposited at wooded and shady sites. Furthermore, while the first eight carcasses were deposited at the first site, the other four were deposited at the second site.

In the study, 12 pig carcasses (Sus scrofa L.), each weighing 100–150kg, were used to represent a human body. Depending on decomposition rates and season, pig carcasses were deposited at the study sites at a rate of approximately one carcass per month. In summer, approximately one carcass per 3 weeks, and in winter, one carcass per two months, was deposited. Placement dates of carcasses are given in Table 1. Consequently, three carcasses in spring, four carcasses in summer, two carcasses in autumn and three carcasses in winter were deposited. The essential authorization rights for studying the animals were taken from Hacettepe University Animal Rights Committee. Following this authorization report, pigs were killed with pentobarbital sodium by a veterinary surgeon in charge from Başkent University. To keep away various rodents and dogs, pigs were enclosed in 3cm wire mesh cages made from extended metal measuring 1m×1.5m×1m (W×L×H), with the ground side open.

Table 1. Date of placement of all pig carcasses.

Site studies varied between three times a day in summer and once a week in winter. The studies were conducted at the warmest time of the day when insects are most active. Aside from these times, studies were also done in the early morning and late evening. Clear weather was preferred for the studies but some were done in rain and snowfall. Weather data were taken by a thermo-hygrometer for ambient temperature, 1.5m ambient temperature and humidity, and by probe thermometer for ground temperatures.

Specimens were collected by forceps and hand. For some species, especially staphylinids and histerids, the carcasses were turned over during the visits and beetles were collected. After the procedure was completed, they were returned to their original position. Some of these specimens were kept alive for observing their interactions with other groups on the carcass and then put in 70% ethanol. The remainder were directly killed in ethlyacetate jars. Ethanol-killed insects were preserved in 15cm³ plastic specimen containers and ethylacetate-killed insects were pinned and put in the collection for identification and observation.

Species identifications were made by Jiří Háva from the Private Entomological Laboratory & Collection, Czech Republic for Dermestidae and Silphidae, Volker Assing from Germany for Staphylinidae, Fabio Penati from Italy for Histeridae and Alexander Kirejtshuk from the Zoological Institute of the Russian Academy of Sciences for Nitidulidae families. Identification of Cleridae species was undertaken using Kim and Jung's [6] identification key.

Back to Article Outline

3. Results and discussion 

Decomposition in this study was examined in five stages: fresh, bloated, active decomposition, advanced decomposition and dry, as in the classification of Carvalho et al. [7] and observed by means of morphological changes.

The fresh stage lasted for 1 day at most except in the winter carcasses and, in contrast, bloating was observed on some summer carcasses after just a few hours (Fig. 2). In the fresh stage, there were no changes in morphology and general appearance. The bloated stage was first observed when the carcasses began to swell. Due to the activity of anaerobic bacteria, swelling continued through this stage and color changes were observed during the progress. This stage lasted between 2.5 days in summer and 10.5 days in autumn on average. For the ninth carcass, which was placed in November, this stage lasted for 85 days (Fig. 2) because of the evident cooling of the season (Fig. 1). Active decomposition stage started with the deflation of the body caused by perforation due to the feeding of fly larvae from outside and the activity of anaerobic bacteria from inside. Dissociation of fur from the body was also observed. Odor was very distinct. The average duration of this stage varied between 13 days in spring, 6 days in summer and 14 days in autumn (Fig. 2). In advanced decomposition stage, the odor began to fade, most of the soft tissues were digested by fly larvae, and towards the end the carcasses began to dry. This stage lasted on average 41 days in spring, 11 days in summer and 24 days on the seventh carcass in autumn. However, the eighth carcass, which was placed in October, continued in advanced stage through to the end of the study because of the onset of winter (Fig. 2). Decomposition stage was characterized with desiccation and only bones, some cartilage and dry tissue remained. There was no evident ending for this stage (Fig. 2).

• 
  • View Large Image
  • Download to PowerPoint

• Fig. 1. 

  Annual temperatures. The average of both site's temperatures which were taken by thermo-hygrometer and probed thermometer.

It is well known that carcasses decompose at different rates depending on season [1], [8], [9]. Pig carcasses generally decompose faster in summer than in other months. For the sixth carcass, which was placed in summer, it took 20 days to reach the dry stage with an average of 34°C, while it took 52 days for the third carcass placed in spring with an average of 29.2°C (Fig. 2). The 9th, 10th, 11th and 12th carcasses had not reached the dry stage by the end of the one-year study period in March 2007. From the findings of our study (Fig. 2) and other studies mentioned earlier, all decomposition stages showed curtailment from spring to summer and prolongation through autumn. Scientists studying decomposition examine the process by separating it into four to six stages [7], [8], [10], [11], [12]. Undoubtedly, the duration of these stages and the availability of attracted insect species change with the season. From the findings, it could be said that decomposition rates are directly proportional to temperature (Fig. 1, Fig. 2).

• 
  • View Large Image
  • Download to PowerPoint

• Fig. 2. 

  Decomposition process. Duration of each stage of all carcasses are given in time series and date of placement of every carcass is indicated with “X”.

In the study, a total of 40 species of Coleoptera, belonging to 6 families, were attracted to the carcasses in a one-year period (Table 2). Availability of these species through the one-year period of study are given in Fig. 3 and the decomposition processes of the first eight pig carcasses are given in Table 3.1, Table 3.2, Table 3.3, Table 3.4, Table 3.5, Table 3.6, Table 3.7, Table 3.8 with the time series of all species. However, considering the duration of their presence, 18 of them were observed only once and then just for a short period (several days at most) on the carcasses (Table 2, light text). They were evaluated as ‘accidental species’ and were not included in the main scope of the study. Twenty-two species were accepted to be important according to their presence (Table 2, bold text). Scarabaeidae, Carabidae and Tenebrionidae were accidental species but observed frequently.

Table 2. List of every accounted species in the study. 22 species which were considered important in decomposition are given in bold.

• 
  • View Large Image
  • Download to PowerPoint

• Fig. 3. 

  Availability of species through one-year period. Bars indicate the duration of that species’ availability over the months.

Table 3.1. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.2. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.3. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.4. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.5. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.6. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.7. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Table 3.8. Time series of first eight pig carcasses with decomposition stages. F: fresh stage, B: bloated stage, AD: active decay stage, AdD: advanced decay stage, D: dry stage.

Insect succession on carcasses develops in a predictable sequence as reported by Anderson [2]. Within this sequence, Diptera is the first insect group to be attracted [13]. According to findings from every carcass in our study, a certain sequence could be seen. Among Coleoptera, silphids were the first attracted group, followed by staphylinids and histerids. All three families were reported as predators [1], [8], [11], thus feeding on fly larvae and frequently found while fly larvae were abundant. As decomposition progressed, dermestids, nitidulids and clerids were attracted to the carcass. While dermestids feed on the dry tissue of carcasses, nitidulids are both necrophage and saprophage and could be observed at advanced stages of decomposition along with dermestids [13], as in our study. These findings are consistent with the findings of Reed [8], Carvalho et al. [7], and Tantawi et al. [9]. Clerids differ from dermestids and nitidulids by being predators, not necrophages [1], [10] and they feed on dermestid larvae and some fly larvae [8]. Although they were seen during early stages, they could also be observed at the advanced decomposition and dry stages.

The staphylinids recorded here were Creophilus maxillosus, Ontholestes murinus, Platydracus flavopunctatus, Philonthus corruscus, Philonthus concinnus, Philonthus politus, Philonthus laminatus, Aleochara lata and Aleochara intricata. All species were found during the active and advanced decay stages when fly larvae were dense, as they are all predators. It was observed that they were arriving earlier on carcasses in the summer and this is related to temperature and the emergence time of fly larvae. Platydracus flavopunctatus could be found on carcasses for only for a 50-day period during the study (Jun to early August), but it was seen on carcasses at every stage of decomposition. Thus, although it is a predator on fly larvae like other staphylinids, it did not show a preference for a particular decomposition stage. Because it can be observed for only for a particular time of year, this species could be important with regards to evaluation of time of death. Aleochara intricata was recorded for a 127-day period on the third pig carcass: it was hypothethised that rainfall during this period could have positively influenced it, resulting in an unexpected prolongation of its presence.

After Staphylinidae, Histeridae was the family having the most number of species on carcasses: Margarinotus brunneus, Saprinus caerulescens, Saprinus subnitescens and Saprinus vermiculatus were the determined species. According to the data, histerids were not seen in the second half of summer when the ambient temperature was at the maximum level (Fig. 1), and it was concluded that they were found mainly during active and advanced decomposition stages.

Dermestidae species, contrary to staphylinids and histerids, fed directly on the carcass itself. Because of this habit, the period of their availability and the decomposition stages during which they could be found were wide. Dermestes frischii and Dermestes undulatus were identified in this study. They began to be seen from the bloated stage but they were mainly involved in the dry stage of decomposition, with their larvae feeding on the carcass. D. frischii arrived earlier than D. undulatus from spring through summer, but arrival was delayed in summer months.

Two Silphidae species were recorded, Thanatophilus ferrugatus and Thanatophilus rugosus, both feeding on fly larvae on the carcass and on the carcass itself as observed by Payne [12]. They were both detected in spring when ambient temperature was relatively cooler (Fig. 1) and are thought to be psychrophilic. T. ferrugatus was found mainly during the active decomposition stage, and it stayed longer, but it was also found during the advanced decomposition stage. Nicrophorus species were not recorded in our study, possibly because of the large size of the pigs used: as stated in Borror et al. [14] and Byrd and Castner [13], Nicrophorus species are found generally around small animal carcasses.

Nitidulidae family is known as saprophilic and necrophilic [8] and is seen typically together with dermestids during the advanced stages of decomposition. Three species were observed here: Nitidula flavomaculata, Nitidula rufipes and Nitidula carnaria. All three species were generally found in spring and autumn. In summer they were seen rarely or not at all. Even though they were identified during the bloated and active decomposition stages in spring and autumn, they were principally found during advanced decomposition and dry stages. N. rufipes stayed longer during the active and advanced decomposition stages than during the dry stage and could be found in the warmer summer months, incontrast to N. flavomaculata, which was not seen in summer.

Of the Cleridae family, which are predators on some flies (Piophilidae) and dermestid larvae [8], Necrobia rufipes and Necrobia violacea were found. They arrived during the active decomposition stage and continued to be found mainly during the advanced decomposition stage until the advanced periods of the dry stage. N. violacea arrived 10 days earlier than N. rufipes in spring and stayed until late summer. Both species arrived at the early stages of decomposition as ambient temperature increased.

Back to Article Outline

4. Conclusions 

The succession of insects on pig carcasses can, in general, be considered to be characterized by the members of two orders, Diptera and Coleoptera. With this study, we examined the latter part of succession, which included the Coleoptera. We have identified the families and species of Coleoptera arriving on pig carcasses in Ankara province, Turkey, their distribution over a single year and for how long and in which decomposition stages they were found over the seasons.

This is the first study done in Turkey on the Coleopteran fauna of carcasses. Data acquired from the study could be used to help interpret the Coleopteran evidence in forensic cases in Ankara and its surroundings in the future. The entomofauna of cadavers and succession studies are newly developing fields in Turkey and need more attention from scientists.

Back to Article Outline

Acknowledgements 

This study was part of a MSc thesis conducted at Hacettepe University Biology Department which was accepted on September 13, 2007. We would like to thank Hacettepe University Scientific Researches Unit for supporting our study with 06D-02 601 001 numbered project, as well as Dr. Fabio Penati from Italy, Dr. Jiří Háva from Czech Republic, Volker Assing from Germany and Dr. Alexander Kirejtshuk from Russia for identifying our specimens at the species level.

Back to Article Outline

References 

1. Kočárek P. Decomposition and Coleoptera succession on exposed carrion of small mammal in Opava, the Czech Republic. European Journal of Soil Biology. 2003;39:31–45
   • View In Article
2. Anderson GS. Insect succession on carrion and its relationship to determining time of death. In:  Byrd JH,  Castner JL editor. Forensic Entomology: The Utility of Arthropods in Legal Investigations. Boca Raton, Florida: CRC Press; 2001;p. 143–175
   • View In Article
3. E.P. Catts, N.H. Haskell, Entomology and Death: A procedural Guide, Clemson, SC, 1990.
   • View In Article
4. Goff ML. A Fly For Prosecution. Harvard University Press; 2000;
   • View In Article
5. Goff ML. Feast of clues: insects in the service of forensics. Sciences. 1991;31(4):30–35
   • View In Article
6. Kim JI, Jung BH. Taxonomic review of the Cleridae (Coleoptera) in Korea (Part 3): Korynetinae, Tarsosteninae and Tillinae. Entomological Research. 2006;36(4):245–252
   • View In Article
7. de Carvalho LML, Thyssen PJ, Goff ML, Linhares AX. Observations on the succession patterns of necrophagous insects on a pig carcass in an urban area of Southeastern Brazil. Aggrawal's Internet Journal of Forensic Medicine and Toxicology. 2004;5(1):33–39
   • View In Article
8. Reed HB. A study of dog carcass communities in Tennessee, with Special references to the insects. The American Midland Naturalist. 1958;59:213–245
   • View In Article
9. Tantawi TI, El-Kady EM, Greenberg B, El-Ghaffar HA. Arthropod succession on exposed rabbit carrion in Alexandria, Egypt. Journal Medical Entomology. 1996;33(4):566–580
   • View In Article
10. Anderson GS, VanLaerhoven SL. Initial studies on insect succession on carrion in southwestern British Columbia. Journal of Forensic Sciences. 1996;41(4):617–625
    • View In Article
11. Wolff M, Uribe A, Ortiz A, Duque P. A preliminary study of forensic entomology in Medellin, Colombia. Forensic Science International. 2001;120:53–59
    • View In Article
    • Abstract
    • Full Text
    • Full-Text PDF (210 KB)
    • CrossRef
12. Payne JA. A summer carrion study of the baby pig Sus scrofa Linnaeus. Ecology. 1965;46:592–602
    • View In Article
    • CrossRef
13. Byrd JH, Castner JL. Forensic Entomology: The Utility of Arthropods in Legal Investigations. Boca Raton, FL: CRC Press; 2001;
    • View In Article
14. Borror DJ, Triplehorn AC, Johnson NF. An Introduction to the Study of Insects. 6th ed.. Philadelphia: Saunnders; 1989;
    • View In Article