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Coleopterofauna found on fresh and frozen rabbit carcasses in Curitiba, Paraná, Brazil

Coleopterofauna encontrada em carcaças de coelho congeladas e frescas em Curitiba, Paraná, Brasil

Abstracts

Many arthropod species are associated with carrion and some of them can be used as forensic indicators in murder investigations to estimate the time of death. Different physical conditions of cadavers may influence the fauna and the importance of freezing and thawing is unknown. The present paper sought to survey the Coleoptera species encountered in frozen and fresh rabbit carcasses, at a forest in Curitiba, Brazil. Four rabbit carcasses, two of them fresh and the other frozen were used. The coleopterofauna was sampled daily, and analyzed using non-parametric tests. A total of 666 beetles were sampled, belonging to 28 species in 10 families. Most of the beetles captured were larvae of Oxelytrum spp. (433) which are known to be necrophagous. The two frozen carcasses accounted for most of the beetles (338 and 180) in comparison with the two fresh carcasses (103 and 45). The tests were based on the most abundant species. Oxelytrum spp. median differed significantly between carcasses (H = 12.47844; p = 0.0059). The two fresh carcasses differed significantly (U = 190.0; p = 0.00019), but there was no significant difference between the frozen carcasses (U = 336.0; p = 0.29755). The data indicate that the freezing process prevents certain species to colonize carcasses, in this case with the dominance of species of Oxelytrum. These data also indicate that careful attention is necessary before using frozen carcasses in forensic entomology studies.

beetles; carrion fauna; forensic entomology; Oxelytrum spp. and cause of death


Muitas espécies de artrópodes são associadas a carcaças e algumas delas podem ser utilizadas em casos de morte violenta como indicadoras forenses do intervalo decorrido desde a morte do indivíduo. Diferentes condições físicas dos cadáveres podem influenciar a fauna, sendo que o efeito do congelamento e descongelamento é desconhecido. Os objetivos do presente trabalho foram levantar as espécies de Coleoptera em carcaças de coelho frescas e congeladas em um remanescente florestal localizado em Curitiba, Brasil. Foram utilizadas quatro carcaças de coelhos, dois frescos e dois previamente congelados. A coleopterofauna foi amostrada diariamente e analisada com testes não paramétricos. Foram coletados 666 espécimes, pertencentes a 28 espécies, de 10 famílias. A maioria dos besouros coletados foi representada por larvas de Oxelytrum spp. (433), as quais são necrófagas. Observou-se um maior número de indivíduos sobre as carcaças congeladas (338 e 180) em comparação com as duas frescas (103 e 45). Os testes foram baseados nas espécies mais abundantes. A mediana das espécies de Oxelytrum diferiu significativamente entre as carcaças (H = 12,47844; p = 0,0059). As duas carcaças frescas diferiram significativamente (U = 190,0; p = 0,00019), porém não houve diferença significativa entre as carcaças congeladas (U = 336,0; p = 0,29755). Os dados indicaram que o processo de congelamento evitou que algumas espécies colonizassem as carcaças, neste caso com dominância de espécies de Oxelytrum. Estes dados também indicam a necessidade de cuidado ao utilizar carcaças congeladas em estudos de entomologia forense.

besouros; fauna necrófaga; entomologia forense; Oxelytrum spp. e carcaça de coelho


1. Introduction

Carrion represents a micro-habitat providing a temporary, changing food source for a distinct community of organisms (Tullis and Goff, 1987TULLIS, K. and GOFF, ML., 1987. Arthropod succession in exposed carrion in a tropical rainforest on O'ahu Island, Hawaii. Journal of Medical Entomology, vol. 24, p. 332-339.). The main organisms associated with this process are bacteria, fungi and various groups of arthropods (Putman, 1978PUTMAN, RJ., 1978. The role of carrion-frequenting arthropodsin the decay process. Ecological Entomology, vol. 3, p. 133-139.). The cadaveric fauna could then be used to establish time of death (postmortem interval) and to know if a human body has been moved or partly concealed during decomposition (Smith, 1986SMITH, KGV., 1986. A Manual of Forensic Entomology. London: Trustees of the British Museum (Natural History).). Among this fauna, Coleoptera is one of the most important orders, and it is considered the main entomological evidence when skeletal human remains are found (Kulshrestha and Satpathy, 2001KULSHRESTHA, P. and SATPATHY, DK., 2001. Use of beetles in forensic entomology. Forensic Science International, vol. 120, p. 15-17.) and when the remains are recovered outdoors (Goff, 1991GOFF, ML., 1991. Comparison of Insect Species Associated with Decomposing Remains Recovered Inside Dwellings and Outdoors on the Island of Oahu, Hawaii. Journal of Forensic Sciences, vol. 36, p. 748-753.).

However the entomological data may depend on the previous and posterior conditions of death, as these factors affect the succession (Byrd and Castner, 2001BYRD, JH. and CASTNER, JL., 2001. Forensic Entomology: The Utility of Arthropods in Legal Investigations. Florida: CRC Press.), which is used in the PMI estimation. This happens because the environmental variables may slow down or speed up insects arrival. Among these factors, season, environmental temperature and air humidity affect insects development (Marchenko, 2001MARCHENKO, MI., 2001. Medicolegal relevance of cadaver entomofauna for the determination of the time of the death. Forensic Science International, vol. 120, p. 89-109.) and species presence (Archer and Elgar, 2003ARCHER, MS. and ELGAR, MA., 2003. Yearly activity patterns in southern Victoria (Australia) of seasonally active carrion insects. Forensic Science International, vol. 132, p. 173-176.). Body access is another important factor (Mann et al., 1990MANN, RW., BASS, VM. and MEADOWS, L., 1990. Time since death and decomposition of the human body: variables and observations in case and experimental field studies. Journal of Forensic Sciences, vol. 35, p. 103-111.). Conditions in which the body is buried (Corrêa and Almeida unpublished data), enclosed in cars (Voss et al., 2008VOSS, SC., FORBES, SL. and DADOUR, IR., 2008. Decomposition and insect succession on cadavers inside a vehicle environment. Forensic Science and Medical Patholology, vol. 4, p. 22-32.), or wrapped in blankets (Goff, 1992GOFF, ML., 1992. Problems in estimation of postmortem interval resulting from the wrapping of a corpse: a case study from Hawaii. Journal of Agricultural Entomology, vol. 9, p. 237-243.) may alter the entomological succession.

Some studies addressed that different physical conditions of corpses may influence the fauna. It is known that the fauna changes in buried, burnt or hanged carcasses (Motter, 1898MOTTER, MG., 1898. A contribution to the study of the fauna of the grave, A study of one hundred and fifity disinterments, with some additional experimental observations. Journal of New York Entomological Society, vol. 6, p. 201-231.; Avila and Goff, 1998AVILA, FW. and GOFF, ML., 1998. Arthropod succession patterns onto burnt carrion in two contrasting habitats in the Hawaiian Islands. Journal of Forensic Sciences, vol. 43, p. 581-586.; Vanlaerhoven and Anderson, 1999VANLAERHOVEN, SL. and ANDERSON, GS., 1999. Insect succession on buried carrion in two biogeoclimatic zones of British Columbia. Journal of Forensic Sciences, vol. 44, p. 32-43.; Shalaby et al., 2000). In burnt corpses, fly oviposition may occur faster and the decomposition process can be hastened by four days (Avila and Goff, 1998AVILA, FW. and GOFF, ML., 1998. Arthropod succession patterns onto burnt carrion in two contrasting habitats in the Hawaiian Islands. Journal of Forensic Sciences, vol. 43, p. 581-586.). Few studies addressed the importance of freezing and thawing over the body (Micozzi, 1986MICOZZI, MS., 1986. Experimental study of postmortem change under field conditions: effects of freezing, thawing, and mechanical injury. Journal of Forensic Sciences, vol. 31, p. 953-961.; Stokes et al., 2009STOKES, KL., FORBES, SL. and TIBBETT, M., 2009. Freezing skeletal muscle tissue does not affect its decomposition in soil: Evidence from temporal changes in tissue mass, microbial activity and soil chemistry based on excised samples. Forensic Sciences International, vol. 183, p. 6-13.) and no studies were found about their effects over the fauna. Such studies are necessary as small changes may alter the whole entomological succession in a highly competitive environment and many studies use defrosted carcasses in succession entomological studies (Payne, 1965PAYNE, JA., 1965. A summer carrion study of the baby pig Sus scrofa Linnaeus. Ecology, vol. 46, p. 591-602.; Tullis and Goff, 1987TULLIS, K. and GOFF, ML., 1987. Arthropod succession in exposed carrion in a tropical rainforest on O'ahu Island, Hawaii. Journal of Medical Entomology, vol. 24, p. 332-339.).

It is known that freezing/thawing allows the formation of ice crystals that lead to body dehydration (Stokes et al., 2009STOKES, KL., FORBES, SL. and TIBBETT, M., 2009. Freezing skeletal muscle tissue does not affect its decomposition in soil: Evidence from temporal changes in tissue mass, microbial activity and soil chemistry based on excised samples. Forensic Sciences International, vol. 183, p. 6-13.), which alter the growth pattern of enteric fauna. Another effect is that the external parts of the body would be the first to thaw being then directly exposed to microorganisms from outside (Zugibe, 1993). Therefore, the body decomposition process occurs “outside-in”, while normally it happens “inside-out” (Micozzi, 1986MICOZZI, MS., 1986. Experimental study of postmortem change under field conditions: effects of freezing, thawing, and mechanical injury. Journal of Forensic Sciences, vol. 31, p. 953-961.). If the freezing is caused by low environmental temperatures, it is known that at 5-13 °C flies will continue visiting the carcasses, but at 0 °C their eggs will die. However, fly larvae may survive if they stay inside the body (Mann et al., 1990MANN, RW., BASS, VM. and MEADOWS, L., 1990. Time since death and decomposition of the human body: variables and observations in case and experimental field studies. Journal of Forensic Sciences, vol. 35, p. 103-111.). The low temperatures effect to carrion beetles is unknown.

Gunn (2006)GUNN, A., 2006. Essential Forensic Biology. Chichester, John Wiley and Sons, Ltd. mentioned that murderers sometimes store their victim's body in a freezer before disposing of it, which was also reported by Zugibe and Costello (1993)ZUGIBE, FT. and COSTELLO, JT., 1993. The iceman murder: One of a series of contract murders. Journal of Forensic Sciences, vol. 38, p. 1404-1408. in the USA, where a human body was stored in a freezer prior to disposal. The freezing/thawing process can also be due to a cold environment or to a deliberate preservation prior to burial or experimental procedures (Stokes et al., 2009STOKES, KL., FORBES, SL. and TIBBETT, M., 2009. Freezing skeletal muscle tissue does not affect its decomposition in soil: Evidence from temporal changes in tissue mass, microbial activity and soil chemistry based on excised samples. Forensic Sciences International, vol. 183, p. 6-13.). In this way, it is necessary to study their effects over the entomofauna to analyse the results when such process is confirmed. Day and Wallman (2006)DAY, DM. and WALLMAN, JF., 2006. A comparison of frozen/thawed and fresh food substrates in development of Calliphora augur (Diptera: Calliphoridae) larvae. International Journal of Legal Medicine, vol. 120, p. 391-394. tested if the freezing/thawing affects the growth of Callliphora augur (Fabricius), and concluded that there was no significant effect. However the effects of this process over the entomological succession, remains unknown.

The present paper sought to survey the Coleoptera encountered in frozen and fresh rabbit carcasses.

2. Materials and Methods

The experiment took place from December 2007 to January 2008 in the “Mata Viva” Reserve (25°26′45″ S 49°13′58″ W; 900 m over sea level), located at Universidade Federal do Paraná (Curitiba, Paraná, Brazil). The average annual temperature varies between 17-18 °C and annual relative humidity between 80-85% (IAPAR 2011). The vegetation is Mixed Rain Forest in different successional stages (Reginato et al., 2008REGINATO, M., MATOS, FB., LINDOSO, GS., SOUZA, CMF., PREVEDELLO, JA., MORAIS, JW. and EVANGELISTA, PHL., 2008. A vegetação na Reserva Mata Viva, Curitiba, Paraná, Brasil. Acta Biológica Paranaense, vol. 37, p. 229-252.).

Four rabbit (Oryctolagus cuniculus L., 1758) carcasses weighting approximately 1 kg were used as bait to sample the Coleoptera. The rabbits were killed by cervical dislocation, being two of them frozen two days prior to the beginning of the experiment and the other two being killed at the local. The carcasses were placed inside metallic cages, 8 meters away from each other, under direct sunlight. Active samplings were conducted daily to capture both immature and adult specimens, which were stored in plastic jars and killed, mounted and identified in laboratory. The samplings were made for 30 days, time period in necessary for the carcass to reach the dry remains stage. The identification was done using keys (Mazur, 2002MAZUR, S., 2002. Review of the Histeridae (Coleoptera) of México. Dugesiana, vol. 8, p. 17-66.; Navarrete-Heredia et al., 2002NAVARRETE-HEREDIA, JL., NEWTON, AF., THAYER, MK., ASHE, JS. and CHANDLER, DS., 2002. Guía ilustrada para los géneros de Staphylinidae (Coleoptera de México). Illustrated guide to the genera of Staphylinidae (Coleoptera) of Mexico. México: Universidad de Guadalajara; CONABIO.; Almeida and Mise, 2009ALMEIDA, LM. and MISE, KM., 2009. Diagnosis and key of the main families and species of South American Coleoptera of forensic importance. Revista Brasileira de Entomologia, vol. 53, p. 227-244.) and specialists help.

Diversity indexes were calculated in Past 1.91 (Hammer et al., 2001HAMMER, O., HARPER, DAT. and RYAN PD., 2001. PAST: Paleontological Statistics software package for education and data analysis. Paleontologia Electronica, vol. 4, p. 1-9.) and statistical tests were conducted using Statistica 7.0 (Statsoft, 2004STATSOFT, 2004. STATISTICA (data analysis software system), Version 7. Available from: www.statsoft.com.
www.statsoft.com...
). The tests were based on the most abundant species, to verify the possible good forensic indicators. First a Kolmorogov-Smirnov test was done to verify if the data fit a normal distribution, as it did not, log (x + 1) and transformations were tried, which again did not fit a normal distribution. As the premises of ANOVA were not met, a non-parametric test (Kruskal-Wallis) was used instead to compare all carcasses. To compare frozen x frozen and fresh x fresh, a Wilcoxon-Mann-Whitney test was used to see if they differed significantly. To compare the diversity found on the carcasses Shannon and Berger-Parker diversity indexes were used.

3. Results and Discussion

A total of 666 beetles were sampled, belonging to 20 species in 10 families. Silphidae had the greater number of specimens, followed by Staphylinidae, Leiodidae and Histeridae. The low number of Staphylinidae was not expected, as species of this family were abundant in 15 kg pig carcasses (Mise et al., 2007MISE, KM., ALMEIDA, LM. and MOURA, MO., 2007. Levantamento da fauna de Coleoptera que habita a carcaça de Sus scrofa L., em Curitiba, Paraná. Revista Brasileira de Entomologia, vol. 51, p. 358-368., 2008MISE, KM., MARTINS, CBC, KÖB, EL. and ALMEIDA, LM., 2008. Longer decomposition process and the influence on Coleoptera fauna associated with carcasses. Brazilian Journal of Biology, vol. 68, p. 907-908.), probably because of the difference in carcass size. Most of the beetles captured were larvae of Oxelytrum spp. (433) which are known to be necrophagous. Such high number was expected as O. discicolle (Brullé 1840) was previously encountered in laboratory-bred Rattus norvegicus (Berkenhout, 1769) carcasses (Moura et al., 1997MOURA, MO., CARVALHO, CJB. and MONTEIRO-FILHO, ELA., 1997. A preliminary analysis of insects of medico-legal importance in Curitiba, State of Paraná. Memórias do Instituto Oswaldo Cruz, vol. 92, p. 269-274.) and Sus scrofa L., 1758 carcasses (Mise et al., 2007MISE, KM., ALMEIDA, LM. and MOURA, MO., 2007. Levantamento da fauna de Coleoptera que habita a carcaça de Sus scrofa L., em Curitiba, Paraná. Revista Brasileira de Entomologia, vol. 51, p. 358-368.), in the same study area. It was also recorded in rabbit carcasses at Rio Grande do Sul state, south of Brazil (Souza et al., 2008SOUZA, ASB., KIRST, FD. and KRÜGER, RF., 2008. Insects of forensic importance from Rio Grande do Sul state in southern Brazil. Revista Brasileira de Entomologia, vol. 52, p. 641-646.) and in human corpses in Cali, Colombia (Barreto et al., 2002BARRETO, M., BURBANO, MA. and BARRETO, P., 2002. Flies (Calliphoridae, Muscidae) and Beetles (Silphidae) from Human Cadavers in Cali, Colombia. Memórias do Instituto Oswaldo Cruz, vol. 97, p. 137-138.) and São Paulo state, Brazil (Carvalho et al., 2000CARVALHO, LML., THYSSEN, PJ., LINHARES, AX. and PALHARES, FAB., 2000. A checklist of arthropods associated with pig carrion and human corpses in southeastern Brazil. Memórias do Instituto Oswaldo Cruz, vol. 95, p. 135-138.).

The succession is illustrated (Tables 1-4), indicating that when analyzed in a week-basis, most species arrival and departure times occur only one time, with few recolonizations. These data are different from the ones obtained by Mise et al. (2007)MISE, KM., ALMEIDA, LM. and MOURA, MO., 2007. Levantamento da fauna de Coleoptera que habita a carcaça de Sus scrofa L., em Curitiba, Paraná. Revista Brasileira de Entomologia, vol. 51, p. 358-368., probably because small carcasses enable only one generation before disappearing.

Table 1
- Species of Coleoptera collected during a four-week study in fresh rabbit carcass (fresh 1) in Curitiba, PR, Brazil.

Table 2
- Species of Coleoptera collected during a four-week study in frozen rabbit carcass (frozen 1) in Curitiba, PR, Brazil.

Table 3
- Species of Coleoptera collected during a four-week study in fresh rabbit carcass (fresh 2) in Curitiba, PR, Brazil.

Table 4
- Species of Coleoptera collected during a four-week study in frozen rabbit carcass (frozen 2) in Curitiba, PR, Brazil.

The frozen carcasses accounted for most of the beetles (338 for frozen 1, and 180 for frozen 2) in comparison with the fresh (103 for fresh 1, and 45 for fresh 2). Regarding the richness, the lowest value was measured in the last frozen carcass, mainly due to the great number of ants found. The richness varied, with 12 and 10 species in the fresh carcasses and 11 and 7 species in the frozen carcasses (Table 5). Comparing the fauna found on the carcasses, the higher Shannon diversity index was found on the fresh ones, which indicates that the freezing process reduces species eveness on carcasses. This is corroborated by the Berger-Parker index, a dominance measure, which was higher on the frozen carcasses because of the high abundance of Oxelytrum species.

Table 5
- Measures of diversity of fresh and frozen rabbit carcasses, calculated based on beetles sampled during four weeks in Curitiba, PR, Brazil.

As Oxelytrum spp. accounted for 65.01% of the specimens and they are known to feed and breed on carcasses (Peck and Anderson, 1985PECK, SB. and ANDERSON, RS., 1985. Taxonomy, phylogeny and biogeography of the carrion beetles of Latin America (Coleoptera: Silphidae). Quaestione Entomologicae, vol. 21, p. 247-317.), their abundance was used to test if the genus can be an indicator when a freezing process occurs.

The median differed significantly when all carcasses were used (H = 12.47844; p = 0.0059). A Wilcoxon-Mann-Whitney test was conducted to test if they differed significantly between treatments (fresh x fresh; frozen x frozen). The two fresh carcasses differed significantly (U = 190.0; p = 0.00019), but there was no significant difference between the frozen carcasses (U = 336.0; p = 0.29755). The data indicate that the freezing process prevents certain species to colonize carcasses, probably reducing competition and therefore allowing a more patterned succession, in this case with the dominance of Oxelytrum spp. Low temperatures (< 4 °C) slow down putrefaction, by interfering in the bacterial activity (Micozzi, 1987), even during the thawing process in environmental temperature (Micozzi, 1986MICOZZI, MS., 1986. Experimental study of postmortem change under field conditions: effects of freezing, thawing, and mechanical injury. Journal of Forensic Sciences, vol. 31, p. 953-961.), reducing also the smell liberated during the first hours. This could be observed in the present study, as the initial decomposition process took longer in the frozen carcasses, but as the study did not aim to compare their decomposition, only their fauna, this could not be measured. Such factors may have benefited beetles, mainly Oxelytrum spp., over other competitors, including flies. These data indicate that a careful approach is necessary before using frozen carcasses in forensic entomology studies, as they may present a different entomological succession. There is a need of studies using larger carcasses and repetitions to define the limit that separates the abundance between frozen and fresh carcasses.

We thank Dra. Cibele Stramare Ribeiro-Costa, MSc. Angélico Asenjo Flores and the reviewers for their helpful contributions to this paper. Also the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (KMM, RCC) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (LMA) for the financial support and scholarship. This is the contribution number 1801 of the Department of Zoology, Universidade Federal do Paraná.

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Publication Dates

  • Publication in this collection
    Aug 2013

History

  • Received
    13 June 2012
  • Accepted
    12 Sept 2012
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
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