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Beetles (Insecta, Coleoptera) associated with pig carcasses exposed in a Caatinga area, Northeastern Brazil/Coleopteros (Insecta, Coleoptera) associados a carcacas de suinos em Caatinga, Nordeste do Brasil.

1. Introduction

Insects are usually the first animals to locate a cadaver, attracted by the odours and gases released by it, and then start to use it as a resource for feeding, reproduction and larval development (Cornaby, 1974). This entomofauna attracts also another kind of fauna, consisting of predatory insects (Smith, 1986). The beetles belong to both ecological categories. Few species are effectively necrophagous, while most of them are predatory, but both categories can provide useful information from the forensic point of view, especially concerning to the estimation of the postmortem interval (PMI) (Catts and Goff, 1992; Santos et al. 2013).

In Brazil, important contributions to diversity, ecology and taxonomy of the fauna associated with carcasses have been made in the last two decades, but the majority of the studies have focussed on Diptera and are concentrated in the Southeast and South regions (Pujol-Luz et al., 2008). However, due to their succession pattern, Coleoptera are the most useful insects for the estimation of PMI when skeletonised corpses are found (Kulshrestha and Satpathy, 2001). In some cases, it is possible to estimate the PMI based on rates of development of some species (Arnaldos et al., 2004). Coleoptera can also be used to support the PMI estimate from Diptera data (Goff and Flynn, 1991).

Regional and seasonal studies are essential to identify specific cadaveric fauna, since each biome and season has its specific fauna because of particular environmental conditions (Mise et al., 2010; Rosa et al., 2011). The main objective was to analyse the diversity of the Coleoptera fauna associated with pig (Sus scrofa Linnaeus, 1758) carcasses, during the dry and wet seasons in Caatinga, a dry forest endemic to Brazil, whose insect fauna is poorly known (Vasconcellos et al., 2010; Creao-Duarte et al. 2013; Alves et al., 2014). Brief comments on the main families of forensic importance are also included, highlighting the richness, abundance, behaviour and ecological aspects of some species.

2. Material and Methods

The study was carried out during October 2010 (dry season) and February 2011 (rainy season) at the Private Reserve for the Environmental Inheritance Fazenda Almas (RPPN Fazenda Almas), in Sao Jose dos Codeiros, state of Paraiba, Brazil (7[degrees] 28' 19" S, 36[degrees] 53' 40" W). The study area is located at an altitude of 650 m a.s.l. and 300 km away from the coast. The vegetation varies from open to dense arboreal Caatinga, with a strong deciduous characteristic during the dry season. The soil is sandy and arid and the topography is irregular, with inselbergs and rocky outcrops (Vasconcellos et al., 2010).

Two male pig carcasses, weighing around 15 kg each, were used in both seasons. The animals were killed with a single gunshot to the head. Each carcass was exposed in an iron cage to prevent interference of vertebrate scavengers. Underneath the cage there was a trap tray buried at ground level containing sawdust in order to collect actively the Coleoptera that take shelter under the carcasses. Four pitfall traps were settled around the cage, 1 m away from it, to passive capture. Each cage was also covered by a modified Shannon trap with a collector tube containing 70% alcohol at the apex (Alves et al., 2014). Coleoptera were collected daily in and from the traps.

The identification of the Coleoptera was done by experts and specific literature (Mazur, 2001; Navarrete-Heredia et al., 2002; Almeida and Mise, 2009; Vaz-deMello et al., 2011; Aballay et al., 2013). All material used was incorporated into the Colecao Entomologica do Departamento de Sistematica e Ecologia at Universidade Federal da Paraiba (DSEC/UFPB).

3. Results and Discussion

A total of 4,851 adults belonging to 19 families and 88 species was collected (Table 1). Staphylinidae was the most abundant family with 2,184 individuals, followed by Histeridae (1,264), Nitidulidae (395), Dermestidae (333), Scarabaeidae (300), Cleridae (120), Carabidae (75) and Trogidae (75), amounting to 97.8% of the specimens.

Under similar conditions different results were obtained by Carvalho et al. (2000), in Campinas, state of Sao Paulo, whose decreasing order of abundance was Scarabaeidae, Histeridae, Silphidae and Staphylinidae. Mise et al. (2007), in Curitiba, State of Parana, found Staphylinidae as the most abundant family, as in the present study, followed by Silphidae, Histeridae and Cleridae. Rosa et al. (2011), in areas of Cerrado, in Uberlandia, State of Minas Gerais, collected mainly Dermestidae, Histeridae, Cleridae and Staphylinidae. These divergent results highlight the importance of local studies for forensic practice in Brazil.

High species richness of beetles associated to carcasses has been registered in the Neotropical region: 62 and 113 species were mentioned respectively by Luederwaldt (1911) and Pessoa and Lane (1941) in Sao Paulo and neighbourhood; 112 species were collected by Mise et al. (2007) in Curitiba, state of Parana; and 41 species were found by Mise et al. (2010) in Manaus, State of Amazonas. These data demonstrate the importance of Coleoptera when sampling strategies do not neglect this taxonomic group.

Smith (1986) considered as Coleoptera families with forensic importance: Carabidae, Hydrophilidae, Silphidae, Leiodidae, Staphylinidae, Histeridae, Cleridae, Anthicidae, Dermestidae, Nitidulidae, Rhizophagidae, Ptinidae, Tenebrionidae, Scarabaeidae, Geotrupidae and Trogidae. Ten of these families were found in the present study and represented 98.7% of the specimens collected (Table 2).

Amongst the collected species, Pterostichus sp., Eremosaprinus sp., Ateuchus carbonarius (Harold, 1868), Canthidium manni Arrow, 1913, Coprophanaeuspertyi (Olsoufieff, 1924), Deltochilum verruciferum Felsche, 1911, Dichotomius geminatus (Arrow, 1913), Acylophorus sp., Philonthusfigulus Erichson, 1840 and Tribolium sp. are reported for the first time associated to carcasses in the Neotropical region.

The most abundant beetles collected, with number of individuals greater than 1% of the total, were represented by 17 species: Atheta iheringi Bernhauer, 1908 (1,685), Euspilotus sp. (461), S. geminata (394), Xerosaprinus diptychus (Marseul, 1855) (331), Dermestes maculatus De Geer, 1774 (330), Philonthus sp. 2 (294), Euspilotus azureus (Sahlberg, 1823) (188), A. carbonarius (129), Necrobia rufipes (De Geer, 1775) (120), Phelister sp. (114), Aleochara bonariensis Lynch, 1884 (102), Histerpunctifer Paykull, 1811 (82), Omorgus suberosus Fabricius, 1775 (75), Omalodes foveola Erichson, 1834 (67), Loxandrus sp. (65), Belonuchus sp. 2 (48) and C. manni (47) (Table 2). These species totaled together 93.1% of all beetles collected. Future specific studies, mainly about succession pattern, life cicle and diet, are required for a better understanding of the relationship of these species with carcasses and thus establish its forensic importance.

Rove beetles (Staphylinidae) are common on carcasses because they are predators of larvae of other insects, with a preference for fly larvae (Navarrete-Heredia et al., 2002; Byrd and Castner, 2010). In addition, larvae of some species of Aleochara are ectoparasites of fly pupae (Smith 1986). Staphylinidae was the most abundant family in the study, with 2,184 specimens, mainly represented by A. iheringi (1,685) and species of Philonthus (326). Most of the Staphylinidade were collected in the rainy season (86.6%), which also showed higher species richness (13) (Table 2).

Mise et al. (2007) highlighted Staphylinidae as the most abundant family, as in this study, with 29 species and 2,450 individuals captured. In many studies conducted in the Neotropical region, due to lack of specialists, the identification of these beetles is done only until genus.

However, there seems to be a similarity of the composition of the Staphylinidae fauna among different regions in Brazil, mainly represented by Aleochara and Philonthus (Souza and Linhares, 1997; Mise et al., 2007; Mise et al., 2010; Rosa et al., 2011; Silva and Santos, 2012). In other countries, several different genera were recorded occurring on carcasses (Wolff et al., 2001; Battan Horenstein and Linhares, 2011; Aballay et al., 2012).

The great abundance of the family Histeridae is mainly due to the fact that their species are predators of larvae of flies, food resource widely available on carcasses (Smith, 1986; Byrd and Castner, 2010). Histeride was the second most abundant family in this study, represented mainly by species of Euspilotus (649), collected mostly during the rainy season (92.4%), and X. diptychus (331), in the dry season (96.1%) (Table 2).

Aballay et al. (2012) foundX. diptychus and five species of Euspilotus on pig carcasses in a different kind of arid environment, in San Juan, Argentina. The other genera and species of Histeride collected are commonly found on carcasses throughout the Neotropical region (Souza and Linhares, 1997; Carvalho et al., 2000; Wolff et al., 2001; Mise et al., 2007, 2010; Battan Horenstein and Linhares, 2011; Silva and Santos, 2012; Aballay et al., 2013).

Larvae and adults of Nitidulidae are generally saprophagous or xylophagous, feeding on decaying or dead wood. However, some species are exclusively phytophagous or mycophagous and others occur on carcasses or are predators (Smith, 1986; Marinoni et al., 2001). Nitidulidae was the third family in order of abundance and was almost totally represented by S. geminata with 394 individuals collected, mostly during the dry season (79.2%) (Table 2).

According to Ewing and Cline (2005), S. geminata is commonly found in leaf litter and in decaying fruits and wood. The species probably plays a facultative necrophagous role in the carcasses, although it has not been observed feeding directly from it. Future studies about the biology of the species need to be done to elucidate this issue. Payne and King (1970), in South Carolina, USA, found nine species of Nitidulidae during advanced stages of decomposition of pigs together with Dermestidae. However, records of the family on carcasses are rare in the Neotropical region (Wolff et al., 2001; Mise et al., 2007; Battan Horenstein and Linhares, 2011; Silva and Santos, 2012).

Many larder beetles (Dermestidae) species, especially those of the genus Dermestes, are of considerable forensic importance. In cases in which the mummification of the body takes place, even indoors, these beetles can accelerate the skeletonisation process (Voigt, 1965; Schroeder et al., 2002) and, even so, adults and larvae can be found associated with the remains years after death (Byrd and Castner, 2010). In the present study, three individuals of Dermestes haemorrhoidalis Kuster, 1852 and 330 individuals of D. maculatus were collected. The last one is the most forensically important Coleoptera species in the Neotropical region and was more abundant in the dry season (69.4%) (Table 2).

Several authors have reported the presence of adults and larvae of D. maculatus on carcasses and corpses in Brazil (Souza and Linhares, 1997; Carvalho et al., 2000; Carvalho et al., 2004; Mise et al., 2007; Rosa et al., 2011) and the rest of the Neotropical region (Iannacone, 2003; Velasquez, 2008; Valdes-Perezgasga et al., 2010; Battan Horenstein and Linhares, 2011; Aballay et al., 2012). Mise et al. (2007), in an Araucaria forest fragment, found only 22 specimens of D. maculatus, while Rosa et al. (2011), in an area of Cerrado, collected 4,874 individuals, the majority in the dry season (94.6%), the same as in the present study. Despite differences between sampling methods, it seems to be clear the divergence in the abundance status of D. maculatus among different habitats, with a preference for drier regions.

With over 19,000 species described, Scarabaeidae vary greatly in biology, ecology and behaviour (Byrd and Castner, 2010). The members of this family are mainly detritivorous, with larvae feeding on dung or pieces of decomposing carcasses (Smith, 1986; Marinoni et al., 2001). Many species dig oviposition chambers and tunnels under or near the carcasses, where pieces of the carcass are deposited to feed the larvae, which can cause postmortem movement of the bodies (Ururahy-Rodrigues et al., 2008). In the present study, this family was the fifth most abundant, with 300 individuals, mostly present in the rainy season (97%). Fifteen species were collected, especially of the subfamily Scarabaeinae, mainly represented by A. carbonarius (43.0%) and C. manni (15.7%) (Table 2), which were very abundant in a study carried out by Hernandez (2007) in the same study area.

In Brazil, the studies by Luederwaldt (1911) and Pessoa and Lane (1941) about Scarabaeidae associated with carcasses of several animals in

Sao Paulo and surrounding cities are historical references. Together, these authors recorded 124 species, most of them belonging to the genera Canthidium, Canthon, Coprophanaeus, Deltochilum and Phanaeus.

Most of Cleridae are predators of larvae of flies and other beetles, but the genus Necrobia has necrophagous habit, with a preference for carcasses and corpses in dry stages of decomposition (Payne and King, 1970; Arnaldos et al., 2004). This family was the sixth in order of abundance and represented only by N. rufipes, with 120 specimens collected and showing preference for the dry season (61.7%) (Table 2).

Rosa et al. (2011) collected that species in great abundance (2,321) in an area of Cerrado, most of them in the dry season as well (94.1%). Adults and larvae of N. rufipes are widely found on carcasses and corpses in Brazil (Luederwaldt, 1911; Souza and Linhares, 1997; Carvalho et al., 2000, 2004; Mise et al., 2007; Silva and Santos, 2012) and elsewhere in the Neotropical region (Wolff et al., 2001; Iannacone, 2003; Valdes-Perezgasga et al., 2010; Battan Horenstein and Linhares, 2011; Aballay et al., 2012).

The diversity of Coleoptera fauna was different from other studies carried out in the Neotropical region, which may be a result not only from different environments, but also the capture method adopted. Ten species were recorded for the first time associated with carcasses in the Neotropical region. Populations of Staphylinidae and Histeridae, the most abundant families, can be considered as affected by seasonality, with only 13.4% and 34.2% of the specimens collected, respectively, in the dry season. Amongst the most collected species, X. diptychus showed to be strongly influenced by the dry season, since 96.1% of the specimens were collected during that period. A. iheringi, representing 34.7% of the total, was the most abundant species. Future studies are required to confirm the role of these beetles on carcasses and its possible forensic potential to Caatinga. In addition, the exceptional Coleoptera fauna found reinforces the need of regional studies about the composition of insects associated with carcasses throughout Neotropical region.

http://dx.doi.org/10.1590/bjb.2014.0072

Received: March 11, 2013--Accepted: May 15, 2013--Distributed: August 31, 2014

Acknowledgements

The authors are thankful to Dr. Edilson Caron (UFPR), Dr. Daniel P. Moura (UFPR) and M.Sc. Carolina N. Liberal (UFPB) for their help with the identifications; Dr. Carla L. Bicho (UEPB), Dr. Patricia J. Thyssen (UFPel) and Dr. Rodrigo C. A. P. Farias (UFPB) for critical comments on the manuscript. Thanks are also due to the "Conselho Nacional de Desenvolvimento Cientifico e Tecnologico" (CNPq) and the "Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior" (CAPES) for providing scholarships to A. C. F. Alves and W. E. Santos.

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Santos, WE. (a) *, Alves, ACF. (a) and Creao-Duarte, AJ. (a)

(a) Laboratorio de Entomologia, Programa de Pos-Graduacao em Ciencias Biologicas (Zoologia), Departamento de Sistematica e Ecologia, Universidade Federal da Paraiba--UFPB, Cidade Universitaria, CEP 58059-900, Joao Pessoa, PB, Brazil

* e-mail: well-bio@hotmail.com
Table 1. Absolute (n) and relative (%) abundance, and species
richness (S) of Coleoptera families associated to pig carcasses
during dry and rainy seasons in a Caatinga area, state
of Paraiba, Brazil.

Family                   Dry season            Rainy season

                   n        %       S      n        %       S

Staphylinidae     292      13.4     6    1,892     86.6    13
Histeridae        433      34.3     4     831      65.7    13
Nitidulidae       312      79.0     1      83      21.0     2
Dermestidae       229      68.8     1     104      31.2     2
Scarabaeidae       9        3       4     291       97     14
Cleridae           74      61.7     1      46      38.3     1
Carabidae          2       2.7      2      73      97.3     6
Trogidae           13      17.3     1      62      82.7     1
Tenebrionidae      35      94.6     6      2       5.4      1
Curculionidae      5       23.8     3      16      76.2     7
Chrysomelidae      3       16.7     2      15      83.3     6
Elateridae         8       100      2      -        -       -
Anobiidae          -        -       -      7       100      1
Erotylidae         3        75      1      1        25      1
Hydrophilidae      3       100      1      -        -       -
Bostrichidae       -        -       -      3       100      1
Mordellidae        -        -       -      2       100      1
Melyridae          -        -       -      1       100      1
Ptiliidae          -        -       -      1       100      1
Total            1,421     29.3    35    3,430     70.7    72

Family                    Total

                   n        %       S

Staphylinidae    2,184    45.02    13
Histeridae       1,264    26.06    13
Nitidulidae       395      8.14     2
Dermestidae       333      6.86     2
Scarabaeidae      300      6.18    15
Cleridae          120      2.47     1
Carabidae          75      1.55     7
Trogidae           75      1.55     1
Tenebrionidae      37      0.76     7
Curculionidae      21      0.43    10
Chrysomelidae      18      0.37     8
Elateridae         8       0.16     2
Anobiidae          7       0.14     1
Erotylidae         4       0.08     1
Hydrophilidae      3       0.06     1
Bostrichidae       3       0.06     1
Mordellidae        2       0.04     1
Melyridae          1       0.02     1
Ptiliidae          1       0.02     1
Total            4,851     100     88

Table 2. Absolute (n) and relative (%) abundance of Coleoptera
species of forensic importance associated to pig carcasses during
dry and rainy seasons in a Caatinga area, State of Paraiba, Brazil.

                                                       Dry season

Family          Species                               n        %

Carabidae       Loxandrus sp.                         1       1.5

                Pterostichus sp.                      -        -

                Carabidae spp. (5)                    1       16.7

Cleridae        Necrobia rufipes (De Geer, 1775)      74      61.7

Dermestidae     Dermestes maculatus De Geer, 1774    229      69.4

                Dermestes haemorrhoidalis             -        -
                Kuster, 1852

Histeridae      Eremosaprinus sp.                     2        50

                Euspilotus azureus                    -        -
                (Sahlberg, 1823)

                Euspilotus sp.                        49      10.6

                Hister punctifer Paykull, 1811        -        -

                Hololepta reichii Marseul, 1853       -        -

                Omalodes foveola Erichson, 1834       -        -

                Phelister sp.                         64      56.1

                Xerosaprinus diptychus               318      96.1
                (Marseul, 1855)

                Histeridae spp. (5)                   -        -

Hydrophilidae   Hydrophilidae sp.                     3       100

Nitidulidae     Stelidota geminata (Say, 1825)       312      79.2

                Nitidulidae sp.                       -        -

Scarabaeidae    Ataenius sp.                          2        50

                Ateuchus carbonarius                  2       1.6
                (Harold, 1868)

                Canthidium manni Arrow, 1913          -        -

                Canthon sp.                           -        -

                Coprophanaeus pertyi                  -        -
                (Olsoufieff, 1924)

                Deltochillum verruciferum             -        -
                Felsche, 1911

                Dichotomius geminatus                 -        -
                (Arrow, 1913)

                Dichotomius nisus (Olivier, 1789)     -        -

                Ontherus digitatus Harold, 1868       1       100

                Onthophagus hirculus                  -        -
                Mannerhein, 1829

                Trichillum sp.                        -        -

                Uroxys sp.                            4       36.4

                Aphodiinae sp. 1                      -        -

                Aphodiinae sp. 2                      -        -

                Melolonthinae sp.                     -        -

Staphylinidae   Acylophorus sp.                       -        -

                Aleochara bonariensis Lynch, 1884     8       7.8

                Atheta iheringi Bernhauer, 1908      177      10.5

                Belonuchus sp. 1                      -        -

                Belonuchus sp. 2                      23      47.9

                Heterothops sp. 1                     1       9.1

                Heterothops sp. 2                     -        -

                Philonthus figulus Erichson, 1840     3       13.6

                Philonthus sp. 1                      -        -

                Philonthus sp. 2                      80      27.2

                Xenopygus analis (Erichson, 1840)     -        -

                Staphylinidae spp. (2)                -        -

Tenebrionidae   Tribolium sp. 1                       13      100

                Tribolium sp. 2                       8       100

                Bolitophagini sp.                     11      100

                Tenebrionidae spp. (4)                3        60

Trogidae        Omorgus suberosus Fabricius, 1775     13      17.3

Total                                               1,402     29.3

                                                      Rainy season

Family          Species                               n        %

Carabidae       Loxandrus sp.                         64      98.5

                Pterostichus sp.                      4       100

                Carabidae spp. (5)                    5       83.3

Cleridae        Necrobia rufipes (De Geer, 1775)      46      38.3

Dermestidae     Dermestes maculatus De Geer, 1774    101      30.6

                Dermestes haemorrhoidalis             3       100
                Kuster, 1852

Histeridae      Eremosaprinus sp.                     2        50

                Euspilotus azureus                   188      100
                (Sahlberg, 1823)

                Euspilotus sp.                       412      89.4

                Hister punctifer Paykull, 1811        82      100

                Hololepta reichii Marseul, 1853       6       100

                Omalodes foveola Erichson, 1834       67      100

                Phelister sp.                         50      43.9

                Xerosaprinus diptychus                13      3.9
                (Marseul, 1855)

                Histeridae spp. (5)                   11      100

Hydrophilidae   Hydrophilidae sp.                     -        -

Nitidulidae     Stelidota geminata (Say, 1825)        82      20.8

                Nitidulidae sp.                       1       100

Scarabaeidae    Ataenius sp.                          2        50

                Ateuchus carbonarius                 127      98.4
                (Harold, 1868)

                Canthidium manni Arrow, 1913          47      100

                Canthon sp.                           1       100

                Coprophanaeus pertyi                  2       100
                (Olsoufieff, 1924)

                Deltochillum verruciferum             13      100
                Felsche, 1911

                Dichotomius geminatus                 25      100
                (Arrow, 1913)

                Dichotomius nisus (Olivier, 1789)     9       100

                Ontherus digitatus Harold, 1868       -        -

                Onthophagus hirculus                  22      100
                Mannerhein, 1829

                Trichillum sp.                        27      100

                Uroxys sp.                            7       63.6

                Aphodiinae sp. 1                      3       100

                Aphodiinae sp. 2                      5       100

                Melolonthinae sp.                     1       100

Staphylinidae   Acylophorus sp.                       1       100

                Aleochara bonariensis Lynch, 1884     94      92.2

                Atheta iheringi Bernhauer, 1908     1,508     89.5

                Belonuchus sp. 1                      2       100

                Belonuchus sp. 2                      25      52.1

                Heterothops sp. 1                     10      90.9

                Heterothops sp. 2                     4       100

                Philonthus figulus Erichson, 1840     19      86.4

                Philonthus sp. 1                      10      100

                Philonthus sp. 2                     214      72.8

                Xenopygus analis (Erichson, 1840)     2       100

                Staphylinidae spp. (2)                3       100

Tenebrionidae   Tribolium sp. 1                       -        -

                Tribolium sp. 2                       -        -

                Bolitophagini sp.                     -        -

                Tenebrionidae spp. (4)                2        40

Trogidae        Omorgus suberosus Fabricius, 1775     62      82.7

Total                                               3,384     70.7

                                                         Total

Family          Species                               n        %

Carabidae       Loxandrus sp.                         65      1.36

                Pterostichus sp.                      4       0.08

                Carabidae spp. (5)                    6       0.13

Cleridae        Necrobia rufipes (De Geer, 1775)     120      2.51

Dermestidae     Dermestes maculatus De Geer, 1774    330      6.90

                Dermestes haemorrhoidalis             3       0.06
                Kuster, 1852

Histeridae      Eremosaprinus sp.                     4       0.08

                Euspilotus azureus                   188      3.93
                (Sahlberg, 1823)

                Euspilotus sp.                       461      9.63

                Hister punctifer Paykull, 1811        82      1.71

                Hololepta reichii Marseul, 1853       6       0.13

                Omalodes foveola Erichson, 1834       67      1.40

                Phelister sp.                        114      2.38

                Xerosaprinus diptychus               331      6.92
                (Marseul, 1855)

                Histeridae spp. (5)                   11      0.23

Hydrophilidae   Hydrophilidae sp.                     3       0.06

Nitidulidae     Stelidota geminata (Say, 1825)       394      8.23

                Nitidulidae sp.                       1       0.02

Scarabaeidae    Ataenius sp.                          4       0.08

                Ateuchus carbonarius                 129      2.70
                (Harold, 1868)

                Canthidium manni Arrow, 1913          47      0.98

                Canthon sp.                           1       0.02

                Coprophanaeus pertyi                  2       0.04
                (Olsoufieff, 1924)

                Deltochillum verruciferum             13      0.27
                Felsche, 1911

                Dichotomius geminatus                 25      0.52
                (Arrow, 1913)

                Dichotomius nisus (Olivier, 1789)     9       0.19

                Ontherus digitatus Harold, 1868       1       0.02

                Onthophagus hirculus                  22      0.46
                Mannerhein, 1829

                Trichillum sp.                        27      0.56

                Uroxys sp.                            11      0.23

                Aphodiinae sp. 1                      3       0.06

                Aphodiinae sp. 2                      5       0.10

                Melolonthinae sp.                     1       0.02

Staphylinidae   Acylophorus sp.                       1       0.02

                Aleochara bonariensis Lynch, 1884    102      2.13

                Atheta iheringi Bernhauer, 1908     1,685    35.21

                Belonuchus sp. 1                      2       0.04

                Belonuchus sp. 2                      48      1.00

                Heterothops sp. 1                     11      0.23

                Heterothops sp. 2                     4       0.08

                Philonthus figulus Erichson, 1840     22      0.46

                Philonthus sp. 1                      10      0.21

                Philonthus sp. 2                     294      6.14

                Xenopygus analis (Erichson, 1840)     2       0.04

                Staphylinidae spp. (2)                3       0.06

Tenebrionidae   Tribolium sp. 1                       13      0.27

                Tribolium sp. 2                       8       0.17

                Bolitophagini sp.                     11      0.23

                Tenebrionidae spp. (4)                5       0.10

Trogidae        Omorgus suberosus Fabricius, 1775     75      1.57

Total                                               4,786     100
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Title Annotation:Original Article
Author:Santos, W.E.; Alves, A.C.F.; Creao-Duarte, A.J.
Publication:Brazilian Journal of Biology
Date:Aug 1, 2014
Words:5017
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