Dung beetles of Brazilian pastures and key to genera identification ( Coleoptera : Scarabaeidae )

The objective of this work was to elaborate supporting tools for the correct identification of Scarabaeidae, by an identification key of genera, and a commented list of the species present in Brazilian pastures. A data survey was performed on the specimens deposited in the main Brazilian collection and reported on the recent scientific literature. The distribution of the species was identified in the Brazilian states, based on information on feeding preference, ecological aspects, and potential for faeces removal action. The species were classified according to their importance for pastures, as: high, medium, and low. A key for the identification of the genera and subgenera of Scarabeidae present in the pastures was constructed through the analysis of the external morphology of the species and, when needed, by the analysis of sexual traits. Twenty genera and 76 species of scarab beetles were recorded for Brazilian pasturelands, among which Dichotomius bos, Dichotomius nisus, Trichillum externepunctatum, Ontherus appendiculatus, Onthophagus aff. hirculus, and Digitonthophagus sp. were considered as the most frequent, widely distributed, abundant, and important. The dichotomous key will contribute to the identification of the genera and subgenera of dung beetles (Scarabaeidae: Scarabaeinae) occurring in the Brazilian pastures.


Introduction
Deposition of manure across pastures and the occurrence of parasitic Diptera are among the main ecological problems caused by the introduction of cattle in several regions of the planet.These problems are most intense where there have been losses of herbivorous mammals from the native megafauna, such as those occurring in South America and Australia (Waterhouse, 1974;Halffter, 1991;Nichols et al., 2008;Vieira et al., 2008).
This deposition of manure, which can accumulate on the pastures' grasses, causes the reduction of green matter available for feeding the animals.Part of the leaves are unable to survive the shade, and some become unpalatable to the cattle (Waterhouse, 1974).
Another problem caused by the deposition of fecal matter in pastures is the proliferation of parasitic insects and worms that use bovine manure as a substrate to complete their life cycle (Waterhouse, 1974;Flechtmann et al., 1995a;Nichols et al., 2008;Vieira et al., 2008).The fecal matter deposited in pastures is also used by scarab beetles (Coleoptera: Scarabaeidae), which are commonly called dung beetles, as they dismantle the fecal matter, mold portions of the feces into a spherical shape, and transport it to burrows excavated in the soil (Halffter & Matthews, 1966).While burying portions of feces, the dung beetles bury other insects and fecal worms together, which are harmful to the herds (Flechtmann et al., 1995a;Louzada & Silva, 2009;Ridsdill-Smith & Edwards, 2011).
Elaborate nesting, associated with the broad geographical distribution and high biomass of many of its species, and the greater number of coprophagous species than other Coleoptera families, make scarab bettles the most important Brazilian coprophagous beetles (Louzada & Silva, 2009).
In Brazil, concern about the advance of the horn fly (Haematobia irritans Linnaeus, 1758) caused Embrapa to introduce, at the end of the 1980s, the Afro-Asian beetle Digitonthophagus gazelle (Fabricius 1787), an important agent in the control of H. irritans (Bianchin et al., 1998;Matavelli & Louzada, 2008).This introduction followed the model previously adopted in other parts of the world (Noriega et al., 2010).At the time, there were no studies on the native fauna of coprophagous beetles of Brazilian rural environments, which corroborated the decision to introduce this exotic species (Vaz-de-Mello, 2000).Existence of wellstructured native communities of dung beetles, which efficiently perform the service of the dismantling and removal of fecal matter, is now recognized in all biomes of the country (Louzada & Silva, 2009).
The number of species present in pastures is regionally affected by the composition of the original vegetation, the time the pastures take to form, their isolation, grass composition, stability and environmental complexity (Almeida et al., 2011).The species of dung beetles present in rural vegetation are numerically and qualitatively different between native and cultivated grasslands (Almeida et al., 2011).Few species are present in all Brazilian biomes, which is indicative that they should be the focus of research in biological control and other services provided by dung beetles in pastures.However, a number of species occur in virtually all types of rural compositions in the country and, therefore, are considered to be of high importance to these environments.Considering, at least, 100 years of inventory of the Scarabaeidae species in the country and the proven efficacy of the inclusion of dung beetles as important biological agents in agropastoral systems, this study became necessary.
The objective of this work was to elaborate supporting tools for the correct identification of Scarabaeidae, by an identification of key genera, and a commented list of the species present in Brazilian pastures.

Materials and Methods
Specimens of coprophagous Scarabaeidae, deposited in the sector of entomology of the zoological collection of Universidade Federal de Mato Grosso, were examined between January 2012 and November 2015.This collection is a reference for Scarabaeidae in Brazil and has duplicates of published specimens (Vieira et al., 2008;Almeida & Louzada, 2009;Costa et al., 2009;Louzada & Silva, 2009).Currently, it is considered quantitatively and qualitatively the largest and most important collection of dung beetles in the country, with specimens from all regions of Brazil and across the globe, making it possible to assemble a list of Brazilian species.
In addition, a literary review of articles published up to November 2015 was carried out in scientific journals (Table 1).From the list of species, it was possible to identify their distribution in the Brazilian states, and information on food preference, ecological aspects, and potential for fecal removal action was added according to classification criteria described by Halffter & Matthews (1966).
Species were classified into high, medium and low importance for pastures.The dung beetles considered highly important, were those most functionally important in Brazilian pastures due to their burial habits and species size.Species with restricted distribution, but with high regional importance, were classified as of medium importance, because they were found with a high number of individuals or with a high body mass.The species of low importance are present in local distribution or low abundance, often with little or totally unknown biology, or with diverse eating and ecological habits, but that eventually frequent the feces in pastures.
From Vaz- de-Mello et al. (2011) and based on the analysis of the external morphology of the species, including -where necessary -the sexual characters, a key was constructed to identify the genera and subgenera of scarab beetles present in Brazilian pastures.

Results and Discussion
Brazilian dung beetle fauna is composed of 716 species and 61 subspecies described so far, belonging to 63 genera (Vaz-de-Mello, 2015).Most of them are associated with forest formations.In the almost 23% of Brazilian territory covered by pastures, only 20 genera and 76 species of dung beetles were recorded, were considered to be of high importance for these environments, since they present a wide distribution and greater body biomass and, potentially, remove the greatest amount of manure to the interior of the soil.Six species were considered of medium importance (Table 2), and 64 species of low importance (Table 3).
The following list of dung beetle genera present in Brazilian pastures were highlighted from the evaluated data, with comments detailing the main species within this environment: Agamopus Bates, 1887 -this genus has four described species, two of which from Brazilian pastures (Halffter & Martínez, 1968), and has at least one new species.Which species that occur in pastures are copronecrophagous and appear to exhibit oviposition behavior in other Scarabaeidae nests of the genera Dichotomius, Isocopris, and Ontherus (Vazde-Mello, 2007) (Table 3, Figure 1).
Ateuchus Weber, 1801 -a highly specious genus, and in urgent need of taxonomic revision, with over than 80 described species, of varied forms, habits and habitats.They often occur with a high number of individuals (Table 3).
Canthidium Erichson, 1847 -a genus with more than 150 species, and an urgent need for taxonomic revision.It presents species of medium and low importance for pastures, among them Canthidium decoratum Perty, 1830, considered an indicator of Cerrado and Canthidium marseuli Harold, 1867, an indicator of native pastures (Almeida &Louzada, 2009) (Tables 2  and 3; Figure 2).
Canthon Hoffmannsegg, 1817 -a genus with over 160 species currently valid, 13 of which were recorded in Brazilian pastures.From species that are widely distributed across pastures all over the country, such as the Canthon mutabilis Lucas, 1857, to species present exclusively in high altitude fields (above 800 m), in Cerrado and Atlantic Forest transition areas, like the Canthon corpulentus Harold, 1868, erroneously cited as Canthon lamproderes Redtenbacher, 1867 according to Vaz- de-Mello et al. (2013).The species Canthon cyanescens Harold, 1868 -erroneously referred to in literature as Canthon latipes (Blanchard, in Blanchard & Brullé, 1845) -and Canthon nigripennis Lansberge, 1874 were eventually observed in pastures near forests and clearings (Table 3; Figure 1).
Deltochilum Eschscholtz, 1822 -a genus with about 90 valid species (Génier, 2012).Deltochilum elevatum Castelnau, 1840 is associated with natural grasslands from Rio Grande do Sul to the Southeast, including grasslands of altitudes above 1,000 m in Minas Gerais (Table 3 and Figure 2).Other native species of the Cerrado and high altitude fields do not seem to be associated with excrement in the pastures.
Diabroctis Gistl, 1857 -a genus with only three species.Diabroctis mimas (Linnaeus, 1758) is collected in practically all of Brazil and in neighboring countries.
It is present from pastures and areas of Cerrado to areas with fragmented forest, in different successive stages of Atlantic Forest, up to 200 m altitude (Gillett et al., 2010) (Table 3 and Figure 2).
Dichotomius Hope, 1838 -a genus with roughly 170 valid species (Nunes & Vaz-de-Mello, 2013), of which 17 are frequent in Brazilian pastures.In general, these species are important because of their high body mass and efficient burial activities of fecal masses in the soil.Two species are considered of great importance for pastures: Dichotomius bos (Blanchard, in Blanchard & Brullé 1845), frequently cited as Dichotomius anaglypticus (Mannerheim, 1829) in the 1990s (Flechtmann et al., 1995a(Flechtmann et al., , 1995b(Flechtmann et al., , 1995c(Flechtmann et al., , 1995d)), is in pastures throughout Brazil and in bordering countries (in and around the Chaco Depression); and Dichotomius nisus (Olivier, 1789), more widely distributed than D. bos, is present in the Brazilian Cerrado and Caatinga regions, entering areas of savannah, pastures, Amazonian riverbanks and in the Llanos of Colombia and Venezuela, up to the north of Roraima.The other 15 species have restricted distribution or a preference for forested environments and, although they frequent pastoral environments, are considered of medium and low importance for pastures (Tables 2 and 3, and Figures 2 and 3).(Boucomont, 1928) MS PR ( 6) RS ( 6) SC (6)   (1) Eventually collected on pasture.
A species of African origin, erroneously identified as Digitonthophagus gazella (Fabricius, 1787) (at the time considered in the genus Onthophagus), was  high solar incidence, including savannas and pastures in the Amazon Region (Matavelli & Louzada, 2008) (Figure 3).There is still uncertainty about the identification of this species present in Brazil, thus it was treated here as simply Digitonthophagus sp.
Eurysternus Dalman, 1824 -in the last review of the genus, conducted by Génier (2009), 53 species were recognized, six of them occurring in pastures in Brazil.Most of the species appear to be associated with forested environments, but with a tolerance to different degrees of anthropization, which allows their collection in pastures adjacent to fragments of forest (Table 3 and Figure 3).
Genieridium Vaz-de-Mello, 2008 -of the seven species described in this genus, Genieridium bidens (Balthasar, 1938) and Genieridium cryptops (Arrow, 1913) are commonly caught in pastures in areas of the Cerrado and Chaco.Other species are also associated with natural grasslands and other nonforested phytophysiognomies of the Cerrado, but, in general, with natural vegetation (Vaz-de-Mello, 2008) (Table 3).
Ontherus Erichson, 1847 -in the most recent review of this genus, 59 species were recognized (Génier, 1996).The majority of them are distributed between the Southeast of Brazil and the Andes mountain range.The species Ontherus appendiculatus (Mannerheim, 1829) is considered of great importance for Brazilian pastures and is in the pastures and grasslands throughout the whole of Brazil.In the extreme north of the Amazon, this species also occurs in forested areas, but in other localities, it eventually frequents forests adjacent to pastures, small fragments of forest or secondary regeneration forests and sand dunes.Ontherus sulcator Fabricius, 1775 was also found in pastures and across the whole Chaco depression, where this species can also be considered of high importance.
In other areas, in the rest of the country, O. sulcator is less common than O. appendiculatus (Table 3, and Figures 3 and 4).
Onthophagus Latreille, 1802 -a genus with about 2,000 species distributed worldwide.The South American species are in urgent need of taxonomic revision.At least three species of the group hirculus are commonly present in the pastures.This group is currently under review.Onthophagus hirculus Mannerheim, 1829, considered to be of high importance for pastures, but is probably a number of species considered together.Originally described in the municipality of Diamantina, in the state of Minas Gerais, Brazil, this species belongs to a complex of closely related species that are distributed throughout grasslands and other phytophysiognomies, with low cover or without canopy cover, throughout the country, including clearings and the borders of Amazonian rivers (Table 2 and 3; Figure 4).
Phanaeus MacLeay, 1819 -a genus with 54 valid species (Edmonds & Zídek, 2012).Two of them are inhabitants of the grasslands and savannas of Brazil and are eventually collected in cultivated pastures (Edmonds, 1994) (Table 3 and Figure 4).
Pseudocanthon Bates, 1887 -a genus with nine described species, two of them found in Brasil, but which seem to represent a complex of species in need of revision (Padilla-Gil & Halffter, 2007;França et al., 2016).Only species associated with Pseudocanthon xanthurus (Blanchard, in Blanchard & Brullé, 1845) are usually collected in pastures, clearings, natural fields, and other nonforested areas throughout the country (Table 3 and Figure 4).
Trichillum Harold, 1868 -to date, this genus has 11 valid species (Vaz-de-Mello, 2008).Unlike most other Scarabaeinae, species of this genus usually remain within the excrement, where they feed and lay their eggs freely (Vaz-de-Mello, 2008;López-Alarcón et al., 2009).The species Trichillum externepunctatum Preudhomme de Borre, 1880 is, on average, 3 mm in length and contributes to the destruction of bovine excrement in pastures, due to the high population that usually occurs in faecal pads.This species is considered of great importance for the pastures, it frequents the nonforested phytophysiognomies areas and anthropized environments -from the south of the Amazon to southern Uruguay -and is bordered to the west by the Andes.Trichillum externepunctatum is the most common species of the genus and coincides geographically with all the other species considered of great importance to the pastures (Vaz-de-Mello, 2008;López-Alarcón et al., 2009) (Table 3 and Figure 4).
Uroxys Westwood, 1842 -most of the 60 valid species are present in forested environments.It features size and ecological functions similar to those of the genus Trichillum (Vaz-de-Mello, 2008;Korasaki et al., 2012) (Table 3).
From the survey conducted, a dichotomous key was developed to contribute to the identification of the genera and subgenera of dung beetles (Scarabaeidae, Scarabaeinae) which occur in the pastures of Brazil.In addition to the species cited and classified according to the degree of their importance, it is possible that on a regional scale, others may be collected, whether or not they frequent bovine feces.In order for these genera not to be left unidentified or to be erroneously identified, all genera with this characteristic were added to the key as follows: Anisocanthon, Anomiopus, Besourenga, Bolbites, Degallieridium, Dendropaemon, Gromphas (Figure 3), Holocanthon, Isocopris, Malagoniella, Oxysternon, Sylvicanthon, and Vulcanocanthon.4. Proleg with trochanto-femoral anterior pit (trochanto-femoral pit is situated in the apical border of trochanter).Length always less 7 mm.5 4' (1').Proleg lacking trochanto-femoral anterior pit.Variable length.12 5 (4).Last abdominal sternite not grossly enlarged, all sternites clearly visible medially.6 5'.Last abdominal sternite greatly expanded medially such that remaining sternites visible only laterally.7 6 (5).Pronotum lacking longitudinal lateral sulcus.Pygidium divided by median discal transverse sulcus.Agamopus Bates, 1887 6'.Side of pronotum with deep longitudinal sulcus.Pygidium lacking median discal sulcus (sometimes basal sulcus sinuated and invading base of disc, but if so, the sulcus is clearly continuous to that one in the base).Uroxys Westwood, 1842 7 (5').Pseudepipleuron expanded twice laterally, posterior expansion partially covering epipleuron and often angulate.Trichillum Harold, 1868 7'.Pseudepipleuron at most with single anterior expansion that never covers the epipleuron.Epipleuron sometimes excavated near metacoxa.8 8 (7').Pseudepipleuron abruptly narrowed posteriorly, distinctly angulate at the level of the metacoxa.9 8'.Pseudepipleuron gradually narrowed posteriorly, not angulate at the level of the metacoxa.10 9 (8).Clypeogenal suture clearly indicated and extending completely to the outer head border frontoclypeal suture distinct, at leastlaterally.Head border incised at junction with clypeogenal suture such that clypeus and gena appear separately rounded.Eutrichillum Martínez, 1969 9'.Frontoclypeal and clypeogenal sutures indistinct; head margin straight or slightly curved at juncture of clypeus and gena.Besourenga Vaz- de-Mello, 2008 10 (8').Dorsal portion of eyes very small and narrow, separated by at least 10 times width.Maximum eyes width less than one-third length.Pseudoepipleuron not twisted longitudinally; with row of setae at least along posterior two-thirds.Length greater than 3.5 mm.Genieridium Vaz-de-Mello, 2008 10'.Dorsal portion of eye separated less than seven times width.Maximum eyes width least half eye length.Pseudoepipleuron glabrous, twisted longitudinally, anterior one-half approximately vertical, posterior one-half approximately horizontal.Length less than 3 mm.11 11 (10').Hipomeron with posterior, longitudinal carinae.Elytral interstriae evenly flattened, discal interstriae with single row setigerous punctures.Leotrichillum Vaz- de-Mello, 2008 11'.Hipomeron lacking posterior carinae.Elytral interstriae distinctly convex apically.Discal interstriae with double row of punctures, only one row of which setigerous.Degallieridium Vaz- de-Mello, 2008 12 (4').Length less than 13 mm and protibia with four teeth.Length of basal metatarsomere longer than that of following three tarsomeres combined; if subequal, then labial palpi with only two palpomeres (rarely third very reduced), the second one longer than the first.Metatarsus with five tarsomeres.Male, generally, with two horns at vertex; females with frontoclypeal and transverse carinae at vertex.13 12'.Other characters variable.Length less than 13 mm, protibia with four teeth or coloration dark.Length of basal metatarsomere less than combined length of following three tarsomeres; if subequal, then labial palpi with three distinct palpomeres, length of third palpomere at least one-half that of the second, and the second palpomere shorter than the first; or metatarsus with fewer than five tarsomeres.14 13 (12).Length greater than 8 mm, robust body with sides distinctly convex.Pronoto uniformly metallic coloration, pronotum evenly metallic, cupreous or greenish reflex, variegated elytra with brown spots.Hipomeron with oblique carina reaching lateral margin at anterior angle and forming rounded tooth in maleor sharp tooth in female; male with a strong internal apical tooth in protibia, strongly curved downwards at apex (African specie introduced

Conclusions
1.The dichotomus key of dung beetles genera and subgenera contributes to identify the insects that occur in Brazilian pastures and their potential to the biological control of parasites that develop in bovine dung pats.

Table 1 .
Geographic localization, sampling method and information sources of Brazilian coprophagous Scarabaeidae in pastures, used to obtain the distribution of these species in the Brazilian territory.Onthophagus aff.hirculus, and Digitonthophagus sp.

.
Onthophagus buculus Mannerheim, 1829 and close species Similar to O. hirculus, originally described in the municipality of Diamantina, in the state of Minas Gerais, region, and associated with pastures and natural fields of Cerrado.Several species under this name require urgent revision.
Onthophagus ranunculus Arrow, 1913 and close species Described as originating in municipality of Natal, in the state of Rio Grande do Norte; close associated to Caatinga and coastal savannas of the Northeast.At least one closely specie occurs in central part of Brazilian Cerrado.This close specie is mistakenly identified as Onthophagus rubrescens Blanchard, 1846, in Louzada & Silva (2009).

Table 3 .
Dung beetle species (Coleoptera: Scarabaeidae: Scarabaeinae) classified as low importance that occur in Brazilian pastures.
pastures surrounded by fragments of Atlantic Forest or in degraded areas from sea level up to about 1,300 m altitude(Almeida & Louzada, 2009; Rossini & Vazde-Mello, 2015)(Table