Identification guide of dung beetle species (Coleoptera: Scarabaeidae: Scarabaeinae) of the Brazilian Pantanal

Abstract The Pantanal is the largest seasonal freshwater wetland on Earth, characterized by the seasonal flooding and complex mosaic vegetation, which determines its biodiversity. Among this biodiversity, dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) are a group of insects that perform important ecological functions, such as: nutrient cycling, seed dispersion and parasite control. In order to mitigate the lack of information on dung beetle fauna of the Brazilian Pantanal, we conducted a bibliographic search of virtually all literature published until november-2020 on dung beetles sampled in the Pantanal. In addition, we had accessed to the records the largest collection of the dung beetle species from Brazilian Pantanal. We recorded 68 dung beetle species of 30 genera. The genera Canthon Holffmanseg 1847 is the most diverse with 13 species recorded. Although our knowledge about the dung beetle fauna in this ecosystem is still incipient, our results demonstrated a high richness of dung beetles in the Brazilian Pantanal. In addition, our study provides first list of dung beetle species and an illustrated dichotomy key to identify genera and some species occurring in the Brazilian Pantanal. Thus, the use of this guide for identification of dung beetle species and a list of species can be important tools to help researchers and provide incentive for new inventories on dung beetle fauna in the Brazilian Pantanal.


Introduction
The Pantanal is the largest seasonal freshwater wetland on Earth (ca.160,000 km 2 ), and also considered a World Heritage Site and Biosphere Reserve (UNESCO, 2000).This extensive wetland is located in Brazil (states of Mato Grosso and Mato Grosso do Sul) with approximately 130,000 km 2 , 15,000 km 2 in Bolivia and 5,000 km 2 in Paraguay (Cunha et al. 2014) and has a vegetation system arranged in a mosaic (i.e., different plant communities scattered side-by-side across space) (Pott et al. 2011).Furthermore, two well-defined ecohydrology cycles can be identified in the Pantanal: dry and rainy.In the dry season, the surface water becomes scarce, being restricted to the perennial rivers (with defined beds) and large ponds (Alho & Sabino 2011;Nunes et al. 2014).Thus, the seasonal flooding and complex mosaic vegetation determine a biodiversity unique adapted to Brazilian Pantanal (Junk et al. 2006;Tomas et al. 2019).
Among this biodiversity, insects, such as dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae), are essential for the maintenance of ecosystem functioning in the Brazilian Pantanal (Correa et al. 2020).Dung beetles are broadly distributed and highly diverse taxonomically and functionally (Halffter & Edmonds 1982;Hanski & Cambefort 1991).They are represented by more than 6,837 species worldwide which belong to 278 genera (Schoolmeesters 2023).Their feeding behavior is quite varied, most species being coprophagous, but there are also species that feed on decaying carcasses, fungi and fruits, and can even be predators or generalists (Halffter & Matthews 1966).They can be classified into three functional groups based on food allocation behavior and/or nesting behavior: (1) roller (telecoprid) species that remove portions of dung, which are rolled away from the food resource and then buried; (2) tunneler (paracoprid) species that construct tunnels below or adjacent to the food resource and transport dung into them; and (3) dweller (endocoprid) species that nest within a dung pad and do not exhibit resource allocation (Halffter & Matthews 1966;Hanski & Cambefort 1991).
When dung beetles bury food resources (e.g.feces, carcass and fruits), they provide important ecological functions and services in natural and anthropogenic ecosystems, such as: increased water infiltration and soil porosity, improved herbaceous plant growth, reduction of livestock gastrointestinal parasite and dung-fly availability (Nichols et al. 2008) and greenhouse gas emissions from dung pats (Slade et al. 2016;Piccini et al. 2017).In addition, these beetles have been widely used as both ecological and biodiversity indicators because they are sensitive to natural and anthropogenic changes (Halffter & Favila 1993;McGeoch et al. 2002;Nichols et al. 2007), are easily sampled with standardized protocols (Correa et al. 2018;Gardner et al. 2008;da Silva & Hernández 2015) and are diverse and relatively well characterized taxonomically (Vaz-de-Mello et al. 2011).
Although studies on dung beetle assemblages have been growing recently in the Brazilian Pantanal (Tissiani et al. 2015;Daniel & Vazde-Mello 2016, Pessôa et al. 2017;Correa et al. 2016Correa et al. , 2019Correa et al. , 2020Correa et al. , 2021Correa et al. , 2022a, b;, b;Correa & da Silva 2022, Gonçalves et al. 2022), our knowledge on dung beetle fauna in this biome is incipient.Indeed, the Pantanal is one of the least known ecosystems in terms of biodiversity of Brazil (Lewinsohn et al. 2005).Therefore, new inventories of dung beetles in different localities are essential to increase new records of dung beetle species in the Brazilian Pantanal.In this study, we bring a list of dung beetle species of the Brazilian Pantanal and an illustrated identification key.

Material and Methods
We used the Scopus and Web of Science databases to search for literature on the dung beetles in the Brazilian Pantanal, following the PRISMA methodology (Moher et al. 2009), which only considers indexed articles.The following search terms were used: (("Dung beetle*" OR "Scarabaeinae*" OR "coprophagous beetles*") AND ("Wetland*" OR "Pantanal*" OR "humid zones")).We complemented the taxonomic diversity search by including articles published in Portuguese from the authors' collection.The search window of time covered articles published between January 2007 to November 2020.
Our search returned 40 articles, regarding dung beetle species in wetlands.The relevant articles were selected using the following criteria: i) the study includes species from Scarabaeinae subfamily, ii) the study is based partly or entirely in Brazilian Pantanal (e.g., Mato Grosso and Mato Grosso do Sul states).Under these criteria, 10 articles were retained for data extraction (e.g.Louzada et al. 2007;Rodrigues et al. 2010;Tissiani et al. 2015;Daniel & Vaz-de-Mello 2016;Pessôa et al. 2017;Vaz-de-Mello et al. 2017;Correa et al. 2016Correa et al. , 2019Correa et al. , 2020)), only species identified at a specific level were considered.In addition, 10 genera have been added to the identification key that have a good chance of being collected in the Brazilian Pantanal region (Vaz-de-Mello personal communication).The genera that are under taxonomic revision are not included in the identification keys with their respective species that occur in the Pantanal.
All previously existing records were reviewed for their identifications (when possible, we used specimen vouchers) for correct species identification.We also list the records of the Entomology Section of the Zoological Collection at the UFMT (CEMT, curator F. Z. Vaz-de-Mello).Currently, it is considered one of the most important collections of dung beetles in the world, with specimens from all regions of Brazil and across the globe, making it possible to assemble a list of species from the different Brazilian biomes (Tissiani et al. 2017).The dung beetle species mentioned in the present study are classified according to their nesting behavior, following the classification by Hanski & Cambefort (1991).
Finally, an identification key was constructed to identify the genera and species of dung beetles present in Brazilian Pantanal.Its main structure from Vaz- de-Mello et al. (2011), and this was refined based on the analysis of the external morphology of the species, includingwhere necessary -the secondary sexual characteristics.
Leica M205A stereomicroscope coupled with a Leica DMC4500 and a Leica Application Suite V4.10.0 Interactive Measurements, Montage was used for the photos.

Discussion
In this study, we provide an updated list of species of dung beetles of the Brazilian Pantanal.No such list had hitherto been published.The closer parallel had been Vaz- de-Mello et al.'s (2017) list of the species of Mato Grosso do Sul state, which indicated those which were present in its Pantanal area.Our study mitigates the lack of information on dung beetles species of the Brazilian Pantanal as a whole, increasing the number of species recorded from 43 (see Vaz-de-Mello et al. 2017) to 68 species (Figure 64A-P and Figure 65A-J).Below is an up-todate commentary on the taxonomic status of the genera that occur in the Pantanal.
Ateuchus Weber, 1801: Genus with paracoprid representatives and 101 species currently recognized as valid distributed in the Americas (Schoolmeesters 2023).Except for some regional works, the genus was last revised by Harold (1868) and identifying its South American species is currently unfeasible relying on published information.During the data survey for this work, these species were reported: Ateuchus carbonarius (Harold, 1868) (Pessôa et al. 2017), Ateuchus latus (Boucomont, 1928) (Vaz-de-Mello et al. 2007), and Ateuchus pruneus (Boucomont, 1928) (Correira et al. 2022b).However, this genus is under revision and only one species could be confirmed as present in the Brazilian Pantanal: Ateuchus aff.viduus (Blanchard, 1846), a species with wide distribution in the Pantanal and southern Cerrado regions (Mario Cupello, personal communication).
Canthon Hoffmannsegg, 1817: It is one of the most diverse genera among the Scarabaeinae, exclusive to the Americas, with currently 163 recognized species (Schoolmeesters 2023).Its distribution ranges from the United States to Uruguay and central-west Argentina, with representatives in all biomes along this range.This genus is divided into nine subgenera, some of which are under revision (Cupello & Vaz-de-Mello 2018 and references cited therein).Overall, their representatives are telecoprids, and may be generalists and predators.In this study, we recorded 13 species: C. chalybaeus Blanchard, 1846, C. curvodilatatus Schmidt, 1920, C. daguerrei Martínez, 1951, C. edentulus Harold, 1868, C. histrio Vaz-de-Mello (2022), in the revision of the genus Tetraechma Blanchard, 1842, two species of Canthon that were reported for the Brazilian Pantanal were transferred to the genus Tetraechma.They are: Canthon apicalis Lucas, 1859 and Canthon lituratus solutus Schmidt, 1920.
Digitonthophagus Balthasar, 1959: An Afro-Asian genus, with 16 species (Genier & Moretto 2017).A species of African origin, Digitonthophagus gazella (Fabricius, 1787), was introduced in Brazil in the 1980s and is currently present in almost the entire national territory (Tissiani et al. 2017;Génier & Moretto 2017).This species is mainly associated with exotic pastures (e.g., African grasses; Urochloa spp.).It benefits from the presence of cattle ranching (Correa et al. 2020), and its occurrence is rare in areas of native vegetation.This species has a high rate of dispersal and fertility and is rapidly established in environments with high solar incidence, including savanna environments and pastures in the Amazon region (Matavelli & Louzada 2008).

Figure 27 .
Figure 27.(A-B) Canthididium sp.apical internal angle of the protibial and mesosternum; (C-D) Ontherus sp apical internal angle of the protibial and mesosternum apical internal angle of the protibial and mesosternum.Scale: A-D, 1mm.

Figure 32 .
Figure 32.(A) E. parallelus.Dorsal body without any metallic luster.Elytra apex bristles straight.Size 9-14mm; (B) E. aeneus.Body dorsally with metallic sheen at least in the elytral sutural striae and anterior part of the clypeus.Bristles at apex of elytra strongly curved in apical half.Scale: A-B, 1mm.

Figure 33 .--
Figure 33.(A) E. nigrovirens.Head surface with most no metallic reflections, except for a narrow metallic green band anteriorly on the clypeus; (B) E. aeneus.Head surface mostly glossy and with strong metallic reflections between ocellates; (C) E. nigrovirens.Lateral edge of male hind tibia curved in half in dorsal view; (D) E. aeneus.Lateral edge of male hind tibia almost straight or straight in the middle in dorsal view.Scale: A-B, 1mm.

Figure 36 .
Figure 36.(A) C. mutabilis.Pronotum in dorsal view, with straight lateral margin and serrated in ventral view; (B) C. curvodilatatus.Pronotum with straight lateral margin, in dorsal and ventral view.Scale: A-B, 1mm.

Figure 56 .
Figure 56.(A) O. appendiculatus.Abdominal sternites medially set, bristles similar to those on the lateral aspect of the metasternum; (B) O. aphodioides.Abdominal sternites glabrous medially, with at most one row of short bristles along the posterior border of the metacoxa.Scale: A-B, 1mm.

Figure 57 .
Figure 57.(A-B) O. appendiculatus.Posterior border of metacoxa smooth.Metasternum with most of the punctuation of the oval lateral edges, with little defined edges; (C-D) O. azteca.Posterior edge of metacoxa slightly serrated.Metasternum with most of the punctuation of the lateral edges rounded, clearly delimited.Scale: A-D, 1mm.

Figure 63 .
Figure 63.(A) D. icaroides, Pronotum and elytra of the same color, dark with greenish reflections; (B) D. cupreicoile, Pronotum yellow with dark spot in the center, elytra of uniform dark coloration.Scale.A-B, 1mm.