JOURNAL OF NATURAL HISTORY, 2016 VOL. 50, NOS. 17–18, 1159–1173 http://dx.doi.org/10.1080/00222933.2015.1103909

Biotic components of dung (Insecta: Coleoptera: : ) from Pantanal – Cerrado Border and its implications for Chaco regionalization Gimo Mazembe Daniela,b and Fernando Z. Vaz-de-Melloc,d aPós-graduação em Entomologia e Conservação da Biodiversidade, Universidade Federal da Grande Dourados, Dourados, Brasil; bCurso de Biologia, Departamento de Ciências Naturais, Universidade Pedagógica de Moçambique, Nampula, Moçambique; cDepartamento de Biologia e Zoologia, Universidade Federal de Mato Grosso, Instituto de Biociências, Cuiabá, Brasil; dFellow of the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

ABSTRACT ARTICLE HISTORY We use a panbiogeographical approach to determine the distribu- Received 30 August 2014 tion pattern of dung beetles from a border region between Accepted 30 September 2015 Cerrado and Rondônia biogeographical provinces in . We Online 16 December 2015 constructed 54 individual tracks and 12 generalized tracks. The KEYWORDS generalized tracks infer historical events that have happened in Distribution pattern; the past, highlighting the significant role of vicariant processes southern Rondônia province; and their influence on the current distribution pattern of dung historical biogeography; new beetles from the Pantanal–Cerrado Border. The study region is a biogeographical district; biogeographical node, including representatives from different panbiogeography biogeographic origins. Contrary to previous suggestions, the Scarabaeinae fauna of southern Rondônia province is not related to Amazonian fauna. Rather, it shows stronger connections with Chaco. Hence we suggest the inclusion of the southern part of the province of Rondônia, representing the Pantanal depression itself, as a new biogeographical district within Chaco province.

Introduction Biodiversity is not evenly distributed on the earth. The distribution patterns of species

Downloaded by [University of Cambridge] at 05:24 08 April 2016 are strongly influenced by historical processes (Halffter 1991). Two approaches have dominated studies of the historical biogeography of continental biotas. The first con- cerns intercontinental waves: dispersal followed by adaptive radiation into the non- colonized niches of the continent (Mayr 1944; Darlington 1957; Simpson 1965; Cracraft 1972, 1973). The second dominant theme concerns the role played by refuges in the distribution and diversification of continental biotas (Haffer 1982, 2008; Prance 1982). Proponents of the refuge theory have claimed that during the drier conditions of the ice ages, the rainforests of Amazon were fragmented by the spread of vegetation adapted to drier conditions (Haffer 1969; Prance 1982). This vicariant process may have driven

CONTACT Gimo Mazembe Daniel [email protected] Current address for Gimo Mazembe Daniel: Scarab Research Group, Department of Zoology & Entomology, University of Pretoria, Hatfield-Pretoria 0083, South Africa © 2015 Taylor & Francis 1160 G.M.DANIELANDF.Z.VAZ-DE-MELLO

speciation in disjunct patches of rainforest, which were continuously present in areas of higher rainfall (Haffer 1982). It is noticeable that the effects of climatic fluctuations of the late Quaternary on the open formations in Central Brazil were not restricted to expansion and contraction among savannahs and forests, but also included complex changes even within the dry diagonal formations (Oliveira and Marquis 2002; Portillo-Quintero and Sánchez-Azofeifa 2010). Several kinds of vegetation (e.g. savannahs, seasonal forests, wet forests and Araucaria forests) were established at least in certain areas and times in the present Cerrado province (Pennington et al. 2000; Portillo-Quintero and Sánchez-Azofeifa 2010). In addition to the climatic fluctuations, other factors such as soils, biological pressure and disturbance could have had a strong palaeoenvironmental effect (Ratter et al. 1988; Prado and Gibbs 1993). These processes probably led to vicariance, resulting in the taxonomic differentiation of biotic components for any group of fauna that are restricted to Cerrado (Portillo-Quintero and Sánchez-Azofeifa 2010). Geologically, the study region is the border between the Chacoan Depression (at the Cuiabá lowland) and the Brazilian Shield (Ab’Saber 1988). Biogeographically speaking, it is a border between southern Rondônia (within which is the Pantanal depression wet- land) and the Cerrado provinces (sensu Morrone 2014, the former is not equivalent to the Brazilian state Rondônia). The region is characterized by an abrupt change of altitude and a complex mosaic of native vegetation, including savannah and forest formations (Oliveira and Marquis 2002). In the Rondônia and Cerrado provinces, dung studies have focused on ecology (Louzada et al. 2007; Da Silva et al. 2010; Correa et al. 2013; Puker et al. 2013; Rodrigues et al. 2013), natural history (Puker et al. 2014) and inventories (Nunes et al. 2012; Daniel et al. 2014). However, there are no studies concerning distribution patterns of these scarabs based on the history of the regions. In this paper, we aim to use a panbiogeo- graphical approach to determine the distribution pattern of dung beetles from the border between the provinces of Rondônia and Cerrado in Brazil.

Material and methods We studied dung beetles from the border region between Pantanal and Cerrado,

Downloaded by [University of Cambridge] at 05:24 08 April 2016 Chapada dos Guimarães, State of Mato Grosso, Central Brazil (between 15°12'S and 15° 30'S; 56°45'W and 56°50'W), (Figure 1). The procedures of dung beetle collection were described by Daniel et al. (2014).

Dung beetle identification At the generic level, we used the identification key provided by Vaz-de-Mello et al. (2011), and at the species level, beetles were identified by the second author. Collected specimens are housed at Seção de Entomologia da Coleção Zoológica da Universidade Federal de Mato Grosso, Cuiabá, Brazil (CEMT). Distribution data of dung beetle species from other localities in the Neotropical region were obtained by consulting the literature and database at CEMT (Table 1). JOURNAL OF NATURAL HISTORY 1161

Figure 1. Geographical localization of Chapada dos Guimarães (Pantanal–Cerrado Border), Mato Grosso, Brazil and its sampled sites.

Table 1. Checklist of the dung beetles species used in panbiogeographical analysis, and the respective source of distribution localities, which was based on the CEMT-UFMT = Coleção entomológica de Mato Grosso, Universidade Federal de Mato Grosso and literature. Species CEMT-UFMT Literature

Downloaded by [University of Cambridge] at 05:24 08 April 2016 Ateuchini Ateuchus striatulus (Preudhomme de Borre, 1886) X Daniel et al. (2014) Besourenga amarillai (Aguilar-Julio) X Daniel et al. (2014) Deltorhinum armatum Génier, 2010 X Génier (2010), Daniel et al. (2014) Generidium bidens (Balthasar) X Vaz-de-Mello and Génier (2005), Daniel et al. (2014) Genieridium cryptops (Arrow) X Vaz-de-Mello and Génier (2005), Daniel et al. (2014) Trichillum adjunctum Martinez X Vaz-de-Mello and Génier (2005), Daniel et al. (2014) Trichillum externepunctatum Preudhomme de Borre X Vaz-de-Mello and Génier (2005), Daniel et al. (2014) Coprini Canthidium multipunctatum Balthasar X Daniel et al. (2014) Canthidium kelleri (Martinez, Halfter & Pereira) X Daniel et al. (2014) Canthidium sladeni Arrow 1903 X Gahan and Arrow (1903) Dichotomius sexadentatus Luderwaldt X Gahan and Arrow (1903), Daniel et al. (2014) (Continued) 1162 G.M.DANIELANDF.Z.VAZ-DE-MELLO

Table 1. (Continued). Species CEMT-UFMT Literature Dichotomius (Dichotomius) longiceps (Taschenberg) X Gahan and Arrow (1903) Dichotomius (Luederwaldtinia) cuprinus (Felsche) X Daniel et al. (2014) Dichotomius (Luederwaldtnia) nisus (Olivier, 1789) X Daniel et al. (2014) Dichotomius (Luederwaldtinia) lycas (Felsche) X Daniel et al. (2014) Dichotomius (Luederwaldtinia) ingens (Luderwalt) X Nunes (2012), Gahan and Arrow 1903 Isocopris foveolatus (Luederwaldt) X Daniel et al. (2014) Isocopris hypocrita (Lucas) X Daniel et al. (2014) Ontherus (Ontherus) carinicollis Luederwaldt X Génier Daniel et al. (2014) Ontherus (Ontherus) dentatus Luederwaldt X Génier Daniel et al. (2014) Ontherus (Ontherus) ulcopygus Génier X Génier Daniel et al. (2014) Ontherus (Ontherus) podiceps Harold X Génier Daniel et al. (2014) Ontherus (Ontherus) virescens (Lucas) X Génier Daniel et al. (2014) Deltochilini Anomiopus mourai Canhedo, 2006 X Canhedo (2006), Daniel et al. (2014) Canthon edentulus Harold X Daniel et al. (2014) Canthon fortemarginatus Balthasar X Daniel et al. (2014) Canthon histrio (LePeletier de Saint-Fargeau & Audinet- X Daniel et al. (2014) Serville) Canthon muticus Harold X Daniel et al. (2014) Canthon chalibaeus Blanchard X Daniel et al. (2014) Canthon maldonadoi Martínez X Daniel et al. (2014) Canthon planus Lucas X Daniel et al. (2014) Canthon virens (Mannerheim) X Daniel et al. (2014) Deltchillum enceladus Kolbe X Silva 2012, Daniel et al. (2014) Deltochillum (Aganhyboma) cupreicolle Blanchard X Silva 2012, Daniel et al. (2014) Deltochilum (Hybomidium) pseudoicarus Balthasar X Daniel et al. (2014) Malagoniela astyanax (Oliver, 1789) X Daniel et al. (2014) Onitecellinni Eurysternus caribaeus (Herbst, 1789) X Geniér 2009, Daniel et al. (2014) Eurysternus jessopi Martinez X Geniér 2009, Daniel et al. (2014) Eurysternus nigrovirens Génier, 2009 X Geniér 2009, Daniel et al. (2014) Phanaeini Dendropaemon viridipennis (Laporte) X Arnaud 2002, Daniel et al. (2014) Coprophanaeus (Coprophanaeus) telamon (Erichson) X Edmonds and Zidek 2010, Daniel et al. (2014) Coprophanaeus (Megaphanaeus) bonariensis (Gory) X Edmonds and Zidek 2010, Daniel et al. (2014) Coprophanaeus (Megaphanaeus) ensifer (Germar) X Edmonds and Zidek 2010, Daniel et al. (2014) mimas (Linnaeus, 1758) X Arnaud 2002, Daniel et al. (2014) Diabroctis mirabilis (Harold) X Arnaud 2002, Daniel et al. (2014) Gromphas inermis Harold X Cupello and Vaz-de-Mello 2013, Daniel et al. (2014) Oxysternon (Oxysternon) conspicillatum (Weber) X Edmonds and Zídek 2004, Daniel et al. (2014) Oxysternon (Oxysternon) palemo Castelnau X Edmonds and Zídek 2004, Daniel et al. (2014) Oxysternon (Mioxysternon) spiniferum curvispinum X Edmonds and Zídek 2004, Daniel et al. (2014) d’Olsoufieff Downloaded by [University of Cambridge] at 05:24 08 April 2016 Oxysternon (Oxysternon) silenus Castelnau X Edmonds and Zídek 2004, Daniel et al. (2014) Phanaeus (Notiophanaeus) kirbyi (Vigors) X Edmonds 1994, Daniel et al. (2014) Phanaeus (Notiophanaeus) melibaeus Blanchard X Edmonds 1994, Daniel et al. (2014) Phanaeus (Notiophanaeus) palaeno Blanchard X Edmonds 1994, Daniel et al. (2014) Sulcophanaeus faunus (Fabricius, 1775) X Edmonds 1994, Daniel et al. (2014)

Track analysis We analysed distributional data of 54 species of dung beetles (Figure 2). The panbio- geographic method was applied, which comprises plotting distributions of species on maps and connecting their localities together via minimum distance lines to obtain individual tracks (Croizat 1958, 1964). Individual tracks that were not in complete congruence were regarded as partial overlap. The overlap of individual tracks of two JOURNAL OF NATURAL HISTORY 1163 Downloaded by [University of Cambridge] at 05:24 08 April 2016

Figure 2. Individual tracks of the dung beetles species for panbiogeographical analysis. 1164 G.M.DANIELANDF.Z.VAZ-DE-MELLO Downloaded by [University of Cambridge] at 05:24 08 April 2016

Figure 2. Continued. JOURNAL OF NATURAL HISTORY 1165 Downloaded by [University of Cambridge] at 05:24 08 April 2016

Figure 2. Continued. 1166 G.M.DANIELANDF.Z.VAZ-DE-MELLO Downloaded by [University of Cambridge] at 05:24 08 April 2016

Figure 2. Continued. JOURNAL OF NATURAL HISTORY 1167

Figure 2. Continued.

or more species produces generalized tracks (Figure 3), which indicate the pre-existence of ancestral biotic components (Croizat 1958, 1964; Craw et al. 1999; Morrone 2004, 2009). The following species were not included in the generalized tracks because of their widespread distribution, such distribution patterns would probably not reflect the history of their origins accurately: Eurysternus caribaeus (Herbst, 1789), Canthon histrio (Lepeletier de Saint-Fargeau & Audinet-Serville), Trichillum externepucntatum Preudhomme de Borre, Diabroctis mimas (Linnaeus, 1758), Dichotomius nisus (Olivier, 1789) and Dichotomius lycas (Felsche). We did not include Canthidium sladeni Arrow,

Downloaded by [University of Cambridge] at 05:24 08 April 2016 1903, Dichotomius ingens (Luderwalt) and Deltorhinum armatum Génier, 2010, because these species are endemic to the region (Daniel et al. 2014) and, due to their restricted occurrence, they would not show correlations between the two biogeographic pro- vinces (Rondônia and Cerrado).

Results We found two main distributional patterns for the species analysed, which seems to correlate with host vegetation type: open formations of the Chacoan dominion and forest formations of the South Brazilian, Parana, Boreal Brazilian and Southeastern Amazonian dominions (sensu Morrone 2014). 1168 G.M.DANIELANDF.Z.VAZ-DE-MELLO Downloaded by [University of Cambridge] at 05:24 08 April 2016

Figure 3. Generalized tracks (GT A–L) of dung beetles, different biotic components observed in the Pantanal–Cerrado Border. JOURNAL OF NATURAL HISTORY 1169

Generalized tracks Generalized track A. Cerrado based on Canthon planus Lucas, Canthon fortemarginatus Balthasar, Canthon muticus Harold, Canthidium multipunctatum Balthasar, Isocopris hypo- crita (Lucas) and Ontherus virescens (Lucas). Generalized track B. Chaco based on Coprophanaeus bonariensis (Gory), Deltochillum cupreicolle (Blanchard) and Dichotomius cuprinus (Felsche). Generalized track C. Cerrado + Parana based on Anomiopus mourai Canhedo, 2006, Ateuchus striatulus (Preudhomme de Borre, 1886), Besourenga amarillai (Aguilar-Julio), Diabroctis mirabilis (Harold), Dendropaemon viridipennis (Laporte), Isocopris foveolatus (Luederwaldt), Ontherus dentatus Luederwaldt, and Oxysternon palemo Castelnau. Generalized track D. Cerrado + Chaco + Parana based on Canthidium kelleri (Martinez, Halfter & Pereira), Canthon edentulus Harold, Canthon maldonadoi Martínez, Dichotomius sexdentatus Luderwaldt, Malagoniella astyanax (Oliver, 1789) and Phanaeus kirbyi (Vigors). Generalized track E. Cerrado + Parana + Araucaria based on Ontherus carinicollis Luederwaldt, and Trichillum adjuctum Martinez. Generalized track F. Cerrado + Chaco + Parana + Atlantic based on Coprophanaeus ensifer (Germar), Eurysternus jessopi Martinez, Deltochilum pseudoicarus Balthasar, and Phanaeus palaeno Blanchard. Generalized track G. Cerrado + Chaco + Parana + Atlantic + Araucaria Forest + Pampaean based on Canthon virens (Mannerheim), Canthon chalibaeus Blanchard, and Gromphas inermis Harold. Generalized track H. Cerrado + Chaco + Parana + Atlantic + Caatinga based on Eurysternus nigrovirens Génier, 2009 and Generidium cryptops (Arrow). Generalized track I. Cerrado + Parana + Atlantic + Araucaria Forest + Caatinga based on Generidium bidens (Balthasar), Ontherus podiceps Génier, and Ontherus ulcopygus Harold. Generalized track J. Cerrado + Tapajós – Xingu based on Phanaeus melibaeus Blanchard, and Oxysternon spiniferum curvispinum d’Olsoufieff. Generalized track K. Cerrado + Tapajós – Xingu + Parana based on Deltochillum enceladus Kolbe, Dichotomius longiceps (Taschenberg) and Sulcophanaeus faunus (Fabricius, 1775). Generalized track L. Cerrado + Western Ecuador + Tapajós – Xingu + Madeira + Imerí Downloaded by [University of Cambridge] at 05:24 08 April 2016 + Guianian Lowlands + Desert based on Coprophanaeus telamon (Erichson), Oxysternon conspicillatum (Weber) and Oxysternon silenus Castelnau.

Discussion The biotic components of dung beetles from Cerrado, which are observed in the upland savannah formations in the region of the Pantanal–Cerrado Border, can be interpreted as a result of a long process of New World savannah formation. The savannahs are believed to have expanded and retracted their ranges within Quaternary climatic cycles. During the cold, dry periods, savannahs expanded in Amazonia while the humid forests retracted to peripheral ecological refuges. During moist and warm periods, humid 1170 G.M.DANIELANDF.Z.VAZ-DE-MELLO

forests spread again while the savannahs retracted to areas approximating their present day ranges (Mayle et al. 2000; Pennington et al. 2000). In the Chaco province, we observed biotic components of dung beetles, which occur in dry and lowland savannah formations in the Pantanal–Cerrado Border. The lowland savannah in this region was formed as a consequence of the subsidence of Chaco, a phenomenon related with Pantanal’s formation and Andes uplift (Silva 1995; Zanella 2002). This could be interpreted as due to a cumulative strain since the late Oligocene, when the Brazilian Shield started its westward migration, together with compression and uplift of the Central Andes. The main phase of the wetland subsidence is very likely related to the last compressional pulse in the Andes, during the upper Pliocene–lower Pleistocene (~2.5 Ma) (Ussami et al. 1999). Since the Chaco vegetation pre-dated this event, flora and fauna typical of the Chaco province are found in the lowland of the Pantanal–Cerrado Border as a relic of their past distribution. Here we found biotic components of dung beetles recorded from the province of Chaco, which are commonly observed in the southern region of Rondônia province. Diagnosis of biogeographical areas proposed by Morrone (2014) for the region of Pantanal (currently this name is a synonym of Rondônia, Morrone 2006:481), should have a relationship with biotic components from southwest of the Amazon, but in this paper we have not found any biotic component spanning both regions. Amazonian dung beetle fauna was only common in the north of Rondônia province. Therefore, it seems that the biota of the northern and southern regions of Rondônia province have different origins. We propose that the Pantanal should be included as a new biogeo- graphical district within Chaco province as opposed to the Rondônia province (Figure 3A; GT B). In the region of the Pantanal–Cerrado Border, forest formations represent floristic intrusions of the Amazonian and Brazilian Atlantic forests into the savannah formations (Oliveira and Ratter 1986). Considerable numbers of dung beetle species are observed with disjunct distribution patterns occurring concomitantly in the Amazonian and Brazilian Atlantic forests. This pattern suggests that those intrusions are remnants of a palaeoforest that was fragmented during the climatic fluctuations in the Quaternary. Therefore, forest formations in the Cerrado form a true connecting network among Amazonian and Parana subregions (Veloso 1966; Cabrera and Willink 1973; Daly and Prance 1989). Hence, we suggest that the connections between the two biomes,

Downloaded by [University of Cambridge] at 05:24 08 April 2016 through patches of wet forest and gallery forests in the region of the Pantanal– Cerrado Border, enable the survival of dung beetles from the Amazonian and Brazilian Atlantic forests.

Conclusions We have found several biotic components of dung beetle fauna from the Pantanal– Cerrado Border. The distributions of those components seem to be well explained by historical events, with a prominent role of Quaternary climatic fluctuations generating vicariant events. The region of the Pantanal–Cerrado Border is a biogeographical node, including representatives from different biogeographic origins. However, the region is not homo- geneous and the fauna of southern Rondônia province (Pantanal Depression) clearly has JOURNAL OF NATURAL HISTORY 1171

strong links with the Chaco province and none with the Amazonian fauna. According to the International code of area nomenclature (Ebach et al. 2008) we propose to formalize the Pantanal area as a biogeographical district within Chaco province (Pantanal district, stat. nov).

Acknowledgements

We are grateful to all human resources of Laboratório de Scarabaeoidologia – UFMT, Rafael Dell Erba (MUZUSP), Carol Potter (Parque Nacional da Chapada dos Guimarães) who helped with fieldwork. Thanks are due to Dr Júan Morrone (UNAM) and three anonymous reviewers for valuable comments that improved this manuscript. We also would like to thank Deon Bakkes (Scarab Research Group, University of Pretoria) and Bruno de Medeiros (Harvard University) for English proofreading.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

We are grateful to CNPq/MCT-MZ (Conselho Nacional de Desenvolvimento Científico e Tecnológico/Ministério de Ciência e Tecnologia de Moçambique), who gave a grant to the first author, process no. 190868/2011-2, and to CNPq (304925/2010-1, 202327/2013-2, 400681/2014-5, 405697/2013-9, 302997/2013-0 and 484035/2013-4) and Fundação de Amparo à Pesquisa do Estado de Mato Grosso (FAPEMAT/CNPq/PRONEM 2014), who supported the second author. We are grateful to ComCerrado network (SISBIOTA – Conselho Nacional de Desenvolvimento Científico e Tecnológico, Ministério da Ciência, Tecnologia e Inovação) and Universidade Federal da Grande Dourados (UFGD) for financial support to the fieldwork.

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