Journal of Natural History, 2014 http://dx.doi.org/10.1080/00222933.2014.908969
Deltochilini and Phanaeini dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) in introduced and native ecosystems of Brazil Anderson Pukera*, César M.A. Correab and Vanesca Korasakic a
Programa de Pós-Graduação em Entomologia, Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, Brazil; bPrograma de Pós-Graduação em Agronomia, Universidade Estadual de Mato Grosso do Sul, Aquidauana, Brazil; cDepartamento de Biologia, Setor de Ecologia, Universidade Federal de Lavras, Lavras, Brazil (Received 11 April 2013; accepted 23 March 2014)
The dung beetle tribes Deltochilini and Phanaeini (Coleoptera: Scarabaeidae: Scarabaeinae) play an important ecological role in the habitats in which they live. Despite much field work on these beetles in the Neotropical region, biological information on many taxa is still unknown. Here we provide information on species of Deltochilini and Phanaeini including temporal distribution of adults, sex ratio (Male : Female) and measurements of the individuals as well as on ecology and general biology of all species sampled in introduced (pasturelands of Brachiaria spp.) and native (patch of the Brazilian savanna) ecosystems of Brazil. Furthermore, our findings may help to understand the complexity of the effects of mixed ecosystems on the biodiversity of dung beetles. Keywords: agro-pastoral landscape; biodiversity conservation; bioindicator; copro-necrophagous beetle; ecological service; landscape ecology; Scarabaeoidea
Introduction Deltochilini Lacordaire (Coleoptera: Scarabaeidae: Scarabaeinae) [=Canthonini Lansberge, synonymy according to Bouchard et al. 2011] is one of the oldest and most diverse scarabaeine tribes. It comprises 873 species with distinct ecological behaviour and wide Neotropical distribution (Davis et al. 2008). This tribe comprises ball-rolling species with different feeding habits, such as mycetophagy, saprophagy and predation, and, most commonly, copro-necrophagy (e.g., Gordon and Cartwright 1974; Hertel and Colli 1998; Vaz-de-Mello et al. 1998; Villalobos et al. 1998; Silveira et al. 2006; Silva et al. 2012). Phanaeini Hope (Coleoptera: Scarabaeidae: Scarabaeinae) is the best known tribe in the Neotropical region with respect to its taxonomy and species distribution (Edmonds 1972, 1994, 2000; Arnaud 2002a, 2002b; Edmonds and Zídek 2004, 2010, 2012; Philips et al. 2004; Price 2009; Cupello and Vaz-de-Mello 2013). This endemic American tribe includes 12 genera and approximately 160 species (Davis and Scholtz 2001; Philips et al. 2004). In general, phanaeines are typical fossorial species which may be either coprophagous, necrophagous or both (Halffter and Matthews 1966; Edmonds 1972). However, several genera exhibit atypical ecologies, most notably myrmecophily in Dendropaemon Perty and Tetramereia Klages (Vaz-deMello et al. 1998; Vaz-de-Mello and Génier 2009) and mycetophagy in two species of Phanaeus MacLeay (Edmonds 1994). *Corresponding author. Email:
[email protected] © 2014 Taylor & Francis
2 A. Puker et al. Scarabaeinae has proven to be an attractive target group for studying wider biodiversity patterns and has consequently been adopted as a reliable bioindicator taxon (Halffter and Favila 1993; Spector 2006; Gardner et al. 2008). The tribes Deltochilini and Phanaeini are common components of most Neotropical dung beetle faunas, being an important group for biogeographic and ecological studies, and are an important functional component in many ecosystems (Nichols et al. 2008). Thus, it is important to understand the life history of these species, their feeding habits, reproductive capacity and other biological and ecological characteristics. To increase the knowledge base on the ecology and general biology of these beetles, we provide here information on the Deltochilini and Phanaeini which inhabit introduced and native landscapes of the Brazilian Cerrado-Pantanal ecotone.
Material and methods Study area The study areas are located in the transitional region between the Cerrado (Brazilian savanna) and Pantanal (wetlands) ecosystems in Aquidauana, Mato Grosso do Sul, Brazil. The climate of the region is Tropical Wet-Humid (Peel et al. 2007) with mean annual temperature of 26°C and annual precipitation varying from 1200 to 1300 mm. Dung beetles were captured in two habitats: in pasturelands with exotic grass (Brachiaria spp.) (20° 26′ 25″ S, 49° 36′ 57″ W) with the constant presence of cattle and in a patch of native forest (Brazilian savanna) with typical wild animals of the Cerrado and Pantanal ecosystems (20° 27′ 37″ S, 49° 40′ 2″ W). The two areas are separated by a distance of 3 km. Regions surrounding the sampling sites are dominated by extensive pasturelands with exotic grass and patches of native vegetation (Correa et al. 2013b). Meteorological data were obtained from the weather station at the ‘Universidade Estadual de Mato Grosso do Sul’ (UEMS) (Aquidauana, Mato Grosso do Sul, Brazil).
Dung beetle sampling Sampling was performed every 2 weeks from January to December 2011 during which traps remained active in the field for 48 h, totalling 96 h of sampling/month. In the exotic pasture, samples from December were lost because the traps were removed by small mammals. In each ecosystem a linear transect was installed to set 10 pitfall traps (diameter 20 cm, height 15 cm) (five traps for each type of bait) which contained approximately 250 mL of a 1.5% liquid detergent solution. Traps were installed at the level of the soil and spaced at a distance of 20 m. Traps were baited with carrion (bovine meat; 3 days of decomposition) alternating with human faeces, placed in plastic recipients (50 mL) at the centre of each trap using a wire. The traps were covered with plastic lids in order to reduce desiccation of the baits and avoid damage caused by rainfall.
Measurements and sex ratio of the dung beetles Body length from clypeal margin to the pygidium and width (considered as the greatest width of the pronotum) were measured for all individuals (n = 753) using a digital calliper. All beetles were dissected and male genitalia extracted. Sex ratio (Male : Female) was calculated for species with >5 sample size in each ecosystem.
Journal of Natural History 3 Identification and deposit of the voucher specimens Beetles captured were sent to the ‘Universidade Federal de Mato Grosso’ (UFMT; Cuiabá, Mato Grosso, Brazil) where they were identified by Prof. Dr. Fernando Z. Vaz-de-Mello. Vouchers are deposited in the UEMS and also in the Entomology Section of the Zoological Collection of the UFMT.
Data analysis We used Generalized Linear Models (GLMs) to test the effect of the baits on abundance and richness of dung beetles in each ecosystem; the baits were used as explanatory variables and abundance and richness as responses. To assess if the richness and abundance of dung beetles attracted to each bait type per ecosystem is influenced by monthly precipitation and average monthly temperature, we used GLMs with the precipitation and temperature as explanatory variables and richness and abundance in each ecosystem and bait type as responses. To determine if there is a relationship between the length and width of Deltochilini and Phanaeini individuals, and verify if the size varies according to the bait preference, sex and the ecosystem, we used GLMs with data of the three most abundant species (see results) using bait, sex and ecosystems as explanatory variables and size as the response, when possible. All GLMs were submitted to residual analysis so as to evaluate adequacy of error distribution (Crawley 2002). All GLMs were performed using the software R (R Development Core Team 2013). To evaluate the efficiency of the sampling programme we assessed the completeness of each bait per ecosystem by calculating the number of observed species (Sobs) as a percentage of the total species richness, which was estimated based on the average of three abundance-based non-parametric estimators: ACE, Chao 1 and Jackknife 1, using the following formula: Sampling Efficiency = [Sobs • 100/ ((ACE + Chao1 + Jack1)/3)]. Richness estimates were calculated using the software EstimateS 7.5, with 500 randomizations (Colwell 2005).
Results Abundance and richness We collected 753 dung beetle individuals of Deltochilini and Phanaeini, representing seven genera and 13 species (Table 1, Table S1). A total of 686 individuals and 11 species were sampled in the native ecosystem, while in the introduced ecosystem only 67 individuals of nine species were captured (Table 1, Table S1). In the native ecosystem, traps baited with carrion captured more individuals per sampling (F1,22 = 4.54; p < 0.05), but the average number of species did not vary among the baits (F1,22 = 3.99; p = 0.058). In the introduced ecosystem, traps baited with human faeces captured more individuals (F1,20 = 24.61; p < 0.001) and species (χ21,20 = 13.47; p < 0.0001). Of a total of 13 Deltochilini and Phanaeini species sampled, four were exclusive to the native ecosystem, two to the introduced ecosystem and seven were common to both. Phanaeus palaeno Blanchard (Phanaeini) with 341 individuals sampled in the native and 37 in the introduced ecosystem was the most abundant species (Table 1). In native ecosystem the richness estimate (ACE, Chao 1, Jackknife 1) indicated a maximum of 12 and 15 species sampled with human faeces and carrion, respectively. In introduced pasture the richness estimate indicated a maximum of 11 and four species
Deltochilini Canthon chalybaeus Blanchard Canthon histrio LePeletier and Serville Canthon virens (Mannerheim) Deltochilum (Deltohyboma) sp. Deltochilum pseudoicarus Balthasar Malagoniella puncticollis Blanchard Phanaeini Coprophanaeus ensifer (Germar) Croprophanaeus spitzi (Pessôa) Diabroctis mimas Linnaeus Diabroctis mirabilis Harold Oxysternon palemo (Laporte) Phanaeus kirbyi Vigors Phanaeus palaeno Blanchard Total 1 7
2 4
Carrion
6 1 2 1 7 36 60
6
1
Human faeces
Introduced
2 10 1 2 1 7 37 67
1 0 6 0 0 0
Subtotal
3 2 1 4 104
1
9 82 1
1
Carrion
38 16 18 337 582
4 1 4 158 5 1
Human faeces
Native
0 1 0 41 18 19 341 686
5 1 13 240 6 1
Subtotal
2 11 1 43 19 26 378 753
6 1 19 240 6 1
Total
Table 1. Abundance and richness of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces, from January to December 2011.
4 A. Puker et al.
Journal of Natural History 5 Table 2. Richness observed, estimated and sample efficiency of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces, from January to December 2011. Estimators
Introduced
Native
Carrion
Human faeces
Carrion
Human faeces
3 3.69 3.00 3.99 84.27
8 10.74 9.5 10.97 76.90
9 15.41 12.00 12.97 66.86
10 11.25 11.00 11.98 87.64
Sobs ACE Chao 1 Jackniffe 1 Sample efficiency (%)
sampled with human faeces and carrion, respectively. In native ecosystem the sampling efficiency was 87.64 and 66.86%, respectively, for human faeces and carrion. In introduced ecosystem the sampling efficiency was 76.90 for human faeces and 84.27% for carrion (Table 2). Seasonal variation In the introduced ecosystem the abundance and richness of the Deltochilini and Phanaeini dung beetles were not correlated with precipitation and temperature (Table 3). In the native ecosystem was the abundance and richness of the Deltochilini and Phanaeini dung beetles attracted by the two baits positively correlated with monthly precipitation and average monthly temperature (Table 3, Figure 1). Table 3. Relationship (GLMs) between monthly precipitation and average monthly temperature with abundance and richness of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces, from January to December 2011. Introduced Carrion Precipitation Abundance Richness
χ2 = 0.06; p = 0.8036 χ2 = 0.03; p = 0.8455
Human faeces Temperature
χ2 = 2.41; p = 0.1202 χ2 = 1.49; p = 0.2211
Precipitation F = 0.87; p = 0.3751 F = 0.44; p = 0.505
Temperature F = 1.40; p = 0.2655 χ2 = 2.30; p = 0.1291
Native Abundance Richness
F = 5.2485; p = 0.0449 F = 5.16; p = 0.0476
F = 19.42; p = 0.0013 χ2 = 23.53; p = 0.0000
F = 21.73; p = 0.0008 F = 5.03; p = 0.0487
F = 5.59; p = 0.0395 χ2 = 12.79; p = 0.0003
6 A. Puker et al.
Figure 1. Monthly precipitation, average monthly temperature and abundance and richness of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of vegetation native (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces, from January to December 2011. Bars on columns represent standard errors.
Journal of Natural History 7 Measurements and sex ratio Considering the data obtained in the two ecosystems, the three most abundant species were P. palaeno (n = 378), Deltochilum (Deltohyboma) sp. (n = 240) and Diabroctis mirabilis Harold (n = 43) (Table 1). Width and length of these three species were correlated: P. palaeno (F1,375 = 1,191.60; p < 0.0001), Deltochilum (Deltohyboma) sp. (F1,235 = 88.69; p < 0.0001) and D. mirabilis (F1,41 = 302.96; p < 0.001), therefore we decided to use the length to infer on the individuals size. Males of P. palaeno are larger than females (F1,375 = 23.73; p < 0.0001), and the females of this species sampled in the native ecosystem were larger than those encountered in the introduced ecosystem (F1,236 = 15.93; p < 0.001). The size of individuals of Deltochilum (Deltohyboma) sp. did not vary according to sex (F1,235 = 2.30; p = 0.1304) or bait type (F1,235 = 0.80; p = 3717). Size of individuals of D. mirabilis also did not vary according to sex (F1,41 = 0.2544; p = 6167). Results of the average length and width of the individuals of all Deltochilini and Phanaeini species sampled in the introduced and native ecosystems are shown in Table S2. The sex ratio (Male : Female) in the introduced habitat ranged from 0.2 for Malagoniella puncticollis Blanchard (Deltochilini) to 1.5 for Coprophanaeus spitzi (Pessôa) (Phanaeini), while in the native habitat ranged from 0.2 for Deltochilum pseudoicarus Balthasar (Deltochilini) to 5.0 for Oxysternon palemo (Laporte) (Phanaeini) (Table S3).
Discussion Abundance and richness patterns In this study we found greater abundance of Deltochilini and Phanaeini beetles in the native ecosystem, which suggests a strong relationship with more heterogeneous and/ or relatively conserved habitats. Native landscapes such as the Brazilian savannas normally serve as habitat for a wide range of animals, and therefore there is a greater availability of different resources (e.g., carrion and faeces). Vegetation structure with greater variation may also contribute to the increase and/or conservation of local abundance and diversity (e.g., Driscoll and Weir 2005). The Brazilian savanna (Cerrado) is a priority area for conservation (a biodiversity hotspot) due to its high degree of endemism and the fact that it is at risk from anthropogenic pressure (Myers et al. 2000). Therefore studies to understand animal communities in this ecosystem are one of the bases for conservation policy (e.g., Correa et al. 2013a). In the two ecosystems studied, dung beetles were attracted to both baits (carrion and faeces). Therefore, we believe that the species sampled in the introduced and native ecosystems are copro-necrophagous. Because only a small number of individuals was obtained for most species, it was not possible to accurately place collected species in more precise trophic guilds (e.g., coprophagous, necrophagous). Considering that the species sampled in the present study are copro-necrophagous, we believe that in the introduced ecosystem, the community of these beetles is maintained due to the presence of cattle dung, which is an abundant resource that may influence the beetles occurrence and distribution. Cattle were introduced to Brazil just over 500 years ago and now an associated fauna of dung beetles is present (Louzada and Carvalho e Silva 2009). The high specialization in coprophagy in the Scarabaeinae group appears to be related to the increased availability of faeces from
8 A. Puker et al. mammals in pasture ecosystems (Halffter and Matthews 1966), since the appearance and availability of dead animal carcasses may be seasonally and spatially limited when compared with faeces availability (Louzada and Lopes 1997). Moreover, a change in vegetation structure may favour the re-emergence of specialized guilds. The presence of specialists, such as necrophagous species, is important because it aids in reducing competition for food and increases the diversity of the guild (Halffter 1991). Phanaeus palaeno was the most abundant species in both ecosystems studied. It is an indicator species of native grassland, one of the physiognomies of the Cerrado (Brazilian savanna) (Almeida and Louzada 2009), therefore adapted to natural open areas (native grassland) and probably for this reason, it is has also adapted to exotic pastures, which are structurally similar to native grasslands. This species is common in Brazilian savannas and is also found in Argentina, Bolivia and Paraguay (Edmonds 1994). The high estimated values of species richness were due to the presence of several unique species during sampling. Moreover, samplings with the two baits along the entire year probably permitted sampling of species with specific emergence, behaviour and/or reproductive periods.
Seasonal variation Only in the native ecosystem were abundance and richness of Deltochilini and Phanaeini dung beetles attracted to human faeces and carcasses positively affected by the monthly precipitation and average monthly temperature (Table 3). This seasonal variation observed in Deltochilini and Phanaeini in the native system reflects a common pattern among dung beetles collected from Brazilian landscapes (e.g., Louzada and Lopes 1997; Hernández and Vaz-de-Mello 2009; Silva et al. 2010). This pattern was probably not observed in the introduced ecosystem due to the low total capture of dung beetles (Table 1).
Measurements and sex ratio Of the 13 species of Deltochilini and Phanaeini sampled, statistical analyses were performed with respect to size for the three most abundant species [P. palaeno, Deltochilum (Deltohyboma) sp. and D. mirabilis], considering both ecosystems. Of these three species, differences were observed in size of the individuals only for P. palaeno, where males were larger than females, and females were larger in the native ecosystem than in pasturelands with exotic grass. Larval feeding (quantity and quality of food) and genetic potential plays an important role on the size of adult insects (e.g., Shingleton et al. 2007), therefore we believe these two fundamental components associated with numerous other environmental factors may have contributed to the variation in size of P. palaeno adults. The larger size of P. palaeno males may play a role in sexual selection and sexual conflict in this species, but our findings do not enable us to state that females select males based on their body size. Due to the proximity of the ecosystems (~3 km) from which the beetles were sampled, we believe that genetic flow is likely to occur among individuals of P. palaeno that were found in the native forest and exotic grassland, but we do not rule out the hypothesis that the native ecosystem may have offered better environmental
Journal of Natural History 9 conditions for larval development of females of this species, resulting in larger size than those found in the introduced ecosystem. The sex ratio varied from 0.2 to 5.0 (Male : Female) among the species of Deltochilini and Phanaeini that were studied (Table S3). Therefore we cannot affirm that these values reflect the reality of the local assemblage, since other factors may be influential, such as different nutritional needs as a function of the lifecycle stage of the insect. For example, to complete the development of its reproductive organs, after emergence adults of only one sex or both may search for food sources. Therefore, it would be useful to investigate if the individuals of each species attracted to on each bait present completely developed reproductive organs. If so, we believe that the bait is an important factor that must be taken into consideration in sex ratio studies of dung beetle species. In this case, the baited trap could be a potential location for encountering the opposite sex and consequently reproduction. If the individuals do not present developed reproductive organs, we believe that attraction to the bait is triggered by a physiological need of individuals to ingest food prior to breeding. Information on the sex ratios of dung beetle species is scarce. In Onthophagus taurus (Schreber) (Onthophagini) the sex ratio may vary with the quality of the resources which the female provides to the offspring (House et al. 2011). In general, males and females require nitrogen; however, females require additional quantities for maturation of their eggs (Hanski and Cambefort 1991). The capture of females in baited traps is probably greater among species that have no sexual cooperation for formation of the nest. In burrowing beetles (e.g., Phanaeini) it has been observed that the role of the male in bisexual cooperation is secondary, and the female is responsible for most of the work for gallery excavation and construction of the nesting mass (Halffter and López 1977; Halffter and Edmonds 1982; Price and May 2009). In most ball-rolling species (e.g., Deltochilini) this process involves bisexual cooperation, wherein the male is responsible for formation of the ball, rolling it and burying it (e.g., Halffter and Edmonds 1982; Favila and Diaz 1996; Rodrigues and Flechtmann 1997). In conclusion, we provide increased knowledge on the biology and especially the ecology of Deltochilini and Phanaeini beetles which make up an important bioindicator group of Neotropical landscapes. Moreover, our findings may aid in understanding the complexity of effects generated by mixed ecosystems on the dung beetles. Acknowledgements AP thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) for scholarship support (process number 140989/2011-0) and the Graduate Program in Entomology of the Federal University of Viçosa (UFV; Viçosa, Minas Gerais, Brazil). CMAC thanks his father, Agenor Martinho Correa, for encouragement and logistical support for execution of this research, CNPq for scholarship support (134418/2013-1), and the Graduate Program in Agronomy of the State University of Mato Grosso do Sul. VK thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) for the research grant received (PNPD institucional). We thank Professor Dr. Cristiano LopesAndrade (UFV) for providing space and equipment at the Laboratory of Systematics and Biology of Coleoptera for sorting of Deltochilini and Phanaeini beetles, Professor Dr. Fernando Z. Vaz-de-Mello (UFMT) for identifying the dung beetle species, and Mr. Gélio Proença Brum for access to the study.
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Table S1. Abundance of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces, from January (I) to December (XII) 2011. Introduced
Native Subtotal
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
XII
I
II
III
IV
V
VI
VII
VIII
IX
X
XI
Subtotal
Total
5
6
XII
Deltochilini Canthon chalybaeus Blanchard
1
1
1
4
Canthon histrio LePeletier & Serville
1
Canthon virens (Mannerheim)
11
Deltochilum (Deltohyboma) sp.
82
36
Deltochilum pseudoicarus Balthasar
3
1
Malagoniella puncticollis Blanchard
2
1
1
2
6
10
10
4
3
8
18
1
1
1
1
2
13
13
69
240
240
6
6
1
7
1
11
1
41
43 19
1
Phanaeini Coprophanaeus ensifer (Germar) Croprophanaeus spitzi (Pessôa)
1 3
2
2
Diabroctis mimas Linnaeus Diabroctis mirabilis Harold
1
1
2
2
10
1
1
1
1
Oxysternon palemo (Laporte)
2 1
1
Phanaeus kirbyi Vigors
3
Phanaeus palaeno Blanchard
4
3
1
6
7
3
Total
13
5
1
7
10
3
1
2
30
5
1
2
1
9
5
1
2
1
7
7
3
1
2
6
4
37
186
46
15
28
9
2
8
9
9
67
330
97
25
39
15
2
3
18
1
1 1
2
4
19
26
1
1
15
30
10
341
378
1
5
28
53
93
686
753
1
Table S2. Average (± Standard Error) length and width (in mm) of the individuals of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces. Introduced
Native
Carrion
Human faeces
Carrion
n Length
Width
Human faeces
n Length
Width
6.49
3.53
n Length
Width
6.87
4.30
Canthon virens (Mannerheim)
8.32 ± 0.21
Deltochilum (Deltohyboma) sp.
n Length
Width
1
5.90 ± 0.30
3.99 ± 0.30
4
8.55
5.95
1
5.40 ± 0.12
9
7.78 ± 0.31
5.34 ± 0.31
4
10.93 ± 0.05
6.28 ± 0.03
82
10.95 ± 0.04
6.25 ± 0.02
158
24.58
14.40
1
21.91 ± 0.36
13.19 ± 0.33
5
9.90
6.43
1
14.17 ± 0.18
38 16
Deltochilini Canthon chalybaeus Blanchard
1
Canthon histrio LePeletier & Serville
Deltochilum pseudoicarus Balthasar Malagoniella puncticollis Blanchard
12.61 ± 0.59
7.09 ± 0.81
6
Phanaeini Coprophanaeus ensifer (Germar)
35.06 ± 1.76
23.25 ± 0.92
2
Croprophanaeus spitzi (Pessôa)
15.13 ± 1.88
9.09 ± 1.68
4
18.78 ± 1.28
12.96 ± 0.83
6
Diabroctis mimas Linnaeus
25.23
18.72
1
Diabroctis mirabilis Harold
23.65 ± 0.19
16.36 ± 0.14
Oxysternon palemo (Laporte) Phanaeus kirbyi Vigors Phanaeus palaeno Blanchard
16.86
11.34
1
19.33
11.98
1
2
21.05 ± 0.78
14.61 ± 0.61
3
20.25 ± 0.25
13.73
9.57
1
12.71 ± 1.02
9.22 ± 0.81
2
13.06 ± 0.21
9.33 ± 0.16
16.23 ± 1.13
10.56 ± 1.07
7
17.12
12.16
1
16.26 ± 0.42
11.32 ± 0.26
18
12.70 ± 0.41
8.87 ± 0.44
36
15.30 ± 1.12
11.22 ± 0.71
4
15.33 ± 0.10
10.88 ± 0.07
337
Table S3. Number of males, females and sex ratio (Male : Female) of Deltochilini and Phanaeini dung beetles (Coleoptera, Scarabaeinae) sampled in pasturelands with exotic grass (Brachiaria spp.) and a patch of native vegetation (Brazilian savanna) (Aquidauana, Mato Grosso do Sul, Brazil) using pitfall traps baited with carrion and human faeces. Introduced
Native
n Male
n Female
Sex ratio
Male
Female
Sex ratio
Deltochilini Canthon chalybaeus Blanchard
1
5
Canthon histrio LePeletier & Serville
1
Canthon virens (Mannerheim)
4
9
0.44
Deltochilum (Deltohyboma) sp.
93
147
0.63
Deltochilum pseudoicarus Balthasar
1
5
0.20
Malagoniella puncticollis Blanchard
1
5
0.20
1
4
1.50
1
Phanaeini Coprophanaeus ensifer (Germar)
2
Croprophanaeus spitzi (Pessôa)
6
Diabroctis mimas Linnaeus
1
Diabroctis mirabilis Harold
2
22
19
1.16
Oxysternon palemo (Laporte)
1
15
3
5.00
Phanaeus kirbyi Vigors
2
5
0.40
5
14
0.36
Phanaeus palaeno Blanchard
9
28
0.32
130
211
0.62
Total
25
42
270
416
