Optimising Methods for Dung Beetle (Coleoptera: Scarabaeidae) Sampling in Brazilian Pastures

Optimising Methods for Dung Beetle (Coleoptera: Scarabaeidae) Sampling in Brazilian Pastures Abstract Dung beetles are globally used in ecological research and are useful for assessing the effects of anthropic and natural changes in environment on biodiversity. Here we investigate how the choice of baits (human feces, cattle dung, carrion or a combination of all three) and sampling season influence the taxonomic and functional diversity of insects captured in traps in Brazilian pastures. We sampled dung beetles in July 2011 (dry season) and January 2012 (rainy season) in eight areas: four pastures with native grasses (e.g., Andropogon spp. and Axonopus spp.) and four pastures with introduced grasses (Urochloa spp.) in Aquidauana, Mato Grosso do Sul, Brazil. To collect the insects, we used pitfall traps baited with carrion, cattle dung and human feces. A total of 7,086 dung beetles of 32 species were captured. In both pasture types, only traps baited with human feces captured similar abundance, species richness, and functional diversity compared with the sum total of beetles captured by the three bait types. The species richness and functional diversity were higher in the rainy season in both pasture types. Our results demonstrate that using human feces alone as bait and sampling dung beetles in the rainy season are potentially sufficient to ensure the greatest number of functional traits, species, and individuals in both pasture types. Thus, the best sampling method observed in this study may be useful for studies focused on dung beetle fauna survey and rigorous comparison among studies on these insects in Brazilian pastures. Dung beetles (Coleoptera: Scarabaeinae) are a group of insects used globally in ecological research to evaluate the effects of anthropic and natural changes the environment on biodiversity (Audino et al. 2014, Bicknell et al. 2014, França et al. 2016). They are stenotopic and thus sensitive to changes in environmental conditions (Hanski and Cambefort 1991), diverse and relatively well characterized taxonomically (Vaz-de-Mello et al. 2011), and relatively inexpensive to collect (Gardner et al. 2008). In addition, they perform important ecological functions, such as nutrient cycling, improving soil fertility, and secondary seed dispersal (for review, see the study by Nichols et al. 2008 and references therein). Despite the validation of this group as bioindicators being relatively recent (McGeoch et al. 2002, Spector 2006), the number of studies using dung beetles has been increasing worldwide, making this group one of the most used as terrestrial bioindicators (Gerlach et al. 2013). Using dung beetles as bioindicators requires a method of effectively sampling the beetles across different types of habitats (Marsh et al. 2013, Correa et al. 2016a). In many studies that have evaluated the impact of anthropogenic changes on dung beetle communities, only human feces were used as bait (Braga et al. 2013, Korasaki et al. 2013, Bicknell et al. 2014, Costa et al. 2017). Human feces are indispensable when the target is to sample greater abundance and species richness, independent of the plant structure (Correa et al. 2016a). In addition, feces of omnivorous mammals (especially humans) are more attractive to dung beetles when compared, for example, with herbivore (Puker et al. 2013) and carnivore feces (Bogoni and Hernandez 2014) and carrion (Correa et al. 2016a). In contrast, due to the trophic specialization of dung beetles (Larsen et al 2006), using multiple baits may attract a more diverse group of beetles and thus result in a better characterization of communities (Audino et al. 2014, Correa et al. 2016a). Grasslands, such as pastures dominated by native (e.g., Adropogon spp. and Axonopus spp.) or introduced grasses (the African grass, Urochloa spp.), predominate in four of the six Brazilian biomes (Overbeck et al. 2015), with an estimated area of 176 million ha (IBGE 2012). However, our knowledge of the differences in dung beetle communities across Brazilian pastures is insipient. One of the reasons for this is the inconsistency in sampling strategy used in most studies carried out in Brazilian pastures. In introduced pastures, most studies have used cattle dung as bait (for a list refer the study by Louzada and Carvalho e Silva 2009, Tissiani et al. 2017), whereas in forests, the most frequently used baits are human feces (Marsh et al. 2013, Audino et al. 2014), decaying fruits (Silva et al. 2012a, Audino et al. 2014), and vertebrate carrion (e.g., Silva et al. 2012a, Audino et al. 2014). Furthermore, sampling period also plays a fundamental role in dung beetle sampling (Halffter et al. 1991). However, little is known about the effects of seasons on the dung beetle sampling in Brazilian pastures (Abot et al. 2012). Studies that assess the attractiveness of baits to dung beetles in Brazilian pastures by comparing community metrics such as abundance, biodiversity, and species composition are well known (Silva et al. 2012b, Puker et al. 2013, Correa et al. 2016b). However, functional diversity metrics are also important; functional diversity is a measure of biodiversity that quantifies the diversity of characters (morphology, life history, and ecological niches) in a community (Cadotte et al. 2011, Gerish et al. 2012, Mouillot et al. 2013). Functional diversity metrics are directly related to ecosystem functions performed by species (Barrágan et al. 2011, Audino et al. 2014); therefore, functional diversity has been used to predict the impact of the loss of species on ecosystem functionality (Barrágan et al. 2011, Audino et al. 2014, Derhé et al. 2016, Goméz-Cifuentes et al. 2017). However, there is still no information on the effect of the different baits and sampling seasons on the functional metrics. An important step to improve dung beetle sampling in pastures is to understand how the collection method can affect the quantification of the community in terms of both, taxonomic and functional diversity. Here, we investigate how the use of baits (human feces, cattle dung, carrion or a combination of all three) and sampling seasons influences the taxonomic and functional diversity of dung beetles captured in Brazilian pastures. Therefore, we sampled dung beetles in cattle grazing native and introduced pastures (Urochloa spp.), using pitfall traps baited with human feces, cattle dung, and carrion during the dry and rainy season to answer the following question: does any individual bait capture the abundance, species richness and functional diversity of dung beetles similar to that captured by all baits summed together in the two pasture types? In addition, we compared the abundance, species richness, and functional diversity of dung beetles captured in the rainy and dry season in both pasture types. Material and Methods Study Sites Samples were collected in four areas of pastures with introduced grasses (Urochloa spp.) and four pastures with native grasses (e.g., Andropogon spp. and Axonopus spp.) in Aquidauana, Mato Grosso do Sul, Brazil (19° 54′36 ″ S, 55° 47′54″ W). The climate of the region, according to the Köppen classification is Aw, that is, tropical hot–wet, with a summer rainy season and dry winter (Alvares et al. 2014). The average temperature is 26°C (12–40°C) and rainfall (average of 1,200 mm yr−1) is characterized by certain periods, such as dry (May to September: monthly average of 30 mm of precipitation) and rainy (October to April: 160 mm). Animals, especially cattle and horses, are extensively produced on these pastures. More detailed description of the study areas are in Correa et al. (2016b). Dung Beetle Sampling and Identification We sampled dung beetles in July 2011 (dry season) and January 2012 (middle of the rainy season). In each of the eight pasture areas, we installed four linear transects (250 m) located ~50 m from the edge of the habitat and separated from the others by 100 m for allocation of the traps. A distance of 100 m was used between transects to ensure independence of the samples (Silva and Hernández 2015). Therefore, we consider the transects as replicates (i.e., 16 replicates per type of pasture). In each transect, we marked out six points separated by 50 m. At each point, we installed a set of three traps, each separated by 3 m in a triangular shape; the traps of each set were baited with ~40 g of human feces, cattle dung, and carrion (decaying beef). Total sampling effort was 1,152 traps, where each bait was repeated 192 times for each pasture type, in rainy and dry season. The traps (15 cm diameter and 9 cm tall), installed at ground level, contained ~250 ml of a 1.5% liquid detergent solution and remained installed in the field for a period of 48 h. Traps were covered with a plastic lid in order to reduce desiccation of the bait and avoid damage caused by potential rainfall. The baits were placed in plastic containers (50 ml) at the center of each trap using a wire as bait holder. Dung beetles were identified to species level by Dr. Fernando Zagury Vaz-de-Mello. Voucher specimens are deposited at the Entomology Section of the Zoological Collection of the Universidade Federal de Mato Grosso (UFMT; Cuiabá, Mato Grosso, Brazil) and in the Entomology Laboratory at the Universidade Estadual de Mato Grosso do Sul (UEMS; Aquidauana, Mato Grosso do Sul, Brazil). Functional Traits We analyzed four functional traits that are directly related to the ecosystemic functions performed by dung beetles and diet: nesting behavior (tunnelers, rollers, or dwellers), diet preference (human feces, cattle dung, carrion, coprophagous/generalist, or generalist), breadth of diet (species attracted to one, two, or three bait types) and body size (Suppl material 1). Data Analysis Taxonomic Metrics in Different Baits and Seasons We used Generalized Linear Mixed Models (GLMMs) to verify the effect of different baits (explanatory variables) in each pasture type on dung beetle abundance and species richness (response variables), using bait types (fixed factor) and seasons (random factor). We used a negative binomial error distribution with log link function for abundance and species richness, since these data showed overdispersion, preventing the use of Poisson error. We used Generalized Linear Models (GLMs) to verify the effect of different seasons (explanatory variables) in each pasture type on dung beetle abundance and species richness (response variables). All GLMs were submitted to residual analysis, so as to evaluate error distribution adequacy (Crawley 2002), and conducted with the “lme4” package using the R v 3.3.1 software (R Development Core Team 2016). Functional Diversity in Different Baits and Seasons We used the “FD” package (R Development Core Team 2016) to calculate two functional diversity indexes: 1) Functional richness (FRic) represents the range of traits in a community quantified by the volume of functional trace space occupied, and 2) functional dispersion (FDis) which indicates the distribution of abundances in the space of functional traits in relation to a weighted centroid in abundance and the volume of space occupied (Laliberté and Legendre 2010). We used GLMMs to verify the effect of different baits (explanatory variables) in each habitat on functional diversity (response variables). We used bait types (fixed factor) and seasons (random factor) with Gaussian error distribution. Finally, we used GLMs to verify the effect of different seasons (explanatory variables) in each pasture type on functional diversity indices (response variables). Appropriate error structure and link function were used for each analysis (Crawley 2002). Results Baits Attractiveness: Taxonomic and Functional Diversity A total of 7,086 individuals were sampled belonging to 32 species of 16 genera and six tribes of dung beetles: Ateuchini (4 genera and 4 species), Coprini (3 genera and 9 species), Deltochilini (3 genera and 11 species), Oniticellini (1 genus and 2 species), Onthophagini (2 genera and 2 species), and Phanaeini (2 genera and 4 species) (Table 1). Table 1. Biodiversity of dung beetles sampled in introduced and native pastures in the dry and rainy seasons in Aquidauana, Mato Grosso do Sul, Brazil Taxon  Dry    Rainy    Total  Introduced  Total  Native  Total  Introduced  Total  Native  Total  C  CD  HF    C  CD  H F    C  CD  HF    C  CD  HF    ATEUCHINI   Ateuchus sp.  14  4  30  48  7  4  51  62  6  24  74  104  27  24  123  176  390   Genieridium bidens (Balthasar)            7  33  40      3  3          43   Trichillum externepunctatum Preudhomme de Borre  4    10  14      54  54  34  41  879  954    12  66  78  1100   Uroxys sp.      7  7      29  29  2  4    6      23  23  65  COPRINI   Canthidium sp.      8  8    2  12  14      2  2  2    24  26  50   Canthidium aff. barbacenicum          11    242  253  5  11  2  18  43  11  266  320  591   Canthidium aff. pinotoides                  12  21  82  115  27  9  253  289  404   Dichotomius bos (Blanchard)  3  7  23  33  4  7  26  37  1  12  126  139    5  77  82  291   Dichotomius glaucus Harold                      2  2      18  18  20   Dichotomius nisus (Olivier)  93  63  671  827  18  47  457  522  4  8  240  252  2  1  76  79  1680   Dichotomius opacipennis Luederwaldt                      1  1  4  1  54  59  60   Ontherus appendiculatus (Mannerheim)  19  3  18  40    3  64  67    1  13  15    2  18  20  142   Ontherus sulcator (Fabricius)                      1            1  DELTOCHILINI   Canthon edentulus Harold      1  1      22  22  1    4  5  17  3  137  157  185   Canthon histrio (Lepelletier and Serville)              9  9      2  2  2  3  76  81  92   Canthon mutabilis Lucas    3  12  15    5  39  44  103  15  109  227  33  20  80  133  419   Canthon ornatus Redtenbacher              13  13  1    2  3      2  2  18   Canthon substriatus Harold                  2    2  4  4  2  9  15  19   Canthon aff. curvodilatatus  1      1          1  1  1  3  1    5  6  10   Canthon aff. virens                            1  7  8  8   Deltochilum aff. komareki                          1  5  7  13  13   Deltochilum pseudoicarus Balthasar                  2    4  6  6  1  34  41  47   Malagoniella astyanax (Olivier)                              30  30  30   Malagoniella puncticollis (Blanchard)  6    13  19      32  32    3  18  21      122  122  194  ONITICELLINI   Eurysternus caribaeus (Herbst)              6  6              9  9  15   Eurysternus nigrovirens Génier              6  6              5  5  11  ONTHOPHAGINI   Digitonthophagus gazella (Fabricius)  1  1  10  12    6  31  37  3  22  14  39  1  19  31  51  139   Onthophagus aff. hirculus    5  98  103    13  299  312  3  1  69  73  17  51  402  470  958  PHANAEINI   Coprophanaeus bonariensis Gory                          1    2  3  3   Coprophanaeus ensifer (Germar)                              1  1  1   Coprophanaeus milon (Blanchard)                  1    1  2          2   Gromphas inermis Brullé      19  19      45  45      18  18      3  3  85   Number of individuals        1147        1604        2015        2320  7086  Taxon  Dry    Rainy    Total  Introduced  Total  Native  Total  Introduced  Total  Native  Total  C  CD  HF    C  CD  H F    C  CD  HF    C  CD  HF    ATEUCHINI   Ateuchus sp.  14  4  30  48  7  4  51  62  6  24  74  104  27  24  123  176  390   Genieridium bidens (Balthasar)            7  33  40      3  3          43   Trichillum externepunctatum Preudhomme de Borre  4    10  14      54  54  34  41  879  954    12  66  78  1100   Uroxys sp.      7  7      29  29  2  4    6      23  23  65  COPRINI   Canthidium sp.      8  8    2  12  14      2  2  2    24  26  50   Canthidium aff. barbacenicum          11    242  253  5  11  2  18  43  11  266  320  591   Canthidium aff. pinotoides                  12  21  82  115  27  9  253  289  404   Dichotomius bos (Blanchard)  3  7  23  33  4  7  26  37  1  12  126  139    5  77  82  291   Dichotomius glaucus Harold                      2  2      18  18  20   Dichotomius nisus (Olivier)  93  63  671  827  18  47  457  522  4  8  240  252  2  1  76  79  1680   Dichotomius opacipennis Luederwaldt                      1  1  4  1  54  59  60   Ontherus appendiculatus (Mannerheim)  19  3  18  40    3  64  67    1  13  15    2  18  20  142   Ontherus sulcator (Fabricius)                      1            1  DELTOCHILINI   Canthon edentulus Harold      1  1      22  22  1    4  5  17  3  137  157  185   Canthon histrio (Lepelletier and Serville)              9  9      2  2  2  3  76  81  92   Canthon mutabilis Lucas    3  12  15    5  39  44  103  15  109  227  33  20  80  133  419   Canthon ornatus Redtenbacher              13  13  1    2  3      2  2  18   Canthon substriatus Harold                  2    2  4  4  2  9  15  19   Canthon aff. curvodilatatus  1      1          1  1  1  3  1    5  6  10   Canthon aff. virens                            1  7  8  8   Deltochilum aff. komareki                          1  5  7  13  13   Deltochilum pseudoicarus Balthasar                  2    4  6  6  1  34  41  47   Malagoniella astyanax (Olivier)                              30  30  30   Malagoniella puncticollis (Blanchard)  6    13  19      32  32    3  18  21      122  122  194  ONITICELLINI   Eurysternus caribaeus (Herbst)              6  6              9  9  15   Eurysternus nigrovirens Génier              6  6              5  5  11  ONTHOPHAGINI   Digitonthophagus gazella (Fabricius)  1  1  10  12    6  31  37  3  22  14  39  1  19  31  51  139   Onthophagus aff. hirculus    5  98  103    13  299  312  3  1  69  73  17  51  402  470  958  PHANAEINI   Coprophanaeus bonariensis Gory                          1    2  3  3   Coprophanaeus ensifer (Germar)                              1  1  1   Coprophanaeus milon (Blanchard)                  1    1  2          2   Gromphas inermis Brullé      19  19      45  45      18  18      3  3  85   Number of individuals        1147        1604        2015        2320  7086  C, Carrion; CD, Cattle dung; and HF, Human feces. View Large In native and introduced pastures, traps baited with human feces captured highest abundance (Native: χ2(3,122) = 166.85, P < 0.001; Introduced: χ2(3,122) = 91.40, P < 0.001, Fig. 1A and B) and species richness (Native: χ2(3,122) = 206.13, P < 0.001; Introduced: χ2(3,122) = 148.22, P < 0.001, Fig. 1A and B) of dung beetles compared with other baits; and the abundance and species richness caught by human feces were not different from the sum of all three baits (control). Fig. 1. View largeDownload slide Mean abundance and richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Error bars represent ± SE. Fig. 1. View largeDownload slide Mean abundance and richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Error bars represent ± SE. In the native pastures, the traps baited with human feces had the highest FDis (F(3,122) = 10.53, P < 0.001) and FRic (F(3,122) = 110.99, P < 0.001) (Fig. 2A) of any bait, and these values were similar to that seen when all three baits were combined (control). In the introduced pastures, human feces and control also had the highest and similar FDis (F(3,122) = 17.94, P < 0.001) and FRic (F(3,122) = 55.71, P < 0.001) (Fig. 2B). Fig. 2. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Fig. 2. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Seasons: Taxonomic and Functional Diversity In the native pastures, dung beetle abundance was similar between the two sampling seasons (F(1,30) = 3.81, P = 0.06) (Fig. 3A), yet in the introduced pastures it was higher during the rainy season (F(1,30) = 9.46, P < 0.001) (Fig. 3B). The highest dung beetle species richness was found during the rainy season in both pasture types: native (F(1,30) = 46.96, P < 0.001) and introduced pastures (F(1,30) = 36.22, P < 0.001) (Fig. 3A and B). Fig. 3. View largeDownload slide Mean abundance and species richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Error bars represent ± SE. Fig. 3. View largeDownload slide Mean abundance and species richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Error bars represent ± SE. In the native pastures, the rainy season had the highest FDis (F(1,30) = 5.18, P = 0.03) and FRic (F(1,30) = 30.96, P < 0.001) (Fig. 4A). In the introduced pastures, the rainy season had the highest FDis (F(1,30) = 97.59, P < 0.001) and FRic (F(1,30) = 49.29, P < 0.001) (Fig. 4B). Fig. 4. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Fig. 4. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Discussion Our findings showed that traps baited with human feces are as efficient as a combination of traps baited with human feces, cattle dung, and carrion for dung beetle sampling in the native and introduced pastures. Dung beetles have a greater preference for dung with higher nutritional quality, which is related to mammal diet (Whipple and Hoback 2012). Studies in the Neotropical region have reported the feeding preference of dung beetles for feces of omnivorous mammals, which usually attracts a greater number of species in relation to herbivore feces (Puker et al. 2013), carnivore feces (Bogoni and Hernandez 2014), and carrion (Correa et al. 2016a). This preference is probably due to the fact that omnivores have a wider range and variety of food items with different sources of protein and other nutrients that are not assimilated and are, therefore, significantly eliminated in the feces (Larsen et al. 2006). For this reason, human feces has been considered essential when seeking to sample the highest dung beetle abundance and species richness, independent of the vegetal structure (Correa et al. 2016a). The majority of research on dung beetle communities in Brazilian introduced pastures has been conducted using cattle dung as bait (see a list in the study by Louzada and Carvalho e Silva 2009, Tissiani et al. 2017). However, our study demonstrated that all species recorded in native and introduced pastures were sampled in human feces (100%), whereas cattle dung sampled 63.3% and 52% of the dung beetle species in native and introduced pastures, respectively (Table 1). These results show that the dung beetle communities sampled in cattle dung is a subset of the community sampled in human feces. Dung beetles are sensitive, effective, and low-cost bioindicators of environmental changes (McGeoch et al. 2002, Gardner et al. 2008). Due to the constant increase in introduced pasture areas in Brazil (Figueiredo et al. 2012), we believe that to collecting dung beetles with human feces or all baits together is more precise and efficient than cattle dung for monitoring the potential impacts that introduced pastures have on the dung beetle biodiversity (Almeida et al. 2011, Correa et al. 2016b). We found that only human feces had similar FDis and FRic to the control in both pasture types. The greater richness of functional traits found in human feces demonstrates the efficiency of this bait type in the sampling functional traits, and demonstrates that this bait type is also able to capture the greater variety of these traits in the study areas. Because of the growing number of studies using functional diversity (Barragán et al. 2011, Audino et al. 2014, Derhé et al. 2016, Gómez-Cifuentes et al. 2017, Correa et al. 2018), our results may be important to assist in the sampling strategy of future researches that aim to evaluate the impacts on the functional diversity of dung beetles in pastures. The highest dung beetle richness was found in the rainy season in both pasture types. Our results demonstrated that sampling dung beetles in the rainy season is potentially more appropriate to capture a larger number of species in Brazilian pastures. Although it is reported that rainfall is the most important climatic factor affecting dung beetle communities in Brazilian pastures, presenting higher abundance and species richness in the rainy season (Aidar et al. 2000, Koller et al. 2007, Abot et al. 2012, Puker et al. 2014), our experimental design does not include replication of seasons, which limits larger generalizations. We found that functional diversity is higher in the rainy season in both native and introduced pasture. This result indicates that the rainy season is potentially more appropriate to sample the greatest number of functional traits and to capture the greatest dispersion of traits in pastures. In addition, this shows that the ecosystem functions performed by dung beetles in pastures are influenced by the season. Since functional diversity is directly related to ecosystem functions (Barragán et al. 2011, Gerisch et al. 2012, Mouillot et al. 2013), and a community with higher functional diversity tends to perform ecosystem processes more efficiently (Batalha et al. 2010), this demonstrates that the ecological functions performed by dung beetles in pastures possibly are higher in the rainy season. We found, through taxonomic and functional responses, that the bait attractiveness patterns and sampling season for dung beetles are similar between native and introduced pastures. Because of the wide use of these insects in ecological research, an accurate sampling of dung beetle populations and/or communities is vital for any study involving their biodiversity (Marsh et al. 2013, Correa et al. 2016a). In addition, the use of a set of different baits may increase the time spent in setting up field traps, physical effort, and financial resources for the project, even with the samples being relatively inexpensive (Gardner et al. 2008). However, the use of baits (individual or combined) and sampling time will depend on the main objective of the research. Conclusions In summary, we demonstrate that human feces is the most suitable bait for the collection of dung beetles and rainy season is potentially more appropriate period for studies directed toward the knowledge of dung beetle fauna that can support data on the species distribution in the Brazilian pastures. Thus, the best sampling method observed in this study may be useful to monitor the potential impacts that introduced pastures have on the dung beetle taxonomic and functional diversity, and rigorous comparison among studies on these insects in Brazilian pastures. Supplementary Data Supplementary data are available at Environmental Entomology online. Acknowledgments We thank the father of the first author, Agenor Martinho Correa, for the encouragement and logistical support and FAPEMIG (APQ – 02696-15) for the financial support. We also thank Fernando Z. Vaz-de-Mello (UFMT) for identification of the dung beetle species; Cleilsom M. Cristaldo (UEMS), Kleyton R. Ferreira (Universidade Federal da Grande Dourados, Dourados, Brazil), Adilson Areco, Flávia Torres, and Vagner dos Santos for the field support, Mrs. Odilon Ribeiro and Zelito Ribeiro for access to their properties and two anonymous reviewers for the fruitful comments on the manuscript. CMAC receives a PhD scholarship from the Conselho Nacional de Desenvolvimento Científico Tecnológico (CNPq, Brazil) (140741/2015-1) from the Entomology Graduate Program, Universidade Federal de Lavras, and a PhD sandwich scholarship from the Coordenação de Aperfeiçoamento de Pessoa de Nível Superior (CAPES, Brazil) (88881.134292/2016-01). References Cited Abot, A. R., Puker A., Taira T. L., Rodrigues S. R., Korasaki V., and Oliveira H. N.. 2012. Abundance and diversity of coprophagous beetle (Coleoptera: Scarabaeidae) caught light trap in a pasture of the Brazilian Cerrado. Stud. Neotrop. Fauna Environ . 47: 53– 60. Google Scholar CrossRef Search ADS   Aidar, T., Koller W., Rodrigues S. R., Silva J. C. C., Balta O. D. S., Oliveira J. M., and Oliveira V. L.. 2000. Besouros coprófagos (Coleoptera: Scarabaeidae) coletados em Aquidauana, MS. An. Soc. Bras. Entomol . 29: 817– 820. Google Scholar CrossRef Search ADS   Almeida, S., Louzada J., Sperber C., and Barlow J.. 2011. 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Optimising Methods for Dung Beetle (Coleoptera: Scarabaeidae) Sampling in Brazilian Pastures

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10.1093/ee/nvx191
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Abstract

Abstract Dung beetles are globally used in ecological research and are useful for assessing the effects of anthropic and natural changes in environment on biodiversity. Here we investigate how the choice of baits (human feces, cattle dung, carrion or a combination of all three) and sampling season influence the taxonomic and functional diversity of insects captured in traps in Brazilian pastures. We sampled dung beetles in July 2011 (dry season) and January 2012 (rainy season) in eight areas: four pastures with native grasses (e.g., Andropogon spp. and Axonopus spp.) and four pastures with introduced grasses (Urochloa spp.) in Aquidauana, Mato Grosso do Sul, Brazil. To collect the insects, we used pitfall traps baited with carrion, cattle dung and human feces. A total of 7,086 dung beetles of 32 species were captured. In both pasture types, only traps baited with human feces captured similar abundance, species richness, and functional diversity compared with the sum total of beetles captured by the three bait types. The species richness and functional diversity were higher in the rainy season in both pasture types. Our results demonstrate that using human feces alone as bait and sampling dung beetles in the rainy season are potentially sufficient to ensure the greatest number of functional traits, species, and individuals in both pasture types. Thus, the best sampling method observed in this study may be useful for studies focused on dung beetle fauna survey and rigorous comparison among studies on these insects in Brazilian pastures. Dung beetles (Coleoptera: Scarabaeinae) are a group of insects used globally in ecological research to evaluate the effects of anthropic and natural changes the environment on biodiversity (Audino et al. 2014, Bicknell et al. 2014, França et al. 2016). They are stenotopic and thus sensitive to changes in environmental conditions (Hanski and Cambefort 1991), diverse and relatively well characterized taxonomically (Vaz-de-Mello et al. 2011), and relatively inexpensive to collect (Gardner et al. 2008). In addition, they perform important ecological functions, such as nutrient cycling, improving soil fertility, and secondary seed dispersal (for review, see the study by Nichols et al. 2008 and references therein). Despite the validation of this group as bioindicators being relatively recent (McGeoch et al. 2002, Spector 2006), the number of studies using dung beetles has been increasing worldwide, making this group one of the most used as terrestrial bioindicators (Gerlach et al. 2013). Using dung beetles as bioindicators requires a method of effectively sampling the beetles across different types of habitats (Marsh et al. 2013, Correa et al. 2016a). In many studies that have evaluated the impact of anthropogenic changes on dung beetle communities, only human feces were used as bait (Braga et al. 2013, Korasaki et al. 2013, Bicknell et al. 2014, Costa et al. 2017). Human feces are indispensable when the target is to sample greater abundance and species richness, independent of the plant structure (Correa et al. 2016a). In addition, feces of omnivorous mammals (especially humans) are more attractive to dung beetles when compared, for example, with herbivore (Puker et al. 2013) and carnivore feces (Bogoni and Hernandez 2014) and carrion (Correa et al. 2016a). In contrast, due to the trophic specialization of dung beetles (Larsen et al 2006), using multiple baits may attract a more diverse group of beetles and thus result in a better characterization of communities (Audino et al. 2014, Correa et al. 2016a). Grasslands, such as pastures dominated by native (e.g., Adropogon spp. and Axonopus spp.) or introduced grasses (the African grass, Urochloa spp.), predominate in four of the six Brazilian biomes (Overbeck et al. 2015), with an estimated area of 176 million ha (IBGE 2012). However, our knowledge of the differences in dung beetle communities across Brazilian pastures is insipient. One of the reasons for this is the inconsistency in sampling strategy used in most studies carried out in Brazilian pastures. In introduced pastures, most studies have used cattle dung as bait (for a list refer the study by Louzada and Carvalho e Silva 2009, Tissiani et al. 2017), whereas in forests, the most frequently used baits are human feces (Marsh et al. 2013, Audino et al. 2014), decaying fruits (Silva et al. 2012a, Audino et al. 2014), and vertebrate carrion (e.g., Silva et al. 2012a, Audino et al. 2014). Furthermore, sampling period also plays a fundamental role in dung beetle sampling (Halffter et al. 1991). However, little is known about the effects of seasons on the dung beetle sampling in Brazilian pastures (Abot et al. 2012). Studies that assess the attractiveness of baits to dung beetles in Brazilian pastures by comparing community metrics such as abundance, biodiversity, and species composition are well known (Silva et al. 2012b, Puker et al. 2013, Correa et al. 2016b). However, functional diversity metrics are also important; functional diversity is a measure of biodiversity that quantifies the diversity of characters (morphology, life history, and ecological niches) in a community (Cadotte et al. 2011, Gerish et al. 2012, Mouillot et al. 2013). Functional diversity metrics are directly related to ecosystem functions performed by species (Barrágan et al. 2011, Audino et al. 2014); therefore, functional diversity has been used to predict the impact of the loss of species on ecosystem functionality (Barrágan et al. 2011, Audino et al. 2014, Derhé et al. 2016, Goméz-Cifuentes et al. 2017). However, there is still no information on the effect of the different baits and sampling seasons on the functional metrics. An important step to improve dung beetle sampling in pastures is to understand how the collection method can affect the quantification of the community in terms of both, taxonomic and functional diversity. Here, we investigate how the use of baits (human feces, cattle dung, carrion or a combination of all three) and sampling seasons influences the taxonomic and functional diversity of dung beetles captured in Brazilian pastures. Therefore, we sampled dung beetles in cattle grazing native and introduced pastures (Urochloa spp.), using pitfall traps baited with human feces, cattle dung, and carrion during the dry and rainy season to answer the following question: does any individual bait capture the abundance, species richness and functional diversity of dung beetles similar to that captured by all baits summed together in the two pasture types? In addition, we compared the abundance, species richness, and functional diversity of dung beetles captured in the rainy and dry season in both pasture types. Material and Methods Study Sites Samples were collected in four areas of pastures with introduced grasses (Urochloa spp.) and four pastures with native grasses (e.g., Andropogon spp. and Axonopus spp.) in Aquidauana, Mato Grosso do Sul, Brazil (19° 54′36 ″ S, 55° 47′54″ W). The climate of the region, according to the Köppen classification is Aw, that is, tropical hot–wet, with a summer rainy season and dry winter (Alvares et al. 2014). The average temperature is 26°C (12–40°C) and rainfall (average of 1,200 mm yr−1) is characterized by certain periods, such as dry (May to September: monthly average of 30 mm of precipitation) and rainy (October to April: 160 mm). Animals, especially cattle and horses, are extensively produced on these pastures. More detailed description of the study areas are in Correa et al. (2016b). Dung Beetle Sampling and Identification We sampled dung beetles in July 2011 (dry season) and January 2012 (middle of the rainy season). In each of the eight pasture areas, we installed four linear transects (250 m) located ~50 m from the edge of the habitat and separated from the others by 100 m for allocation of the traps. A distance of 100 m was used between transects to ensure independence of the samples (Silva and Hernández 2015). Therefore, we consider the transects as replicates (i.e., 16 replicates per type of pasture). In each transect, we marked out six points separated by 50 m. At each point, we installed a set of three traps, each separated by 3 m in a triangular shape; the traps of each set were baited with ~40 g of human feces, cattle dung, and carrion (decaying beef). Total sampling effort was 1,152 traps, where each bait was repeated 192 times for each pasture type, in rainy and dry season. The traps (15 cm diameter and 9 cm tall), installed at ground level, contained ~250 ml of a 1.5% liquid detergent solution and remained installed in the field for a period of 48 h. Traps were covered with a plastic lid in order to reduce desiccation of the bait and avoid damage caused by potential rainfall. The baits were placed in plastic containers (50 ml) at the center of each trap using a wire as bait holder. Dung beetles were identified to species level by Dr. Fernando Zagury Vaz-de-Mello. Voucher specimens are deposited at the Entomology Section of the Zoological Collection of the Universidade Federal de Mato Grosso (UFMT; Cuiabá, Mato Grosso, Brazil) and in the Entomology Laboratory at the Universidade Estadual de Mato Grosso do Sul (UEMS; Aquidauana, Mato Grosso do Sul, Brazil). Functional Traits We analyzed four functional traits that are directly related to the ecosystemic functions performed by dung beetles and diet: nesting behavior (tunnelers, rollers, or dwellers), diet preference (human feces, cattle dung, carrion, coprophagous/generalist, or generalist), breadth of diet (species attracted to one, two, or three bait types) and body size (Suppl material 1). Data Analysis Taxonomic Metrics in Different Baits and Seasons We used Generalized Linear Mixed Models (GLMMs) to verify the effect of different baits (explanatory variables) in each pasture type on dung beetle abundance and species richness (response variables), using bait types (fixed factor) and seasons (random factor). We used a negative binomial error distribution with log link function for abundance and species richness, since these data showed overdispersion, preventing the use of Poisson error. We used Generalized Linear Models (GLMs) to verify the effect of different seasons (explanatory variables) in each pasture type on dung beetle abundance and species richness (response variables). All GLMs were submitted to residual analysis, so as to evaluate error distribution adequacy (Crawley 2002), and conducted with the “lme4” package using the R v 3.3.1 software (R Development Core Team 2016). Functional Diversity in Different Baits and Seasons We used the “FD” package (R Development Core Team 2016) to calculate two functional diversity indexes: 1) Functional richness (FRic) represents the range of traits in a community quantified by the volume of functional trace space occupied, and 2) functional dispersion (FDis) which indicates the distribution of abundances in the space of functional traits in relation to a weighted centroid in abundance and the volume of space occupied (Laliberté and Legendre 2010). We used GLMMs to verify the effect of different baits (explanatory variables) in each habitat on functional diversity (response variables). We used bait types (fixed factor) and seasons (random factor) with Gaussian error distribution. Finally, we used GLMs to verify the effect of different seasons (explanatory variables) in each pasture type on functional diversity indices (response variables). Appropriate error structure and link function were used for each analysis (Crawley 2002). Results Baits Attractiveness: Taxonomic and Functional Diversity A total of 7,086 individuals were sampled belonging to 32 species of 16 genera and six tribes of dung beetles: Ateuchini (4 genera and 4 species), Coprini (3 genera and 9 species), Deltochilini (3 genera and 11 species), Oniticellini (1 genus and 2 species), Onthophagini (2 genera and 2 species), and Phanaeini (2 genera and 4 species) (Table 1). Table 1. Biodiversity of dung beetles sampled in introduced and native pastures in the dry and rainy seasons in Aquidauana, Mato Grosso do Sul, Brazil Taxon  Dry    Rainy    Total  Introduced  Total  Native  Total  Introduced  Total  Native  Total  C  CD  HF    C  CD  H F    C  CD  HF    C  CD  HF    ATEUCHINI   Ateuchus sp.  14  4  30  48  7  4  51  62  6  24  74  104  27  24  123  176  390   Genieridium bidens (Balthasar)            7  33  40      3  3          43   Trichillum externepunctatum Preudhomme de Borre  4    10  14      54  54  34  41  879  954    12  66  78  1100   Uroxys sp.      7  7      29  29  2  4    6      23  23  65  COPRINI   Canthidium sp.      8  8    2  12  14      2  2  2    24  26  50   Canthidium aff. barbacenicum          11    242  253  5  11  2  18  43  11  266  320  591   Canthidium aff. pinotoides                  12  21  82  115  27  9  253  289  404   Dichotomius bos (Blanchard)  3  7  23  33  4  7  26  37  1  12  126  139    5  77  82  291   Dichotomius glaucus Harold                      2  2      18  18  20   Dichotomius nisus (Olivier)  93  63  671  827  18  47  457  522  4  8  240  252  2  1  76  79  1680   Dichotomius opacipennis Luederwaldt                      1  1  4  1  54  59  60   Ontherus appendiculatus (Mannerheim)  19  3  18  40    3  64  67    1  13  15    2  18  20  142   Ontherus sulcator (Fabricius)                      1            1  DELTOCHILINI   Canthon edentulus Harold      1  1      22  22  1    4  5  17  3  137  157  185   Canthon histrio (Lepelletier and Serville)              9  9      2  2  2  3  76  81  92   Canthon mutabilis Lucas    3  12  15    5  39  44  103  15  109  227  33  20  80  133  419   Canthon ornatus Redtenbacher              13  13  1    2  3      2  2  18   Canthon substriatus Harold                  2    2  4  4  2  9  15  19   Canthon aff. curvodilatatus  1      1          1  1  1  3  1    5  6  10   Canthon aff. virens                            1  7  8  8   Deltochilum aff. komareki                          1  5  7  13  13   Deltochilum pseudoicarus Balthasar                  2    4  6  6  1  34  41  47   Malagoniella astyanax (Olivier)                              30  30  30   Malagoniella puncticollis (Blanchard)  6    13  19      32  32    3  18  21      122  122  194  ONITICELLINI   Eurysternus caribaeus (Herbst)              6  6              9  9  15   Eurysternus nigrovirens Génier              6  6              5  5  11  ONTHOPHAGINI   Digitonthophagus gazella (Fabricius)  1  1  10  12    6  31  37  3  22  14  39  1  19  31  51  139   Onthophagus aff. hirculus    5  98  103    13  299  312  3  1  69  73  17  51  402  470  958  PHANAEINI   Coprophanaeus bonariensis Gory                          1    2  3  3   Coprophanaeus ensifer (Germar)                              1  1  1   Coprophanaeus milon (Blanchard)                  1    1  2          2   Gromphas inermis Brullé      19  19      45  45      18  18      3  3  85   Number of individuals        1147        1604        2015        2320  7086  Taxon  Dry    Rainy    Total  Introduced  Total  Native  Total  Introduced  Total  Native  Total  C  CD  HF    C  CD  H F    C  CD  HF    C  CD  HF    ATEUCHINI   Ateuchus sp.  14  4  30  48  7  4  51  62  6  24  74  104  27  24  123  176  390   Genieridium bidens (Balthasar)            7  33  40      3  3          43   Trichillum externepunctatum Preudhomme de Borre  4    10  14      54  54  34  41  879  954    12  66  78  1100   Uroxys sp.      7  7      29  29  2  4    6      23  23  65  COPRINI   Canthidium sp.      8  8    2  12  14      2  2  2    24  26  50   Canthidium aff. barbacenicum          11    242  253  5  11  2  18  43  11  266  320  591   Canthidium aff. pinotoides                  12  21  82  115  27  9  253  289  404   Dichotomius bos (Blanchard)  3  7  23  33  4  7  26  37  1  12  126  139    5  77  82  291   Dichotomius glaucus Harold                      2  2      18  18  20   Dichotomius nisus (Olivier)  93  63  671  827  18  47  457  522  4  8  240  252  2  1  76  79  1680   Dichotomius opacipennis Luederwaldt                      1  1  4  1  54  59  60   Ontherus appendiculatus (Mannerheim)  19  3  18  40    3  64  67    1  13  15    2  18  20  142   Ontherus sulcator (Fabricius)                      1            1  DELTOCHILINI   Canthon edentulus Harold      1  1      22  22  1    4  5  17  3  137  157  185   Canthon histrio (Lepelletier and Serville)              9  9      2  2  2  3  76  81  92   Canthon mutabilis Lucas    3  12  15    5  39  44  103  15  109  227  33  20  80  133  419   Canthon ornatus Redtenbacher              13  13  1    2  3      2  2  18   Canthon substriatus Harold                  2    2  4  4  2  9  15  19   Canthon aff. curvodilatatus  1      1          1  1  1  3  1    5  6  10   Canthon aff. virens                            1  7  8  8   Deltochilum aff. komareki                          1  5  7  13  13   Deltochilum pseudoicarus Balthasar                  2    4  6  6  1  34  41  47   Malagoniella astyanax (Olivier)                              30  30  30   Malagoniella puncticollis (Blanchard)  6    13  19      32  32    3  18  21      122  122  194  ONITICELLINI   Eurysternus caribaeus (Herbst)              6  6              9  9  15   Eurysternus nigrovirens Génier              6  6              5  5  11  ONTHOPHAGINI   Digitonthophagus gazella (Fabricius)  1  1  10  12    6  31  37  3  22  14  39  1  19  31  51  139   Onthophagus aff. hirculus    5  98  103    13  299  312  3  1  69  73  17  51  402  470  958  PHANAEINI   Coprophanaeus bonariensis Gory                          1    2  3  3   Coprophanaeus ensifer (Germar)                              1  1  1   Coprophanaeus milon (Blanchard)                  1    1  2          2   Gromphas inermis Brullé      19  19      45  45      18  18      3  3  85   Number of individuals        1147        1604        2015        2320  7086  C, Carrion; CD, Cattle dung; and HF, Human feces. View Large In native and introduced pastures, traps baited with human feces captured highest abundance (Native: χ2(3,122) = 166.85, P < 0.001; Introduced: χ2(3,122) = 91.40, P < 0.001, Fig. 1A and B) and species richness (Native: χ2(3,122) = 206.13, P < 0.001; Introduced: χ2(3,122) = 148.22, P < 0.001, Fig. 1A and B) of dung beetles compared with other baits; and the abundance and species richness caught by human feces were not different from the sum of all three baits (control). Fig. 1. View largeDownload slide Mean abundance and richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Error bars represent ± SE. Fig. 1. View largeDownload slide Mean abundance and richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Error bars represent ± SE. In the native pastures, the traps baited with human feces had the highest FDis (F(3,122) = 10.53, P < 0.001) and FRic (F(3,122) = 110.99, P < 0.001) (Fig. 2A) of any bait, and these values were similar to that seen when all three baits were combined (control). In the introduced pastures, human feces and control also had the highest and similar FDis (F(3,122) = 17.94, P < 0.001) and FRic (F(3,122) = 55.71, P < 0.001) (Fig. 2B). Fig. 2. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Fig. 2. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among baits. Seasons: Taxonomic and Functional Diversity In the native pastures, dung beetle abundance was similar between the two sampling seasons (F(1,30) = 3.81, P = 0.06) (Fig. 3A), yet in the introduced pastures it was higher during the rainy season (F(1,30) = 9.46, P < 0.001) (Fig. 3B). The highest dung beetle species richness was found during the rainy season in both pasture types: native (F(1,30) = 46.96, P < 0.001) and introduced pastures (F(1,30) = 36.22, P < 0.001) (Fig. 3A and B). Fig. 3. View largeDownload slide Mean abundance and species richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Error bars represent ± SE. Fig. 3. View largeDownload slide Mean abundance and species richness of dung beetles sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Error bars represent ± SE. In the native pastures, the rainy season had the highest FDis (F(1,30) = 5.18, P = 0.03) and FRic (F(1,30) = 30.96, P < 0.001) (Fig. 4A). In the introduced pastures, the rainy season had the highest FDis (F(1,30) = 97.59, P < 0.001) and FRic (F(1,30) = 49.29, P < 0.001) (Fig. 4B). Fig. 4. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Fig. 4. View largeDownload slide Mean ± SE of dung beetles functional diversity sampled in native (A) and introduced (B) pastures in Aquidauana, Mato Grosso do Sul, Brazil. Different letters above the bars indicate statistically significant differences among seasons. Discussion Our findings showed that traps baited with human feces are as efficient as a combination of traps baited with human feces, cattle dung, and carrion for dung beetle sampling in the native and introduced pastures. Dung beetles have a greater preference for dung with higher nutritional quality, which is related to mammal diet (Whipple and Hoback 2012). Studies in the Neotropical region have reported the feeding preference of dung beetles for feces of omnivorous mammals, which usually attracts a greater number of species in relation to herbivore feces (Puker et al. 2013), carnivore feces (Bogoni and Hernandez 2014), and carrion (Correa et al. 2016a). This preference is probably due to the fact that omnivores have a wider range and variety of food items with different sources of protein and other nutrients that are not assimilated and are, therefore, significantly eliminated in the feces (Larsen et al. 2006). For this reason, human feces has been considered essential when seeking to sample the highest dung beetle abundance and species richness, independent of the vegetal structure (Correa et al. 2016a). The majority of research on dung beetle communities in Brazilian introduced pastures has been conducted using cattle dung as bait (see a list in the study by Louzada and Carvalho e Silva 2009, Tissiani et al. 2017). However, our study demonstrated that all species recorded in native and introduced pastures were sampled in human feces (100%), whereas cattle dung sampled 63.3% and 52% of the dung beetle species in native and introduced pastures, respectively (Table 1). These results show that the dung beetle communities sampled in cattle dung is a subset of the community sampled in human feces. Dung beetles are sensitive, effective, and low-cost bioindicators of environmental changes (McGeoch et al. 2002, Gardner et al. 2008). Due to the constant increase in introduced pasture areas in Brazil (Figueiredo et al. 2012), we believe that to collecting dung beetles with human feces or all baits together is more precise and efficient than cattle dung for monitoring the potential impacts that introduced pastures have on the dung beetle biodiversity (Almeida et al. 2011, Correa et al. 2016b). We found that only human feces had similar FDis and FRic to the control in both pasture types. The greater richness of functional traits found in human feces demonstrates the efficiency of this bait type in the sampling functional traits, and demonstrates that this bait type is also able to capture the greater variety of these traits in the study areas. Because of the growing number of studies using functional diversity (Barragán et al. 2011, Audino et al. 2014, Derhé et al. 2016, Gómez-Cifuentes et al. 2017, Correa et al. 2018), our results may be important to assist in the sampling strategy of future researches that aim to evaluate the impacts on the functional diversity of dung beetles in pastures. The highest dung beetle richness was found in the rainy season in both pasture types. Our results demonstrated that sampling dung beetles in the rainy season is potentially more appropriate to capture a larger number of species in Brazilian pastures. Although it is reported that rainfall is the most important climatic factor affecting dung beetle communities in Brazilian pastures, presenting higher abundance and species richness in the rainy season (Aidar et al. 2000, Koller et al. 2007, Abot et al. 2012, Puker et al. 2014), our experimental design does not include replication of seasons, which limits larger generalizations. We found that functional diversity is higher in the rainy season in both native and introduced pasture. This result indicates that the rainy season is potentially more appropriate to sample the greatest number of functional traits and to capture the greatest dispersion of traits in pastures. In addition, this shows that the ecosystem functions performed by dung beetles in pastures are influenced by the season. Since functional diversity is directly related to ecosystem functions (Barragán et al. 2011, Gerisch et al. 2012, Mouillot et al. 2013), and a community with higher functional diversity tends to perform ecosystem processes more efficiently (Batalha et al. 2010), this demonstrates that the ecological functions performed by dung beetles in pastures possibly are higher in the rainy season. We found, through taxonomic and functional responses, that the bait attractiveness patterns and sampling season for dung beetles are similar between native and introduced pastures. Because of the wide use of these insects in ecological research, an accurate sampling of dung beetle populations and/or communities is vital for any study involving their biodiversity (Marsh et al. 2013, Correa et al. 2016a). In addition, the use of a set of different baits may increase the time spent in setting up field traps, physical effort, and financial resources for the project, even with the samples being relatively inexpensive (Gardner et al. 2008). However, the use of baits (individual or combined) and sampling time will depend on the main objective of the research. Conclusions In summary, we demonstrate that human feces is the most suitable bait for the collection of dung beetles and rainy season is potentially more appropriate period for studies directed toward the knowledge of dung beetle fauna that can support data on the species distribution in the Brazilian pastures. Thus, the best sampling method observed in this study may be useful to monitor the potential impacts that introduced pastures have on the dung beetle taxonomic and functional diversity, and rigorous comparison among studies on these insects in Brazilian pastures. Supplementary Data Supplementary data are available at Environmental Entomology online. Acknowledgments We thank the father of the first author, Agenor Martinho Correa, for the encouragement and logistical support and FAPEMIG (APQ – 02696-15) for the financial support. We also thank Fernando Z. Vaz-de-Mello (UFMT) for identification of the dung beetle species; Cleilsom M. Cristaldo (UEMS), Kleyton R. Ferreira (Universidade Federal da Grande Dourados, Dourados, Brazil), Adilson Areco, Flávia Torres, and Vagner dos Santos for the field support, Mrs. Odilon Ribeiro and Zelito Ribeiro for access to their properties and two anonymous reviewers for the fruitful comments on the manuscript. CMAC receives a PhD scholarship from the Conselho Nacional de Desenvolvimento Científico Tecnológico (CNPq, Brazil) (140741/2015-1) from the Entomology Graduate Program, Universidade Federal de Lavras, and a PhD sandwich scholarship from the Coordenação de Aperfeiçoamento de Pessoa de Nível Superior (CAPES, Brazil) (88881.134292/2016-01). References Cited Abot, A. R., Puker A., Taira T. L., Rodrigues S. R., Korasaki V., and Oliveira H. N.. 2012. Abundance and diversity of coprophagous beetle (Coleoptera: Scarabaeidae) caught light trap in a pasture of the Brazilian Cerrado. Stud. Neotrop. Fauna Environ . 47: 53– 60. Google Scholar CrossRef Search ADS   Aidar, T., Koller W., Rodrigues S. R., Silva J. C. C., Balta O. D. S., Oliveira J. M., and Oliveira V. L.. 2000. Besouros coprófagos (Coleoptera: Scarabaeidae) coletados em Aquidauana, MS. An. Soc. Bras. Entomol . 29: 817– 820. Google Scholar CrossRef Search ADS   Almeida, S., Louzada J., Sperber C., and Barlow J.. 2011. 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Environmental EntomologyOxford University Press

Published: Feb 1, 2018

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